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Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon 93133
Robert A. Shoemaker
Keith A. Seifert
Sarah Hambleton
Biodiversity Theme (Mycology and Botany), Agriculture and Agri-Food Canada, Ottawa, K1A 0C6 Canada
Joseph W. Spatafora
Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon 93133
Pedro W. Crous
Centraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD, Utrecht, The Netherlands
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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We present an expanded multigene phylogeny of the Dothideomycetes. The final data matrix consisted of four loci (nuc SSU rDNA, nuc LSU rDNA, TEF1, RPB2) for 96 taxa, representing five of the seven orders in the current classification of Dothideomycetes and several outgroup taxa representative of the major clades in the Pezizomycotina. The resulting phylogeny differentiated two main dothideomycete lineages comprising the pseudoparaphysate Pleosporales and aparaphysate Dothideales. We propose the subclasses Pleosporomycetidae (order Pleosporales) and Dothideomycetidae (orders Dothideales, Capnodiales and Myriangiales). Furthermore we provide strong molecular support for the placement of Mycosphaerellaceae and Piedraiaceae within the Capnodiales and introduce Davidiellaceae as a new family to accommodate species of Davidiella with Cladosporium anamorphs. Some taxa could not be placed with certainty (e.g. Hysteriales), but there was strong support for new groupings. The clade containing members of the genera Botryosphaeria and Guignardia resolved well but without support for any relationship to any other described orders and we hereby propose the new order Botryosphaeriales. These data also are consistent with the removal of Chaetothyriales and Coryneliales from the Dothideomycetes and strongly support their placement in the Eurotiomycetes.
Key words: bitunicate asci, hamathecium, loculoascomycetes, pseudoparaphyses
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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Although to a casual observer there is little to distinguish the flask-, spherical- or disk-shaped fruiting bodies of the Dothideomycetes from several other ascomycete groups, they share a distinctive pattern of development. The asci bearing the sexual spores develop in locules already formed lysigenously within vegetative hyphae. This, defined as ascolocular development, is in contrast to ascohymenial development found in the majority of other fungal classes. Ascohymenial development generates asci in a broad hymenium interspersed with apically free paraphyses and the reproductive structure is derived from cells after fertilization.
Building on earlier descriptions of ascolocular development Nannfeldt (1932)
proposed the group "Ascoloculares" and in 1955 this was formally proposed as a class "Loculoascomycetes" by Luttrell (1955). The importance of ascus morphology and dehiscence, in addition to the presence of surrounding elements inside the ascostromata, was emphasized (Luttrell 1951). The bitunicate ascus remains a defining character in modern dothideomycete taxonomy. It consists of a thick extensible inner layer (endotunica) and a thin inextensible outer layer (ectotunica). Most species release their ascospores by the extension of the inner ascus wall and the rupture of the outer wall, similar to a jack-in-the-box (fissitunicate), but variations are numerous. Another character of note, the centrum, defined as the tissues and cells occupying the cavity of the sexual structure, was expanded by Luttrell when he described three different ascostromatal developmental types exemplified by the genera Dothidea, Pleospora and Elsinoë forming part of the currently accepted orders, Dothideales, Pleosporales and Myriangiales (see tolweb.org/Dothideomycetes for details). The hamathecium (Eriksson 1981) (i.e. the sterile centrum tissues existing between the asci) is one of the most reliable characters used to delineate ordinal classifications within the Dothideomycetes. The presence of pseudoparaphyses (sterile cells extending down from the upper portion of the ascoma, initially attached at both ends, although the upper part may become free) is a notable character for the Pleosporales, together with mainly ostiolate flask-shaped pseudothecia. Conversely the absence of pseudoparaphyses and the presence of fascicles of asci are important in the Dothideales. The Myriangiales also do not have pseudoparaphyses but produce single globose asci in multiple locules. Several additional orders currently accepted are defined by combinations of centrum and ascomal characters. For a summary of different centrum types and features see Kirk et al (2001 p 224–225).
The different classification systems proposed thus far exhibited an emphasis on varying characters. For instance, the presence and morphology of characters in the hamathecium, together with ascostroma shape were used as the main characters to define ordinal groups by Luttrell (1955), while von Arx and Müller (1975) emphasized the form of the ascus and the specific opening of the ascoma. Although basing her classification on the work of Luttrell, Barr (1987) employed additional characters such as the morphology of pseudoparaphyses.
The best studied species in this group tend to be plant pathogens on important agricultural crops. Therefore a large body of work in dothideomycete taxonomy and systematics concerns descriptions of anamorphs, the predominant morphological state encountered on agricultural crops; in fact several families in this class (e.g. Pleosporaceae, Mycosphaerellaceae, Tubeufiaceae) include a high proportion of anamorphic species. These include both hyphomycetes and coelomycetes. Many of the hyphomycetes have sympodially proliferating conidiogenous cells. Phoma-like and other coelomycetes occur in several families (e.g. Leptosphaeriaceae, Lophiostomataceae); these have ostiolate pycnidia lined with phialidic, annellidic or holoblastic conidiogenous cells and produce small, aseptate conidia in slime. Other important species include the group now informally referred to as the "black yeasts" (some of which also belong to the Eurotiomycetes) characterized by the production of dark, slimy colonies and sporulation patterns that resemble the budding of true yeasts but actually are reduced versions of phialidic, annellidic or sympodially proliferating conidiogenous cells (de Hoog 1974). A selection of the variety of morphological structures exhibited by teleomorph and anamorph forms in the Dothideomycetes is shown (FIG. 1).
