The subunit of RNA N6-methyladenosine methyltransferase OsFIP regulates early degeneration of microspores in rice
N6-Methyladenosine (m6A) RNA methylation plays important roles during development in different species. However, knowledge of m6A RNA methylation in monocots remains limited. In this study, we reported that OsFIP and OsMTA2 are the components of m6A RNA methyltransferase complex in rice and uncovere...
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| Published in | PLoS genetics Vol. 15; no. 5; p. e1008120 |
|---|---|
| Main Authors | , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
22.05.2019
Public Library of Science (PLoS) |
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| Online Access | Get full text |
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| Abstract | N6-Methyladenosine (m6A) RNA methylation plays important roles during development in different species. However, knowledge of m6A RNA methylation in monocots remains limited. In this study, we reported that OsFIP and OsMTA2 are the components of m6A RNA methyltransferase complex in rice and uncovered a previously unknown function of m6A RNA methylation in regulation of plant sporogenesis. Importantly, OsFIP is essential for rice male gametogenesis. Knocking out of OsFIP results in early degeneration of microspores at the vacuolated pollen stage and simultaneously causes abnormal meiosis in prophase I. We further analyzed the profile of rice m6A modification during sporogenesis in both WT and OsFIP loss-of-function plants, and identified a rice panicle specific m6A modification motif "UGWAMH". Interestingly, we found that OsFIP directly mediates the m6A methylation of a set of threonine protease and NTPase mRNAs and is essential for their expression and/or splicing, which in turn regulates the progress of sporogenesis. Our findings revealed for the first time that OsFIP plays an indispensable role in plant early sporogenesis. This study also provides evidence for the different functions of the m6A RNA methyltransferase complex between rice and Arabidopsis. |
|---|---|
| AbstractList | N
6
-Methyladenosine (m
6
A) RNA methylation plays important roles during development in different species. However, knowledge of m
6
A RNA methylation in monocots remains limited. In this study, we reported that
OsFIP
and
OsMTA2
are the components of m
6
A RNA methyltransferase complex in rice and uncovered a previously unknown function of m
6
A RNA methylation in regulation of plant sporogenesis. Importantly,
OsFIP
is essential for rice male gametogenesis. Knocking out of
OsFIP
results in early degeneration of microspores at the vacuolated pollen stage and simultaneously causes abnormal meiosis in prophase I. We further analyzed the profile of rice m
6
A modification during sporogenesis in both WT and OsFIP loss-of-function plants, and identified a rice panicle specific m
6
A modification motif “UGWAMH”. Interestingly, we found that
OsFIP
directly mediates the m
6
A methylation of a set of threonine protease and NTPase mRNAs and is essential for their expression and/or splicing, which in turn regulates the progress of sporogenesis. Our findings revealed for the first time that
OsFIP
plays an indispensable role in plant early sporogenesis. This study also provides evidence for the different functions of the m
6
A RNA methyltransferase complex between rice and Arabidopsis.
