83
Mycological Progress 3(2): 83–94, May 2004
Phylogeny of Hyaloperonospora based on nuclear ribosomal
internal transcribed spacer sequences
Markus GÖKER1, Alexandra RIETHMÜLLER2, Hermann VOGLMAYR3, Michael WEISS1, Franz
OBERWINKLER1
Phylogenetic relationships in Hyaloperonospora (Oomycetes) were investigated by molecular analyses using internal
transcribed spacer (ITS) sequences and collections from different host plants. Trees were inferred with Bayesian Markov
chain Monte Carlo, neighbor-joining and maximum parsimony methods and rooted with Perofascia. The results are discussed with respect to host taxonomy and species concepts of downy mildews from the literature. Molecular data mainly
support the use of narrow species delimitations and host range as a taxonomic marker. Hyaloperonospora brassicae turns out
to be a non-monophyletic assemblage of different species. New combinations are proposed in accordance with the phylogenetic trees.
Taxonomic novelties: Hyaloperonospora crispula (Fuckel) Göker, Riethmüller, Voglmayr, Weiß & Oberwinkler; Hyaloperonospora
arabidopsis (Gäumann) Göker, Riethmüller, Voglmayr, Weiß & Oberwinkler; Hyaloperonospora cardaminopsis (Gustavsson) Göker,
Riethmüller, Voglmayr, Weiß & Oberwinkler; Hyaloperonospora cochleariae (Gäumann) Göker, Riethmüller, Voglmayr, Weiß & Oberwinkler; Hyaloperonospora galligena (Blumer) Göker, Riethmüller, Voglmayr, Weiß & Oberwinkler; Hyaloperonospora berteroae
(Gäumann) Göker, Riethmüller, Voglmayr, Weiß & Oberwinkler; Hyaloperonospora iberidis (Gäumann ex Gäumann) Göker, Riethmüller, Voglmayr, Weiß & Oberwinkler; Hyaloperonospora isatidis (Gäumann) Göker, Riethmüller, Voglmayr, Weiß & Oberwinkler;
Hyaloperonospora hesperidis (Gäumann) Göker, Riethmüller, Voglmayr, Weiß & Oberwinkler; Hyaloperonospora thlaspeos-arvensis
(Gäumann) Göker, Riethmüller, Voglmayr, Weiß & Oberwinkler; Hyaloperonospora cheiranthi (Gäumann) Göker, Riethmüller, Voglmayr,
Weiß & Oberwinkler; Hyaloperonospora barbareae (Gäumann) Göker, Riethmüller, Voglmayr, Weiß & Oberwinkler.
robably the most difficult problem in the taxonomy of
the plant parasitic Oomycetes or downy mildews (Peronosporaceae) is species definition and delimitation.
Hence, debate about the different species concepts in use is
controversial (see SKALICKY 1964 or HALL 1996 for a more
recent survey). These difficulties are reflected by the numerous
principal changes in the species concepts applied in Peronospora from the very beginning of its taxonomy.
Peronospora represents the largest genus of downy mildews; CONSTANTINESCU (1991) lists about 600 binomials
which were correctly ascribed to it. According to the view presented in the seminal work of DE BARY (1863), Peronospora
specimens from the same family of host plants should be ascribed to a single species. Most students of Peronosporaceae
following DE BARY adopted his concept. However, oospore
P
Lehrstuhl für Spezielle Botanik und Mykologie, Botanisches Institut,
Universität Tübingen, Auf der Morgenstelle 1, D-72076 Tübingen,
Germany
2 Fachgebiet Ökologie, Fachbereich 18 Naturwissenschaften, Universität Kassel, Heinrich-Plett-Str. 40, D-34132 Kassel, Germany
3 Institut für Botanik, Universität Wien, Rennweg 14, A-1030 Wien,
Austria
* Corresponding author: Markus Göker, E-mail: markus.goeker@unituebingen.de, Phone: 0049-7071-2973226, Fax: 0049-7071-295344
1
morphology, which was regarded to be especially useful in
Peronospora taxonomy by SCHROETER (1886) and FISCHER
(1892), contradicts specialization on host families in some
cases (GUSTAVSSON 1959b, VOGLMAYR 2003).
A major shift in Peronospora taxonomy came through the
work of GÄUMANN (1918, 1923) who carried out extensive series of conidial measurements. In cases where he considered
differences in conidial length and width as significant, new
species were erected. Although GÄUMANN (1918, 1923) performed cross-infection experiments in relatively few cases, he
concluded that specialization on host species or genera rather
than host families should be used for delimiting species in
Peronospora.
SAVULESCU (1948) mainly followed GÄUMANN’S treatment. On the other hand, GÄUMANN’S concept was criticized
by GUSTAVSSON (1959b) for underestimating the amount of
variance in conidial size and shape between collections from
different sites. According to his opinion, such morphological characters were much less reliable than ecological ones.
However, GUSTAVSSON (1959b) accepted GÄUMANN’S (1918,
1923) principle to take the host range as a basis for species
delimitation in Peronospora and advocated a narrow species
concept, too. Another tendency in Peronospora taxonomy was
to totally reject GÄUMANN’S (1918, 1923) ideas and to return
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84
to DE BARY’S (1863) original concept of merging all Peronosporas parasitizing members of the same host family. This
was exemplified by YERKES & SHAW (1959), who ascribed all
Peronospora specimens on Brassicaceae to a single species,
Peronospora parasitica.
