Alternative splicing diversifies the transcriptome and proteome of the rice blast fungus during host infection

RNA Biol. 2022;19(1):373-385. doi: 10.1080/15476286.2022.2043040. Epub 2021 Dec 31.

Abstract

Alternative splicing (AS) contributes to diversifying and regulating cellular responses to environmental conditions and developmental cues by differentially producing multiple mRNA and protein isoforms from a single gene. Previous studies on AS in pathogenic fungi focused on profiling AS isoforms under a limited number of conditions. We analysed AS profiles in the rice blast fungus Magnaporthe oryzae, a global threat to rice production, using high-quality transcriptome data representing its vegetative growth (mycelia) and multiple host infection stages. We identified 4,270 AS isoforms derived from 2,413 genes, including 499 genes presumably regulated by infection-specific AS. AS appears to increase during infection, with 32.7% of the AS isoforms being produced during infection but absent in mycelia. Analysis of the isoforms observed at each infection stage showed that 636 AS isoforms were more abundant than corresponding annotated mRNAs, especially after initial hyphal penetration into host cell. Many such dominant isoforms were predicted to encode regulatory proteins such as transcription factors and phospho-transferases. We also identified the genes encoding distinct proteins via AS and confirmed the translation of some isoforms via a proteomic analysis, suggesting potential AS-mediated neo-functionalization of some genes during infection. Comprehensive profiling of the pattern of genome-wide AS during multiple stages of rice-M. oryzae interaction established a foundational resource that will help investigate the role and regulation of AS during rice infection.

Keywords: Alternative splicing; functional diversification; magnaporthe oryzae; pathogenicity; proteome; rice; transcriptome.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Alternative Splicing
  • Ascomycota
  • Fungal Proteins / genetics
  • Fungal Proteins / metabolism
  • Magnaporthe* / genetics
  • Magnaporthe* / metabolism
  • Oryza* / genetics
  • Oryza* / metabolism
  • Plant Diseases / genetics
  • Plant Diseases / microbiology
  • Proteome / genetics
  • Proteomics
  • Transcriptome

Substances

  • Fungal Proteins
  • Proteome

Supplementary concepts

  • Pyricularia oryzae

Grants and funding

This work was supported by grants from the National Research Foundation of Korea [NRF-2020R1A2B5B03096402, NRF-2015M3A9B8028679, and NRF-2018R1A5A1023599] and the Korea Institute of Planning and Evaluation for Technology in Food, Agriculture and Forestry through Agricultural Microbiome Program [918017-04-1-CG000]. The USDA National Institute of Food & Agriculture and Federal Appropriations [National Institute of Food and Agriculture Project PEN04655] and the Brian Pool program of the National Research Foundation of Korea [NRF-2019H1D3A2A01054562] supported S.Ka.