New species of Penzigomyces, Sporidesmium and Stanjehughesia from plant
debris in Spain
Julio Mena-Portales1, Margarita Hernández-Restrepo*2, 3, Josep Guarro4, David W. Minter5
and Josepa Gené4
1
Instituto de Ecología y Sistemática, Ministerio de Ciencia, Tecnología y Medio Ambiente, La Habana 19 C.P.
11900, Cuba.
2
CBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands. * Corresponding
author: m.hernandez@cbs.knaw.nl.
3
Department of Microbiology and Plant Pathology, Forestry and Agricultural Biotechnology Institute (FABI),
University of Pretoria, Pretoria 0002, South Africa.
4
Unitat de Micologia, Institut d’Investigació Sanitària Pere Virgili (IISPV), Universitat Rovira i Virgili, 43201
Reus, Spain.
5
CABI Bioscience. Bakeham Lane, Egham, Surrey, TW20 9TY, UK
Abstract: Four new species of Sporidesmium complex collected on plant debris in different
protected areas of the Iberian Peninsula are described and illustrated. Penzigomyces
basiacutus is characterized by its obclavate to rostrate conidia with a narrowly obconictruncate basal cell and verruculose apical cell. Sporidesmium corniculatum is distinguished
from other species of the genus by its occasional furcate and only transversely septate conidia
and Sporidesmium tunicatum by its obclavate to rostrate, verrucose conidia with an apical
mucilaginous sheath tunica. Stanjehughesia obclavorostrata is distinguished by its obclavate
to rostrate conidia with the basal cell sometimes darker than the rest.
Key words: anamorphic fungi, Hyphomycetes, Spain, taxonomy.
1
Introduction
The Sporidesmium complex is a large anamorphic group of dematiaceous fungi with nearly
250 species mostly colonizing branches, trunks and dead leaves of many plants.
Sporidesmium was established by Link in 1809, but the traditional concept of the genus is
based on the Ellis’s description of S. ehrenbergii (Ellis, 1958, 1971). Sporidesmium has been
considered a heterogeneous genus (Sutton & Hodges, 1979; Hughes, 1979) and repeatedly
revised (Kirk 1982, Subramanian 1992, Hernández-Gutiérrez & Sutton 1997, Shoemaker &
Hambleton 2001).
Following the criteria of Hughes (1979), Kirk (1982) established the genus
Sporidesmiella P.M.Kirk for species with few septa and cuneate to obovoid conidia.
Subramanian (1992) segregated a large number of Sporidesmium species, according to the
type of conidiophore proliferation and conidial septation, into the genera Ellisembia Subram.,
Penzigomyces Subram., Polydesmus Mont., Repetophragma Subram., Sporidesmiella
P.M.Kirk, Sporidesmium Link, and Stanjehughesia Subram. A few other species were
transferred to other genera such as Acarocybellina Subram., Gangliophora Subram.,
Hemicorynesporella Subram., and Janetia M.B.Ellis. Sporidesmium densum (Sacc. & Roum.)
Mason & S.Hughes was considered congeneric with Polydesmus elegans Durieu & Mont., the
type species of the genus, which was not accepted by Hernández-Gutiérrez & Sutton (1997)
who proposed the genus Imimyces A.Hern. & Sutton for Sp. densum and other similar species.
In addition, these authors erected the genus Linkosia A.Hern. & Sutton to accommodate Sp.
coccothrinacis A.Hern. & J.Mena as the type, and proposed seven new combinations.
Linkosia was characterized by distoseptate conidia formed on conidiogenous cells, which
arise directly from the fertile hyphae. Shoemaker & Hambleton (2001) did not accept
Imimyces because they considered that the specimen designated as the type species was a
Polydesmus and therefore proposed the genus Imycles for the rest of Imimyces species defined
by Hernández-Gutiérrez & Sutton (1997). However, Réblová (1999) questioned the validity
2
of these genera because she considered that their diagnostic characters on the natural substrate
differed from those in culture, and also due to the lack of correlation with anamorphteleomorph connections previously established. Wu & Zhuang (2005) considered the
distinction between Penzigomyces-Sporidesmium and Ellisembia-Imycles very difficult when
based on conidiophore proliferation and conidiogenous cell morphology, and preferred to
simplify the taxonomic system considering Imycles and Penzigomyces as synonyms of
Ellisembia and Sporidesmium, respectively. Shenoy et al. (2006), using molecular techniques,
demonstrated that most of these segregate anamorphic genera were phylogenetically
heterogeneous, but Seifert et al. (2011) accepted all segregated genera of Sporidesmium sensu
lato as morphologically different groups that were useful for identification purposes.