Recently, CONSTANTINESCU & FATEHI (2002) presented
molecular and morphological evidence to split the genus Peronospora into three genera, Peronospora s. str., Hyaloperonospora, and Perofascia. Within Hyaloperonospora, six species
were accepted due to differences in morphology of conidia
and conidiophores, H. lunariae, H. floerkeae, H. lepidii-perfoliati, H. niessleana, H. tribulina, and H. parasitica. As far
as the latter should comprise the vast majority of Brassicaceae-infecting Peronosporas, the concept of these authors is
somewhat similar to that of YERKES & SHAW (1959). On the
other hand, CONSTANTINESCU & FATEHI (2002) stated that
the phenetic approach may suffer from limitations and that the
taxonomy of Peronospora „will be better tackled by using
molecular techniques“.
CONSTANTINESCU & FATEHI’S (2002) proposal to divide
Peronospora into three genera was confirmed by the molecular studies of GÖKER et al (2003) and VOGLMAYR (2003).
These authors found sequence differences within H. parasitica
as large as between the different Hyaloperonospora species
recognized by CONSTANTINESCU & FATEHI (2002) and concluded that H. parasitica s. l. should be split up according to
the phylogenetic relationships inferred from molecular results.
However, these molecular studies included a relatively small
sample of Hyaloperonospora species.
To get a more comprehensive picture, the present work focuses on Hyaloperonospora and Perofascia. More taxa and,
as far as possible, several specimens from the same host species were included. The internal transcribed spacer (ITS)
region of the nuclear rDNA was used to estimate phylogenetic relationships. Suitability of ITS for clarifying infrageneric relationships was demonstrated by FÖRSTER, CUMMINGS
& COFFEY (2000) and COOKE et al (2000) for Phytophthora,
MATSUMOTO et al (1999) for Pythium, and VOGLMAYR (2003)
for Peronospora.
Material and methods
Sample sources, DNA extraction, PCR, and sequencing
The organisms included in this study are listed in Table 1. The
nomenclature followed CONSTANTINESCU & FATEHI (2002), but
we used the narrow species concept of GÄUMANN (1918, 1923,
1926) for the species ascribed to Hyaloperonospora parasitica. In these cases we applied CONSTANTINESCU’S (1991) nomenclature, including the changes proposed by GÖKER et al.
(2003). Samples which could not unequivocally be assigned
to any of GÄUMANN’S species were named Hyaloperonospora
parasitica s. l. Microscopical examination of specimens was
carried out as previously described (GÖKER et al. 2003).
© DGfM 2004
GÖKER et al.: Phylogeny of Hyaloperonospora
DNA extraction, PCR, and cycle sequencing procedures
were performed acccording to RIETHMÜLLER et al. (2002). We
used the PCR and cycle sequencing primers described in
COOKE et al. (2000) and additionally ITS4-H (5’-TCC TCC
GCT TAT TAA TAT GC), a modification of ITS4. In case
very similar sequences were obtained from different host species or strikingly different sequences were found on specimens
from the same host species, the whole procedure was repeated,
starting with DNA extraction.
Data analysis
ITS sequences were assembled, checked and edited with Se-Al
version 2.0 (RAMBAUT 1996. Available from http://evolve.
zoo.ox.ac.uk/software). The corresponding nexus file was
edited in PAUP* version 4.0b10 (SWOFFORD 2002). The computer program MrBayes (version 3.0B; HUELSENBECK & RONQUIST 2001) was used to perform Metropolis-coupled Markov
chain Monte Carlo analyses (see HUELSENBECK et al. 2002 for
a recent survey) based on the general time reversible model
including gamma distributed substitution rates and a portion
of invariable sites (GTR+I+G; see SWOFFORD et al 1996). Four
incrementally heated simultaneous Markov chains were run
over 1 000 000 generations from which every 100th tree was
sampled. From these, the first 1000 trees were discarded.
MrBayes was used to compute a 50 % majority rule consensus (containing also compatible groupings with lower frequency) of the remaining trees to obtain estimates for the a
posteriori probabilities of groups of species. Branch lengths
were computed as mean values over the sampled trees. This
analysis was repeated five times on Macintosh G4 computers,
always starting with random trees and default parameter values to test whether the results were reproducible.
For neighbor-joining analysis (SAITOU & NEI 1987), the
data were first analysed with Modeltest version 3.04 (POSADA
& CRANDALL 1998) to find the most appropriate models of
DNA substitution, which were then used for calculation of
neighbor-joining trees in the BIONJ version of GASCUEL
(1997), using PAUP* (SWOFFORD 2002). Support for internal
nodes was estimated by bootstrap analysis (FELSENSTEIN 1985)
using 10 000 replicates.
In PAUP* (SWOFFORD 2002), a heuristic search under the
maximum parsimony criterion (e.g., FITCH 1971) was performed using 10 000 replicates with random addition of sequences and subsequent TBR branch swapping (MULTREES
option in effect, STEEPEST option not in effect), each replicate being limited to 100 000 rearrangements. A second search
strategy followed the parsimony ratchet approach (NIXON
1999) as implemented in PAUPRat (SIKES & LEWIS 2001)
using default values. No shorter trees than in the first approach
could be obtained. Gaps were treated as fifth state; a cost of 2
was assigned to transversions and a cost of 1 to transitions and
gap insertions. Bootstrap analysis with 1000 replicates (FELSENSTEIN 1985) was performed as in the first heuristic search
approach mentioned above, but this time using 20 rounds of
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Mycological Progress 3(2) / 2004
random sequence addition and subsequent branch swapping
during each bootstrap replicate. To compute Bremer decay indices (BREMER 1988), TreeRot version 2 (SORENSON 1999)
was used in conjunction with PAUP* with a search strategy
identical to that used for bootstrapping.
