Capturing an Early Gene Induction Event during Wood Decay by the Brown Rot Fungus Rhodonia placenta

Claire E. Anderson, Jiwei Zhang, Lye Meng Markillie, Hugh D. Mitchell, William B. Chrisler, Matthew J. Gaffrey, Galya Orr, Jonathan S. Schilling

Research output: Contribution to journalArticlepeer-review

3 Scopus citations


Brown rot fungi dominate wood decomposition in coniferous forests, and their carbohydrate-selective mechanisms are of commercial interest. Brown rot was recently described as a two-step, sequential mechanism orchestrated by fungi using differentially expressed genes (DEGs) and consisting of oxidation via reactive oxygen species (ROS) followed by enzymatic saccharification. There have been indications, however, that the initial oxidation step itself might require induction. To capture this early gene regulation event, here, we integrated fine-scale cryosectioning with whole-transcriptome sequencing to dissect gene expression at the single-hyphal-cell scale (tens of micrometers). This improved the spatial resolution 50-fold, relative to previous work, and we were able to capture the activity of the first 100 μm of hyphal front growth by Rhodonia placenta in aspen wood. This early decay period was dominated by delayed gene expression patterns as the fungus ramped up its mechanism. These delayed DEGs included many genes implicated in ROS pathways (lignocellulose oxidation [LOX]) that were previously and incorrectly assumed to be constitutively expressed. These delayed DEGs, which include those with and without predicted functions, also create a focused subset of target genes for functional genomics. However, this delayed pattern was not universal, with a few genes being upregulated immediately at the hyphal front. Most notably, this included a gene commonly implicated in hydroquinone and iron redox cycling: benzoquinone reductase. IMPORTANCE Earth's aboveground terrestrial biomass is primarily wood, and fungi dominate wood decomposition. Here, we studied these fungal pathways in a common "brown rot"-type fungus, Rhodonia placenta, that selectively extracts sugars from carbohydrates embedded within wood lignin. Using a space-for-time design to map fungal gene expression at the extreme hyphal front in wood, we made two discoveries. First, we found that many genes long assumed to be "on" (constitutively expressed) from the very beginning of decay were instead "off" before being upregulated, when mapped (via transcriptome sequencing [RNA-seq]) at a high resolution. Second, we found that the gene encoding benzoquinone reductase was "on" in incipient decay and quickly downregulated, implying a key role in "kick-starting" brown rot.

Original languageEnglish (US)
JournalApplied and environmental microbiology
Issue number8
StatePublished - Apr 2022

Bibliographical note

Funding Information:
This material is based on work supported by Department of Energy (DOE) Environmental Molecular Science Laboratory (EMSL) User Facility award EUP 50799 to J.S.S. and J.Z. and DOE Biological and Environmental Research award DE-SC0019427 to J.S.S. and J.Z. A portion of the research was performed using EMSL (grid.436923.9), a DOE Office of Science User Facility sponsored by the Biological and Environmental Research program. This material is based upon work supported by the National Science Foundation Graduate Research Fellowship Program under grant number CON-75851, project 00074041, to C.E.A. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the National Science Foundation. We give additional thanks to the Bioproducts and Biosystem Engineering department at the University of Minnesota for its support of C.E.A. through Pawek and Forest Worker fellowships.

Publisher Copyright:
© 2022 American Society for Microbiology. All rights reserved.


  • RNA
  • biodegradation
  • decomposition
  • lignocellulose
  • transcriptomics
  • Reactive Oxygen Species/metabolism
  • Gene Expression
  • Polyporales
  • Wood/microbiology
  • Benzoquinones/metabolism
  • Oxidoreductases/metabolism

PubMed: MeSH publication types

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


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