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Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4
Jan Kohlmeyer
Brigitte Volkmann-Kohlmeyer
Institute of Marine Sciences, University of North Carolina at Chapel Hill, Morehead City, North Carolina 28557
Mary L. Berbee
Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4
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ABSTRACT |
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In this paper, we investigate the phylogenetic placement of Pleospora gaudefroyi using partial SSU as well as ITS ribosomal DNA sequences. Both SSU and ITS data sets agreed in the placement of P. gaudefroyi. Parsimony and neighbor-joining analyses of each data set placed P. gaudefroyi within the Pleosporaceae with 100% bootstrap support. Pleospora gaudefroyi was sister taxon in the Pleosporaceae represented by Alternaria alternata, Cochliobolus sativus, Pleospora herbarum, Pyrenophora tritici-repentis and Setosphaeria rostrata. Pleospora gaudefroyi was separated from other genera in the Pleosporaceae in 94% of the bootstrap replicates in parsimony and neighbor-joining analyses. When P. gaudefroyi was constrained to monophyly with P. herbarum, all resulting trees were significantly worse than the optimal tree in both Kishino-Hasegawa and Shimodaira-Hasegawa tests. Pleospora gaudefroyi was therefore excluded from Pleospora, and transferred to the new genus Decorospora placed in the Pleosporaceae. Decorospora (Dothideomycetes) has characteristic ascospores enclosed in a sheath with 4–5 apical extensions. The distribution and substrate types for D. gaudefroyi are summarized and updated based on additional collections.
Key words: Dothideomycetes, Loculoascomycetes, marine mycology, Pleosporaceae, Pleosporales, Shimodaira-Hasegawa Tests
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONTAXONOMYLITERATURE CITED |
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). Ascospores in P. gaudefroyi produce a characteristic gelatinous sheath that is thought to be exosporial in origin, having a tripartite outer boundary (Yusoff et al 1994). Upon release from the ascus, this hyaline layer swells once in contact with water, and transforms into a thick sheath, generally bearing two extensions at each polar region of the ascospores. One pair of extensions is formed on either side of the pole in a plane through the long axis of the ascospore. The planes stand at a 90° angle to each other, so that in side view only three of the extensions are visible. They are about as wide and long as the ascospore, and taper towards the apex (Kohlmeyer 1962).
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). However, even though Pleospora herbarum and P. gaudefroyi are morphologically similar, an anamorph is unknown for P. gaudefroyi, and P. herbarum ascospores lack the sheath characteristic of P. gaudefroyi. Kohlmeyer (1962) reestablished P. gaudefroyi, arguing that the presence of the ascospore sheath with its apical extensions, as well as the marine habitat of P. gaudefroyi, are sufficient to keep it separate from P. herbarum. In this study, we use phylogenetic analyses of partial SSU and ITS ribosomal DNA sequences to investigate the following questions: Are P. gaudefroyi and P. herbarum conspecific, congeneric, or should they be placed in distinct genera? In case P. gaudefroyi cannot be retained in Pleospora, in which genus should it be placed?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONTAXONOMYLITERATURE CITED |
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. We obtained the culture from the Centraalbureau voor Schimmelcultures (CBS), Baarn, The Netherlands (CBS 332.63), where it had been deposited in 1963 by J. Kohlmeyer. DNA was isolated with a standard phenol-chloroform extraction (Lee and Taylor 1990) from mycelium scraped off a PDA Petri dish. The SSU ribosomal DNA region was PCR amplified by NS1 and cITS5, the complement to ITS5 (White et al 1990). Sequencing reactions were performed with an ABI Prism BigDye Terminator Cycle Sequencing Ready Reaction Kit (PE Biosystems, Mississauga, Canada) using NS1, NS2, and cITS5 (White et al 1990), NS19 (Gargas and Taylor 1992), MB1, MB2, and Bas3 (Inderbitzin et al 2001). The ITS ribosomal DNA region was PCR amplified and sequenced by ITS4 / ITS5 (White et al 1990). Sequences were determined automatically on an ABI 377XL Automatic Sequencer (Perkin Elmer Corp., Norwalk, Connecticutt, USA), and assembled in AutoAssembler Version 1.4 (Applied Biosystems, Perkin Elmer Corp., Norwalk, Connecticutt, USA).