Results
Sequence alignment
The final length of the alignment was 1569 bp. However, the
total length was partly due to three large insertions in the ITS
2 region. An insertion from positions 650 to 994 in the final
alignment was present in the two specimens of P. lepidii-sativi and an insertion of similar length (base positions 1147 to
1445) in P. parasitica s. str., confirming the results of VOGLMAYR (2003). Peronospora brassicae f. sp. brassicae and P.
sisymbrii-loeselii were characterized by an insertion from position 1034 to 1104. All insertions were homologous to parts
of the proper ITS 2 (data not shown). After exclusion of these
large insertions, 854 bp remained for phylogenetic analysis.
The final alignment and the trees obtained have been deposited in TreeBASE (http://www.treebase.org/) as SN1750.
Bayesian analysis
Based on the results of CONSTANTINESCU & FATEHI (2002), the
phylogenetic trees were rooted with the three Perofascia specimens included in our sample that appeared as a well-separated, monophyletic group. A Perofascia-rooted majority-rule
consensus tree from Bayesian analysis is shown in Fig. 1. We
did not observe significant deviations in other consensus trees
obtained from the independent runs of Bayesian analysis.
The basal subdivision into Perofascia and Hyaloperonospora was highly supported by an a posteriori probability
of 100 % (Fig. 1). Within Hyaloperonospora, P. arabis-alpinae and a group containing specimens from Cardamine, Rorippa, Barbarea, and Arabis hosts separates basally, the latter
group with a support of 100 %. The remaining Hyaloperonospora specimens are distributed over a highly supported
cluster (95 %). Within the latter group, a sister group relationship of Hyaloperonospora niessleana to the other taxa is also
highly supported (100 %). For the remaining groups backbone resolution is relatively low, with high support mainly
restricted to assemblages of specimens from the same host
species. However, two clusters of 13 and 25 specimens, respectively, were highly supported by 100 % a posteriori probability and well resolved within. The latter cluster is composed
of an assemblage of specimens belonging to Peronospora dentariae, supported by 94 %, and a cluster containing Peronospora diplotaxidis, P. teesdaliae, P. cochleariae on Armoracia,
and Hyaloperonospora brassicae, H. lunariae, H. tribulina
and H. parasitica s. l. on Sisymbrium volgense. The P. diplotaxidis and H. brassicae specimens, respectively, did not cluster together. The second highly supported cluster is divided
into a group comprising Peronospora crispula, P. thlaspeosalpestris, Hyaloperonospora thlaspeos-perfoliati, and H. parasitica s. l. from Lepidium ruderale, supported by 100 % a
posteriori probability, and a poorly (64 %) supported cluster
containing P. arabidopsidis, P. erophilae, a P. cochleariae
specimen from Cochlearia danica, and P. cardaminopsidis.
Neighbor joining
The application of Modeltest version 3.04 proposed the models HKY+G or TVM+I+G (see SWOFFORD et al 1996 for a
survey of these DNA substitution models) using likelihood
ratio tests or the Akaike information criterion, respectively.
Most parts of tree topologies resulting from neighbor-joining
analysis based on HKY+G or TVM+I+G, respectively, especially branches which obtained high bootstrap support, were
in agreement with the results from Bayesian inference (data
not shown).
Maximum parsimony
Heuristic maximum parsimony analysis yielded 51 316 most
parsimonious trees of length 1551 from 854 islands; the consistency index of these was 0.5152 (0.4987 when uninformative characters were excluded) and the retention index (FARRIS
1989) 0.8764. The strict consensus tree of the most parsimonious trees is shown in Fig. 2. The consensus is topologically
similar to the Bayesian tree, and most of the above-mentioned
highly supported groups are present in parsimony analysis, too.
Discussion
Relations between parasite phylogeny and taxonomy
of brassicacean hosts
In general, specimens from the same host species appeared in
the same cluster, displaying only few or no sequence differences. Exceptions were the specimens from horseradish (Armoracia rusticana) that clustered together with specimens from
Brassica napus or Sinapis arvensis, respectively, and the specimens of Diplotaxis tenuis, which appeared closely related
to Peronospora lobulariae or P. brassicae, respectively. The
Hyaloperonospora sequence from Lepidium ruderale originated from a coinfection together with Perofascia lepidii. Both
Hyaloperonospora- and Perofascia-like haustoria and conidiophores were observed on the heavily distorted host stems
and leaves (data not shown).
Collections from the same host genus but different host
species did not always cluster together. For instance, the specimens from Cardamine impatiens and C. bulbifera are widely separated from the parasites of C. flexuosa, C. amara, C.
hirsuta, and C. pratensis. Likewise, the collection from Sisymbrium volgense seems to be only distantly related to the
specimens from S. officinale and S. loeselii. The Hyaloperonospora specimens from Arabis alpina and A. soyeri were not
revealed as sister groups, either.
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GÖKER et al.: Phylogeny of Hyaloperonospora
Fig. 1: 50 % majority-rule consensus tree with mean branch lengths including also compatible groupings of lower frequencies
from a Bayesian Markov chain Monte Carlo analysis of nuclear ITS data. Numbers on branches represent their respective a
posteriori probabilities. Probability values below 50 % are not shown. H. = Hyaloperonospora, P. = Peronospora, C. = Cardamine, R. = Rorippa, L. = Lepidium.
