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Persoonia 45, 2020: 68 –100 ISSN (Online) 1878-9080
www.ingentaconnect.com/content/nhn/pimj https://doi.org/10.3767/persoonia.2020.45.03
RESEARCH ARTICLE
INTRODUCTION
Plant parasitic rusts within the order Pucciniales represent
one of the largest groups of fungal plant pathogens, which
occur on ferns to advanced monocots and dicots (Aime 2006,
Webster & Weber 2007). Approximately 7 800 rust species are
currently recognised worldwide, with many species causing
significant economic losses to agricultural or forest crop plants
(Arthur 1934, Hiratsuka et al. 1992, Cummins & Hiratsuka
2003). Among them, cedar rusts are one of the most important
genera of phytopathogens (Helfer 2005). These pathogens
belong to the genus Gymnosporangium, which previously has
been placed in the family Pucciniaceae (Pucciniales, Basidio-
mycota), and are obligate biotrophic phytopathogens (Cummins
& Hiratsuka 1983, 2003). Presently over 64 species have been
recorded, having a demicyclic (macrocyclic or microcyclic in a
few species) life cycle with a telial stage on gymnosperm trees
in Cupressaceae, and an aecial stage on trees of the apple
tribe, Maleae, in the family Rosaceae (Kern 1973, Shen et al.
2018, Farr & Rossman 2019).
Within the genus Gymnosporangium, cedar-apple rusts repre-
sent some of the most serious and devastating diseases occur-
ring in apple plantations worldwide (Sinclair & Lyon 2005, Zhao
et al. 2016, Lâce 2017). They occur on leaves, fruits and stems
of Malus species, cause premature defoliation, and eventually
kill their hosts plants (Helfer 2005). Hitherto, up to 17 Gymno-
sporangium species are known as causal agents of apple rust
diseases, having mostly been reported from temperate regions
in Asia, Africa, Europe and North America (Farr & Rossman
2019). Eleven Gymnosporangium species have been reported
on 16 Malus species and their hybrids in Asia (Azbukina 1972,
Wang & Guo 1985, Hiratsuka et al. 1992, Zhuang et al. 2012),
and nine Gymnosporangium species have been reported on 17
Malus species and their hybrids in North America (Arthur 1934,
Ziller 1974). Six Gymnosporangium spp. have been reported
on M. baccata, M. domestica, M. pumila and M. sylvestris in
Europe, and only one Gymnosporangium species has been
reported from Africa (Hylander 1953, Jørstad 1962, Wilson &
Henderson 1966, Farr & Rossman 2019). Among them, G. asia-
ticum, G. clavipes, G. globosum, G. juniper-virginianeae and
G. yamadae are listed as quarantine pests in Asia, Europe,
and North America (Duan et al. 2017, EPPO 2017, 2018).
Accurate and efficient species recognition, as well as a better
understanding of their life cycle are thus important for plant
quarantine and effective disease control.
Traditional taxonomy of Gymnosporangium relies on morpho-
logical distinctions in spermogonia and teliospores at generic
and suprageneric level, and this genus has long been placed
in Pucciniaceae (Dietel 1928, Cummins & Hiratsuka 1983,
2003). However, recent molecular studies revealed a phylo-
genetic distinction of Gymnosporangium from other members
of the Pucciniaceae (Maier et al. 2003, Wingfield et al. 2004,
Aime 2006) but did not conclusively resolve the relationship
of Gymnosporangium within other recognized families in the
order Pucciniales. Species recognition relies on the morpho-
logy of known spore stages, i.e., the telia or aecia occurring
on different host species (Kern 1908, 1973, Sydow & Sydow
1915, Hiratsuka et al. 1992, Cummins & Hiratsuka 2003). Host
Gymnosporangium species on Malus: species delineation,
diversity and host alternation
P. Zhao1, X.H. Qi2, P.W. Crous3,4, W.J. Duan5, L. Cai1*
1 State Key Laboratory of Mycology, Institute of Microbiology, Chinese
Academy of Sciences (CAS), Beijing, 100101, China;
corresponding author e-mail: cail@im.ac.cn.
2 Guangdong Institute of Microbiology, Guangdong Academy of Sciences,
Guangzhou, 510070, China.
3 Westerdijk Fungal Biodiversity Institute, P.O. Box 85176, 3508 AD Utrecht,
The Netherlands.
4 Department of Biochemistry, Genetics and Microbiology, Forestry and
Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria
0028, South Africa.
5 Ningbo Academy of Inspection and Quarantine, Ningbo, 315012, China.
Key words
Apple rust
host alternation
new taxa
species delimitation
Abstract Gymnosporangium species (Pucciniaceae, Pucciniales, Basidiomycota) are the causal agents of cedar-
apple rust diseases, which can lead to significant economic losses to apple cultivars. Currently, the genus contains
17 described species that alternate between spermogonial/ aecial stages on Malus species and telial stages on
Juniperus or Chamaecyparis species, although these have yet to receive a modern systematic treatment. Further-
more, prior studies have shown that Gymnosporangium does not belong to the Pucciniaceae sensu stricto (s.str.),
nor is it allied to any currently defined rust family. In this study we examine the phylogenetic placement of the genus
Gymnosporangium. We also delineate interspecific boundaries of the Gymnosporangium species on Malus based
on phylogenies inferred from concatenated data of rDNA SSU, ITS and LSU and the holomorphic morphology of
the entire life cycle. Based on these results, we propose a new family, Gymnosporangiaceae, to accommodate
the genus Gymnosporangium, and recognize 22 Gymnosporangium species parasitic on Malus species, of which
G. lachrymiforme, G. shennongjiaense, G. spinulosum, G. tiankengense and G. kanas are new. Typification of
G. asiaticum, G. fenzelianum, G. juniperi-virginianae, G. libocedri, G. nelsonii, G. nidus-avis and G. yamadae are
proposed to stabilize the use of names. Morphological and molecular data from type materials of 14 Gymnospor-
angium species are provided. Finally, morphological characteristics, host alternation and geographical distribution
data are provided for each Gymnosporangium species on Malus.
Article info Received: 27 October 2019; Accepted: 4 December 2019; Published: 10 January 2020.
69
P. Zhao et al.: Gymnosporangium on Malus
specificity is generally also employed for species recognition
(Sydow & Sydow 1915, Kern 1964, Parmelee 1971). However,
due to their diverse life cycles, overlapping host ranges, and
lacking uredinial stages in most species, considerable disagree-
ments on species delimitation still exist (Kern 1970, Peterson
1982, Novick 2008). In addition, several morphological charac-
teristics in aecial or telial stages have been employed as im-
portant criteria in distinguishing species, but their phylogenetic
significance has not been evaluated. Thus, previous reports
of 17 Gymnosporangium species on Malus species remain
dubious due to the lack of a consistent species concept. Our
previous studies have shown that the recognition of all spore
stages is essential for species recognition (Zhao et al. 2016).
Nevertheless, the connection between aecial and telial stages
and the characterisation of holomorphic morphology remain
unknown for most species.
In this study, comprehensive morphological and molecular
studies were conducted among rusts occurring on Malus and
their potential alternate hosts. The objectives of the current
study were:
1. to determine the phylogenetic placement of Gymnospor-
angium in the order Pucciniales (Basidiomycota);
2. to clarify the species boundaries of Gymnosporangium
species on Malus;
3. to confirm the connection of potential alternate hosts of
Gymnosporangium where possible;
4. to describe the taxonomic novelties based on molecular
phylogeny and morphology.
MATERIALS AND METHODS
Materials examined in this study
A total of 464 dried fungarium specimens were examined from
different herbaria to cover the largest possible Malus host spe-
cies distribution based on published taxonomic literature (Kern
1973, Farr & Rossman 2019). Specimens with either aecial
or telial stages were chosen according to the name on the
attached labels and their host information. Among them, 186
specimens were on the telial hosts Juniperus and Libocedrus
species, and 242 specimens were on Malus species and other
related hosts. Fungarium specimens were loaned from the
following fungaria: The Mycological Herbarium of Institute of
Microbiology, CAS, China (HMAS); Plant Pathology Herbarium,
Cornell University, Ithaca, New York, USA (CUP); New York
Botanical Garden, New York, USA (NYBG) and New York State
Museum, New York, USA (NYS). To supplement fungarium
material, 36 fresh collections were also included. Among these
464 specimens, type specimens of the following species were
included for comparative studies: G. aurantiacum, G. betheli,
G. biseptatum, G. connersii, G. distortum, G. exterum, G. fenze-
lianum, G. fraternum, G. gracile, G. hara eanum, G. japonicum,
G. kernia num, G. nelsoni, G. nidus-avis and G. yamadae.
Molecular phylogeny and species delimitation
Several rust sori were excised from each specimen and DNA
was extracted by means of a Gentra Puregene Tissue Kit
(Qiagen, Valencia, CA) according to the manufacturer’s instruc-
tions. For some old fungarium specimens, DNA extraction was
diluted 50–100-fold to successfully amplify the target fragment.
To study the phylogenetic position of each taxon, three nuclear
ribosomal RNA gene regions, the internal transcribed spacer re-
gions and intervening 5.8S nrRNA gene (ITS), the large subunit
(LSU) and the small subunit (SSU) rDNA were amplified, and a
nested PCR method was employed to improve the amplification.
Detailed information of primers and annealing temperatures
of these target fragments followed that of Zhao et al. (2016).
To clarify the phylogenetic placement of the genus Gymnospor-
angium, sequences of rDNA SSU-ITS-LSU from 703 repre-
sentative taxa belonging to 77 genera within the order Puc-
ciniales, which cover 14 morphologically defined families,
were included for phylogenetic analyses. These representative
taxa were selected based on previous phylogenetic studies as
listed in Table S1. Due to alignment difficulties, ITS1 regions
in all taxa were excluded from further analyses. Eight species
of Helicobasidium, Insolibasidium, Jola, Septobasidium and
Tuberculina of three orders, Helicobasidiales, Platygloeales
and Septobasidiales from the subphylum Pucciniomycotina
were selected as outgroups. At species level in Gymnospo-
rangium, rDNA SSU, ITS and LSU were successfully amplified
from 184 fungarium specimens, and sequence data of rDNA
SSU, ITS and LSU from 212 specimens of Gymnosporangium
were retrieved from GenBank. All these specimens used for
phylogenetic studies were listed in Table S2, together with
their GenBank accession numbers and other information.
Endoraecium tropicum was selected as outgroup based on
phylogeny of the order Pucciniales. In the final alignment, raw
sequence data were aligned by Bioedit v. 7.0.9 (Thompson et
al. 1997), and multiple alignments were performed with MAFFT
v. 7.394 (Katoh et al. 2017). SSU, ITS and LSU were combined
to yield the best results for the phylogeny. Topologies were
constructed based on maximum likelihood (ML) analyses using
RAxML v. 0.95 (Stamatakis 2006). Bayesian Markov chain
Monte Carlo (MCMC) analyses were performed using MrBayes
v. 3.1.2 (Huelsenbeck & Ronquist 2001), and Bayesian poste-
rior probabilities (Bpp) were calculated. In ML and Bayesian
analyses, the best-fit substitution model was estimated using
Modeltest v. 3.7 (Posada & Crandall 1998).
Morphological examination
Detailed morphological characters of each loaned specimen
were observed under the dissecting microscope (DM) (SMZ745,
Nikko, Japan), light microscope (LM) (Axio Imager A2, ZEISS,
Germany) and a scanning electron microscope (SEM) (Quanta
200, FEITM, USA) as outlined in Zhao et al. (2017). Morphologi-
cal characteristics were compared with that of the type speci-
mens, original descriptions, and other published descriptions of
species involved (e.g., Kern 1908, 1973, Sydow & Sydow 1915,
Arthur 1934, Kuprevich & Tranzschel 1957, Wilson & Hender-
son 1966, Hiratsuka et al. 1992, Lee & Kakishima 1999a, b,
Yun et al. 2009). The different spore stages of rust fungi were
designated by the following Roman numerals: spermogonia/
spermatia (0), aecia/aeciospores (I), uredinia/urediniospores
(II), telia/ teliospores (III), and basidia/basidiospore (IV).
RESULTS
To clarify the phylogenetic relationship and familial placement
of the genus Gymnosporangium, representative taxa of the
Pucciniaceae and closely related families were included in the
ML and Bayesian inference, which resulted in similar topolo-
gies. The phylogeny provides the best phylogenetic coverage
of species, genera and families in Pucciniales to date, and up
to 33 potential familial groups were recognised (Fig. 1a–e, Fig.
S1). We recognised polyphyly of 14 traditional morphologically
defined families within the order Pucciniales (Fig. 1a– e). Within
the family Pucciniaceae, species in Puccinia or Uromyces
species were clustered together in one phylogenetic group
representing Pucciniaceae s.str. (Fig. 1a, S1). However, spe-
cies in Gymnosporangium were found in one well-supported
phylogenetic group (Bootstrap values = 1.000/ 90), and it was
phylogenetically distinct from Pucciniaceae s.str. (Fig. 1a– d),
although species in both phylogenetic groups had previously
been classified in the Pucciniaceae due to morphological simi-
70 Persoonia – Volume 45, 2020
Cronartium ribicola HMAS57284
Chrysomyxa purpurea KX225401
Chrysomyxa diebuensis KX225393 (T)
Chrysomyxa rhododendri GU049467+GU049560
Chrysomyxa sp. 1 HMAS248121
Chrysomyxa rhododendri AY657009+DQ200930+AY700192
Chrysomyxa empetri GU049434+GU049526
Cronartium arizonicum HMAS56424
Sphenospora kevorkianii DQ354522+DQ354521
Chrysomyxa neoglandulosi GU049498+GU049550
Chrysomyxa rhododendri KJ746824+KJ698630
Chrysomyxa nagodhii GU049431+GU049524
Cronartium ribicola ZP-R588
Macruropyxis sp. 1 ZP-R1351
Cronartium ribicola HMAS52871
Cronartium ribicola KU320184
Chrysomyxa tsukubaense AB191242+AB191241 (T)
Cronartium comandrae JN943237
Cronartium ribicola DQ533975+AF522166
Cronatium sp. HMAS3228
Cronartium ribicola HMAS38589
Macruropyxis sp. 2 KU532277+KU532269+KU532273
Cronartium ribicola ZP-R524
Chrysomyxa rhododendri HMAS1883383
Peridermium harknessii M94339+L76506
Chrysomyxa chiogenis GU049452+GU049532
Cronatium ribicola HMAS38376
Chrysocyclus sp. 1 ZP-R2060
Chrysocelis muehlenbeckiae EU851158
Chrysomyxa rhododendri GU049471+GU049570
Cronartium ribicola ZP-R1318
Cronartium strobilinum JN943192
Macruropyxis sp. 2 ZP-R597
Macryriotxus fraxini ZP-R638
Cronartium occidentale L76507
Cronartium appalachianum L76484
Chrysocyclus sp. 2 ZP-R905
Endocronartium harknessii AY665785+DQ206982+AY700193 (AFTOL-ID 456)
Macruropyxis sp. 3 ZP-R316
Chrysocyclus cestri EU851157
Cronartium comandrae MG806102
Chrysomyxa vaccinii GU049463+GU049561
Cronartium ribicola HMAS37553
Chrysomyxa purpurea KX225403 (T)
Cronartium ribicola HMAS112046
Macruropyxis sp. 2 ZP-R618
Chrysomyxa monesis GU049479+GU049566
Chrysomyxa woroninii GU049462+GU049540
Macruropyxis fraxini KP858144+KP858145 (T)
Chrysomyxa ledicola GU049417+GU049520
Chrysomyxa pyrolae GU049487+FJ666456
Cronartium comandrae HMAS2656
Cronartium ribicola ZP-R486
Chrysomyxa zhuoniensis KX225396 (T)
Macruropyxis sp. 2 ZP-R596
Peridermium bethelii L76479
Cronartium ribicola R901
Cronartium quercuum JN943198+DQ185028
Cronartium comandrae L76481
Cronartium coleosporioides AY955834
Cronartium conigenum L76486
Sphenospora smilacina KM217371+KM217354
Cronartium quercuum ZP-R7
Macruropyxis sp. 1 ZP-R579
Chrysomyxa piperiana GU049497+GU049565
Sphenorchidium xylopiae CUP-737
Chrysomyxa arctostaphyli NG 013161+NG 027640 (AFTOL-ID 442)
Chrysomyxa ledi HM037711+HM037707
Chrysomyxa qilianensis KR824128 (T)
Cronartium arizonicum L76504
Macryriotxus fraxini DQ354523+DQ354522
1/98
0.93/91
0.79/-
0.8/98
1/100
0.70/67
0.97/0.77
0.74/-
0.70/-
0.75/-
0.74/-
0.77/55
0.77/100
0.71/97
1/99
0.74/-
0.86/94 1/100
0.76/60
0.77/810.99/94
0.76/60
0.77/70
0.90/50
0.96/79
0.85/-
0.80/-
1/95
1/81
0.93/51
0.90/70
-/61
0.76/97
0.78/73
Coleosporiaceae 1
(Phylogenetic group 4)
Cronartiaceae
(Phylogenetic group 3)
(Phylogenetic group 2)
Family incertae sedis
Pucciniaceae
sensu stricto
(Phylogenetic group 1)
Fig. 1 Multilocus phylogenetic tree of order Pucciniales based on rDNA SSU-ITS-LSU sequence data. Support values indicated at nodes. Bayesian posterior
probabilities ≤ 50 % and Maximum Likelihood bootstrap (ML) ≤ 50 % were indicated by dash line (–). Family names were listed after each taxon based on
Cummins & Hiratsuka (2003).
71
P. Zhao et al.: Gymnosporangium on Malus
Fig. 1 (cont.)
Melampsora rostrupii EU808038+JN934942
Melampsora albertensis JX416848+JX416843
Melampsora weirii GU049472+FJ666458
Melampsora sp. 2 ZP-R386
Melampsora pruinosae GQ479899+JN934938
Melampsora epiphylla KF780787+KF780670 (T)
Melampsora salicis-bakko KC631854+KC685611 (T)
Coleosporium solidaginis GU058009
Melampsora salicis-albae KF780757+KF780640
Coleosporium pedicularidis KP017554+KP017564
Coleosporium sp. 2 ZP-R1383
Coleosporium euodiae KP017557+KP017567
Coleosporium solidaginis HQ317530
Melampsora salicis-sinicae KC631839+KC685596 (T)
Coleosporium zanthoxyli ZP-R895
Melampsora salicis-purpureae KF780766+KF780649 (T)
Coleosporium carpesii ZP-R1302
Melampsora sp. 5 HMAS248120
Melampsora sp.3 HMAS248119
Melampsora kamikotica KF780760+KF780643 (T)
Coleosporium sp. 2 ZP-R202
Melampsora occidentalis JN881740+JN934934
Melampsora larici-tremulae JN881744+JN934956
Coleosporium senecionis KJ746818+KJ716348
Melampsora sp. 3 ZP-R397
Coleosporium plumeriae KF879087
Melampsora coleosporioides KF780755+KF780638
Coleosporium solidaginis ZP-R726
Coleosporium geranii ZP-R875
Melampsora aecidioides EU808021+FJ666510
Melampsora weirii GU049474+GU049545
Melampsora pakistanica KX237555+KX237556
Melampsora weirii GU049473+GU049544
Melampsora medusae f. sp. deltoidis GQ479307+JN934962
Melampsora pulcherrima GQ479320+JN934941
Melampsora lini AY125396+L20283
Melampsora salicis-viminalis KF780732+KF780615 (T)
Melampsora magnusiana GQ479845+JN934927
Melampsora microsora KF780834+KF780717 (T)
Coleosporium campanulae KP017555+KP017565
Coleosporium sp. 1 ZP-R1381
Coleosporium sp. 2 ZP-R1384
Melampsora sp. 1 ZP-R536
Melampsora laricis-pentandrae KF780801+KF780684
Coleosporium solidaginis DQ354558+DQ354559
Coleosporium sp. 2 ZP-R9
Melampsora sp. 1 ZP-R489
Melampsora microspora JN881737+JN934931
Melampsora sp. 4 CUP-606
Coleosporium tussilaginis ZP-R1311
Melampsora yezoensis KF780833+KF780730 (T)
Melampsora medusae f. sp. tremuloides GQ479883
Melampsora sp. 1 ZP-R488
Coleosporium asterum AY123287+AF522165
Melampsora allii-populina JN881728+JN934902
Melampsora nujiangensis JN881739+JN934933
Melampsora pinitorqua EU808035+FJ666523
Melampsora abietis-canadensis JN881733+JN934918
Melampsora sp. 2 ZP-R608
Coleosporium sp. 1 HMAS248103
Coleosporium sp. 1 ZP-R399
Coleosporium senecionis ZP-R619
Melampsora salicis-argyraceae KF780733+KF780616 (T)
Coleosporium tussilaginis KT199383+KT199395
Coleosporium tussilaginis ZP-R2010
Melampsora ferrinii KJ136570+KJ136563 (T)
Coleosporium sp. 2 HMAS248099
1/100
1/100
0.79/100
1/100
0.96/-
0.91/83
1/100
1/99
0.91/95 0.85/100
1/100
1/94
0.86/71
1/100
0.73/62
1/100
-/87
1/99
0.70/60
0.75/97
0.72/57
0.98/99
0.87/99
0.98/77
0.75/50
0.70/54
-/78
0.70/69
1/100
1/100
1/91
Melampsoraceae
(Phylogenetic group 6)
Coleosporiaceae 2
(Phylogenetic group 5)
72 Persoonia – Volume 45, 2020
Fig. 1 (cont.)
Uredinopsis pteridis KM249869
Pucciniastrum boehmeriae AB221452
Melampsoridium hiratsukanum KF031565+KF031547
Pucciniastrum coriariae ZP-R412
Uredinopsis sp. AY123306+AF522181
Gerwasia rubi ZP-R345
Phragmidium tormentillae DQ354552+DQ3545532
Phragmidium mucronatum ZP-R509
Pileolaria toxicodendri DQ092921+AY745698
Melampsoridium hiratsukanum KF031550+KF031533
Triphragmium sp 1. ZP-R410
Naohidemyces vaccinii KJ698628
Pileolaria terebinthi HM639744
Hyalopsora polypodii AB011015+AF426229
Pucciniastrum boehmeriae AB221452
Triphragmium ulmariae AY125402+AF426219
Pucciniastrum coriariae ZP-R113
Phragmidium potentillae KT199403
Kuehneola uredinis DQ092919+DQ911604+AY745696
Gymnoconia peckiana JF907677
Naohidemyces vaccinii DQ354562+DQ354563
Milesina philippinensis KM249868
Kuehneola uredinis MF158088+MF158087
Phragmidium sp. 3 ZP-R484
Kuehneola uredinis GU058013
Pileolaria brevipes AY123314+DQ323924
Trachyspora intrusa DQ354549+DQ354550
Phragmidium mexicanum LN795902+LN795901
Pucciniastrum myosotidii ZP-R1356
Gerwasia rubi AY125388+KT199397
Pileolaria toxicodendri ZP-R252
Thekopsora rubiae KC415802+KC416009
Phragmidium violaceum KJ746822+KJ716351
Pucciniastrum pustulatum KJ746816+KJ698631
Phragmidium rubi-idaei AY125405+KU059163
Pucciniastrum coriariae ZP-R420
Phragmidium mucronatum HQ412646
Phragmidium violaceum ZP-R214
Phragmidium barnardii AY125406+KT199402
Pucciniastrum circaeae AB221456+AB221387
Phragmidium tuberculatum AY123313+KJ841923
Phragmidium sp. 2 ZP-R318
Pucciniastrum goeppertianum AY123305+AF522180
Melampsoridium betulinum AY125391+AF125177+DQ354561
Triphragmium sp 1. ZP-R565
Phragmidium rosae-multiflorae KU059176
Phragmidium mucronatum ZP-R615
Gymnoconia peckiana GU058010
Uredinopsis filicina AF426237
Phragmidium sp. 4 ZP-R110
Pucciniastrum epilobii AY123303+AF522179
Trachyspora intrusa AF426220
Pucciniastrum boehmeriae AB221449
Pileolaria sp. 1 ZP-R1369
Triphragmium ulmariae AY125401+JF907676
Pileolaria sp. 2 ZP-R659
Pucciniastrum boehmeriae AB221451+AB221391
Pucciniastrum boehmeriae KF711854
Phragmidium mexicanum ZP-R1391
Phragmidium sp. 3 HMAS248114
Thekopsora nipponica KC415793+KC416003
Hyalopsora polypodii KJ746817+KJ698627
Melampsorella caryophyllacearum AY123298+AF426232
Hyalospora aspidiotus AY123291
Phragmidium mexicanum ZP-R1384
Pucciniastrum myosotidii KJ746815+KJ716347
Melampsoridium hiratsukanum KF031552+KF031535
Melampsoridium sp. 1 ZP-R711
Pucciniastrum goeppertianum AY123305+AF522180
Thekopsora minima KT199391+KC763340
Phragmidium punjabense KX358855
Phragmidium sp. 3 ZP-R491
Phragmidium mexicanum ZP-R576
Melampsoridium hiratsukanum KF031551+KF031542
Pileolaria toxicodendri ZP-R475
Phragmidium mexicanum ZP-R1382
Melampsoridium betulinum ZP-R490
Pucciniastrum boehmeriae AB221450+AB221393
Gerwasia rubi ZP-R328
1/89
-/71
0.87/87
0.92/81
0.89/65
0.99/84
-/60
0.97/79
0.99/85
0.76/51
0.76/92
1/100
1/100
-/70
0.98/84
1/97
1/74
1/91
0.75/-
0.77/60
0.70/60
1/91
0.76/98 1/100
0.97/85
1/100
0.76/53
0.99/66
1/100
1/100
1/99
1/99
1/95
0.82/61
1/100
1/97
-/74
0.70/69
1/100
0.91/80
1/99
0.75/68
1/100
0.77/85
1/98
1/95
0.98/57
(Phylogenetic group 12)
(Phylogenetic group 11)
Phragmidiaceae 1
(Phylogenetic group 10)
Pileolariaceae 1
(Phylogenetic group 9)
(Phylogenetic group 8)
(Phylogenetic group 7)
Family incertae sedis
Pucciniastraceae
Raveneliaceae 1
Phragmidiaceae 2
73
P. Zhao et al.: Gymnosporangium on Malus
Fig. 1 (cont.)
Allodus podophylli DQ354544+DQ354543 (T)
Gymnosporangium speciosum KJ720160
Allodus podophylli AB011054
Gymnosporangium yamadae HMAS80628
Gymnosporangium asiaticum ZP-R201
Allodus podophylli JQ423259
Gymnosporangium niitakayamense KP308395
Tranzschelia fusca KX228775
Gymnosporangium kanas ZP-R481
Ochropsora ariae KX228773+KX228778
Neophysopella euvitis AB354787+AB354750
Neophysopella meliosmae KC815596+KC815655
Neophysopella ampelopsidis KC815570+KC815629
Gymnosporangium clavipes KJ720155
Neophysopella sp. 1 ZP-R244
Nyssopsora sp 1. ZP-R360
Gymnosporangium globosum KJ720174
Gymnosporangium ellisii KJ720156
Uromycladium tepperianum KJ633027+KJ632995+KJ632988
Ochropsora ariae KX228772+KX228777
Gymnosporangium asiaticum ZP-R1375
Gymnosporangium niitakayamense KY964758
Tranzschelia discolor KX985768
Tranzschelia mexicana KP308391
Nyssopsora sp 1. ZP-R523
Rostelia sp. 1 ZP-R470
Gymnosporangium vauqueliniae KJ720186
Gymnosporangium yamadae ZP-R637
Uromycladium sp. 1 HMAS248122
Gymnosporangium trachysorum KJ720184
Gymnosporangium corniculans KJ720167
Uromycladium notabile KJ6330301+KJ633011+KJ632992
Gymnosporangium tremellloides KJ720164
Gymnosporangium asiaticum HMAS17719
Rostelia sp. 2 HMAS248111
Gymnosporangium asiaticum HMAS172366
Neophysopella orientalis KC815657+KC815598
Gymnosporangium huanglongense KT19168+KT19162
Gymnosporangium connersii HMAS75220
Allodus podophylli ZP-R419
Gymnosporangium juniperi-virginianae
KJ720176
Gymnosporangium asiaticum KP308392
Nyssopsora echinata AY123312
Neophysopella vitis KC815576+KC815635
Uromycladium simplex KJ633029+KJ633010+KJ632990
Neophysopella meliosmae-myrianthae KC815601+KC815542
Gymnosporangium niitakayamense KY964760
Gymnosporangium asiaticum ZP-R203
Neophysopella sp. 1 HMAS248115
Gymnosporangium asiaticum CUP-20544
Gymnosporangium nootkatense KJ720159
Nyssopsora echinata U77061
Rostelia sp. 1 ZP-R469
Gymnosporangium nelsonii ZP-R83
Gymnosporangium kernianum KJ720177
Gymnosporangium kanas HMAS246105 (T)
Allodus podophylli JQ423258
Gymnosporangium asiaticum KP308394
Uromycladium fusisporum KJ633009+KJ632991+KJ633031
Neophysopella montana KC815584+KC815643
Uromycladium robinsonii KJ633032+KJ633012+KJ632989
Gymnosporangium nidus-avis KJ720181
Gymnosporangium multiporum KJ720179
Gymnosporangium brucensis KJ720188
Allodus sp 1. KJ720156
Allodus sp 1. NYSF53829
Gymnosporangium asiaticum ZP-R960
Leucotelium pruni-persicae AB097452+AB097450
Gymnosporangium brucensis KJ720189
Gymnosporangium exiguum KJ720170
Gymnosporangium sabinae KJ720183
Allodus podophylli ZP-R244
Gymnosporangium cupressi KJ720169
Allodus podophylli JQ423260
Gymnosporangium huanglongense NR154077+KT19161
Gymnosporangium asiaticum ZP-R215
Gymnosporangium nelsonii KJ720180
Gymnosporangium asiaticum ZP-R204
Tranzschelia pruni-spinosae KX228774
Gymnosporangium yamadae ZP-R635
Gymnosporangium asiaticum ZP-R1376
Gymnosporangium connersii KJ720166
0.75/61
0.93/70
0.73/98
0.89/81
0.97/98
0.82/64
0.82/64
0.85/96
0.84/94
1/100
1/100
0.89/95
-/65
-/63
1/91
1/100
1/95
1/60
1/92
0.90/84
0.80/-
1/91
1/100
1/99
0.95/79
1/90
1/84
0.90/80
1/100
0.70/-
0.96/54
0.84/74
1/97
0.95/-
0.72/60
1/100
0.81/87 0.80/51
1/100
1/100
0.96/99
0.86/100
0.79/99
(Phylogenetic group 19)
Gymnosporangiaceae fam. nov.
(Phylogenetic group 18)
(Phylogenetic group 17)
(Phylogenetic group 16)
(Phylogenetic group 15)
(Phylogenetic group 14)
(Phylogenetic group 13)
(Phylogenetic group 20)
(Phylogenetic group 21)
Pileolariaceae 2
Raveneliaceae 2
Uropyxidaceae 1
Chaconiaceae 1
Uropyxidaceae
2
Phakopsoraceae
1
Family incertae sedis
Family incertae sedis
74 Persoonia – Volume 45, 2020
Fig. 1 (cont.)
