PMS1T, Producing Phased Small-interfering RNAs, Regulates Photoperiod-sensitive Male Sterility in Rice

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2016 Dec 15

PMID 27965387

Citations 123

Authors

Yourong Fan

Jiangyi Yang

Sandra M Mathioni

Jinsheng Yu

Jianqiang Shen

Xuefei Yang

Lei Wang

Qinghua Zhang

Zhaoxia Cai

Caiguo Xu

Xianghua Li

Jinghua Xiao

Blake C Meyers

Qifa Zhang

Affiliations

Soon will be listed here.

Abstract

Phased small-interfering RNAs (phasiRNAs) are a special class of small RNAs, which are generated in 21- or 24-nt intervals from transcripts of precursor RNAs. Although phasiRNAs have been found in a range of organisms, their biological functions in plants have yet to be uncovered. Here we show that phasiRNAs generated by the photopheriod-sensetive genic male sterility 1 (Pms1) locus were associated with photoperiod-sensitive male sterility (PSMS) in rice, a germplasm that started the two-line hybrid rice breeding. The Pms1 locus encodes a long-noncoding RNA PMS1T that was preferentially expressed in young panicles. PMS1T was targeted by miR2118 to produce 21-nt phasiRNAs that preferentially accumulated in the PSMS line under long-day conditions. A single nucleotide polymorphism in PMS1T nearby the miR2118 recognition site was critical for fertility change, likely leading to differential accumulation of the phasiRNAs. This result suggested possible roles of phasiRNAs in reproductive development of rice, demonstrating the potential importance of this RNA class as regulators in biological processes.

Citing Articles

Advances in plant male sterility for hybrid seed production: an overview of conditional nuclear male sterile lines and biotechnology-based male sterile systems.

Vasupalli N, Mogilicherla K, Shaik V, Rao K, Bhat S, Lin X Front Plant Sci. 2025; 16:1540693.

PMID: 39974728 PMC: 11835859. DOI: 10.3389/fpls.2025.1540693.

Transcriptome and WGCNA reveals the potential genetic basis of photoperiod-sensitive male sterility in soybean.

Yang Y, He S, Xu L, Wang M, Chen S, Bai Z BMC Genomics. 2025; 26(1):131.

PMID: 39934659 PMC: 11816801. DOI: 10.1186/s12864-025-11314-5.

Targeted mutation of / combined with the RUBY reporter enables an efficient two-line system for hybrid seed production in .

Shen X, Dong Q, Zhao X, Hu L, Bala S, Deng S Hortic Res. 2025; 12(1):uhae270.

PMID: 39897731 PMC: 11783330. DOI: 10.1093/hr/uhae270.

Epigenetics in the modern era of crop improvements.

Xue Y, Cao X, Chen X, Deng X, Deng X, Ding Y Sci China Life Sci. 2025; .

PMID: 39808224 DOI: 10.1007/s11427-024-2784-3.

Genetic and molecular mechanisms underlying the male sterility in rice.

Sohail A, Lu C, Xu P J Appl Genet. 2024; .

PMID: 39627604 DOI: 10.1007/s13353-024-00923-7.

References

Yuan B, Shen X, Li X, Xu C, Wang S . Mitogen-activated protein kinase OsMPK6 negatively regulates rice disease resistance to bacterial pathogens. Planta. 2007; 226(4):953-60. DOI: 10.1007/s00425-007-0541-z. View

Nonomura K, Morohoshi A, Nakano M, Eiguchi M, Miyao A, Hirochika H . A germ cell specific gene of the ARGONAUTE family is essential for the progression of premeiotic mitosis and meiosis during sporogenesis in rice. Plant Cell. 2007; 19(8):2583-94. PMC: 2002623. DOI: 10.1105/tpc.107.053199. View

Song X, Wang D, Ma L, Chen Z, Li P, Cui X . Rice RNA-dependent RNA polymerase 6 acts in small RNA biogenesis and spikelet development. Plant J. 2012; 71(3):378-89. DOI: 10.1111/j.1365-313X.2012.05001.x. View

Li J, Reichel M, Millar A . Determinants beyond both complementarity and cleavage govern microR159 efficacy in Arabidopsis. PLoS Genet. 2014; 10(3):e1004232. PMC: 3953016. DOI: 10.1371/journal.pgen.1004232. View

Zhang Q, Shen B, Dai X, Mei M, Saghai Maroof M, Li Z . Using bulked extremes and recessive class to map genes for photoperiod-sensitive genic male sterility in rice. Proc Natl Acad Sci U S A. 1994; 91(18):8675-9. PMC: 44669. DOI: 10.1073/pnas.91.18.8675. View