© DGfM 2004
Mycological Progress 3(2) / 2004
87
Fig. 2: Maximum parsimony analysis of the ITS data set. A strict consensus tree of 51 316 trees of length 1551 found in heuristic search is shown. Numbers above branches are bootstrap values from 1000 replicates, numbers below branches represent
Bremer support indices. Abbreviations are as in Fig. 1. Suggested species boundary in accordance with GÄUMANN’S (1918,
1923) taxonomy (■), suggested species boundary in disagreement with GÄUMANN’S views (×), species delimitations can not be
inferred from phylogenetic trees with certainty (❍).
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88
Other discrepancies between parasite phylogeny and current host taxonomy may be due to flaws of the latter. For instance, the parasites of Thlaspi, H. thlaspeos-perfoliati and P.
thlaspeos-alpestris on the one hand and P. thlaspeos-arvensis
on the other hand, are not closely related, but Thlaspi seems to
be a non-monophyletic assemblage (KOCH & MUMMENHOFF
2001). The downy mildew on horseradish had been assigned
to P. cochleariae as Armoracia rusticana was first described
as Cochlearia armoracia, but already VON HAYEK (1911)
doubted whether Armoracia and Cochlearia are closely related at all. Hence, the loose relationship between the P. cochleariae specimens from Armoracia rusticana and Cochlearia danica, respectively, does not imply incongruence between host
and parasite phylogenies (see also GUSTAVSSON 1959a).
Inferring conclusions about relations between host and parasite phylogeny in the Hyaloperonospora-Brassicaceae complex is difficult as host taxonomy so far was mainly based on
JANCHEN’S (1942) morphological system. Recent molecular
studies in Brassicaceae reported striking differences (e.g.,
MUMMENHOFF, FRANZKE & KOCH 1997, KOCH, BISHOP &
MITCHELL-OLDS 1999) between phylogenetic trees inferred
from DNA data and classical hypotheses derived from morphology. However, these articles mainly focused on infratribal (e.g., MUMMENHOFF, BRÜGGEMANN & BOWMAN 2001) or
interfamiliar relationships (e.g., HALL, SYTSMA & ILTIS 2002).
Hypotheses about the degree of congruence between host and
Hyaloperonospora phylogenetic trees is further complicated
by the partial lack of backbone resolution in the latter. However, as high support of terminal branches was achieved in all
phylogenetic methods applied, conclusions can be drawn with
respect to the different species concepts for Hyaloperonospora
found in the literature.
ITS phylogenies and species concepts
Considering genetic distances our data do not support the view
of DE BARY (1863) to merge all Peronospora specimens growing on members of the same host family into a single species.
As already demonstrated by VOGLMAYR (2003), H. tribulina,
a parasite of Tribulus (Zygophyllaceae), is nested within Brassicaceae-infecting members of Hyaloperonospora. A similar
situation is found in P. crispula found on Reseda (Resedaceae),
which is closely related to Hyaloperonospora specimens from
Thlaspi and Lepidium. Taxonomic inconsistencies caused by
different classifications of P. crispula following DE BARY
(1863) were already emphasized by GÄUMANN (1918).
Hyaloperonospora parasitica sensu CONSTANTINESCU &
FATEHI (2002) is not a monophyletic assemblage. Instead, H.
lunariae, H. niessleana and H. tribulina, which were regarded
as separate species by these authors are nested within H. parasitica s. l. The present results confirm the opinion of VOGLMAYR (2003) and GÖKER et al (2003) that molecular data concur with narrow species delimitations in Hyaloperonospora.
The lack of morphological differences between several Hyaloperonospora specimens (CONSTANTINESCU and FATEHI 2002)
© DGfM 2004
GÖKER et al.: Phylogeny of Hyaloperonospora
does not necessarily imply that they belong to the same species. Our suggestions for species boundaries in accordance
with this point of view are depicted in Fig. 2. In the case of
Peronospora buniadis, genetic distances do not reveal with
certainty whether it should be regarded as conspecific with P.
hesperidis. Similarly, it remains unclear whether or not the
two specimens of P. thlaspeos-alpestris included in our sampling represent a monophyletic grouping.
At first sight, molecular support for narrow species circumscriptions seems to be in accordance with GÄUMANN’S
(1918, 1923) taxonomical proposals. However, several parts
of the phylogenetic trees derived from ITS sequences disagree
with his arrangements (Fig. 2). For example, GÄUMANN (1918)
ascribed Hyaloperonospora specimens occurring on Erysimum crepidifolium to P. erysimi. Instead, the genetic distance
between our collection from that host and the P. cheiranthi
specimen is negligible (FIGS. 1, 2). Molecular trees support
the view that the Hyaloperonospora specimens from Cardamine impatiens do not belong to P. dentariae as suggested by
GÄUMANN (1923). Instead, the P. nasturtii-aquatici sample is
nested within the P. dentariae cluster. Our results are not necessarily in conflict with presumable host ranges derived from
GÄUMANN’S (1918, 1923) cross-infection experiments with
Erysimum and Cheiranthus as host genera, since he did not
include E. crepidifolium, nor did he use conidia from C. impatiens or Nasturtium officinale to inoculate other Cardamine
species. On the other hand, the phylogenetic trees presented
here support GUSTAVSSON’S (1959b) opinion that GÄUMANN
(1918, 1923) partly overestimated differences in conidial morphology.
