Typical members of the Basidiomycota are well characterized by several important characters (Fig. 4 d, c, e): A normally short monokaryotic phase is followed by plasmogamy (1), allowing compatible nuclei to establish dikarya (2). These are maintained during the whole ontogeny (3) until the formation of meiosporangia (4, 5), alltogether resulting in a basidiocarp (6). The majority of basidiomycetous fungi produce basidia with characteristically curved sterigmata (Fig. 4, d 5, e), microstructures that are capable to eject basidiospores by a highly elaborate mechanism (Pringle et al. 2005). Such ballistospores are not restricted to meiosporangia, they can be produced even by single cells (Fig. 4 c) as in „jumping yeasts“, e.g. the ballistoconidia of Sporobolomyces (Kluyver & van Niel 1924, 1927), and those of Sporidiobolus (Nyland 1949), a dimorphic fungus with clamp connections and teliospores. – In addition to this unique set of characteristics there exist other specific features for Basidiomycota, like septal pores, cell wall ultrastructure and metabolisms (Oberwinkler 1978). – The above mentioned phylogenetic hypotheses based on molecular data unanimously group Basidiomycota as a monophylum, comprising some 31,000 described species (Kirk et al. 2008). How molecular techniques revolutionize the knowledge of basidiomycete evolution has recently been reviewed by Yang (2011).
Fig. 4: The dikaryomycotic fungi, Ascomycota and Basidiomycota. a: Fossils of Ascomycota are known from the Devonian. The perithecium is approximately 400 µm in diameter and develops in the stomatal chamber of Asteroxylon. Their morphology is identical with extant representatives. The dikaryophases of typical Asco- and Basidiomycota are illustrated schematically (red arrows). b: In Ascomycetes the dikaryophase is restricted to short hyphae between the ascogon and the asci. d: In the majority of Basidiomycetes the dikaryophase extends to more or less the whole life cycle. e: Ballistospores ejected from sterigmata are typical for basidiomycetous meiosporangia, the basidia. c: A similar mechanism can occur in ballistosporous yeasts of Basidiomycetes. a from Taylor et al. (1999). Orig. F. Oberwinkler.
Evolution of morphological structures
Species of the Basidiomycota are known as yeasts, dimorphic fungi, simple hyphae, hyphal networks, and basidiocarps of different complexities. Their most characteristic feature is the basidium that evolved in various morphological types. Basidiospores have undergone considerable structural and functional changes during evolution. Septal pore ultrastructures show a remarkable evolutionary development, and other subcellular structures exist of high phylogenetic importance. An evolution of structures from budding single cells and ballistosporic yeasts to hyphal growth with convergently evolving basidiocarps marks main steps of basidiomycetous phylogeny.
Yeasts and dimorphic fungi
Fundamental properties of ascomycetous Saccharomyces cerevisiae yeast communities have been summarized by Honigberg (2011). Strain-to-strain variation appears to depend on the variability in the expression and function of adhesin proteins. Yeast colonies are embedded in a common protective matrix that also may play an important role for diffusible signals between cells to organize different community structures and functions. It can be expected that basidiomycetous yeasts behave similarly.
Budding was already intensively studied and taxonomically interpreted by Brefeld (1881, 1888), but his findings were largely neglected later. Yeast budding of basidiospores and the capability to form yeast colonies is wide spread in different relationships of the Pucciniomycotina, the Ustilaginomycotina, and the Tremellomycetes. When a filamentous basidiomycetous fungus is capable of growing with single cells, the yeast typically develops in the first ontogenetic stage by basidiospore or conidial germination. The transition from single cells to hyphal growth certainly is a major evolutionary step. Thus, the yeast stage reflects phylogenetically old Basidiomycota.
Fig. 5: Microbotryum saponariae, germination of smut spores. The germination hypha is a transversely septate basidium that buds off basidiospores (sporidia). A yeast colony develops by continuous budding of single cells. Orig. F. Oberwinkler.
Evolutionary trends in basidiomycetous yeasts:
Life cycle in the single cell stage > dimorphic ontogeny: yeast – hyphae – yeast > loss of the yeast phase
It is most likely that the origin of Basidiomycota goes back to yeasts with specific features different from ascomycetous yeasts. None of the so far known extant taxa can be considered as such a candidate, for example species of the genera Bensingtonia, Kurtzmanomyces, Rhodosporidium, Sporobolomyces, and Sterigmatomyces of the Pucciniomycotina.