During a survey of anamorphic fungi on plant debris in different protected areas of the
Iberian Peninsula four interesting species morphologically compatible with the Sporidesmium
complex were collected. Based on the conidial morphology, size and pigmentation, these
species are proposed here as new.
Materials and Methods
Samples of plant material were processed using the methodology described by CastañedaRuiz (2005). Fungal specimens were studied and illustrated following Hernández-Restrepo et
al. (2012). After testing different media and culture conditions, attempts to establish
monoconidial cultures of the species described, failed and, therefore, only dried material
could be preserved. Specimens are deposited in the herbarium of Centraalbureau voor
Schimmelcultures, Utrecht, The Netherlands (CBS) and Facultat de Medicina i Ciències de la
Salut, Reus, Spain (FMR).
Taxonomy
Penzigomyces basiacutus Hern.-Restr., J.Mena, Gené & Guarro, sp. nov. Figs 1-2
MYCOBANK NO: MB 814910
3
Fig. 1. Penzigomyces basiacutus. a. Habit. b. Conidiophores. c. Conidia. Scale
bar = 10 µm.
4
Fig. 2. Penzigomyces basiacutus. a–d. Conidiophores. e–g. Conidia. Scale bar
= 10 µm.
5
ETYMOLOGY: Referring to the narrowly obconic-truncate basal cell of conidia.
DESCRIPTION: Colonies effuse, black, hairy. Mycelium partly immersed in the substrate,
hyphae pale brown, septate, branched, 1.5–2.5 um wide. Conidiophores macronematous,
mononematous, solitary, simple, cylindrical, straight, smooth, septate, dark brown, up to 216
µm long, 5–7.5 µm wide, 7.5–17.5 µm at the bulbous base, 2.5–4 µm at the apex.
Conidiogenous cells monoblastic, terminal, lageniform, smooth-walled, brown, 6–12 × 4.5–
5.5 µm, with up to seven lageniform percurrent proliferations. Conidia apical, solitary, dry, 3–
15-septate, obclavate to rostrate, 28–73 × 8.5–12.5 µm, 4.5–5.5 µm wide at the rostrate apex,
1.5–2.5 µm wide at the acute base, brown to dark brown, becoming pale brown toward the
apex, basal cell narrowly obconic-truncate, pale to mid- brown, slightly verruculose at the
apex. Sexual morph unknown.
SPECIMEN EXAMINED: SPAIN, Aragón, National Park of Ordesa y Monte Perdido. On
dead wood. Jun. 2009. M.Hernández-Restrepo, J.Mena & J.Cano (holotype CBS H-21044,
isotype FMR 11158).
The genus Penzigomyces was established by Subramanian (1992) for former
Sporidesmium species characterized by doliiform, lageniform or nodose percurrent
conidiogenous cell proliferations and euseptate conidia. However, Wu & Zhuang (2005)
considered Penzigomyces a synonym of Sporidesmium. Seifert et al. (2011) provisionally
recognized all genera segregated from Sporidesmium on the basis of conidiogenous cell
morphology and proliferation and conidial septation.
Penzigomyces basiacutus can be distinguished by its obclavate conidia with a
verruculose rostrum and a truncate base with a terminal narrowly obconic cell. The conidia
somewhat resemble those of P. australiensis (M.B.Ellis) Subram., P. nodipes (Penz. & Sacc.)
Subram. and P. uapacae (M.B.Ellis) Subram. However, in P. australiensis the conidia are
smooth, 7–9-septate and measure 40–65 × 11–16 µm (Ellis 1976). Wu & Zhuang (2005)
widened its concept by including a Chinese specimen with conidia measuring 42–80 × 10–13
6
µm, (1.5–3 µm at the rounded apex and 3–5 µm at the conico-truncate base) and 9–13 septa.
