Two closely related Rho GTPases, Cdc42 and RacA, of the en-dophytic fungus Epichloë festucae have contrasting roles for ROS production and symbiotic infection synchronized with the host plant

PLoS Pathog. 2018 Jan 25;14(1):e1006840. doi: 10.1371/journal.ppat.1006840. eCollection 2018 Jan.

Abstract

Epichloë festucae is an endophytic fungus which systemically colonizes temperate grasses to establish symbiotic associations. Maintaining symptomless infection is a key requirement for endophytes, a feature that distinguishes them from pathogenic fungi. While pathogenic fungi extend their hyphae by tip growth, hyphae of E. festucae systemically colonize the intercellular space of expanding host leaves via a unique mechanism of hyphal intercalary growth. This study reports that two homologous Rho GTPases, Cdc42 and RacA, have distinctive roles in the regulation of E. festucae growth in planta. Here we highlight the vital role of Cdc42 for intercalary hyphal growth, as well as involvement of RacA in regulation of hyphal network formation, and demonstrate the consequences of mutations in these genes on plant tissue infection. Functions of Cdc42 and RacA are mediated via interactions with BemA and NoxR respectively, which are expected components of the ROS producing NOX complex. Symbiotic defects found in the racA mutant were rescued by introduction of a Cdc42 with key amino acids substitutions crucial for RacA function, highlighting the significance of the specific interactions of these GTPases with BemA and NoxR for their functional differentiation in symbiotic infection.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Endophytes / metabolism
  • Endophytes / physiology
  • Epichloe / metabolism
  • Epichloe / physiology*
  • Fungal Proteins / physiology
  • Host-Pathogen Interactions / genetics
  • Lolium / microbiology
  • Organisms, Genetically Modified
  • Plants / microbiology*
  • Reactive Oxygen Species / metabolism*
  • Symbiosis* / genetics
  • Symbiosis* / physiology
  • cdc42 GTP-Binding Protein / genetics
  • cdc42 GTP-Binding Protein / physiology*
  • rac1 GTP-Binding Protein / genetics
  • rac1 GTP-Binding Protein / physiology*
  • rho GTP-Binding Proteins / physiology

Substances

  • Fungal Proteins
  • Reactive Oxygen Species
  • cdc42 GTP-Binding Protein
  • rac1 GTP-Binding Protein
  • rho GTP-Binding Proteins

Grants and funding

This work was supported in part by the Novartis Foundation Japan for the Promotion of Science (to DT), Toyoaki scholarship foundation (to DT), a Grants-in-Aid for Scientific Research on Innovative Areas “Signaling functions of reactive oxygen species” (No. 23117719) from MEXT, Japan (to DT), a Grant-in-Aid for Scientific Research (C) Generative Research Fields (No. 16KT0145) (to DT), and Grant-in-Aid for JSPS Fellows (No. 13J03668) from the Japan Society for the Promotion of Science (to YK). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.