In recent dimorphic basidiomycetous species, the yeast stage is at the beginning of the life cycle. This might be a good example for considering ontogeny as a recapitulation of phylogeny. Another convincing fact for such an interpretation is that yeasts in recent Basidiomycota occur in evolutionarly old groups, like most Pucciniomycotina, the Mixiomycetes, Agaricostilbomycetes, Cystobasidiomycetes, Septobasidiales, and Microbotryomycetes. In this subdivision, however, yeasts are not kown from Cryptocolacomycetes, Classiculomycetes, Atractiellomycetes, and Pucciniomycetes except of Septobasidiales, if this is a member of the class.
In most Ustilaginomycotina and the basal Agaricomycotina, the Tremellomycetes, ontogenetic yeasts are present. In the true smut fungi, Ustilaginomycotina, remarkable anamorphic yeast genera are Malassezia and Tilletiopsis p.pte. In this relationship, yeasts are not known from the Tilletiales, the bunts.
Yeasts in Agaricomycotina are restricted to the phylogenetically basal Tremellomycetes. They are recorded from all presentely accepted orders, the Tremellales, Filobasidiales, and Cystofilobasidiales. The class comprises also a considerable assemblage of anamorphic taxa of the genera Trichosporon, Bullera p.pte., Cryptotrichosporon, and Cryptococcus p.pte., grouped in the Trichonosporales, an order based on a molecular hypothesis.
In deep-sea environments Bass et al. (2007) recorded an unknown wide diversity of basidiomycete-like organisms with close similarities to basidiomycetous yeast groups. Curious exceptions, as a sequence taxon that clusters with the polyporaceous genus Antrodia, remains an unsolved riddle.
Morphology of hyphae and hyphal systems
When Gimeno et al. (1992) found that diploid Saccharomyces cerevisiae can undergo dimorphic transitions to grow with (pseudo)hyphae in response to starvation for nitrogen, further experimental work was initiated to elucidate this process. The yeast-to-hyphal transition in Candida albicans, also an ascomycetous yeast, is closely bound to virulence gene expression (Thompson et al. 2011). The expression of genes important for hyphal growth as well as those for virulence are simultaneously controlled by several transcriptional regulators in this case. Recently it could be shown that regulation of filamentous growth in Saccharomyces cervisiae depends on evolutionarily conserved signalling pathways (Cullen & Sprague 2012). Here, evolutionary trends become obvious on the level of functional molecular processes.
Hyphae have an apical growth organized by a Spitzenkörper (Girbardt 1957, 1969; Steinberg 2007; Jones & Sudbery 2010) and the capability to produce complex networks of macroscopic dimensions. However, these structures never are tissues as in plants. This holds also for rather tight structures, as for example those of sclerotia. During evolution, hyphae and hyphal systems have undergone remarkable adaptive changes convergently, certainly as a response to environmental conditions.
Fig. 6: Conocybe subovata (a) and C. lactea (b-f). a: Basidiocarp and longitudinal section of cap. b: Swollen subglobose subhymenial hyphae showing a sequence of cells in a generative hypha (arrows). c: Part of the hymenium with basidia of different developmental stages. d: Detail of stipe surface with a cluster of cystidioles. e: Longitudinal section of cap showing specialized hyphal structures. f: Thick-walled basidiospore with germ pore (arrow). Bar for microscopic figures 20 µm and 10 µm for the basidiospore. Orig. F. Oberwinkler.
Evolutionary trends in basidiomycetous hyphae and hyphal systems:
Hyphae monokaryotic > multinucleate > dikaryotic > diploid
Hyphae with clamps > without clamps?
Hyphae cylindrical > swollen > globose
Hyphae thin-walled > thick-walled
Hyphal system monomitic > dimitic > trimitic
Hyphal system monomitic > sarcodimitic > sarcotrimitic
Cell walls hyaline > pigmented
In the majority of basidiomycetous fungi the monokaryotic state is comparatively short (Fig. 4, d 1), the dikaryon, however, extends to most of the vegetative and generative parts. Molecular communication occurs between the paired nuclei of a dikaryon (Anderson & Kohn 2007). Also fruiting in a monokaryotic or diploid state is occasionally possible. – Multinucleate hyphae occur in the fern parasite Mixia osmundae (Nishida et al. 1995), a species that has a basal position in phylogenetic dendrograms based on molecular data. In addition, highly multinucleate hyphal cells are known from Heterobasidion annosum (Korhonen 1978, Chase et al. 1983) and from Agaricus bisporus (Raper et al. 1972).
