The fungal ribonuclease-like effector protein CSEP0064/BEC1054 represses plant immunity and interferes with degradation of host ribosomal RNA

PLoS Pathog. 2019 Mar 11;15(3):e1007620. doi: 10.1371/journal.ppat.1007620. eCollection 2019 Mar.

Abstract

The biotrophic fungal pathogen Blumeria graminis causes the powdery mildew disease of cereals and grasses. We present the first crystal structure of a B. graminis effector of pathogenicity (CSEP0064/BEC1054), demonstrating it has a ribonuclease (RNase)-like fold. This effector is part of a group of RNase-like proteins (termed RALPHs) which comprise the largest set of secreted effector candidates within the B. graminis genomes. Their exceptional abundance suggests they play crucial functions during pathogenesis. We show that transgenic expression of RALPH CSEP0064/BEC1054 increases susceptibility to infection in both monocotyledonous and dicotyledonous plants. CSEP0064/BEC1054 interacts in planta with the pathogenesis-related protein PR10. The effector protein associates with total RNA and weakly with DNA. Methyl jasmonate (MeJA) levels modulate susceptibility to aniline-induced host RNA fragmentation. In planta expression of CSEP0064/BEC1054 reduces the formation of this RNA fragment. We propose CSEP0064/BEC1054 is a pseudoenzyme that binds to host ribosomes, thereby inhibiting the action of plant ribosome-inactivating proteins (RIPs) that would otherwise lead to host cell death, an unviable interaction and demise of the fungus.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Ascomycota / pathogenicity*
  • Fungal Proteins / chemistry
  • Fungal Proteins / genetics
  • Fungal Proteins / metabolism*
  • Gene Expression Regulation, Fungal
  • Host-Pathogen Interactions / immunology*
  • Plant Diseases / immunology
  • Plant Diseases / microbiology
  • Plant Immunity / immunology*
  • Plants / immunology*
  • Plants / microbiology
  • Protein Conformation
  • RNA, Plant / genetics
  • RNA, Plant / metabolism*
  • RNA, Ribosomal / genetics
  • RNA, Ribosomal / metabolism*
  • Sequence Homology

Substances

  • Fungal Proteins
  • RNA, Plant
  • RNA, Ribosomal