Dasyspora guianensis JF263503+ JF263479 (T)
Dasyspora nitidae JF263506+ JF 263487 (T )
Dasyspora mesoamericana JF263504+ JF 263480 (T )
Dasyspora winteri JF263508+ JF 263492 (T )
Dasyspora frutescenti s JF 263501+JF 263471 (T )
Dasyspora frutescenti s JF 263499+JF 263467 (T )
Dasyspora amazonica JF263496+J F263460 ( T)
Dasyspora emarginatae JF263498+ JF 263465 (T )
Dasyspora gregaria JF263502+ JF 263477 (T )
Dasyspora echinata JF263497+JF263462 ( T)
Dasyspora segregaria JF263507+ JF 263488 (T )
Austropuccinia psidii KM282154 (T)
Austropuccinia psidii KF318458+KF318434+KF318453
Dietelia duguetiae KM217365+KM217382
Puccorchidium popowiae KM217353 (T )
Puccorchidium polyalthiae JF263509+ JF 263493
Sphenorchidium xylopiae KM217372+KM217355 ( T)
Sphaerophragmium ac aciae KJ862350+KJ862429
Kweilingia divina DQ354554
Kweilingia divina EF192212
Kweilingia sp. 1 ZP-R388
Dasturella divina AY123288
Dasturella divina ZP-R833
Prospodium tuberculatum KJ396196+KJ396195
Prospodium lippiae DQ831024+ DQ 354555 (AFTOL-ID 1401)
Prospodium gentryi KY800407
Porotenus biporus JF263510+ JF263494
Ravenelia ec hinata D Q145756
Ravenelia ec hinata var. ectypa DQ 323925
Ravenelia havanensis DQ354556+ DQ3545572
Kernkampella breyniae KJ862428+KJ862346
Phakopsora pachyrhizi HMAS70143
Phakopsora pachyrhizi ZP-R381
Phakopsora pachyrhizi HMAS49224
Phakopsora pachyrhizi ZP-R283
Phakopsora pachyrhizi DQ354536+DQ354537
Phakopsora sp. 1HMAS248098
Phakopsora sp. 1ZP-R208
Phakopsora sp. 2 ZP-R451
Cerotelium fici KP753385
Phakopsora tecta DQ354535
Batistopsora pistila KF528043+KF528026
Batistopsora crucis-filii KF528041+KF528016
Batistopsora crucis-filii DQ354538+ DQ 354539
Phakopsora myrtacearum NR_132913+KP729473 (T )
Cerotelium fici MF 580676
Phakopsora cherimoliae KF528040+KF528011
Massee ёlla capparis JX 136798
Phakopsora argentinensis KF528039+KF528009
Phakopsora phyllanthi KF528042+KF528025
Endoraecium irroratum KJ862407+KJ862366+KJ862312 (T )
Endoraecium podalyriifolium KJ862414+KJ862387+KJ862334 (T )
Endoraecium maslinii KJ862408+KJ862367+KJ862314 (T )
Endoraecium falciforme KJ862405+KJ862360+KJ862439 ( T)
Endoraecium tropicum KJ862417+KJ862392+KJ862337 ( T)
Endoraecium auriculiforme KJ862355+KJ862298 (T )
Racospermyces koae DQ323919+ DQ 323918
Olivea sp 1. ZP-R212
Olivea scitula DQ354540+ DQ 354541
Achrotelium sp. 1 HMAS45350
HMAS11840
HMAS248101
Achrotelium ichinocarpi ZP-R1394
Achrotelium ichnocarpi KT199381+KT199393
Hemileia vastatrix DQ354565+ DQ354566
Hemileia aff. wrightiae KT199386+KT199400
Mikronegeria alba DQ354569
Mikronegeria fuc hs iae KJ746826+KJ716350
Blastospora s milacis ZP-R2040
Blastospora smilac is D Q354567+D Q354568
Zaghouania phillyreae ZP-R223
Zaghouania phillyreae ZP-R222
Zaghouania sp. 1 ZP-R262
Zaghouania sp. 1 HMAS248117
Cys topsora notelaeaeKT199384+KT199396
Caeoma torreyae AY123284+AF522183
Tuberculina sp. KJ746823+KJ698632
Helicobasidium longisporum AY292432+AY292405
Helicobasidium mompa U77064+AY292429+AY254179
Platygloea disciformis DQ234563+ DQ234556+AY629314
Insolibasidium deformans AY123292+AF522169
Jola cf. javensis DQ416206+ DQ416207
Septobasidium fumigatum DQ 241415+D Q241451+D Q241484
Septobasidium alni DQ241405+ DQ 241441+DQ 241474
Helicobasidiales
Platygloeales
Septobasidiales
Phakopsoraceae 2
Raveneliaceae
3
Sphaerophragmiaceae
1/100
1/100
0.99/75
1/100
0.95/84
1/98
1/96
0.82/75 -/-
0.80/72
0.91/87
0.80/72
-/-
-/-
0.86/84
1/91
1/100
1/100
1/100
0.91/86
1/100
1/97
1/100
1/100
1/100
1/100
1/100
1/97
1/92
1/100
0.83/75
1/88
1/100
1/100
0.76/68
1/94
0.80/59
0.90/-
1/100 1/100
1/82
0.99/98
0.85/76
0.90/59
1/81 1/100
1/99
0.90/72
1/100
-/55
-/52
1/91
1/100
1/100
1/100
1/100
1/100
-/55
1/99
-/-
1/100
Phakopsora meibomiae EU851164+GQ146467
(Phylogenetic group 26)
(Phylogenetic group 25)
(Phylogenetic group 22)
(Phylogenetic group 23)
(Phylogenetic group 22)
(Phylogenetic group 33)
Mikronegeriaceae
1
(Phylogenetic group 32)
(Phylogenetic group 31)
(Phylogenetic group 30)
(Phylogenetic group 29)
(Phylogenetic group 28)
(Phylogenetic group 27)
Family incertae sedis
Prospodium tuberculatu m K
J396
1
96
+K
J396
1
95
Prospodium lippiaeD
Q
831024+D
Q
354555
(
AFT
O
L-ID 1401
)
Prospodium gentr
y
i K Y
800
4
07
Porotenus biporus
J
F2
635
1
0
+
J
F2
63
4
9
4
R li hi t
DQ1 4 6
1/100
1
/82
0
.
99/98
0.85/76
0 8 / 6
(
Ph
y
lo
g
enetic
g
roup 24
)
Achrotelium sp. 1
Achrotelium sp. 1
Raveneliaceae 3
Uropyxidaceae
3
Pileolariaceae 3
Chaconiaceae 2
Chaconiaceae 3
Mikronegeriaceae
2
Family incertae sedis
Family incertae sedis
75
P. Zhao et al.: Gymnosporangium on Malus
Juniperus sp. HMAS6725
Amelanchier sp. KJ720167
Malus sp. ZP-R633
Aroma atropurpurea CUP-776
Juniperus horizontalis NYBG199427
Malus domestica CUP-51030
Malus baccata HMAS80528
Malus coronaria CUP-24468
Malus domestica CUP-19705
Malus domestica CUP-19919
Juniperus virginiana KJ720176
Juniperus sp. AY123289+AF522167
Pyrus calleryana KY798386
Juniperus chinensis GU058012
Juniperus virginiana NYBG3009468
Malus micromalus LIG_4
Malus prunifolia HMAS36992
Juniperus chinensis NYBG3009549
Juniperus horizontalis NYBG193254
Malus micromalus LIG_1
Juniperus virginiana NYBG461220
Malus micromalus CUP-20612
Malus domestica CUP-731
Juniperus chinensis KR814566+KT719163
Malus domestica CUP-21697
Malus domestica CUP-20165
Juniperus virginiana HMAS43709
Malus prunifolia HMAS30992
Crataegus sp. KY798356
Malus domestica CUP-14
Juniperus virginiana DQ267127+AY629316 (AFTOL-ID 712)
Juniperus virginiana MG917687+MG907217
Malus coronaria CUP-45235
Juniperus virginiana KJ720174
Juniperus chinensis cv. kaizuka FJ848763
Malus domestica CUP-20161
Juniperus virginiana KJ720184
Malus micromalus LIG_2
Malus miura NYBG2584
Malus domestica CUP-20164
Juniperus chinensis HMAS82779
Malus baccata HMAS55351
Malus domestica CUP-1553
Juniperus virginiana NYBG23036
Malus domestica CUP-17321
Malus sp. ZP-R634
Malus sp. CUP-20162
Malus micromalus HMAS199333
Malus ioensis CUP-595
Juniperus chinensis FJ559375
Malus baccata HMAS74424
Juniperus chinensis HMAS79065
Amelanchier alnifolia HM591299
Malus coronaria CUP-55712
G. connersii KJ720166
Juniperus chinensis HMAS82179
Juniperus horizontalis KJ720180
Juniperus sabina HMAS143619
Malus coronaria CUP-24473
Malus domestica KY964761
Malus micromalus LIG_3
Juniperus chinensis HMAS47229
Malus toringo FJ455091
Crataegus brunetiana CUP-55918
Malus domestica CUP-20153
Malus domestica CUP-20257
Malus angustifolia CUP-24472
Juniperus horizontalis KJ720163
Juniperus virginiana KY798387
Juniperus scopulorum HQ317506
Malus sp. ZP-R635
Malus micromalus HMAS55353
Malus domestica CUP-882
Malus coronaria CUP-45235
Malus sp. ZP-R83
Juniperus virginiana NYBG237070
Amelanchier canadensis CUP-3087
Juniperus chinensis KJ720187
Malus spectabilis NYBG53757
Malus micromalus ZP-R16
Juniperus chinensis HMAS135611
Juniperus virginiana NYBG237046
Juniperus chinensis KR814567+KT719164
Juniperus virginiana HQ317510
Juniperus horizontalis NYBG193243
Juniperus scopulorum HMAS2218
Pyrus sp. KY800408
Juniperus chinensis var. kaizuka FJ848764
Juniperus virginiana NYBG1391099
Malus glaucescens CUP-594
Malus baccata HMAS80628
Malus domestica CUP-20157
Malus domestica CUP-24468
Malus micromalus HMAS243188
G. trachysorum
G. corniculans
Gymnosporangium
sp. 1
G. nelsonii
G. juniperi-virginianae
G. yamadae
100/1.00
100/1.00
66/-
77/0.91
84/0.95
100/1.00
100/1.00
68/-
68/0.95
-/0.75
59/0.91
64/0.75
98/1.00
75/-
-/0.80
91/1.00
77/0.95
-/0.75
83/1.00
59/-
Fig. 2 Multilocus phylogenetic tree of Gymnosporangium species based on rDNA SSU, ITS and LSU sequence data. One of the best trees were shown and
support values indicated at nodes. ML bootstrap ≤ 50 % and Bayesian posterior probabilities ≤ 50 % were indicated by dash line (–). Taxa names in bold
represent species with their aecial hosts on Malus species.
76 Persoonia – Volume 45, 2020
Fig. 2 (cont.)
Photinia niitakayamensis
KP308395
Malus pumila
ZP-R1376
Juniperus chinensis cv. kaizuka FJ848744
Malus spectabilis
HMAS12970
Pyrus lindleyi MF3773961
M. ioensis var. plena CUP-57311
Juniperus chinensis var. globosa
FJ848767
Malus pumila
ZP-R215
Juniperus przewalskii
NR154077+KT719161
Juniperus chinensis
HMAS47728
Malus pumila
ZP-R779
Sabina chinensis
HMAS165302
Malus pumila
HMAS26416
Malus pumila
HMAS56909
Malus pumila
HMAS14327
Juniperus chinensis
KR814569+KT719166
Malus pumila
ZP-R228
Juniperus chinensis HMAS172366
Juniperus chinensis
KY964754
Pyrus pyrifolia
KP308394
Juniperus chinensis
KY964736
Juniperus chinensis var. kaizuka
FJ848747
Juniperus chinensis
KR814568+KT719165
Malus pumila
ZP-R205
Malus domestica HMAS135289
Cotoneaster dammeri HMAS248105
Juniperus chinensis KX355285
Juniperus chinensis
EF990780
Juniperus chinensis cv. kaizuka FJ848741
Juniperus przewalskii
KT719168+KT719162
Pyrus pyrifolia
KP308393
Malus sp. HMAS24616
Malus spectabilis
HMAS55351
Juniperus chinensis
KP308392
Photinia niitakayamensis
KY964759
Juniperus chinensis var. kaizuka
FJ848743
Juniperus chinensis KX355282
Malus pumila
ZP-R773
Juniperus chinensis var. sargentii
FJ848769
Malus pumila
ZP-R203
Juniperus chinensis var. globosa FJ848768
Juniperus chinensis KY964753
Photinia niitakayamensis
KY964760
Malus pumila
HMAS135598
Malus pumila
ZP-R614
Malus pumila
ZP-R204
Juniperus chinensis
KX355281
Cotoneaster dammeri ZP-R481
Juniperus chinensis
KX355284
Malus pumila
HMA14328
Malus pumila
ZP-R774
Juniperus chinensis KY964737
Juniperus chinensis
HMAS47228
Juniperus chinensis
HMAS11935
Malus domestica
HMAS11217
Juniperus chinensis
KJ720161
Sabina tibetica
HMAS37835
Malus pumila
ZP-R876
Juniperus excelsa
HMAS45640
Juniperus chinensis
HMAS165302
Malus pumila
ZP-R301
Malus sp. CUP-20544
Photinia niitakayamensis
KY964758
Malus pumila
HMAS38649
Malus pumila
ZP-R1412
Malus pumila
ZP-R778
Malus pumila
ZP-R961
Juniperus chinensis var. kaizuka
FJ848745
Juniperus chinensis
HMAS2503
Malus sp. CUP-17524
Juniperus chinensis var. sargentii
FJ848742
Malus pumila
ZP-R1375
Malus pumila
HMAS17719
Malus sp. NYBG60678
Malus pumila
ZP-R960
Juniperus chinensis var. kaizuka
FJ848746
Malus asiatica
HM172325
Malus spectabilis
HMAS11219
Juniperus chinensis KX355286
Juniperus chinensis
HMAS47229
Pyrus lindleyi
MF377396
Malus pumilia HMAS38650
Cupressus duclouxia
HMAS135599
Malus pumila
ZP-R201
Juniperus chinensis
HMAS172366
Juniperus chinensis cv. kaizuka
FJ848750
G. niitakayamense
G. huanglongense
G. kana
s
sp. nov.
G. asiaticum
100/1.00
99/1.00
94/1.00
100/1.00
58/0.78
66/0.71
65/-
71/0.83
Malus spectabilis HMAS26416 G. spinulosa sp. nov.
77
P. Zhao et al.: Gymnosporangium on Malus
Fig. 2 (cont.)
G. globosum
G. torminali-juniperini
Juniperus phoenicea subsp. turbinata KP261044
Juniperus koehneana KX528447+KX814560
Malus kansuensis HMAS38649
Juniperus virginiana HMAS14419
Pyrus communis HM1142211
Juniperus sp. KF925318
Juniperus chinensis KJ720183
Pyrus communis KP2610391
Malus kansuensis HMAS33357
Pyrus communis JN969966
Juniperus sp. HMAS14315
Juniperus phoenicea subsp. turbinata KT160251+KT160253
Sorbus alnifolia KJ720182
Malus sylvestris CUP-56165
Malus communis NYBG461234
Juniperus koehneana NR1540731+KR814560
Juniperus rigida FJ848770
Juniperus formosana KY964743
Sorbus americana KY764066
Pyrus communis AF426209
Juniperus virginiana KJ720181
Juniperus phoenicea subsp. turbinata KT160250+KT160254
Pyrus communis KY964764
Juniperus phoenicea subsp. turbinata KM403108+KM403111
Juniperus communis KJ720185
Juniperus virginiana NYBG237085
Malus pumila HMAS44394
Sorbus torminalis MG572220
Juniperus chinensis FJ848751
Malus spectabilis HMAS12940
Crataegus mexicana KX137840
Juniperus rigida KJ720168
Juniperus sabina HMAS143609
Juniperus rigida FJ848766
Juniperus virginiana NYBG237080
Juniperus oxycedrus KT160252
Juniperus chinensis var. horizontalis FJ848758
Jniperus juvenescens NYBG461234
Sorbus torminalis MH169341
Amelanchier ovalis KP261040+KP261041
Juniperus sp. KF925320
Malus pumila HMAS44514
Malus kansuensis ZP-R14
Juniperus deppeana KM382968
Juniperus phoenicea subsp. turbinata KM403109
Juniperus sp. KF925317
Juniperus przewalskii KX528446+KX528444
Juniperus sp. KF925316
Juniperus virginiana NYBG14419
Juniperus sp. KF925319
Malus kansuensis ZP-R3
Juniperus chinensis FJ848752
Sorbus aucuparia MG561881
Pyrus communis KY964762
Juniperus chinensis var. globosa FJ848759
Chamaecyparis pisifera KJ720178
Pyrus amygdaliformis KY964763
Sorbus aucuparia MG573215
Cupressus arizonica KJ720169
Juniperus chinensis HMAS79186
Sorbus aucuparia MG572221
Amelanchier sp. CUP-227
Pyrus calleryana KU593568
Sorbus aucuparia AF426210
Juniperus oxycedrus KM486547+KM486546
Juniperus virginiana NYBG237071
Juniperus chinensis var. horizontalis FJ848756
Malus sp. CUP-1553
Juniperus przewalskii KX528564+KX528444
Juniperus koehneana KR814562+KR814561
Sorbus aucuparia MG573154+MG573213
Juniperus koehneana KR814565+KR814562
Pyrus communis CUP-12342
Juniperus communis KJ720173
Juniperus communis MG573153+MG573214
Juniperus oxycedrus KM4031101
Juniperus chinensis FJ848755
Crataegus mexicana KX137841
Pyrus communis JN969964
Juniperus chinensis var. sargentii FJ848757
Juniperus virginiana NYBG237094
Sorbus randaiensis KY964751
Juniperus rigida FJ848771
Juniperus formosana KY964741
Juniperus sp. KF925321
Pyrus communis JN969963
Pyrus communis JN969962
Juniperus sabina CUP-0477
Sorbus randaiensis KY964747
Pyrus calleryana JN969965
G. sabinae AY512845
G. sabinae
G. prezewaskii
G. fenzelianum
G. cornutum
G. corniforme
G. amelanchieris
G. nidus-avis
G. monticola
G. japonicum 1
G. miyabei
G. gaeumannii
G. japonicum 2
94/1.00
93/1.00
99/1.00
90/1.00
64/0.80
97/1.00
83/0.94
51/-
91/1.00
77/0.75
57/-
100/1.00
96/1.00
75/0.91
55/-
G. nipponicum
89/1.00
76/0.77
89/0.97
86/1.00
56/-
73/0.89
64/-
77/0.81
78 Persoonia – Volume 45, 2020
Fig. 2 (cont.)
Gymnosporangium
sp. 2
Juniperus communis
KP261048
Pyrus calleryana
KT821552
Chamaecyparis thyoides
KJ720171
Amelanchier ovalis
KY440115
Juniperus communis
KP261048+KP261049
Juniperus oxycedrus
KM486542+KM486544
Juniperus oxycedrus
KU183500
Juniperus communis CUP-2146
Chamaecyparis thyoides
KJ720156
Amelanchier alnifolia
MG907206+MG907218
Juniperus virginiana
KJ720160
M. asiatica
ZP-R420
Crataegus orientalis
HM114220
M. asiatica
ZP-R511
Chamaecyparis
sp. ZP-R1389
Crataegus
sp. NYBG461394
Malus
sp. ZP-R1375
Malus
sp. HMAS248123
G. clavipes
KJ720155
Juniperus virginiana
NYS-F-775
Endoraecium tropicum
KJ862417+KJ862392+KJ862337
Juniperus communis
AF426211
Cydonia oblonga
KM486543+KM486545
Malus communis HMAS24626
Cupressus funebris
HMAS133735
G. clavipes
AY123309
Juniperus communis HMAS67951
Juniperus communis NYBG23203
Malus
sp. ZP-R627
Juniperus oxycedrus
KT160259
G. clavipes
U41566
Vauquelinia angustifolia
KJ720186
Malus domestica
DQ354546+DQ354545
Malus
sp. CUP-13530
Malus
sp. HMAS55353
Juniperus virginiana
KJ720159
Juniperus deppeana
KM382069
Gillenia trifoliata
KJ720170
Pyrus
sp. HMAS244164
Amelanchier sp.
KJ720164
Malus communis CUP-43859
Juniperus monosperma
KJ720179
Juniperus virginiana
CUP-18207
Crataegus monogyna
KY440114
Malus
sp. HMAS248123
Calocedrus decurrens
HMAS45643
Juniperus communis
KT160260
Crataegus
sp. KM382067
Juniperus utahensis
KJ720177
Calocedrus decurrens
HMAS49246
Calocedrus decurrens
AY123290+AF522168
Crataegus mongyna
KP261045
Crataegus mongyna
HM114219
Juniperus sp.
GU058011
Crataegus mongyna
MH595612
Malus
sp. CUP-2613
Juniperus phoenicea
subsp.
turbinata
KT160257+KT16026
Crataegus mongyna
MH595615
Crataegus mongyna
KP261042+KP261043
Crataegus mongyna
MH595614
Juniperus oxycedrus
KP261046+KP261047
Crataegus mongyna
MH595613
Gymnosporangium
sp. KJ720165
Cotoneaster melanopcarpus
HMAS52880
G. gracile
G. confusum
G. tremelloides
G. clavariiforme
G. fraternum
G. tiankengensis sp. nov
.
G. clavipes
G. shennongjiaensis
sp. nov.
G. lachrymiformis sp. nov.
G. libocedri
G. ellisii
G. nootkatense
G. cunninghamianum
G. speciosum
G. kernianum
G. multiporum
G. vauqueliniae
G. exiguum
Gymnosproangium
sp. 3
G. tsingchenensis
100/1.00
63/0.77
100/1.00
100/1.00
86/1.00
100/1.00
76/0.85
91/1.00
68/-
69/0.85
100/0.95
98/1.00
87/0.92
94/-
100/1.00
63/-100/1.00
100/1.00
100/1.00
100/1.00
100/1.00
77/-
57/-
64/0.78
61/-
73/0.85
64/-
larities in spermogonia and teliospores (Cummins & Hiratsuka
1983, 2003). Gymnosporangium is phylogenetically close
to the Mayapple rust Allodus podophylli (Pucciniales family
incertae sedis), Neophysopella (Phakopsoraceae sensu lato
(s.lat.)) and several genera in the Sphaerophragmiaceae (Fig.
1d). Morphologically, Gymnosporangium differs from these
phylogenetically related genera or families (Cummins & Hi-
ratsuka 1983, 2003). Gymnosporangium has Roestelia-type
aecia and multiseptate teliospores without apparent spines or
long projections, which clearly differs from the genus Allodus
(Minnis et al. 2012). Besides, Gymnosporangium has Group
V (type 4) spermogonia, Roestelia-type aecia and pedicel-
late teliospores, and these morphologies clearly differentiate
it from Neophysopella in Phakopsoraceae s.lat., which has
Group VI (type 7) spermogonia and sessile teliospores with
2–7 layers (Ji et al. 2019). In addition, Gymnosporangium
differs from the genera Austropuccinia, Dasyspora, Puccor-
chidium, Sphaerophragmium and Sphenorchidium in the family
Sphaerophragmiaceae, which has Group V (type 4) or Group
VI (type 5) spermogonia, Aecidium-type aecia and teliospores
with both vertically or transverse septa (Beenken 2017). Lastly,
Gymnosporangium has a special host combination, with its
telial stage occurring on gymnosperms and aecial stage on
angiosperms. Such host alternation is distinctive from most
of the rusts on gymnosperms, which have aecial stages on
gymnosperms but uredinial/ telial stages on angiosperms.
Thus, we propose a new family, Gymnosporangiaceae, to ac-
commodate the genus Gymnosporangium based on morpho-
logical differences and a molecular distinction from other fami-
lies in the order Pucciniales.
Within the genus Gymnosporangium, sequence data were suc-
cessfully generated from 184 specimens. Additional rDNA SSU,
ITS and LSU sequences from 212 specimens from GenBank
were aligned for phylogenetic analyses. In total a 2 723 bp
alignment of SSU, ITS and LSU, TrNef+G was selected as the
best-fit substitution model. Maximum likelihood and Bayesian
79
P. Zhao et al.: Gymnosporangium on Malus
analyses of the combined dataset resulted in similar topologies
with only minor changes in poorly supported branches. Maxi-
mum likelihood best tree topology is shown in Fig. 2. These
396 specimens clustered into 32 well-supported phylogenetic
groups. Among them, rust specimens on Malus were found in
22 phylogenetic groups. The morphological distinction in aecial
or telial stages of these 22 groups were further characterised
after examination by LM and SEM. With the aid of morphological
and molecular data, a total of 22 Gymnosporangium species
were confirmed occurring on Malus species. The connection of
spermogonial/ aecial and uredinial/telial stages of 13 species
were further clarified. Species boundaries, host ranges and geo-
graphical distributions of all Gymnosporangium on Malus spe-
cies were confirmed and illustrated below.
TAXONOMY
Family: Gymnosporangiaceae P. Zhao & L. Cai, fam. nov. —
MycoBank MB831269
Etymology. Name derived from the type genus, Gymnosporangium.
Type genus. Gymnosporangium R. Hedw. ex DC., Fl. Franç. 2: 216. 1805.
Spermogonia Group V (type 4), bounding structures with well-
developed peripheral flexuous hyphae. Aecia Roestelia-type,
subepidermal, with well-developed peridia, aeciospores catenu-
late, with intercalary cells. Uredinia Uredo-type, subepidermal,
urediniospores borne singly on pedicels. Telia subepidermal,
erumpent as cushions, crests or horns, teliospores aseptate
to multiseptate, borne singly on gelatinising pedicels. Basidia
external.
Type species. Gymnosporangium fuscum DC., Fl. Franç. 2: 216. 1805,
on Juniperus sabina.
GYMNOSPORANGIUM SPECIES ON MALUS
Gymnosporangium asiaticum Miyabe ex G. Yamada, Sho-
kubutsu Byorigaku (Pl. Path) Tokyo Hakubunkwan 37(9):
304. 1904 — Fig. 3
Synonyms. Roestelia koreensis Henn. (as ‘koreaënsis’), Monsunia 1: 5.
1899.
Gymnosporangium photiniae F. Kern, Bull. New York Bot. Gard. 7: 443.
1911.
Gymnosporangium chinense Long, J. Agric. Res. 1(4): 354. 1914.
Gymnosporangium haraeanum Syd. & P. Syd., Ann. Mycol. 10(4): 405.
1912.
Gymnosporangium koreense H.S. Jacks., J. Agric. Res. 5: 1006. 1916.
Gymnosporangium spiniferum Syd. & P. Syd., Ann. Mycol. 10(1): 78.
1912.
Gymnosporangium taianum F. Kern, Mem. New York Bot. Gard. 10(5):
307. 1964.
Gymnosporangium unicorne H.Y. Yun, Mycologia 101(6): 806. 2009.
Typus. Japan, Hokkaido, Sapporo-shi, 0, I on Cydonia vulgaris, III on J. chi-
nensis, K. Miyabe (lectotype designated here, MBT389888, Yamada (1904:
303 (0, I, III), f. 37).
Epitypification. Japan, Gifu prefecture, Mino, Kawauye-mura, III on J. chi-
nensis, 3 Oct. 1912, K. Hara, CUP-0016 (epitype designated here, MBT389889),
SSU, ITS and LSU sequences GenBank MN642598, MN642593 and
MN642617.
Spermogonia not found. Aecia foliicolous and caulicolous, hypo-
phyllous, roestelioid; peridium tubular, lacerating at apex or
spreading, 4–7 mm high, peridial cells linear-rhomboid, 55–103
× 18–31 μm, outer walls smooth, inner walls small papillae
and side walls moderately rugose; aeciospores globoid, ovoid,
large coronate, 18–26 × 14–22 μm, walls yellowish, 1.0– 2.0
μm thick. Uredinia absent. Telia foliicolous or on green stems,
developing on witches’ broom but without causing swelling on
stem, aggregated bluntly conical, hemispherical, pulvinate or
somewhat wedge-shaped; 2–6 mm high, brownish orange;
teliospores 2-celled, broadly to narrowly ellipsoid, 31–50 ×
16–27 μm, walls 1.0 – 2.5 mm, pale orange to orange, pores
1 or 2 near septum or 1 apical in upper cell; pedicels cylindrical,
hyaline, 2.5–5.0 μm diam.
Additional materials examined. China, Beijing, Huai Rou District, 0, I on
M. pumila, 2 May 2016, P. Zhao, ZP-R201, ZP-R203 & ZP-R204; Beijing,
Yun Meng Mountain, 0, I on M. pumila, 11 July 2016, P. Zhao, ZP-R205, ZP-
R215 & ZP-R228; Beijing, 0, I on M. prunifolia, Z.Y. Zhang, HMAS135598;
Beijing, 0, I on M. pumila, 2 Aug. 1976, L. Guo, HMAS38650; Beijing, 0, I on
M. pumila, 22 Oct. 1984, Y.C. Dai, HMAS56909; Beijing, 0, I on M. specta-
bilis, 2 Dec. 1947, F.L. Tai, HMAS12970; Beijing, Xiangshan Mountain, III
on J. chinensis, 27 May 2006, L. Guo, HMAS172366; Beijing, Xiangshan
Mountain, III on J. chinensis, 4 May 1979, Y.C. Wang, HMAS47229; Beijing,
III on J. chinensis, 22 Mar. 1932, F.L. Tai, HMAS11935; Beijing, III on J. chin-
ensis, 6 Apr. 1935, Y.C. Wang, HMAS22173; Guangdong, Guangzhou, III on
J. chinensis, 26 Mar. 1973, Y.C. Wang, HMAS47228; Guang Xi, Shenmu, 27
Aug. 2015, P. Zhao, ZP-R876; Hebei, Qingyuan, 0, I on Malus sp., 18 Aug.
1932, Q.X. Wu, HMAS14327; Hei Longjiang, Greater Khingan Mountains, 10
Aug. 2015, P. Zhao, ZP-R960 & ZP-R961; Jiangsu, Nanjing, 0, I on M. pumila,
22 Sept. 1927, F.L. Tai, HMAS11217; Shaanxi, Wugong, 27 Aug. 1973, T.Y.
Zhang, HMAS38649; Shaanxi, Xian, 0, I on Pyrus bretschneideri, 5 June
1939, collector unknown, HMAS33358; Sichuan, Chengdu, 18 May 1958,
W.Q. Deng, HMAS26414; Sichuan, Yi Bin, 0, I on M. pumila, 18 May 2016,
P. Zhao, ZP-R301; Tibet, Changdu, III on J. tibetica, 9 June 1976, Y.C. Chen,
HMAS37835; Xinjiang, Altay, 0, I on Malus sp., 1 Sept. 1987, Z.Y. Zhao,
HMAS92418 & HMAS92422; Yunnan, III on J. chinensis, 15 Apr. 1990, X.T.
Zhou, HMAS165302; Yunnan, Kunming, 0, I on M. pumila, 13 May 2016,
P. Zhao, ZP-R773, ZP-R774, ZP-R778 & ZP-R779; Yunnan, Kunming, III
on Cupressus duclouxiana, 6 Apr. 1989, Y.X. Wang, HMAS135599. – USa,
California, Berkeley, III on J. excelsa, 3 Sept. 1958, H.E. Parks, HMAS45640;
New York, Ulster, 0, I on Malus sp., 28 Oct. 2009, H.E. Thomas, CUP-17524;
Yonkers, 0, I on M. ioensis var. plena, 2 Aug. 1928, D.S. Welch, CUP-57311.
– UK, III on J. sabina, 1 May 1889, C.B. Plowright, HMAS2503.
Host range and geographical distribution confirmed in this study — Cu-
pressus duclouxiana – China; Juniperus chinensis cv. globosa – South
Korea; Juniperus chinensis cv. kaizuka – South Korea; Juniperus chinensis
cv. sargentii – South Korea; Juniperus chinensis – China, South Korea;
Juniperus sabina – Japan, UK; Juniperus tibetica – China; Malus asiatica –
China; Malus ioensis var. plena – USA; Malus pumila – China, Japan, USA;
Malus prunifolia – China; Malus spectabilis – China; Pyrus lindleyi – China;
Pyrus pyrifolia – China.
Additional host range and geographical distribution reported in previous
studies — Chaenomeles cardinalis – Japan; Chaenomeles cathayensis –
China; Chaenomeles eburnea – Japan; Chaenomeles japonica – Japan,
South Korea; Chaenomeles lagenaria – Japan, South Korea; Chaenomeles
sinensis – China, Japan, South Korea; Chaenomeles speciosa – China,
Japan, South Korea; Chaenomeles × superba – Japan; Crataegus cuneata
– China; Crataegus pinnatifida – China; Crataegus wilsonii – China; Cydonia
oblonga – China; Juniperus chinensis var. procumbens – Japan; Juniperus
scopulorum – Japan; Juniperus scopulorum var. pyramidalis – Japan; Juni-
perus squamata – Japan; Juniperus virginiana – Japan; Photinia villosa var.
brunnea – South Korea; Pyrus betulaefolia – China; Pyrus bretschneideri
– China, Japan; Pyrus calleryana – China; Pyrus communis – China; Pyrus
montana var. rehderi – China; Pyrus pyrifolia – Japan, South Korea, USA;
Pyrus serotine – China; Pyrus serrulata – China; Pyrus ussuriensis – China,
Japan, South Korea (Farr & Rossman 2019).
Notes — Gymnosporangium asiaticum was first reported
on leaves of J. chinensis in Japan by Miyabe (1903), but
he did not publish a description of this species in any form.