In P. nodipes the conidia are smooth-walled, 11–14-septate, sometimes constricted at the
septa, and measure 36–67 × 6.5–8 µm, (1.5–4 µm wide below the acute apex and 2.5–4 µm at
the base); in addition this species is mainly found on palms and orchids in tropical areas (Ellis
1976, Wu & Zhuang 2005). The conidia of P. uapacae are 5–8-septate, pale to mid brown and
smooth-walled and measure 50–80 × 7–10 µm, tapering to 3–4 µm wide near the apex and 3–
4 µm wide at the base (Ellis 1958, 1976).
Sporidesmium corniculatum J.Mena, Hern.-Restr., Gené & Guarro, sp. nov. Figs 3–4
MYCOBANK NO.: MB 814911
ETYMOLOGY: referring to the occasional presence of furcate conidia.
DESCRIPTION: Colonies effuse, black, hairy. Mycelium partly immersed in the substratum,
hyphae pale brown, septate, branched, 1.5–2 µm wide. Conidiophores macronematous,
mononematous, solitary, simple, cylindrical, straight, septate, dark brown, smooth, 45–70 µm
long, 5–7 µm wide, 7.5–8 µm at the base, 3.5–5 µm at the apex. Conidiogenous cells
monoblastic, integrated, terminal, smooth-walled, brown, 5–10 × 5 µm. Conidia apical,
solitary, dry, 13–26-septate, obclavate to rostrate, sometimes furcate with two arms, 60–137.5
× 10–12.5 µm, 3–5 µm wide at the base, 4–8.5 µm at the apex, mid- to dark brown, remaining
pale brown towards the apex, smooth-walled; arms 5–17-septate, 25–92.5 × 6–9 µm. Sexual
morph unknown.
SPECIMEN
EXAMINED:
SPAIN, Aragon, Natural Park Valles Occidentales. On bark.
Mar. 2012. M.Hernández-Restrepo & J.Capilla (holotype CBS H-21046, isotype FMR
12431).
The occasional presence of branched conidia and several percurrent proliferations
could justify the inclusion of this species in other genera such as Actinocladium Ehrenb.,
Ceratosporella Höhn. or Triposporium Corda. The conidiogenesis of the members of these
genera is similar to that of the Sporidesmium complex. However, the low frequency of furcate
7
Fig. 3. Sporidesmium corniculatum. a. Habit. b. Conidiophore. c. Conidia. Scale
bar = 10 µm.
8
Fig. 4. Sporidesmium corniculatum. a–c. Conidiophores with conidia attached.
d–e. Conidia. Scale bar = 10 µm.
9
conidia observed in the Spanish specimen was the reason for including our isolate in
Sporidesmium sensu Subramanian (1992).
The only species of Sporidesmium having typically furcate conidia is Sp. taiwanense
Matsushima (1983), but in this species the conidiophores are 0–2-septate, highly variable in
length (6-50 µm), the conidiogenous cells are determinate, and in the conidia, septa are
constricted, sometimes oblique and rarely longitudinal, and the basal cell is obconic,
pedicellate and brown. Wu & Zhang (2005) suggested that Sp. taiwanense was better
accommodated in Stanjehughesia on the basis of its euseptate and clavate conidia on discrete
conidiogenous cells. However, a new combination was not established since the authors did
not study the type material.
Ellisembia karadkensis Rajeshkumar & SK Singh has been recently described with
simple or branched conidia (Rajeshkumar et al. 2012); however, they are distoseptate, a
character used by Subramanian (1992) to segregate Ellisembia from Sporidesmium. Other
characters that distinguish E. karadkensis from Sp. corniculatum are that the furcate conidia
are longer (190–250 µm long), narrower below the apex (2–2.7 µm wide) and have 10–35
distosepta.
Sporidesmium tunicatum M. Hern.-Restr., J. Mena, Gené & Guarro sp. nov. Fig. 5–6
MYCOBANK NO.: MB 814912
ETYMOLOGY: referring to the tunica, a mucilaginous sheath surrounding the conidial apex.