Mei M, Chen L, Zhang Z, Li Z, Xu C, Zhang Q . pms3 is the locus causing the original photoperiod-sensitive male sterility mutation of 'Nongken 58S'. Sci China C Life Sci. 2010; 42(3):316-22. DOI: 10.1007/BF03183609. View

Llave C, Xie Z, Kasschau K, Carrington J . Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science. 2002; 297(5589):2053-6. DOI: 10.1126/science.1076311. View

Chen H, Chen L, Patel K, Li Y, Baulcombe D, Wu S . 22-Nucleotide RNAs trigger secondary siRNA biogenesis in plants. Proc Natl Acad Sci U S A. 2010; 107(34):15269-74. PMC: 2930544. DOI: 10.1073/pnas.1001738107. View

Han B, Wang W, Li C, Weng Z, Zamore P . Noncoding RNA. piRNA-guided transposon cleavage initiates Zucchini-dependent, phased piRNA production. Science. 2015; 348(6236):817-21. PMC: 4545291. DOI: 10.1126/science.aaa1264. View

10.

Zhai J, Jeong D, De Paoli E, Park S, Rosen B, Li Y . MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev. 2011; 25(23):2540-53. PMC: 3243063. DOI: 10.1101/gad.177527.111. View

11.

Zhou H, Liu Q, Li J, Jiang D, Zhou L, Wu P . Photoperiod- and thermo-sensitive genic male sterility in rice are caused by a point mutation in a novel noncoding RNA that produces a small RNA. Cell Res. 2012; 22(4):649-60. PMC: 3317565. DOI: 10.1038/cr.2012.28. View

12.

Mohn F, Handler D, Brennecke J . Noncoding RNA. piRNA-guided slicing specifies transcripts for Zucchini-dependent, phased piRNA biogenesis. Science. 2015; 348(6236):812-817. PMC: 4988486. DOI: 10.1126/science.aaa1039. View

13.

Ding J, Lu Q, Ouyang Y, Mao H, Zhang P, Yao J . A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. Proc Natl Acad Sci U S A. 2012; 109(7):2654-9. PMC: 3289353. DOI: 10.1073/pnas.1121374109. View

14.

Johnson C, Kasprzewska A, Tennessen K, Fernandes J, Nan G, Walbot V . Clusters and superclusters of phased small RNAs in the developing inflorescence of rice. Genome Res. 2009; 19(8):1429-40. PMC: 2720183. DOI: 10.1101/gr.089854.108. View

15.

Zhou Y, Cai H, Xiao J, Li X, Zhang Q, Lian X . Over-expression of aspartate aminotransferase genes in rice resulted in altered nitrogen metabolism and increased amino acid content in seeds. Theor Appl Genet. 2009; 118(7):1381-90. DOI: 10.1007/s00122-009-0988-3. View

16.

Song X, Li P, Zhai J, Zhou M, Ma L, Liu B . Roles of DCL4 and DCL3b in rice phased small RNA biogenesis. Plant J. 2011; 69(3):462-74. DOI: 10.1111/j.1365-313X.2011.04805.x. View

17.

Kelley D, Rinn J . Transposable elements reveal a stem cell-specific class of long noncoding RNAs. Genome Biol. 2012; 13(11):R107. PMC: 3580499. DOI: 10.1186/gb-2012-13-11-r107. View

18.

Chen A, Yu K, Fan L, Li J, Yang C, Huang A . Germline genetic variants disturbing the Let-7/LIN28 double-negative feedback loop alter breast cancer susceptibility. PLoS Genet. 2011; 7(9):e1002259. PMC: 3164678. DOI: 10.1371/journal.pgen.1002259. View

19.

Mishra P, Humeniuk R, Mishra P, Longo-Sorbello G, Banerjee D, Bertino J . A miR-24 microRNA binding-site polymorphism in dihydrofolate reductase gene leads to methotrexate resistance. Proc Natl Acad Sci U S A. 2007; 104(33):13513-8. PMC: 1948927. DOI: 10.1073/pnas.0706217104. View

20.

Liu N, Shan Y, Wang F, Xu C, Peng K, Li X . Identification of an 85-kb DNA fragment containing pms1, a locus for photoperiod-sensitive genic male sterility in rice. Mol Genet Genomics. 2001; 266(2):271-5. DOI: 10.1007/s004380100553. View