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, Berbee 1996). A more recent phylogeny produced from protein gene coding data (Liu and Hall 2004) was inferred as supporting the taxonomic concepts for a monophyletic lineage for ascostromatic taxa, but the ontogenetic designations were considered oversimplified by some (Lumbsch et al 2005). Other studies combining data from protein-coding genes and the ribosomal operon have shown the paraphyly of ascostromatic, bitunicate lineages (Lutzoni et al 2004, Reeb et al 2004). An example is the group of fungi that recently were transferred to the Eurotiomycetes based on nuclear small subunit ribosomal sequences, the "black yeasts" of the Chaetothyriales (Winka et al 1998). Together with the Verrucariales and Pyrenulales these bitunicate taxa have been placed within a separate subclass, the Chaetothyriomycetidae (Miadlikowska and Lutzoni 2004), which is sister of the Eurotiomycetidae (Lutzoni et al 2004, Reeb et al 2004) in the class Eurotiomycetes (also see Geiser et al in this issue).
Several studies provide the groundwork for a phylogenetically based classification for the Dothideomycetes. Most have used nuclear small subunit ribosomal data, but nuclear large subunit ribosomal and mitochondrial small subunit sequences also were used (Lindemuth et al 2001, Lumbsch and Lindemuth 2001). This allowed for the reassessment of specific morphological characters proposed in earlier work. Specifically, poor support for phylogenetic groups based on the morphology of pseudoparaphyses was found while phylogenetic correlation of their presence or absence was well supported (Liew et al 2000, Lumbsch and Lindemuth 2001), although a single exception to this was noted (Silva-Hanlin and Hanlin 2000). In spite of these recent examples of interordinal, molecular-based phylogenetic studies, a large number of species within the ascostromatic Ascomycota remain listed as Dothideomycetes or Chaetothyriomycetes incertae sedis (Eriksson 2006). Furthermore the question of whether Dothideomycetes represents a natural group derived from a single ancestor is not settled and the need to investigate its relationships to a number of the bitunicate lichen species such as the currently separate class Arthoniomycetes remains essential. The main focus of this study however is to provide an extension of previous ribosomal DNA-based phylogenetic studies and combine a number of smaller phylogenetic analyses within the framework of a multiple gene analysis showing intraordinal relationships in the Dothideomycetes.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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Phylogenetic analysis.— – Maximum and weighted parsimony (MP and WP) analyses were performed on a combined dataset with a total of 117 taxa that included 96 Dothideomycetes. Nineteen taxa contained data for only three loci to maximize taxon sampling. The majority of the missing data were in the terminal branches of the tree, and care was taken to include complete data sampling for taxa on branches underpinned by the more basal nodes. Two taxa with only ribosomal data (AFTOL ID 1856 Phoma herbarum and AFTOL ID 1864, Didymella cucurbitacearum) also were included to clarify the position of the clade surrounding Phoma herbarum. Removal of these taxa did not significantly affect support values in other parts of the tree. Likewise a comparison of a parsimony and Bayesian analysis with and without complete sets of characters yielded trees with congruent topologies. DNA sequences from a single strain (Leptosphaeria maculans DAOM 229267) inadvertently were included twice in the final analysis but were left in the final tree to ensure correct comparison across all approaches. We rooted the tree with three taxa from the class Pezizomycetes as outgroups (Pyronema domesticum, Caloscypha fulgens Gyromitra californica) (not shown in figure).
For the WP analyses the unambiguously aligned regions were subjected to symmetric step matrices for eight partitions (i.e. nuc SSU rDNA, nuc LSU rDNA and six codon positions of TEF1 and RPB2) to incorporate the differences in substitution rates and patterns as described in Lutzoni et al (2004). MP and WP analyses were performed with only parsimony informative characters with these settings: 100 replicates of random sequence addition, TBR branch swapping and MULTREES in effect. Maximum likelihood was performed with PHYML (Guindon and Gascuel 2003) using a GTR+I+
model of evolution. In all preceding cases nodal support was verified by nonparametric bootstrapping under the conditions mentioned, using 500 replicates.
