Rice apoplastic CBM1-interacting protein counters blast pathogen invasion by binding conserved carbohydrate binding module 1 motif of fungal proteins

PLoS Pathog. 2022 Sep 29;18(9):e1010792. doi: 10.1371/journal.ppat.1010792. eCollection 2022 Sep.

Abstract

When infecting plants, fungal pathogens secrete cell wall-degrading enzymes (CWDEs) that break down cellulose and hemicellulose, the primary components of plant cell walls. Some fungal CWDEs contain a unique domain, named the carbohydrate binding module (CBM), that facilitates their access to polysaccharides. However, little is known about how plants counteract pathogen degradation of their cell walls. Here, we show that the rice cysteine-rich repeat secretion protein OsRMC binds to and inhibits xylanase MoCel10A of the blast fungus pathogen Magnaporthe oryzae, interfering with its access to the rice cell wall and degradation of rice xylan. We found binding of OsRMC to various CBM1-containing enzymes, suggesting that it has a general role in inhibiting the action of CBM1. OsRMC is localized to the apoplast, and its expression is strongly induced in leaves infected with M. oryzae. Remarkably, knockdown and overexpression of OsRMC reduced and enhanced rice defense against M. oryzae, respectively, demonstrating that inhibition of CBM1-containing fungal enzymes by OsRMC is crucial for rice defense. We also identified additional CBM-interacting proteins (CBMIPs) from Arabidopsis thaliana and Setaria italica, indicating that a wide range of plants counteract pathogens through this mechanism.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis*
  • Cellulose
  • Cysteine
  • Fungal Proteins / genetics
  • Oryza* / genetics
  • Xylans

Substances

  • Fungal Proteins
  • Xylans
  • Cellulose
  • Cysteine

Grants and funding

TT was supported by Japan Society for the Promotion of Science, KAKENHI 18K06121. RT was supported by Japan Society for the Promotion of Science, KAKENHI 15H05779 and 20H05681. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.