Thereafter, Yamada (1904) validly described this species in
the textbook of plant pathology with both description and line
drawings. However, despite the existence of the valid name of
G. asia ticum, Sydow & Sydow (1912) renamed rusts collected
by K. Hara from at Kawaue-mura, Gifu prefecture of Japan as
G. haraeanum. Subsequently, G. haraeanum was widely ac-
cepted as synonym of G. asiaticum due to its morphological
similarities, host ranges and locality (Hiratsuka 1955, Hiratsuka
et al. 1992). In addition, by using fresh materials from juniper
from which Sydow’s type was collected, Hara and other tax-
onomists confirmed leaf-inhabiting rusts on J. chinensis as
G. asiaticum based on inoculation tests (Tanaka 1922). Due
80 Persoonia – Volume 45, 2020
Fig. 3 Morphology of G. asiaticum. a. Aecia (A) on the hypophyllous leaf surface; b. roestelioid aecia with peridia (P); c. ultrastructure of peridium observed
by SEM; d. linear-rhomboid peridial cells observed by LM; e. ultrastructure of peridial cells observed by SEM, Out layer with smooth surface, inner surface with
irregular papillae; f. globoid or ellipsoid aeciospores with verrucose spines; g. aeciospores with scattered germ pores (G); h. label of type specimen designated
in this study; i. telia on the branches of Juniperus species; j. telia on green stems developing on witches’ broom; k. 2-celled and pedicellate teliospores; l. telio-
spores with cylindrical, hyaline pedicels and germ pore (G). — Scale bars: c– g = 20 µm; k– l = 20 µm.
81
P. Zhao et al.: Gymnosporangium on Malus
to the lack of holotype specimen information in the original
description, and our failure to locate any type, we have desig-
nated illustrations of Yamada (1904) as lectotype. In addition,
we designated an epitype specimen, which was collected by
Hara in 1912 at Kawaue-mura, Gifu prefecture of Japan. We
successfully generated both morphological and molecular data
from the epitype material. This species is hitherto reported from
Asian countries, the East part of Russia and some regions in
North America (Ziller 1974, Hiratsuka et al. 1992, Zhuang et
al. 2012). It is still absent from the European Union and listed
as a quarantine pest in the European and Mediterranean
Plant Protection Organization (EPPO) A2 List due to its severe
threat to apple and pear plantations (EPPO 2018). Hitherto,
five Gymnosporangium species, G. chinense, G. haraeanum,
G. japonicum, G. koreense and G. spiniferum were frequently
regarded as synonyms of G. asiaticum (Kern 1973, Hiratsuka et
al. 1992). Among them, these species with the exception of G.
japonicum, were confirmed to be conspecific with G. asiaticum
after systematic studies of type materials (Yun et al. 2009).
Here we confirmed the species boundaries of G. asiaticum, and
further revealed a recently proposed new species, G. unicorne,
to be conspecific to G. asiaticum. In addition, G. taianum on
Cupressus duclouxiana (HMAS135599), which has aecial hosts
on Chaenomeles, Crataegus, Photina and telial hosts on Juni-
perus species and their varieties, is conspecific to G. asiaticum.
According to Kern (1973), G. asiaticum has its telial stage on
Juniperus, and has its aecial host on Chaenomeles, Cydonia
and Pyrus. In this study, we reported five Malus species, i.e.,
M. asiatica, M. ioensis var. plena, M. pumila, M. prunifolia and
M. spectabilis, as new aecial hosts. We also confirmed its telial
hosts on Cupressus duclouxiana, J. chinensis, J. sabina, J. tibe-
tica and their varieties.
Gymnosporangium clavariiforme (Wulfen) DC., Fl. Franç.
2: 217. 1805 — Fig. 4
Basionym. Tremella clavariiformis Wulfen, (as ‘clavariaeformis’), Col-
lectanea ad botanicam, chemiam, et historiam naturalem spectantia 2: 174.
1791.
Spermogonia not found. Aecia foliicolous and caulicolous, hypo-
phyllous; peridium roestelioid, tubular, lacerating at apex or
spreading, 1.5–3 mm high, peridial cells rhomboid, 77–148 ×
15–29 μm, outer walls smooth, inner walls evenly echinulate;
aeciospores globoid, large coronate, 16–30 × 18–25 μm, walls
yellowish, 1.0– 3.0 μm thick. Uredinia absent. Telia caulicolous,
aggregated, bluntly conical, hemispherical, pulvinate or some-
what wedge-shaped; 2–4 mm high, brownish orange; telio-
spores 2-celled, broadly to narrowly ellipsoid, 46–97 × 15–21
μm, walls 1.0 – 2.5 μm, pale orange to orange, pores 1 or 2 near
septum or 1 apical in upper cell; pedicels cylindrical, hyaline,
3.0–7.5 μm diam.
Additional materials examined. Germany, Bavaria, Eichstätt, slope called
Haselberg, c. 1 km NW of the municipal district Landershofen, limestone
grassland with shrubs, on branches and twigs of J. communis, 14 Apr. 1991,
D. Triebel & G. Rambold, Microfungi Exsiccati 90, HMAS67951. – USa, North
Carolina, 0, I on M. domestica, 15 Sept. 1901, A. George, CUP-12076; Utah,
Zion National Park, Kolob Canyon, 0, I on Amelanchier sp., 20 Aug. 1973,
collector unknown, NYBG3011548; Wyoming, Laramie Mountains, III on
J. communis var. sibirica, G.B. Cummins, NYBG3011553.
Host range and geographical distribution confirmed in this study —
Amelanchier sp. – USA; Juniperus communis – Germany; Juniperus com-
munis var. sibirica – USA; Malus domestica – USA.
Additional host range and geographical distribution reported in previous
studies — Amelanchier alnifolia – Canada, USA; Amelanchier bartramiana
– Canada, USA; Amelanchier canadensis – Canada, USA; Amelanchier
florida – Canada, USA; Amelanchier gaspensis – Canada, USA; Amelanchier
humilis – Canada, USA; Amelanchier intermedia – Canada, USA; Amelan-
chier laevis – Canada, USA; Amelanchier lucida – Canada; Amelanchier
oblongifolia – USA; Amelanchier ovalis – Germany; Amelanchier polycarpa
– USA; Amelanchier pumila – USA; Amelanchier rotundifolia – Turkey;
Amelanchier spicata – Canada, USA; Amelanchier stolonifera – USA;
Amelanchier utahensis – USA; Amelanchier wiegandii – Canada, USA;
Aronia arbutifolia – USA; Cotoneaster integerrimus var. uniflorus – Russia;
Cotoneaster melanocarpus – Russia; Cotoneaster nummularius – Turkey;
Cotoneaster uniflorus – Russia; Crataegomespilus asnieresi – Sweden;
Crataegomespilus grandiflora – Germany; Crataegus aronia – Turkey; Cra-
taegus azarolus – Israel, Turkey; Crataegus brevispina – Spain; Crataegus
calycina – Finland, Norway, Sweden; Crataegus chrysocarpa – Canada;
Crataegus columbiana – Oregon; Crataegus cuneata – China; Crataegus
curvisepala – Canada; Crataegus dahurica – Russia; Crataegus heldreichii
– Greece; Crataegus intricata – Norway; Crataegus laevigata – Poland, UK;
Crataegus macracantha – Norway; Crataegus maximowiczii – China, Russia;
Crataegus microphylla – Turkey; Crataegus monogyna – Algeria, Bulgaria,
Denmark, Finland, France, Germany, Greece, Iraq, Israel, Morocco, New
Zealand, Norway, Poland, Spain, Sweden, UK, USSR; Crataegus monogyna
subsp. azarella – Greece; Crataegus monogyna subsp. monogyna – Turkey;
Crataegus nigra – Denmark, Norway, Sweden, USSR; Crataegus orienta-
lis – Turkey; Crataegus oxyacantha – Canada, Denmark, Finland, France,
Germany, Italy, Norway, Spain, Sweden, UK; Crataegus oxyacantha var.
rosea – Canada; Crataegus pentagyna – Germany, Greece; Crataegus
pinnatifida – China, South Korea; Crataegus pinnatifida var. psiloda – South
Korea; Crataegus rhipidophylla – Canada; Crataegus rhipidophylla var.
rhipidophylla – Poland; Crataegus sanguinea – Finland, Norway; Crataegus
scabrifolia – China; Crataegus sorbifolia – Germany; Crataegus succulenta
– Canada, Norway; Crataegus wilsonii – China; Crataegus × lambertiana
– Norway; Cydonia oblonga – Canada, Greece, USA; Cydonia vulgaris –
Canada, USA; Juniperus communis – Austria, Denmark, Finland, France,
Germany, Greece, New Zealand, Norway, Poland, Spain, Sweden, UK, USA;
Juniperus communis var. depressa – Canada, USA; Juniperus communis
var. hibernica – USA; Juniperus communis var. stricta – Denmark; Juniperus
drupacea – Turkey; Juniperus excelsa – Turkey; Juniperus foetidissima –
Turkey; Juniperus nana – Russia; Juniperus oxycedrus – Bulgaria, France,
Germany, Greece, Spain, Turkey, USSR; Juniperus rigida – Korea; Juniperus
sibirica – Russia; Malus sylvestris – Greece, Turkey; Mespilus germanica
– Turkey; Pyrus arbutifolia – USA; Pyrus communis – Canada, Denmark,
Greece, Iraq, Norway, Poland, Sweden, UK, USA; Pyrus pyrifolia – USA;
Pyrus syriaca – Turkey; Pyrus × communis – Norway; Sorbus aria – Greece,
Norway; Sorbus aucuparia – Bulgaria; Sorbus intermedia – Norway; Sorbus
prattii – China (Farr & Rossman 2019).
Notes — Gymnosporangium clavariiforme was initially de-
scribed on J. communis, and is characterised by its large pe-
ridial cells with sparsely echinulate papillae and caulicolous telia
with narrowly ellipsoid teliospores (Kern 1908, 1911, Yun et al.
2009). The aecial stage was confirmed on the plant genera
Amelanchier, Aronia, Cotoneaster, Crataegus, Cydonia, Malus,
Pyrus and Sorbus (Kern 1973, Farr & Rossman 2019). This
species is relatively common in temperate regions in Asia,
Europe and North America (Tai 1979, Wang & Guo 1985, Yun
et al. 2009, Zhuang et al. 2012). Based on morphological and
molecular data, M. domestica was further confirmed as one
new aecial host.
Gymnosporangium clavipes Cooke & Peck, Ann. Rep. N.Y.
State Mus. Nat. 25: 89. 1873 — Fig. 5
Synonyms. Caeoma germinale Schwein., Trans. Amer. Philos. Soc. 4(2):
294. 1832.
Gymnosporangium germinale F. Kern, Bull. Torrey Bot. Club 35: 506.
1908.
Podisoma clavipes Cooke & Peck, J. Quekett Micros. Club 2: 267. 1871.
Typus. USa, New York, Albany, Bethlehem, III on J. virginiana, P.H.
Charles, NYS-F-775 (isosyntype), SSU, ITS and LSU sequences GenBank
MK488179, MK518847 and MK518583.
Spermogonia not found. Aecia mainly fructicolous, sometimes
caulicolous, roestelioid; peridium cylindric, becoming fimbriate,
0.5–2 mm high, peridial cells rhomboid, 69–105 × 33– 51 μm,
outer walls smooth, inner walls tuberculate, verrucose with
ridge-like papillae; aeciospores globoid, echinulate, 27–49 ×
24–37 μm, walls yellowish, 2.0–5.0 μm thick. Uredinia absent.
Telia caulicolous on fusiform swellings of the smaller branches,
applanate, dark brown, becoming tremelloid or patelliform when
82 Persoonia – Volume 45, 2020
Fig. 4 Morphology of G. clavariiforme. a. Aecia (A) on the hypophyllous leaf surface; b. aecia on fruit; c. ultrastructure of peridia (P) observed by SEM;
d. rhomboid peridial cells observed by LM; e. ultrastructure of peridial cells observed by SEM; f. globoid or ellipsoid aeciospores with scattered germ pores
(G) observed by LM; g. verrucose aeciospores observed by SEM; h. telia on the branches of Juniperus species; i. label of type specimen designated in this
study; j. telia (T) on branches of Juniperus species; k. 2-celled and pedicellate teliospores; l. teliospores with cylindrical and hyaline pedicels. — Scale bars:
c = 200 µm; d– e = 50 µm; f– g, k– l = 20 µm.
expanded, frequently covering the whole hypertrophied area;
teliospores 2-celled, ellipsoid, 32–85 × 23– 32 μm, walls 1.0 –
2.5 μm, pale orange to orange, pores 1 or 2 near septum or 3
apical in upper cell, pedicels carotiform, 10– 24 μm diam near
the pore.
Additional materials examined. Canada, Quebec, 0, I on Malus sp., 13
Aug. 1957, J.A. Parmelee, CUP-48508. – USa, New York, 0, I on Malus sp.,
date and collector unknown, CUP-13530; Massachusetts, III on J. virginiana,
5 May 1966, collector unknown, NYBG3011007; Missouri, 0, I on Crataegus
sp., 12 July 1990, J. Ewan, NYBG461394; New York, Tompkins, Ithaca,
Woods, III on J. virginiana, 28 May 1904, W.D. Benjamin, CUP-18207.
Host range and geographical distribution confirmed in this study — Cra-
taegus sp. – USA; Juniperus virginiana – USA; Malus domestica – USA;
Malus sp. – Canada, USA; Pyrus calleryana – USA.
Additional host range and geographical distribution reported in previous
studies — Amelanchier alnifolia – Canada, USA; Amelanchier alnifolia
var. semiintegrifolia – Canada; Amelanchier arborea – USA; Amelanchier
bartramiana – Canada, USA; Amelanchier canadensis – Canada, USA;
Amelanchier florida – Canada; Amelanchier humilis – Canada, USA;
Amelanchier huronensis – Canada; Amelanchier intermedia – Canada, USA;
Amelanchier laevis – Canada; Amelanchier lucida – Canada; Amelanchier
oblongifolia – USA; Amelanchier sanguinea – Canada, USA; Amelanchier
spicata – Canada, USA; Aronia arbutifolia – Canada, USA; Aronia floribunda
– Canada, USA; Aronia melanocarpa – Canada, USA; Aronia prunifolia –
USA; Chaenomeles japonica – USA; Cotoneaster acutifolia – Canada, USA;
Cotoneaster acutifolius – Canada; Cotoneaster lucida – Canada; Crataegus
aestivalis – USA; Crataegus beata – Canada; Crataegus caesia – Canada;
Crataegus chrysocarpa – Canada; Crataegus coccinea – USA; Crataegus
columbiana – Canada; Crataegus crus-galli – USA; Crataegus curvisepala –
Canada; Crataegus douglasii – Canada, USA; Crataegus fucosa – Canada,
83
P. Zhao et al.: Gymnosporangium on Malus
USA; Crataegus mexicana – Mexico; Crataegus michauxii – USA; Crataegus
monogyna – Canada; Crataegus oxyacantha – Canada, USA; Crataegus
pedicellata – Canada, USA; Crataegus punctata – Canada, USA; Cratae-
gus spathulata – USA; Crataegus succulenta – Canada; Cydonia oblonga
– Canada, USA; Cydonia vulgaris – USA; Juniperus chinensis – Canada,
USA; Juniperus communis – Canada, USA; Juniperus communis var. de-
pressa – Canada, USA; Juniperus horizontalis – Canada, USA; Juniperus
phoenicea – Portugal; Juniperus scopulorum – Canada, USA; Juniperus
virginiana var. depressa – Canada; Mespilus germanica – USA; Photinia
villosa – USA; Pyrus arbutifolia – Canada; Pyrus communis – USA; Pyrus
pyrifolia – USA; Sorbus americana – Canada, USA; Sorbus aucuparia –
Canada; Sorbus decora – Canada; Sorbus occidentalis – Canada; Sorbus
sitchensis – Canada; Sorbus sitchensis var. grayii – Canada; Sorbus sitch-
ensis var. sitchensis – Canada (Farr & Rossman 2019).
Notes — Gymnosporangium clavipes was one of earliest
species reported from North America, and is characterised by
its relatively large aeciospores with tuberculate peridial cells,
2-celled teliospores with carotiform pedicels. The aecial stage
of this species was first described as Caeoma germinale on
Crataegus species, and the telial stage was described on
J. virginiana as ‘Podisoma clavipes’ (Arthur 1934). Later these
two species were confirmed as two phases of G. clavipes, and
host ranges of this species was systematically reported based
on inoculation tests (Crowell 1940). Host alternation of this
species was reported on Juniperus and a series of species
in Amelanchier, Aronia, Chaenomeles, Crataegus, Cydonia,
Malus, Mespilus and Photinia in the Rosaceae (Crowell 1940,
Laundon 1977). In the aecial stage, several Malus species,
i.e., M. angustifolia, M. floribunda, M. pumila, M. spectabilis,
M. sylvestris and several unidentified Malus species were re-
ported as aecial hosts of G. clavipes (Farr & Rossman 2019).
Gymnosporangium clavipes is distributed in North America,
Central America and Caribbean countries, and it is listed as one
of the important quarantine pests in the EU and Asian countries
(EPPO 2018). Here we successfully generated sequence data
from the type material, and further confirmed host alternation of
G. clavipes on J. virginiana and species of Crataegus, Malus,
Pyrus and related species.
Gymnosporangium corniculans F. Kern, Mycologia 2(5):
236. 1910
Spermogonia not found. Aecia foliicolous or caulicolous, hypo-
phyllous, roestelioid; peridium cornute, tardily dehiscent by side
lacerations, 1.5–3.5 mm high, causing hypertrophy, peridial
Fig. 5 Morphology of G. clavipes. a. Aecia (A) on the surface of fruits; b. aecia on the fruits; c. ultrastructure of peridia (P) observed by SEM; d. rhomboid
peridial cells observed by LM; e. ultrastructure of peridial cells observed by SEM; f. globoid or ellipsoid aeciospores with scattered germ pores (G) observed
by LM; g. verrucose aeciospores observed by SEM; h. telia (T) on the branches of Juniperus species; i. 2-celled teliospores with pedicels carotiform, with up
to 24 μm near the pore. — Scale bars: c = 200 µm; d– g, i = 20 µm.
84 Persoonia – Volume 45, 2020
cells rhomboid, 55–103 × 18 – 31 μm, outer walls smooth,
side walls rugose, inner walls with small papillae of irregular
shape, densely distributed; aeciospores globoid, ovoid, large
coronate, 18–34 × 16–27 μm, walls yellowish, 1.0 – 2.5 μm
thick. Uredinia absent. Telia caulicolous, globoid galls generally
3–12 mm diam, terete, cylindric to acuminate, brownish orange;
teliospores 2-celled, broadly to narrowly ellipsoid, 31–56 ×
16–30 μm, walls 1.0– 2.5 μm, pale orange to orange, pores 1
or 2 near septum; pedicel cylindrical, hyaline, 2.0–3.5 μm diam.
Materials examined. China, Guizhou, Anshun, III on J. chinensis, 1 Apr.
1999, M.H. Liu, HMAS79065. – USa, Connecticut, East Grandy, 0, I on
M. domestica, 29 Aug. 1931, Spaulding & Eno, CUP-19705 & CUP-19706;
New York, Tompkins, Ithaca, 0, I on A. canadensis, date unknown, H.H.
Whetzel, CUP-3087.
Host range and geographical distribution confirmed in this study —
Amelanchier canadensis – USA; Juniperus chinensis – China; Juniperus
horizontalis – USA; Malus domestica – USA.
Additional host range and geographical distribution reported in previous
studies — Amelanchier alnifolia – Canada; Amelanchier intermedia –
USA; Amelanchier oblongifolia – USA; Amelanchier rotundifolia – USA;
Amelanchier sanguinea – Canada, USA; Juniperus virginiana – USA (Farr
& Rossman 2019).
Notes — This species is characterised by its cornuted form
of the aecia and small papillae of irregular shape in peridial
cells. It was first described on J. horizontalis in Michigan in the
USA and Canada (Kern 1964). This species is mainly reported
with their aecial stage on Amelanchier in North America. In this
study we found M. domestica as a new aecial host. We further
confirmed it occurs in China, the first record outside North
America.
Gymnosporangium cornutum Arthur ex F. Kern, Bull. New
York Bot. Gard. 7: 444. 1911
Spermogonia not found. Aecia foliicolous and caulicolous, hypo-
phyllous; peridium tubular, lacerating at apex or spreading, 4–7
mm high, peridial cells rhomboid, 55–103 × 18–31 μm, outer
walls smooth, inner walls small papillae with irregular shape
and side walls moderately rugose; aeciospores globoid, ovoid,
minute coronate, 18–26 × 14–22 μm, walls yellowish, 1.0– 2.0
μm thick. Uredinia absent. Telia foliicolous or on green stems,
developing on witches’ broom but without causing swelling on
stem, aggregated bluntly conical, hemispherical, pulvinate or
somewhat wedge-shaped, 2–6 mm high, brownish orange;
teliospores 2-celled, broadly to narrowly ellipsoid, 31–50 ×
16–27 μm, walls 1.0–2.5 μm, pale orange to orange, pores
1 or 2 near septum or 1 apical in upper cell, pedicel cylindrical,
hyaline, 2.0–4.5 μm diam.
Materials examined. aUStria, Carinthia, Koralpe, 0, I on S. aucuparia, 28
Aug. 2011, C. Scheuer, NYBG463. – China, Beijing, 0, I on M. spectabilis, 2
June 1947, HMAS12940. – Finland, Kiiminki, 0, I on S. aucuparia, 30 July
1962, P.S. Jokela, NYBG3011886. – USa, Connecticut, III on J. virginiana,
11 June 1964, C.T. Rogerson, NYBG3070932.
Host range and geographical distribution confirmed in this study — Juni-
perus virginiana – USA; Malus spectabilis – China; Sorbus aucuparia – Aus-
tria, Finland.
Additional host range and geographical distribution reported in previous
studies — Amelanchier ovalis – Germany; Juniperus communis – Bulgaria,
Denmark, Finland, Norway, Poland, Sweden, Turkey, UK, USA; Juniperus
communis var. depressa – Canada, USA; Juniperus communis var. montana
– Japan; Juniperus communis var. nipponica – Japan; Juniperus conferta
– Japan; Juniperus rigida – China, Japan, South Korea; Juniperus sibirica
– Japan, Russia, USA; Malus fusca – Canada; Malus pumila – Greece;
Malus sylvestris – Greece; Pyrus americana – USA; Pyrus aucuparia – USA;
Pyrus sitchensis – USA; Sorbus alnifolia – South Korea; Sorbus americana
– Canada, Norway; Sorbus amurensis – Russia; Sorbus aria – Greece;
Sorbus arranensis – Norway; Sorbus aucuparia – Belarus, Bulgaria, Canada,
Denmark, Germany, Japan, Norway, Poland, Russia, Sweden, Turkey, UK;
Sorbus commixta – Japan; Sorbus decora – Canada; Sorbus discolor – China;
Sorbus hybrida – Denmark, Finland, Norway, Sweden; Sorbus intermedia
– Finland, Norway, Sweden; Sorbus intermedia var. arranensis – Norway;
Sorbus kamtschatcensis – Russia; Sorbus koehneana – China; Sorbus
meinichii – Finland, Norway; Sorbus neglecta – Norway; Sorbus occiden-
talis – Canada; Sorbus sambucifolia – Japan, Russia; Sorbus sambucifolia
var. pseudogracilis – Japan; Sorbus sargentiana – UK; Sorbus scopulina
– Canada; Sorbus sibirica – Russia; Sorbus sitchensis – Canada; Sorbus
sitchensis var. grayii – Canada; Sorbus sitchensis var. sitchensis – Canada;
Sorbus tianschanica – China, Norway; Sorbus umbellata – Turkey; Sorbus
ursina – Nepal; Sorbus × thuringiaca – UK (Farr & Rossman 2019).
Notes — Gymnosporangium cornutum was first described
on J. sibirica in Colorado in the USA, and it was recorded on
three Malus species (i.e., M. fusca, M. pumila and M. sylvestris)
in North America and Europe (Farr & Rossman 2019). Here we
confirmed M. spectabilis as an additional aecial host for this
species.
Gymnosporangium fenzelianum F.L. Tai & C.C. Cheo, Bull.
Chin. Bot. Soc. 3: 60. 1937 — Fig. 6
Synonym. Roestelia fenzeliana (F.L. Tai & C.C. Cheo) F. Kern, Revised
Taxonomic Account of Gymnosporangium (Univ. Park & London): 85. 1973.
Typus. China, Shaanxi, Taibai Mountain, 0, I on M. kansuensis, 23 Aug.
1934, F.L. Tai, HMAS6983 (holotype).
Epitypification. China, Shaanxi, Taibai Mountain, 0, I on M. kansuensis, 28
July 1938, Y.C. Wang, HMAS33357 (epitype designated here, MBT388922),
ITS and LSU sequences GenBank MN605695 and MN605773.
Spermogonia, uredinia and telia not found. Aecia foliicolous,
hypophyllous, roestelioid; peridium tubular, cornuted, spread-
ing or erect after dehiscence, 0.8–1.5 mm high, peridial cells
prismatic, 43–96 × 27–64 μm, rugose with closely set ridges of
various length; aeciospores globoid, ovoid, verrucose, 22–36 ×
20–24 μm, walls slightly brown, 1–3 μm thick, germ pores scat-
tered, 4–8.
Additional materials examined. China, Shaanxi, Taibai Mountains, 0, I
on M. kansuensis, 26 June 1958, Y.C. Wang, HMAS24436; Shaanxi, Taibai
Mountains, 0, I on M. kansuensis, 9 Sept. 1958, Y.C. Wang, HMAS24438;
Shaanxi, Taibai Mountains, 0, I on M. kansuensis, 11 Aug. 2014, P. Zhao,
ZP-R3 & ZP-R14; Gansu, Zhouqu, 3 Sept. 1992, J.Y. Zhuang, HMAS172210.
Host range and geographical distribution — Malus kansuensis – China.
Notes — Gymnosporangium fenzelianum was first reported
on M. kansuensis in China (Tai 1979), and it is characterised
by its lanceolate spindles on peridial cells and relatively large
aeciospores. This species was once transferred to the genus
Roestelia, and a new combination R. fenzeliana was proposed
(Kern 1973). Here we resurrected the name G. fenzelianum,
and introduced an epitype for this species. Although we failed
to find the telial stage of this species, morphological and phylo-
genetic distinction of this species from other Gymnosporangium
species was confirmed.
Gymnosporangium globosum (Farl.) Farl., Bot. Gaz. 11(9):
236. 1886
Basionym. Gymnosporangium fuscum var. globosum Farl., Anniv. Mem.
Boston. Soc. Nat. Hist.: 34. 1880.
Spermogonia not found. Aecia hypophyllous, foliicolous and
caulicolous, roestelioid; peridium cylindric, becoming fimbriate
0.5–2 mm high, peridial cells rhomboid, 69–105 × 33– 51 mm,
outer walls smooth, side walls rugose, inner walls small papillae
with irregular verruculose with ridge-like papillae; aeciospores
globoid, large coronate, 27–49 × 24–37 mm, walls yellowish,
2.0–5.0 mm thick. Uredinia absent. Telia caulicolous on fusiform
or gall-like swellings of the smaller branches, applanate, dark
brown, becoming tremelloid or patelliform when expanded; telio-
spores 2-celled, ellipsoid, 32–85 × 23–32 mm, walls 1.0 – 2.5
85
P. Zhao et al.: Gymnosporangium on Malus
mm, pale orange to orange, pores 1 or 2 near septum or 3 api-
cal in upper cell, pedicel cylindrical, hyaline, 2.5– 3.0 μm diam.
Additional materials examined. USa, Massachusetts, 0, I on Crataegus
sp., 13 Sept. 1966, H.E. Bigelow, NYBG4897; New York, Bronx County, 0, I
on Crataegus sp., 16 July 1978, collector unknown, NYBG3010437; New
York, Bronx County, III on Juniperus sp., 21 May 1983, collector unknown,
NYBG3010436; New York, Geneva, 0, I on Malus sp., 22 Aug. 1908, J.A.
Maney, CUP-1553; New York, Tompkins County, III on J. virginiana, 10 May
1946, collector unknown, NYBG3010433.
Host range and geographical distribution confirmed in this study — Cra-
taegus sp. – USA; Juniperus virginiana – USA; Juniperus sp. – USA; Malus
sp. – USA.
Additional host range and geographical distribution reported in previous
studies — Amelanchier × humilis-laevis – USA; Crataegus acutiloba – USA;
Crataegus anomala – Canada, USA; Crataegus apposita – USA; Crataegus
asperifolia – USA; Crataegus beata – Canada; Crataegus brainerdii – USA;
Crataegus brunetiana – Canada, USA; Crataegus caesia – Canada; Cratae-
gus calpodendron – Canada, USA; Crataegus chrysocarpa – Canada; Cra-
taegus chrysocarpa var. phoenicea – Canada; Crataegus coccinea – Canada,
USA; Crataegus coccinioides – USA; Crataegus colorata – USA; Crataegus
conjuncta – USA; Crataegus conspicua – USA; Crataegus crus-galli – Can-
ada, USA; Crataegus curvisepala – Canada; Crataegus cyclophylla – USA;
Crataegus delectabilis – Canada; Crataegus delucida – USA; Crataegus
demissa – USA; Crataegus dissimilis – USA; Crataegus dissona – USA;
Crataegus eamesi – USA; Crataegus edsoni – USA; Crataegus egglestonii
– USA; Crataegus festiva – USA; Crataegus floribunda – Canada, USA;
Crataegus forbesae – USA; Crataegus fretalis – USA; Crataegus fuscosa –
Canada, USA; Crataegus genialis – USA; Crataegus glandulosa – Canada,
USA; Crataegus glaucophylla – Canada, USA; Crataegus gracilior – USA;
Crataegus holmesiana – USA; Crataegus intricata – Canada, USA; Crataegus
jesupii – USA; Crataegus lavallei – USA; Crataegus macracantha – Canada,
USA; Crataegus macrosperma – USA; Crataegus margaretta – Canada, USA;
Crataegus mcgeeae – USA; Crataegus membranacea – USA; Crataegus
mexicana – USA; Crataegus mollis – Canada, USA; Crataegus monogyna
– Canada, USA; Crataegus neo-londinensis – USA; Crataegus neofluvia-
lis – USA; Crataegus oxyacantha – Canada, USA; Crataegus pedicellata
– Canada; Crataegus pedicillata – Canada; Crataegus pentandra – USA;
Crataegus pequotorum – USA; Crataegus pertomentosa – USA; Crataegus
Fig. 6 Morphology of G. fenzelianum. a. Labels of the holotype specimen; b. aecia (A) on the hypophyllous leaf surface; c. rhomboid or oblong peridial cells
observed by LM; d. ultrastructure of peridial cells observed by SEM; f. globoid or ellipsoid aeciospores with scattered germ pores observed by LM; g. verrucose
aeciospores observed by SEM. — Scale bars: c– f = 20 µm.
86 Persoonia – Volume 45, 2020
pinnatifida – South Korea; Crataegus pinnatifida var. major – South Korea;
Crataegus pisifera – USA; Crataegus pringlei – USA; Crataegus pruinosa –
USA; Crataegus pruinosa var. latisepala – USA; Crataegus punctata – USA;
Crataegus quinebaugensis – USA; Crataegus rhombifolia – USA; Crataegus
roanensis – Canada, USA; Crataegus rotundifolia – Canada, USA; Cra-
taegus sanguinea – Canada, USA; Crataegus scabrida – USA; Crataegus
schweinitziana – USA; Crataegus silvicola var. beckwithae – USA; Crataegus
straminea – USA; Crataegus submollis – Canada, USA; Crataegus suc-
culenta – USA; Crataegus tenella – USA; Crataegus tomentosa – Canada,
USA; Crataegus viridis – USA; Juniperus barbadensis – China; Juniperus
chinensis – Canada, USA; Juniperus communis var. depressa – USA;
Juniperus horizontalis – Canada, China, USA; Juniperus prostrata – USA;
Juniperus scopulorum – Canada; Juniperus silicicola – USA; Juniperus
virginiana – USA; Malus angustifolia – USA; Malus baccata – USA; Malus
domestica – USA; Malus floribunda – USA; Malus pumila – Canada; Malus
sylvestris – USA; Pyrus americana – USA; Pyrus angustifolia – USA; Pyrus
communis – Canada, USA (Farr & Rossman 2019).