In his 1926 work, GÄUMANN recognized three formae speciales within Peronospora brassicae – a species which was
erected by him in 1918 –, namely f. sp. brassicae, f. sp. sinapidis, and f. sp. raphani. Whereas in infection experiments f.
sp. brassicae seemed to be confined to some members of the
genus Brassica, f. sp. sinapidis and f. sp. raphani displayed a
limited ability to infect Brassica and thus were mainly restricted to Sinapis and Raphanus, respectively (GÄUMANN
1926). These results were confirmed by HIURA & KANEGAE
(1934), MCMEEKIN (1969) and DICKINSON & GREENHALGH
(1977) who found a susceptibility of Brassica species and varieties to conidia from Raphanus but not vice versa. FOSTER’S
(1947) experiments revealed high resistance in both mustard
and radish varieties after inoculation with conidia from cabbage. These ecological differences are in agreement with our
molecular results, since the Hyaloperonospora specimens
from Brassica, Sinapis, and Raphanus, respectively, show distinct differences in ITS sequences (Fig. 1). Furthermore,
strong support is achieved that H. brassicae represents a nonmonophyletic assemblage. If the narrow species concept advocated here is applied, the formae speciales of H. brassicae
should be regarded as three separate species.
Among the different species concepts in Hyaloperonospora, that of GUSTAVSSON (1959b), emphasizing host range
and applying narrow species delimitation, is most congruent
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Mycological Progress 3(2) / 2004
with the results from molecular phylogenetic inference. However, the Hyaloperonospora specimens from Diplotaxis tenuis
had marked differences in ITS sequences (Fig. 1). Likewise,
horseradish (Armoracia rusticana) seems to be susceptible to
both Peronospora brassicae f. sp. brassicae and P. brassicae
f. sp. sinapidis. It may be concluded that Hyaloperonospora
species are not necessarily confined to closely related host
plants and that some host species are susceptible to several
Hyaloperonospora species. However, further studies are required to reveal whether the molecular results presented here
corroborate this hypothesis or whether they represent an example of reticulate evolution (e.g., LEGENDRE 2000) leading
to differences between gene trees and species trees.
Taxonomic implications of the current study
Hyaloperonospora isatidis (Gäumann) Göker, Riethmüller, Voglmayr, Weiß & Oberwinkler, comb. nov.
= Peronospora isatidis Gäumann – Beihefte zum Botanischen Centralblatt 35(1): 526, 1918 (basionym).
Hyaloperonospora hesperidis (Gäumann) Göker, Riethmüller, Voglmayr, Weiß & Oberwinkler, comb. nov.
= Peronospora hesperidis Gäumann – Beihefte zum Botanischen
Centralblatt 35(1): 525, 1918 (basionym).
Hyaloperonospora thlaspeos-arvensis (Gäumann) Göker,
Riethmüller, Voglmayr, Weiß & Oberwinkler, comb. nov.
= Peronospora thlaspeos-arvensis Gäumann – Beihefte zum Botanischen Centralblatt 35(1): 530, 1918 (basionym).
Hyaloperonospora cheiranthi (Gäumann) Göker, Riethmüller, Voglmayr, Weiß & Oberwinkler, comb. nov.
= Peronospora cheiranthi Gäumann – Beihefte zum Botanischen
Centralblatt 35(1): 524, 1918 (basionym).
For Hyaloperonospora species not listed in CONSTANTINESCU
& FATEHI (2002), nor in GÖKER et al (2003), nor below, we
suggest the use of „Hyaloperonospora parasitica s. l.“. Whereas molecular analyses support a narrow species concept,
sequence data are not always in agreement with the species
boundaries proposed by GÄUMANN (1918, 1923; cf. FIG 2).
Where such discrepancies occur, further studies are necessary
to achieve a natural classification. However, in many cases
sequence analysis agrees with classical taxonomy (Fig. 2), and
it is appropriate to propose the following new combinations:
According to § 32.5 of the International Code of Botanical
Nomenclature (GREUTER et al 1999) we adjusted the epithets
“arabidopsidis” and “cardaminopsidis” to their correct Latin
termination following STEARN (1992) and ZABINKOVA (1968).
Hyaloperonospora crispula (Fuckel) Göker, Riethmüller,
Voglmayr, Weiß & Oberwinkler, comb. nov.
Acknowledgements
= Peronospora crispula Fuckel – Fungi rhenani 23, 1863 (basionym).
Hyaloperonospora arabidopsis (Gäumann) Göker, Riethmüller, Voglmayr, Weiß & Oberwinkler, comb. nov.
= Peronospora arabidopsidis Gäumann – Beihefte zum Botanischen
Centralblatt 35(1): 529, 1918 (basionym).
Hyaloperonospora cardaminopsis (Gustavsson) Göker,
Riethmüller, Voglmayr, Weiß & Oberwinkler, comb. nov.
= Peronospora cardaminopsidis Gustavsson – Opera Botanica 3(1):
105, 1959 (basionym).
Hyaloperonospora barbareae (Gäumann) Göker, Riethmüller, Voglmayr, Weiß & Oberwinkler, comb. nov.
= Peronospora barbareae Gäumann – Beihefte zum Botanischen
Centralblatt 35(1): 521, 1918 (basionym).
The authors are grateful to H. Jage (Kemberg, Germany) and
W. Dietrich (Annaberg-Buchholz, Germany) for providing
herbarium specimens. The present paper is part of the GLOPP
(Global Information System for the Biodiversity of Plant Pathogenic Fungi) project financed by the Bundesministerium
für Bildung und Forschung (BMBF), which is gratefully acknowledged.
