A toxin-antidote system contributes to interspecific reproductive isolation in rice

Abstract Breakdown of reproductive isolation facilitates flow of useful trait genes into crop plants from their wild relatives. Hybrid sterility, a major form of reproductive isolation exists between cultivated rice (Oryza sativa) and wild rice (O. meridionalis, Mer). Here, we report the cloning of...

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Main Authors: Shimin You, Zhigang Zhao, Xiaowen Yu, Shanshan Zhu, Jian Wang, Dekun Lei, Jiawu Zhou, Jing Li, Haiyuan Chen, Yanjia Xiao, Weiwei Chen, Qiming Wang, Jiayu Lu, Keyi Chen, Chunlei Zhou, Xin Zhang, Zhijun Cheng, Xiuping Guo, Yulong Ren, Xiaoming Zheng, Shijia Liu, Xi Liu, Yunlu Tian, Ling Jiang, Dayun Tao, Chuanyin Wu, Jianmin Wan
Format: Article
Language:English
Published: Nature Portfolio 2023-11-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-023-43015-6
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author Shimin You
Zhigang Zhao
Xiaowen Yu
Shanshan Zhu
Jian Wang
Dekun Lei
Jiawu Zhou
Jing Li
Haiyuan Chen
Yanjia Xiao
Weiwei Chen
Qiming Wang
Jiayu Lu
Keyi Chen
Chunlei Zhou
Xin Zhang
Zhijun Cheng
Xiuping Guo
Yulong Ren
Xiaoming Zheng
Shijia Liu
Xi Liu
Yunlu Tian
Ling Jiang
Dayun Tao
Chuanyin Wu
Jianmin Wan
author_facet Shimin You
Zhigang Zhao
Xiaowen Yu
Shanshan Zhu
Jian Wang
Dekun Lei
Jiawu Zhou
Jing Li
Haiyuan Chen
Yanjia Xiao
Weiwei Chen
Qiming Wang
Jiayu Lu
Keyi Chen
Chunlei Zhou
Xin Zhang
Zhijun Cheng
Xiuping Guo
Yulong Ren
Xiaoming Zheng
Shijia Liu
Xi Liu
Yunlu Tian
Ling Jiang
Dayun Tao
Chuanyin Wu
Jianmin Wan
author_sort Shimin You
collection DOAJ
description Abstract Breakdown of reproductive isolation facilitates flow of useful trait genes into crop plants from their wild relatives. Hybrid sterility, a major form of reproductive isolation exists between cultivated rice (Oryza sativa) and wild rice (O. meridionalis, Mer). Here, we report the cloning of qHMS1, a quantitative trait locus controlling hybrid male sterility between these two species. Like qHMS7, another locus we cloned previously, qHMS1 encodes a toxin-antidote system, but differs in the encoded proteins, their evolutionary origin, and action time point during pollen development. In plants heterozygous at qHMS1, ~ 50% of pollens carrying qHMS1-D (an allele from cultivated rice) are selectively killed. In plants heterozygous at both qHMS1 and qHMS7, ~ 75% pollens without co-presence of qHMS1-Mer and qHMS7-D are selectively killed, indicating that the antidotes function in a toxin-dependent manner. Our results indicate that different toxin-antidote systems provide stacked reproductive isolation for maintaining species identity and shed light on breakdown of hybrid male sterility.
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spelling doaj.art-d05086a5bf6341268f64699daec01d6f2023-11-20T09:54:02ZengNature PortfolioNature Communications2041-17232023-11-0114111310.1038/s41467-023-43015-6A toxin-antidote system contributes to interspecific reproductive isolation in riceShimin You0Zhigang Zhao1Xiaowen Yu2Shanshan Zhu3Jian Wang4Dekun Lei5Jiawu Zhou6Jing Li7Haiyuan Chen8Yanjia Xiao9Weiwei Chen10Qiming Wang11Jiayu Lu12Keyi Chen13Chunlei Zhou14Xin Zhang15Zhijun Cheng16Xiuping Guo17Yulong Ren18Xiaoming Zheng19Shijia Liu20Xi Liu21Yunlu Tian22Ling Jiang23Dayun Tao24Chuanyin Wu25Jianmin Wan26State Key Laboratory for Crop Genetics & Germplasm Enhancement and Utilization, Nanjing Agricultural University, Zhongshan Biological Breeding LaboratoryState Key Laboratory for Crop Genetics & Germplasm Enhancement and Utilization, Nanjing Agricultural University, Zhongshan Biological Breeding LaboratoryState Key Laboratory for Crop Genetics & Germplasm Enhancement and Utilization, Nanjing Agricultural University, Zhongshan Biological Breeding LaboratoryState Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Science, Chinese Academy of Agricultural Sciences (CAAS)State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Science, Chinese Academy of Agricultural Sciences (CAAS)State Key Laboratory for Crop Genetics & Germplasm Enhancement and Utilization, Nanjing Agricultural University, Zhongshan Biological Breeding LaboratoryYunnan Seed Laboratory/Yunnan Key Laboratory for Rice Genetic Improvement, Food Crops Research Institute, Yunnan Academy of Agricultural Sciences (YAAS)Yunnan Seed Laboratory/Yunnan Key Laboratory for Rice Genetic Improvement, Food Crops Research Institute, Yunnan Academy of Agricultural Sciences (YAAS)State Key Laboratory for Crop Genetics & Germplasm Enhancement and Utilization, Nanjing Agricultural University, Zhongshan Biological Breeding LaboratoryState Key Laboratory for Crop