Notes — This species was first reported on J. virginiana
in the USA (Farlow 1906). It resembles G. sabinae but differs
Fig. 7 Morphology of G. juniperi-virginianae. a. Aecia (A) on the hypophyllous leaf surface; b. foliicolous and roestelioid aecia (A) on the leaf surface;
c. roestelioid aecia with tubular peridium (P) observed by SEM; d. rhomboid peridial cells observed by LM; e. ultrastructure of peridial cells observed by SEM;
f. globoid or ellipsoid aeciospores with scattered germ pores (G) observed by LM; g. verrucose aeciospores with large coronate papillae observed by SEM;
h. caulicolous telia formed globoid galls on stem of juniper. i. globoid telia with cylindrical-acuminate sori; j. 2-celled and pedicellate teliospores with cylindrical
and hyaline pedicels; k. teliospores with germ pores (G). — Scale bars: c– e = 50 µm; f– g, j– k = 20 µm.
87
P. Zhao et al.: Gymnosporangium on Malus
in its telia with globose galls, roestelioid aecia and the ultra-
structure of peridial cells and aeciospores. Five Malus species,
i.e., M. angustifolia, M. baccata, M. floribunda, M. pumila and
M. sylvestris, were reported as hosts of G. globosum, and this
species was listed as an important quarantine pest in the EU
and China (EPPO 2018) although existence of this species in
China has already been reported (Zhuang et al. 2012). Here we
confirmed the delimitation of this species, and further clarified
the host alternation between Crataegus, Juniperus and Malus.
Gymnosporangium juniperi-virginianae Schwein., Schr. Nat.
Ges. Leipzig 1: 74. 1822 — Fig. 7
Synonyms. Gymnosporangium macropus Link, Willd. Sp. Pl. 4, 6(2): 128.
1825.
Gymnosporangium virginianum Spreng., Syst. Veg., edn. 16, 4(1): 562.
1827.
Podisoma juniperi-virginianae (Schwein.) Fr., Syst. Mycol. (Lundae) 3(2):
507. 1832.
Aecidium pyratum Schwein., Trans. Amer. Philos. Soc., n. s. 4(2): 2896.
1832.
Roestelia pyrata (Schwein.) Thaxt., Proc. Amer. Acad. Arts 22: 262. 1886.
Roestelia pyrata (Schwein.) Plowr., Monogr. Brit. Ured. Ustil. (London):
57. 1889.
Typus. USa, North Carolina, Carteret, on J. virginiana, 3 Apr. 1977, J.J. Kohl-
meyer, NYBG1391099 (neotype designated here, MBT388923), SSU, ITS
and LSU sequences GenBank MN604985, KU288647 and KU342712.
Spermogonia not found. Aecia foliicolous, hypophyllous, roeste-
lioid; peridium tubular, at first cylindric, fimbriate to base and
strongly recurved, 0.5–1.5 mm high, peridial cells long and nar-
row, 67–103 × 16 – 43 μm, much curved, outer walls with smooth
surface, inner walls with small papillae and walls moderately
rugose; aeciospores globoid, ovoid or broadly ellipsoid, 18 –34
× 14–22 μm, walls yellowish, 1.0–3.0 μm thick, walls surface
with large coronate papillae. Uredinia absent. Telia caulico-
lous, on globoid or reniform galls, 10–40 mm diam, cylindrical
or cylindrical-acuminate, golden-brown or somewhat reddish
surrounded at base by a raised ring of host tissue, 1–4 cm
long, orange; teliospores 2-celled, ellipsoid, 35–66 × 16–23
μm, walls 1.0 – 2.5 mm, brownish, pores 2, septate, pedicel
cylindrical, hyaline, 2.5–3.5 μm diam.
Additional materials examined. USa, Connecticut, 0, I on M. pumila, 4
Sept. 1931, G.H. Hepting, CUP-19812; Columbia, Clermont, 0, I on Malus
sp., 1 Aug. 1909, H. Wilson, CUP-28110; Connecticut, Cos Cob, Montgomery
Nursery, III on J. scopulorum, 8 Mar. 1932, collector unknown, CUP-57206;
Connecticut, III on J. virginiana, 11 May 1992, S.R. Hill, NYBG23036; Dakota,
III on J. scopulorum, 11 June 1927, Brenckle & Stevens, HMAS2218; Indiana,
Avilla, 0, I on Malus sp., 8 May, 1908, H.H. Whetzel, CUP-2985; Indiana, 0,
I on J. virginiana, 11 May 1900, J.C. Arthur, HMAS43709; Indiana, 0, I on
M. coronaria, 12 July 1902, H.H. Thomas, CUP-45235; Iowa, Ames, III on
Juniperus sp., 1 Nov. 1929, D.B. Yu, HMAS14325; Iowa, III on Juniperus sp.,
N.L. Gardner, HMAS49243; Iowa, 0, I on M. coronaria, 31 July 1899, H.H.
Thomas, CUP-55712; Massachusetts, III on J. virginiana, date unknown, H.E.
Ahles, NYBG237046; Massachusetts, 0, I on M. domestica, 22 Aug. 1910,
collector unknown, CUP-21697 & CUP-25670; Massachusetts, 0, I on M. do-
mestica, 26 Sept. 1931, collector unknown, CUP-19919; New York, Dutchess,
Hyde Park, III on J. virginiana, 14 May, 1968, H.E. Ahles, NYBG3011022 &
NYBG3011024; New York, 0, I on M. glaucescens, 26 Sept. 1917, collector
unknown, CUP-594; New York, 0, I on M. ioensis, 26 Sept. 1917, collector
unknown, CUP-595; New York, 0, I on M. domestica, 15 June 1908, collector
unknown, CUP-21686 & CUP-17321; New York, 0, I on M. domestica, 9 Sept.
1925, collector unknown, CUP-14980; New York, 0, I on M. domestica, 9 Sept.
1930, collector unknown, CUP-882, CUP-20156, CUP-20157, CUP-20160,
CUP-20161, CUP-20162, CUP-20164, CUP-20165, CUP-20166, CUP-
20202, CUP-20208, CUP-20209, CUP-20210 & CUP-20211; New York, 0, I
on M. soularidi, 27 Sept. 1917, collector unknown, CUP-596; North Carolina,
Carteret, on J. virginiana, 3 Apr. 1977, J.J. Kohlmeyer, NYBG461220; New
York, III on J. virginiana, 4 June 1967, collector unknown, NYBG237070; North
Carolina, 0, I on M. coronaria, 25 July 1934, G.B. Cummins, CUP-24473;
North Dakota, III on Juniperus sp., 12 Aug. 1915, O.A. Stevens, HMAS6725;
Tennessee, Cades Cove, Smoky Mountains Park, 0, I on M. angustifolia,
G.B. Cummins, CUP-4826; Tennessee, 0, I on M. angustifolia, 14 Aug. 1934,
G.B. Cummins, CUP-24472; Tennessee, 0, I on M. coronaria, 14 Aug. 1934,
G.B. Cummins, CUP-24468 & CUP-20257; Virginia, 0, I on M. domestica,
7 Aug. 1897, W.A. Murrill, CUP-9367; West Virginia, 0, I on M. domestica,
5 Aug. 1930, collector unknown, CUP-20151, CUP-20218, CUP-20223 &
CUP-20231.
Host range and geographical distribution confirmed in this study — Juni-
perus scopulorum – USA; Juniperus virginiana – USA; Juniperus sp. – USA;
Malus angustifolia – USA; Malus coronaria – USA; Malus domestica – USA;
Malus glaucescens – USA; Malus pumila – USA; Malus soulardi – USA.
Additional host range and geographical distribution reported in previous
studies — Crataegus mollis – USA; Juniperus chinensis – USA; Juniperus
chinensis f. globosa – USA; Juniperus communis var. depressa – USA;
Juniperus horizontalis – USA; Juniperus horizontalis f. alpine – USA; Juni-
perus pinchotii – USA; Juniperus scopulorum— Canada, USA; Juniperus
silicicola – USA; Juniperus utahensis – USA; Juniperus virginiana var. crebra
– Canada; Pyrus angustifolia – USA; Pyrus baccata – USA; Pyrus coronaria
– USA; Pyrus floribunda – USA; Pyrus ioensis – USA; Pyrus ioensis var.
plena – USA (Farr & Rossman 2019).
Notes — Gymnosporangium juniperi-virginianae was first
reported on J. virginiana in the USA, and it is characterised by
roestelioid aecia up to 1.5 mm high, rugose peridial cells and
telia within a large roundish gall. This species was first described
by Schweinitz (1822) on J. virginiana in North Carolina in USA,
but no specimen information was listed in the original descrip-
tion. Thereafter, Farlow (1880) described it with a line drawing
as G. macropus. Subsequent comprehensive studies of the
genus Gymnosporangium were conducted by Kern (1911), and
morphology, type locality and host information were discussed
without any type specimen information. We failed to locate
type materials of this species, and thus designated a neotype
specimen of G. juniperi-virginianae based on its morphology,
host and location. This species has frequently been reported
in North America and Canada as causal agent of notorious
rust diseases on commercial apple cultivars, and some Asian
countries and the European Union list this rust fungus as one of
the most important plant quarantine fungi (EPPO/CABI 1996b,
EPPO 2017, 2018). Twelve Malus species, i.e., M. angustifolia,
M. baccata, M. coronaria, M. domestica, M. floribunda,
M. fusca, M. glaucescens, M. ioensis, M. pumila, M. sieboldii,
M. spectabilis and M. sylvestris, were reported as aecial hosts
(Farr & Rossman 2019). We confirmed seven Malus species as
aecial hosts of this species, and two additional Malus species,
M. coronaria and M. soulardi were reported as new aecial hosts.
Thus, species boundaries, host alternations and geographic
distributions of this quarantine species were confirmed.
Gymnosporangium lachrymiforme P. Zhao & L. Cai, sp. nov.
— MycoBank MB832743; Fig. 8
Etymology. Epithet refers to aecia with long balanoid peridia.
Typus. China, Guizhou, Guiyang City, 0, I on Malus sp., 14 May 2015,
P. Zhao (holotype HMAS248123). ITS and sequences GenBank MN605716
and MN605794.
Spermogonia, uredinia and telia not found. Aecia foliicolous, hypo-
phyllous, roestelioid; peridium balanoid, 3.0–8.5 mm high, rup-
ture and becoming lacerate at side, peridial cells oblong, 47–85
× 24– 33 μm, outer walls smooth, inner walls and side walls
densely verrucose with small papillae; aeciospores globoid
or broadly ellipsoid, 15–29 × 14–24 μm, walls slightly brown,
2 μm thick; germ pores scattered, 3–7.
Additional material examined. China, Guizhou, Guiyang City, 0, I on Malus
sp., 14 May 2015, P. Zhao, ZP-R1448.
Host range and geographical distribution — Malus sp. – China.
Notes — This rust was found on one unidentified Malus spe-
cies in China, and it was characterised by its balanoid aecia
with linear and relatively shorter peridia. This species resembles
G. sabinae in its balanoid aecia, but the length of peridia, and
88 Persoonia – Volume 45, 2020
dimensions of the peridial cells clearly differentiate the two
species. Among other Gymnosporangium species reported
on Malus, the aecial stage of this species only resembles
G. hemisphericum in the dimension and shape of peridial cells
and aeciospores (Hiratsuka et al. 1992). However, our new
species differs in the balanoid aecia with relatively long peridia.
Based on these morphological and molecular differences, we
proposed it as a new species.
Gymnosporangium libocedri (Henn.) F. Kern, Bull. Torrey
Bot. Club 35: 509. 1908 — Fig. 9
Basionym. Phragmidium libocedri Henn., Hedwigia 37: 271. 1898.
Synonyms. Gymnosporangium aurantiacum Syd. & P. Syd., Ann. Mycol.
2(1): 28. 1904, nom. inval.
Gymnosporangium blasdaleanum F. Kern, Bull. New York Bot. Gard. 7:
437. 1911.
Typus. USa, California, Potter Valley, Mendocino C, III on Calocedrus
decurrens, 1894, A. Purpurs, B17504 (holotype).
Epitypification. USa, California, Along Moro Rock Trail, Giant Forest, Se-
quoia National Park, III on Calocedrus decurrens, 10 July 1930, J.P. Tracy,
HMAS49246 (epitype designated here, MBT388924). SSU, ITS and LSU se-
quences GenBank MN605009, MN605717 and MN605795.
Spermogonia not found. Aecia foliicolous, hypophyllous, roes-
telioid; peridium cornuted, horned, margin lacerate, spreading
or recurved, 1.5–3 mm high, peridial cells rhomboid, 77–148
× 15 – 29 μm, outer walls and inner walls verrucose; aecio-
spores globoid, 13–25 × 10–23 μm, walls yellowish, 1.0 –1.5
μm thick, verrucose with refractive granules. Uredinia absent.
Telia foliicolous, usually without distortions of the stems, but
sometimes producing witches’ brooms, roundish oval, 0.8– 2.0
mm across, pulvinate, reddish brown; teliospores 2–5-celled,
linear-oblong, 41–86 × 14 –22 μm, walls 1.0 –1.5 μm, pale
orange to orange, pores 2, septate except apical in uppermost
cells; pedicels cylindrical, 5.0–20 μm diam.
Additional materials examined. China, Guizhou, 0, I on M. sylvestris, 26
Sept. 2016, P. Zhao, ZP-R471. – USa, Berkeley, III on C. decurrens, 1 June
1936, S.T. Parks, HMAS45643; California, III on C. decurrens, 10 July 1930,
J.P. Tracy, HMAS2616; Maine, 0, I on Malus sp., 28 May 1939, A.E. Prince,
HMAS243537, HMAS243649 & HMAS243651; Maine, III on J. communis var.
depressa, 28 May 1939, A.E. Prince, HMAS43589.
Host range and geographical distribution confirmed in this study — Calo-
cedrus decurrens – USA; Juniperus communis var. depressa – USA; Malus
sp. – USA.
Additional host range and geographical distribution reported in previous
studies — Amelanchier alnifolia – USA; Amelanchier florida – USA; Ame-
lanchier pallida – USA; Chaenomeles japonica – USA; Crataegus douglasii –
USA; Cydonia oblonga – USA; Heyderia decurrens – USA; Juglans californica
– USA; Malus baccata – USA; Malus floribunda – USA; Malus fusca – USA;
Malus ioensis – USA; Malus sylvestris – USA; Pyrus communis – USA; Pyrus
fusca – USA; Sorbus americana – USA; Sorbus aucuparia – USA; Sorbus
hybrida – USA (Farr & Rossman 2019).
Notes — This species was first described on Calocedrus de-
currens in California, USA, and it is characterised by its ver-
rucose aeciospores with refractive granules, 2–5-celled telio-
spores with terete pedicels up to 20 μm diam (Arthur 1934,
Kern 1973). Hennings (1900) first described it on Calocedrus
decurrens as Phragmidium libocedri, and later Sydow & Sydow
(1904) proposed a new name G. aurantiacum Syd. & P. Syd.
based on specimens collected from the same host and regions.
Although he treated Phragmidium libocedri as synonym of
G. au rantiacum Syd. & P. Syd., this name is invalid because
it was already occupied (Chevallier 1826). After examination
of these specimens, Kern (1908) proposed a combination
G. libocedri, and further treated Phragmidium libocedri as
synonym. Here we selected a specimen as epitype of G. libo-
cedri. The information of species identity, host alternation and
geographic distribution of this species was further clarified
and host alternation from Calocedrus and Malus species was
confirmed in our study, which was previously known based on
inoculation tests conducted by Kern (1911). In the previous
Fig. 8 Morphology of G. lachrymiforme. a. Aecia with balanoid peridia (P) on the hypophyllous leaf surface; b. peridium with cornuted apex; c. oblong peridial
cells observed by LM; d. ultrastructure of peridial cells observed by SEM; d. globoid or ellipsoid aeciospores with scattered germ pores (G) observed by LM;
e. ultrastructure of aeciospores observed by SEM. — Scale bars: c– f = 20 µm.
89
P. Zhao et al.: Gymnosporangium on Malus
study, M. angustifolia, M. fusca and M. ioensis were reported
as aecial hosts, and here we further confirmed one additional
telial host, J. communis var. depressa.
Gymnosporangium miyabei G. Yamada & I. Miyake, Bot.
Mag. (Tokyo) 22: 23. 1908
Synonyms. Roestelia solenoides Dietel, Bot. Jahrb. Syst. 32: 631. 1903.
Roestelia solitaria Miyabe, Bot. Mag. (Tokyo) 17: 34. 1903.
Gymnosporangium solenoides F. Kern, Bull. New York Bot. Gard. 7: 450.
1911.
Spermogonia not found. Aecia foliicolous, hypophyllous, roes-
telioid, borne on frustum-like protuberances; peridia cornute
form, dehiscent at apex, not becoming much lacerate 2.5–5.0
mm high, peridial cells rhomboid, 52–109 × 15–33 μm, outer
walls smooth, inner walls densely verrucose, with small oval or
irregular papillae; aeciospores globose, 15–27 × 10 – 23 μm,
walls yellowish, 1.0 –1.5 μm thick, large verrucose, granules on
surface up to 1.6 μm, two or more gathered. Uredinia absent.
Telia caulicolous, on fusiform or irregular swellings with knotty
rough surface, pulvinate, applanate, or somewhat wart-like;
teliospores chiefly 2-celled, occasionally with 1 or 3 cells, nar-
Fig. 9 Morphology of G. libocedri. a. Aecia (A) on the hypophyllous leaf surface; b. linear-rhomboid peridial cells observed by LM; c. ultrastructure of peridial
cells observed by SEM; d. globoid or ellipsoid aeciospores with scattered germ pores observed by LM; e. ultrastructure of aeciospores with apparent germ
pores (G) observed by SEM; f. foliicolous telia (T); g. 2-celled and pedicellate teliospores with cylindrical and hyaline pedicels; h. 3- or 4-celled teliospores
observed by LM. — Scale bars: b– c = 50 µm; d– e, g– h = 20 µm.
90 Persoonia – Volume 45, 2020
rowly ellipsoid, 34–89 × 14–23 μm, walls 1–3.5 μm, brownish,
pores usually 1 in a cell apical, sometimes near the septum in
the upper cell, pedicels cylindrical, 3.0–4.5 μm diam.
Additional materials examined. China, Jiangsu, Nanjing, III on J. chinensis,
5 Apr. 1932, F.L. Tai, HMAS11150; Jiangsu, Nanjing, 0, I on M. spectabilis,
22 Sept. 1928, F.L. Tai, HMAS11186 & HMAS11201; Shaanxi, Wugong, III
on J. chinensis var. kaizuca, 16 Apr. 1940, S.E. Liu, HMAS22178. – Finland,
Nyland, 0, I on M. sylvestris, 8 Sept. 1912, S. Salmenlinna, HMAS70746;
Nyland, 0, I on M. sylvestris, 1 Sept. 1949, H.H. Roivainen, CUP-56156.
Hosts range and geographical distribution confirmed in this study —
Chamaecyparis pisifera – Japan; Juniperus chinensis – China; Juniperus
sp. – USA; Malus sylvestris – Finland.
Additional host range and geographical distribution reported in previous
studies — Chamaecyparis pisifera – Japan; Chamaecyparis pisifera var.
plumosa – Japan; Chamaecyparis pisifera var. squarrosa – Japan; Micro-
meles alnifolia – Japan; Micromeles japonica – Japan; Pyrus miyabei – Japan;
Sorbus alnifolia – Japan, South Korea; Sorbus commixta – Japan; Sorbus
japonica – Japan (Farr & Rossman 2019).
Notes — This species was first reported from Japan with
its telial host on Chamaecyparis pisifera, and aecial hosts on
Micromeles alnifolia and M. japonica (Yamada & Miyake 1908).
This rust is characterised by the dimensions of its peridial cells,
aeciospores with large verrucose ornamentations and densely
verrucose peridial cells. In addition, it has 1–3-celled teliospores
with cylindrical pedicels. Here we confirmed the host alternation
of this species between Chamaecyparis, Juniperus and Malus,
and the species delineation and geographic distribution of this
species was clarified.
Gymnosporangium monticola H.Y. Yun, Mycologia 101:
803. 2009
Typus. SoUth Korea, Gyeonggi, Gwacheon, III on J. rigida, 10 Apr. 2001,
H.Y. Yun, HKFRI-2018 (holotype).
Spermogonia not found. Aecia foliicolous, fructicolous, roeste-
lioid; peridium cornuted, rupturing and lacerate, 0.5–3.0 mm
high, peridial cells roundish rhomboid, 42–93 × 14– 22 µm long,
outer walls smooth, inner walls with small papillae; aeciospores
globose or ovoid, 16–31 × 14–26 µm, walls yellow-brown,
1.0–2.5 µm thick, minutely coronate. Uredinia absent. Telia
caulicolous, forming irregularly fusiform swellings of smaller
branches, applanate or pulvinate, dark brown, 14–55 µm;
teliospores 2–3-celled, broadly ellipsoid, 28–55 × 15 –31 µm,
walls orange, with thin-walled, 1.4–2.8 µm thick, 1–2 pores
near septum or 1 apical in upper cell; pedicels cylindrical, 2.0–
4.5 μm diam.
Additional materials examined. China, Sichuan, Wolong, 0, I on M. kan-
suensis, 23 Sept. 1982, Y.C. Wang, HMAS44514. – Japan, Shizuaka, III on
J. rigida, 1 Apr. 1924, M. Hara, HMAS11145.
Host range and geographical distribution confirmed in this study — Ju-
niperus rigida – Japan, South Korea; Malus kansuensis – China; Sorbus
alnifolia – South Korea.
Notes — Gymnosporangium monticola was first described
on J. rigida in South Korea, and this species resembles G. cor-
nutum but differs in the size of aecia, shape of peridial cells,
dimensions of peridial cells and morphology of its telial and
teliospores (Yun et al. 2009). It was described with S. alnifolia
as aecial host and J. rigida as telial host. Based on our morpho-
logical and molecular studies, host alternation was confirmed,
and M. kansuensis was reported as a new aecial host.
Gymnosporangium nelsonii Arthur, Bull. Torrey Bot. Club 28:
665. 1901 — Fig. 10
Synonyms. Aecidium nelsonii (Arthur) Farl., Bibliogr. Index N. Amer. Fungi
1(1): 68. 1905.
Gymnosporangium durum F. Kern, Bull. Torrey Bot. Club 34: 460. 1907.
Typus. USa, Wyoming, Laramie Hills, J. scopulorum, 10 May 1895, A. Nel-
son, NYBG638372 (isotype, designated as lectotype here, MBT388925).
SSU, ITS and LSU sequences GenBank MN642599, MN642594 and
MN642618.
Spermogonia not found. Aecia foliicolous, occasionally fructicol-
ous, roestelioid; peridium cornuted, rupturing by few longitu-
dinal slits along sides, 2.5–5.0 mm high, peridial cells linear-
rhomboid, 55–106 × 18–32 µm long, outer cells smooth, inner
walls densely rugose with elongate small papillae; aeciospores
globose or ovoid, 18–31 × 14–26 µm, walls yellow-brown,
2.0–2.5 µm thick, densely verrucose. Uredinia absent. Telia
caulicolous, on globoid galls up to 28 mm diam, cylindrical-
cornute, sometimes wedge-shaped, irregularly compressed;
teliospores 2-celled, narrowly or broadly ellipsoid, 38–69 ×
20–33 µm, walls orange, with thin-walled, 0.5–2.5 µm thick,
pore 1 or 2 per cell at septum, pedicel cylindrical, hyaline,
5.0–9.5 µm diam.
Additional materials examined. Canada, Ontario, Algoma, 0, I on Ame-
lanchier sp. 15 Sept. 1972, J.A. Parmelee, NYBG212838. – USa, New York,
0, I on A. alnifolia, 25 Aug. 1986, collector unknown, NYBG3009186; New
York, 0, I on Peraphyllum ramosissimum, 11 July 1993, C.T. Rogerson, NYBG
NYBG3009187; Illinois, Kane County, 0, I on Peraphyllum ramosissimum,
26 Aug. 1994, C.T. Rogerson, NYBG3009190; Illinois, Kane County, III on
J. scopulorum, 11 May 1990, C.T. Rogerson, NYBG3009191; Utah, San Juan
College, III on J. utahensis, 13 May 1945, A.S. Rhoads, CUP-65684; Utah,
Weber, III on J. scopulorum, 7 May 1987, C.T. Rogerson, NYBG3009188.
Host range and geographical distribution confirmed in our studies —
Amelanchier alnifolia – USA; Amelanchier sp. – Canada; Juniperus scopulo-
rum – Canada, USA; Juniperus utahensis – USA; Peraphyllum ramosissimum
– USA.
Additional host range and geographical distribution reported in previous
studies — Amelanchier alnifolia – Canada; Amelanchier alnifolia var. cu-
sickii – Canada, USA; Amelanchier alnifolia var. semiintegrifolia – Canada;
Amelanchier bakeri – USA; Amelanchier cusickii – Canada; Amelanchier
florida – USA; Amelanchier goldmanii – USA; Amelanchier huronensis –
Canada; Amelanchier intermedia – Canada; Amelanchier laevis – Canada;
Amelanchier mormonica – USA; Amelanchier oreophila – USA; Amelanchier
polycarpa – USA; Amelanchier pumila – USA; Amelanchier sanguinea –
Canada; Amelanchier utahensis – USA; Crataegus oxyacantha – USA;
Cydonia oblonga – USA; Cydonia vulgaris – USA; Juniperus californica
– USA; Juniperus deppeana – USA; Juniperus flaccida – USA; Juniperus
horizontalis – Canada, USA; Juniperus monosperma – USA; Juniperus oc-
cidentalis – USA; Juniperus osteosperma – USA; Malus diversifolia – USA;
Malus fusca – USA; Malus rivularis – USA; Pyrus communis – USA; Pyrus
diversifolia – USA; Pyrus fusca – USA; Sorbus occidentalis – USA; Sorbus
scopulina – USA; Sorbus sitchensis – USA (Farr & Rossman 2019).
Notes — Gymnosporangium nelsonii was first reported on
J. scopulorum in the USA. The connection with its aecial host
Amelanchier was confirmed in the early 20th century (Arthur
1934). The taxonomic status of this species in relation to G. cor-
niculans has been considered dubious for a long time. Here
we confirmed the phylogenetic distinction of the two species by
employing morphological and sequence data from a lectotype
specimen, which support these two taxa as independent spe-
cies. Hitherto, three Malus species, M. diversifolia, M. fusca
and M. rivularis were reported as aecial hosts of G. nelsonii
(Farr & Rossman 2019). We confirm the host alternation of
G. nelsonii on Amelanchier and Juniperus, and another aecial
host, Peraphyllum ramosissimum, was confirmed as a new
aecial host.
Gymnosporangium nidus-avis Thaxt., Connecticut Agric.
Exp. Sta. Bull. 107: 6. 1891 — Fig. 11
Synonyms. Puccinia nidus-avis (Thaxt.) Kuntze, Revis. Gen. Pl. (Leipzig)
3(3): 507. 1898.
Tremella nidus-avis (Thaxt.) Arthur, Proc. Indiana Acad. Sci.: 136. 1901.
Gymnosporangium juvenescens F. Kern, Bull. New York Bot. Gard. 7:
448. 1911.
91
P. Zhao et al.: Gymnosporangium on Malus
Typus. USa, Connecticut, 0, I on A. canadensis, 11 June 1889, R. Thaxter,
CUP-227 (isotype). SSU, ITS and LSU sequences GenBank MN605014,
MN605719 and MN605797.
Spermogonia not found. Aecia hypophyllous, foliicolous, fructi-
colous and caulicolous, roestelioid; peridium cylindrical, lac-
erate along sides, 2.0–4.5 mm high, peridia cells rhomboid,
55–94 × 15–27 µm long, outer cells smooth, inner walls densely
rugose; aeciospores globose or ovoid, 22–35 × 16–26 µm,
walls yellow-brown, 2.0–3.5 µm thick, densely verrucose.
Uredinia absent. Telia caulicolous, brush-like witches’ broom
or birds’ nests, ligulate or pulvinate; teliospores 2-celled, oc-
casionally 1–4-celled, 34–55 × 16– 27 µm, walls orange, with
thin-walled, 1.0–2.5 µm thick, pore 1 or 2 per cell at septum,
pedicel cylindrical, hyaline, 3.5–7.5 µm diam.
Additional materials examined. USa, Arizona, Coconino County, 0, I on
A. utahensis, 27 Aug. 1994, C.T. Rogerson, NYBG3009270; New Jersey,
Monmouth County, 0, I on M. communis, 6 May 1984, C.T. Rogerson,
NYBG461234; New York, Bruce, III on J. horizontalis, 20 May 1957, R.F. Cain,
NYBG33324; New York, Bruce, III on J. virginiana, 6 May 1984, W.R. Buck,
NYBG3011033; New York, Tompkins, Ithaca, III on Juniperus sp., 17 Mar.
1905, V.H. James, CUP-19416; Utah, Cache County, 0, I on A. alnifolia, 18
Aug. 1940, C.T. Rogerson, NYBG3009399.
Fig. 10 Morphology of G. nelsonii. a. Aecia (A) on the hypophyllous leaf surface; b. aecia with yellowish peridia (P) on the fruit; c. linear-rhomboid peridial
cells observed by LM; d. ultrastructure of peridial cells observed by SEM; e. globoid or ellipsoid aeciospores with scattered germ pores (G) observed by LM;
f. ultrastructure of aeciospores observed by SEM; g. telia on the stem with globoid galls formation; h. 1- or 2-celled and pedicellate teliospores observed by
LM. — Scale bars: c– d = 50 µm; e– f, h = 20 µm.
92 Persoonia – Volume 45, 2020
Host range and geographical distribution confirmed in this study —
Amelanchier alnifolia – USA; Amelanchier canadensis – USA; Malus com-
munis – USA; Juniperus horizontalis – USA; Juniperus virginiana – USA.
Additional host range and geographical distribution reported in previous
studies — Amelanchier alnifolia – Canada; Amelanchier alnifolia var. semi-
integrifolia – Canada; Amelanchier canadensis – Canada; Amelanchier
cusickii – Canada; Amelanchier florida – Canada; Amelanchier huronensis
– Canada; Amelanchier intermedia – Canada, USA; Amelanchier laevis –
Canada, USA; Amelanchier mormonica – USA; Amelanchier oblongifolia
– USA; Amelanchier stolonifera – USA; Amelanchier utahensis – USA;
Amelanchier vulgaris – USA; Cydonia oblonga – USA; Cydonia vulgaris –
USA; Juniperus chinensis – South Korea; Juniperus horizontalis – Canada;
Juniperus scopulorum – USA; Juniperus silicicola – USA; Juniperus virginiana
– Canada; Malus sylvestris – USA (Farr & Rossman 2019).
Notes — This species was initially described by Thaxter
(1891), with the aecial stage first reported on A. canadensis and
telial stage on J. virginiana (Farlow 1906, Parmelee 1979). It is
characterised by producing brush-like witches’ broom or birds’
nests telia and 1–4-celled teliospores with terete pedicels. We
successfully generated rDNA sequence data from the isotype
specimen, and further confirmed taxonomic identity, host alter-
nation and geographic distribution of this species. Here, one
new aecia host of G. nidus-avis, i.e., M. communis, is reported
for the first time.
Fig. 11 Morphology of G. nidus-avis. a. Label of type specimen and aecia (A) on the hypophyllous leaf surface; b. aecia with peridia (P) on the hypophyllous
leaf surface; c. aecia (A) on the fruit; d. linear-rhomboid peridial cells observed by SEM; e. globoid or ellipsoid aeciospores with scattered germ pores observed
by LM; f. ultrastructure of aeciospores observed by SEM; g. foliicolous telia (T) with pulvinate sori; h. 2-celled and pedicellate teliospores with cylindrical and
hyaline pedicels, occasionally with 1- or 3-celled teliospores. — Scale bars: d = 50 µm; e– f, h = 20 µm.
93
P. Zhao et al.: Gymnosporangium on Malus
Gymnosporangium shennongjiaense P. Zhao & L. Cai, sp.
nov. — MycoBank MB832744; Fig. 12
Etymology. Epithet refers to the locality where the type specimen was
collected.
Typus. China, Hubei, Shennongjia, 0, I on M. asiatica, 9 Sept. 1984,
L. Guo (holotype HMAS55353). SSU, ITS and LSU sequences GenBank
MN605025, MN605723 and MN605801.
Spermogonia, uredinia and telia not found. Aecia hypophyl-
lous, roestelioid, foliicolous and caulicolous, 0.5– 2.0 mm high;
peridium cylindric, becoming fimbriate, peridial cells rhomboid-
oblong, 69–105 × 33–51 mm, outer walls smooth, inner walls
verruculose with ridge-like papillae; aeciospores globoid, large
coronate, 27–49 × 24–37 µm, walls yellowish, 2.0 –5.0 µm thick.
