Analysis of the Phlebiopsis gigantea genome, transcriptome and secretome provides insight into its pioneer colonization strategies of wood

PLoS Genet. 2014 Dec 4;10(12):e1004759. doi: 10.1371/journal.pgen.1004759. eCollection 2014 Dec.

Abstract

Collectively classified as white-rot fungi, certain basidiomycetes efficiently degrade the major structural polymers of wood cell walls. A small subset of these Agaricomycetes, exemplified by Phlebiopsis gigantea, is capable of colonizing freshly exposed conifer sapwood despite its high content of extractives, which retards the establishment of other fungal species. The mechanism(s) by which P. gigantea tolerates and metabolizes resinous compounds have not been explored. Here, we report the annotated P. gigantea genome and compare profiles of its transcriptome and secretome when cultured on fresh-cut versus solvent-extracted loblolly pine wood. The P. gigantea genome contains a conventional repertoire of hydrolase genes involved in cellulose/hemicellulose degradation, whose patterns of expression were relatively unperturbed by the absence of extractives. The expression of genes typically ascribed to lignin degradation was also largely unaffected. In contrast, genes likely involved in the transformation and detoxification of wood extractives were highly induced in its presence. Their products included an ABC transporter, lipases, cytochrome P450s, glutathione S-transferase and aldehyde dehydrogenase. Other regulated genes of unknown function and several constitutively expressed genes are also likely involved in P. gigantea's extractives metabolism. These results contribute to our fundamental understanding of pioneer colonization of conifer wood and provide insight into the diverse chemistries employed by fungi in carbon cycling processes.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Basidiomycota / genetics*
  • Basidiomycota / growth & development*
  • Basidiomycota / metabolism*
  • Cell Wall / genetics
  • Cell Wall / metabolism
  • Cellulose / metabolism
  • Fungal Proteins / metabolism*
  • Gene Expression Regulation, Fungal
  • Genome, Fungal*
  • Lignin / metabolism
  • Molecular Sequence Annotation
  • Transcriptome
  • Wood / metabolism
  • Wood / microbiology*

Substances

  • Fungal Proteins
  • lignocellulose
  • Cellulose
  • Lignin

Grants and funding

The major portions of this work were performed under US Department of Agriculture Cooperative State, Research, Education, and Extension Service Grant 2007-35504-18257 (to DC and RAB). The US Department of Energy Joint Genome Institute is supported by the Office of Science of the US Department of Energy under Contract DE-AC02-05CH11231. This work was also supported by the HIPOP (BIO2011-26694) project of the Spanish Ministry of Economy and Competitiveness (MINECO) (to FJRD), the PEROXICATS (KBBE-2010-4-265397) and INDOX (KBBE-2013-.3.3-04-613549) European projects (to ATM), and the Chilean National Fund for Scientific and Technological Development Grant 1131030 (to LFL). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.