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

Abstract

Summary 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.

Arginine Methyltransferase PeRmtC Regulates Development and Pathogenicity of Penicillium expansum via Mediating Key Genes in Conidiation and Secondary Metabolism

“…Arginine methylation has been shown to be involved in various biological processes in fungi [ 15 , 18 ]. However, the roles of PRMTs in post-harvest fungal pathogens had not been previously characterized.…”

“…Nevertheless, the roles of PRMT5 homologs in other filamentous fungi are quite different except for A. nidulans RmtC, which can also affect conidiation and radial growth [ 16 ]. For instance, M. oryzae HSL7 and F. graminearum ATM4 had no obvious effect on vegetative growth or conidiation [ 18 , 22 ]. Deletion of N. crassa skb−1 almost doubled the production of macro-conidia [ 21 ].…”

“…Up to now, studies on the regulation of fungal SM biosynthesis by PRMT5 homologs are limited. Interestingly, we found that PeRmtC could affect pigment biosynthesis in P. expansum , whereas MoHSL7 had no effect on the colony color of M. oryzae [ 18 ]. Given that pigments are known to protect microorganisms against environmental stress and often have antimicrobial activity [ 39 , 40 ], the pigments and their roles in the growth and development P. expansum are worthy of identification.…”

“…As reported, filamentous fungi harbor four PRMTs, which are homologous to mammalian PRMT1 (type I), PRMT3 (type I), PRMT5 (type II), and yeast RMT2 (type IV), respectively [ 15 ]. Homologs of PRMT1, PRMT3, and PRMT5 were found to affect the growth, development, secondary metabolism, and stress response of fungi to different extents, and PRMT1 homologs were involved in the virulence of a few important plant fungal pathogens, including Aspergillus flavus , Fusarium graminearum , and Magnaporthe oryzae [ 16 , 17 , 18 , 19 , 20 ]. In addition, there may be reciprocal regulation among homologs of PRMT1, PRMT3, and PRMT5 that affects transcriptional levels of PRMTs in F. graminearum , the arginine methylation profiles in Neurospora crassa , and the protein secretion, secondary metabolism, and detoxification in A. nidulans [ 15 , 21 , 22 ], whereas, the biological function of RMT2 homologs in fungal pathogens is not yet clear.…”

Evidence of a New MoYpd1p Phosphotransferase Isoform in the Multistep Phosphorelay System of Magnaporthe oryzae

“…The broad spectrum of spliced mRNA and, consequently, the vast diversity of corresponding proteins illustrates the strong impact of AS on basic regulatory processes and signaling mechanisms within eukaryotic organisms. Whereas almost 95% of human multi-exon genes are alternatively spliced [ 16 , 17 ], the genomes of fungal species have remarkably fewer introns and fewer AS events, but this in no way reduces its importance [ 13 ]. However, the biological impact of AS on the molecular mechanisms of cellular signaling in fungi remains mostly unexplored.…”