Initial incongruence in the single gene trees for the taxa used was tested by examining single gene analyses with WP under the conditions previously mentioned for a set of taxa containing data for all four loci. A 70% majority rule consensus tree was compared in each case. Phylogenetic analysis using Bayesian inference of maximum likelihood was performed with a parallelized version of MrBayes v 3.1.2 across four processors (Altekar et al 2004). MrBayes was run with these parameters: a general time reversible model of DNA substitution (GTR) with gamma-distributed rate variation across sites (invariance, partitioning across genes and codons). A Markov chain Monte Carlo (MCMC) analysis with metropolis coupling was run starting from a random tree for 5 x 106 generations, sampling every 100th cycle. Four chains were run simultaneously with the initial 1000 cycles discarded as burn-in. Two additional runs with 5 x 106 generations were compared to confirm that stationarity in likelihood values was reached and compared. The phylogenies obtained in all cases were congruent. A 50% majority rule tree from a total of 45 000 trees obtained from a single run is presented (FIG. 2).
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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) with all of the bootstrap proportions as well as the Bayesian posterior probabilities. Internodes were considered strongly supported if they received all of bootstrap proportions 
70% and posterior probabilities 95 % (Lutzoni et al 2004).
Overview.— –
The tree (FIG. 2) contains representatives of the major classes in the Ascomycota, as defined previously (Eriksson 2001). The supraclass relationships in our analysis indicated no support for a close relationship between the Dothideomycetes and Sordariomycetes, alluded to in an earlier study (Lutzoni et al 2004) and the sister relationships of the Sordariomycetes and Leotiomycetes are supported in agreement with recent data (Lumbsch et al 2005). A few taxon pairs containing isolates used in previous works have remarkably high similarity to each other over all four loci. Two examples noted in this analysis were incorrectly identified strains, namely "Clathrospora diplospora" CBS 174.52 = Alternaria alternata and "Epipolaeum longisetosum = Raciborskiomyces longisetosus" CBS 180.53 = Cladosporium herbarum.
Non-Dothideomycete bitunicate groups..
Several lineages historically associated with the loculoascomycetes, such as the two species representing the Coryneliales, also were included. The placement of Caliciopsis orientalis together with Caliciopsis pinea (FIG. 2) indicates a close relationship with the Eurotiomycetidae (Geiser et al this issue). Other ordinal groups traditionally associated with the Dothideomycetes and now placed in the Eurotiomycetes were mentioned earlier. These groups share a number of centrum characters with members of the Dothideomycetes, such as the presence of periphysoids (Verrucariales, Chaetothyriales) and periphysate ostioles (Verrucariales, Chaetothyriales, Pyrenulales). The phylogeny (FIG. 2) confirms the separation of the Chaetothyriales and Verrucariales from the Dothideomycetes.
Dothideomycetes-Arthoniomycetes clade.. The relationship of the Dothideomycetes and Arthoniomycetes (node A) is well supported by Bayesian and maximum likelihood but not parsimony, although in an analysis without third codon positions, support by MP bootstrap and WP bootstrap increased. The internal node supporting the monophyly of the Dothideomycetes (node B) also had higher support in maximum likelihood and the two parsimony processes when the more saturated third codon positions were omitted. In more complete analyses containing characters from the RPB1 locus, this node was moderately supported and the Trypethelium strain is shown inside the Dothideomycetes (see Spatafora et al this issue).
Although taxon sampling for the Arthoniomycetes is sparse in our dataset, these levels of support (FIG. 2) largely agree with other recent large analyses where the Dothideomycetes is resolved as monophyletic but with low statistical support (Lumbsch et al 2005). A possible sister relationship of Dothideomycete/Arthoniomycetes has been proposed (Barr 1987, Tehler 1990) and there is some phylogenetic support for this (Lumbsch et al 2005, Lutzoni et al 2004). Clear differences between the groups exist, such as the ascohymenial type development of the Arthoniomycetes apothecium (Henssen and Thor 1994). More thorough sampling of Arthoniomycetes will test the monophyly of its relationship with the Dothideomycetes. It is premature to comment on the ultimate monophyly of the Dothideomycetes, but it seems quite reasonable that increased sampling of taxa and genes could increase support for this node. As pointed out by Lumbsch et al (2005), most of the large scale interclass relationships have been in conflict in recent publications and taxon sampling should be an important consideration before making major classification changes.
Dothideomycetes..
The addition of protein gene data illustrates that the lineages clustering around the core orders Pleosporales and Dothideales correlate with the presence or absence of pseudoparaphyses and other centrum characteristics. The node supporting the Dothideales, Capnodiales, Myriangiales and Mycosphaerellaceae (C) is strongly supported. This node was unaffected when third base codon positions were removed, but a small increase in parsimony bootstrap support was noted at node M, combining the Dothideales and Myriangiales, although ML bootstrap decreased. Saturation and the specific evolutionary model applied might have influenced this. Node C might indicate a single loss of pseudoparaphyses in all the terminal clades. However previous molecular phylogenies based on nuc SSU rDNA data have shown the presence of members of the aparaphysate genus Leptosphaerulina nested within the Pleosporales (Silva-Hanlin and Hanlin 2000), which could imply multiple, isolated losses of this character in other parts of the tree.