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© DGfM 2004
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Accepted: 26.1.2004
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Mycological Progress 3(2) / 2004
Tab. 1: Collection data of the taxa studied and GenBank accession numbers of the respective ITS sequences. The taxa were
grouped taxonomically; the classification follows CONSTANTINESCU (1991) including some changes proposed in CONSTANTINESCU & FATEHI (2002) and GÖKER et al (2003), respectively. Collectors: HJ, H. Jage; WD, W. Dietrich; OF, O. Foitzik; HV,
H. Voglmayr; MG, M. Göker. Vouchers: M, Botanische Staatssammlung Munich, TUB, University of Tübingen; WU, University of Vienna. Hosts differing from the type hosts are marked with a star
Taxon
Collection data
Host
Origin/source/collector
Collection number/
DNA isolation number
GenBank
accession
no.
H. brassicae (Gäumann)
Göker et al. f. sp. brassicae
Brassica napus L.
ssp. napus 1
Germany, Sachsen-Anhalt,
Prettin; leg HJ
J 3675/01; 24-8 (TUB)
AY531409
H. brassicae f. sp. brassicae
Brassica napus L.
ssp. napus 2
Germany, Sachsen-Anhalt,
Kohnberg; leg HJ
J 795/01; 26-9 (TUB)
AY531407
H. brassicae f. sp. raphani
Raphanus
raphanistrum L.
Germany, Baden-Württemberg, Tübingen; leg. MG
1858; 14-8 (TUB)
AY531413
H. brassicae f. sp. sinapidis
Sinapis alba L. 1
Germany, Baden-Württemberg, Tübingen; leg. MG
1866, 14-3 (TUB)
AY531403
H. brassicae f. sp. sinapidis
Sinapis alba L. 2
Germany, Baden-Württemberg, Niedernhall; leg. MG
1868; 15-4 (TUB)
AY531404
H. camelinae (Gäumann)
Göker et al.
Camelina sativa (L.)
Cr. 1 *
Austria, Upper Austria,
St. Willibald; leg. HV
HV 444-447; 21-6
(WU)
AY531456
H. camelinae
Camelina sativa (L.)
Cr. 2 *
Austria, Burgenland, Kittsee;
leg. HV
HV 14 (WU)
AY531457
H. erophilae (Gäumann)
Göker et al.
Erophila verna (L.)
Chev. 1
Germany, Bavaria, Munich;
leg. MG
1883; 17-5 (TUB)
AY531439
H. erophilae
Erophila verna (L.)
Chev. 2
Germany, Baden-Württemberg, Criesbach; leg. MG
1961; 19-4 (TUB)
AY531440
H. lunariae (Gäumann)
Constantinescu
Lunaria rediviva L. 1
Germany, Bavaria, Munich;
leg. MG
1946; 18-10 (TUB)
AY531402
H. lunariae
Lunaria rediviva L. 2
Austria, Lower Austria,
Lilienfeld; leg. HV
HV 362 (WU)
AY531401
H. niessleana (Berlese)
Constantinescu
Alliaria petiolata (Bieb.)
Cavara & Grande 1
Germany, Baden-Württemberg, Tübingen; leg. MG
1843; 4-1 (TUB)
AY531465
H. niessleana
Alliaria petiolata (Bieb.)
Cavara & Grande 2
Austria, Vienna; leg. HV
HV 575 (WU)
AY531464
H. parasitica (Persoon:
Fries) Constantinescu
Capsella bursapastoris (L.) Med. 1
Austria, Lower Austria,
Pfaffstätten; leg. HV
HV 746 (WU)
AY531451
H. parasitica
Capsella bursapastoris (L.) Med. 2
Germany, Baden-Württemberg, Criesbach; leg. MG
1964; 19-1 (TUB)
AY531452
H. parasitica s. l.
Arabis soyeri Reut. &
Huet*
Austria, Carinthia, Flattach;
leg. HV
HV 508-510 (WU)
AY531392
H. parasitica s. l.
Lepidium ruderale L.*
Germany, Sachsen-Anhalt,
Wendelsheim; leg HJ
J 3189/01; 22-8 (TUB)
AY531446
H. parasitica s. l.
Sisymbrium volgense
Bieb. ex E. Fournier*
Germany, Sachsen-Anhalt,
Langenbogen; leg HJ
J 661/01; 24-2 (TUB)
AY531426
H. thlaspeos-perfoliati
(Gäumann) Göker et al.
Thlaspi perfoliatum L. 1
Germany, Baden-Württemberg, Niedernhall; leg. MG
1882; 17-4 (TUB)
AY531431
H. thlaspeos-perfoliati
Thlaspi perfoliatum L. 2
Germany, Baden-Württemberg, Öschingen; leg. MG
1879; 17-9 (TUB)
AY531432
H. tribulina (Passerini)
Constantinescu
Tribulus terrestris L.
Hungary, Bacs-Kiskun,
Lakitelek/Tisza; leg. HV
HV 692 (WU)
AY531414
Arabidopsis thaliana
(L.) Heynh. 1
Germany, Baden-Württemberg, Kreßbach; leg. MG
1880; 17-1 (TUB)
AY531441
Hyaloperonospora
Peronospora
P. arabidopsidis Gäumann
© DGfM 2004
92
GÖKER et al.: Phylogeny of Hyaloperonospora
Tab. 1: Continued
Taxon
Collection data
Host
Origin/source/collector
Collection number/
DNA isolation number
GenBank
accession
no.
P. arabidopsidis
Arabidopsis thaliana
(L.) Heynh. 2
Germany, Sachsen-Anhalt,
Tornau; leg HJ
J 635/01; 24-4 (TUB)
AY531434
P. arabis-alpinae Gäumann
Arabis alpina L.
Austria, Lower Austria; leg.
