Evolutionary trends in basidiomycetous wood-decay fungi
White rot > brown rot > successive degradation of lignin
Wood decay (Fig. 17) is one of the most important ecological functions in Basidiomycota that evolved in complex interrelationships with climax vegetations dominated by trees. Decomposition of wood is an intergrading process of parasitism and saprophytism. Many wood decay fungi start with parasitic phases endophytically, often causing the death of their hosts, and finally continue to break down dead wood. The distinction of white and brown rot is sometimes important, but not always clearly distinctive. In white rot, lignin and cellulose are degraded, while in brown rot lignin remains to a high percentage. White rot is considered as plesiomorphic and brown rot as several times convergently derived (Hibbett & Donoghue 2001). Even when most wood-decay species are white rots, the brown rots associated with coniferous wood are the most important decomposers in boreal forests. The lignin residues bind nitrogen and cations, thus being essential in nutrient-poor, acidic soils of conifer forests in the Northern Hemisphere. How cellulolysis functions in absence of ligninolysis in brown rots is not known Eastwood et al. (2011).
The Dacrymycetales constitutes a monophylum in a rather basic position of the Agaricomycotina (Fig. 17). Basidiocarps are typically gelatinous, basidia two-sterigmate, and basidiospores nearly always septate and germinating with microconidia (Fig. 40). In a well developed stage most species synthesize carotenoids. Dacrymycetales live on wood of conifers and deciduous trees and play an important role in wood decay, predominantly in very early stages of the decomposition and in many cases on fully exposed wood. Quick changes in the water content of the substrate can interrupt the growth and wood decay, but re-soakening will initiate these activities immediately. Seifert (1983) studied the wood decay caused by 17 species of the Dacrymyetales. He found typical brown-rotted wood, but also the capability of removing significant amounts of lignin in many species, including Dacrymyces stillatus, D. capitatus, D. dictyosporus, Dacryopinax spathularia, Calocera cornea, C. lutea, and Cerinomyces ceraceus.
Traditionally, generic concepts in Dacrymycetales are based on basidiocarp morphology, hyphal and spore characeristics (Oberwinkler 1993). Few and fragmentary phylogenetic hypotheses, based on molecular data available at present, do not support older systematic arrangements.
Fig. 40. Ontogeny of Dacrymyces stillatus and traditional genera of the Dacrymycetales, defined by basidiocarp morphology. Two-sterigmate basidia, septate basidiospores, microconidia and gelatinous basidiocarps characterize most of the Dacrymycetales species. Genera can by classified in a cyphelloid and a clavarioid group. However, this groupings appear not to reflect phylogenetic processes. Orig. F. Oberwinkler.
Formerly, the Auriculariaceae were included in the Tremellales s.l., and circumscribed by species with auricularioid, i.e. mature transversaly septate basidia. However, considering septal pore ultrastructure, spore germination, and substrate dependencies, allowed new circumscriptions of Auriculariales and Tremellales. Poroid Tremellaceae, like Aporpium caryae, Protodaedalea japonica and Protomerulius brasiliensis, as studied by Bandoni et al. (1982) are Auriculariales with longitudinally septate basidia. Based on molecular data, Weiß & Oberwinkler (2001) proposed a phylogenetic hypothesis for the Auriculariales with five groups (Fig. 41): (1) Myxarium and Hyaloria with sphaerpedunculate basidia; (2) Basidiodendron species with globose spores and gloeocystidia; (3) Bourdotia and Ductifera with gloeocystidia; (4) Heterochaetella, Protodontia, Protomerulius, and Tremellodendropsis; (5) Auricularia, Exidia, Exidiopsis, Heterochaete and Eichleriella.
Evolutionary trends in Auriculariales:
Basidiocarp resupinate > stalked
Hymenium smooth > odontioid > hydnoid
Basidia auricularioid > tremelloid
Cystidia lacking > gloeocystidia
White rot > brown rot
Most Auriculariales are white rot fungi, like species of Aporpium, Auricularia, Ductifera, Eichleriella, Exidia, Exidiopsis, Heterochaete, Myxarium, and Protodaedalea, but Tremiscus helvelloides causes a brown rot and Pseudohydnum gelatinosum is reported as a white and brown rot fungus (Seifert 1983).
Fig. 41. Macro- and micromorphology of basidiocarps, dolipore with parenthesomes and phylogenetic hypothesis for representative species and genera of the Auriculariales. a Auricularia auricula-judae, b Exidiopsis effusa, c dolipore with continuous parenthesomes. The colored dots in the dendrogram refer to positions of species and genera in the phyogenetic tree. Neighbour-joining analysis of an alignment of nuclear DNA coding for the 5h terminal domain of the 28 S ribosomal large subunit. Genetic distances were computed according to the Kimura two-parameter model. Branch lengths are scaled in terms of expected numbers of nucleotide substitutions per site. Dendrogram from Weiß & Oberwinkler (2001). Septal pore orig. R. Bauer, illustrations orig. F. Oberwinkler.