Phylogenetic analyses of SSU rDNA data sets –
In a BLAST search, the SSU ribosomal DNA (SSU rDNA) sequence of Pleospora gaudefroyi had highest percentage similarity to species of Pyrenophora, Cochliobolus, Pleospora, Setosphaeria, and Alternaria, in that order. A representative of each of these genera was included in the phylogenetic analyses. The remainder of the taxa retrieved from GenBank were chosen to represent the monophyletic sister group to Rhytidhysteron rufulum (Winka and Eriksson 1998, Liew et al 2000). Thus, a total of 27 partial SSU rDNA sequences were retrieved from GenBank (Table I). The sequences were manually aligned with the homologous sequence of Pleospora gaudefroyi using Se-Al v1.d1 (Rambaut 1999). The resulting data matrix contained 28 taxa and 1720 characters. The following 14 sequences were approximately 1060 bp in length: Trematosphaeria hydrela, Mycosphaerella citrullina, Sporormiella australis, Pseudotrichia aurata, Pleomassaria siparia, Phaeodothis winteri, Montagnula opulenta, Massariosphaeria phaeospora, Melanomma pulvis-pyrius, Massarina australiensis, Massaria platani, Leptospora rubella, Didymella exigua, and Delitschia winteri. The sequence of Rhytidhysteron rufulum was approximately 1600 bp in length, whereas the remaining 13 sequences, including P. gaudefroyi, were around 1700 bp long. The data matrix was analysed in PAUP* 4.0b3 (Swofford 2001) using parsimony and neighbor-joining with default settings, unless noted otherwise. Rhytidhysteron rufulum was used as outgroup. This alignment was submitted to TreeBase (M1158).
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): Out of 378 possible pairwise comparisons for the 28 taxa, 13 were above 0.05 substitutions per site. The maximal estimated pairwise distance was 0.058 substitutions per site between P. gaudefroyi and Phaeodothis winteri. Bootstrap support for the branches was based on 500 replicates with random taxon addition. The parsimony-based Kishino-Hasegawa test was applied using default settings in PAUP* (Swofford 2001).
For computational reasons, a smaller data set comprising the taxa of the Pleosporaceae (Alternaria alternata, Cochliobolus sativus, Pleospora herbarum, Pyrenophora tritici-repentis, Setosphaeria rostrata) and P. gaudefroyi was used in the likelihood-based, non-parametric Shimodaira-Hasegawa tests (SHT) as implemented in the program SHTests v1.0 (Rambaut 2000). A Jukes-Cantor model of evolution was used. The number of bootstrap replicates was 500. The topology of the most likely tree needed for the SHT was obtained in PAUP* (Swofford 2001) using a Jukes-Cantor model of evolution.
Phylogenetic analyses of the ITS rDNA data set –
Species of Alternaria were closest matches to the ITS ribosomal DNA (ITS rDNA) sequence of P. gaudefroyi in a BLAST search. Clustal W (1.74) (Thompson et al 1994) was used for aligning the P. gaudefroyi ITS rDNA sequence with homologous regions from the following taxa retrieved from GenBank (Table I): Alternaria alternata, Cochliobolus sativus, two different sequences named Leptosphaeria maculans, Pleospora herbarum, Pyrenophora tritici-repentis, and Setosphaeria rostrata. The resulting data set contained 8 taxa and 625 characters. Parsimony analyses were performed as described for the large SSU rDNA data set. Leptosphaeria maculans (M96384) was used as outgroup.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONTAXONOMYLITERATURE CITED |
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This study focused on the placement of P. gaudefroyi, which in both MP and neighbor-joining (NJ) trees was unambiguous: Pleospora gaudefroyi grouped with 100% support as the sister group to the Pleosporaceae (Fig. 5). The monophyly of the Pleosporaceae without P. gaudefroyi was supported by 94% bootstrap support in both MP and NJ analyses. Outside the P. gaudefroyi-Pleosporaceae group, at a 60% bootstrap support-level, the branching order of the NJ tree did not contradict results obtained in other studies (data not shown) (Winka and Eriksson 1998, Liew et al 2000). The MP tree differed by the disposition of Massariosphaeria phaeospora, which was sister taxon to a poorly supported clade containing taxa from Didymella exigua to P. herbarum (Fig. 5).
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The conflict between NJ and MP trees was consistent with previous work which also provided contradicting information about the branching order within the Pleosporaceae: Based on ITS and GPD sequences, Berbee et al (1999) found that the relationship between species of Pleospora and A. alternata could not be resolved.
Kishino-Hasegawa test – To investigate the possibility of a monophyletic genus Pleospora, P. gaudefroyi was constrained to group with P. herbarum in the large data set. In this scenario, nine most parsimonious trees were obtained, measuring 359 steps each, 11 steps more than the MP tree. According to the parsimony-based Kishino-Hasegawa test (KHT), all of the constrained MP trees were significantly worse than the unconstrained MP tree (P < 0.05).