Hyphae with and without clamps are more or less equally frequent in Basidiomycota. Clamps are not required for extending the dikaryon. There is no doubt that clamps and croziers are homologous in structure and function (Anderson & Kohn 2007). However, it remains unclear when and where they evolved, and it is unlikely that they have multiple convergent origins.
Generative hyphae and basidia are nearly always thin-walled, as are hyphae in short living basidiocarps or parts of them, e.g. in most Agaricales and Boletales, and many other Basidiomycota. Swelling of thin-walled hyphae during basidiocarp development is often correlated with the expansion of a pileus, as in Russulales and Agaricales (Fig. 6 b, c, e). – Gloeoplerous hyphae may well represent a synapomorphy in Russulales (Fig. 49).
Thick-walled hyphae have been evolved manifold convergently, for example in the Polyporales (Figs. 13 b, 43), the Hymenochaetales (Fig. 42) an some Russulales (Fig. 49). Also di- and trimitic hyphal systems (Corner 1932) are the result of convergent adaptive radiations in several groups of the Agaricomycotina. Such structures lack in Pucciniomycotina and Ustilaginomycotina, and they are restricted to higher evolved taxa in the Agaricomycotina (Fig. 7). Sarcodimitic and -trimitic hyphal systems (Corner 1966) have also to be considered as derived but may have gone lost, too (Readhead 1987). The hyphal systems of the stipititrama of Oudemansiella and Xerula, or sections of Oudemansiella could not used by Yang et al. (2009) for meaningful characterisation of these taxa.
Coprinopsis cinerea is an experimental model for studying the multicellular development in fungi (Stajich et al. 2010). The 37-megabase genome was sequenced and assembled into 13 chromosomes. This is an essential resource in understanding the evolution of multicellularity in Basidiomycota.
Fig. 7: Main distribution of complex hyphal systems marked in red. The phylogram is a compilation from data of various authors.
Cystidia are lacking in Pucciniomycotina, rather rare in Ustilaginomycotina, and sparsely distributed in basal lineages of the Agaricomycotina. In contrast, cystidia originated in a huge diversity convergently in derived Agaricomycotina, and they are not homologous in many cases. Cystidia are very often thick-walled. Pigmentation of cell walls and also of cytoplasmatic components is another derived character in many basidiomycetous fungi, possibly often correlated with protective functions.
The basidium is a multifunctional cell for the essential steps in sexual reproduction, i.e. karyogamy and meiosis (Figs. 3, 4 d 3). Basidiospores are developed outside of the meiosporangium. Development and morphology of basidia vary considerably. This variation requires closer consideration.
When a terminal hyphal cell functions as a meiosporangium, finally four haploid nuclei are in that cell. The simplest way to use these nuclei for dispersal is a compartmentation of the hyhal-like meiosporangium by three transverse septa, thus forming four haploid cells. In fact, under experimental conditions, auricularioid basidial cells may produce yeasts, ballistospores, microconidia or hyphae (Bauer & Oberwinkler 1986a,b) or may even disintegrate and function as propagules themselves. Such behavior is still different from ascospore formation inside the meiosporangium. Depending on the meiosporangial cell shape, basidial fragmentation may vary from transverse to longitudinal inclusive of oblique septa.
Fig. 8. Some basidial types, not to scale. Transversally septate: a Puccinia, rust fungi. b Heterogastridium, Pucciniomycotina. c Microbotryum, Microbotryomycetes. Holobasidia in the Ustilaginomycotina: d Entyloma, f Neovossia, g Exobasidium. e Longitudinally septate phragmobasidium of Tremella. Holobasidia: h Dacrymyces, i Tulasnella, j Botryobasidium. g SEM Orig. P. Blanz. Orig. F. Oberwinkler.
Evolutionary trends in basidial morphology:
Phragmobasidia > holobasidia
Meiosporangium transversally septate > holobasidium
Meiosporangium transversally septate > longitudinally septate > holobasidium
No probasidium > probasidium thin-walled > thick-walled (teliospore)
Fig. 9: Main distribution of phragmobasidial taxa marked in red. The phylogram is a compilation from data of various authors.