N
6
-Methyladenosine (m
6
A) is the most abundant internal modification of eukaryotic mRNA, and m
6
A mRNA methylation affects almost every stage of mRNA metabolism. However, the components of the m
6
A methyltransferase complex and their functions in monocots are completely unknown. In this study, we identified the components of the m
6
A RNA methyltransferase complex in rice, and uncovered a hitherto unknown function of m
6
A RNA methylation in regulating early microspore apoptosis. We also systematically analyzed the characteristics of m
6
A modification during sporogenesis for the first time, and revealed the sporogenesis stage-specific distribution of m
6
A peaks along genes and the specific modification motif in rice, which are different from that of other species and other developmental stages. The target genes of m
6
A methyltransferase complex member
OsFIP
were also identified in this study. Given the important roles of posttranscriptional mRNA regulation in gene expression and sporogenesis in plants, the findings of this study should stimulate more studies exploring the role of plant m
6
A methyltransferase and other components. N6-Methyladenosine (m6A) RNA methylation plays important roles during development in different species. However, knowledge of m6A RNA methylation in monocots remains limited. In this study, we reported that OsFIP and OsMTA2 are the components of m6A RNA methyltransferase complex in rice and uncovered a previously unknown function of m6A RNA methylation in regulation of plant sporogenesis. Importantly, OsFIP is essential for rice male gametogenesis. Knocking out of OsFIP results in early degeneration of microspores at the vacuolated pollen stage and simultaneously causes abnormal meiosis in prophase I. We further analyzed the profile of rice m6A modification during sporogenesis in both WT and OsFIP loss-of-function plants, and identified a rice panicle specific m6A modification motif “UGWAMH”. Interestingly, we found that OsFIP directly mediates the m6A methylation of a set of threonine protease and NTPase mRNAs and is essential for their expression and/or splicing, which in turn regulates the progress of sporogenesis. Our findings revealed for the first time that OsFIP plays an indispensable role in plant early sporogenesis. This study also provides evidence for the different functions of the m6A RNA methyltransferase complex between rice and Arabidopsis. N.sup.6 -Methyladenosine (m.sup.6 A) RNA methylation plays important roles during development in different species. However, knowledge of m.sup.6 A RNA methylation in monocots remains limited. In this study, we reported that OsFIP and OsMTA2 are the components of m.sup.6 A RNA methyltransferase complex in rice and uncovered a previously unknown function of m.sup.6 A RNA methylation in regulation of plant sporogenesis. Importantly, OsFIP is essential for rice male gametogenesis. Knocking out of OsFIP results in early degeneration of microspores at the vacuolated pollen stage and simultaneously causes abnormal meiosis in prophase I. We further analyzed the profile of rice m.sup.6 A modification during sporogenesis in both WT and OsFIP loss-of-function plants, and identified a rice panicle specific m.sup.6 A modification motif "UGWAMH". Interestingly, we found that OsFIP directly mediates the m.sup.6 A methylation of a set of threonine protease and NTPase mRNAs and is essential for their expression and/or splicing, which in turn regulates the progress of sporogenesis. Our findings revealed for the first time that OsFIP plays an indispensable role in plant early sporogenesis. This study also provides evidence for the different functions of the m.sup.6 A RNA methyltransferase complex between rice and Arabidopsis. N6-Methyladenosine (m6A) RNA methylation plays important roles during development in different species. However, knowledge of m6A RNA methylation in monocots remains limited. In this study, we reported that OsFIP and OsMTA2 are the components of m6A RNA methyltransferase complex in rice and uncovered a previously unknown function of m6A RNA methylation in regulation of plant sporogenesis. Importantly, OsFIP is essential for rice male gametogenesis. Knocking out of OsFIP results in early degeneration of microspores at the vacuolated pollen stage and simultaneously causes abnormal meiosis in prophase I. We further analyzed the profile of rice m6A modification during sporogenesis in both WT and OsFIP loss-of-function plants, and identified a rice panicle specific m6A modification motif "UGWAMH". Interestingly, we found that OsFIP directly mediates the m6A methylation of a set of threonine protease and NTPase mRNAs and is essential for their expression and/or splicing, which in turn regulates the progress of sporogenesis. Our findings revealed for the first time that OsFIP plays an indispensable role in plant early sporogenesis. This study also provides evidence for the different functions of the m6A RNA methyltransferase complex between rice and Arabidopsis.N6-Methyladenosine (m6A) RNA methylation plays important roles during development in different