Mitochondrial Dysfunction Causes Oxidative Stress and Tapetal Apoptosis in Chemical Hybridization Reagent-Induced Male Sterility in Wheat
Male sterility in plants has been strongly linked to mitochondrial dysfunction. Chemical hybridization agent (CHA)-induced male sterility is an important tool in crop heterosis. Therefore, it is important to better understand the relationship between mitochondria and CHA-induced male sterility in wh...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2018-01-01
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| Series: | Frontiers in Plant Science |
| Subjects: | |
| Online Access: | http://journal.frontiersin.org/article/10.3389/fpls.2017.02217/full |
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Article |
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DOAJ |
| language |
English |
| format |
Article |
| sources |
DOAJ |
| author |
Shuping Wang Shuping Wang Yingxin Zhang Qilu Song Zhengwu Fang Zheng Chen Yamin Zhang Lili Zhang Lin Zhang Na Niu Shoucai Ma Junwei Wang Yaqin Yao Zanmin Hu Gaisheng Zhang |
| spellingShingle |
Shuping Wang Shuping Wang Yingxin Zhang Qilu Song Zhengwu Fang Zheng Chen Yamin Zhang Lili Zhang Lin Zhang Na Niu Shoucai Ma Junwei Wang Yaqin Yao Zanmin Hu Gaisheng Zhang Mitochondrial Dysfunction Causes Oxidative Stress and Tapetal Apoptosis in Chemical Hybridization Reagent-Induced Male Sterility in Wheat Frontiers in Plant Science mitochondrial dysfunction oxidative stress tapetal programmed cell death chemical hybridization agent wheat |
| author_facet |
Shuping Wang Shuping Wang Yingxin Zhang Qilu Song Zhengwu Fang Zheng Chen Yamin Zhang Lili Zhang Lin Zhang Na Niu Shoucai Ma Junwei Wang Yaqin Yao Zanmin Hu Gaisheng Zhang |
| author_sort |
Shuping Wang |
| title |
Mitochondrial Dysfunction Causes Oxidative Stress and Tapetal Apoptosis in Chemical Hybridization Reagent-Induced Male Sterility in Wheat |
| title_short |
Mitochondrial Dysfunction Causes Oxidative Stress and Tapetal Apoptosis in Chemical Hybridization Reagent-Induced Male Sterility in Wheat |
| title_full |
Mitochondrial Dysfunction Causes Oxidative Stress and Tapetal Apoptosis in Chemical Hybridization Reagent-Induced Male Sterility in Wheat |
| title_fullStr |
Mitochondrial Dysfunction Causes Oxidative Stress and Tapetal Apoptosis in Chemical Hybridization Reagent-Induced Male Sterility in Wheat |
| title_full_unstemmed |
Mitochondrial Dysfunction Causes Oxidative Stress and Tapetal Apoptosis in Chemical Hybridization Reagent-Induced Male Sterility in Wheat |
| title_sort |
mitochondrial dysfunction causes oxidative stress and tapetal apoptosis in chemical hybridization reagent-induced male sterility in wheat |
| publisher |
Frontiers Media S.A. |
| series |
Frontiers in Plant Science |
| issn |
1664-462X |
| publishDate |
2018-01-01 |
| description |
Male sterility in plants has been strongly linked to mitochondrial dysfunction. Chemical hybridization agent (CHA)-induced male sterility is an important tool in crop heterosis. Therefore, it is important to better understand the relationship between mitochondria and CHA-induced male sterility in wheat. This study reports on the impairment of mitochondrial function duo to CHA-SQ-1, which occurs by decreasing cytochrome oxidase and adenosine triphosphate synthase protein levels and theirs activities, respiratory rate, and in turn results in the inhibition of the mitochondrial electron transport chain (ETC), excessive production of reactive oxygen species (ROS) and disruption of the alternative oxidase pathway. Subsequently, excessive ROS combined with MnSOD defects results in damage to the mitochondrial membrane, followed by ROS release into the cytoplasm. The microspores underwent severe oxidative stress during pollen development. Furthermore, chronic oxidative stress, together with the overexpression of type II metacaspase, triggered premature tapetal apoptosis, which resulted in pollen abortion. Accordingly, we propose a metabolic pathway for mitochondrial-mediated male sterility in wheat, which provides information on the molecular events underlying CHA-SQ-1-induced abortion of anthers and may serve as an additional guide to the practical application of hybrid breeding. |
| topic |
mitochondrial dysfunction oxidative stress tapetal programmed cell death chemical hybridization agent wheat |
| url |
http://journal.frontiersin.org/article/10.3389/fpls.2017.02217/full |
