l e t t e r sTo elucidate the genetic bases of mycorrhizal lifestyle evolution, we sequenced new fungal genomes, including 13 ectomycorrhizal (ECM), orchid (ORM) and ericoid (ERM) species, and five saprotrophs, which we analyzed along with other fungal genomes. Ectomycorrhizal fungi have a reduced complement of genes encoding plant cell walldegrading enzymes (PCWDEs), as compared to their ancestral wood decayers. Nevertheless, they have retained a unique array of PCWDEs, thus suggesting that they possess diverse abilities to decompose lignocellulose. Similar functional categories of nonorthologous genes are induced in symbiosis. Of induced genes, 7-38% are orphan genes, including genes that encode secreted effector-like proteins. Convergent evolution of the mycorrhizal habit in fungi occurred via the repeated evolution of a 'symbiosis toolkit', with reduced numbers of PCWDEs and lineage-specific suites of mycorrhiza-induced genes.Fungi are often described as either saprotrophs, which degrade complex organic substrates, or biotrophs, which obtain carbon compounds from living hosts. Among the latter, ECM fungi provide crucial ecological services in interacting with forest trees. They are portrayed as mutualists trading host photoassimilates for nutrients and having limited capacity to decompose soil lignocellulose 1-3 , as a result of their reduced repertoire of PCWDEs 4-6 . However, recent studies are challenging this view [7][8][9][10] . An improved understanding of the ability of ECM fungi to decompose lignocellulose is needed to resolve mechanisms of nutrient cycling in forests. The ECM lifestyle in Laccaria bicolor is associated with the expression of new mycorrhizainduced small secreted proteins (MiSSPs) that are required for establishment of symbiosis 11,12 . Mycorrhizal symbioses have arisen repeatedly during fungal evolution and include not only ECM associations but also those with ERM and ORM mycorrhizae 13 . It is not known whether these symbioses share the genomic features found in L. bicolor 4 and Tuber melanosporum 5 . Here we assess whether there Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists
TTh he e p pl la an nt t c ce el ll l w wa al ll l d de ec co om mp po os si in ng g m ma ac ch hi in ne er ry y u un nd de er rl li ie es s t th he e f fu un nc ct ti io on na al l d di iv ve er rs si it ty y o of f f fo or re es st t f fu un ng gi i T Th he e p pl la an nt t c ce el ll l w wa al ll l d de ec co om mp po os si in ng g m ma ac ch hi in ne er ry y u un nd de er rl li ie es s t th he e f fu un nc ct ti io on na al l d di iv ve er rs si it ty y o of f f fo or re es st t f fu un ng gi i
Summary• Parasitism and saprotrophic wood decay are two fungal strategies fundamental for succession and nutrient cycling in forest ecosystems. An opportunity to assess the trade-off between these strategies is provided by the forest pathogen and wood decayer Heterobasidion annosum sensu lato.• We report the annotated genome sequence and transcript profiling, as well as the quantitative trait loci mapping, of one member of the species complex: H. irregulare. Quantitative trait loci critical for pathogenicity, and rich in transposable elements, orphan and secreted genes, were identified.• A wide range of cellulose-degrading enzymes are expressed during wood decay. By contrast, pathogenic interaction between H. irregulare and pine engages fewer carbohydrate-active enzymes, but involves an increase in pectinolytic enzymes, transcription modules for oxidative stress and secondary metabolite production.• Our results show a trade-off in terms of constrained carbohydrate decomposition and membrane transport capacity during interaction with living hosts. Our findings establish that saprotrophic wood decay and necrotrophic parasitism involve two distinct, yet overlapping, processes.
A fluctuating environment may facilitate co-existence of species, and high species richness may be important for maintaining ecosystem processes under changing environmental conditions. A positive relationship has been found between species richness and primary production in many experiments, and there is now an increasing interest whether similar relationships also apply to microorganisms and decomposition. Basidiomycete fungi are the primary decomposers of wood with the functional groups brown and white rot fungi, which differ with respect to decay strategy. In this study, 16 species of boreal wood decay fungi, 8 brown rot fungi and 8 white rot fungi, were assembled in artificial communities. The aims were to study species persistence, wood decomposition and metabolic efficiency in fungal communities of increasing levels of species richness under constant and fluctuating temperature regimes. Species persistence was generally low, but temperature fluctuations facilitated co-existence of species. Decomposition was highest at intermediate diversity levels under the fluctuating temperature regime. Metabolic efficiency, estimated as the amount of fungal mycelium formed per amount of degraded wood, decreased with increasing community complexity under the fluctuating temperature regime. Brown and white rot fungi differed in decomposition rates and metabolic efficiency, but no synergistic effects were found where the two functional groups were mixed. This study demonstrates how niche differentiation in a variable environment may act to maintain diversity and function. In our experiment, differences in functional responses to the varying temperature rather than resource partitioning between brown and white rot fungi had significant effects. Niche differentiation is likely to be particularly important in maintaining species diversity in communities of wood decaying fungi, which are known from previous studies to be characterised by intense competition, and where otherwise metabolically costly interactions lead to species exclusion and dominance by highly competitive species.
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