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 inProceedings of the National Academy of Sciences - PNAS Vol. 113; no. 52; pp. 15144 - 15149
Main Authors Fan, Yourong, 范优荣, Yang, Jiangyi, 杨江义, Mathioni, Sandra M., Yu, Jinsheng, 於金生, Shen, Jianqiang, 沈建强, Yang, Xuefei, 杨雪菲, Wang, Lei, 王磊, Zhang, Qinghua, 张清华, Cai, Zhaoxia, 蔡朝霞, Xu, Caiguo, 徐才国, Li, Xianghua, 李香花, Xiao, Jinghua, 肖景华, Meyers, Blake C., Zhang, Qifa, 张启发
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 27.12.2016
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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.
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
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  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
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  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
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  surname: Xiao
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  organization: National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China
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  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
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  surname: Zhang
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  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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10.1094/MPMI-20-5-0492
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DocumentTitleAlternate PMS1T confers photoperiod-sensitive male sterility
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Keywords long-noncoding RNA
phasiRNA
photoperiod-sensitive male sterility
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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.
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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
URI https://www.jstor.org/stable/26473042
https://www.ncbi.nlm.nih.gov/pubmed/27965387
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