Introduction

A common traditional circumscription of fungi is „eukaryotic heterotrophs with a stationary growth in most cases“. In fact, in many textbooks, including those for academic uses, downy mildews, slime molds and labyrinthuloids are treated besides the main bulk of „true fungi“. Already de Bary (1884) called Myxomycetes „Mycetozoa“ in his famous book „Vergleichende Morphologie und Biologie der Pilze, Mycetozoen und Bacterien“, thus very clearly refering to their behaviour as amoebae. He also illustrated very precisely the different flagellates of Phytophthora and chytrids. When unicellular Eukaryotes were compared structurally and functionally, it turned out that the number of flagellae, their outer appearance, and the swimming direction is of utmost importance in separating the very big eukaryotic relationships. It became clear that Heterokonts with tinsel- and whip-like flagellae are related and should be separated from Opithokonts with a single posterior flagellum, as in animals and lower fungi. These data were available in premolecular times and adequate classifiction schemes did exist. Nowadays, phylogenetic studies are based on molecular data, favourably complemented by additional features (Fig. 1).

The complete genomes of 21 fungi, three animals and Arabidopsis thaliana were used by Kuramae et al. (2006) to construct a high confidence tree with excellent nodal support for each branch. Chitin Fungi are the sister group of animals. Other fungal-like organisms could not be included in this study because sequenced genomes were not available at that time. – In an overview of the phylogeny of Eukaryotes, Baldauf (2008) distinguished five main groups, one of them, the Unikonts containing the Opisthokonts and Amoebozoa (= Mycetozoa), the RAS-assemblage (Rhizaria, Alveolates, and Stramenopiles) comprising the Oophyta, i.e. the „false fungi“ including the downy mildews. – A phylogeny with six supergroups has been published by Hampl et al. (2009), placing fungi and fungal-like organisms in similar phylogenetic clades. – „The six-kingdom, two-empire classification of life“ was introduced by Cavalier-Smith (2010), essentially confirming the big evolutionary lines of previous phylogenetic hypotheses. Parfrey et al. (2011) combined multigene data of an extensive sampling together with diverse fossils to estimate the timing of divergence of major eukaryotic clades. True fungi may have diverged from the common opisthokont origin more than 1200 Ma. Amoebozoa are calculated to be 1500-1700 Ma old. The downy mildew Phytophthora infestans is of middle phanerozoic origin, thus adequately corresponding to the appearance of potential hostplants.

Fig. 1: A simplified scheme for the phylogeny of Eukaryotes based on recent hypotheses of various authors (see text). The main three fungal groups (black triangles) are considered here. Their independent origin is illustrated. The true fungi, also called Chitin Fungi, represent a sister group of the animals, a monophylum charaterized by opisthokontic flagellates. The slimemolds, Mycetozoa (Myxomycetes) belong into the amoebozoic relationship. False fungi, called Oomycetes by mycologists, are derived from Heterokonts, now called Stramenopiles. Compiled by F. Oberwinkler.

Fig. 2: A hypothesis for the phylogeny of Chitin Fungi. They may have diverged from the common opisthokont origin more than 900-1200 Ma ago. This scheme refers also to fossil records (red columns). It is obvious that fungi with flagellate stages represent the oldest relationships. Recent representatives are grouped in the Chytridiomycota. Flagellates are lacking in all other true fungi. According to Liu et al. (2006), the loss of the flagellum happened only once in the fungal lineage. Glomeromycota are considered to be asexual fungi. They are the sister group to the dikaryomycotic fungi, comprising the Ascomycota and Basidiomycota. Compiled from various sources by F. Oberwinkler.

