Rice FLOURY SHRUNKEN ENDOSPERM 5 Encodes a Putative Plant Organelle RNA Recognition Protein that Is Required for cis-Splicing of Mitochondrial nad4 Intron 1

Abstract Background The sequences of several important mitochondrion-encoded genes involved in respiration in higher plants are interrupted by introns. Many nuclear-encoded factors are involved in splicing these introns, but the mechanisms underlying this splicing remain unknown. Results We isolated...

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Main Authors: Liang Wang, Wenwei Zhang, Shijia Liu, Yunlu Tian, Xi Liu, Haigang Yan, Yue Cai, Xuan Teng, Hui Dong, Rongbo Chen, Xiaokang Jiang, Yihua Wang, Jianmin Wan
Format: Article
Language:English
Published: SpringerOpen 2021-03-01
Series:Rice
Subjects:
Online Access:https://doi.org/10.1186/s12284-021-00463-2
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author Liang Wang
Wenwei Zhang
Shijia Liu
Yunlu Tian
Xi Liu
Haigang Yan
Yue Cai
Xuan Teng
Hui Dong
Rongbo Chen
Xiaokang Jiang
Yihua Wang
Jianmin Wan
author_facet Liang Wang
Wenwei Zhang
Shijia Liu
Yunlu Tian
Xi Liu
Haigang Yan
Yue Cai
Xuan Teng
Hui Dong
Rongbo Chen
Xiaokang Jiang
Yihua Wang
Jianmin Wan
author_sort Liang Wang
collection DOAJ
description Abstract Background The sequences of several important mitochondrion-encoded genes involved in respiration in higher plants are interrupted by introns. Many nuclear-encoded factors are involved in splicing these introns, but the mechanisms underlying this splicing remain unknown. Results We isolated and characterized a rice mutant named floury shrunken endosperm 5 (fse5). In addition to having floury shrunken endosperm, the fse5 seeds either failed to germinate or produced seedlings which grew slowly and died ultimately. Fse5 encodes a putative plant organelle RNA recognition (PORR) protein targeted to mitochondria. Mutation of Fse5 hindered the splicing of the first intron of nad4, which encodes an essential subunit of mitochondrial NADH dehydrogenase complex I. The assembly and NADH dehydrogenase activity of complex I were subsequently disrupted by this mutation, and the structure of the mitochondria was abnormal in the fse5 mutant. The FSE5 protein was shown to interact with mitochondrial intron splicing factor 68 (MISF68), which is also a splicing factor for nad4 intron 1 identified previously via yeast two-hybrid (Y2H) assays. Conclusion Fse5 which encodes a PORR domain-containing protein, is essential for the splicing of nad4 intron 1, and loss of Fse5 function affects seed development and seedling growth.
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spelling doaj.art-ea2c57cbfcb3443db126447d1551f1222022-12-21T22:23:39ZengSpringerOpenRice1939-84251939-84332021-03-0114111310.1186/s12284-021-00463-2Rice FLOURY SHRUNKEN ENDOSPERM 5 Encodes a Putative Plant Organelle RNA Recognition Protein that Is Required for cis-Splicing of Mitochondrial nad4 Intron 1Liang Wang0Wenwei Zhang1Shijia Liu2Yunlu Tian3Xi Liu4Haigang Yan5Yue Cai6Xuan Teng7Hui Dong8Rongbo Chen9Xiaokang Jiang10Yihua Wang11Jianmin Wan12State Key Laboratory for Crop Genetics and Germplasm Enhancement, Jiangsu Plant Gene Engineering Research Center, Nanjing Agricultural UniversityState Key Laboratory for Crop Genetics and Germplasm Enhancement, Jiangsu Plant Gene Engineering Research Center, Nanjing Agricultural UniversityState Key Laboratory for Crop Genetics and Germplasm Enhancement, Jiangsu Plant Gene Engineering Research Center, Nanjing Agricultural UniversityState Key Laboratory for Crop Genetics and Germplasm Enhancement, Jiangsu Plant Gene Engineering Research Center, Nanjing Agricultural UniversityState Key Laboratory for Crop Genetics and Germplasm Enhancement, Jiangsu Plant Gene Engineering Research Center, Nanjing Agricultural UniversityState Key Laboratory for Crop Genetics and Germplasm Enhancement, Jiangsu Plant Gene Engineering Research Center, Nanjing Agricultural UniversityState Key Laboratory for Crop Genetics and Germplasm Enhancement, Jiangsu