When colonizing land habitats, the availability of sufficient water and nutrients was a challenge for plants, and mutualistic associations of thalli and roots with fungi were the most important coevolutionary processes. Arbuscular mycorrhizae (Figs. 2, 3) are known from the Ordovician (Redecker et al. 2000) and they are most common mycorrhizal partners in all groups of land plants. The evolutionary switch of certain ecologically most important plant groups to other fungi to improve symbiosis, is not yet understood. Climax vegetations in temperate zones of the Northern and partly the Southern Hemisphere are in fact obligate ectomycorrhizal communities with trees of the Pinaceae, Fagales and Salicaceae. In plant associations dominated by Ericales the ericoid mycorrhizae play an essential role. Early ontogenetic stages in orchid development depend on specific endotrophic fungal partners, and heterotrophic orchids require an obligat mycorrhization.
In Sebacinales all mycorrhizal types occur that are known in Basidiomycota. Tulasnellales appear to be frequent in orchid mycorrhizae and in Aneuraceae, but also occur in the main autotrophic partners, the Pinaceae and the Fagales.
Evolutionary trends in mycorrhizae:
Root associated fungi > hyphal sheaths > intercellular hyphal growth
Root parasites > endophytes > endomycorrhizae
Exclusively mycorrhizal: Sebacinales
Exclusively ectomycorrhizal: Thelephorales
Saprobic > ectomycorrhizal: Cantharellales, Gomphales
Wood decay > ectomycorrhizal: Russulales, Atheliales, Boletales, Agaricales
Fig. 44. Sebacina epigaea in a mixed forest with fructifications on soil (arrows and insert to the right). The ectomycorrhizal species are associated with pine roots in this forest, but can grow also on roots of other ectomycorrhizal host trees. Under favorable conditions fructifications appear frequently in autumn. Orig. F. Oberwinkler.
Little attention was paid to mostly inconspicuous Sebacina species and related fungi until their obligatory association with plant roots was detected and molecular screenings revealed an enormous unknown and cryptic diversity (Weiß et al. 2011). It turned out that Sebacinales are mycobionts in ectomycorrhizae of Pinaceae, Fagales, Myrtaceae, and also in Polygonum viviparum (Mühlmann et al. 2008), living in subalpine and alpine grass vegetations. Sebacinales also constitute orchid mycobionts (Warcup 1988, Selosse et al. 2002b, Weiß et al. 2004b, Suárez et al. 2008) and they are capable to form ericoid, arbutoid, and cavendishioid mycorrhizae (Berch et al. 2002, Selosse et al. 2002a, Setaro et al. 2006a,b, Selosse et al. 2007, Kottke et al. 2008). In addition, Sebacinales associate with thalli of jungermannioid liverworts (Kottke et al. 2003, Nebel et al. 2004).
Evolutionary trends in Sebacinales:
Basidiocarps lacking > resupinate > pustulate > erumpent > stereoid > clavarioid
Hyphae thin-walled > thick-walled
Growth saprobic > endophytic > mycorrhizal
Liverwort associates > ectomycobionts of Pinaceae, Fagales and others
Liverwort associates > endomycorrhizae in orchids and Ericales
As in nearly all other monophyla of the Agaricomycotina, also in the Sebacinales basidiocarps evolved from inconspicuous generative hyphal networks to corticioid, pustulate, stalked-stereoid, and clavarioid structures (Fig. 45). More elaborate basidiomata and hymenia, like porioid, hydnoid, or agaricoid are not known. Hyphae are clampless at least in species with basidiocarps. Rarely, thick-walled hyphae occur, as in Sebacina dimitica. Basidia are longitudinally septate, and basidiospores often germinate with secondary spores.
As the Thelephorales, also Sebacinales appear to be exclusively mycorrhizal fungi. Ectomycorrhizae, arbutoid and orchid mycorrhizae have only been found in group A of a phylogenetic tree, while ericoid and cavendishioid mycorrhizae are restricted to group B (Weiß et al. 2004b, Selosse et al. 2007, Weiß et al. 2011). It is premature to interprete evolutionary trends in these clusterings. Also, host specificities cannot be recognized so far. As in other mycorrhizal taxa, major evolutionary steps in land plants, liverworts, Pinaceae, Fagales, Ericales, orchids and others, certainly had a strong influence on adaptive radiations of Sebacinales, but these are not yet understood.