Shimodaira-Hasegawa tests –
The KHT was designed to compare the fit of two a priori specified tree topologies to a data set (Goldman et al 2000). However, we wanted to test if a priori topologies with a monophyletic genus Pleospora were significantly different from the best tree derived from the data set. The appropriate test to use in this case was the likelihood-based non-parametric Shimodaira-Hasegawa tests (SHT) (Goldman et al 2000). This test allowed multiple comparisons of a priori hypotheses to the ML tree inferred from the data set. For the small data set containing six taxa, 15 a priori hypotheses could be formulated corresponding to the 15 unrooted tree topologies with P. herbarum and P. gaudefroyi as sister taxa. Subsequently, the number of a priori hypotheses was reduced to three, since we considered Cochliobolus sativus and Setosphaeria rostrata to be sister taxa. This assumption was based on a study by Berbee et al (1999) where the phylogenetic relationships of species of Alternaria, Cochliobolus, Pleospora, Pyrenophora, and Setosphaeria, were investigated using a data set with ITS and GPD sequences. The results showed members of Cochliobolus and Setosphaeria to be sister groups with 72% bootstrap support. This agreed with results from RAPD data, where representatives of Cochliobolus and Setosphaeria were more similar to one another than either one of them to Pyrenophora (Bakonyi et al 1995). Pyrenophora also differed ecologically from both Cochliobolus and Setosphaeria: Members of Pyrenophora were predominantly found on grasses of the Pooideae, whereas Cochliobolus and Setosphaeria occured generally on members of the Chloridoideae (Alcorn 1983, Watson and Dallwitz 1992). Thus, using the program SHTests v1.0 (Rambaut 2000), the three a priori hypotheses were compared to the ML tree obtained in PAUP*. All three were significantly worse than the ML tree (P < 0.02).
Phylogenetic analysis of the ITS rDNA data set – The ITS rDNA data set consisting of eight taxa was subjected to a parsimony analysis with Leptosphaeria maculans (M96384) as outgroup. Out of 625 characters, 198 were variable (32%), of which 113 were parsimony informative (18%). One most parsimonious (MP) tree was obtained, measuring 410 steps (CI = 0.759, RI = 0.434). Pleospora gaudefroyi grouped with 100% bootstrap support with Alternaria alternata, Cochliobolus sativus, Pleospora herbarum, Pyrenophora tritici-repentis, and Setosphaeria rostrata (data not shown). The latter five taxa formed a monophyletic group with 61% bootstrap support. The remaining bootstrap support percentages were below 50% (data not shown). The ITS alignment contained many ambiguously aligned sites, so that we chose to emphasize results based on easily alignable SSU rDNA data. However, the placement of P. gaudefroyi in ITS rDNA anlyses was consistent with results from SSU rDNA data.
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DISCUSSION |
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Decorospora, a new genus in the Pleosporaceae –
Phylogenetic analyses indicated that of all included taxa, D. gaudefroyi was closest related to members of the Pleosporaceae sensu Eriksson (1999): In both parsimony and neighbor-joining analyses, D. gaudefroyi and the remainder of the Pleosporaceae formed a monophyletic group with 100% bootstrap support (Fig. 3). Thus, Decorospora is placed in the Pleosporaceae.
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TAXONOMY |
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Genus Pleosporacearum. Ascomata subglobosa ad ellipsoidea, immersa, ostiolata, epapillata vel breve papillata, carbonacea, nigra. Peridium cellulis pachydermis luminibus grandis, in sectione longitudinali texturam angularem formantibus. Hamathecium pseudoparaphysibus septatis, ramosis. Asci octospori, clavati, breve pedunculati, pachydermi, fissitunicati, sine apparatu apicale. Ascosporae biseriatae, ellipsoideae, muriformes, brunneae, tunica gelatinosa tectae; tunica extensa ad apices ambos in 2 vel 3 protuberationes subconicas.
A genus of Pleosporaceae. Ascomata subglobose to ellipsoidal, immersed, ostiolate, epapillate or short papillate, carbonaceous, black (Fig. 1). Peridium composed of thick-walled cells with large lumina, forming a textura angularis in longitudinal section. Hamathecium composed of septate, ramose pseudoparaphyses (Fig. 4). Asci eight-spored, clavate, short pedunculate, thick-walled, fissitunicate, without apical apparatuses (Figs. 3 and 4). Ascospores biseriate, ellipsoidal, muriform, brown, covered by a gelatinous sheath that is slightly constricted around the center and drawn out at each apex into 2 or rarely 3 subconical extensions (Fig. 2).
Type species. Decorospora gaudefroyi (Pat.) Inderbitzin, Kohlm. & Volkm.-Kohlm.
Etymology. From the Latin decorus: beautiful, and sporus: spore, in reference to the ornate ascospores.
