1 Recent Developments in the Molecular Taxonomy of Fungi
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1 1 Recent Developments in the Molecular Taxonomy of Fungi ROLAND W.S. WEBER 1 CONTENTS I. Introduction... 1 II. Non-Fungal Organisms Studied by Mycologists... 2 A. Slime Moulds B. Plasmodiophora and Related Species C. Straminipila... 4 D. Haptoglossa... 5 III. The Basal Fungi... 5 A. Microsporidia B. Chytrids C. Zygomycete-Type Fungi D. Glomeromycota IV. Ascomycota... 7 A. Taphrinomycotina B. Saccharomycotina... 7 C. Pezizomycotina... 7 V. Basidiomycota... 9 A. Pucciniomycotina... 9 B. Ustilaginomycotina C. Agaricomycotina VI. Conclusions References I. Introduction Taxonomy is the science of classification, i.e. the grouping of organisms into defined categories (taxa). Ideally, a classification scheme should be natural in the sense that all organisms in a given taxon should be related to each other by common ancestry. Traditionally, however, this was not necessarily the case with fungi because taxonomic approaches based on morphological and microscopic characters, later augmented by ultrastructural and biochemical features, did not always distinguish between homologies and analogies. Traditional taxonomies were arbitrary also in the sense that different taxonomists proposed widely differing classification 1 Obstbau Versuchs- und Beratungszentrum/Fruit Research and Advisory Centre (OVB) Jork, Moorende 53, Jork, Germany; roland.weber@lwk-niedersachsen.de schemes, depending on which features they regarded as relevant and at which taxonomic level. The past two decades have witnessed a revolution in the taxonomy of fungi because it became possible to generate and analyse homologous DNA sequences of functionally conserved genes (initially mainly ribosomal DNA sequences) on a routine basis, leading to a more objective comparison of taxa. Initial attempts at molecular phylogeny created considerable complications because each phylogenetic tree was usually based on the analysis of a single gene, and widely different phylogenies could result if different genes were used. The situation around the turn of the millennium and in the following years was therefore comparable to a football game with shifting goal-posts, as especially those involved in teaching fungal taxonomy will recall with horror. Several publications also reflect the fluid state of the discipline at that time, especially The Mycota VIIA and VIIB (McLaughlin et al. 2001) and the ninth edition of Ainsworth and Bisby s Dictionary of the Fungi (Kirk et al. 2001). These works have become outdated quite rapidly in terms of taxonomic concepts, though not, of course, in their valuable information on general biological features of the fungi. The third edition of Introduction to Fungi (Webster and Weber 2007), although principally intended to be used as a textbook pursuing a holistic approach to the fungi rather than as a taxonomic work, also had to be based on the taxonomy of the period. By the time of manuscript submission in March 2006, the outlines of certain natural groups of fungi had become apparent, but these could neither be delimited clearly, nor was it possible to assign formal names to many of them for lack of existence, validation or general acceptance. This state of transition led a large consortium of fungal taxonomists to join forces and develop a classification scheme based on multi-gene phylogenies in the hope that this would provide a Physiology and Genetics, 1st Edition The Mycota XV T. Anke and D. Weber (Eds.) Springer Verlag Berlin Heidelberg 2009
2 2 Roland W.S. Weber sound, permanent framework. Following the establishment of a communications platform ( deep hypha ), the AFTOL (assembling the fungal tree of life) project supported most of the immense amount of DNA sequencing work and data analysis (Blackwell et al. 2006). Both undertakings were funded by the United States National Science Foundation (NSF). The entire November/December 2006 issue of Mycologia was dedicated to reports of the results of these efforts, and a classification scheme synthesising the main findings was published by Hibbett et al. (2007). These authors emphasised the broad support and input which their scheme had received from numerous taxonomists, and called on the worldwide mycological community to adopt their unified system with generally accepted taxon names in future. To this end, many of the names of higher taxa proposed by Hibbett et al. (2007) are based on concepts readily recognised by most mycologists, which greatly facilitates the usage of their scheme. An arguable exception is the re-naming of higher taxa after key species, which would replace e.g. Urediniomycetes by Pucciniomycotina or Hymenomycetes by Agaricomycotina. It is reassuring to see that the introduction of these terms is an ongoing process with occasional inconsistencies even