DESCRIPTION: Colonies effuse, black, hairy. Mycelium partly immersed, hyphae pale brown,
septate, branched, 1.5–3 µm wide. Conidiophores macronematous, mononematous, solitary,
simple, cylindrical, straight, septate, dark brown, smooth, 110–180 µm long, 6–7.5 µm wide,
8.5–12.5 µm at the base, 4–5 µm at the apex, proliferation 0–1, percurrent. Conidiogenous
cells monoblastic, integrated, terminal, smooth-walled, brown, 19–25 × 5–6 µm. Conidia
apical, solitary, dry, 6–10 (mostly 8)-septate, obclavate, sometimes rostrate, 43–75 × 9–13
µm, 3–5 µm wide at the base, 2.5–3.5(–5) µm at the apex, dark olivaceous brown, becoming
10
Fig. 5. Sporidesmium tunicatum. a. Habit. b. Conidia. c. Conidiophores. Scale
bar = 10 µm.
11
Fig. 6. Sporidesmium tunicatum. a. Conidiophore. b–d. Conidia. Scale bar = 10
µm.
12
Fig. 7. Stanjehugesia obclavorostrata. a. Habit. b. Conidiophores. c.
Conidia. Scale bar = 10 µm.
13
Fig. 8. Stanjehugesia obclavorostrata. a. Conidiophores (arrows indicate
the conidiogenous cells). b, c. Conidia. Scale bar = 10 µm.
14
pale brown towards the apex, verrucose at the central cells, apical tunica 9–15 × 10–30 µm.
Sexual morph unknown.
SPECIMEN
EXAMINED:
SPAIN, Galicia, Natural Park As Fragas do Eume. On dead
wood. May 2010. M.Hernández-Restrepo, J.Mena & J.Guarro (holotype CBS H-21045,
isotype FMR 11243).
Sporidesmium tunicatum differs from congeneric species (Ellis, 1958, 1971, 1976;
Matsushima, 1971, 1975; Wu & Zhuang, 2005) by the unique combination of the sometimes
rostrate, usually 8-septate, verrucose conidia with an apical mucilaginous sheath.
Sporidemium hainanense W.P.Wu is the most similar species, but its conidia are smooth and
shorter (40-50 µm) (Wu & Zhuang, 2005).
Stanjehughesia obclavorostrata J.Mena, M.Hern.-Restr., Gené & Guarro, sp. nov. Figs 7–8
MYCOBANK NO.: MB 814913
ETYMOLOGY: referring to the conidial morphology.
DESCRIPTION: Colonies on natural substrate effuse, black. Mycelium partly immersed, hyphae
branched, septate, subhyaline to pale brown, 1.5–3.5 μm wide. Conidiophores reduced to a
single conidiogenous cell. Conidiogenous cells monoblastic, determinate, ampulliform or
lageniform, erect, straight or flexuous, thick and smooth-walled, mostly solitary, sometimes
caespitose, brown to dark brown, 13.5–20(–24) μm long, 7.5–12.5 μm wide at the bulbous
base, 4.5–5 μm wide at the truncate apex. Conidia apical, solitary, dry, (7–)9–16-euseptate,
straight or slightly curved, obclavate, sometimes rostrate, rarely obclavate-fusiform, 52.5–145
× 10–15 μm, brown, smooth-walled; apical cell rounded, light brown, 5.5–9(–11) μm wide;
basal cell obconical, frequently slightly darker than the rest of cells, 3.5–4 μm wide. Sexual
morph unknown.
SPECIMEN EXAMINED: SPAIN, Castilla-La Mancha, Natural Park Alto Tajo. On dead
wood. 5 May 2011. M.Hernández-Restrepo, J.Mena & J.Guarro (holotype CBS H-21047,
isotype FMR 12067).
15
Only other two species of Stanjehughesia such as St. hormiscioides (Corda) Subram.
and St. curviapicis (Goh & K.D.Hyde) D.A.C.Almeida & Gusmão (=St. hamatiella W.P.Wu)
have conidia with a subhyaline or pale brown apical cell and conico-truncate basal cell
usually darker than the rest as occurs in St. obclavorostrata (Subramanian 1992, Wu &
Zhuang 2005, Almeida et al. 2014).