Phragmobasidia are restricted to Pucciniomycotina, Ustilaginomycotina, and the basal Agaricomycotina Tremellales, Sebacinales, and Auriculariales (Fig. 9). This distribution pattern certainly reflects an important evolutionary trend from phragmo- to holobasidia. However, it has to be considered that within these phragmobasidial groups frequent evolutionary transitions from phragmo- to holobasidia took place (Figs. 10, 19, 24, 36). These cases do not contradict the above interpretation, as do not the transitions from transversally to longitudinally septate meiosporangia (Oberwinkler 1982). In the Ustilaginomycotina phragmobasidia occur only in the Ustilaginaceae and few other taxa, while holobasidiate species are present in all orders, inclusive of those that are considered as basal ones. In the Pucciniomycotina holobasidia occur in Chionosphaera and Pachnocybe.
A probasidium may be defined as a terminal cell of a hypha in which karyogamy takes place. Such cells need not to change their morphology. When meiosis also occurs in the same cell, more space is needed. Such a precondition may initiate the broadening of a premeiotic cell that is called probasidium. Often probasidia function as resting spores, structurally recognizable by considerably thickened cell walls, and often called teliospores (Figs. 10 b, 26, 32, 33, 36, 37, 39).
Fig. 10. Some basidial types of Tremellomycetes. a Tremella mesenterica, b Cystofilobasidium capitatum, c Filobasidium floriforme, d Filobasidiella neoformans. Orig. F. Oberwinkler.
Evolutionary trends in basidial sterigmata and basidiospore release:
Sterigmata curved > straight > reduced > lacking
Sterigmata lateral > terminal
Sterigmata 4 > 2 > 1 sterigma
Sterigmata 4 > more than 4
Sterigmata long > sterigmata lacking
Basidiospores budding off > forcible discharge > passive release
The most important structural and functional feature in basidiomycetous fungi is the sterigma and its ballistosporic mechanism (Figs. 4 c, e, 8 g, i, j, 36, 47 g). Basidia that forcibly discharge basidiospores have curved sterigmata with very thin terminal spicula and asymmetrically growing out basidiospores. This is a good example of structural prerequisites for a specific function that always should be illustrated correctly. Changes in the sterigma morphology indicate the loss of active spore discharge. – The transition of auricularioid basidia to holobasidiate ones is always coordinated with a terminal arrangement of sterigmata. – Reduction of sterigmata from four to two occurs in many relationships indepently, the reduction to only one sterigma, however, is rare. Also, the increase of sterigmata (Fig. 8 g, j) is comparatively rare and scattered in unrelated taxa.
A remarkable diversity of structural and functional features have evolved in basidiospores, most of them as a result of adaptive radiation.
Evolutionary trends in basidiospores:
Spore wall thin > thick > without germ pore > with germ pore
Spore wall hyaline > pigmented
Spore wall smooth > ornamented
Spore unicellular > bicellular > multicellular
Spore germination variable, with yeasts, secondary ballistospores, conidia, and/or hyphae > hyphae
Unicellular, hyaline, thin- and smooth-walled basidiospores are predominant in most of the Basidiomycota. Few important exceptions are mentioned here: the russuloid basidiospore (Fig. 49) is unique in cell wall ultrastructure and the amyloid reaction of the spore ornament. In Hymenochaetales (Fig. 42) basidiospores are mostly hyaline and thin-walled, but thick-walled and pigmented ones also occur. Boletales have thick-walled and often intensively pigmented spores (Fig. 52), occasionally also strongly ornamented spore walls as in Strobilomyces. The evolutionary trends in basidiospore features of Agaricales were highlighted by Garnica et al. (2007).
In comparison to Ascomycota, multicellular meiospores are rare in Basidiomycota. Notable exceptions can be found in the Exobasidiales (Fig. 36), Cryptobasidiales (Fig. 36), and Dacrymycetales (Fig. 40). The convergent origin and functional aspects of these spore types can not be explained yet.
Often basidiospore germination in Pucciniomycotina and Ustilaginomycotina as well as in basal groups of the Agaricomycotina is unfixed, i.e. yeasts, secondary spores, microconidia or hyphae may primarily develop. The huge bulk of higher Agaricomycotina species has basidiospores that germinate exclusively with hyphae.
Basidiocarps evolved from simple to complex structures many times convergently, thus improving the efficiency of spore production quantitatively and of dispersal mechanisms qualitatively. The evolution of structurally increasing complexity in basidiocarps appears to be a highly intricate process. In a phylogenetic hypothesis of the Auriculariales (Fig. 41), for example the Myxarium and Auricularia clades may indicate progressive evolutionary lines (Weiß & Oberwinkler 2001) towards stalked-capitate and cyphelloid, respectively.