The Chitin Fungi (Fig. 2) appear monophyletic in all representative phylogenetic hypotheses based on molecular data (e.g. Lutzoni et al. 2004, James et al. 2006, Hibbett et al. 2007, Stajich et al. 2009, Wang et al. 2009). However, the phylogenetic position of the Microsporidia is still under question, and quite recently the discovery of fungal zooflagellates as members of freshwater picoeukaryotes (Lefèvre et al. 2007), now called Cryptomycota (Jones et al. 2011), compels an expanded arrangement of major fungal clades. – A fungal phylogeny was created by Fitzpatrick et al. (2006) based on a dataset of 345,829 genes that were extracted from 42 fungal genomes. The resulting supertree and concatenated phylogeny were highly congruent. All higher taxa, Zygomycota, Ascomycota with Saccharomycotina and Pezizomycotina as well as Basidiomycota were supported by 100% bootstrap scores. For Basidiomycota only Ustilago maydis, Cryptococcus neoformans, Phanerochaete chrysosporium, and Coprinopsis (as Coprinus) cinereus were included. A fungal phylogeny based on 82 complete genomes, using the composition vector method, was published by Wang et al. (2009). Again, nearly always 100% bootstrap supported clades were obtained, confirming the main fungal groups as well as lower taxa up to species, especially in extensively sampled ascomycetous yeasts. In Basidiomycota, Puccinia graminis and Sporobolomyces roseus represented the Pucciniomycotina, Ustilago maydis and Malassezia globosa the Ustilaginomycotina, Cryptocococcus neoformans and C. gattii the Tremellales, Phanerochaete chrysosporium and Postia placenta the Polyporales, and Coprinopsis (as Coprinus) cinereus and Laccaria bicolor the Agaricales. The rapid development of sequencing techniques initated more and more genome projects. „The fungal genome initiative represents an organized genome sequencing effort to promote comparative and evolutionary studies across the fungal kingdom“ (Cuomo & Birren 2010). – Studying the genes of the meiotic transcriptional program of Coprinopsis cinereus, Saccharomyces cerevisiae and Schizosaccharomyces pombe, Burns et al. (2010) concluded that these fungi diverged 500–900 million years ago.

Fig. 3: Classification of Chitin Fungi. Opisthokontic zoospores and gametes are known from Chytridiomycota. All other Chitin fungi are non flagellate. Sexual reproduction of Zygomycota is by gametangiogamy. Glomeromycota are considered to live exclusively asexual. However, their multinucleate stages may eventually allow recombination (den Bakker et al. 2010). They are the mycobionts of arbuscular mycorrhizae. Only one species, Geosiphon pyriforme, is known to harbour Nostoc obligatorily. The meiosporangium of the Ascomycota is the ascus, the most important morphological and functional feature of the group. Asexual stages are common in Ascomycota. Obligate mutualistic connections with algae and cyanobacteria are probably as diverse as non-lichenized Ascomycota. There are evidences that the latter are mostly derived from lichens (Lutzoni et al. 2001). Ascomycetous fungi are also mycobionts of diverse mycorrhizae. Basidiomycota are characterized by meiosporangia developing basidiospores externally. Asexual stages and mycorrhizal associations are widespread in Basidiomycota, while basidiolichens are comparatively rare. Orig. F. Oberwinkler.

Combined approaches considering fossil records and molecular clocks yielded substantial information about the timing of eukaryotic and fungal evolution. Taylor & Berbee (2006) used fossil calibration points and a dataset of 50 genes for 25 fungi, plants and animals to investigate divergence times in fungi. To determine the Ascomycota/Basidiomycota split they considered three calibration points with the result of extremely differing divergence dates. The plant Eu-Dicotyledons/Monocotyledons divergence of approximately 200 Ma ago yields an Ascomycota/Basidiomycota split of 400 Ma, thus being in accordance with the time of an early land plant radiation. However, the 400 Ma years old fungal fossil from the Rhynie Chert, Paleopyrenomycites devonicus (Taylor et al. 2005), considered to be a member of the Sordariomycetes, would then be a deep branching Ascomycete. Lücking et al. (2009a) have recalibrated the fungal tree of life compared to the evolution of green plants and reassessed the systematics of Paleopyrenomycites. They reestimated the origin of fungi between 760 Ma and 1.06 Ba, Chytridiomycota, Zygomycota and Glomeromycota approximately 600-700 Ma, Basidiomycota and Ascomycota between 500-650 Ma ago.