The Irreversible Loss of a Decomposition Pathway Marks the Single Origin of an Ectomycorrhizal Symbiosis
Open Access
- 18 July 2012
- journal article
- research article
- Published by Public Library of Science (PLoS) in PLOS ONE
- Vol. 7 (7), e39597
- https://doi.org/10.1371/journal.pone.0039597
Abstract
Microbial symbioses have evolved repeatedly across the tree of life, but the genetic changes underlying transitions to symbiosis are largely unknown, especially for eukaryotic microbial symbionts. We used the genus Amanita, an iconic group of mushroom-forming fungi engaged in ectomycorrhizal symbioses with plants, to identify both the origins and potential genetic changes maintaining the stability of this mutualism. A multi-gene phylogeny reveals one origin of the symbiosis within Amanita, with a single transition from saprotrophic decomposition of dead organic matter to biotrophic dependence on host plants for carbon. Associated with this transition are the losses of two cellulase genes, each of which plays a critical role in extracellular decomposition of organic matter. However a third gene, which acts at later stages in cellulose decomposition, is retained by many, but not all, ectomycorrhizal species. Experiments confirm that symbiotic Amanita species have lost the ability to grow on complex organic matter and have therefore lost the capacity to live in forest soils without carbon supplied by a host plant. Irreversible losses of decomposition pathways are likely to play key roles in the evolutionary stability of these ubiquitous mutualisms.This publication has 47 references indexed in Scilit:
- Living inside plants: bacterial endophytesCurrent Opinion in Plant Biology, 2011
- Evolutionary transitions in bacterial symbiosisProceedings of the National Academy of Sciences of the United States of America, 2011
- Genome and transcriptome analyses of the mountain pine beetle-fungal symbiont Grosmannia clavigera , a lodgepole pine pathogenProceedings of the National Academy of Sciences of the United States of America, 2011
- Economic contract theory tests models of mutualismProceedings of the National Academy of Sciences of the United States of America, 2010
- TOPALi v2: a rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktopsBioinformatics, 2008
- A Rapid Bootstrap Algorithm for the RAxML Web ServersSystematic Biology, 2008
- Worlds within worlds: evolution of the vertebrate gut microbiotaNature Reviews Microbiology, 2008
- Isolation of Fungal Cellobiohydrolase I Genes from Sporocarps and Forest Soils by PCRApplied and Environmental Microbiology, 2008
- Major evolutionary transitions in ant agricultureProceedings of the National Academy of Sciences of the United States of America, 2008
- Phylogenies and the Comparative MethodThe American Naturalist, 1985