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Title: Evolution of substrate-specific gene expression and RNA editing in brown rot wood-decaying fungi

Abstract

Fungi that decay wood have characteristic associations with certain tree species, but the mechanistic bases for these associations are poorly understood. We studied substrate-specific gene expression and RNA editing in six species of wood-decaying fungi from the 'Antrodia clade' (Polyporales, Agaricomycetes) on three different wood substrates (pine, spruce, and aspen) in submerged cultures. We identified dozens to hundreds of substrate-biased genes (i.e., genes that are significantly upregulated in one substrate relative to the other two substrates) in each species, and these biased genes are correlated with their host ranges. Evolution of substrate-biased genes is associated with gene family expansion, gain and loss of genes, and variation in cis- and trans- regulatory elements, rather than changes in protein coding sequences. We also demonstrated widespread RNA editing events in the Antrodia clade, which differ from those observed in the Ascomycota in their distribution, substitution types, and the genomic environment. Moreover, we found that substrates could affect editing positions and frequency, including editing events occurring in mRNA transcribed from wood-decay-related genes. Finally, this work shows the extent to which gene expression and RNA editing differ among species and substrates, and provides clues into mechanisms by which wood-decaying fungi may adapt to different hosts.

Authors:
 [1];  [2];  [3];  [3];  [4]; ORCiD logo [5];  [3];  [3];  [6];  [2];  [1]
  1. Clark Univ., Worcester, MA (United States)
  2. US Dept. of Agriculture (USDA), Madison, WI (United States)
  3. Univ. of Minnesota, St. Paul, MN (United States)
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
  6. Univ. of Toronto, ON (Canada)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1619121
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 13; Journal Issue: 6; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; functional genomics; fungal ecology; molecular evolution

Citation Formats

Wu, Baojun, Gaskell, Jill, Zhang, Jiwei, Toapanta, Christina, Ahrendt, Steven, Grigoriev, Igor V., Blanchette, Robert A., Schilling, Jonathan S., Master, Emma, Cullen, Daniel, and Hibbett, David S. Evolution of substrate-specific gene expression and RNA editing in brown rot wood-decaying fungi. United States: N. p., 2019. Web. doi:10.1038/s41396-019-0359-2.
Wu, Baojun, Gaskell, Jill, Zhang, Jiwei, Toapanta, Christina, Ahrendt, Steven, Grigoriev, Igor V., Blanchette, Robert A., Schilling, Jonathan S., Master, Emma, Cullen, Daniel, & Hibbett, David S. Evolution of substrate-specific gene expression and RNA editing in brown rot wood-decaying fungi. United States. https://doi.org/10.1038/s41396-019-0359-2
Wu, Baojun, Gaskell, Jill, Zhang, Jiwei, Toapanta, Christina, Ahrendt, Steven, Grigoriev, Igor V., Blanchette, Robert A., Schilling, Jonathan S., Master, Emma, Cullen, Daniel, and Hibbett, David S. Mon . "Evolution of substrate-specific gene expression and RNA editing in brown rot wood-decaying fungi". United States. https://doi.org/10.1038/s41396-019-0359-2. https://www.osti.gov/servlets/purl/1619121.
@article{osti_1619121,
title = {Evolution of substrate-specific gene expression and RNA editing in brown rot wood-decaying fungi},
author = {Wu, Baojun and Gaskell, Jill and Zhang, Jiwei and Toapanta, Christina and Ahrendt, Steven and Grigoriev, Igor V. and Blanchette, Robert A. and Schilling, Jonathan S. and Master, Emma and Cullen, Daniel and Hibbett, David S.},
abstractNote = {Fungi that decay wood have characteristic associations with certain tree species, but the mechanistic bases for these associations are poorly understood. We studied substrate-specific gene expression and RNA editing in six species of wood-decaying fungi from the 'Antrodia clade' (Polyporales, Agaricomycetes) on three different wood substrates (pine, spruce, and aspen) in submerged cultures. We identified dozens to hundreds of substrate-biased genes (i.e., genes that are significantly upregulated in one substrate relative to the other two substrates) in each species, and these biased genes are correlated with their host ranges. Evolution of substrate-biased genes is associated with gene family expansion, gain and loss of genes, and variation in cis- and trans- regulatory elements, rather than changes in protein coding sequences. We also demonstrated widespread RNA editing events in the Antrodia clade, which differ from those observed in the Ascomycota in their distribution, substitution types, and the genomic environment. Moreover, we found that substrates could affect editing positions and frequency, including editing events occurring in mRNA transcribed from wood-decay-related genes. Finally, this work shows the extent to which gene expression and RNA editing differ among species and substrates, and provides clues into mechanisms by which wood-decaying fungi may adapt to different hosts.},
doi = {10.1038/s41396-019-0359-2},
journal = {The ISME Journal},
number = 6,
volume = 13,
place = {United States},
year = {Mon Feb 04 00:00:00 EST 2019},
month = {Mon Feb 04 00:00:00 EST 2019}
}

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