Additional materials examined. China, Guizhou, Guiyang City, 0, I on
Malus sp., 14 May 2015, P. Zhao, ZP-R511; Sichuan, Guangyuan, Huaying,
Tianchi, 0, I on M. asiatica, 21 May 2016, P. Zhao, ZP-R420.
Hosts range and geographical distribution — Malus asiatica – China;
Malus sp. – China.
Notes — This novel species differs from other Gymnospor-
angium species but resembles G. clavipes in aecial morphology,
such as the dimension of peridial cells and aeciospores, position
of aecia and peridia. Detailed morphological comparison indi-
cated that the ornamentation of peridial cells and aeciospores
can differentiate the two species. Gymnosporangium shennon-
gjiaense has peridial cells with a verruculose inner walls, which
differs from the tuberculate inner walls of G. clavipes. It also has
aeciospores with large coronate walls, while G. clavipes has
echinulate aeciospores. Molecular data further supported the
phylogenetic distinction of the two species (Fig. 2). This novel
species is found on M. asiatica and one unidentified Malus
species in the southwest part of China, but its telial host is still
unknown.
Gymnosporangium spinulosum P. Zhao & L. Cai, sp. nov. —
MycoBank MB832745; Fig. 13
Etymology. Epithet refers to special spines on the surface of peridia and
aeciospores.
Typus. China, Sichuan, Chengdu, 0, I on M. spectabilis, 19 May 1955,
Y.C. Wang (holotype HMAS26416). SSU, ITS and LSU sequences GenBank
MN605030, MN605727 and MN605805.
Spermogonia, uredinia and telia not found. Aecia foliicolous, hypo-
phyllous, roestelioid, 4–9 mm high, tubular; peridium cornuted,
rupturing at apex, peridial cells rhomboid or oblong, 55–86 ×
14–23 μm, outer cells rugose, inner walls densely verrucose
with long papillae up to 5 μm; aeciospores globoid, 14–25 ×
13–22 μm, walls slightly brown, 2 μm thick, evenly thickened,
walls large coronate, basal parts columnar and upper parts
separated into several long protuberances.
Additional materials examined. China, Jiangsu, Suzhou, 0, I on M. specta-
bilis, 7 Sept. 1929, H.T. Chang, HMAS11219.
Host range and geographical distribution — Malus spectabilis – China.
Notes — This species is characterised by its special orna-
mentation in peridial cells and aeciospores. In addition, it has
relatively small aeciospores. Compared to other Gymnospor-
angium species, it resembles G. asiaticum in the dimension
of its aeciospores, and the two species have commonly been
Fig. 12 Morphology of G. shennongjiaense. a. Aecia (A) on the hypophyllous leaf surface; b. peridia (P) on the hypophyllous surface of leaf; c. oblong peridial
cells with apparently thickened side walls; d. ellipsoid aeciospores with apparently thickened apex; e. globoid or ellipsoid aeciospores with scattered germ
pore (G). — Scale bars: c– e = 20 µm.
94 Persoonia – Volume 45, 2020
confused in the past (Wang & Guo 1985, Zhuang 2012). How-
ever, these two species clearly differ in ornamentation of peri-
dial cells and aeciospores. This novel species has peridial
cells with papillae up to 5 μm long, which clearly differs from
those in G. asiaticum. Besides, it has aeciospores with basal
parts columnar and upper parts separated into several long
protuberances, and this character can clearly differentiate the
two species. Phylogenetic results further supported this species
distinct from G. asiaticum and other species.
Gymnosporangium tiankengense P. Zhao & L. Cai, sp. nov.
— MycoBank MB832746; Fig. 14
Etymology. Epithet refers to the locality where the type specimen was
collected.
Typus. China, Guangxi, Bai Se, Leye County, Shenmu Tiankeng, 0, I on
Malus sp., 18 June 2017, P. Zhao (holotype HMAS248124). SSU, ITS and
LSU sequences GenBank MN605026, MN605725 and MN605803.
Spermogonia, uredinia and telia not found. Aecia foliicolous,
hypophyllous, roestelioid; peridium tubular, spreading or erect,
3–8.5 mm high, peridial cells rhomboid-oblong, 34–77 × 17– 32
mm, outer walls smooth, inner walls small papillae and side
walls moderately rugose; aeciospores globoid, ovoid, large
coronate, 16–24 × 14–20 mm, walls yellowish, 1.0 – 2.0 mm
thick, germ pore 3–7, scattered.
Additional materials examined. China, Guangxi, Bai Se, Leye County,
Shenmu Tiankeng, 0, I on Malus sp., 18 June 2017, P. Zhao, ZP-R1375.
Host range and geographical distribution — Malus sp. – China.
Notes — This species is characterised by its relatively
smaller peridial cells and aeciospores. Aecial morphological
differences of this rust were distinct from other Gymnospor-
angium species on Malus species, except G. libocedri (Kern
1973). Based on our morphological comparison, G. libocedri
has relatively short peridia on aecia, and large peridial cells
Fig. 13 Morphology of G. spinulosum. a. Labels of the holotype specimen and aecia (A) on the hypophyllous leaf surface; b. peridia (P) on the hypophyllous
surface of leaf; c. peridia (P) on the fruit; d. ultrastructure of peridium observed by SEM; e. rhomboid peridial cells observed by LM; f. ultrastructure of peridial
cells with long papillae; g. long papillae on peridial cell surface observed by SEM; h. globoid or ellipsoid aeciospores with scattered germ pore (G); i. verrucose
aeciospores observed by SEM. — Scale bars: d = 200 µm; e– f, h– i = 20 µm; g = 5 µm.
95
P. Zhao et al.: Gymnosporangium on Malus
(77–148 × 15 – 29 μm), which clearly differs from our newly
proposed species. The ornamentation of aeciospores in G. libo-
cedri is verrucose with refractive granules and its peridial cells
with verrucose outer walls and inner walls. In addition, this new
species resembles to G. shennongjiaense but differs in length
of peridia, dimension of peridial cells and aeciospores. These
morphological characters can clearly differentiate the two spe-
cies, and molecular data further supported the phylogenetic
distinction of this species from other Gymnosporangium spe-
cies. This species was discovered at the edges of Tiankeng in
Guangxi province in southwest part of China.
Gymnosporangium tremelloides R. Hartig, Lehrb. Kaum-
krankh. 55. 1882
Spermogonia not found. Aecia hypophyllous, foliicolous, roeste-
lioid; peridium cylindrical, becoming fimbriate to base, twisted or
spreading, 0.5–2.5 mm high, peridial cells rhomboid, 62–105
× 16–24 µm long, outer cells smooth, inner walls rugose,
with irregular ridges, roundish or irregular ridge-like papillae
interspersed; aeciospores globose or ovoid, 33–45 × 26–36
µm, walls yellow-brown, 2.0–3.5 µm thick, densely echinu-
late. Uredinia absent. Telia caulicolous on fusiform or gall-like
swellings of small branches, applanate, becoming tremelloid or
patelliform; teliospores 2-celled, ellipsoid, 35–75 × 16–28 µm,
walls orange, with thin-walled, 1.0–2.5 µm thick, 2–3 pores,
2 pores in lower cell near the septum and 1 sometimes in apical
walls, pedicel cylindrical, hyaline, 2.5–3.5 µm diam.
Materials examined. Finland, Kerava Alikerava, Harjula, 0, I on M. bac-
cata var. mandshurica, J. Roivainen, CUP-56396; AI, Kökar Lindö, 0, I on
M. silvestris, 1 Sept. 1949, H. Roivainen, CUP-56165. – USa, Wyoming,
Albany County, III on J. communis, 7 June 1993, W.R. Buck, NYBG23203.
Host range and geographical distribution confirmed in this study — Malus
baccata – Norway; Malus domestica – Bulgaria, Denmark, Finland, Norway,
Poland, Sweden; Malus sylvestris – Bulgaria, Denmark, Finland, Norway,
Poland, Sweden, Turkey.
Additional host range and geographical distribution reported in previous
studies — Crataegus oxyacantha – Norway; Crataegus sanguinea var. chloro-
carpa – Norway; Crataegus succulenta – Norway; Cydonia oblonga – Norway,
Sweden; Juniperus communis – Canada, Denmark, Finland, France, Ger-
many, Norway, Poland, Sweden, Turkey, USA; Juniperus communis subsp.
nana – Poland; Juniperus communis var. montana – Canada, USA; Juniperus
sibirica – Russia; Malus baccata – Sweden; Malus domestica – Bulgaria,
Denmark, Finland, Norway, Poland, Sweden, Turkey; Malus sylvestris –
Denmark, Finland, Germany, Norway, Poland, Sweden, Turkey; Pyrus
communis – Turkey; Sorbus aria – Bulgaria, Denmark, Germany, Norway,
Poland, Sweden, Turkey; Sorbus aucuparia – Sweden, Turkey; Sorbus
chamaemespilus – Germany; Sorbus dumosa – USA; Sorbus hupehensis
– China; Sorbus koehneana – China; Sorbus obtusifolia – Norway; Sorbus
occidentalis – Canada; Sorbus rehderiana – China; Sorbus rupicola – Nor-
way; Sorbus scopulina – Canada; Sorbus sitchensis – Canada; Sorbus
sitchensis var. grayii – Canada; Sorbus sitchensis var. sitchensis – Canada
(Farr & Rossman 2019).
Notes — Gymnosporangium tremelloides was validly de-
scribed instead of the name G. juniperinum, which epithet was
recognized as a nomen ambiguum (Kern 1973). This species
is characterised by its relatively larger aeciospores and peridial
cells with rugose inner walls, tremelloid telia, and it is widely
distributed in Africa, Asia, North America and Europe (Farr &
Rossman 2019). This species was reported with its aecial stage
on three Malus species and several Pyrus and Sorbus species,
and its telial stage was reported on J. communis and J. sibirica
(Crowell 1940, Kern 1973). Here we confirmed its aecial stage
on three Malus species, and host alternation was verified by
molecular data.
Gymnosporangium yamadae Miyabe ex G. Yamada, Sho-
kubutse Byorigaku (Pl. Path) Tokyo Hakubunkwan 379:
306. 1904 — Fig. 15
Synonym. Gymnosporangium yamadae Miyabe, Bot. Mag. (Tokyo) 17:
34. 1902, nom. inval.
Gymnosporangium yamadae (Miyabe) Kern, Bull. New York Bot. Gard.
7: 466. 1911.
Fig. 14 Morphology of G. tiankengense. a. Aecia on the hypophyllous leaf surface; b. erect peridia (P) on the hypophyllous leaf surface; c. oblong peridial
cells observed by LM; d. ultrastructure of peridial cells observed by SEM; e. globoid or ellipsoid aeciospores with scattered germ pores (G) observed by LM;
f. verrucose aeciospores observed by SEM. — Scale bars: c– f = 20 µm.
96 Persoonia – Volume 45, 2020
Typus. Japan, Hokkaido, Sapporo-shi, 0, I on M. domestica, III on J. chin-
ensis, K. Miyabe (lectotype designated here, MBT389911, Yamada (1904:
306 (0, I, III), f. 38).
Epitypification. Japan, Aomori, Mutsu, Kuroshi, 0, I on M. domestica, 30 July
1913, M. Miura, NYBG2584 (epitype designated here, MBT389912). SSU,
ITS and LSU sequences GenBank MN605048, MN605735 and MN605813.
Spermogonia not found. Aecia hypophyllous, foliicolous, roes-
telioid, 3–6 mm high; peridium cornuted, rupturing in a lace-like
network along the sides, peridial cells linear-rhomboid, 55–131
× 16–34 µm, verrucose with long papillae, outer walls smooth,
inner and side walls sparsely echinulate; aeciospores globoid
or ovoid, 17–27 × 16–26 µm, walls dark yellow, 1.5– 2.5 µm
thick, with small coronate. Uredinia absent. Telia foliicolous, or
caulicolous, on globose swellings or small galls up to 9 mm high;
teliospores 2-celled, ellipsoid or obovoid, 31–56 × 15–28 µm,
walls 1.0–2.7 µm, pale orange to orange, pores 2 near sep-
tum or 1 apical in upper cell, frequently with an obtuse hyaline
papilla at apex, pedicel cylindrical, hyaline, 2.5–3.5 µm diam.
Additional materials examined. China, Beijing, 0, I on M. baccata, 19 Sept.
1992, S.X. Wei, HMAS80528; Beijing, 0, I on M. baccata, 13 Aug. 1947, col-
Fig. 15 Morphology of G. yamadae. a. Label of type specimen and aecia (A) on the hypophyllous leaf surface; b. linear-rhomboid peridial cells observed by
LM; c. ultrastructure of peridial cells observed by SEM; d. globoid or ellipsoid aeciospores with scattered germ pores (G) observed by LM; e. ultrastructure
of aeciospores observed by SEM; f. foliicolous telia with pulvinate sori; g. 2-celled and pedicellate teliospores with cylindrical and hyaline pedicels; h. 3- or
4-celled teliospores observed by LM. — Scale bars: b– c = 50 µm; d– e, g– h = 20 µm.
97
P. Zhao et al.: Gymnosporangium on Malus
lector unknown, HMAS17719 & HMAS17707; Beijing, 0, I on M. baccata,
19 Sept. 1998, J.Y. Zhuang, HMAS157814, HMAS157815 & HMAS157816;
Beijing, 0, I on M. micromalus, 10 Dec. 2008, J.Y. Zhuang, HMAS243188 &
HMAS199333; Beijing, 0, I on Malus sp., date unknown, Dorsett & Morse,
NYBG67267; Beijing, III on J. chinensis, Y.C. Wang, HMAS47229; Gansu,
Lanzhou, 0, I on M. prunifolia, 30 June 1974, D. Fu, HMAS36992; Hubei,
Shennongjia, 0, I on Malus sp., L. Guo, HMAS55350 & HMAS55351; Inner
Mongolia, Hohhot, III on J. chinensis, 15 May 1992, Z.S. Hou, HMAS82779;
Jiangsu, Nanjing, 0, I on M. spectabilis, 7 Sept. 1929, F.L. Tai, HMAS11220;
Jiangsu, Wuxi, 0, I on Malus sp., Q.X. Wu, HMAS14327; Shaanxi, Xian, 0, I on
M. mandshurica, 26 Sept. 1963, Y.C. Wang, HMAS34430; Shanxi, Taiyuan,
0, I on M. prunifolia, 19 June 1974, B. Li, HMAS36991; Yunnan, Diqing,
Shangri-La, 0, I on M. micromalus, P. Zhao, ZP-R16, ZP-R6001, ZP-R6003
& ZP-R6004. – Japan, Iwate prefecture, Mrioka, 0, I on M. communis, data
unknown, K. Togashi, NYBG3009547; Tokyo, 0, I on Malus spectabilis, 23
June 1994, N. Nambu, NYBG53757; Saitama prefecture, Kamine-mura, 0, I
on M. halliana, 30 June 1931, Y. Shibasaki, NYBG3009548 & NYBG3009550.
– USa, New York, 0, I on M. micromalus, 14 Aug. 1934, G.B. Cummins,
CUP-20612.
Host range and geographical distribution confirmed in this study — Juni-
perus chinensis – China, Japan; Juniperus chinensis var. kaizuka – South
Korea; Malus baccata – China; Malus communis – Japan; Malus toringo
– South Korea; Malus mandshurica – China; Malus micromalus – China;
Malus prunifolia – China; Malus spectabilis – China, Japan.
Additional host range and geographical distribution reported in previous
studies — Juniperus chinensis – USA; Juniperus chinensis var. procumbens
– Japan; Juniperus chinensis var. sargentii – Japan; Juniperus sargentii –
Russia; Juniperus squamata – Japan; Malus platycarpa – Japan; Malus
prunifolia – Japan; Malus spontanea – Japan; Malus theifera – Japan; Malus
toringo – South Korea; Malus transitoria – Japan; Malus yunnanensis – Japan
(Farr & Rossman 2019).
Notes — This species was first reported on J. chinensis
based on Japanese specimens (Miyabe 1903), but the name
was invalid because no description of this species was pro-
posed. One year later, Yamada (1904) described this species
in the textbook of plant pathology validating it with a description.
Due to lack of holotype specimen, we designated type illustra-
tions of Yamada (1904) as lectotype. In addition, we desig-
nated an epitype specimen, which was collected in Japan on
M. domestica in Aomori prefecture in Japan, which is adjacent
to type locality. The host alternation of this species between
M. domestica, M. spectablilis, M. sieboldii and J. chinensis
was confirmed by Miyabe (1903). Thereafter, a new name,
G. yamadae (Miyabe) F. Kern (1911) was used to describe this
fungus based on its type specimen on M. spectabilis, which was
collected by N. Nambu in Tokyo. Due to nomenclatural priori-
ty, the name proposed by Kern in 1911 should be abandoned
for use, and it was also conspecific to G. yamadae Miyabe
ex G. Yamada based on our morphological examination of
specimens used for species description by Kern. In terms of
quarantine, this species is listed as a quarantine pest in North
America due to the severe damage it causes on commercial
Malus and Pyrus species (EPPO/CABI 1996a). We confirmed
species delineation, host alternation and geographic distribu-
tion, which are of vital importance to plant quarantine.
ADDITIONAL TAXONOMIC NOVELTY RECOGNIZED IN
THIS STUDY
Gymnosporangium kanas P. Zhao & L. Cai, sp. nov. — Myco-
Bank MB831270; Fig. 16
Etymology. Epithet refers to Kanas Lake, where the type specimen was
collected.
Typus. China, Xinjiang, Altay Prefecture, Kanas Lake, aecial stage on
Cotoneaster dammeri, 16 Aug. 2016, P. Zhao (holotype HMAS248105). SSU,
ITS and LSU sequences GenBank MK488124, MK518825 and MK518469.
Spermogonia Group (type 4), foliicolous, epiphyllous, subepi-
dermal, determinate, black or dark brown, 0.1–0.4 mm, with
strongly concave hymenia, bounding structures with well-deve-
loped periphyses. Aecia Roestelia-type, fructicolous, roestel-
ioid, white finger-like tubes develop all over fruit, 4–7 mm high,
tubular, rupturing at apex; peridium cylindrical, retaining more or
less tubular shape, erect or spreading, peridial cells verrucose-
rugose, 39–91 µm long, 19–27 µm wide, aeciospores globoid
Fig. 16 Morphology of G. kanas. a. Spermogonia (S) on the epiphyllous leaf surface; b. aecia only found on fruits; c. peridia cells (P) on fruits; d. globoid or
ellipsoid urediniospores observed by light microscope, germ pores (G) scattered; e. peridial cells cylindrical, retaining more or less tubular shape, verrucose-
rugose. — Scale bars: a– c = 0.5 mm; d– e = 20 µm.
98 Persoonia – Volume 45, 2020
or broadly ellipsoid, 20–28 × 16– 22 µm, verrucose, walls 1.5– 3
µm thick. Uredinia and telia not found.
Additional material examined. China, Xinjiang, Altay Prefecture, Kanas
Lake, aecial stage on Cotoneaster dammeri, 16 Aug. 2016, P. Zhao, ZP-R481.
KEY TO GYMNOSPORANGIUM SPECIES RECOGNIZED
IN THIS STUDY
1. Aecia with balanoid peridium, peridial cells oblong, aecio-
spores relatively small, 15–29 × 14–24 μm, walls large co-
ronate...........................G. lachrymiforme
1. Aecia with tubular peridium . . . . . . . . . . . . . . . . . . . . . . 2
2. Peridial cells prismatic, 43 – 96 × 27–64 μm, rugose with
set ridges, peridium cornuted, aeciospores verrucose ..
.................................G. fenzelianum
2. Peridial cells rhomboid or oblong . . . . . . . . . . . . . . . . . 3
3. Peridial cells inner walls densely verrucose with long
papillae, aeciospores walls large coronate, basal parts
columnar and upper parts separated into several long
protuberances ..................... G. spinulosum
3. Peridial cells inner walls with small papillae .........4
4. Aeciospores echinulate . . . . . . . . . . . . . . . . . . . . . . . . . 5
4. Aeciospores not echinulate . . . . . . . . . . . . . . . . . . . . . . 6
5. Peridial cells inner walls tuberculate, teliospores 2-celled,
pedicels carotiform, 10–24 μm diam ...... G. clavipes
5. Peridial cells inner walls rugose, teliospores 2-celled,
pedicels cylindrical, less than 2.5–3.5 µm diam .......
.................................G. tremelloides
6. Peridial cells inner walls and side walls evenly echinulate,
77–148 × 15–29 μm, aeciospores large coronate, telio-
spores 46–97 × 15–21 μm, pedicels cylindrical, 3.0 –7.5 μm
diam.............................G. clavariiforme
6. Peridial cells inner walls and side walls not echinulate . 7
7. Aeciospores verrucose .........................8
7. Aeciospores coronate .........................12
8. Aeciospores verrucose with refractive granules, peridial
cells inner walls verrucose, teliospores 2–5-celled, pedicels
cylindrical, up to 20 μm diam ............G. libocedri
8. Aeciospores verrucose without refractive granules.... 9
9. Aeciospores large verrucose with large processes, peridial
cells densely verrucose, teliospores 1–3-celled G. miyabei
9. Aeciospores densely verrucose.................. 10
10. Peridial cells inner walls densely rugose with elongate small
papillae, telia on globoid galls up to 28 mm diam, telio spores
2-celled, 38–69 × 20–33 µm, pedicel cylindrical, hya-
line, 5.0–9.5 µm diam . . . . . . . . . . . . . . . . . . .G. nelsonii
10. Peridial cells inner walls densely rugose without elongate
small papillae................................ 11
11. Peridium cylindrical, lacerate along sides, telia caulico-
lous, brush-like witches’ broom or birds’ nests, teliospores
1–4-celled ..........................G. nidus-avis
11. Peridium cylindrical, rupturing at apex .......G. kanas
12. Peridial cells inner walls and side walls moderately rugose,
aeciospores 18–34 × 14– 22 μm, telia globoid or reniform
galls, 10–40 mm diam, teliospores 2-celled, 35–66 ×
16–23 μm ...................G. juniperi-virginianae
12. Peridial cells side walls rugose, inner walls small papillae
with irregular verruculose with ridge-like papillae .... 13
13. Aeciospores small coronate, processes 0.3– 0.6 μm in
height ..................................... 14
13. Aeciospores large coronate, processes over 1 μm in
height ..................................... 16
14. Peridial cells oblong to rhomboid, telia caulicolous, for-
ming irregularly fusiform swellings of smaller branches,
teliospores 2–3-celled.................G. monticola
14. Peridial cells linear-rhomboid, teliospores 2-celled . . . 15
15. Peridium tubular, peridial cells 55–103 × 18–31 μm, telia
developing on witches’ broom, aggregated bluntly conical,
hemispherical, pulvinate or somewhat wedge-shaped ..
................................... G. cornutum
15. Peridium cornuted, rupturing in a lace-like network along
the sides, telia on globose swellings or small galls up to
9 mm diam ......................... G. yamadae
16. Peridium cornuted, tardily dehiscent by side lacerations,
causing hypertrophy, telia globoid galls up to 12 mm diam
................................. G. corniculans
16. Peridial cells rhomboid-oblong . . . . . . . . . . . . . . . . . . 17
16. Peridial cells linear-rhomboid . . . . . . . . . . . . . . . . . . . 18
17. Peridia minute, up to 2 mm in height, peridial cells relatively
large, 69–105 × 33–51 mm, aeciospores large, 27–49 ×
24–37 µm ....................G. shennongjiaense
17. Peridia up to 8.5 mm in height, peridial cells small, 34–77
× 17–32 mm, aeciospores small, 16–24 × 14– 20 mm ..
................................G. tiankengense
18. Peridia up to 7 mm in height, aeciospores small, 18– 26 ×
14–22 μm, telia developing on witches’ broom, hemispheri-
cal, pulvinate or somewhat wedge-shaped, teliospores
small, 31–50 × 16–27 μm .............G. asiaticum
18. Peridia minute, up to 2 mm in height, aeciospores large,
27–49 × 24–37 mm, telia caulicolous on fusiform or gall-
like swellings, teliospores large, 32–85 × 23– 32 mm
...................................G. globosum
DISCUSSION
Differentiation of Gymnosporangium from other rust
genera
Since the establishment of the genus Gymnosporangium based
on rust collections on juniper hosts in Europe, this genus
has long been classified in the family Pucciniaceae due to its
pedicellate teliospores and Group V spermogonia (Hiratsuka
& Hiratsuka 1980, Hiratsuka et al. 1992, Cummins & Hiratsuka
2003). However, recent phylogenetic studies suggested its
phylogenetic distinction from core Pucciniaceae (Puccinia/
Uromyces) (Maier et al. 2003, Aime 2006, Aime et al. 2018).
Here we included representative taxa from the order Puccini-
ales to determine the phylogenetic relationship of Gymnospo-
rangium species to other rust genera, especially those in the
family Pucciniaceae. More than 77 genera from 14 families in
the Pucciniales were involved, and until now, this phylogeny
provides the highest coverage of genera within this order. We
confirmed the monophyly of the genus Gymnosporangium, and
being distinct from other genera in the family Pucciniaceae.
Morphologically, Gymnosporangium produces teliospores with
gelatinous pedicels and Roestelia-type aecia, which clearly dif-
fer from other genera in Pucciniaceae (Sydow & Sydow 1915,
Arthur 1934, Kern 1973, Cummins & Hiratsuka 2003). In addi-
tion, the life cycle of the genus Gymnosporangium is unique,
having a telial stage on gymnosperms and aecial stage on an-
giosperms, and such host alternation is different from most rusts
on gymnosperms, which have aecial stages on gymnosperms
but uredinial/ telial stages on angiosperms (Cummins & Hirat-
suka 2003). Phylogenetic results also supported morphological
distinctions. Thus, we proposed a new family, Gymnosporan-
giaceae to accommodate the genus Gymnosporangium. Our
phylogenetic results of the order Pucci niales further emphasized
the need for a taxonomic revision of rust fungi at family level,
and the taxonomic criteria (mainly the structure of spermogonia
and morphology of teliospores) used by Cummins & Hiratsuka
99
P. Zhao et al.: Gymnosporangium on Malus
(1983) were shown to be inappropriate at family level. Further
comparative studies need to be conducted to resolve the con-
fusion surrounding the circumscription of families and genera
within the Pucciniales.
Taxonomic importance of rust fungi using holomorphic
morphology
Hitherto approximately 64 Gymnosporangium species and 14
species of its asexual morph Roestelia have been reported
(Kern 1973, Lee & Kakishima 1999a, b, Shen et al. 2018). Most
of the reported Gymnosporangium species lack an uredinial
stage in their life cycles, and both aecial and telial host ranges
have long been proven to be ineffective for species recogni-
tion (Kern 1973, Hiratsuka et al. 1992, Zhao et al. 2016). Thus,
morphological characteristics in aecial structures, i.e., type of
aecia, surface ornamentation of peridial cells, and shape, size
and colour of aeciospores, served as important taxonomic cri-
teria at species level (Sydow & Sydow 1915, Lee & Kakishima
1999a, b). Previously, aecia within this genus were divided
into two types, roestelioid and aecidioid, and roestelioid aecia
were further divided into five types based on shape and type
of rupture (Parmelee 1965, Kern 1973). Furthermore, 12 types
of surface structures in aeciospores and 10 types of peridial
cell walls were further recognized among Gymnosporangium
species (Lee & Kakishima 1999a, b). Our phylogenetic studies
support the effectiveness of above-mentioned characters for
species recognition. However, these characters alone were still
insufficient for species recognition, and the morphology of the
telial stage, i.e., septation of teliospores, morphology of pedicel
cells and shape of telia, are essential for identification. With the
aid of molecular information, the connection of aecia and telia
provided additional morphological characters for species recog-
nition, especially for those that shared similar morphologies in
certain spore stages. In addition, the lack of life cycle informa-
tion sometimes led to confusion, such as G. asiaticum and its
synonyms G. chinense, G. haraeanum, G. koreanse, G. spini-
ferum and G. unicorne. Due to the lack of life cycle informa-
tion, they were proposed as distinct species based on slight
differ ences in teliospore morphology (Sydow & Sydow 1915,
Yun et al. 2009). Here we confirmed the host alternation of
G. asiaticum, and further confirmed these above-mentioned
species as conspecific to G. asiaticum. Thus, morphological
characteristics in the whole life cycle are of vital importance to
facilitate accurate species delimitation.
The complexity of host specificity in Gymnosporangium
species on Malus
Our studies further emphasised no clear host specificity among
Gymnosporangium species in both aecial and telial stages. At
plant generic level, most of these Gymnosporangium species
have their aecial stage on two or more genera within Rosaceae,
and some species, such as G. clavariiforme, can parasitize
plants in up to 13 genera in Rosaceae (Crowell 1940, Novick
2008). At species level, many Gymnosporangium species
shared the same telial or aecial hosts and no host specificity was
found. In the telial stage, J. communis was confirmed as telial
host for five Gymnosporangium species, i.e., G. clavariiforme,
G. cornutum, G. gaeumannii, G. gracile and G. tremelloides.
A similarly situation was found on J. chinensis, J. oxycedrus,
J. przewalskii and J. virginiana, where they served as hosts of
two or even more Gymnosporangium species. Similarly, in the
aecial stage, M. domestica, M. pumila and M. spectabilis were
found to be hosts of two or more Gymnosporangium species.
Such an overlap in hosts might be caused by complicated
evolutionary processes of speciation within the genus. In our
previous studies, we found host switches, duplication, losses
and failure to diverge all played certain roles in driving specia-
tion in Gymnosporangium (Zhao et al. 2016). Thus, multiple
speciation mechanisms exist within the genus which might
force the phenomena of overlapping host ranges in both aecial
and telial stages.
Contributions of taxonomic studies to plant protection
and quarantine
Within the genus Gymnosporangium, several species are listed
as important quarantine pests worldwide due to their potential
threats to commercial fruit cultivars. In the European Union,
G. clavipes, G. globosum, G. juniperi-virginianae and G. yama-
dae are listed in the EPPO A1 list, and G. asiaticum is listed in
the A2 list (EPPO 2018). In Asia, G. clavipes, G. fuscum, G. glo-
bosum and G. juniperi-virginianae are treated as quarantine
pests in China, Japan, South Korea and adjacent regions (Duan
et al. 2017). In North America, G. fuscum and G. yamadae are
listed as quarantine pests in the USA and Canada (https://www.
aphis.usda.gov/aphis/ourfocus/planthealth/import-information/
rppl/rppl-table). Currently, detection of these quarantine pests
relies mainly on morphological characteristics worldwide (EPPO
2017, 2018). However, complexity of host alternation and
diverse forms of structures in aecial and telial stages render
correct identification impossible, and thus successful intercep-
tion of these pests in quarantine departments of many coun-
tries remains problematic (Duan et al. 2017). In this study we
focused on Gymnosporangium species infecting commercial
apple cultivars and their relatives, and conducted molecular and
morphological studies on these above-mentioned quarantine
pests. Typification studies were conducted on G. asiaticum,
G. fenzelianum, G. juniperi-virginianae, G. libocedri, G. nelsonii,
G. nidus-avis and G. yamadae, and morphological data in both
aecial and telia stages and DNA sequences were generated,
especially from type materials. In addition, host alternation of
each species was verified. All these data can be effective for
both morphological and molecular detection of those quarantine
pests. In addition, comparison of sequence variation of rDNA
SSU, ITS and LSU among Gymnosporangium species revealed
that concatenated data of ITS and LSU obtained a better
resolution at the species level, and therefore we recommend
this locus as effective barcode for Gymnosporangium species.
Acknowledgements This work was financially supported by National
Nature Science Foundation of China (31670017), the China National Funds
for Distinguished Young Scholars (31725001), the Biological Resources
Programme, Chinese Academy of Sciences (KFJ-BRP-009) and the Project
for Fundamental Research on Science and Technology, Ministry of Science
and Technology of China (2014FY120100). We express our gratitude to
Dr Yi-Jian Yao (State Key Laboratory of Mycology, Institute of Microbiology,
CAS, Beijing, China), Dr Scott LaGreca (Cornell Plant Pathology Herbarium,
Section of Plant Pathology & Plant-Microbe Biology, Cornell University, NY,
USA), and Dr Barbara M. Thiers (The New York Botanical Garden, NY,
USA), for providing dried specimens for this study. Finally, we are grateful
to Dr Cathie M. Aime (Botany & Plant Pathology, Purdue University, USA)
for improving the manuscript.