in publications by leading AFTOL authors. Therefore, the main purpose of the present chapter is to give a brief overview of the current taxonomic concept, highlighting changes from equivalent taxonomic groupings delimited in earlier schemes represented by Webster and Weber (2007), McLaughlin et al. (2001) and Kirk et al. (2001). At the same time, the likely stability of the AFTOL system is evaluated. Since work by this consortium did not cover organisms unrelated to Fungi but nonetheless studied by mycologists, their current phylogenetic and taxonomic placement is also summarised. Finally, there is a brief consideration of problems and potential of current fungal taxonomy in mycology teaching. II. Non-Fungal Organisms Studied by Mycologists Genera such as Phytophthora, Pythium, Peronospora, Plasmopara or Plasmodiophora are so intrinsically linked with the history of mycology and fungal plant pathology that they continue to be studied in mycological laboratories and to be taught in mycology lectures and practical classes. Slime moulds and other non-fungal protists will be encountered by mycologists during forays. Protists are subjected to two mutually incompatible classification systems: a zoological one governed by the International Code of Zoological Nomenclature and a mycological one according to the International Code of Botanical Nomenclature. The resulting confusion is multiplied by the rapid discovery of new protist species and new relationships between existing taxa by molecular phylogenetic approaches. Adl et al. (2005, 2007), recognising that neither of the two Codes provides a stable classification system for these organisms, broke free of both and established a scheme which retainsasmanyofthecommonlyknownnames as possible. This move is supported by many protozoologists. Some five or six kingdom-sized super-groups of eukaryotes can be resolved by current phylogenetic studies based on multi-gene analyses and modern analytical methods (Simpson and Roger 2004; Keeling et al. 2005). All but one of these harbour organisms studied by mycologists (Fig. 1.1). An overview of formal and informal names of relevant higher taxa is given in Fig A. Slime Moulds Slime moulds may exist vegetatively as amoebae (cellular slime moulds) or as multinucleate plasmodia (plasmodial slime moulds). Both ingest particulate food by phagocytosis. Reproduction is by means of single-spored or multi-spored structures termed sporocarps or sorocarps, respectively. Flagellate stages (swarmers) bearing two whiplashtype flagella may be present in the life cycle of certain groups (myxogastrids, dictyostelids). The separation of a small group, the acrasids, from the bulk of slime moulds has long been recognised on the basis of phylogenetic studies (Baldauf et al. 2000) and finds its morphological manifestation in the shape of the amoeba which produces a single lobed (lobose) anterior pseudopodium in acrasids, as opposed to the pointed (filose) pseudopodia emitted by amoebae of all other slime moulds. Acrasids are now grouped among the Excavata. All other slime moulds, including both cellular and plasmodial forms, belong to three phylogenetically related groups
3 Recent Developments in the Molecular Taxonomy of Fungi 3 Fig A hypothetical phylogenetic tree of eukaryotes showing five supergroups, based on molecular phylogenies, other molecular characters and morphological and biochemical evidence. Dotted lines indicate relationships resolved on preliminary evidence only, whereas relationships were left unresolved where there was no evidence of branching order. Groups traditionally studied by mycologists are printed in capital letters. Re-drawn from Keeling et al. (2005), with permission from Elsevier within the Amoebozoa (Fig. 1.1). Dictyostelid slime moulds are cellular forms, represented by the well-known Dictyostelium discoideum with its camp-mediated aggregation of thousands of amoebae into a pseudoplasmodium, which goes on to form a slug and ultimately a sorocarp (see Kessin 2001). Protostelid slime moulds may form filose amoebae or small plasmodia, whereas in myxogastrid forms such as Fuligo septica or Physarum polycephalum, the plasmodium is dominant, amoebae being reduced in the life cycle to a brief period following spore germination (see Webster and Weber 2007). B. Plasmodiophora and Related Species Plasmodiophora brassicae is the cause of club root of brassicas. Infection is initiated when a zoospore with two whiplash-type flagella encysts on a root hair. The penetration mechanism is highly characteristic in that a bullet-shaped stylet is forced by turgor pressure from the spore cyst through the root cell wall, injecting a small wall-less amoeba into the host cytoplasm. Plasmodia capable of phagocytosis develop from this amoeba and migrate deeper into the root tissue, breaking through plant cell walls along their way.