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doaj-0fe30deb4f1049da9a731f236c61e35d2020-11-24T23:58:48ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2018-01-01810.3389/fpls.2017.02217310601Mitochondrial Dysfunction Causes Oxidative Stress and Tapetal Apoptosis in Chemical Hybridization Reagent-Induced Male Sterility in WheatShuping Wang0Shuping Wang1Yingxin Zhang2Qilu Song3Zhengwu Fang4Zheng Chen5Yamin Zhang6Lili Zhang7Lin Zhang8Na Niu9Shoucai Ma10Junwei Wang11Yaqin Yao12Zanmin Hu13Gaisheng Zhang14Key Laboratory of Crop Heterosis of Shaanxi Province, College of Agronomy, Northwest A&F University, National Yangling Agricultural Biotechnology and Breeding Center, Yangling Branch of State Wheat Improvement Centre, Wheat Breeding Engineering Research Center, Ministry of Education, Yangling, ChinaHubei Key Laboratory of Waterlogging Disaster and Agricultural Use of Wetland, College of Agronomy, Yangtze University, Jingzhou, ChinaInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, ChinaKey Laboratory of Crop Heterosis of Shaanxi Province, College of Agronomy, Northwest A&F University, National Yangling Agricultural Biotechnology and Breeding Center, Yangling Branch of State Wheat Improvement Centre, Wheat Breeding Engineering Research Center, Ministry of Education, Yangling, ChinaHubei Key Laboratory of Waterlogging Disaster and Agricultural Use of Wetland, College of Agronomy, Yangtze University, Jingzhou, ChinaKey Laboratory of Crop Heterosis of Shaanxi Province, College of Agronomy, Northwest A&F University, National Yangling Agricultural Biotechnology and Breeding Center, Yangling Branch of State Wheat Improvement Centre, Wheat Breeding Engineering Research Center, Ministry of Education, Yangling, ChinaKey Laboratory of Crop Heterosis of Shaanxi Province, College of Agronomy, Northwest A&F University, National Yangling Agricultural Biotechnology and Breeding Center, Yangling Branch of State Wheat Improvement Centre, Wheat Breeding Engineering Research Center, Ministry of Education, Yangling, ChinaKey Laboratory of Crop Heterosis of Shaanxi Province, College of Agronomy, Northwest A&F University, National Yangling Agricultural Biotechnology and Breeding Center, Yangling Branch of State Wheat Improvement Centre, Wheat Breeding Engineering Research Center, Ministry of Education, Yangling, ChinaDepartment of Anaesthesia and Intensive Care, The Chinese University of Hong Kong, Hong Kong, ChinaKey Laboratory of Crop Heterosis of Shaanxi Province, College of Agronomy, Northwest A&F University, National Yangling Agricultural Biotechnology and Breeding Center, Yangling Branch of State Wheat Improvement Centre, Wheat Breeding Engineering Research Center, Ministry of Education, Yangling, ChinaKey Laboratory of Crop Heterosis of Shaanxi Province, College of Agronomy, Northwest A&F University, National Yangling Agricultural Biotechnology and Breeding Center, Yangling Branch of State Wheat Improvement Centre, Wheat Breeding Engineering Research Center, Ministry of Education, Yangling, ChinaKey Laboratory of Crop Heterosis of Shaanxi Province, College of Agronomy, Northwest A&F University, National Yangling Agricultural Biotechnology and Breeding Center, Yangling Branch of State Wheat Improvement Centre, Wheat Breeding Engineering Research Center, Ministry of Education, Yangling, ChinaCollege of Life Sciences, Northwest A&F University, Yangling, ChinaInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, ChinaKey Laboratory of Crop Heterosis of Shaanxi Province, College of Agronomy, Northwest A&F University, National Yangling Agricultural Biotechnology and Breeding Center, Yangling Branch of State Wheat Improvement Centre, Wheat Breeding Engineering Research Center, Ministry of Education, Yangling, ChinaMale sterility in plants has been strongly linked to mitochondrial dysfunction. Chemical hybridization agent (CHA)-induced male sterility is an important tool in crop heterosis. Therefore, it is important to better understand the relationship between mitochondria and CHA-induced male sterility in wheat. This study reports on the impairment of mitochondrial function duo to CHA-SQ-1, which occurs by decreasing cytochrome oxidase and adenosine triphosphate synthase protein levels and theirs activities, respiratory rate, and in turn results in the inhibition of the mitochondrial electron transport chain (ETC), excessive production of reactive oxygen species (ROS) and disruption of the alternative oxidase pathway. Subsequently, excessive ROS combined with MnSOD defects results in damage to the mitochondrial membrane, followed by ROS release into the cytoplasm. The microspores underwent severe oxidative stress during pollen development. Furthermore, chronic oxidative stress, together with the overexpression of type II metacaspase, triggered premature tapetal apoptosis, which resulted in pollen abortion. Accordingly, we propose a metabolic pathway for mitochondrial-mediated male sterility in wheat, which provides information on the molecular events underlying CHA-SQ-1-induced abortion of anthers and may serve as an additional guide to the practical application of hybrid breeding.http://journal.frontiersin.org/article/10.3389/fpls.2017.02217/fullmitochondrial dysfunctionoxidative stresstapetal programmed cell deathchemical hybridization agentwheat |