species. However, knowledge of m6A RNA methylation in monocots remains limited. In this study, we reported that OsFIP and OsMTA2 are the components of m6A RNA methyltransferase complex in rice and uncovered a previously unknown function of m6A RNA methylation in regulation of plant sporogenesis. Importantly, OsFIP is essential for rice male gametogenesis. Knocking out of OsFIP results in early degeneration of microspores at the vacuolated pollen stage and simultaneously causes abnormal meiosis in prophase I. We further analyzed the profile of rice m6A modification during sporogenesis in both WT and OsFIP loss-of-function plants, and identified a rice panicle specific m6A modification motif "UGWAMH". Interestingly, we found that OsFIP directly mediates the m6A methylation of a set of threonine protease and NTPase mRNAs and is essential for their expression and/or splicing, which in turn regulates the progress of sporogenesis. Our findings revealed for the first time that OsFIP plays an indispensable role in plant early sporogenesis. This study also provides evidence for the different functions of the m6A RNA methyltransferase complex between rice and Arabidopsis. |
| Audience | Academic |
| Author | Bai, Mei Yu, Yang Feng, Yan-Zhao Liao, Jian-You Lei, Meng-Qi Zhou, Yan-Fei Zhang, Yu-Chan Wu, Hong Yang, Yu-Wei Zhang, Fan Chen, Yue-Qin |
| AuthorAffiliation | 3 State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, College of Life Sciences, South China Agricultural University, Guangzhou, P. R. China 2 Medical Research Center, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou, China The University of Adelaide, AUSTRALIA 1 Guangdong Provincial Key Laboratory of Plant Resources, State Key Laboratory for Biocontrol, School of Life Sciences, Sun Yat-Sen University, Guangzhou, P. R. China |
| AuthorAffiliation_xml | – name: The University of Adelaide, AUSTRALIA – name: 3 State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, College of Life Sciences, South China Agricultural University, Guangzhou, P. R. China – name: 2 Medical Research Center, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou, China – name: 1 Guangdong Provincial Key Laboratory of Plant Resources, State Key Laboratory for Biocontrol, School of Life Sciences, Sun Yat-Sen University, Guangzhou, P. R. China |
| Author_xml | – sequence: 1 givenname: Fan surname: Zhang fullname: Zhang, Fan – sequence: 2 givenname: Yu-Chan orcidid: 0000-0003-0612-8059 surname: Zhang fullname: Zhang, Yu-Chan – sequence: 3 givenname: Jian-You surname: Liao fullname: Liao, Jian-You – sequence: 4 givenname: Yang surname: Yu fullname: Yu, Yang – sequence: 5 givenname: Yan-Fei surname: Zhou fullname: Zhou, Yan-Fei – sequence: 6 givenname: Yan-Zhao surname: Feng fullname: Feng, Yan-Zhao – sequence: 7 givenname: Yu-Wei surname: Yang fullname: Yang, Yu-Wei – sequence: 8 givenname: Meng-Qi surname: Lei fullname: Lei, Meng-Qi – sequence: 9 givenname: Mei surname: Bai fullname: Bai, Mei – sequence: 10 givenname: Hong surname: Wu fullname: Wu, Hong – sequence: 11 givenname: Yue-Qin surname: Chen fullname: Chen, Yue-Qin |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31116744$$D View this record in MEDLINE/PubMed |
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| Copyright | COPYRIGHT 2019 Public Library of Science 2019 Zhang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2019 Zhang et al 2019 Zhang et al |
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| DOI | 10.1371/journal.pgen.1008120 |
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| Notes | new_version ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 The authors declare that they have no competing financial interests. |
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| SubjectTerms | Adenosine - analogs & derivatives Amino Acid Motifs Amino acids Arabidopsis Arabidopsis - genetics Arabidopsis - growth & development Arabidopsis - metabolism Biology and Life Sciences Botanical research CRISPR Degeneration Gametogenesis Gametogenesis, Plant Gene expression Gene Expression Regulation, Plant Genetic aspects Genetic research Laboratories Life sciences Loss of Function Mutation Mammals Meiosis Meiotic Prophase I Messenger RNA Methylation Methyltransferases Methyltransferases - genetics Methyltransferases - metabolism Mutation N6-methyladenosine Nucleoside-Triphosphatase - genetics Nucleoside-Triphosphatase - metabolism Oryza Oryza - genetics Oryza - growth & development Oryza - metabolism Physical Sciences Physiological aspects Plant Proteins - genetics Plant Proteins - metabolism Pollen - genetics Pollen - growth & development Pollen - metabolism Prophase Proteases Protein Subunits - genetics Protein Subunits - metabolism Proteins Research and Analysis Methods Ribonucleic acid Rice RNA RNA, Plant Species Specificity Splicing Spores Sporogenesis Stem cells Threonine Transferases |
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| Title | The subunit of RNA N6-methyladenosine methyltransferase OsFIP regulates early degeneration of microspores in rice |
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