PMS1T, producing phased small-interfering RNAs, regulates photoperiod-sensitive male sterility in rice
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...
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Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 113; no. 52; pp. 15144 - 15149 |
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Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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United States
National Academy of Sciences
27.12.2016
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Subjects | |
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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. |
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AbstractList | 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. New discoveries have been continuously made in recent years on the roles of noncoding RNAs in regulating biological processes. Phased small-interfering RNAs (phasiRNAs) may be the newest member discovered in recent years. The photoperiod-sensitive male sterility (PSMS) rice is a very valuable germplasm that started the era of two-line hybrid rice. Here we show that phasiRNAs generated by a long-noncoding RNA PMS1T encoded by the Pms1 locus regulates PSMS in rice. This work provides a case associating the phasiRNAs with a biological trait, especially an agriculturally highly important trait, thus confirming that the phasiRNAs indeed have biological functions. 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. |
Author | Xiao, Jinghua 蔡朝霞 Mathioni, Sandra M. 张启发 李香花 王磊 徐才国 Xu, Caiguo Shen, Jianqiang Zhang, Qinghua Fan, Yourong 杨江义 杨雪菲 沈建强 Yang, Jiangyi Li, Xianghua Yang, Xuefei Meyers, Blake C. Cai, Zhaoxia Wang, Lei 於金生 肖景华 范优荣 张清华 Yu, Jinsheng Zhang, Qifa |
Author_xml | – sequence: 1 givenname: Yourong surname: Fan fullname: Fan, Yourong organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China – sequence: 2 fullname: 范优荣 organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China – sequence: 3 givenname: Jiangyi surname: Yang fullname: Yang, Jiangyi organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China – sequence: 4 fullname: 杨江义 organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China – sequence: 5 givenname: Sandra M. surname: Mathioni fullname: Mathioni, Sandra M. organization: Department of Plant and Soil Sciences, Delaware Biotechnology Institute, University of Delaware, Newark, DE 19711 – sequence: 6 givenname: Jinsheng surname: Yu fullname: Yu, Jinsheng organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China – sequence: 7 fullname: 於金生 organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China – sequence: 8 givenname: Jianqiang surname: Shen fullname: Shen, Jianqiang organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China – sequence: 9 fullname: 沈建强 organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China – sequence: 10 givenname: Xuefei surname: Yang fullname: Yang, Xuefei organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China – sequence: 11 fullname: 杨雪菲 organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China – sequence: 12 givenname: Lei surname: Wang fullname: Wang, Lei organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China – sequence: 13 fullname: 王磊 organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China – sequence: 14 givenname: Qinghua surname: Zhang fullname: Zhang, Qinghua organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China – sequence: 15 fullname: 张清华 organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China – sequence: 16 givenname: Zhaoxia surname: Cai fullname: Cai, Zhaoxia organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China – sequence: 17 fullname: 蔡朝霞 organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China – sequence: 18 givenname: Caiguo surname: Xu fullname: Xu, Caiguo organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China – sequence: 19 fullname: 徐才国 organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China – sequence: 20 givenname: Xianghua surname: Li fullname: Li, Xianghua organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China – sequence: 21 fullname: 李香花 organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China – sequence: 22 givenname: Jinghua surname: Xiao fullname: Xiao, Jinghua organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China – sequence: 23 fullname: 肖景华 organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China – sequence: 24 givenname: Blake C. surname: Meyers fullname: Meyers, Blake C. organization: Department of Plant and Soil Sciences, Delaware Biotechnology Institute, University of Delaware, Newark, DE 19711 – sequence: 25 givenname: Qifa surname: Zhang fullname: Zhang, Qifa organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China – sequence: 26 fullname: 张启发 organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27965387$$D View this record in MEDLINE/PubMed |
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Copyright | Volumes 1–89 and 106–113, copyright as a collective work only; author(s) retains copyright to individual articles Copyright National Academy of Sciences Dec 27, 2016 |
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DocumentTitleAlternate | PMS1T confers photoperiod-sensitive male sterility |
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Issue | 52 |
Keywords | long-noncoding RNA phasiRNA photoperiod-sensitive male sterility |
Language | English |
License | Freely available online through the PNAS open access option. |
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Notes | SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 14 ObjectType-Article-1 ObjectType-Feature-2 content type line 23 3Present address: School of Agriculture and Food Science, The Key Laboratory for Quality Improvement of Agricultural Products of Zhejiang Province, Zhejiang A&F University, Linan 311300, China. Contributed by Qifa Zhang, November 21, 2016 (sent for review October 5, 2016; reviewed by Gynheung An and Yaoguang Liu) Author contributions: Y.F., J. Yang, and Qifa Zhang designed research; Y.F., J. Yang, S.M.M., J. Yu, J.S., X.Y., L.W., Qinghua Zhang, and Z.C. performed research; C.X., X.L., J.X., and B.C.M. contributed new reagents/analytic tools; Y.F., J. Yang, and Qifa Zhang analyzed data; and Y.F., J. Yang, and Qifa Zhang wrote the paper. Reviewers: G.A., Kyung Hee University; and Y.L., South China Agricultural University. 1Present address: College of Life Science and Technology, Guangxi University, Nanning 530004, China. 2Present address: Donald Danforth Plant Science Center, St. Louis, MO 63132. |
ORCID | 0000-0003-3436-6097 |
OpenAccessLink | https://www.pnas.org/content/pnas/113/52/15144.full.pdf |
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PublicationDate | 2016-12-27 |
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Snippet | 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.... New discoveries have been continuously made in recent years on the roles of noncoding RNAs in regulating biological processes. Phased small-interfering RNAs... |
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StartPage | 15144 |
SubjectTerms | Biological Sciences Fertility Male sterility Plant breeding Polymorphism Ribonucleic acid Rice RNA |
Title | PMS1T, producing phased small-interfering RNAs, regulates photoperiod-sensitive male sterility in rice |
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