4 4 Roland W.S. Weber Fig Organisms not belonging to the Fungi yet traditionally studied by mycologists, in a mycological system (Webster and Weber 2007) and in the protistological classification scheme of Adl et al. (2005). Organisms grouped within a phylum but already suspected at the time of being phylogenetically unrelated to each other are separated by dotted boxes. Orders united by a bracket are currently grouped together in Peronosporales by many authors Archibald and Keeling (2004) and others have provided evidence that Plasmodiophora and allied genera (Spongospora, Polymyxa) are related to Cercozoan protists. Adl et al. (2005) have also placed plasmodiophorids among the Cercozoa within the kingdom Rhizaria (see Fig. 1.1). C. Straminipila Organisms possessing cellulose-containing cell walls, an inner mitochondrial membrane folded into tubular rather than plate-like cristae, morphologically recognisable Golgi stacks, biflagellate heterokont zoospores (i.e. with one flagellum of the tinsel and the other of the whiplash type), and a lysine biosynthetic pathway via a,e-diaminopimelic acid (DAP) rather than a-aminoadipic acid (AAA), are accommodated in a kingdom named Chromista by workers emphasising the lack of chlorophyll b in its photosynthetic members, or Straminipila by others highlighting the tinsel-type flagellum with its uniquely complex architecture. Straminipila/ Chromista are now grouped together with Alveolata (dinoflagellates, ciliates, and other taxa; Fast et al. 2002) in the kingdom Chromalveolata (Simpson and Roger 2004; Keeling et al. 2005). Several phyla within the Straminipila are of relevance to mycology. The phylum Labyrinthulomycota contains marine organisms in which individual vegetative cells produce a network of slime tracks. In addition, each cell is surrounded by a wall comprising a Golgi-derived L-galactose polymer. In Labyrinthulales, the cells move within their slime tracks, whereas in Thraustochytriales the slime track forms a rhizoid-like network at the base of a thallus-like structure (see Webster and Weber 2007). Both orders produce heterokont zoospores. Hyphochytriomycota resemble chytrid fungi in forming thalli comprised of one or more sporangia linked by rhizoids. The zoospore contains only a forward-directed tinsel flagellum, the backward-pointing whiplash flagellum having been lost during the course of evolution. By far the most important group of straminipilous organisms from a mycological perspective is the phylum Oomycota. Included here are organisms with heterokont zoospores and oogamous sexual reproduction, e.g. filamentous water moulds such as the Saprolegniales (Saprolegnia, Achlya), thallic aquatic saprotrophs or parasites of algae and other organisms, and filamentous species adapted to the terrestrial environment. Terrestrial straminipilous fungi have traditionally been separated into Pythiales (saprotrophic forms and necrotrophic pathogens especially of plants), Peronosporales and Sclerosporaceae (obligately biotrophic downy mildews of dicotyledonous plants and grasses, respectively). However, several recent phylogenetic analyses point towards intercalations between these taxa (Riethmüller et al. 2002; Villa et al. 2006; Thines et al. 2008) so that they may all eventually be united in one group (e.g. Peronosporales), at the possible exclusion of Albugo (Hudspeth et al. 2003). The collateral abandonment or revision of well-known genera such as Pythium, Phytophthora or Peronospora
5 Recent Developments in the Molecular Taxonomy of Fungi 5 has not yet been completed. In view of the ongoing trend to name higher taxa on the basis of exemplar genera, it may be deemed necessary to replace the term Oomycota/Oomycetes by Peronosporomycetes (Dick 2001). D. Haptoglossa Haptoglossa spp. infect rotifers or nematodes by a forceful injection mechanism very similar to that of Plasmodiophora (see above), although a walled sporidium instead of a wall-less amoeba enters the living host. Further, zoospores of Haptoglossa, where formed, appear to be anisokont, i.e. with two whiplash-type flagella of unequal length, like those of Plasmodiophora. Nonetheless, molecular phylogenetic studies have shown Haptoglossa spp. to be members of Straminipila, and indeed to belong to the Peronosporomycetes (Hakariya et al. 2007). Haptoglossa had also been grouped there by Adl et al. (2005) and, more intuitively, by earlier workers. III. The Basal Fungi James et al. (2006a) published a 70-author paper about the trunk of the fungal phylogenetic tree based on analyses of six functionally conserved genes, i.e. the nuclear ribosomal DNA operon (18S-, 28S-, 5.8S-rDNA), the ribosomal elongation factor gene EF1a, and the RNA polymerase II subunit genes RPB1 and RPB2. As a result of this fundamental work and numerous other contributions, the taxonomy of the basal fungi was modified extensively by Hibbett et al. (2007), as summarised in Fig The two established phyla, Chytridiomycota and Zygomycota, were broken into a total of eight groups, to which a further phylum, the Microsporidia, was added. A. Microsporidia The inclusion of the Microsporidia within the Fungi has been highly controversial until very recently (e.g. Keeling et al. 2000; Tanabe et al. 2002), and the continued use of the zoological term Microsporidia is a reminder of that debate. Included in this phylum are the most basal fungi according to current phylogenetic knowledge. Fig Classification of the lower fungi according to the current AFTOL scheme (Hibbett et al. 2007) in comparison with Webster and Weber (2007) summarising earlier approaches. Groups highlighted by an asterisk were mentioned by these authors but not discussed in detail. Supplementary data from Kirk et al. (2001) are indicated in square brackets These organisms are obligate parasites of animals, infecting their host cells by injection of a small protoplast from a spore through a tube initially coiled up inside the spore, then extruded by osmotic pressure (Keeling and Fast 2002). Such an infection mechanism is reminiscent of that found in Plasmodiophora (Cercozoa) or Haptoglossa (Chromalveolata, Straminipila) with which Microsporidia are not related. Instead, their closest relative in the analysis by James et al. (2006a) was the chytrid fungus Rozella allomycis, an endoparasite of Allomyces. Whereas R. allomycis possesses a posteriorly uniflagellated zoospore typical of the chytrids, Microsporidia do not, indicating that
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