REFERENCES
Aime MC. 2006. Toward resolving family-level relationships in rust fungi
(Uredinales). Mycoscience 47: 112–122.
Aime MC, Castlebury LA, Abbasi M, et al. 2018. Competing sexual and
asexual generic names in Pucciniomycotina and Ustilaginomycotina (Basi-
diomycota) and recommendations for use. IMA Fungus 9: 75– 89.
Arthur JC. 1934. Manual of the rusts in United States and Canada. Purdue
Research Foundation, Lafayette, Indiana, USA.
Azbukina Z. 1972. Rust fungi of Far East Lec. Komarovianae (Komarov
Read.). Vladivost 19: 15– 62.
Beenken L. 2017. Austropuccinia: a new genus name for the myrtle rust
Puccinia psidii placed within the redefined family Sphaerophragmiaceae
(Pucciniales). Phytotaxa 1: 53– 61.
Chevallier FF. 1826. Flore générale des environs de Paris. Vol. 1. Imprimerie
Decourchant, Paris, France.
100 Persoonia – Volume 45, 2020
Crowell IH. 1940. The geographical distribution of the genus Gymnosporan-
gium. Canadian Journal of Research 18: 469– 488.
Cummins GB, Hiratsuka Y. 1983. Illustrated genera of rust fungi. 2nd edn.
American Phytopathological Society Press, St. Paul, Minnesota, USA.
Cummins GB, Hiratsuka Y. 2003. Illustrated genera of rust fungi, 3rd edn.
American Phytopathological Society, St. Paul, Minnesota, USA.
Dietel P. 1928. Uredinales. In: Engler A, Prantl K (eds), Die natürlichen Pflanzen-
familien, Vol. 2: 24– 98. Engelmann, Leipzig.
Duan WJ, Yan J, Cai L, et al. 2017. The current status and future prospect
of fungal quarantine in China. Mycosystema 36: 1311–1331.
EPPO. 2017. EPPO A1 and A2 lists of pests recommended for regulation as
quarantine pests. EPPO Standards PM 1/2(26). Available online: https://
gd.eppo.int/download/standard/2/pm1-002-28-en.pdf. Accessed Septem-
ber 2018.
EPPO. 2018. EPPO Global Database. Available online: https://gd.eppo.int.
Accessed September 2018.
EPPO/CABI. 1996a. Gymnosporangium yamadae. In: Smith IM, McNamara
DG, Scott PR, et al. (eds), Quarantine pests for Europe. 2nd edn. CAB
International, Wallingford, UK.
EPPO/ CABI. 1996b. Gymnosporangium juniperi-virginianae. In: Smith IM,
McNamara DG, Scott PR, et al. (eds), Quarantine pests for Europe. 2nd
edn. CAB International, Wallingford, UK.
Farlow WG. 1880. The Gymnosporangia or cedar-apples of the United States.
Anniversary memoirs of the Boston Society of Natural History. Boston
Society of Natural History, Boston, USA.
Farlow WG. 1906. A bibliographical index of North American fungi. The
American Naturalist 40: 146.
Farr DF, Rossman AY. 2019. Fungal databases, U.S. National Fungus Col-
lections, ARS, USDA. https://nt.ars-grin.gov/fungaldatabases/. Accessed
February 2019.
Helfer S. 2005. Overview of the rust fungi (Uredinales) occurring on Rosaceae
in Europe. Nova Hedwigia 81: 325– 370.
Hennings P. 1900. Fungi japonici. Botanische Jahrbucher für Systematic.
28: 259– 280.
Hiratsuka N. 1955. Uredinological studies. Kasai Publishing Co., Tokyo,
Japan.
Hiratsuka N, Sato S, Katsuya K, et al. 1992. The rust flora of Japan: 465–
483. Tsukuba Shuppankai, Tsukuba, Ibaraki, Japan.
Hiratsuka Y, Hiratsuka N. 1980. Morphology of spermogonia and taxonomy
of rust fungi. Reports of the Tottori Mycological Institute 18: 257–268.
Huelsenbeck JP, Ronquist F. 2001. MrBayes: Bayesian inference of phylo-
genetic trees. Bioinformatics 17: 754–755.
Hylander N. 1953. Enumerato Uredinearum Scandinavicarum. Opera Bo-
tanica 1: 1–102.
Ji JX, Li Z, Li Y, et al. 2019. Life cycle of Nothoravenelia japonica and its
phylogenetic position in Pucciniales, with special reference to the genus
Phakopsora. Mycological Progress 18: 855– 864.
Jørstad I. 1962. Distribution of the Uredinales within Norway. Nytt Magasin
for Botanik 9: 61–134.
Katoh K, Rozewicki J, Yamada KD. 2017. MAFFT online service: multiple
sequence alignment, interactive sequence choice and visualization.
Briefings in Bioinformatics 20(4): 1160–1166. doi: https:// doi.org/ 10.1093/
bib/ bbx108.
Kern FD. 1908. Studies in the genus Gymnosporangium. Bulletin of the
Torrey Botanical Club 35: 499–511.
Kern FD. 1911. A biologic and taxonomic study of the genus Gymnosporan-
gium. Bulletin of the New York Botanical Garden 7: 391–494.
Kern FD. 1964. Lists and keys of the cedar rusts of the world. Memoirs of
the New York Botanical Garden 10: 305–326.
Kern FD. 1970. The uredial stage in Gymnosporangium. Bulletin of the Torrey
Botanical Club 97: 159–161.
Kern FD. 1973. A revised taxonomic account of Gymnosporangium. Penn-
sylvania State University Press, New York, USA.
Kuprevich VF, Tranzschel VG. 1957. Rust fungi. 1. Family Melampsoraceae.
In: Savich VP (ed), Cryptogamic plants of the USSR. Vol. 4: 1–518. Bota-
nicheskogo Instituta, Komarova, Russia.
Lâce B. 2017. Gymnosporangium species – an important issue of plant
protection. Proceedings of the Latvian Academy of Sciences. Section B
708: 95–102.
Laundon G. 1977. Gymnosporangium clavipes. CMI Descriptions of Patho-
genic Fungi and Bacteria No. 543. CAB International, Wallingford, UK.
Lee SK, Kakishima M. 1999a. Surface structures of peridial cells of Gymno-
sporangium and Roestelia (Uredinales). Mycoscience 40: 121–131.
Lee SK, Kakishima M. 1999b. Aeciospore surface structures of Gymnospo-
rangium and Roestelia (Uredinales). Mycoscience 40: 109–120.
Maier W, Begerow D, Weiss M, et al. 2003. Phylogeny of the rust fungi: an
approach using nuclear large subunit ribosomal DNA sequences. Canadian
Journal of Botany 81: 12– 23.
Minnis AM, McTaggart AR, Rossman AY, et al. 2012. Taxonomy of mayapple
rust: the genus Allodus resurrected. Mycologia 104: 942– 950.
Miyabe K. 1903. On Japanese species of Gymnosporangium. Botanical
Magazine Tokyo 17: 34– 35.
Novick RS. 2008. Phylogeny, taxonomy, and life cycle evolution in the cedar
rust fungi (Gymnosporangium). PhD thesis, Yale University, New Haven,
USA.
Parmelee JA. 1965. The genus Gymnosporangium in eastern Canada. Ca-
nadian Journal of Botany 43: 239– 267.
Parmelee JA. 1971. The genus Gymnosporangium in western Canada. Ca-
nadian Journal of Botany 49: 903– 926.
Parmelee JA. 1979. Gymnosporangium nidus-avis. Fungi canadenses 139:
1–2.
Peterson RS. 1982. Rust fungi (Uredinales) on Cupressaceae. Mycologia
74: 903– 910.
Posada D, Crandall KA. 1998. MODELTEST: testing the model of DNA
substitution. Bioinformatics 14: 817–818.
Schweinitz LD. 1822. Synopsis fungorum Carolinae superioris. Schriften der
Naturforschenden Gesellschaft zu Leipzig 1: 2–131.
Shen YM, Chung WH, Huang TC, et al. 2018. Unveiling Gymnosporangium
corniforme, G. unicorne, and G. niitakayamense sp. nov. in Taiwan. Myco-
science 59: 218– 228.
Sinclair WA, Lyon HH. 2005. Diseases of trees and shrubs. 2nd edn. Cornell
University Press. Ithaca, New York, USA.
Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phyloge-
netic analyses with thousands of taxa and mixed models. Bioinformatics
22: 2688– 2690.
Sydow H, Sydow P. 1904. Neue und kritische Uredineen. Annales Mycologici.
2(1): 27–31.
Sydow H, Sydow P. 1912. Novae fungorum species. VIII. Annales Mycologici
10: 405– 410.
Sydow P, Sydow H. 1915. Monographia Uredinearum. III: Melampsoraceae,
Zaghouaniaceae, Coleosporiaceae. Leipzig, Berlin, Borntraeger, Germany.
Tai FL. 1979. Sylloge Fungorum Sinicorum. Science Press, Beijing. [In
Chinese.]
Tanaka T. 1922. New Japanese fungi. Mycologia 14: 282–295.
Thaxter R. 1891. The Connecticut species of Gymnosporangium (cedar ap-
ples). Bulletin of the Connecticut Agricultural Experiment Station. 107: 1–6.
Thompson JD, Gibson TJ, Plewniak F, et al. 1997. The CLUSTAL X windows
interface: flexible strategies for multiple sequence alignment aided by quality
analysis tools. Nucleic Acids Research 25: 4876– 4882.
Wang YC, Guo L. 1985. Taxonomic studies on Gymnosporangium in China.
Acta Mycologica Sinica 4: 24– 34.
Webster J, Weber RWS. 2007. Introduction to fungi. 3rd edn. Cambridge
University Press, Cambridge.
Wilson M, Henderson DM. 1966. The British rust fungi. Cambridge University
Press, Cambridge.
Wingfield BD, Ericson L, Szaro T, et al. 2004. Phylogenetic patterns in the
Uredinales. Australasian Plant Pathology 33: 327–335.
Yamada G. 1904. Red-spot disease of apples. In: Omori J, Yamada G (eds),
Text-book of plant pathology: 306–308. Japan.
Yamada G, Miyake I. 1908. Eine neue Gymnosporangium. Botanical Maga-
zine Tokyo 22: 21–28.
Yun HY, Hong SG, Rossman AY, et al. 2009. The rust fungus Gymnosporan-
gium in Korea including two new species, G. monticola and G. unicorne.
Mycologia 101: 790– 809.
Zhao P, Kakishima M, Wang Q, et al. 2017. Resolving the Melampsora epitea
complex. Mycologia 109: 391–407.
Zhao P, Liu F, Li YM, et al. 2016. Inferring phylogeny and speciation of
Gymno sporangium species, and their coevolution with host plants. Scientific
Reports 6: 29339.
Zhuang JY, Wei SX, Wang YC. 2012. Flora fungorum sinicorum. Vol 41.
Uredinales IV. Science Press, Beijing, China.
Ziller WG. 1974. The tree rusts of western Canada. Environment Canada
Forestry Service, Ottawa, Canada.
Supplementary material
Fig. S1 Detailed information of taxa of the family Pucciniaceae s.str. in
Fig. 1. Support values indicated at nodes. Bayesian posterior probabilities
≤ 50 % and Maximum Likelihood bootstrap (ML) ≤ 50 % were indicated by
dash line (–).
Table S1 rDNA sequence data from selected genera in the Pucciniales
used for phylogenetic studies.
Table S2 A list of species, specimens and GenBank accession numbers of
sequences used for phylogenetic studies at species level.
Supplementary material
Puccinia wolgensis on Stipa hohenackeriana AY956566
Cumminsiella mirabilissima on Mahonia aquifolium AF426206
Puccinia graminis f. sp. phlei-pratensis on Phleum pratense DQ417392
Puccinia thlaspeos L76177
Puccinia pittieriana on Solanum tuberosum EU851138
Puccinia amari on Panicum
sp. KX190839
Puccinia actaeae-elymi on Elymus europaeus JX533543
Puccinia actaeae-agropyri on Actaea spicata DQ917746
Puccinia kuehnii on Saccharum sp. GQ283009
Puccinia serpylli on Thymus sipyleus subsp. sipyleus KU872009
Puccinia mixta on Allium schoenoprasum KU296896
Puccinia cygnorum on Kunzea ericifolia EF490601
Puccinia phlomidis on Phlomis sp. KU872008
Puccinia substriata on Digitaria sp. GU058028
Puccinia graminis f. sp. avenae on Avena sativa DQ417391
Puccinia drabae on Draba incana EU014054
Puccinia durangensis on Piptochaetium pringlei HM131356
Uromyces laburni f. sp. genistae-tinctoriae on Genista tinctoria AF180155
Puccinia agrophila on Schizachyrium sp. GU058016
Uromyces striolatus on Euphorbia cyparissias AF180201
Puccinia heterospora on Abutilon sp. KU296886
Puccinia sp. 2 on Cirsium japonicum ZP-R2065
Uromyces euphorbiae-corniculati on Lotus corniculatus AF180164
Puccinia cumminsii on Panicum sp. KX190845
Puccinia porri on Allium porrum KU296909
Puccinia coronata f.sp. avenae AY114290
Puccinia veronicae-longifoliae
on
Veronica
sp. JQ627618
Uromyces trifolii-repentis on Trifolium resupinatum EU014070
Puccinia buxi on Buxus microphylla var. japonica KY800409
Puccinia carduorum on Carduus nutans JN204184
Puccinia pascua on Panicum virgatum KX190903
Puccinia striiformis f. sp. hordei
on
Hordeum vulgare
DQ460729
Puccinia persistens on Elytrigia repens DQ460722
Puccinia windhoekensis on Coccinia rehmannii DQ917710
Puccinia distincta on Bellis perennis AF468040
Edythea quitensis on Berberis hallii KX298151
Puccinia poae-nemoralis on Poa annua HM057154
Puccinia millegranae on Panicum millegrana KX190873
Uromyces pisi-sativi on Pisum sativuma DQ521578
Puccinia novopanici on Panicum virgatum KX190888
Edythea quitensis on Berberis hallii KX298153
Uromyces setariae-italicae on Setaria verticillata HQ412654
Puccinia nigrescens on Salvia verticillata subsp. amasiaca KU872005
Puccinia sp. 1 on Host unknown ZP-R10
Puccinia platyspora on Alcea rosea KT827312
Uromyces jonesii on Ranunculus alismifolius HQ317559
Endophyllum euphorbiae-sylvaticae on Euphorbia amygdaloides AF426200
Puccinia oxalidis on Oxalis sp. KJ801859+EU851130
Puccinia polysora on Zea mays HQ189433
Puccinia lobata on Malvella lepidota KT827302
Puccinia salviae on Salvia sp. KU872006
Puccinia recondita
AF511082
Puccinia otzeniani on Lampranthus otzenianus DQ917742
Puccinia brachypodii
GQ457303
Puccinia holcina on Holcus mollis DQ513000
Puccinia agropyrina on Elymus repens JX533542
Puccinia sporoboli var. robusta on Calamovilfa sp. GU058003
Puccinia persistens subsp. triticina
on
Aegilops taushii
AY956549
Puccinia mesembryanthemi on Psilocaulon leptarthron DQ917728
Uromyces scutellatus on Euphorbia cyparissias AF180198+DQ917713
Puccinia andropogonis on Lupinus perennis DQ344519
Pucciniosira pallidula on Triumfetta semitriloba DQ354534
Puccinia consimilis on Arabis pulchra var. pallens AF182972
Uromyces neotropicalis on Cucurbitaceae undet DQ021885 (T)
Puccinia sp. 3 on Smilax china ZP-R1303
Puccinia codyi on Smelowskia borealis U88233
Puccinia graminicola on Panicum virgatum KX190872
Puccinia sherardiana on Sphaeralcea sp. KT827314
Puccinia allii on Allium sativum KM249851
Puccinia asparagi AY217136
Uromyces transversalis on Gladiolus sp. JQ776984+KM249864
Uromyces dactylidis on Dactylis glomerata KM667950+KM667943
Uromyces beticola KY678771
Puccinia cannacearum on Canna indica JQ303103
Edythea quitensis on Berberis hallii KX298150
Puccinia hydrocotyles on Hydrocotyle bonplandii GU936635
Puccinia triticina on Triticum aestivum DQ417416
Puccinia graminis f. sp. dactylis on Dactylis glomerata DQ417390
Puccinia recondita f. sp. secalis on Secale cereale DQ417426
Puccinia setariae on Setaria parviflora KX190907
Puccinia knersvlaktensis on Mesembryanthemum nodiflorum DQ917726
Puccinia esclavensis
on
Zuloagaea bulbosa
KX190861
Puccinia pappophori on Pappophorum vaginatum KX190902
Uromyces punctatus on Euphorbia cyparissias AF180163
Puccinia cf. allii on Allium sativum KU296883
Edythea quitensis on Berberis hallii KX298152
Puccinia ballotiflora on Salvia greggii KF381491
Uromyces gladioli on Gladiolus sp. GU936633
Uromyces hawksworthii on Passovia ovata NR132920+KR821140 (T)
Puccinia myrsiphylli on Asparagus asparagoides DQ821712+KM249854
Puccinia coleataeniae on Coleataenia anceps subsp. anceps KX190843
Puccinia annularis on Teucrium chamaedrys subsp. chamaedrys KU872010
Puccinia crotonopsidis on Croton michauxii KX190844
Puccinia gansensis NR_111525 (T)
Puccinia pseudostriiformis on Poa pratensis AY956560
Puccinia helianthi on Helianthus sp. KM096426
Puccinia caricina on Carex rostrata U88234
Puccinia striiformis on Triticum aestivum KY354584
Uromyces aemulus AF511081
Puccinia aridariae on Mesembryanthemum guerichianum DQ917724
Puccinia corticioides on Phyllostachys glauca HM446348
Uromyces sporobolicola on Sporobolus pyramidatus HQ317560
Puccinia heterogenea on Malva arborea KT827293
Puccinia trebouxi on Melica jacquemontii EU770614
Puccinia malvacearum on Alcea sp. EF561641 (AFTOL-ID 1629)
Puccinia peradeniyae on Panicum repens KX190906
Puccinia argentata on Impatiens noli-tangere KC433402
Puccinia calcitrapae var. centaureae on Centaurea calcitrapa JN204183
Puccinia chunjii on Triticum aestivum HQ012446
Puccinia hordei-secalini on Hordeum secalinum DQ460723
Puccinia cnici-oleracei on Aster sp. GU058017
Pucciniosira sp. on Cestrum sp. EU851145
Puccinia cerinthes-agropyrina on Agropyron sp.DQ460720
Uromyces novissimus on Cayaponia sp. EU851147
Puccinia acroptili on Rhaponticum repens JN204187
Pucciniosira solani on Solanum aphyodendron EU851137
Uromyces laburni f. sp. laburni on Genista sagittalis AF180157
Puccinia subalpina on Elymus caninus JX533544
Puccinia linkii on Viburnum edule KM851040
Puccinia tanaceti on Tanacetum vulgare HQ201325
Uromyces acuminatus on Honkenya peploides GU109282
Puccinia graminis f. sp. poae on Poa pratensis DQ417389
Puccinia carthami on Carthamus tinctorius AF064822+AY787782
Puccinia pammelii on Euphorbia corollata KX190900
Puccinia aberrans on Smelowskia calycina U88232
Puccinia monoica on Arabis puberula AF182997
Puccinia komarovii on Impatiens parviflora KC460263
Puccinia striiformis f. sp. tritici on Triticum aestivum GU382673
Puccinia graminis on Festcua arundinacea DQ417385
Puccinia atra on Setaria grisebachii KX190840
Puccinia hemerocallidis on Hemerocallis sp. KM249855
Puccinia cf. helianthi on Helianthus annuus DQ917711
Uromyces probus on Sisyrinchium bellum KT267172
Uromyces pisi on Fpisum sativum cv. Messire J468405+AF426201
Puccinia graminis f. sp. lolii on Lolium sp. DQ460726
Puccinia sessilis AY217135
Puccinia bromina on Bromus sp. DQ460719
Puccinia emaculata on Panicum virgatum EU915294
Puccinia chrysanthemi on Chrysanthemum sp. KX369039
Puccinia magnusiana on Phragmites sp. GU058000
Uromyces scillarum on Allium sp. AY302495
1/100
1/100
0.90/95
1/96
0.90/82
0.89/82
1/95
0.80/86 1/81
1/100
1/98
0.90/96
-/71
1/100
0.75/87
0.86/79
1/100
-/72
Pucciniaceae sensu stricto
Fig. S1 Detailed information of taxa of the family Pucciniaceae
s.str. in Fig. 1. Support values indicated at nodes. Bayesian posterior
probabilities ≤ 50 % and Maximum Likelihood bootstrap (ML) ≤ 50 %
were indicated by dash line (–).
Pucciniaceae s.str.
Supplementary material
Chardoniella gynoxidis on Ageratina popayanense GU936636
Puccinia wyomensis on Agropyron sp. JX533541
Puccinia sp. 10 on Carpinus turczaninowii ZP-R307
Puccinia sp. 10 on Carpinus turczaninowii ZP-R6007
Puccinia melanocephala on Saccharum officinarum KU886368
Puccinia sp. 13 on Triarrhena sacchariflora ZP-R505
Puccinia purpurea on Sonchus asper ZP-R286
Uromyces ari triphylli on Arisaema triphyllum DQ354528+DQ354529
Puccinia sorghi AY114291
Puccinia sp. 22 on Miscanthus sinensis ZP-R594
Puccinia sp. 5 on Inula japonica ZP-R121
Puccinia sp. 3 on Allium thunbergii ZP-R503
Puccinia asarina on Asarum europaeum DQ917732
Puccinia sp. 19 on Saposhnikovia divaricata ZP-R118
Puccinia sp. 8 on Potentilla freyniana ZP-R567
Puccinia sp. 21 on Oxalis acetosella ZP-R1355
Puccinia erianthi on Saccharum arundinaceum ZP-R453
Puccinia sp. 17 on Akebia quinata ZP-R268
Puccinia mysuruensis on Psychotria nervosa KC847089 (T)
Uromyces lomandracearum on Lomandra sp. KT199392+KM249862
Puccinia sp. 14 on Phragmites communis ZP-R717
Puccinia sp. 19 on Saposhnikovia divaricata ZP-R107
Puccinia sp. 16 on Arundinella anomala ZP-R872
Puccinia sp. 8 on Polygonum chinense ZP-R955
Puccinia sp. 3 on Allium wallichii ZP-R500
Uromyces gageae on Gagea lutea KY996750+AF426208
Puccinia cf. mesnieriana on Rhamnus prunifolia KF661263
Puccinia chloridis on Chloris virgata KM096427
Puccinia peperomiae on Piper sp. EU851146
Puccinia virgata on Sorghastrum nutans KX190911
Endophyllum sempervivi on Sempervivum tectorum DQ917747
Puccinia erianthi on Saccharum arundinaceum ZP-R240
Puccinia vincae on Vinca major AY222047
Puccinia jasmini on Jasminum sp. KU872007
Uromyces muscari on Hyacinthoides hispanica HQ317552
Stereostratum corticioides on Indocalamus latifolius ZP-R1004
Ceratocoma jacksoniae on Daviesia sp. KT199382+KT199394
Puccinia lantanae on Lantana camara EU851144
Puccinia taeniatheri on Taeniatherum asperum AY956557
Puccinia phyllostachydis on Bambusa sp. HMAS80647
Puccinia sp. 6 on Agropyron cristatum ZP-R2070
Puccinia sp. 14 on Phragmites communis ZP-R800
Puccinia coronati-hordei on Hordeum vulgare var. nudum KU500626
Puccinia sp. 21 on Oxalis acetosella ZP-R1386
Puccinia sp. 10 on Carpinus turczaninowii ZP-R557
Puccinia saxifragae on Saxifraga stellaris DQ359699
Puccinia bartholomaei on Asclepias viridis EF583820
Puccinia sp. 7 on Halerpestes ruthenica ZP-R116
Stereostratum corticioides on Phyllostachys dulcis ZP-R1003
Uromyces cestri on Cestrum tomentosum EU851136
Puccinia sp. 11 on Akebia quinata ZP-R268
Puccinia violae on Viola sp. 1 ZP-R80
Puccinia purpurea on Clematis smilacifolia ZP-R467
Uromyces ixiae on Babiana cf. sambucina DQ917739
Puccinia wiehei on Setaria sphacelata var. splendida KX190913
Puccinia sp. 22 on Artemisia argyi ZP-R269
Puccinia digitata on Rhamnus ilicifolia KX036376
Uromyces zygadeni on Toxicoscordion venenosum HQ317555
Uromyces otaviensis on Ipomoea verbascoides DQ917715
Puccinia sp. 18 on Sinobambusa tootsik ZP-R450
Puccinia coronati-agrostidis NR_111528 (T)
Uromyces reichertii on Allium sp. ZP-R1413
Uromyces holwayi on Lilium columbianum HQ317553
Puccinia sp. 19 on Rhamnus globosa ZP-R641
Puccinia coronata var. avenae f. sp. graminicola on Holcus lanatus HM131252
Puccinia symphoricarpi on Symphoricarpos albus GU058006
Puccinia sp. 8 on Polygonum aviculare ZP-R880
Puccinia symphoricarpi on Syneilesis aconitifolia ZP-R639
Stereostratum corticioides on Indocalamus latifolius ZP-R1001
Puccinia miscanthidii on Miscanthus ecklonii KX908214
Puccinia striiformoides KP056207+KM391670
Puccinia sp. 13 on Triarrhena sacchariflora HMAS37742
Puccinia sp. 17 on Pennisetum alopecuroides ZP-R487
Puccinia phyllostachydis on Bambusa sp. HMAS12370
Puccinia sp. 15 on Clematis finetiana ZP-R654
Puccinia sp. 13 on Thalictrum aquilegifolium ZP-R649
Puccinia sp. 9 on Pennisetum alopecuroides ZP-R277
Puccinia galeniae on Aizoon canariense DQ917730
Chardoniella gynoxidis on Ageratina popayanensis EU851131
Puccinia sp. 13 on Thalictrum aquilegifolium ZP-R101
Puccinia nakanishikii on Cymbopogon citratus GU058002
Puccinia arenariae on Cerastium arvense subsp. strictum ZP-R521
Puccinia sp. 17 on Laurus nobilis ZP-R310
Puccinia sp. 21 on Camellia japonica ZP-R1387
Puccinia sparganioidis on Spartina patens GU058027
Puccinia sp. 16 on Sageretia thea ZP-R445
Puccinia sp. 7 on Thalictrum aquilegifolium ZP-R117
Uromyces lycoctoni on Aconitum napellus DQ917749
Puccinia coronati-japonica on Calamagrostis arundinacea HM131317
Uromyces hordeinus AY187086
Puccinia oxyriae on Oxyria digyna DQ917735
Puccinia sp. 13 on Triarrhena sacchariflora ZP-R485
Puccinia sp. 11 on Rheum palmatum ZP-R515
Puccinia sp. 8 on Potentilla freyniana HMAS36767
Puccinia stipina on Stipa sareptana MF002135
Puccinia sp. 10 on Rhamnus globosa ZP-R658
Puccinia arenariae on Dianthus barbatus DQ917731
Puccinia sp. 3 on Paederia scandens ZP-R455
Puccinia sp. 20 on Akebia quinata ZP-R405
Puccinia coronati-brevispora on Bromus inermis NR111526 (T)
Puccinia liliacearum on Ornithogalum umbellatum KX260148
Puccinia sp. 11 on Rheum palmatum ZP-R493
Uromyces aloes on Aloe arborescens DQ917740
Puccinia sp. 12 on Pennisetum sp. ZP-R440
Uromyces reichertii on Allium sp. AF511084
Uromyces salsolae EU872159
Puccinia sp. 4 on Prunus padus ZP-R1410
Puccinia sp. 18 on Sinobambusa farinosa ZP-R1357
Puccinia sp. 8 on Potentilla chinense ZP-R2049
Puccinia coronata var. coronata on Holcus lanatus HM057141
Puccinia sp. 15 on Pennisetum alopecuroides ZP-R850
Puccinia windsoriae on Tridens sp. GU057995
Puccinia dactylidina on Dactylis glomerata JX533546
Puccinia horiana on Chrysanthemum morifolium EU816921
Puccinia sp. 10 on Eleusine indica ZP-R294
Puccinia poarum on Tussilago sp. DQ831029+DQ831028
Puccinia purpurea on Sorghum sp. GU057999
Puccinia sp. 8 on Polygonum chinense ZP-R289
Puccinia sp. 20 on Akebia quinata ZP-R43
Puccinia heucherae on Heuchera sp. DQ359702
Puccinia sp. 18 on Akebia quinata ZP-R433
Puccinia sp. 3 on Ficus abelii ZP-R1348
Puccinia kusanoi on Yushania niitakayamensis KX610657
Chardoniella gynoxidis on Ageratina popayanensis EU851134
Stereostratum corticioides on Phyllostachys dulcis ZP-R1002
Puccinia tetragoniae on Tetragonia echinata DQ917733
0.80/86
0.85/55
1/90 1/100
0.70/64 0.90/91
0.87/89
0.7/91
0.70/69 -/51
1/100
1/100
0.99/100
-/81
1/95
0.81/-
1/99
0.81/63 0.81/53
0.76/70
-/71 0.90/95
0.83/90 -/73
1/98
-/79
Pucciniaceae sensu stricto
Fig. S1 (cont.)
Pucciniaceae s.str.
