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Mobile ARGONAUTE 1d binds 22-nt miRNAs to generate phasiRNAs important for low-temperature male fertility in rice

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Abstract

Phased small interfering RNAs (phasiRNAs) are abundantly expressed in anthers and linked to environment-related male fertility in grasses, yet how they function under different environmental conditions remains unclear. Here, we identified a rice (Oryza sativa) low temperature-induced Argonaute (AGO) protein, OsAGO1d, that is responsible for generating phasiRNAs and preserving male fertility at low temperature. Loss of OsAGO1d function causes low-temperature male sterility associated with delayed programmed cell death of tapetal cells during anther development. OsAGO1d binds miR2118 and miR2275 family members and triggers phasiRNA biogenesis; it also binds 21-nt phasiRNAs with a 5′ terminal U. In total, phasiRNAs from 972 loci are OsAGO1d-dependent. OsAGO1d protein moves from anther wall cells into meiocytes, where it loads miR2275 to produce 24-nt phasiRNAs. Together, our results show that OsAGO1d acts as a mobile signal to fine-tune phasiRNA production and this function is important for male fertility at low temperature.

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Acknowledgements

This work was supported by the National Science Foundation of China to (31788103, 32170620), the Chinese Academy of Sciences (QYZDY-SSW-SMC022, XDB27030201, XDA24010302) and the State Key Laboratory of Plant Genomics.

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Authors and Affiliations

  1. State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, 100101, China

    Fuyan Si, Haofei Luo, Chao Yang, Jie Gong, Bin Yan, Chunyan Liu, Xianwei Song & Xiaofeng Cao

  2. The Municipal Key Laboratory of the Molecular Genetics of Hybrid Wheat, Institute of Hybrid Wheat, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, China

    Jie Gong

  3. Innovative Academy of Seed Design (INASEED), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, 100101, China

    Xianwei Song

  4. College of Life Sciences, University of the Chinese Academy of Sciences, Beijing, 100039, China

    Xiaofeng Cao

  5. CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Beijing, 100101, China

    Xiaofeng Cao

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  1. Fuyan Si
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Si, F., Luo, H., Yang, C. et al. Mobile ARGONAUTE 1d binds 22-nt miRNAs to generate phasiRNAs important for low-temperature male fertility in rice. Sci. China Life Sci. 66, 197–208 (2023). https://doi.org/10.1007/s11427-022-2204-y

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