A high diversity of basidiocarps, hymenial types and trophic stages has been evolved in the Russulales (Fig. 49). The group, recognized already by Malençon (1931) as „La série des Astérosporées“, was characterized and enlarged to cover taxa of nearly all basidiocarp types by Oberwinkler (1977). The order has been confirmed and repeatedly studied molecularly. In a detailed phylogenetic hypothesis by Miller et al. (2006) Aleurodiscus is included in the Stereaceae, Boidinia and Gloeopeniophora in the Russulaceae together with well-known sequestrate genera, Heterobasidion in the Bondarzewiaceae, Laxitextum and Dentipellis in the Hericiaceae, Leucogaster in the Albatrellaceae, Gloidon and Lentinellus in the Auriscalpiaceae, and inter alia Scytinostroma and Vararia in the Peniophoraceae. Species of the Albatrellaceae and Russulaceae are ectomycorrhizal, but probably not the Boidinia species that cluster with the Russulaceae. In total, evolutionary changes in basidiocarp morphology led from simple to agaricoid structures and finally, many times convergently to gasteroid and hypogeous forms. The evolutionary progression of gasteromycetation in the Russulaceae has been depicted as a series by Albee-Scott (2007) from the epigeous Russula romellii to the hypogeous Macowanites americanus, and finally to the hypogeous Gymnomyces abietis, and also in the Albatrellaceae from „Polyporus“ sylvestris over Mycolevis siccigleba to Leucophlebs spinispora.
Evolutionary trends in basidiocarps:
Basidiocarp inconspicuous > corticioid > odontioid, irpicoid, merulioid, porioid
Basidiocarp inconspicuous > cyphelloid, clavarioid, hydnoid
Basidiocarp inconspicuous > cantharelloid, boletoid
Basidiocarp inconspicuous > ...... agaricoid > cyphelloid
Various basidiocarp types > gasteroid
Molecular data of Boletales (Binder & Hibbett 2006) allow the interpretation of evolutionary trends in basidiocarps from resupinate or polyporoid to agaricoid and boletoid as well as frequent convergent gasteromycetation processes (Fig. 52). The authors assume that the ancestor was a brown-rot producing fungus with morphologically simple basidiocarps.
Fig. 11. The multiple convergent evolution of basidiocarps in proposed monophyla of the former Basidiomycetes is illustrated in this scheme from premolecular times, modified after Oberwinkler (1977). In Homobasidiomycetes the orders Hymenochaetales, Polyporales, Boletales, Russulales and Thelephorales were distinguished. Russulales, marked in red, was of specific interest to document the new systematics. The Agaricales could not be resolved, however genera of clear affinities to the other orders were transferred to them. While secotioid taxa were included in their proper relationships, the non-secotioid Gasteromycetes could not be affiliated with any hymenomycetous fungi. Also some heterobasidiomycetous orders, the Auriculariales, Dacrymycetales, and in part the Uredinales, were included in that scheme. Already at that time, several gastroid Heterobasidiomycetes had been recognized. Finally, it was obvious that basidiomycetous yeasts are restricted to heterobasidiomycetous relationships.
Even in trees with other focus (e.g. Garcia-Sandoval et al. 2011) and therefore very selective samplings for Russulales and Boletales, the evolutionary trends mentioned above, are confirmed.
In a comprehensive molecular study of cyphellaceous fungi, Bodensteiner et al. (2004) concluded that cyphelloid forms have about 12 or more independent origins within the Agaricales. There are many more in other relationships of the Agaricomycotina, e.g. the Auriculariales (Fig. 41) or Dacrymycetales (Fig. 40).
The regressive, polyphyletic process of gasteromycetation (Fig. 12) occurs in many basidiomycetous relationships and is well studied and documented in several cases.
The evolutionary trends for multiple convergent evolution of sequestrate forms are definitely unidirectional from hymenomycetoid to gasteroid types, well documented by secotioid taxa (Fig. 13), comparative micromorphology, and molecularphylogenetic hypotheses. Gasteromycetes that could not be affiliated to Hymenomycetes on morphological grounds (Oberwinkler 1977, Fig. 11) are now integrated in diverse relationships of the Agaricomycotina through molecular data, like the gomphoid-phalloid clade (Phallomycetidae, Hosaka et al. 2006) with the Geastrales, Hysterangiales, and Phallales.