Stanjehughesia hormiscioides, the type species of the genus, has become objected to
complex taxonomic and nomenclatural problems. The current name for this species, as
recognized by both Index Fungorum (http://www.indexfungorum.org/) and MycoBank
(http://es.mycobank.org/) is Sporidesmium hormiscioides Corda, which would imply the
establishment of a new type for Stanjehughesia Subram. Based on Ellis (1958, 1976) and
Hughes & Illman (1974), conidia are described and illustrated as arising from single
conidiogenous cells from micronematous conidiophores. We follow Subramanian (1992) and
Wu & Zhuang (2005) including this species in Stanjehughesia.
In contrast to St. obclavorostrata, conidia of St. hormiscioides are cylindrical-fusoid to
subcylindrical and larger, i.e. 65–270 × 10–17 μm (Ellis 1958, 1976;, Hughes & Illman 1974).
Hughes (1958) observed that the conidia of St. hormiscioides are morphologically very
variable; some specimens produced long conidia with subulate distal ends (conidia in an
European collection were up to 400 μm long), while in other specimens the conidia are
shorter and more cylindrical with a broad blunt apex.
Stanjehughesia curviapicis is distinguished by its hamate conidia with a characteristic
curved or circinate apex, which are also narrower than those of St. obclavorostrata. The
conidia of a specimen of St. curviapices described as Janetia curviapices Goh & K.D.Hyde
measure 65–100 × 5.5–7.5 µm (Goh & Hyde 1996) while those of the specimen described as
St. hamatiella measure 70–140 × 7–8.5 μm (Wu & Zhuang 2005).
Stanjehughesia obclavorostrata also slightly resembles St. fasciculata J.Mena,
G.Delgado & Guarro, St. fusiformis W.P.Wu, St. polypora W.P.Wu and St. ventricosa
16
Marinc., M.J.Wingf. & Crous. However, conidia of St. fasciculata are smaller (70–100 × 9–
10.5 µm) and have a globose mucilaginous appendage at the apex (Mena et al. 2001, Wu &
Zhuang 2005); in St. fusiformis they are shorter and narrower (6–8-septate, 65–85 × 7–8 µm)
(Wu & Zhuang 2005); conidia of St. polypora are longer (110–165 µm long) and conidial
cells have a germ pore (Wu & Zhuang 2005); while those of St. ventricosa are somewhat
similar in size and septal number, but the basal cell is not darker than the rest (Marincowitz et
al. 2008).
Some species described in Janetia could belong to Stanjehughesia, mainly after Goh
& Hyde (1996) who modified Ellis’ original generic concept of Janetia to include species
with simple conidiophores or synnemata, monoblastic or polyblastic, denticulate
conidiogenous cells, and euseptate or distoseptate, and obclavate or cylindrical conidia.
Among species of Janetia with a darker conidial basal cell, J. capnophila S.Hughes is
comparable with St. obclavorostrata by their similar conidial morphology. However, J.
capnophila is associated with sooty moulds, its conidia germinate at the apex to produce a
hypha frequently anastomosing with other conidia, and several conidial cells may become
conidiogenous (Hughes 1983).
ACKNOWLEDGEMENTS
This study was supported by the Spanish Ministerio de Ciencia y Tecnología, grant CGL
2011-27185.
REFERENCES
ALMEIDA, D.A.C., A.N. MILLER & L.F.P. GUSMÃO 2014: New species and
combinations of conidial fungi from the semi-arid Caatinga biome of Brazil. – Nova
Hedwigia 98: 431–447.
17
CASTAÑEDA-RUIZ, R.F. 2005: Metodología en el estudio de los hongos anamorfos. – In:
Anais do V Congresso Latino Americano de Micología, Brasilia: 182–183.
ELLIS, M.B. 1958: Clasterosporium and some allied Dematiaceae. Phragmosporae I. –
Mycol. Papers 70: 1–89.
ELLIS, M.B. 1971: Dematiaceous Hyphomycetes. – Commonwealth Mycological Institute,
Kew. 608 pp.
ELLIS, M.B. 1976: More Dematiaceous Hyphomycetes. – Commonwealth Mycological
Institute, Kew. 507 pp.
GOH, T.K. & K.D. HYDE 1996: Janetia curviapicis, a new species, and an emended
description of the genus. – Mycologia 88: 1014–1021.