Genetics & Germplasm Enhancement and Utilization, Nanjing Agricultural University, Zhongshan Biological Breeding LaboratoryState Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Science, Chinese Academy of Agricultural Sciences (CAAS)State Key Laboratory for Crop Genetics & Germplasm Enhancement and Utilization, Nanjing Agricultural University, Zhongshan Biological Breeding LaboratoryState Key Laboratory for Crop Genetics & Germplasm Enhancement and Utilization, Nanjing Agricultural University, Zhongshan Biological Breeding LaboratoryState Key Laboratory for Crop Genetics & Germplasm Enhancement and Utilization, Nanjing Agricultural University, Zhongshan Biological Breeding LaboratoryState Key Laboratory for Crop Genetics & Germplasm Enhancement and Utilization, Nanjing Agricultural University, Zhongshan Biological Breeding LaboratoryState Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Science, Chinese Academy of Agricultural Sciences (CAAS)State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Science, Chinese Academy of Agricultural Sciences (CAAS)State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Science, Chinese Academy of Agricultural Sciences (CAAS)State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Science, Chinese Academy of Agricultural Sciences (CAAS)State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Science, Chinese Academy of Agricultural Sciences (CAAS)State Key Laboratory for Crop Genetics & Germplasm Enhancement and Utilization, Nanjing Agricultural University, Zhongshan Biological Breeding LaboratoryState Key Laboratory for Crop Genetics & Germplasm Enhancement and Utilization, Nanjing Agricultural University, Zhongshan Biological Breeding LaboratoryState Key Laboratory for Crop Genetics & Germplasm Enhancement and Utilization, Nanjing Agricultural University, Zhongshan Biological Breeding LaboratoryState Key Laboratory for Crop Genetics & Germplasm Enhancement and Utilization, Nanjing Agricultural University, Zhongshan Biological Breeding LaboratoryYunnan Seed Laboratory/Yunnan Key Laboratory for Rice Genetic Improvement, Food Crops Research Institute, Yunnan Academy of Agricultural Sciences (YAAS)State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Science, Chinese Academy of Agricultural Sciences (CAAS)State Key Laboratory for Crop Genetics & Germplasm Enhancement and Utilization, Nanjing Agricultural University, Zhongshan Biological Breeding LaboratoryAbstract Breakdown of reproductive isolation facilitates flow of useful trait genes into crop plants from their wild relatives. Hybrid sterility, a major form of reproductive isolation exists between cultivated rice (Oryza sativa) and wild rice (O. meridionalis, Mer). Here, we report the cloning of qHMS1, a quantitative trait locus controlling hybrid male sterility between these two species. Like qHMS7, another locus we cloned previously, qHMS1 encodes a toxin-antidote system, but differs in the encoded proteins, their evolutionary origin, and action time point during pollen development. In plants heterozygous at qHMS1, ~ 50% of pollens carrying qHMS1-D (an allele from cultivated rice) are selectively killed. In plants heterozygous at both qHMS1 and qHMS7, ~ 75% pollens without co-presence of qHMS1-Mer and qHMS7-D are selectively killed, indicating that the antidotes function in a toxin-dependent manner. Our results indicate that different toxin-antidote systems provide stacked reproductive isolation for maintaining species identity and shed light on breakdown of hybrid male sterility.https://doi.org/10.1038/s41467-023-43015-6
spellingShingle Shimin You
Zhigang Zhao
Xiaowen Yu
Shanshan Zhu
Jian Wang
Dekun Lei
Jiawu Zhou
Jing Li
Haiyuan Chen
Yanjia Xiao
Weiwei Chen
Qiming Wang
Jiayu Lu
Keyi Chen
Chunlei Zhou
Xin Zhang
Zhijun Cheng
Xiuping Guo
Yulong Ren
Xiaoming Zheng
Shijia Liu
Xi Liu
Yunlu Tian
Ling Jiang
Dayun Tao
Chuanyin Wu
Jianmin Wan
A toxin-antidote system contributes to interspecific reproductive isolation in rice
Nature Communications
title A toxin-antidote system contributes to interspecific reproductive isolation in rice
title_full A toxin-antidote system contributes to interspecific reproductive isolation in rice
title_fullStr A toxin-antidote system contributes to interspecific reproductive isolation in rice
title_full_unstemmed A toxin-antidote system contributes to interspecific reproductive isolation in rice
title_short A toxin-antidote system contributes to interspecific reproductive isolation in rice
title_sort toxin antidote system contributes to interspecific reproductive isolation in rice
url https://doi.org/10.1038/s41467-023-43015-6
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