OsALKBH9-mediated m6A demethylation regulates tapetal PCD and pollen exine accumulation in rice

Jun Tang; Dekun Lei; Junbo Yang; Shuyan Chen; Xueping Wang; Xiaoxin Huang; Shasha Zhang; Zhihe Cai; Shanshan Zhu; Jianmin Wan; Guifang Jia

doi:10.1111/pbi.14354

OsALKBH9-mediated m⁶A demethylation regulates tapetal PCD and pollen exine accumulation in rice

Plant Biotechnol J. 2024 Apr 17. doi: 10.1111/pbi.14354. Online ahead of print.

Authors

Jun Tang^#^{1

2}, Dekun Lei^#³, Junbo Yang^#^{1

4}, Shuyan Chen¹, Xueping Wang¹, Xiaoxin Huang¹, Shasha Zhang¹, Zhihe Cai¹, Shanshan Zhu², Jianmin Wan³, Guifang Jia^{1

5

6}

Affiliations

¹ Synthetic and Functional Biomolecules Center, Beijing National Laboratory for Molecular Sciences, Key Laboratory of Bioorganic Chemistry and Molecular Engineering of Ministry of Education, College of Chemistry and Molecular Engineering, Peking University, Beijing, China.
² Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, China.
³ National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, China.
⁴ Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, Guangdong, China.
⁵ Peking-Tsinghua Center for Life Sciences, Peking University, Beijing, China.
⁶ Beijing Advanced Center of RNA Biology, Peking University, Beijing, China.

^# Contributed equally.

PMID: 38634166
DOI: 10.1111/pbi.14354

Abstract

The N⁶-methyladenosine (m⁶A) mRNA modification is crucial for plant development and stress responses. In rice, the male sterility resulting from the deficiency of OsFIP37, a core component of m⁶A methyltransferase complex, emphasizes the significant role of m⁶A in male fertility. m⁶A is reversible and can be removed by m⁶A demethylases. However, whether mRNA m⁶A demethylase regulates male fertility in rice has remained unknown. Here, we identify the mRNA m⁶A demethylase OsALKBH9 and demonstrate its involvement in male fertility regulation. Knockout of OsALKBH9 causes male sterility, dependent on its m⁶A demethylation activity. Cytological analysis reveals defective tapetal programmed cell death (PCD) and excessive accumulation of microspores exine in Osalkbh9-1. Transcriptome analysis of anthers shows up-regulation of genes involved in tapetum development, sporopollenin synthesis, and transport pathways in Osalkbh9-1. Additionally, we demonstrate that OsALKBH9 demethylates the m⁶A modification in TDR and GAMYB transcripts, which affects the stability of these mRNAs and ultimately leads to excessive accumulation of pollen exine. Our findings highlight the precise control of mRNA m⁶A modification and reveal the pivotal roles played by OsALKBH9-mediated m⁶A demethylation in tapetal PCD and pollen exine accumulation in rice.

Keywords: OsALKBH9; demethylase; exine; m6A; rice; tapetal PCD.

Abstract

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