HERNÁNDEZ-GUTIÉRREZ, A & B.C. SUTTON 1997: Imimyces and Linkosia, two new
genera segregated from Sporidesmium sensu lato, and description of Polydesmus. – Mycol.
Res. 101: 201–209.
HERNÁNDEZ-RESTREPO, M., C. SILVERA-SIMÓN, J. MENA-PORTALES, A.
MERCADO-SIERRA, J. GUARRO et al. 2012: Three new species and a new record of
Diplococcium from plant debris in Spain. – Mycol. Progr. 11:191–199.
HUGHES, S.J. 1958: Revisiones hyphomycetum aliquot cum appendice de nominibus
rejiciendis. – Can. J. Bot. 36: 727–836.
HUGHES, S.J. 1979: Relocation of species of Endophragmia auct. with notes on relevant
generic names. – N. Z. J. Bot. 17: 139–188.
HUGHES, S.J. 1983: New Zealand Fungi 32. Janetia capnophila sp. nov. and some allies. –
N. Z. J. Bot. 21:177–182.
HUGHES S.J. & W.I. ILLMAN 1974: Sporidesmium hormiscioides. – Fungi Canadenses 58:
1–2.
18
KIRK, P.M. 1982: New or interesting Microfungi VI. Sporidesmiella gen. nov.
(Hyphomycetes). – Trans. Br. Mycol. Soc. 79: 479–489.
MARINCOWITZ, S., P.W. CROUS, J.Z. GROENEWALD & M.J. WINGFIELD 2008:
Microfungi occurring on Proteaceae in the fynbos. – CBS-KNAW Fungal Biodiversity
Centre, Utrecht, The Netherlands. CBS Biodiversity Series 7: 1–166.
MATSUSHIMA, T. 1971: Microfungi of the Solomon Islands and PapuaNew Guinea. –
Published by the author, Kobe, Japan. 78 pp.
MATSUSHIMA, T. 1975: Icones microfungorum a Matsushima lectorum. – Published by the
author, Kobe, Japan. 209 pp.
MATSUSHIMA, T. 1983: Matsushima Mycological Memoirs 3: 1–90. – Published by the
author, Kobe, Japan.
MENA, J., G. DELGADO, A. MERCADO, J. GENÉ, J. GUARRO et al. 2001: New or
interesting hyphomycetes from the Biosphere Reserve of Sierra del Rosario, Cuba. –
Mycologia 93: 751–757.
RAJESHKUMAR, K.C., S.C. KAJALE, S.A. SUTAR & S.K. SINGH 2012: Ellisembia
karadkensis sp. nov. from southern Western Ghats, India. – Mycotaxon 121: 181–186.
RÉBLOVÁ, M. 1999: Studies in Chaetosphaeria sensu lato III. Umbrinosphaeria
gen. nov., and Miyoshiella with Sporidesmium anamorphs. – Mycotaxon 71: 13–43.
SEIFERT, K., G. MORGAN-JONES, W. GAMS & B. KENDRICK 2011: The genera of
Hyphomycetes. – CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands. CBS
Biodiversity Series 9: 1–997.
SHENOY, B.D., R. JEEWON, W.P. WU, D.J. BHAT & K.D. HYDE 2006: Ribosomal and
RPB2 DNA sequence analyses suggest that Sporidesmium and morphologically similar
genera are polyphyletic. – Mycol. Res. 110: 916–928.
19
SHOEMAKER, R.A. & S. HAMBLETON 2001: “Helminthosporium” asterinum,
Polydesmus elegans, Imimyces, and allies. – Can. J. Bot. 79: 592–599.
SUBRAMANIAN, C.V. 1992: A reassessment of Sporidesmium (Hyphomycetes) and some
related taxa. – Proc. Indian natn. Sci. Acad. Part B 58: 179–190.
SUTTON, B.C. & C.S. HODGES 1979: Eucalyptus microfungi: Chaetophragmopsis gen.
nov. and other hyphomycetes. – Nova Hedwigia 29: 593–607.
WU, W. & W. ZHUANG 2005: Sporidesmium, Endophragmiella and related genera from
China. – Fungal Diversity Press. 351 pp. Hong Kong.
20