Plant Gene Engineering Research Center, Nanjing Agricultural UniversityState Key Laboratory for Crop Genetics and Germplasm Enhancement, Jiangsu Plant Gene Engineering Research Center, Nanjing Agricultural UniversityState Key Laboratory for Crop Genetics and Germplasm Enhancement, Jiangsu Plant Gene Engineering Research Center, Nanjing Agricultural UniversityState Key Laboratory for Crop Genetics and Germplasm Enhancement, Jiangsu Plant Gene Engineering Research Center, Nanjing Agricultural UniversityState Key Laboratory for Crop Genetics and Germplasm Enhancement, Jiangsu Plant Gene Engineering Research Center, Nanjing Agricultural UniversityState Key Laboratory for Crop Genetics and Germplasm Enhancement, Jiangsu Plant Gene Engineering Research Center, Nanjing Agricultural UniversityState Key Laboratory for Crop Genetics and Germplasm Enhancement, Jiangsu Plant Gene Engineering Research Center, Nanjing Agricultural UniversityAbstract Background The sequences of several important mitochondrion-encoded genes involved in respiration in higher plants are interrupted by introns. Many nuclear-encoded factors are involved in splicing these introns, but the mechanisms underlying this splicing remain unknown. Results We isolated and characterized a rice mutant named floury shrunken endosperm 5 (fse5). In addition to having floury shrunken endosperm, the fse5 seeds either failed to germinate or produced seedlings which grew slowly and died ultimately. Fse5 encodes a putative plant organelle RNA recognition (PORR) protein targeted to mitochondria. Mutation of Fse5 hindered the splicing of the first intron of nad4, which encodes an essential subunit of mitochondrial NADH dehydrogenase complex I. The assembly and NADH dehydrogenase activity of complex I were subsequently disrupted by this mutation, and the structure of the mitochondria was abnormal in the fse5 mutant. The FSE5 protein was shown to interact with mitochondrial intron splicing factor 68 (MISF68), which is also a splicing factor for nad4 intron 1 identified previously via yeast two-hybrid (Y2H) assays. Conclusion Fse5 which encodes a PORR domain-containing protein, is essential for the splicing of nad4 intron 1, and loss of Fse5 function affects seed development and seedling growth.https://doi.org/10.1186/s12284-021-00463-2cis-splicingMitochondrianad4 intron 1NADH dehydrogenaseOryza sativaSeed development
spellingShingle Liang Wang
Wenwei Zhang
Shijia Liu
Yunlu Tian
Xi Liu
Haigang Yan
Yue Cai
Xuan Teng
Hui Dong
Rongbo Chen
Xiaokang Jiang
Yihua Wang
Jianmin Wan
Rice FLOURY SHRUNKEN ENDOSPERM 5 Encodes a Putative Plant Organelle RNA Recognition Protein that Is Required for cis-Splicing of Mitochondrial nad4 Intron 1
Rice
cis-splicing
Mitochondria
nad4 intron 1
NADH dehydrogenase
Oryza sativa
Seed development
title Rice FLOURY SHRUNKEN ENDOSPERM 5 Encodes a Putative Plant Organelle RNA Recognition Protein that Is Required for cis-Splicing of Mitochondrial nad4 Intron 1
title_full Rice FLOURY SHRUNKEN ENDOSPERM 5 Encodes a Putative Plant Organelle RNA Recognition Protein that Is Required for cis-Splicing of Mitochondrial nad4 Intron 1
title_fullStr Rice FLOURY SHRUNKEN ENDOSPERM 5 Encodes a Putative Plant Organelle RNA Recognition Protein that Is Required for cis-Splicing of Mitochondrial nad4 Intron 1
title_full_unstemmed Rice FLOURY SHRUNKEN ENDOSPERM 5 Encodes a Putative Plant Organelle RNA Recognition Protein that Is Required for cis-Splicing of Mitochondrial nad4 Intron 1
title_short Rice FLOURY SHRUNKEN ENDOSPERM 5 Encodes a Putative Plant Organelle RNA Recognition Protein that Is Required for cis-Splicing of Mitochondrial nad4 Intron 1
title_sort rice floury shrunken endosperm 5 encodes a putative plant organelle rna recognition protein that is required for cis splicing of mitochondrial nad4 intron 1
topic cis-splicing
Mitochondria
nad4 intron 1
NADH dehydrogenase
Oryza sativa
Seed development
url https://doi.org/10.1186/s12284-021-00463-2
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