The novel roles of RNA m6A modification in regulating the development, infection, and oxidative DNA damage repair of Phytophthora sojae

N6-methyladenosine (m6A), a vital post-transcriptional regulator, is among the most prevalent RNA modifications in eukaryotes. Nevertheless, the biological functions of m6A in oomycetes remain poorly understood. Here, we showed that the PsMTA1 and PsMTA2 genes are orthologs of human METTL4, while the PsMET16 gene is an ortholog of human METTL16. These genes are implicated in m6A modification and play a critical role in the production of sporangia and oospores, the release of zoospores, and the virulence of Phytophthora sojae. In P. sojae, m6A modifications are predominantly enriched in the coding sequence and the 3' untranslated region. Notably, the PsMTA1 knockout mutant exhibited reduced virulence, attributed to impaired tolerance to host defense-generated ROS stress. Mechanistically, PsMTA1-mediated m6A modification positively regulates the mRNA lifespan of DNA damage response (DDR) genes in reaction to plant ROS stress during infection. Consequently, the mRNA abundance of the DDR gene PsRCC1 was reduced in the single m6A site mutant ΔRCC1/RCC1A2961C, resulting in compromised DNA damage repair and reduced ROS adaptation-associated virulence in P. sojae. Overall, these results indicate that m6A-mediated RNA metabolism is associated with the development and pathogenicity of P. sojae, underscoring the roles of epigenetic markers in the adaptive flexibility of Phytophthora during infection.

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Publication Details

Journal
PLoS Pathogens
Published
2024-09-23
DOI
https://doi.org/10.1371/journal.ppat.1012553
Citations
9
Primary Topic
RNA modifications and cancer
Type
article
Field-Weighted Citation Impact
2.10

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article

The novel roles of RNA m6A modification in regulating the development, infection, and oxidative DNA damage repair of Phytophthora sojae

Tongshan Cui, Fan Zhang, Zhiwen Wang, Shanshan Chen et al.
9 citations
PLoS Pathogens
RNA modifications and cancer
2.10
article

The novel roles of RNA m6A modification in regulating the development, infection, and oxidative DNA damage repair of Phytophthora sojae

Tongshan Cui, Fan Zhang, Zhiwen Wang, Shanshan Chen, Can Zhang, Borui Zhang, Xili Liu
article en
9 citations

Abstract

N6-methyladenosine (m6A), a vital post-transcriptional regulator, is among the most prevalent RNA modifications in eukaryotes. Nevertheless, the biological functions of m6A in oomycetes remain poorly understood. Here, we showed that the PsMTA1 and PsMTA2 genes are orthologs of human METTL4, while the PsMET16 gene is an ortholog of human METTL16. These genes are implicated in m6A modification and play a critical role in the production of sporangia and oospores, the release of zoospores, and the virulence of Phytophthora sojae. In P. sojae, m6A modifications are predominantly enriched in the coding sequence and the 3' untranslated region. Notably, the PsMTA1 knockout mutant exhibited reduced virulence, attributed to impaired tolerance to host defense-generated ROS stress. Mechanistically, PsMTA1-mediated m6A modification positively regulates the mRNA lifespan of DNA damage response (DDR) genes in reaction to plant ROS stress during infection. Consequently, the mRNA abundance of the DDR gene PsRCC1 was reduced in the single m6A site mutant ΔRCC1/RCC1A2961C, resulting in compromised DNA damage repair and reduced ROS adaptation-associated virulence in P. sojae. Overall, these results indicate that m6A-mediated RNA metabolism is associated with the development and pathogenicity of P. sojae, underscoring the roles of epigenetic markers in the adaptive flexibility of Phytophthora during infection.

PLoS PathogensVol. 20(9)
China Agricultural University (CN), Northwest A&F University (CN)
Purdue University, Oregon State University, National Natural Science Foundation of China, National Key Research and Development Program of China
Openalex Percentile: Top 12%
RNA modifications and cancer
2.10
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