Supplementary material
Puccinia sp. 36 on Iris lactea ZP-R353
Puccinia xanthosiae on Xanthosia rotundifolia KF690685+KF690706
Puccinia aegopodii on Aegopodium podagraria DQ917698
Uromyces setariae-italicae on Setaria italica ZP-R851
Puccinia haemodori on Conostylis candicans KF690676+KF690694
Puccinia sp. 37 on Sonchus arvensis ZP-R245
Puccinia calthicola on Caltha palustris DQ917701
Uromyces scaevolae on Scaevola calendulacea KF690686+KF690707
Puccinia saccardoi on Velleia sp. KF690682+KF690702
Puccinia miscanthi on Plantago depressa ZP-R333
Puccinia violae on Viola cucullata DQ354508+DQ354509
Puccinia violae on Viola sp. ZP-R1180
Puccinia oxyriae on Oxyria sinensis ZP-R115
Puccinia circaeae on Circaea lutetiana DQ917716
Puccinia dioicae on Oenothera fruticosa GU058019
Puccinia sp. 26 on Clematis florida ZP-R239
Puccinia thaliae on Canna indica JX206994
Puccinia caricis on Grossulariaceae sp. DQ354515+DQ354514
Puccinia luzulae-maximae on Luzula sylvatica DQ917689
Puccinia tokyensis on Cryptotaenia japonica ZP-R451
Puccinia sp. 32 on Saussurea japonica ZP-R715
Puccinia sp. 25 on Hydrocotyle nepalensis ZP-R578
Puccinia latimamma on Fallopia multiflora ZP-R387
Uromyces sp. 2 on Geranium wilfordii ZP-R1497
Puccinia sp. 25 on Anemone vitifolia ZP-R624
Uromyces sp. 1 on Gaura parviflora ZP-R2065
Puccinia nepalensis on Rumex nepalensis KX225481+KX225482
Puccinia rupestris on Carex rupestris EF635898
Puccinia dioicae on Scrophularia ningpoensis ZP-R873
Puccinia sp. 25 on Calystegia hederacea ZP-R362
Dietelia portoricensis on Mikania micrantha DQ354516
Puccinia sp. 28 on Sium suave ZP-R803
Puccinia cyperi on Cyperus iria KU296885
Puccinia thaliae on Acanthopanax senticosus ZP-R1300
Puccinia sp. 37 on Serratula cardunculus ZP-R804
Puccinia sp. 26 on Rumex acetosa ZP-R230
Puccinia albescens on Adoxa moschatellina MF002126
Puccinia sp. 29 on Filipendula almata ZP-R565
Puccinia vaginatae on Saussurea alpina EF635902
Puccinia caricina var. ribis-ferrugineae on Carex ferruginea DQ917694
Puccinia firma on Carex firma DQ917696
Uromyces bidenticola on Bidens pilosa ZP-R288
Puccinia sp. 27 on Viola japonica var. stenopetala ZP-R571
Puccinia melampodii on Parthenium hysterophorus EU659697
Puccinia ribesii-diversicoloris on Carex flacca DQ917695
Puccinia sp. 35 on Aristolochia debilis ZP-R1380
Puccinia obscura on Luzula sylvatica FJ655874+FJ669234
Puccinia senecionis on Senecio cacaliaster s.sp. hercynicus x ovatus DQ917699
Uromyces junci on Pulicaria dysenterica AF426203
Puccinia tokyensis on Cryptotaenia japonica ZP-R339
Puccinia sp. 29 on Zanthoxylum bungeanum ZP-R394
Puccinia canaliculata on Cyperus rotundus HQ412647
Puccinia sp. 25 on Rostellularia humilis ZP-R382
Puccinia sp. 25 on Morus rubra ZP-R242
Puccinia lagenophorae on Emilia sonchifolia KT199388+KF690677+KF690696
Puccinia xanthii on Xanthium strumarium EU659695
Puccinia sp. 34 on Cotinus coggygria ZP-R667
Dietelia portoricensis on Mikania micrantha AY125389
Puccinia pelargonii-zonalis on Pelargonium sp. AY123316
Puccinia bistortae on Polygonum bistorta DQ917697
Puccinia stylidii on Stylidium armeria KT199389+KJ622216+KJ622215
Puccinia virgaureae on Solidago virgaurea DQ917709
Uromyces plumbarius on Gaura lindheimeri KP313731
Puccinia tokyensis on Cryptotaenia japonica ZP-R406
Puccinia oxyriae on Oxyria sinensis ZP-R1363
Uromyces commelinae on Commelina communis KF982855
Uromyces caricis on Prosopsis pubescens NYS-F-653
Diorchidium woodii on Millettia grandis KM217370+KM217352
Uromyces bidenticola on Bidens pilosa ZP-R1366
Puccinia sp. 34 on Epilobium royleanum ZP-R657
Puccinia caricis-montanae on Carex alba DQ917686
Puccinia miscanthi on Plantago depressa ZP-R122
Puccinia virgaureae on Solidago virgaurea ZP-R281
Puccinia latimamma on Fallopia multiflora ZP-R1398
Puccinia gilgiana on Lechenaultia linarioides KF690673+KF690690
Puccinia senecionis-acutiformis on Senecio ovatus DQ917690
Puccinia silvatica on Taraxacum agg AY222048
Puccinia sp. 33 on host unknown ZP-R1345
Puccinia impatientis on Adoxa moschatellina DQ917700
Uromyces sp. 1 on Gaura parviflora ZP-R6
Puccinia spegazzinii on Mikania micrantha EU851150
Puccinia sp. 31 on Rumex acetosa ZP-R119
Puccinia cyperi on Cyperus iria ZP-R452
Puccinia tatarinovii on Prenanthes tatarinowii KU950447
Puccinia tokyensis on Cryptotaenia japonica ZP-R447
Puccinia linosyridis-caricis on Carex humilis DQ917685
Puccinia carucus on Carex sp. ZP-R1034
Uromyces ficariae on Ranunculus ficaria AF426204
Puccinia sp. 30 on Clematis florida ZP-R1364
Puccinia dampierae on Dampiera sp. KF690672+KF690689
Puccinia tokyensis on Cryptotaenia japonica ZP-R1372
0.75/88
-/73
0.95/89
-/55
1/99
0.90/93 1/100
0.99/90
1/89
-/54
0.77/72
0.90/72
0.74/54
1/95
1/98
1/99
0.99/94
0.90/83
0.70/81 0.93/92
0.71/76
Pucciniaceae sensu stricto
Fig. S1 (cont.)
Pucciniaceae s.str.
Supplementary material
Puccinia sp. 40 on Carpinus turczaninowii ZP-R367
Puccinia funkiae on Hosta albomarginata (T) NYBG35134
Puccinia eupatorii-columbiani on Austroeupatorium sp. EU851153
Puccinia ursiniae on Ursinia anthemoides KT199390+KF690684+KF690705
Uromyces appendiculatus on Phaseolus vulgaris ZP-R458
Uromyces dolicholi on Rhynchosia senna var. texana HQ317563
Uromyces coloradensis on Vicia sp. HQ317564
Puccinia iridis on Iris sp. ZP-R482
Puccinia infra-aequatorialis on Cirsium japonicum ZP-R802
Puccinia sp. 38 on Cicer sp. ZP-R456
Puccinia similis on Artemisia carvifolia ZP-R705
Puccinia infra-aequatorialis on Cirsium japonicum HMAS52872
Miyagia pseudosphaeria on Sonchus oleraceus AY125411+DQ354517
Puccinia urticae-acutiformis on Cymbopogon citratus ZP-R558
Uromyces viciae-fabae on Vicia sp. ZP-R2065
Puccinia calcitrapae var. bardanae on Arctium tomentosum KP240635+KP240633
Puccinia hieracii on Taraxacum mongolicum ZP-R501
Puccinia sp. 46 on Sanguisorba officinalis ZP-R650
Puccinia punctiformis on Cirsium japonicum ZP-R103
Puccinia nishidana on Saussurea setidens HM022141
Puccinia elaeagni on Elaeagnus pungens ZP-R407
Uromyces hedysari-obscuri on Hedysarum boreale var. mackenziei HQ317573
Puccinia polygoni-amphibii on Persicaria sp. ZP-R716
Puccinia convolvuli on Calystegia sepium ZP-R410
Puccinia lapsanae on Lapsana sp. HQ412649
Uromyces trifolii on Trifolium repens GU936634
Uromyces ciceris-arietini on Cicer arietinum GU058030
Puccinia crupinae on Crupina vulgaris HQ184334
Uromyces lupini on Lupinus arcticus HQ317570
Puccinia sp. 41 on Ziziphus oenoplia ZP-R892
Puccinia sp. 44 on Paederia sp. ZP-R1393
Puccinia sp. 41 on Ziziphus oenoplia ZP-R889
Puccinia iridis on Iris tectorum ZP-R221
Puccinia sp. 40 on Cremastra appendiculata ZP-R1353
Puccinia similis on Artemisia cana GU168943
Puccinia patriniae on Indigofera tinctoria ZP-R874
Puccinia sp. 43 on Artemisia sp. ZP-R236
Puccinia punctiformis on Cirsium arvense DQ917706
Uromyces caricis-sempervirentis on Carex sempervirens DQ917714
Puccinia convolvuli on Calystegia sepium ZP-R1312
Puccinia patriniae on Patrinia scabiosaefolia ZP-R404
Uromyces vignae on Phaseolus vulgaris AB115726+AB115634
Puccinia jaceae on Centaurea macrocephala KX468973+KX468974
Puccinia sp. 39 on Pseudostellaria davidii ZP-R280
Puccinia iridis on Iris lactea ZP-R1402
Puccinia gigantea on Epilobium angustifolium AF426198
Puccinia convolvuli on Calystegia sepium DQ354511+AB125954+GU058018
Puccinia convolvuli on Calystegia sepium ZP-R429
Puccinia sp. 38 on Ranunculus japonicus ZP-R416
Uromyces viciae-fabae on Vicia faba KJ746821+KJ716343
Puccinia lapsanae on Lapsana humilis ZP-R105
Puccinia similis on Artemisia sp. ZP-R1420
Uromyces sp. on Euphorbia hirta KU133293
Puccinia elaeagni on Elaeagnus pungens ZP-R297
Puccinia polygoni-amphibii on Persicaria amphibia DQ917702
Puccinia hieracii on Taraxacum sp. HQ317515
Uromyces laburni on Caragana sinica ZP-R120
Uromyces appendiculatus on Phaseolus vulgaris ZP-R446
Uromyces appendiculatus on Phaseolus vulgaris HMAS80583
Puccinia convolvuli on Calystegia sepium ZP-R1388
Puccinia sp. 42 on Artemisia sacrorum ZP-R859
Puccinia sp. 45 on Campsis grandiflora ZP-R308
Puccinia vernoniae-mollis on Vernonia sp. EU851151
Puccinia cardui-pycnocephali on Carduus nutans ZP-R207
Puccinia urticae-acutiformis on Carex acutiformis AF426202
Chrysocelis lupini on Lupinus sp. KJ162157
Puccinia sp. 42 on Artemisia sacrorum ZP-R896
Puccinia cardui-pycnocephali on Carduus pycnocephali AY125410
Puccinia sp. 44 on Paederia sp. ZP-R473
Puccinia sp. 40 on Carpinus turczaninowii ZP-R369
Puccinia sp. 44 on Paederia sp. ZP-R106
Puccinia iridis on Belamcanda chinensis KX611089+KM249853
Uromyces appendiculatus on Phaseolus vulgaris ZP-R466
Puccinia sp. 39 on Bletilla striata ZP-R668
Puccinia punctiformis on Ulmus lamellosa ZP-R219
Puccinia menthae on Mentha spicata KJ746825+DQ354513
Puccinia jaceae on Centaurea cyanus ZP-R10
Puccinia patriniae on Belamcanda chinensis ZP-R1334
Puccinia bardanae on Arctium lappa DQ917703
Puccinia balsamorrhizae on Hemerocallis sp. DQ354518+JN204182
Uromyces phaseoli on Pisum sp. HQ317516
Puccinia sp. 38 onHemerocallis citrina ZP-R298
Puccinia patriniae on Arundinella anomala ZP-R852
Puccinia sp. 38 on Miscanthus sinensis ZP-R311
Puccinia caricis-stipatae on Carex stipata AB188134+AB190888
Puccinia patriniae on Patrinia scabiosaefolia ZP-R621
Puccinia chardoniensis on Baccharis trinervis EU851149
Puccinia convolvuli on Calystegia sepium ZP-R352
Uromyces appendiculatus var. crassitunicatus on Macroptilium atropurpureum KU296911
Puccinia sp. 45 on Ficus microcarpa ZP-R1360
Puccinia sp. 43 on Nandina domestica ZP-R235
Puccinia urticae-acutiformis on Carex sp. ZP-R529
Puccinia impedita on Salvia sp. EU851152
0.70/60
0.96/92
0.99/68
1/86
1/94
1/96
0.77/53
1/99
1/100
0.90/89
0.76/66
0.98/95
1/94
-/51
-/89
0.95/57
1/56
0.92/75
0.74/81
-/70
1/90
0.84/68
0.92/69
Pucciniaceae s. str.
Fig. S1 (cont.)
Pucciniaceae s.str.
Supplementary material
Genera Taxa References
Achrotelium 1 McTaggart et al. (2016).
Aecidium 2 –*
Allodus 1 Aime (2006), Minnis et al. (2012).
Anthomyces 1 –
Atelocauda 1 Wingfield et al. (2004).
Batistopsora 2 Aime (2006), Beenken (2014).
Blastospora 1 Aime (2006).
Caeoma 2 Wingfield et al. (2004), Crane et al. (2005).
Ceratocoma 1 McTaggart et al. (2016).
Cerotelium 1 Maier et al. (2015).
Chardoniella 1 Zuluaga et al. (2011).
Chrysocelis 2 Zuluaga et al. (2011).
Chrysocyclus 1 Zuluaga et al. (2011).
Chrysomyxa 16 Aime (2006), Feau et al. (2011), Padamsee & McKenzie (2014), Cao et al. (2017b).
Coleosporium 10 Sjamsuridzal et al. (1999), Wingfield et al. (2004), Su et al. (2012), Yang et al. (2014).
Cronartium 3 Vogler & Bruns (1998), Aime (2006), Liu et al. (2015).
Cumminsiella 1 Maier et al. (2003), Aime (2006).
Cystopsora 1 McTaggart et al. (2016).
Dasturella 1 Wingfield et al. (2004).
Dasyspora 11 Beenken et al. (2012).
Desmella 1 McTaggart et al. (2014).
Diaphanopellis 1 Cao et al. (2017b).
Dietelia 2 Wingfield et al. (2004), Aime (2006).
Diorchidium 2 Beenken et al. (2012), Beenken & Wood (2015).
Edythea 1 –
Endocronartium 1 Vogler & Bruns (1998).
Endophyllum 5 Wood & Crous (2005), Maier et al. (2007).
Endoraecium 6 McTaggart et al. (2015).
Gerwasia 1 Wingfield et al. (2004), McTaggart et al. (2014).
Gymnoconia 1 Wingfield et al. (2004), Yun et al. (2011), AFTOL-ID 1630.
Gymnosporangium 21 Novick (2008), Zhao et al. (2016).
Hamaspora 1 McTaggart et al. (2015).
Hemileia 4 Wingfield et al. (2004), Aime (2006), McTaggart et al. (2015).
Hyalopsora 2 Sjamsuridzal et al. (1999), Maier et al. (2003), Wingfield et al. (2004), Padamsee & McKenzie (2014).
Kernkampella 1 McTaggart et al. (2015).
Kuehneola 1 Shands et al. (2018), AFTOL-ID 987.
Kweilingia 1 Blomquist et al. (2009).
Leucotelium 2 –
Macruropyxis 3 Beenken & Wood (2015), Martin et al. (2017).
Maravalia 2 Zuluaga et al. (2011), McTaggart et al. (2016).
Masseella 1 Liberato et al. (2014).
Melampsora 31 Tian et al. (2004), Vialle et al. (2013), Zhao et al. (2015), Zhao et al. (2017).
Melampsorella 1 Maier et al. (2003), Wingfield et al. (2004).
Melampsoridium 2 Maier et al. (2003), Wingfield et al. (2004), McKenzie et al. (2013).
Mikronegeria 2 Aime (2006), Padamsee & McKenzie (2014).
Milesina 1 Wingfield et al. (2004), McTaggart et al. (2014).
Miyagia 1 Wingfield et al. (2004), Aime (2006).
Naohidemyces 1 Aime (2006), Padamsee & McKenzie (2014).
Nyssopsora 3 Wingfield et al. (2004), Swann & Taylor (1995).
Ochropsora 2 Sjamsuridzal et al. (1999).
Olivea 1 Aime (2006).
Phakopsora 13 Aime (2006), Chatasiri & Ono (2008), Zuluaga et al. (2011), Maier et al. (2015), Pota et al. (2015).
Phragmidium 10 Wingfield et al. (2004), Deadman et al. (2011), McTaggart et al. (2016), Ali et al. (2017).
Physopella 2 Sjamsuridzal et al. (1999), Wingfield et al. (2004).
Pileolaria 3 Wingfield et al. (2004), Aime (2006), AFTOL-ID 988.
Porotenus 1 Matheny et al. (2006), Beenken et al. (2012).
Prospodium 3 Pegg et al. (2013), AFTOL-ID 1401.
Puccinia 241 Kropp et al. (1997), Raguso & Roy (1998), Maier et al. (2003), Wingfield et al. (2004), Engkhaninun et al. (2005), Aime (2006),
Szabo (2006), Maier et al. (2007), Langrella et al. (2008), Zale et al. (2008), Alaei et al. (2009), Pedley (2009), Seier et al.
(2009), Dixon et al. (2010), Jin et al. (2010), Sampangi et al. (2010), Deadman et al. (2011), Scholler et al. (2011), Zuluaga
et al. (2011), Bruckart et al. (2012), Liu & Hambleton (2012), Padamsee & McKenzie (2012), Liu & Hambleton (2013), Liu et
al. (2013), Blomquist et al. (2014), Tan et al. (2014), Padamsee & McKenzie (2014), Demers et al. (2015), Liu et al. (2015),
Mulvey & Hambleton (2015), Kabaktepe et al. (2016), Mahadevakumar et al. (2016), McTaggart et al. (2016), Demers et al.
(2017), Shen & Huang (2017), AFTOL-ID 1629.
Pucciniastrum 8 Wingfield et al. (2004), Liang et al. (2006), Padamsee & McKenzie (2014).
Pucciniosira 3 Aime (2006), Zuluaga et al. (2011).
Puccorchidium 1 Beenken & Wood (2015).
Racospermyces 1 Wingfield et al. (2004), Scholler & Aime (2006), Liu et al. (2015).
Ravenelia 5 Aime (2006).
Roestelia 3 Novick (2008).
Sphaerophragmium 1 McTaggart et al. (2015).
Sphenorchidium 1 Beenken & Wood (2015).
Sphenospora 3 Aime (2006), Beenken & Wood (2015).
Thekopsora 4 McTaggart et al. (2016), Yang et al. (2014), Yang et al. (2015).
Trachyspora 1 Maier et al. (2003), Aime (2006).
Tranzschelia 5 Deadman et al. (2007), Blomquist et al. (2015).
Triphragmium 1 Maier et al. (2003), Wingfield et al. (2004), Yun et al. (2011).
Uredinopsis 2 Sjamsuridzal et al. (1999), Wingfield et al. (2004), McTaggart et al. (2014).
Uredo 4 Hernandez et al. (2005), McTaggart et al. (2016).
Uromyces 57 Pfunder et al. (2001), Maier et al. (2003), Anikster et al. (2004), Wingfield et al. (2004), Aime (2006), Dixon et al. (2010), Yun
et al. (2010), Zuluaga et al. (2011), Liu et al. (2015), Souza et al. (2015), McTaggart et al. (2016), AFTOL-ID 976.
Uromycladium 4 McTaggart et al. (2015).
75 542
* Sequence data originated from unpublished projects.
Table S1 rDNA sequence data from selected genera in the Pucciniales used for phylogenetic studies.
Supplementary material
Gymnosporangium amelanchieris 20141009 Amelanchier ovalis 0,I – KP261040 KP261041 Fernández & Alvarado (2016)
20140331-1 Juniperus oxycedrus III – KM486541 KM486546 Fernández & Alvarado (2016)
G. asiaticum HMAS135599 Cupressus duclouxia III MN604940 MN605664 MN605742 This study
CUP-0016 Juniperus chinensis III MN642598 MN642593 MN642617 This study
HMAS11935 Juniperus chinensis III MN604941 MN605665 MN605743 This study
HMAS165302 Juniperus chinensis III MN604942 MN605666 MN605744 This study
HMAS172366 Juniperus chinensis III MN604943 KU288703 KU342779 This study
HMAS2503 Juniperus chinensis III MN604944 MN605667 MN605745 This study
HMAS47228 Juniperus chinensis III MN604945 KU342736 KU342774 This study
HMAS47229 Juniperus chinensis III MN604946 KU288643 KU342776 This study
HMAS47728 Juniperus chinensis III MN604947 MN605668 MN605746 This study
HMAS165301 Juniperus chinensis III MN604973 KU288658 KU342771 This study
HMAS37835 Juniperus tibetica III MN604974 – – This study
IBA5704 Juniperus chinensis III KJ720161b Novick (2008)
F0027941 Juniperus chinensis III KP308392b Shen et al. (2018)
BJFC-R01834 Juniperus chinensis III – KR814568 KT719165 Cao et al. (2016)
BJFC-R01835 Juniperus chinensis III – KR814569 KT719166 Cao et al. (2016)
TNM F0029761 Juniperus chinensis III KX355281b Shen et al. (2018)
TNM F0029762 Juniperus chinensis III KX355282b Shen et al. (2018)
TNM F0029763 Juniperus chinensis III KX355284b Shen et al. (2018)
TNM F0029764 Juniperus chinensis III KX355285b Shen et al. (2018)
TNM F0029765 Juniperus chinensis III KX355286b Shen et al. (2018)
TNM F0030602 Juniperus chinensis III KY964736b Shen et al. (2018)
TNM F0030603 Juniperus chinensis III KY964737b Shen et al. (2018)
TNM F0030601 Juniperus chinensis III KY964753b Shen et al. (2018)
NTU F100002 Juniperus chinensis III KY964754 b Shen et al. (2018)
HKRFI 2073 Juniperus chinensis III – – EF990780 Yun et al. (2009)
HKFRI 1974 Juniperus chinensis cv. kaizuka III – – FJ848741 Yun et al. (2009)
HKFRI 1977 Juniperus chinensis cv. kaizuka III – – FJ848744 Yun et al. (2009)
HKFRI 2074 Juniperus chinensis cv. kaizuka III – – FJ848750 Yun et al. (2009)
HKFRI 1971 Juniperus chinensis var. globosa III – – FJ848767 Yun et al. (2009)
HKFRI 1972 Juniperus chinensis var. globosa III – – FJ848768 Yun et al. (2009)
HKFRI 1976 Juniperus chinensis cv. kaizuka III – – FJ848743 Yun et al. (2009)
HKFRI 1978 Juniperus chinensis cv. kaizuka III – – FJ848745 Yun et al. (2009)
HKFRI 1979 Juniperus chinensis cv. kaizuka III – – FJ848746 Yun et al. (2009)
HKFRI 1980 Juniperus chinensis cv. kaizuka III – – FJ848747 Yun et al. (2009)
HKFRI 1975 Juniperus chinensis var. sargentii III – – FJ848742 Yun et al. (2009)
HKFRI 1973 Juniperus chinensis var. sargentii III – – FJ848769 Yun et al. (2009)
HMAS45640 Juniperus excelsa III MN604948 MN605669 MN605747 This study
CUP-57311 Malus ioensis var. plena 0,I MN604949 MN605670 MN605748 This study
HMAS172325 Malus asiatica 0,I MN604950 MN605671 MN605749 This study
HMAS11217 Malus domestica 0,I MN604951 MN605672 MN605750 This study
HMAS135289 Malus domestica 0,I MN604952 KU288657 KU342773 This study
HMA14328 Malus pumila 0,I MN604953 KU288661 KU342772 This study
HMAS135598 Malus pumila 0,I – MN605673 MN605751 This study
HMAS14327 Malus pumila 0,I – KU288671 KU342775 This study
HMAS17719 Malus pumila 0,I MN604954 MN605674 MN605752 This study
HMAS26426 Malus pumila 0,I MN604955 MN605675 MN605753 This study
HMAS56909 Malus pumila 0,I MN604956 MN605676 MN605754 This study
ZP-R1375 Malus pumila 0,I MK488389 MK518977 MK518675 This study
Table S2 List of species, specimens and GenBank accession numbers of sequences used for phylogenetic studies at species level.
Species Specimen No.a Host Spore stage GenBank Accession No.c References
SSU ITS LSU
Supplementary material
G. asiaticum (cont.) ZP-R1376 Malus pumila 0,I MN604957 MK518987 MK518686 This study
ZP-R1412 Malus pumila 0,I MN604958 MN605677 MN605755 This study
ZP-R201 Malus pumila 0,I MN604959 MK518959 MK518654 This study
ZP-R203 Malus pumila 0,I MK488432 MK518960 MK518655 This study
ZP-R204 Malus pumila 0,I MK488480 MK519005 MK518708 This study
ZP-R205 Malus pumila 0,I – MK518866 MK518740 This study
ZP-R215 Malus pumila 0,I MK488223 MK518867 MK518531 This study
ZP-R228 Malus pumila 0,I MN604961 MN605678 MN605756 This study
ZP-R301 Malus pumila 0,I MN604962 MN605679 MN605757 This study
ZP-R324 Malus pumila 0,I MN604963 – MK518712 This study
ZP-R336 Malus pumila 0,I MK488175 MN605680 MN605758 This study
ZP-R422 Malus pumila 0,I MK488176 MK518845 MK518501 This study
ZP-R614 Malus pumila 0,I MK488124 MK518825 MK518469 This study
ZP-R617 Malus pumila 0,I MK488162 – – This study
ZP-R773 Malus pumila 0,I MN604964 MN605681 MN605759 This study
ZP-R774 Malus pumila 0,I MN604965 – – This study
ZP-R778 Malus pumila 0,I MN604966 MN605682 MN605760 This study
ZP-R779 Malus pumila 0,I MN604967 MN605683 MN605761 This study
ZP-R783 Malus pumila 0,I MK488171 – – This study
ZP-R876 Malus pumila 0,I MN604968 MN605684 MN605762 This study
ZP-R960 Malus pumila 0,I MK488181 MK518849 MK518506 This study
ZP-R961 Malus pumila 0,I MN604969 MN605685 MN605763 This study
ZP-R6021 Malus pumila 0,I MK488289 MK518911 – This study
HMAS38650 Malus pumila 0,I MN604970 MN605686 MN605764 This study
HMAS11219 Malus spectabilis 0,I MN604971 MN605687 MN605765 This study
HMAS12970 Malus spectabilis 0,I – MN605688 MN605766 This study
HMAS55351 Malus spectabilis 0,I MN604972 MN605689 MN605767 This study
CUP-20544 Malus sp. 0,I MK488173 MK519048 MK518500 This study
CUP-17524 Malus sp. 0,I – MN605690 MN605768 This study
HMAS24616 Malus sp. 0,I – KU288672 KU342766 This study
NYBG60678 Malus sp. 0,I MK488214 MK518863 MK518527 This study
NTU F100003 Pyrus lindleyi 0,I MF377396a Shen et al. (2018)
TNM F0027942 Pyrus pyrifolia 0,I KP308393a Shen et al. (2018)
TNM F0027943 Pyrus pyrifolia 0,I KP308394a Shen et al. (2018)
G. clavariiforme LD 1019 Crataegus orientalis 0,I HM114220b Dervis et al. (2010)
CUP-2146 Juniperus communis III – KU288679 KU342767 This study
HMAS67951 Juniperus communis III MN604975 KU288644 KU342765 This study
HMAS24626 Malus communis 0,I MN604976 KU288672 KU342766 This study
G. clavipes NYBG461394 Crataegus sp. 0,I MN604977 MN605691 MN605769 This study
CPO 18.01 Crataegus sp. 0,I – – KM382067 Dervis et al. (2010)
NYS-F-775 Juniperus virginiana III MK488179 MK518847 MK518583 This study
CUP-18207 Juniperus virginiana III MN604978 MN605692 MN605770 This study
RN140 Juniperus virginiana III KJ720155b Novick (2008)
BPI 871102 Malus domestica 0,I DQ354546 – – Aime et al. (2018)
CUP-13530 Malus sp. 0,I MN604979 – – This study
GCU41566 unknown 0,I U41566 – – Swann & Taylor (1995)
ECS159 unknown 0,I AY123309 – – Wingfield et al. (2004)
G. confusum 20140808B-H22 Crataegus mongyna 0,I – KP261042 KP261043 Fernández & Alvarado (2016)
20180506-M1 Crataegus mongyna 0,I MH595612b Shen et al. (2018)
Table S2 ( cont.)
Species Specimen No.a Host Spore stage GenBank Accession No.c References
SSU ITS LSU
Supplementary material
G. confusum (cont.) 20180513-M6 Crataegus mongyna 0,I MH595613b Shen et al. (2018)
20180520-M7 Crataegus mongyna 0,I MH595614b Shen et al. (2018)
20180526-M11 Crataegus mongyna 0,I MH595615b Shen et al. (2018)
20140330-2 Juniperus oxycedrus III – KP261046 KP261047 Fernández & Alvarado (2016)
20150227-M14 Juniperus phoenicea subsp. turbinata III – KT160257 KT16026 Fernández & Alvarado (2016)
G. corniculans CUP-3087 Amelanchier canadensis 0,I MN604980 MN605693 MN605771 This study
BPI 738115 Amelanchier sp. 0,I KJ720167b Novick (2008)
CUP-19705 Malus domestica 0,I MN604981 MN605694 MN605772 This study
RSP 98-140 Juniperus virginiana III KJ720174b Novick (2008)
G. corniforme TNM F0028736 Juniperus formosana III KY964741b Shen et al. (2018)
TNM F0028738 Juniperus formosana III KY964743b Shen et al. (2018)
TNM F0030469 Sorbus randaiensis III KY964751b Shen et al. (2018)
TNM F0029302 Sorbus randaiensis III KY964747b Shen et al. (2018)
G. cornutum PPR0020M2 Juniperus communis III – MG573153 MG573214 Prats & Alvarado (unpubl.)
HKFRI 2105 Juniperus rigida III – – FJ848766 Yun et al. (2009)
HMAS12940 Malus spectubilis 0,I – KU288667 KU342735 This study
BPI 910184 Sorbus americana 0,I KY764066b Demers et al. (unpubl.)
PPR1299CM1 Sorbus aucuparia 0,I – – MG573215 Fernández & Alvarado (unpubl.)
WM 1093 Sorbus aucuparia 0,I – – AF426210 Maier et al. (2003)
PPR1307CM2 Sorbus aucuparia 0,I – MG573154 MG573213 Prats & Alvarado (unpubl.)
20170926-H1 Sorbus aucuparia 0,I – – MG561881 Prats P. Alvarado P (unpubl.)
G. ellisii RN23 Chamaecyparis thyoides III KJ720156b Novick (2008)
G. exiguum RSP 04-86 Gillenia trifoliata 0,I KJ720170b Novick (2008)
G. fenzelianum HMAS33357 Malus kansuensis 0,I – MN605695 MN605773 This study
HMAS38649 Malus kansuensis 0,I – KU288690 KU342752 This study
ZP-R14 Malus kansuensis 0,I – MN605696 MN605774 This study
ZP-R3 Malus kansuensis 0,I – MN605697 MN605775 This study
G. fraternum RSP80-14 Chamaecyparis thyoides III KJ720171b Novick (2008)
G. gaeumannii BPI118807 Cupressus arizonica III KJ720173b Novick (2008)
RSP99-98 Juniperus communis III KJ720169b Novick (2008)
G. globosum ENCB121368 Crataegus mexicana 0,I – – KX137840 Alvarado-Rosales et al. (2015)
ENCB121369 Crataegus mexicana 0,I – – KX137841 Alvarado-Rosales et al. (2015)
NYBG237085 Juniperus virginiana III MN604982 KU288654 KU342713 This study
CUP-1553 Malus sp. 0,I MN604983 MN605698 MN605776 This study
G. gracile 20160606-M2 Amelanchier ovalis 0,I KY440115b Fernández & Alvarado (unpubl.)
20160519 Crataegus monogyna 0,I KY440114b Fernández & Alvarado (unpubl.)
20140529-1a Cydonia oblonga 0,I – KM486543 KM486545 Fernández & Alvarado (2016)
20150417-M1 Juniperus communis III KT160260b Fernández & Alvarado (2016)
20140330-2 Juniperus communis III – – KP261047 Fernández & Alvarado (2016)
20120515 Juniperus communis III – KP261048 KP261049 Fernández & Alvarado (unpubl.)
HML 841 Juniperus communis III – – AF426211 Maier et al. (2003)
20140326-1 Juniperus oxycedrus III – KM486542 KM486544 Fernández & Alvarado (unpubl.)
20150321-1-M1 Juniperus oxycedrus III – KU183500 – Fernández & Alvarado (2016)
G. huanglongense BJFC R01984 Juniperus przewalskii III – NR154077 KT719161 Cao et al. (2017a)
BJFC R01985 Juniperus przewalskii III – KT719168 KT719162 Cao et al. (2017a)
Table S2 ( cont.)
Species Specimen No.a Host Spore stage GenBank Accession No.c References
SSU ITS LSU
Supplementary material
G. japonicum 1 HMAS79186 Juniperus chinensis III – KU288669 KU342722 This study
HKFRI 1987 Juniperus chinensis III – – FJ848751 Yun et al. (2009)
HKFRI 1988 Juniperus chinensis III – – FJ848752 Yun et al. (2009)
HKFRI 1992 Juniperus chinensis III – – FJ848755 Yun et al. (2009)
HKFRI 1993 Juniperus chinensis var. horizontalis III – – FJ848756 Yun et al. (2009)
HMAS14315 Juniperus sp. III – KU288641 KU342745 This study
20170926-H1 Sorbus aucuparia 0,I – – MG572221 Fernández & Alvarado (unpubl.)
G. japonicum 2 HKFRI 1997 Juniperus chinensis var. globosa III – – FJ848759 Yun et al. (2009)
HKFRI 1995 Juniperus chinensis var. horizontalis III – – FJ848758 Yun et al. (2009)
HKFRI 1994 Juniperus chinensis var. sargentii III – – FJ848757 Yun et al. (2009)
G. juniperi-virginianae NYBG461220 Juniperus virginiana III MN604984 KU288652 KU342743 This study
NYBG1391099 Juniperus virginiana III MN604985 KU288647 KU342712 This study
NYBG237070 Juniperus virginiana III MN604986 KU288656 KU342718 This study
NYBG237046 Juniperus virginiana III MN604987 KU288655 KU342719 This study
NYBG23036 Juniperus virginiana III MN604988 KU288637 KU342710 This study
HMAS43709 Juniperus virginiana III MN604989 – – This study
RSP98-137 Juniperus virginiana III KJ720176a Novick (2008)
MCA3585 Juniperus virginiana III – MG917687 MG907217 Fernández & Alvarado (unpubl.)
PBM2530 Juniperus virginiana III – DQ267127 AY629316 Matheny & Hibbett (unpubl.)
