The Rheb GTPase promotes pheromone blindness via a TORC1-independent pathway in the phytopathogenic fungus Ustilago maydis

PLoS Genet. 2022 Nov 14;18(11):e1010483. doi: 10.1371/journal.pgen.1010483. eCollection 2022 Nov.

Abstract

The target of the rapamycin (TOR) signaling pathway plays a negative role in controlling virulence in phytopathogenic fungi. However, the actual targets involved in virulence are currently unknown. Using the corn smut fungus Ustilago maydis, we tried to address the effects of the ectopic activation of TOR on virulence. We obtained gain-of-function mutations in the Rheb GTPase, one of the conserved TOR kinase regulators. We have found that unscheduled activation of Rheb resulted in the alteration of the proper localization of the pheromone receptor, Pra1, and thereby pheromone insensitivity. Since pheromone signaling triggers virulence in Ustilaginales, we believe that the Rheb-induced pheromone blindness was responsible for the associated lack of virulence. Strikingly, although these effects required the concourse of the Rsp5 ubiquitin ligase and the Art3 α-arrestin, the TOR kinase was not involved. Several eukaryotic organisms have shown that Rheb transmits environmental information through TOR-dependent and -independent pathways. Therefore, our results expand the range of signaling manners at which environmental conditions could impinge on the virulence of phytopathogenic fungi.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Blindness
  • Fungal Proteins / genetics
  • Fungal Proteins / metabolism
  • Fungi / metabolism
  • Mechanistic Target of Rapamycin Complex 1 / metabolism
  • Pheromones / metabolism
  • Ras Homolog Enriched in Brain Protein / genetics
  • Ras Homolog Enriched in Brain Protein / metabolism
  • Ustilago* / genetics
  • Zea mays / metabolism

Substances

  • Pheromones
  • Ras Homolog Enriched in Brain Protein
  • Mechanistic Target of Rapamycin Complex 1
  • Fungal Proteins

Supplementary concepts

  • Ustilago maydis

Grants and funding

This work was supported by Ministerio de Ciencia e Innovación (MCIN) Grant PID2020-120242GB-I00 (MCIN/ AEI/10.13039/501100011033) to JPM. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.