HV
HV 408 (WU)
AY531466
P. barbareae Gäumann
Barbarea vulgaris
R. Br. 1
Austria, Tyrol, Schattwald;
leg. MG
1862; 13-6 (TUB)
AY531395
P. barbareae
Barbarea vulgaris
R. Br. 2
Germany, Saxonia,
Wolkenstein; leg. WD
D 21/4/00; 20-10 (TUB)
AY531396
P. berteroae Gäumann
Berteroa incana (L.)
DC. 1
Germany, Saxonia,
Gohlis; leg HJ
J 1165a/01; 23-8 (TUB)
AY531450
P. berteroae
Berteroa incana (L.)
DC. 2
Germany, Sachsen-Anhalt,
Prettin; leg HJ
J 3697/01; 24-6 (TUB)
AY531449
P. buniadis Gäumann
Bunias orientalis L.
Austria, Lower Austria,
Traismauer; leg. HV
HV 969-971; 27-5 (WU)
AY531453
P. cardamines-laciniatae
Gäumann
Cardamine bulbifera
(L.) Cr. 1
Austria, Lower Austria,
Gießhübl; leg. HV
HV 77-80; 21-2 (WU)
AY531399
P. cardamines-laciniatae
Cardamine bulbifera
(L.) Cr. 2
Austria, Lower Austria,
Kaltenleutgeben; leg. HV
HV 151-152; 21-5 (WU)
AY531398
P. cardaminopsidis A.
Gustavsson
Cardaminopsis
arenosa (L.) HAY.
Germany, Saxonia,
Plattenthal; leg. WD
D 23/7/97; 20-3 (TUB)
AY531435
P. cheiranthi Gäumann
Erysimum cheiri (L.)
Cr.
Germany, Sachsen-Anhalt,
Plossig; leg HJ
J 3786/01; 22-3 (TUB)
AY531460
P. cochleariae Gäumann
Armoracia rusticana
G.M. Sch. 1*
Austria, Upper Austria,
Raab; leg. HV
HV 1006-1008; 21-11 (WU) AY531406
P. cochleariae
Armoracia rusticana
G.M. Sch. 2*
Germany, Sachsen-Anhalt,
Deichhaus; leg HJ
J 3914a/01; 23-9 (TUB)
AY531405
P. cochleariae
Armoracia rusticana
G.M. Sch. 3*
Germany, Baden-Württemberg, Welschingen; leg HJ
J 2520/01; 26-10 (TUB)
AY531408
P. cochleariae
Cochlearia danica L.
Germany, Sachsen-Anhalt,
Teutschenthal; leg HJ
J 672/01; 24-1 (TUB)
AY531442
P. crispula Fuckel
Reseda lutea L. 1*
Austria, Burgenland, Apetlon;
leg. HV
HV 1028-1030; 21-12 (WU) AY531437
P. crispula
Reseda lutea L. 2*
Germany, Sachsen-Anhalt,
Wittenberg; leg HJ
J 1875/01; 22-12 (TUB)
AY531438
P. dentariae Rabenhorst
Cardamine amara L.*
Czech Republic, Krusne Hory,
Krystofovy Hamry; leg. WD
D 25/5/99; 20-8 (TUB)
AY531420
P. dentariae
Cardamine flexuosa
With. 1*
Czech Republic, Krusne Hory,
Vejprty; leg. WD
D 24/4/99; 20-4 (TUB)
AY531418
P. dentariae
Cardamine flexuosa
With. 2*
Germany, Baden-Württemberg, Tübingen; leg HV
HV 833-834; 21-8 (WU)
AY531423
P. dentariae
Cardamine hirsuta
L. 1*
Germany, Baden-Württemberg, Tübingen; leg. HV
HV 791; 21-7 (WU)
AY531422
P. dentariae
Cardamine hirsuta
L. 2*
Germany, Nordrhein-Westfalen, Wuppertal; leg. MG
1821; 5-1, 5-8 (TUB)
AY531421
P. dentariae
Cardamine impatiens
L. 1*
Austria, Tyrol, Schattwald;
leg. MG
1840; 13-10 (TUB)
AY531400
P. dentariae
Cardamine impatiens
L. 2*
Germany, Baden-Württemberg, Tübingen; leg. MG
1939; 18-6 (TUB)
AY531397
P. dentariae
Cardamine pratensis
L.*
Germany, Baden-Württemberg, Niedernhall; leg. MG
1885; 17-8 (TUB)
AY531417
P. aff. dentariae
Cardamine (Dentaria)
sp.*
USA, Tennessee, Great
Smoky Mts Natl. Park; leg. HV
HV 2.4.P.P.; 21-1 (WU)
AY531424
© DGfM 2004
93
Mycological Progress 3(2) / 2004
Tab. 1: Continued
Taxon
Collection data
Host
Origin/source/collector
Collection number/
DNA isolation number
GenBank
accession
no.
P. diplotaxidis Gäumann
Diplotaxis tenuifolia
(L.) DC. 1
Germany, Sachsen-Anhalt,
Wittenberg; leg. HJ
J 3073/01; 23-11 (TUB)
AY531412
P. diplotaxidis
Diplotaxis tenuifolia
(L.) DC. 2
Germany, Sachsen-Anhalt,
Dessau; leg HJ
J 4011/01; 26-12 (TUB)
AY531411
P. erysimi Gäumann
Erysimum crepidifolium
Germany, Sachsen-Anhalt,
Könnern; leg HJ
J 1156/01; 26-8 (TUB)
AY531459
P. galligena Blumer
Aurinia saxatilis (L.)
