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.

Guangzhou Key Laboratory of Chinese Medicine Research on Prevention and Treatment of Osteoporosis The 3rd Affiliated Hospital of Guangzhou University of Chinese Medicine No 263 Longxi Avenue Guangzhou People's Republic of China

Institute of Medical Plant Physiology and Ecology School of Pharmaceutical Sciences Guangzhou University of Chinese Medicine 510006 Guangzhou People's Republic of China

Institution of Fruit Tree Research Guangdong Academy of Agricultural Sciences; Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization Guangdong Provincial Key Laboratory of Tropical and Subtropical Fruit Tree Research 510640 Guangzhou People's Republic of China

Key Laboratory of Chinese Medicinal Resource from Lingnan Ministry of Education Guangzhou People's Republic of China

Laboratory of Hormonal Regulations in Plants Institute of Experimental Botany Czech Academy of Sciences 165 02 Prague 6 Czech Republic

School of Life Sciences Sun Yat sen University 510275 Guangzhou People's Republic of China

State Key Laboratory of Dampness Syndrome of Chinese Medicine Guangzhou University of Chinese Medicine Guangzhou People's Republic of China

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Photosystems under high light stress: throwing light on mechanism and adaptation