Anamorphs play an important role in the life cycles of many orders of Dothideomycetes. Many are coelomycetes, especially phialidic, Phoma-like anamorphs, which may be a plesiomorphic anamorph character in the class, perhaps serving some kind of spermatial function. In the Pleosporaceae and Mycosphaerellaceae hyphomycetes with sympodially proliferating conidiogenous cells with scars, and dry conidia, are particularly common and strictly anamorphic species may comprise the majority in these families. The Capnodiales, with their multitude of hyphomycete and coelomycete synanamorphs, and the helicoconidial anamorphs of the Tubeufiaceae, contain particularly distinctive anamorph groups. The anamorph genera of both hyphomycetes and coelomycetes, lacking teleomorph connections, continue to be examined for their phylogenetic relationships, many of them undoubtedly will be found to be associated with the Dothideomycetes. Several clades are well supported (FIG. 2) and will be discussed in more detail below.
Aparaphysate Dothideomycetes.— –
We hereby propose an emendation of the subclass Dothideomycetidae (nom. nud.) (Kirk et al 2001), which has been superceded by the Dothideomycetes O.E. Erikss. and Winka (2000). Dothideomycetidae sensu Lutzoni et al (2004) also was included in the Sordariomycetes as subclass Dothideomycetidae along with the subclass Sordariomycetidae (syn. Sordariomycetes s. str.) and Arthoniomycetidae (syn. Arthoniomycetes), although there was no strong statistical support for this broadened concept of Sordariomycetes. We validate and emend the concept of Dothideomycetidae sensu Kirk et al (2001) to include the bitunicate orders Dothideales, Capnodiales and Myriangiales, which lack paraphyses, pseudoparaphyses and paraphysoids. This emended subclass overlaps with the Loculoparenchymatomycetidae (Barr 1983) but differs by including the Myriangiales and excluding the Asterinales, now listed under its constituent families as Dothideomycetes et Chaetothyriomycetes incertae sedis by Eriksson (2006).
Dothideomycetidae P.M. Kirk, P.F. Cannon, J.C. David & J.A. Stalpers, ex Schoch, Spatafora, Crous et Shoemaker, subclass nov.
Dothideomycetidae P.M. Kirk, P.F. Cannon & J.C. David & J.A. Stalpers, in Kirk et al, Dictionary of Fungi, 9th ed., p 165, 572. 2001 (nom. nud.).
Ascomata immersa vel erumpentia vel superficialia, minuta vel magnitudine media, separata vel in stromate basilari aggregata, unilocularia vel plurilocularia, ostiolata, nonnumquam periphysata. Pseudoparaphyses absentes, periphysoideae nonnumquam praesentes. Asci globosi vel ellipsoidei vel clavati vel subcylindrici. Ascosporae hyalinae vel subhyalinae vel fuscae, unicellulares vel pluriseptatae vel muriformes. Anamorphoses seu coelomycetes seu hyphomycetes.
Ascomata immersed, erumpent or sometimes superficial, minute, small or medium-sized; separate or merged or grouped on basal stroma, uni- to multiloculate apical pore mostly present, when present ostiolar canal at times periphysate, stromatic tissues may contain pseudoparenchymatous cells. Pseudoparaphyses lacking, periphysoids may be present; Asci globose, subglobose, ovoid to ellipsoid, saccate, oblong, clavate or subcylindrical, Ascospores hyaline, subhyaline or dark brown, variable in shape and size, one celled or one to several septate or muriform.
Anamorphs coelomycetous and/or hyphomycetous.
Type order.. Dothideales (1897) Lindau in Engler & Prantl, Nat. Pflanzenfam. 1(1):373. 1897.
Represented orders.. Dothideales Lindau 1897, Capnodiales Woron. 1925, Myriangiales Starbäck 1899.
Dothideales..
Species from this order generally have smaller ascomata and fewer asci than the pseudoparaphysate Pleosporales (node D) and traditionally have been segregated because of the absence of pseudoparaphyses in their pseudothecia. The species included in this order encompass saprotrophs, hemibiotrophs and biotrophs. It is represented by eight species in our analysis, including the recent epitype isolate of Dothidea sambuci, the type of the genus Dothidea (Shoemaker et al 2003). The family Dothideaceae includes biotrophs, necrotrophs and saprobes on plant tissue. Stylodothis puccinoides was redescribed as a separate species from Dothidea but remains closely associated with the genus in our phylogeny.
Three members of the Dothioraceae are polyphetic in the tree. The so-called black yeast anamorphs associated with Dothideomycetes tend to occur in this family, with Aureobasidium pullulans (probably an anamorph species complex based on the ITS sequences deposited in GenBank), and the micro-morphologically similar Hormonema dematioides (teleomorph Sydowia polyspora, perhaps also a complex of anamorph species) (de Hoog 1974). These species are found commonly on moist surfaces of plants and can convert from yeast to meristematic growth under nutritional stress. Some progress in the resolution of the nature of Aureobasidium pullulans has been made here with the linkage of Columnosphaeria fagi (H.J. Hudson) M.E. Barr to a "neotype" culture CBS 584.75 of A. pullulans var. pullulans (SUPPLEMENTARY TABLE I).
Capnodiales..
