Evolutionary dynamics of host specialization in wood-decay fungi

Franz-Sebastian Krah,Claus Bässler,Christoph Heibl,David S Hibbett,John Soghigian,Hanno Schaefer

doi:10.1186/s12862-018-1229-7

Abstract

BackgroundThe majority of wood decomposing fungi are mushroom-forming Agaricomycetes, which exhibit two main modes of plant cell wall decomposition: white rot, in which all plant cell wall components are degraded, including lignin, and brown rot, in which lignin is modified but not appreciably removed. Previous studies suggested that brown rot fungi tend to be specialists of gymnosperm hosts and that brown rot promotes gymnosperm specialization. However, these hypotheses were based on analyses of limited datasets of Agaricomycetes. Overcoming this limitation, we used a phylogeny with 1157 species integrating available sequences, assembled decay mode characters from the literature, and coded host specialization using the newly developed R package, rusda.ResultsWe found that most brown rot fungi are generalists or gymnosperm specialists, whereas most white rot fungi are angiosperm specialists. A six-state model of the evolution of host specialization revealed high transition rates between generalism and specialization in both decay modes. However, while white rot lineages switched most frequently to angiosperm specialists, brown rot lineages switched most frequently to generalism. A time-calibrated phylogeny revealed that Agaricomycetes is older than the flowering plants but many of the large clades originated after the diversification of the angiosperms in the Cretaceous.ConclusionsOur results challenge the current view that brown rot fungi are primarily gymnosperm specialists and reveal intensive white rot specialization to angiosperm hosts. We thus suggest that brown rot associated convergent loss of lignocellulose degrading enzymes was correlated with host generalism, rather than gymnosperm specialism. A likelihood model of host specialization evolution together with a time-calibrated phylogeny further suggests that the rise of the angiosperms opened a new mega-niche for wood-decay fungi, which was exploited particularly well by white rot lineages.

Highlights

The majority of wood decomposing fungi are mushroom-forming Agaricomycetes, which exhibit two main modes of plant cell wall decomposition: white rot, in which all plant cell wall components are degraded, including lignin, and brown rot, in which lignin is modified but not appreciably removed
For Hyphoderma we used only the two species where decay mode references were found. To estimate how this strategy might affect our interpretations, we re-sampled a single species per genus from our final dataset and repeated the analyses described below 100 times
Phylogenetic signal For decay mode, we found a phylogenetic D value of − 0.38, which had a high probability resulting from a Brownian motion phylogenetic structure (P = 0.998) and a corresponding low probability resulting from a random phylogenetic structure (P = 0.00, Fig. 3a)

Summary

Introduction

The majority of wood decomposing fungi are mushroom-forming Agaricomycetes, which exhibit two main modes of plant cell wall decomposition: white rot, in which all plant cell wall components are degraded, including lignin, and brown rot, in which lignin is modified but not appreciably removed. Previous studies suggested that brown rot fungi tend to be specialists of gymnosperm hosts and that brown rot promotes gymnosperm specialization. These hypotheses were based on analyses of limited datasets of Agaricomycetes. Overcoming this limitation, we used a phylogeny with 1157 species integrating available sequences, assembled decay mode characters from the literature, and coded host specialization using the newly developed R package, rusda. Woody plant cell walls consist mainly of the lignocellulose complex which is composed of the polymeric polysaccharides cellulose, hemicellulose and lignin heteropolymers [4, 5]. Angiosperms often have lower amounts of non-structural secondary compounds (plant extractives) than gymnosperms [12,13,14,15], with some exceptions, e.g., species of the genera Quercus, Fagus or Malus [16]

Methods

Results

Discussion

Conclusion