DAOM 234434 Juniperus virginiana III – HQ317510 – Liu et al. (2015)
HMAS2218 Juniperus scopulorum III – – KU342767 This study
HMAS6725 Juniperus sp. III – – KU342736 This study
TDB1345 Juniperus sp. III – AY123289 AF522167 Wingfield et al. (2004)
CUP-24472 Malus angustifolia 0,I MN604990 MN605699 MN605777 This study
HMAS74424 Malus baccata 0,I MN642602 MN642597 MN642621 This study
CUP-24468 Malus coronaria 0,I MN604991 MN605700 MN605778 This study
CUP-55712 Malus coronaria 0,I MN604992 MN605701 MN605779 This study
CUP-45235 Malus coronaria 0,I MN604993 MN605702 MN605780 This study
CUP-24473 Malus coronaria 0,I MN604994 MN605703 MN605781 This study
CUP-20257 Malus domestica 0,I MN604995 KU288678 KU342716 This study
CUP-17321 Malus domestica 0,I MN604996 MN605704 MN605782 This study
CUP-1551 Malus domestica 0,I MN604997 MN605705 MN605783 This study
TNM F0029763 Malus domestica 0,I KY964761b Shen et al. (2018)
CUP-20153 Malus domestica 0,I MN604999 MN605707 MN605785 This study
CUP-51030 Malus domestica 0,I MN605000 MN605708 MN605786 This study
CUP-731 Malus domestica 0,I MN605001 MN605709 MN605787 This study
CUP-21697 Malus domestica 0,I MN605002 MN605710 MN605788 This study
CUP-20161 Malus domestica 0,I MN605003 – – This study
CUP-20164 Malus domestica 0,I MN605004 MN605711 MN605789 This study
CUP-19919 Malus domestica 0,I – MN605712 MN605790 This study
CUP-882 Malus domestica 0,I MN605005 MN605713 MN605791 This study
CUP-20157 Malus domestica 0,I – MN605714 MN605792 This study
CUP-14 Malus domestica 0,I MN642601 MN642596 MN642620 This study
CUP-20165 Malus domestica 0,I MN605006 KU288677 KU342708 This study
CUP-24469 Malus domestica 0,I MN605007 – – This study
CUP-594 Malus glaucescens 0,I MN604998 MN605706 MN605784 This study
CUP-595 Malus ioensis 0,I – KU288676 KU342709 This study
CUP-20162 Malus sp. 0,I MN605008 MN605715 MN605793 This study
Table S2 ( cont.)
Species Specimen No.a Host Spore stage GenBank Accession No.c References
SSU ITS LSU
Supplementary material
G. kanas HMAS248105 Cotoneaster dammeri 0,I MK488124 MK518825 MK518469 This study
ZP-R481 Cotoneaster dammeri 0,I MK488115 MK518821 MK518463 This study
ZP-R614 Cotoneaster dammeri 0,I MK488124 MK518825 MK518469 This study
G. kernianum RSP05-37 Juniperus utahensis III KJ720177b Novick (2008)
G. lachrymiforme HMAS248123 Malus sp. 0,I – MN605716 MN605794 This study
G. libocedri U1469 Amelanchier alnifolia III – MG907206 MG907218 Aime et al. (2018)
HMAS49246 Calocedrus decurrens III MN605009 MN605717 MN605795 This study
HMAS45643 Calocedrus decurrens III MN605010 MN605718 MN605796 This study
TDB1519 Calocedrus decurrens III AY123290 AF522168 – Wingfield et al. (2004)
G. miyabei IBA 6650 Chamaecyparis pisifera III KJ720178b Novick (2008)
DAOM186133 Juniperus communis III KJ720185 b Novick (2008)
CUP-56165 Malus sylvestris 0,I – KU288675 KU342748 This study
G. monticola HKFRI 1983 Juniperus rigida III – – FJ848770 Yun et al. (2009)
RN152 Juniperus rigida III KJ720168a Novick (2008)
HKFRI 1985 Juniperus rigida III – – FJ848771 Yun et al. (2009)
HMAS44394 Malus pumila 0,I – KU288683 KU342754 This study
HMAS44514 Malus pumila 0,I – KU288696 KU342753 This study
G. multiporum RSP05-41 Juniperus monosperma III KJ720179b Novick (2008)
G. nelsonii CUP-55918 Crataegus brunetiana 0,I MN642600 MN642595 MN642619 This study
DAOM226326 Juniperus horizontalis III KJ720166b Novick (2008)
RSP01-237 Juniperus horizontalis III KJ720163b Novick (2008)
RSP 99-93 Juniperus horizontalis III KJ720180b Novick (2008)
NYBG193254 Juniperus horizontalis III MN605011 KU288663 KU342740 This study
NYBG193243 Juniperus horizontalis III MN605012 KU288653 KU342739 This study
NYBG199427 Juniperus horizontalis III MN605013 – – This study
NYBG638372 Juniperus scopulorum III MN642599 MN642594 MN642618 This study
BPI 880709 Amelanchier alnifolia 0,I – – HM591299 Schilder et al. (2011)
ZP-R83 Malus sp. 0,I MK488097 MK518808 MK518447 This study
G. nidus-avis CUP-227 Amelanchier sp. 0,I MN605014 MN605719 MN605797 This study
NYBG461234 Juniperus juvenescens III MN605015 KU288701 KU342758 This study
NYBG237071 Juniperus virginiana III MN605016 KU288688 KU342762 This study
HMAS14429 Juniperus virginiana III MN605017 MN605720 MN605798 This study
NYBG237094 Juniperus virginiana III MN605018 KU288686 KU342755 This study
NYBG237080 Juniperus virginiana III MN605019 KU288700 KU342757 This study
NYBG14419 Juniperus virginiana III MN605020 KU288681 KU342756 This study
RSP 05-29 Juniperus virginiana III KJ720181b Novick (2008)
NYBG461235 Malus communis 0,I MN605021 – – This study
G. niitakayamense TNM F0030470 Photinia niitakayamensis 0,I KY964759 b Shen et al. (2018)
TNM F0027944 Photinia niitakayamensis 0,I KP308395 b Shen et al. (2018)
TNM F0030464 Photinia niitakayamensis 0,I KY964758 b Shen et al. (2018)
TNM F0030474 Photinia niitakayamensis 0,I KY964760b Shen et al. (2018)
G. nipponicum HMAS 31297 Sorbus alnifolia 0,I KJ720182b Novick (2008)
G. nootkatense PUR 63656 Juniperus virginiana III KJ720159 b Novick (2008)
Table S2 ( cont.)
Species Specimen No.a Host Spore stage GenBank Accession No.c References
SSU ITS LSU
Supplementary material
G. prezewaskii BJFC R01859 Juniperus koehneana 0,I – NR_154073 KR814560 Cao et al. (2017)
BJFC-R02084 Juniperus koehneana 0,I – KX528447 KX814560 Cao et al. (2017)
BJFC-R02083 Juniperus przewalskii III – KX528446 KX528444 Cao et al. (2017)
BJFC-R01860 Juniperus przewalskii III – KR814564 KR814561 Cao et al. (2017)
G. sabinae DB 1548 Juniperus chinensis III – – AY512845 Begerow et al. (unpubl.)
RN43 Juniperus chinensis III KJ720183b Novick (2008)
20140331-6 Juniperus phoenicea subsp. turbinata III – KM403109 – Fernández & Alvarado (unpubl.)
20140331-7 Juniperus phoenicea subsp. turbinata III – KP261044 – Fernández & Alvarado (unpubl.)
CUP-0477 Juniperus sabina III MN605022 MN605721 MN605799 This study
20150325-2-M2 Juniperus oxycedrus III – KT160252 – Fernández & Alvarado (2016)
20140330-3 M2 Juniperus oxycedrus III KM403110b Fernández & Alvarado (2016)
BG1 Juniperus sp. III KF925316b Filipp & Spornberger (unpubl.)
BG2 Juniperus sp. III KF925317b Filipp & Spornberger (unpubl.)
BG3 Juniperus sp. III KF925318b Filipp & Spornberger (unpubl.)
BG4 Juniperus sp. III KF925319b Filipp & Spornberger (unpubl.)
BG5 Juniperus sp. III KF925320b Filipp & Spornberger (unpubl.)
BG6 Juniperus sp. III KF925321b Filipp & Spornberger (unpubl.)
TNM F0030476 Pyrus amygdaliformis 0,I KY964763b Shen et al. (2018)
GYMSAB 0004 Pyrus calleryana 0,I – – JN969965 Kenaley et al. (2012)
BPI 893287 Pyrus calleryana 0,I KU593568b Hansen (unpubl.)
GYMSAB 0001 Pyrus communis 0,I – – JN969962 Kenaley et al. (2012)
20140923 H2 Pyrus communis 0,I – KP261039 – Fernández & Alvarado (2016)
GYMSAB 0005 Pyrus communis 0,I – – JN969966 Kenaley et al. (2012)
20141009 Pyrus communis 0,I – KP261040 – Fernández & Alvarado (2016)
LD 1022 Pyrus communis 0,I HM114221b Dervis (unpubl.)
TNM F0030477 Pyrus communis 0,I KY964764b Shen et al. (2018)
GYMSAB 0003 Pyrus communis 0,I – – JN969964 Kenaley et al. (2012)
WM 1347 Pyrus communis 0,I – – AF426209 Maier et al. (2003)
GYMSAB 0002 Pyrus communis 0,I – – JN969963 Kenaley et al. (2012)
G. shennongjiaense ZP-R420 Malus asiatica 0,I MN605023 MK518924 MK518604 This study
ZP-R511 Malus asiatica 0,I MN605024 MN605722 MN605800 This study
HMAS55353 Malus sp. 0,I MN605025 MN605723 MN605801 This study
ZP-R627 Malus sp. 0,I – MN605724 MN605802 This study
G. speciosum RSP99-96 Juniperus virginiana III KJ720160b Novick (2008)
G. spinulosum HMAS26416 Malus spectubilis 0,I MN605030 MN605727 MN605805 This study
G. tiankengense HMAS248124 Malus sp. 0,I MN605026 MN605725 MN605803 This study
ZP-R1375 Malus sp. 0,I MN605027 MN605726 MN605804 This study
G. torminali-juniperini 20170805 Sorbus torminalis 0,I – MG572220 – Fernández & Alvarado (unpubl.)
G. trachysorum NYBG3009468 Juniperus virginiana III MN605031 MN605728 MN605806 This study
BPI 910169 Juniperus virginiana III KY798387b Demers (unpubl.)
RN 91 Juniperus virginiana III KJ720184b Novick (2008)
BPI 910170 Pyrus calleryana 0,I KY798386b Demers (unpubl.)
G. tremelloides NYBG23203 Amelanchier sp. 0,I MN605028 KU288639 KU342768 This study
CPO 18.03 Juniperus deppeana III KM382069 – – Nieto-Lopez (unpubl.)
CUP-43859 Malus communis 0,I MN605029 KU288680 KU342769 This study
G. tsingchenensis HMAS133735 Cupressus funebris III MN605032 – – This study
Table S2 ( cont.)
Species Specimen No.a Host Spore stage GenBank Accession No.c References
SSU ITS LSU
Supplementary material
Table S2 ( cont.)
Species Specimen No.a Host Spore stage GenBank Accession No.c References
SSU ITS LSU
G. vauqueliniae RSP05-87 Vauquelinia angustifolia 0,I KJ720186b Novick (2008)
G. yamadae CUP-776 Aroma atropurpurea 0,I MN605033 MN605729 MN605807 This study
BPI 893269 Crataegus sp. 0,I KY798356b Demers (unpubl.)
NYBG3009549 Juniperus chinensis III MN605034 MN605730 MN605808 This study
HKFRI 2000 Juniperus chinensis III – – FJ559375 Yun et al. (2009)
HKFRI 2001 Juniperus chinensis III KJ720187b Novick (2008)
PPQ5009 Juniperus chinensis III GU058012b Dixon et al. (2010)
BJFC-R01822 Juniperus chinensis III – KR814566 KT719163 Cao et al. (2016)
BJFC-R01823 Juniperus chinensis III – KR814567 KT719164 Cao et al. (2016)
HMAS47229 Juniperus chinensis III MN605035 MN605731 MN605809 This study
HMAS82779 Juniperus chinensis III MN605036 KU288646 KU342730 This study
HKFRI 2002 Juniperus chinensis cv. kaizuka III – – FJ848763 Yun et al. (2009)
HMAS143619 Juniperus sabina III MN605037 KU288649 KU342742 This study
HMAS80528 Malus baccata 0,I MN605038 MN605732 MN605810 This study
HMAS55351 Malus baccata 0,I MN605039 – – This study
LIG_1 Malus micromalus 0,I MN605040 MN605733 MN605811 This study
LIG_2 Malus micromalus 0,I MN605041 KU288660 KU342728 This study
LIG_3 Malus micromalus 0,I MN605042 KU288638 KU342729 This study
LIG_4 Malus micromalus 0,I MN605043 KU288666 KU342725 This study
HMAS243188 Malus micromalus 0,I MN605044 KU288659 KU342726 This study
HMAS55352 Malus micromalus 0,I – KU288695 KU342727 This study
CUP-20612 Malus micromalus 0,I MN605045 MN605734 MN605812 This study
HMAS199333 Malus micromalus 0,I MN605046 KU288674 KU342724 This study
ZP-R16 Malus micromalus 0,I MN605047 – – This study
NYBG2584 Malus miura 0,I MN605048 MN605735 MN605813 This study
HMAS36992 Malus prunifolia 0,I MN605049 KU288662 KU342732 This study
NYBG53757 Malus toringo 0,I MN605050 MN605736 MN605814 This study
ZP-R633 Malus sp. 0,I MN605052 MN605737 MN605815 This study
ZP-R634 Malus sp. 0,I MN605053 MN605738 MN605816 This study
ZP-R635 Malus sp. 0,I MK488462 MK519020 MK518722 This study
ZP-R637 Malus sp. 0,I MK488413 MK518995 MK518699 This study
NYBG53751 Malus spectabilis 0,I MN605051 – – This study
HMAS30992 Malus prunifolia 0,I MN605054 MN605739 MN605817 This study
Gymnosporangium sp. 1 HMAS79065 Juniperus chinensis III – KU288684 KU342721 This study
HMAS135611 Juniperus chinensis III – KU288699 KU342736 This study
DAOM 234634 Juniperus scopulorum III HQ317506 Liu et al. (2015)
R046 Pyrus sp. 0,I KY800408 Demers (unpubl.)
Gymnosporangium sp. 2 LD 1021 Crataegus mongyna 0,I HM114219 Demers (unpubl.)
20140618 Crataegus mongyna 0,I – – KP261045 Fernández & Alvarado (2016)
HMAS52880 Cotoneaster melanopcarpus 0,I MN605055 MN605740 MN605818 This study
DAOM220748 Cotoneaster melanopcarpus 0,I KJ720165b Novick (2008)
LD1015 Juniperus sp. III GU058011b Dixon et al. (2010)
CUP-2613 Malus sp. 0,I MN605056 MK518910 MK518582 This study
Gymnosporangium sp. 3 ZP-R1389 Chamaecyparis sp. III MN605057 MN605741 MN605819 This study
Endoraecium tropicum BRIP56557 Acacia tropica III KJ862417 KJ862392 KJ862337 McTaggart et al. (2015)
a CUP: Plant Pathology Herbarium, Cornell University, Ithaca, New York, USA; HMAS: The Mycological Herbarium of Institute of Microbiology, CAS, China; NYBG: New York Botanical Garden, New York, USA; NYS: New York State Museum, New York, USA, ZP: Personal collection
by Peng Zhao.
b represents the specimens with SSU, ITS and LUS sequence together.
c Sequence data generated from this study were listed in bold format.
Supplementary material
REFERENCES
Alaei H, De Backer M, Nuytinck J, et al. 2009. Phylogenetic relationships of
Puccinia horiana and other rust pathogens of Chrysanthemum × morifo-
lium based on rDNA ITS sequence analysis. Mycological Research 113:
668– 683.
Ali B, Sohail Y, Mumtaz AS, et al. 2017. Phragmidium punjabense, a new
species of rust fungus on Rosa brunonii in the outer Himalayan ranges of
Murree, Pakistan. Nova Hedwigia 105: 385– 396.
Aime MC. 2006. Toward resolving family-level relationships in rust fungi
(Uredinales). Mycoscience 47: 112–122.
Aime MC, Bell CD, Wilson AW. 2018. Deconstructing the evolutionary com-
plexity between rust fungi (Pucciniales) and their plant hosts. Studies in
Mycology 89: 143–152.
Alvarado-Rosales D, Nieto-López EH, Téliz-Ortiz D, et al. 2015. First re-
port of Gymnosporangium clavipes Cooke & Peck affecting Crataegus
mexicana var. Chapeado and C. gracilior in Mexico. Research in Plant
Disease. 21: 250–253.
Anikster Y, Szabo LJ, Eilam T, et al. 2004. Morphology life cycle biology and
DNA sequence analysis of rust fungi on garlic and chives from California.
Phytopathology 94: 569– 577.
Beenken L. 2014. Pucciniales on Annona (Annonaceae) with special focus
on the genus Phakopsora. Mycological Progress 13: 791–809.
Beenken L, Wood AR. 2015. Puccorchidium and Sphenorchidium two new
genera of Pucciniales on Annonaceae related to Puccinia psidii and the
genus Dasyspora. Mycological Progress 14: 49.
Beenken L, Zoller S, Berndt R. 2012. Rust fungi on Annonaceae II: the genus
Dasyspora Berk. & M.A. Curtis. Mycologia 104: 659– 681.
Blomquist CL, McKemy JM, Aime MC, et al. 2009. First report of bamboo
rust caused by Kweilingia divina on Bambusa domestica in Los Angeles
County California. Plant Disease 93: 201.
Blomquist CL, Scheck HJ, Woods PW, et al. 2014. First detection of Puccinia
ballotiflora on Salvia greggii. Plant Disease 98: 1270.
Blomquist CL, Scholler M, Scheck HJ. 2015. Detection of rust caused by
Tranzschelia mexicana on Prunus salicifolia in the United States. Plant
Disease 99: 1856.
Bruckart WL, Eskandari FM, Berner DK, et al. 2012. Comparison of Puccinia
acroptili from Eurasia and the USA. Botany 90: 465– 471.
Cao B, Tao SQ, Tian CM, Liang YM. 2017a. Coleopuccinia in China and its
relationship to Gymnosporangium. Phytotaxa 347: 235–242.
Cao B, Tian CM, Liang YM. 2016. Gymnosporangium huanglongense sp.
nov. from western China. Mycotaxon 131: 375– 383.
Cao J, Tian CM, Liang YM, et al. 2017b. Two new Chrysomyxa rust species
on the endemic plant Picea asperata in western China and expanded
description of C. succinea. Phytotaxa 292: 218– 230.
Chatasiri S, Ono Y. 2008. Phylogeny and taxonomy of the Asian grapevine
leaf rust fungus, Phakopsora euvitis, and its allies (Uredinales). Myco-
science 49: 66–74.
Crane PE, Yamaoka Y, Engkhaninun J, et al. 2005. Caeoma tsukubaense
n. sp., a rhododendron rust fungus of Japan and southern Asia and its
relationship to Chrysomyxa rhododendri. Mycoscience 46: 143–147.
Deadman ML, Al Sadi AM, Al Maqbali YM, et al. 2011. Additions to the rust
fungi Pucciniales from northern Oman. Sydowia 63: 155–168.
Deadman ML, Maqbali YA, Subhi AA, et al. 2007. First report of rust caused
by Tranzschelia discolor on peach in Oman. Plant Disease 91: 638.
Demers JE, Liu M, Hambleton S, et al. 2017. Rust fungi on Panicum. My-
cologia 109: 1–17.
Demers JE, Romberg MK, Castlebury LA. 2015. Microcyclic rusts of hollyhock
Alcea rosea. IMA Fungus 6: 477–482.
Dervis S, Dixon L, Doğanlar M, et al. 2010. Gall production on hawthorns
caused by Gymnosporangium spp. in Hatay province, Turkey. Phytopar-
asitica 38: 391–400.
Dixon LJ, Castlebury LA, Aime MC, et al. 2010. Phylogenetic relationships
of sugarcane rust fungi. Mycological Progress 9: 459– 468.
Engkhaninun J, Ono Y, Kakishima M. 2005. Phylogenetic relationships of four
Puccinia species parasitic on Artemisia in Japan. Mycoscience 46: 61–65.
Feau N, Vialle A, Allaire M, et al. 2011. DNA barcoding in the rust genus
Chry somyxa and its implications for the phylogeny of the genus. Mycologia
103: 1250–1266.
Fernández JL, Alvarado P. 2016. First DNA sequencing for Gymnosporan-
gium amelanchieris and G. gracile. Boletín de la Sociedad Micológica de
Madrid 40: 105–119.
Hernandez J, Aime MC, Henkel TW. 2005. The rust fungi Uredinales of
Guyana. Sydowia 57: 189– 222.
Jin Y, Szabo LJ, Carson M. 2010. Century-old mystery of Puccinia striiformis
life history solved with the identification of Berberis as an alternate host.
Phytopathology 100: 432– 435.
Kabaktepe S, Mutlu B, Karakus S, et al. 2016. Puccinia marrubii Pucciniaceae
a new rust species on Marrubium globosum subsp. globosum from Nigde
and Malatya in Turkey. Phytotaxa 272: 277–284.
Kenaley S, Daughtrey M, O’Brien D, et al. 2012. First report of the pear trellis
rust fungus, Gymnosporangium sabinae, on Pyrus calleryana (‘Bradford’
and ‘Chanticleer’) and P. communis in New York State. Plant Disease
96: 1373.
Kropp BR, Hansen DR, Wolf PG, et al. 1997. A study on the phylogeny of
the dyer’s woad rust fungus and other species of Puccinia from Crucifers.
Phytopathology 87: 565– 571.
Langrella SRH, Glenb M, Alfenasc AC. 2008. Molecular diagnosis of Puccinia
psidii guava rust – a quarantine threat to Australian eucalypt and Myrtaceae
biodiversity. Plant Pathology 57: 687–701.
Liang YM, Tian CM, Kakishima M. 2006. Phylogenetic relationships on 14
morphologically similar species of Pucciniastrum in Japan based on rDNA
sequence data. Mycoscience 47: 137–144.
Liberato JR, McTaggart AR, Shivas RG. 2014. First report of Masseeëlla
capparis in Australia. Australasian Plant Disease Notes 9: 121.
Liu M, Hambleton S. 2012. Puccinia chunjii, a close relative of the cereal
stem rusts revealed by molecular phylogeny and morphological study.
Mycologia 104: 1056–1067.
Liu M, Hambleton S. 2013. Laying the foundation for a taxonomic review
of Puccinia coronata s.l. in a phylogenetic context. Mycological Progress
12: 63– 89.
Liu M, McCabe E, Chapados JT, et al. 2015. Detection and identification
of selected cereal rust pathogens by TaqMan real-time PCR. Canadian
Journal of Plant Pathology 37: 92–105.
Liu M, Szabo LJ, Hambleton S, et al. 2013. Molecular phylogenetic relation-
ships of the brown leaf rust fungi on wheat rye and other grasses. Plant
Disease 97: 1408–1417.
Mahadevakumar S, Szabo LJ, Eilam T, et al. 2016. A new rust disease on
wild coffee Psychotria nervosa caused by Puccinia mysuruensis sp. nov.
Plant Disease 100: 1371–1378.
Maier W, Begerow D, Weiss M, et al. 2003. Phylogeny of the rust fungi: an
approach using nuclear large subunit ribosomal DNA sequences. Canadian
Journal of Botany 81: 12–23.
Maier W, McTaggart AR, Roux J, et al. 2015. Phakopsora myrtacearum
sp. nov., a newly described rust Pucciniales on eucalypts in eastern and
southern Africa. Plant Pathology 65: 189–195.
Maier W, Wingfield BD, Mennicken M, et al. 2007. Polyphyly and two emerging
lineages in the rust genera Puccinia and Uromyces. Mycological Research
111: 176–185.
Martin LA, Lloyd Evans D, Castlebury LA, et al. 2017. Macruropyxis fulva
sp. nov., a new rust Pucciniales infecting sugarcane in southern Africa.
Australasian Plant Pathology 46: 63–74.
Matheny PB, Gossmann JA, Zalar P, et al. 2006. Resolving the phylogenetic
position of the Wallemiomycetes: an enigmatic major lineage of Basidi-
omycota. Canadian Journal of Botany 84: 1794–1805.
McKenzie EHC, Padamsee M, Dick M. 2013. First report of rust on Alnus in
New Zealand is Melampsoridium betulinum, not M. hiratsukanum. Plant
Pathology & Quarantine 3: 59– 65.
McTaggart AR, Doungsa-ard C, Geering AD, et al. 2015. A co-evolutionary
rela tionship exists between Endoraecium (Pucciniales) and its Acacia hosts
in Australia. Persoonia 35: 50– 62.
McTaggart AR, Geering ADW, Shivas RG. 2014. Uredinopsis pteridis and
Desmella aneimiae the first rust fungi Pucciniales reported on ferns Pteri-
dophyta in Australia. Australasian Plant Disease Notes 9: 149.
McTaggart AR, Shivas RG, Doungsa-ard C, et al. 2016. Identification of
rust fungi Pucciniales on species of Allium in Australia. Australasian Plant
Patho logy 45: 581–592.
Minnis AM, McTaggart AR, Rossman AY, et al. 2012. Taxonomy of mayapple
rust: the genus Allodus resurrected. Mycologia 104: 942– 950.
Mulvey RL, Hambleton S. 2015. Stem rust of highbush-cranberry Viburnum
edule caused by Puccinia linkii near Juneau Alaska. Plant Disease 99: 893.
Novick RS. 2008. Phylogeny, taxonomy, and life cycle evolution in the cedar
rust fungi Gymnosporangium. PhD thesis. Yale University, New Haven,
Connecticut, USA.
Padamsee M, McKenzie EHC. 2012. First report of Puccinia thaliae on canna
lily in New Zealand and in some Pacific island countries. Australasian Plant
Disease Notes 7: 139–141.
Padamsee M, McKenzie EHC. 2014. A new species of rust fungus on the New
Zealand endemic plant Myosotidium from the isolated Chatham Islands.
Phyto taxa 174: 223– 230.
Pedley KF. 2009. PCR-based assays for the detection of Puccinia horiana
on chrysanthemums. Plant Disease 93: 1252–1258.
Supplementary material
Pegg GS, Giblin FR, McTaggart AR, et al. 2013. Puccinia psidii in Queens-
land, Australia: disease symptoms, distribution and impact. Plant Pathology
63: 1005–1021.
Pfunder M,Schurch S, Roy BA. 2001. Sequence variation and geographic
distribution of pseudoflower-forming rust fungi Uromyces pisi s. lat. on
Euphorbia cyparissias. Mycological Research 105: 57–66.
Pota S, Chatasiri S, Unartngam J, et al. 2015. Taxonomic identity of a Pha-
kopsora fungus causing the grapevine leaf rust disease in Southeast Asia
and Australasia. Mycoscience 56: 198– 204.
Raguso RA, Roy BA 1998. Floral scent production by Puccinia rust fungi that
mimic flowers. Molecular Ecology 7: 1127–1136.
Sampangi RK, Aime MC, Mohan SK. 2010. First report of rust caused by
Puccinia similis on Artemisia tridentata in Idaho and Oregon. Plant Disease
94: 380.
Schilder AMC, Lizotte E, Yun HY, et al. 2011. First report of Juneberry rust
caused by Gymnosporangium nelsonii on Juneberry in Michigan. Plant
Disease 95: 770.
Scholler M, Aime MC. 2006. On some rust fungi Uredinales collected in an
Acacia koa – Metrosideros polymorpha woodland, Mauna Loa Road, Big
Island, Hawaii. Mycoscience 47: 159–165.
Scholler M, Lutz M, Wood AR, et al. 2011. Taxonomy and phylogeny of Puc-
cinia lagenophorae: a study using rDNA sequence data morphological and
host range features. Mycological Progress 10: 175–187.
Seier MK, Morin L, Van der Merwe M, et al. 2009. Are the microcyclic rust
species Puccinia melampodii and Puccinia xanthii conspecific? Mycological
Research 113: 1271–1282.
Shands AC, Crandall SG, Miles. 2018. First report of leaf rust on california
blackberry (Rubus ursinus) caused by Kuehneola uredinis in California.
Plant Disease 102: 682.
Shen YM, Chung WH, Huang TC, et al. 2018. Unveiling Gymnosporangium
corniforme, G. unicorne, and G. niitakayamense sp. nov. in Taiwan. My-
coscience 59: 218– 228.
Shen YM, Huang TC. 2017. First report of rust caused by Puccinia kusanoi
affec ting yushan cane Yushania niitakayamensis in Taiwan. Plant Disease
101: 385.
Sjamsuridzal W, Nishida H, Ogawa H, et al. 1999. Phylogenetic positions of
rust fungi parasitic on ferns: Evidence from 18S rDNA sequence analysis.
Mycoscience 40: 21–27.
Souza ESC, Chaves ZM, Soares WRO, et al. 2015. Uromyces hawksworthii
nom. nov. for Aecidium goyazense on Phthirusa stelis Loranthaceae from
the Brazilian Cerrado. IMA Fungus 6: 155–162.
Su D, Fu JF, Zhou RJ, et al. 2012. Severe outbreak of rust caused by Co-
leosporium pulsatillae detected on Pulsatilla spp. in China. Plant Disease
98: 1154.
Swann EC, Taylor JW. 1995. Phylogenetic perspectives on basidiomycete
systematics: evidence from the 18S rRNA gene. Canadian Journal of
Botany 73: 862– 868.
Szabo LJ. 2006. Deciphering species complexes: Puccinia andropogonis
and Puccinia coronata examples of differing modes of speciation. Myco-
science 47: 130–136.
Tan MK, Collins D, Chen Z, et al. 2014. A brief overview of the size and
composition of the myrtle rust genome and its taxonomic status. Mycol-
ogy 5: 52– 63.
Tian CM, Shang YZ, Zhuang JY, et al. 2004. Morphological and molecular
phylogenetic analysis of Melampsora species on poplars in China. Myco-
science 45: 56– 66.
Vialle A, Feau N, Frey P, et al. 2013. Phylogenetic species recognition reveals
host-specific lineages among poplar rust fungi. Molecular Phylogenetics
and Evolution 66: 628– 644.
Vogler DR, Bruns TD. 1998. Phylogenetic relationships among the pine
stem rust fungi Cronartium and Peridermium spp. Mycologia 90: 244– 257.
Wingfield BD, Ericson L, Szaro T, et al. 2004. Phylogenetic patterns in the
Uredinales. Australasian Plant Pathology 33: 327–335.
Wood AR, Crous PW. 2005. Epidemic increase of Endophyllum osteospermi
(Uredinales, Pucciniaceae) on Chrysanthemoides monilifera. Biocontrol
Science and Technology 15: 117–125.
Yang T, Tian CM, Liang YM, et al. 2014. Thekopsora ostryae Pucciniastraceae
Pucciniales a new species from Gansu northwestern China. Mycoscience
55: 246– 251.
Yang T, Tian CM, Liang YM, et al. 2015. Two new rust fungi of Thekopsora
on Cornus Cornaceae from western China. Phytotaxa 56: 461–469.
Yun HY, Hong SG, Rossman AY, et al. 2009. The rust fungus Gymnosporan-
gium in Korea including two new species, G. monticola and G. unicorne.
Mycologia 101: 790– 809.
Yun HY, Minnis AM, Dixon LJ, et al. 2010. First report of Uromyces acumina-
tus on Honckenya peploides the endangered sea beach sandwort. Plant
Disease 94: 279.
Yun HY, Minnis AM, Kim YH, et al. 2011. The rust genus Frommeella revis-
ited: a later synonym of Phragmidium after all. Mycologia 103: 1451–1463.
Zale J, Freshour L, Agarwal S, et al. 2008. First report of rust on switchgrass
Panicum virgatum caused by Puccinia emaculata in Tennessee. Plant
Disease 92: 1710
Zhao P, Kakishima M, Wang Q, et al. 2017. Resolving the Melampsora epitea
complex. Mycologia 109: 391–407.
Zhao P, Liu F, Li YM, et al. 2016. Inferring phylogeny and speciation of Gym-
nosporangium species, and their coevolution with host plants. Scientific
Reports 6: 29339.
Zhao P, Wang QH, Tian CM, et al. 2015. Integrating a numerical taxonomic
method and molecular phylogeny for species delimitation of Melampsora
species Melampsoraceae, Pucciniales on willows in China. PLoS One
17: e0144883.
Zuluaga C, Buriticá P, Marín M. 2011. Phylogenetic analysis of rust fungi
Uredinales from the Colombian Andean region using 28S ribosomal DNA
sequences. Revista de Biología Tropical 59: 517–540.
