Arginine methylation is required for remodelling pre-mRNA splicing and induction of autophagy in rice blast fungus

New Phytol. 2020 Jan;225(1):413-429. doi: 10.1111/nph.16156. Epub 2019 Sep 30.

Abstract

Protein arginine methyltransferases (PRMTs) regulate many physiological processes, including autophagy. However, the direct roles of the various PRMTs during autophagosome formation remain unclear. Here, we characterised the function of MoHMT1 in the rice blast fungus, Magnaporthe oryzae. Knockout of MoHMT1 results in inhibited growth and a decreased ability to cause disease lesions on rice seedlings. MoHMT1 catalyses the di-methylation of arginine 247, 251, 261 and 271 residues of MoSNP1, a U1 small nuclear ribonucleoprotein (snRNP) component, likely in a manner dependent on direct interaction. RNA-seq analysis revealed that alternative splicing of pre-mRNAs of 558 genes, including the autophagy-related (ATG) gene MoATG4, was altered in MoHMT1 deletion mutants, compared with wild-type strains under normal growth conditions. During light exposure or nitrogen starvation, MoHMT1 localises to autophagosomes and MoHMT1 mutants display defects in autophagy induction. Under nitrogen starvation, six additional MoATG genes were identified with retained introns in their mRNA transcripts, corresponding with a significant reduction in transcripts of intron-spliced isoforms in the MoHMT1 mutant strain. Our study shows that arginine methylation plays an essential role in accurate pre-mRNA splicing necessary for a range of developmental processes, including autophagosome formation.

Keywords: Magnaporthe oryzae; MoSNP1; autophagy; pathogenicity; pre-mRNA splicing; protein arginine methyltransferase (PRMT).

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Arginine / metabolism*
  • Autophagosomes / metabolism
  • Autophagosomes / ultrastructure
  • Autophagy / genetics*
  • Fungal Proteins / chemistry
  • Fungal Proteins / metabolism
  • Gene Deletion
  • Genome, Fungal
  • Hyphae / growth & development
  • Magnaporthe / cytology*
  • Magnaporthe / genetics*
  • Magnaporthe / pathogenicity
  • Methylation
  • Oryza / microbiology*
  • Plant Diseases / genetics
  • Plant Diseases / microbiology*
  • Protein Binding
  • RNA Precursors / genetics*
  • RNA Splicing / genetics*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Spliceosomes / metabolism
  • Spores, Fungal / growth & development

Substances

  • Fungal Proteins
  • RNA Precursors
  • RNA, Messenger
  • Arginine

Associated data

  • GENBANK/MGG_03982
  • GENBANK/MGG_04584
  • GENBANK/MGG_17318
  • GENBANK/MGG_09290
  • GENBANK/MGG_03894
  • GENBANK/MGG_15607
  • GENBANK/GSE129291