The node I is well supported in this multigene analysis. This same node is present in a ribosomal rDNA phylogeny containing "Raciborskiomyces longisetosus" as erroneous name for a Cladosporium species with Capnodium citri (Lumbsch and Lindemuth 2001). Synapomorphies are limited in this expanded order and these taxa have not been grouped together before. The presence of short, periphyses-like cells in the ostiolar pore of some genera of the Capnodiales such as Capnodium also are reported from other families, including the Mycosphaerellaceae (von Arx and Müller 1975) and might be a synapomorphy uniting these taxa. We hereby propose an expansion of the current Capnodiales to include the Mycosphaereallaceae and Piedraiaceae. The constituent families are discussed below.
Capnodiaceae..
An ascostromatal family without pseudoparaphyses, the Capnodiaceae are leaf epiphytes associated with the honeydew of insects. Also known as sooty molds, they tend to live in complex communities, with multiple species, and often multiple fungal parasites of those species, inhabiting a common, sooty mass. They are noted for the production of darkly pigmented hyphae, often of very characteristic morphology (Hughes 1976, Reynolds 1998). The members of this order have superficial ascostromata with ovoid asci in fascicles and hyaline to dark, one to multiseptate ascospores. The sooty molds are highly pleomorphic and often highly pleoanamorphic. The order includes many anamorphic species, all dematiaceous, including several conidiomatal, mycelial (often with dry-spored, blastic phragmo- or dictyoconidia) or presumably spermatial (usually phialidic) hyphomycete genera or pycnidial synanamorphs (Hughes 1976).
Mycosphaerellaceae..
The Mycosphaerellaceae is characterized by small pseudothecial ascomata that are immersed in host tissue, single and superficial, or imbedded in a pseudoparenchymatal stroma, papillate, ostiolate, lacking interascal tissue. Asci vary from ovoid to saccate to subcylindrical, usually stipitate, with or without an apical chamber, lacking any other apical mechanism. Ascospores are hyaline to slightly pigmented, 1-septate, but in some cases also 3-septate, and sometimes are enclosed in a sheath. Mycosphaerella has close to 30 anamorph genera associated with it, most of which have cicatrized, sympodially proliferating conidiogenous cells and single or acropetally catenate, dry conidia. The two clades delineated within Mycosphaerella here also were recognized in a separate study employing multiple genes to resolve relationships in Mycosphaerella (Hunter et al 2006). Node I1 contains the type of Mycosphaerella, M. punctiformis, and the bulk of Mycosphaerella species, while the second clade (above I4) appears to contain more extremotolerant species (Crous et al unpubl data).
Mycosphaerella is distinguished from Davidiella (Cladosporium anamorphs) by lacking irregular lumens or inclusions in its ascospores and not having anamorphs with protruberant, thickened, darkened, Cladosporium-like scars (Braun et al 2003, Aptroot 2006). As shown in this study Davidiella with its Cladosporium anamorphs (type species Davidiella tassiana, anamorph Cladosporium herbarum) clusters in a well supported clade apart from Mycosphaerella s.str. (Mycosphaerellaceae), and thus a new family is proposed for clade I1.
Davidiellaceae Schoch, Spatafora, Crous et Shoemaker, fam. nov.
Ascomata Mycosphaerellae similia, sed lumen ascosporarum forma variabile et anamorphe Cladosporium.
Ascomata immersed to erumpent, small or medium-sized; separate or aggregated, uniloculate, apical pore present, periphysate; wall of several layers of brown, thickened, pseudoparenchymatal cells. Pseudoparaphyses lacking. Asci bitunicate, 8-spored, ob-ovoid to ellipsoid or subcylindrical, fasciculate, with or without apical chamber. Ascospores hyaline to pale brown, smooth to somewhat roughened, mucous sheath sometimes present, one-septate, thick-walled, with irregular lumens. Anamorphs are species of Cladosporium.
Typus.. Davidiella tassiana (De Not.) Crous & U. Braun, Mycol. Prog. 2:8. 2003.
The position of a single representative of the Piedraiaceae, Piedraia hortae, is refined here as associated with the Capnodiales and allies but not the Myriangiales as reported earlier (Lindemuth et al 2001). This species was described with an ascus containing only one thin wall (Shoemaker and Egger 1982). The specialized parasites in this family are almost exclusively associated with human hair in tropical regions. It is shown with low parsimony bootstrap support (I3) with Trimmatostroma abietis, a meristematic anamorph species isolated from conifer needles and rock surfaces. This species was shown to be closely related to Mycosphaerella and its allies in a recently published molecular phylogeny (Selbman et al 2005).
Myriangiales..
The Myriangiales are reported to be related to the Dothideales (node M), although without any significant bootstrap support for this placement. They generally have ascostromata without ostioles in monoascal locules. The species of the type genus, Myriangium, has globose asci scattered at many levels in an undifferentiated stromatic mass (Sivanesan 1984). The order includes saprobic, epiphytic or biotrophic organisms. The anamorphs of this order, when known, generally are acervular coelomycetes with polyphialidic conidiogenous cells, such as the Sphaceloma anamorphs of Elsinoë species (Kirk et al 2001).