Species of Hymenochaete, Hydnochaete, Clavariachete, Inonotus, Phellinus, Cyclomyces, and related surrogate genera often share dimitic hyphal systems (Fig. 42), thick walled, brown setae, the lack of clamps, brown hyphal pigments darkening with KOH, and exoenzymes that degrade cellulose and lignin, thus causing white rot. Basidiocarps (Fig. 42) evolved from corticioid-stereoid to hydnoid and clavarioid, as well as to polyporoid and stalked ones with pilei and hymenia with pores or the unique concentrically arranged lamellae.
Phylogenetic hypotheses based on molecular data broadened the scope of the order to include the Hyphodontia clade and Tubulicrinis spp., and very surprisingly the Rickenella clade comprising also Hyphoderma praetermissum and Resinicium spp. (Larsson et al. 2006).
Evolutionary trends in Hymenochaetales:
Basidiocarp corticioid > stereoid > odontioid > clavarioid > polyporoid > agaricoid // no gasteroid forms
Parasitic < > saprobic > specific successions of lignin degraders
Host specificity broad > narrow > cospecific
Wood decay not selective > restricted to heart-wood
Wood decay > mycorrhizae
Fig. 42. Hymenochaetales s.str. The micromorphology of the Hymenochaetales has a unique set of features as illustrated in the hymenial part. Traditionally, genera were circumscribed and named according to their habit appearance and easily recognizable macroscopic characters, as Hymenochaete, Hydnochaete, Calvariachaete, or Cyclomyces. The adaptation to exposed habitats, as on trunks of trees nearly up to the crowns, required traits of structural changes to fulfill functionality, as the „woody“ context of the console-like fructifications in Phellinus and many other species. The perennial life strategy was based on the tough dimitic hyphal system allowing thin-walled generative hyphae to survive inside the fructification and to add new hymenial layers to the polyporous underside under favorable weather conditions. Illustrations not to scale. Orig. F. Oberwinkler.
Strong parasitism on trees is wide spread within the Hymenochaetales, as is shown by the short living Inonotus hispidus on Malus and other hosts, as well as by perennial ones, like Phellinus cinereus and P. nigricans on Betula, P. hartigii on Abies, P. pini on Pinus, P. pomaceus on Prunus, P. populicola and P. tremulae on Populus, P. robustus on Quercus, and many others. The examples document high host specifities as a common feature in these wood decayers. Also many stereoid Hymenochaete species are highly specialized: H. carpatica on Acer pseudoplatanus, H. cinnamomea on Corylus, H. mougeotii on Abies, H. rubiginosa and H. subfuliginea on Quercus, H. tabacina on Salix, and others.
Molecular phylogenetic hypotheses include also very inconspicuous fungi in the Hymenochaetales, for example Sphaerobasidium and Repetobasidium species that occur exclusively on strongly brown-rotted wood, and that obviously are capable for further degrading such substrates.
In ectomycorrhizal fungal successions of Pinus banksiana stands following wildfire, a distinct sequence of early-stage ectomycorrhizal fungi, including the hymenochaetoid Coltricia perennis, was found by Visser (1995). Tedersoo et al. (2007) detected ectomycorrhizae of Coltricia and Coltriciella on Caesalpiniaceae, Dipterocarpaceae and Myrtaceae in the Seychelles. The evolutionary switches from wood decay to mycorrhizal associations remain unclear.
Polyporales and related wood-decay fungi
To trace evolutionary trends, the organisms considered must be monophyletic. Recent phylogenetic hypotheses confirmed the Polyporales as a monophylum (e.g. Hibbett et al. 2007, Larsson 2007, Garcia-Sandoval et al. 2011), however its higher level relationships varied considerably. The core Polyporales (Fig. 43) are white-rot fungi comprising taxa with a broad range of basidiocarps (Fig. 11).
Fig. 43. Polyporales, micromorphology and basidiocarps. Di- and trimitic hyphal systems are common in Polyporales. Basidicarps are often console-like or stalked, rarely gastroid as in Cryptoporus, and they can originate from sclerotia, ramify and terminate with many distinct pilei. Porioid hymenia are most frequent, but stereoid and agaricoid ones occur, too. Orig. F. Oberwinkler.
Also species of the phlebioid clade produce a white rot, but the Antrodia clade shares brown rot species with the reversal of Grifola frondosa to white rot (Garcia-Sandoval et al. 2011).
The Gloeophyllales comprise corticioid to stereoid species (Veluticeps, Boreostereum, Chaetodermella), polypores (Gloeophyllum), and agarics (Neolentinus, Heliocybe), most of which grow on coniferous wood and cause a brown rot. Relaxed molecular clock analyses indicate that the Gloeophyllales arose in the Cretaceous, when the Pinaceae were already present (Garcia-Sandoval et al. 2011).
In the recently described Amylocorticiales, Anomoloma produces a white rot, some Anomoporia species are associated with brown rot, and wood-decay characteristics in other species are not known. (Binder et al. 2010).
Wood-decay by species of the Russulales, Boletales, and Agaricales will be discussed briefly in connection with the origin of ectomycorrhizae in these orders.