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N⁶-methyladenosine RNA modification regulates photosynthesis during photodamage in plants.

ABSTRACT: N⁶-methyladenosine (m⁶A) modification of mRNAs affects many biological processes. However, the function of m⁶A in plant photosynthesis remains unknown. Here, we demonstrate that m⁶A modification is crucial for photosynthesis during photodamage caused by high light stress in plants. The m⁶A modification levels of numerous photosynthesis-related transcripts are changed after high light stress. We determine that the Arabidopsis m⁶A writer VIRILIZER (VIR) positively regulates photosynthesis, as its genetic inactivation drastically lowers photosynthetic activity and photosystem protein abundance under high light conditions. The m⁶A levels of numerous photosynthesis-related transcripts decrease in vir mutants, extensively reducing their transcript and translation levels, as revealed by multi-omics analyses. We demonstrate that VIR associates with the transcripts of genes encoding proteins with functions related to photoprotection (such as HHL1, MPH1, and STN8) and their regulatory proteins (such as regulators of transcript stability and translation), promoting their m⁶A modification and maintaining their stability and translation efficiency. This study thus reveals an important mechanism for m⁶A-dependent maintenance of photosynthetic efficiency in plants under high light stress conditions.

SUBMITTER: Zhang M

PROVIDER: S-EPMC9718803 | biostudies-literature | 2022 Dec

REPOSITORIES: biostudies-literature

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N6-methyladenosine RNA modification regulates photosynthesis during photodamage in plants.

Zhang Man M Zeng Yunping Y Peng Rong R Dong Jie J Lan Yelin Y Duan Sujuan S Chang Zhenyi Z Ren Jian J Luo Guanzheng G Liu Bing B Růžička Kamil K Zhao Kewei K Wang Hong-Bin HB Jin Hong-Lei HL

Nature communications 20221202 1

N6-methyladenosine (m6A) modification of mRNAs affects many biological processes. However, the function of m6A in plant photosynthesis remains unknown. Here, we demonstrate that m6A modification is crucial for photosynthesis during photodamage caused by high light stress in plants. The m6A modification levels of numerous photosynthesis-related transcripts are changed after high light stress. We determine that the Arabidopsis m6A w ...[more]

PMID: 36460653

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Project description:N6-methyladenosine (m6A) modification is a major RNA epigenetic regulatory mechanism. The dynamics of m6A levels in viral genomic RNA and their mRNAs have been shown to have either pro- or antiviral functions, and therefore, m6A modifications influence virus-host interactions. Currently, no reports are available on the effect of m6A modifications in the genome of Peste des petits ruminants virus (PPRV). In the present study, we took PPRV as a model for nonsegmented negative-sense single-stranded RNA viruses and elucidate the role of m6A modification on viral replication. We detected m6A-modified sites in the mRNA of the virus and host cells, as well as the PPRV RNA genome. Further, it was found that the level of m6A modification in host cells alters the viral gene expression. Knockdown of the METTL3 and FTO genes (encoding the m6A RNA modification writer and eraser proteins, respectively) results in alterations of the levels of m6A RNA modifications in the host cells. Experiments using these genetically modified clones of host cells infected with PPRV revealed that both higher and lower m6A RNA modification in the host cells negatively affect PPRV replication. We found that m6A-modified viral transcripts had better stability and translation efficiency compared to the unmodified mRNA. Altogether, from these data, we conclude that the m6A modification of RNA regulates PPRV replication. These findings contribute toward a way forward for developing novel antiviral strategies against PPRV by modulating the dynamics of host m6A RNA modification. IMPORTANCE Peste des petits ruminants virus (PPRV) causes a severe disease in sheep and goats. PPRV infection is a major problem, causing significant economic losses to small ruminant farmers in regions of endemicity. N6-methyladenosine (m6A) is an important RNA modification involved in various functions, including virus-host interactions. In the present study, we used stable clones of Vero cells, having knocked down the genes encoding proteins involved in dynamic changes of the levels of m6A modification. We also used small-molecule compounds that interfere with m6A methylation. This resulted in a platform of host cells with various degrees of m6A RNA modification. The host cells with these different microenvironments were useful for studying the effect of m6A RNA modification on the expression of viral genes and viral replication. The results pinpoint the level of m6A modifications that facilitate the maximum replication of PPRV. These findings will be useful in increasing the virus titers in cultured cells needed for the economical development of the vaccine. Furthermore, the findings have guiding significance for the development of novel antiviral strategies for limiting PPRV replication in infected animals.

Dataset Information

N⁶-methyladenosine RNA modification regulates photosynthesis during photodamage in plants.

Publications

N<sup>6</sup>-methyladenosine RNA modification regulates photosynthesis during photodamage in plants.

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