Decorospora gaudefroyi (Pat.) Inderbitzin, Kohlm. et Volkm.-Kohlm., comb. nov. Figs. 1–4
Pleospora salsolae Fuckel var. schoberiae Sacc., Michelia 2, 69. 1880
Pleospora schoberiae (Sacc.) Berl., Icon. Fung. 2, 23. 1895
Pleospora herbarum (Fr.) Rabenh. var. salicorniae (Jaap) Jaap, Ann. Mycol. 14, 17. 1916 (non Pleospora herbarum f. salicorniae Auersw. in Rabenhorst, Fungi Europaei Exsiccati, Cent. 2, No. 145. 1860, invalid name) Specimens examined. FRANCE. PAS DE CALAIS: Marais de la Pointe de Touquet, near Etaples, 56°12'30''N, 0°48'40''W, on Suaeda maritima, 15 Aug. 1879, O. Hariot (HOLOTYPE PC); sub Pleospora salsolae f. schoberiae, from Herb. E. Gaudefroy. CROATIA: Island of Rab, Lopar, 44°49'N, 14°45'E, on Halimione portulacoides, 16 Oct. 1971, J. & E. Kohlmeyer J.K. 2903 (IMS); same location and date, on Salicornia sp., J. & E. Kohlmeyer J.K. 2904 (IMS). ARGENTINA. BUENOS AIRES: Near Villa del Mar, SE of Bahia Blanca, 38°49'S, 62°19'W, on Salicornia sp., 23 Oct. 1973, J. & E. Kohlmeyer J.K. 3520 & 3522 (IMS); same location and date, on Salicornia ambigua, J. & E. Kohlmeyer J.K. 3521 (IMS). CANADA. BRITISH COLUMBIA: On small island in Malaspina Inlet near Lund, ca 50°03'N, 124°47'W, on Salicornia virginica, P. Inderbitzin P162 (UBC F14076). Data on other collections have already been reported in the literature (see paragraph on Geographic Distribution).
Commentary –
Decorospora gaudefroyi has been fully described and illustrated by Kohlmeyer and Kohlmeyer (1964, 1979). Yusoff et al (1994) described the ultrastructure of D. gaudefroyi ascospores with surrounding sheath while still in the ascus (i.e., without the unfolded sheath extensions), and Hyde et al (1986) depicted an ascospore with extended sheath in SEM. Ascospore ornamentations, found among many marine ascomycetes (Kohlmeyer and Volkmann-Kohlmeyer 1991) are considered adaptations to the marine habitat, enhancing the attachment of spores to submerged substrates (Hyde et al 1986). Because of its characteristically ornamented ascospores (Fig. 2), D. gaudefroyi cannot be confused with any other marine ascomycete. A superficially similar species is Nimbospora octonae Kohlm. (Halosphaeriales) which, however, has ascospores with a gelatinous sheath, enclosing a number of subulate appendages (Kohlmeyer 1985). Other marine species with somewhat extended ascospore sheaths are Frondicola tunitricuspis K.D. Hyde and Carinispora nypae K.D. Hyde (Hyde 1992), whereas the sheath in Massarina armatispora K.D. Hyde, Vrijmoed, Chinnaraj & E. B. G. Jones appears simply drawn out at the poles (Hyde et al 1992). Ascospore sheaths without extensions occur frequently also in terrestrial ascomycetes, e.g., in Phaeosphaeria and Massariosphaeria (Eriksson 1967, Leuchtmann 1984).
Substrates.
Decorospora gaudefroyi is an obligate marine fungus, growing at or above the high water mark. It is not host-specific, as it occurs on a variety of cellulosic substrates, such as dead marsh plants, driftwood and pilings. Among the host plants found so far are Halimione portulacoides (L.) Aellen, Salicornia ambigua Michx., Salicornia virginica L., Salicornia spp., and Suaeda maritima (L.) Dum. The species is able to grow under conditions of high salinity, as it was found in a salina in southern France with a salinity of 60
, and formed ascomata even on the salt-encrusted top of a piling (Kohlmeyer 1962). In pure culture D. gaudefroyi grows well, decomposes balsa wood, and even dissolves cellulose of a tunicate mantle (Kohlmeyer 1962).
Geographic distribution.
Decorospora gaudefroyi appears to be restricted to temperate waters. In Europe it was collected at the northern coast of France (Patouillard 1886), at the Mediterranean coast of France (Kohlmeyer 1962), at the North Sea coast of England (Webster and Lucas 1961), at the German coast of the North Sea (Jaap 1907; H. Sydow Mycotheca Germanica 1097), and in Croatia (this paper). In North America the species was found in the USA (Massachusetts, Gessner and Lamore 1978) and in Canada (British Columbia, this paper). The only collections of D. gaudefroyi from the southern hemisphere are from Argentina (this paper). Decorospora gaudefroyi can be compared in its habitat and geographical distribution with Passeriniella obiones (P. Crouan & H. Crouan) K. D. Hyde & Mouzouras. The latter grows also on decaying marsh plants and wood, and occurs throughout Europe, on the United States east coast, in British Columbia and Argentina (Kohlmeyer and Kohlmeyer 1979).
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Accepted for publication November 27, 2001.
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