Desv. 1
Germany, Bavaria, Munich;
leg. MG
1942; 18-3 (TUB)
AY531448
P. galligena
Aurinia saxatilis (L.)
Desv. 2
Germany, Baden-Württemberg, Eichstetten; leg. MG
2099; 20-12 (TUB)
AY531447
P. hesperidis Gäumann
Hesperis matronalis
L. 1
Czech Republic, Krusne Hory,
Potucky; leg. WD
D 19/5/00; 20-6 (TUB)
AY531455
P. hesperidis
Hesperis matronalis
L. 2
Germany, Sachsen-Anhalt,
Klein-Wanzleben; leg HJ
J 589/01; 23-6 (TUB)
AY531454
P. iberidis Gäumann
Iberis sempervirens
L.*
Germany, Sachsen-Anhalt,
Rachilk; leg HJ
J 3514/01; 22-6 (TUB)
AY531461
P. isatidis Gäumann
Isatis tinctoria L.
Germany, Sachsen-Anhalt,
Rollesdorf; leg HJ
J 928/01; 22-5 (TUB)
AY531443
P. lepidii-sativi Gäumann
Cardaria draba (L.)
Desv. 1
Austria, Burgenland, Kittsee;
leg. HV
HV 115-116; 21-3 (WU)
AY531462
P. lepidii-sativi
Cardaria draba (L.)
Desv. 2
Austria, Lower Austria,
Guntramsdorf; leg. HV
HV 246 (WU)
AY531463
P. lobulariae Ubriszy &
Vörös
Lobularia maritima
(L.) Desv.
Germany, Sachsen-Anhalt,
Arendsee; leg HJ
J 3454/01; 22-10 (TUB)
AY531410
P. nasturtii-aquatici
Gäumann
Nasturtium officinale
R. Br.
Germany, Sachsen-Anhalt,
Sülldorf; leg HJ
J 3493/01; 24-3 (TUB)
AY531419
P. nesliae Gäumann
Neslia paniculata
(L.) Desv.
Austria, Lower Austria,
Theresienfeld; leg HV
HV 203 (WU)
AY531458
P. rorippae-islandicae
Gäumann
Rorippa islandica
(Gunnerus) Borbas
Germany, Thüringen,
Stadtroda; leg. OF
20-2 (M)
AY531393
P. rorippae-islandicae
Rorippa palustris (L.)
Bess.*
Germany, Saxonia;
Marienberg; leg. WD
D 15/6/97; 20-1 (TUB)
AY531394
P. sisymbrii-loeselii
Gäumann
Sisymbrium loeselii
L. 1
Germany, Sachsen-Anhalt,
Köthen; leg HJ
J 73/01; 23-5 (TUB)
AY531428
P. sisymbrii-loeselii
Sisymbrium loeselii
L. 2
Germany, Sachsen-Anhalt,
Heuckewalde; leg HJ
J 243/01; 23-10 (TUB)
AY531427
P. sisymbrii-officinalis
Gäumann
Sisymbrium officinale
(L.) Scop.
Austria, Upper Austria,
Raab; leg. HV
HV 1003-1005; 21-10 (WU) AY531425
P. sisymbrii-sophiae
Gäumann
Descurainia sophia
(L.) Webb ex Prantl 1
Austria, Lower Austria,
Weiden; leg. HV
HV 150; 21-4 (WU)
AY531429
P. sisymbrii-sophiae
Descurainia sophia
(L.) Webb ex Prantl 2
Austria, Lower Austria,
Hundsheim; leg. HV
HV 276 (WU)
AY531430
P. teesdaliae Gäumann
Teesdalia nudicaulis
(L.) R. Br. 1
Germany, Saxonia,
Zschepa; leg HJ
J 1186/01; 23-2 (TUB)
AY531415
P. teesdaliae
Teesdalia nudicaulis
(L.) R. Br. 2
Germany, Bavaria, Markt
Pleinfeld; leg HJ
J 1243/01; 23-4 (TUB)
AY531416
P. thlaspeos-alpestris
Gäumann
Thlaspi caerulescens
J. & C. Presl 1
Germany, Saxonia, Oberummersdorf; leg HJ
J 450/01; 22-11 (TUB)
AY531436
P. thlaspeos-alpestris
Thlaspi caerulescens
J. & C. Presl 2
Czech Republic, Krusne Hory,
Vejprty; leg. WD
D 24/4/99; 20-5 (TUB)
AY531433
P. thlaspeos-arvensis
Gäumann
Thlaspi arvense L. 1
Germany, Baden-Württemberg, Niedernhall; leg. MG
1852; 15-1 (TUB)
AY531444
© DGfM 2004
94
GÖKER et al.: Phylogeny of Hyaloperonospora
Tab. 1: Continued
Taxon
Origin/source/collector
Collection number/
DNA isolation number
GenBank
accession
no.
Thlaspi arvense L. 2
Austria, Upper Austria, St.
Willibald; leg. HV
HV 762 (WU)
AY531445
Perofascia lepidii (Mac
Alpine) Constantinescu
Lepidium ruderale L. 1
Germany, Sachsen-Anhalt,
Wendelsheim; leg HJ
J 3189/01; 22-8 (TUB)
AY531468
Perofascia lepidii
Lepidium ruderale L. 2
Germany, Sachsen-Anhalt,
Röden; leg. HJ
J 2068/01; 22-9 (TUB)
AY531467
Perofascia lepidii
Lepidium densiflorum
Schrader*
GenBank/CONSTANTINESCU &
FATEHI (2002)
P. thlaspeos-arvensis
Collection data
Host
Perofascia
© DGfM 2004
AF465760