Paraphysate Dothideomycetes.
We hereby propose a new subclass for the pseudoparaphysate taxa supported by node D1.
Pleosporomycetidae Schoch, Spatafora, Crous et Shoemaker, subclass nov.
Ascomata perithecialia vel hysterothecialia vel cleistothecialia, immersa vel erumpentia. Hamathecii pseudoparaphyses cellulares vel trabeculatae, maturae nonnumquam deliquescentes. Asci bitunicati, plerumque basilares, nonnumquam lateraliter extendentes, cylindrici vel clavati vel oblongi vel saccati. Ascosporae colore, forma septisque variabiles, plerumque heteropolares sed nonnumquam etiam symmetricae.
Ascomata perithecioid, hysterothecioid or cleistothecioid, conchate or dolabrate, immersed, erum-pent or superficial; globose, sphaeroid, turbinate, ovoid, obpyriform, conoid, doliiform, dimidiate. Hamathecium of wide to narrow cellular or trabeculate pseudoparaphyses, deliquescing at maturity in some. Asci bitunicate, usually basal, at times extending laterally, cylindric, clavate, oblong or saccate. Ascospores variable in pigmentation, shape and septation, usually with bipolar asymmetry, but some symmetrical.
Type order.. Pleosporales Luttrell ex M.E. Barr.
Represented order.. Pleosporales Luttrell ex M.E. Barr.
Pleosporales..
The Pleosporales is the largest order in the Dothideomycetes. It contains several well known plant pathogens such as Cochliobolus heterostrophus, the causative agent for southern blight on corn, Leptosphaeria maculans, causing black leg on rape seed and Phaeosphaeria nodorum causing stagonospora blotch in cereals. In this analysis a strain of Delitschia winteri is placed above node D, supporting the rest of the Pleosporales according to Eriksson’s broad concept (2001). Delitschia shares features common to several bitunicate species occurring on dung; they are darkly pigmented, usually strongly constricted ascospores with germ slits (Barr 2000). The family Delitschiaceae was described by Barr (2000) for species previously placed in the Sporormiaceae. The delineation is based on an ostiole containing periphyses and asci with wide outer ascus walls and an ocular chamber containing refractive rods. This placement was confirmed with nuc SSU rDNA sequence comparisons (Kruys 2005). A combined nuc SSU analysis of Delitschia winteri grouped it close to another species of the genus, D. didyma (AF242264
[GenBank]
), confirming the identification of the strain used (results not shown). Members of this family are hypersaprotrophic on old dung and exposed wood.
There was also strong support for the monophyly of Pleosporales, with Lophium mytilinum branching at its most basal node (D1). This species is found as a saprobe on wood and on cones of conifers and is listed incertae sedis as part of the Mytilinidiaceae (Eriksson 2006). The family contains species with characteristic conch shaped ascomata. Analyzing additional taxa from the Mytilinidiaceae and related groups also will be important to investigate ancestral character states for the Pleosporales but they should be placed as Pleosporomycetidae incertae sedis for now.
The morphology of ascospores has played an important role in delimiting families in the Pleosporales. However, as noted from some of the first molecular based phylogenies of the Dothideomycetes, several family relationships might be poorly supported (Lindemuth et al 2001). Perhaps the strains chosen are not good exemplars for their families or are derived from misidentified specimens. However it seems unlikely that this can account for all the relationships (FIG. 2) and a reassessment at this level of classification seems urgent. Here we will discuss only briefly a selection of highlighted families (FIG. 2).
The most basal node inside the Pleosporales (D2) supports two members of the Testudinaceae, provisionally included among Ascomycota incertae sedis by Eriksson (2006). Members of this family are mainly isolated from soil and produce reduced, cleistothecioid ascostromata. This clade unexpectedly contains the ostiolate marine species, Verruculina enalia (Didymosphaeriaceae) as also noted in an earlier phylogenetic analysis (Kruys 2005). The next well supported clade above node D3 supports the Sporormiaceae. These fungi are found commonly on dung but some occur on other substrates (e.g. wood, soil and plant debris). A large number of species in this group have germ slits. This morphological variability was confirmed in a phylogenetic study using DNA sequences from multiple ribosomal loci (Kruys 2005).
The Lophiostomataceae and Melanommataceae are inferred as paraphyletic in the next set of clades (above D4 and D5), with one clade including two species of Lophiostoma (Lophiostomataceae 1). This clade also contains one species of Trematosphaeria heterospora, which was classified as Lophiostoma heterosporum (Barr 1992). The second clade (Lophiostomataceae 2) includes members of the Lophiostomataceae and Pleomassariaceae as well as Melanommataceae. Node D5 contains a diverse group of species isolated from diseased and decaying plants as well as soil (each currently classified under a different family). This overlapped with relationships reported before, using molecular-based phylogenies (Liew et al 2000, 2002), but like many of the other clades will require more intense sampling to address family and genus descriptions.