Fig. 45. Fructifications of Sebacinales and micromorphology of Sebacina incrustans. Sebacina species produce resupinate and incrusting basidiocarps on soil, litter and wood on the forest floor. Efibulobasidium and Craterocolla have gelatinous fructifications growing on dead wood. Tremellodendron and Tremelloscypha species grow on the forest floor. The micromorphology of Sebacina incrustans is typical also for other Sebacinales. Orig. F. Oberwinkler.
Because of the unique basidial development and morphology (Fig. 46) and their importance as liverwort and orchid mycorrhizal fungi, it seems appropriate to keep Tulasnellales as an order separate from the Cantharellales.
Fig. 46. Tulasnella spp. a Fully developped basidiocarp of Tulasnella sp. on the underside of a Betula pubescens-trunk. b Hymenium of Tulasnella calospora with different stages of basidial development. c SEM photograph of Tulasnella vermispora, one spore attached to the sterigma. Orig. F. Oberwinkler.
Evolutionary trends in Tulasnellales:
Basidiocarps lacking > resupinate
Hyphae with clamps > unclamped
Growth parasitic? > endophytic > mycorrhizal
Mycothalli > endomycorrhizae in orchids > ectomycorrhizae of Pinaceae, Fagales and others
The thallose species of Aneuraceae, a family of the Metzgeriales, have Tulasnella mycobionts (Nebel et al. 2004, Preussing et al. 2010) and were considered by Krause et al. (2011) as a model of early evolved symbiotic associations. Cryptothallus mirabilis is a myco-heterotrophic liverwort and specialized as an epiparasite on Tulasnella species that form ectomycorrhizae with surrounding trees like Betula pubescens, Pinus pinaster and P. muricata (Bidartondo et al. 2003). – Tulasnella spp. as mycobionts in orchids have been reported from various parts of the world (e.g. Shefferson et al. 2005, 2007, Suárez et al. 2009, Cruz et al. 2010, Yuan et al. 2010). Even when Tulasnellales are the preferred mycobionts of orchids, Sebacinales, Thelephorales, Agaricales, and also Tuberales associate with them.
In a molecular screening of orchid mycorrhizae from Southern Ecuador (Kottke et al. 2009), sequence taxa clustered with the Atractiellomycetes, a relationship of the Pucciniomycotina. A specific cell organelle, the symplechosome (Fig. 16), found in intracellular hyphae, confirmed the molecular identification of these fungi. So far, this finding is unique and requires confirmation trough additional sampling. The origin of these fungi remains unclear. There are no other mycorrhizal fungi known in the Pucciniomycotina and also not in the Ustilaginomycotina.
The cantharelloid clade, as circumscribed in phylogenetic hypotheses by Moncalvo et al. (2006) comprises the genera Botryobasidium, Sistotrema, Clavulina, Multiclavula, Craterellus, Cantharellus, and Hydnum. The authors also included the Ceratobasidiaceae and Tulasnellaceae in the Cantharellales. Species of Botryobasidium and Sistotrema are saprotrophs, Multiclavula species are basidiolichens, and Clavulina, Craterellus, Cantharellus, and Hydnum are ectomycorrhizal fungi. There is no synapomorphy known for the taxa included in the Cantharellales.
Fig. 47. Morphology of Cantharellus cibarius. a-d basidiocarps in different developmental stages, c longitudinal section. e hyphal arrangement of pileus surface, f subhymenial hyphae, g part of the hymenium with basidia of different ages, h basidiospores. After Oberwinkler (1977), modified with additions.
Evolutionary trends in Cantharellales:
Basidiocarps resupinate > clavarioid > stalked capitate
Hymenium smooth > irregular > hydnoid > cantharelloid
Saprotrophic > lichenized
Saprotrophic > ectomycorrhizal
The evolutionary transitions from crustose to cantharelloid fructifications cannot be reconstructed. Also the origin of lichenization remains unclear, but all Multiclavula species are clavarioid. According to the proposed phylogenetic hypothesis of Moncalvo et al. (2006), Cantharellus and related genera constitute a clade separate from Clavulina, thus indicating that ectomycorrhizal fungi evolved at least twice in Cantharellales.