The more terminal branches in the Pleosporales (D6) include well studied families containing important plant pathogens, saprobes and animal pathogens with numerous anamorphs. Didymella cucurbitacearum forms a clade with the anamorphs Ascochyta pisi and Phoma herbarum (D8), parasites on agricultural crops. Leptosphaeria (Leptosphaeriaceae), shown on a single branch, is a large genus with pale to dark brown and septate ascospores. Members of this family have flask-shaped pseudothecia with narrow asci and a characteristic thin apex. Many species are associated with coelomycetous anamorphs. Phoma anamorphs are particularly common (Camara et al 2001, Verkley et al 2004). The Phaeosphaeriaceae (D9) are distinguished from the Leptosphaeriaceae by ascomal wall morphology and all have pycnidial coelomycetes, mostly classified in Stagonospora, characterized by holoblastic or sometimes annellidic conidiogenesis and the production of phragmoconidia. Unnamed pycnidial microconidial anamorphs also are reported in some species (Leuchtmann 1984). In a poorly supported clade a trio of species without any clear phylogenetic placement are noted. Two of these species are anamorphs, Coniothyrium palmarum and Pyrenochaeta nobilis, linked to the teleomorphs Leptosphaeria and Herpotrichia.
The next well supported node (D10) contains the Pleosporaceae, which have ascostromata that are mainly flask-shaped pseudothecia embedded in the substrate with 1-septate to muriform ascospores. In addition to species found in marine environments and as parasites on animals a number of important grass and cereal crop parasite genera, Cochliobolus, Pyrenophora and Lewia, are included in this family. The sexual states are normally well linked with single anamorph genera. Important anamorph species include the well known genera Alternaria (with Ulocladium paraphyletic within it), Stemphylium, the so-called helminthosporia (Bipolaris, Curvularia, Drechslera, Exserohilum) and a few other genera such as Dendryphion and Dendryphiopsis.
Dothideomycetes incertae sedis.— –
A number of orders could not be placed in any of the two subclasses defined and will be discussed in more detail. Two orders, Jahnulales and Patellariales, currently listed by Eriksson (2006) are not included in this analysis but a separate comparison using deposited sequences from nuc SSU obtained from GenBank combined with our complete taxa revealed them to be separate from the groups referred to in this paper (data not shown).
Members of Hysteriales have been reported with pseudoparaphyses in apothecioid ascomata with elongated openings (von Arx and Müller 1975, Barr 1987, Luttrell 1974) and are often saprobes on wood or weak parasites of woody plants. Four members of the Hysteriales agreeing mainly with Luttrell’s original definitions are included (FIG. 2) and it is clear that these are not a monophyletic group, a proposition also mentioned by Luttrell (1973). Farlowiella carmichaeliana could not be resolved with any certainty.
The phylogeny also supports a relationship between the dung fungus Phaeotrichum benjaminii and Tyrannosorus pinicola (FIG. 2). Phaeotrichum is characterized by dark-brown, septate spores and cleistothecioid ascostromata. T. pinicola produces ostiolate ascostromata with characteristic long, sharp spines and have been isolated from wood and plant material. The multiple germ slits that were described for T. pinicola may be linked to the terminal germ pores characteristic of P. benjaminii.
Node E supports Kirschsteiniothelia aethiops with its Dendryphiopsis atra anamorph. These two species also appear unrelated to other species in the genus (Shearer 1993) based on nuc SSU rDNA data and the genus is reportedly heterogenous (Hawksworth and Eriksson 2003). K. aethiops does not have close associations with the Pleosporaceae and should be placed in a separate family.
The Tubeufiaceae clade (above node G) contains species with a variety of nutritional modes. They often are reported as saprobes from terrestrial and freshwater environments, but some species are hyperparasites and others can parasitize insects. Teleomorphs consist of brightly colored ascostromata, with long, hyaline, multiseptate ascospores (Rossman 1987). The best-known anamorphs of the Tubeufiaceae are helicosporous hyphomycetes and well known genera include Helicodendron, Helicomyces and Helicoon. Recent DNA sequence-based comparisons did not find strong correlation between these anamorph forms and phylogenetic groups. (Tsui et al 2006). Combining recent focused phylogenies into a large scale dataset is required before placement of this group in the current classification.
Botryosphaeriaceae..
The position of the Botryosphaeriaceae (H) within the Dothideomycetes has been enigmatic. The taxonomy of this group of plant-associated fungi has relied mostly on anamorph descriptions; sequence data recently have linked several anamorph genera to the genus Botryosphaeria (Jacobs and Rehner 1998). Associated anamorphs were divided into two groups, those with thin-walled, hyaline conidia (Fusicoccum), and those with thick-walled, pigmented conidia (Diplodia) (Denman et al 2000). In a recent phylogenetic study employing LSU sequence data to resolve relationships among members of the Botryosphaeriaceae, Crous et al (2006) segregated Botryosphaeria into several genera, supported by morphological differences of their anamorphs. From the phylogenetic results obtained in this study, it is clear that the Botryosphaeriaceae deserves an order separate from the Pleosporales and Dothideales, which is introduced below.
Botryosphaeriales Schoch, Crous & Shoemaker, ord. nov.
Family.. Botryosphaeriaceae Theiss. & P. Syd., Ann. Mycol. 16:16 (1918).
Type.. Botryosphaeria Ces. & De Not., Comment Soc. crittog. Ital. 1:211 (1863)..
Type species.. B. dothidea (Moug. : Fr.) Ces. & De Not., Comment Soc. crittog. Ital. 1:212 (1863).
Ascomata unilocularia vel plurilocularia, pariete multistratoso fusco inclusa, singularia vel aggregata, raro in stromate submersa. Asci bitunicati, endotunica crassa, stipitati vel sessiles, clavati, camera apicali distincta, pseudoparaphysibus hyalinis, septatis, ramosis vel simplicibus intermixti. Ascosporae hyalinae vel pigmentatae, unicellulares vel septatae, ellipsoideae vel ovoideae, nonnumquam appendicibus vel tunica gelatinosis praeditae. Anamorphoses: conidiomata pycnidialia, unilocularia vel multilocularia, saepe in stromate submersa, cellulis conidiogenis phialidicis, conidia hyalina vel pigmentata, tenui- vel crassitunicata proferentibus, quae nonnumquam appendicibus vel tunica gelatinosis praedita sunt.
Ascomata uni- to multilocular with multilayered dark brown walls, occurring singularly or in clusters, frequently embedded in stromatic tissue. Asci bitunicate, with a thick endotunica, stalked or sessile, clavate, with a well developed apical chamber, intermixed with hyaline, septate pseudoparaphyses, branched or not. Ascospores hyaline to pigmented, septate or not, ellipsoid to ovoid, with or without mucoid appendages or sheath. Anamorphs have uni-to multilocular pycnidial conidiomata, frequently embedded in stromatic tissue, with hyaline, phialidic conidiogenous cells, and hyaline to pigmented, thin-to thick-walled conidia, which sometimes have mucoid appendages or sheaths.
Conclusion.— –
This multigene phylogeny contributes to the overall phylogenetic classification of the Dothideomycetes. We emend a previously proposed subclass, the Dothideomycetidae, and propose a new one, the Pleosporomycetidae, based on the presence or absence of pseudoparaphyses as defined by Barr (1987) based on Luttrell (1955). The orders according to Eriksson (2006) are largely upheld with the exception of the Hysteriales, but we also expand this classification with an additional order, the Botryosphaeriales, and redefine the Capnodiales to include the currently defined Mycosphaerellaceae and Piedraiaceae. A new family, the Davidiellaceae, is proposed to accommodate Davidiella species with Cladosporium anamorphs. Several clades did not correlate with familial relationships under Eriksson’s classification (2006) and should be addressed in subsequent analyses. Similarly a number of small clades are incertae sedis and remain to be addressed in the future. The strains used in this study, although validated by morphological examinations in previous publications (e.g. Berbee 1996) as well as by comparisons with sequences from GenBank, should continue to be validated by more intensive taxon sampling in a number of clades. The value of additive sampling in this study, where two strains used in previous studies could be shown to be misidentified, supports this.
One large gap in this analysis is the absence of lichenized lineages. A single unidentified Trypethelium species was included, but numerous lichenized ascostromatic bitunicate species (such as those in the Pyrenulales) remain candidates for placement in the Dothideomycetes. In fact a study by Del Prado et al (2006) shows good support for a placement of the lichenized Trypetheliaceae within the Dothideomycetes. In addition, numerous lineages remain unresolved in this class. For example the current classification of Eriksson (2006) contains 23 families placed in orders but more than 40 families remain listed as Chaetothyriomycetes et Dothideomycetes incertae sedis. It appears likely that, in the process of combining the comprehensive body of work already done on the biology, ontogeny and morphology of these fungi within a molecular-based phylogenetic context, they will continue to surprise and challenge us well into the future.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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1 Corresponding author. E-mail: schochc{at}science.oregonstate.edu
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LITERATURE CITED |
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P.W. Crous, U. Braun, K. Schubert, and J.Z. Groenewald Delimiting Cladosporium from morphologically similar genera Stud Mycol, January 1, 2007; 58(1): 33 - 56. [Abstract] [Full Text] [PDF]
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K. Schubert, J. Z. Groenewald, U. Braun, J. Dijksterhuis, M. Starink, C.F. Hill, P. Zalar, G.S. de Hoog, and P.W. Crous Biodiversity in the Cladosporium herbarum complex (Davidiellaceae, Capnodiales), with standardisation of methods for Cladosporium taxonomy and diagnostics Stud Mycol, January 1, 2007; 58(1): 105 - 156. [Abstract] [Full Text] [PDF]
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G.S. de Hoog, A.S. Nishikaku, G. Fernandez-Zeppenfeldt, C. Padin-Gonzalez, E. Burger, H. Badali, N. Richard-Yegres, and A.H.G. G. van den Ende Molecular analysis and pathogenicity of the Cladophialophora carrionii complex, with the description of a novel species Stud Mycol, January 1, 2007; 58(1): 219 - 234. [Abstract] [Full Text] [PDF]
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