Disruption of Energy Metabolism and Reactive Oxygen Species Homeostasis in Honglian Type-Cytoplasmic Male Sterility (HL-CMS) Rice Pollen

Honglian type-cytoplasmic male sterility (HL-CMS) is caused by the inter-communication between the nucleus and mitochondria. However, the mechanisms by which sterility genes regulate metabolic alterations and changes in mitochondrial morphology in the pollen of HL-CMS remain unclear. In this study,...

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Main Authors: Wang Mingyue, Zhao Weibo, Feng Xiaoya, Chen Yi, Li Junhao, Fu Jinmei, Yan Yingchun, Chu Zhaohui, Huang Wenchao
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Rice Science
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Online Access:http://www.sciencedirect.com/science/article/pii/S1672630824000891
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author Wang Mingyue
Zhao Weibo
Feng Xiaoya
Chen Yi
Li Junhao
Fu Jinmei
Yan Yingchun
Chu Zhaohui
Huang Wenchao
author_facet Wang Mingyue
Zhao Weibo
Feng Xiaoya
Chen Yi
Li Junhao
Fu Jinmei
Yan Yingchun
Chu Zhaohui
Huang Wenchao
author_sort Wang Mingyue
collection DOAJ
description Honglian type-cytoplasmic male sterility (HL-CMS) is caused by the inter-communication between the nucleus and mitochondria. However, the mechanisms by which sterility genes regulate metabolic alterations and changes in mitochondrial morphology in the pollen of HL-CMS remain unclear. In this study, we compared the morphological differences between the pollen of the male sterile line YA and the near-isogenic line NIL-Rf6 using hematoxylin-eosin staining and 4ʹ,6-diamidino-2-phenylindole (DAPI) staining. HL-CMS is characterized by gametophytic sterility, where the aborted pollen grains are empty, and the tapetal layer remains intact. Transmission electron microscopy was employed to observe mitochondrial morphological changes at the microspore stage, revealing significant mitochondrial alterations, characterized by the formation of 'large spherical mitochondria', occurred at the binucleate stage in the YA line. Additionally, metabolomics analysis revealed decreased levels of metabolites associated with the carbohydrate and flavonoid pathways. Notably, the decrease in flavonoids was found to contribute to an elevation in reactive oxygen species (ROS) levels. Therefore, we propose a model in which rice fertility is modulated by the levels of pollen carbohydrates and flavonoid metabolites, with impaired mitochondrial energy production and reduced flavonoid biosynthesis as the main causes of ROS accumulation and pollen abortion in rice.
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spelling doaj-art-45fa6d1a897a4c20b9cfcc6e38a69f322025-02-12T05:30:49ZengElsevierRice Science1672-63082025-01-013218193Disruption of Energy Metabolism and Reactive Oxygen Species Homeostasis in Honglian Type-Cytoplasmic Male Sterility (HL-CMS) Rice PollenWang Mingyue0Zhao Weibo1Feng Xiaoya2Chen Yi3Li Junhao4Fu Jinmei5Yan Yingchun6Chu Zhaohui7Huang Wenchao8State Key Laboratory of Hybrid Rice, Key Laboratory for Research and Utilization of Heterosis in Indica Rice, the Ministry of Agriculture and Rural Affairs / Department of Genetics, College of Life Sciences, Wuhan University, Wuhan 430072, ChinaState Key Laboratory of Hybrid Rice, Key Laboratory for Research and Utilization of Heterosis in Indica Rice, the Ministry of Agriculture and Rural Affairs / Department of Genetics, College of Life Sciences, Wuhan University, Wuhan 430072, ChinaState Key Laboratory of Hybrid Rice, Key Laboratory for Research and Utilization of Heterosis in Indica Rice, the Ministry of Agriculture and Rural Affairs / Department of Genetics, College of Life Sciences, Wuhan University, Wuhan 430072, ChinaState Key Laboratory of Hybrid Rice, Key Laboratory for Research and Utilization of Heterosis in Indica Rice, the Ministry of Agriculture and Rural Affairs / Department of Genetics, College of Life Sciences, Wuhan University, Wuhan 430072, ChinaState Key Laboratory of Hybrid Rice, Key Laboratory for Research and Utilization of Heterosis in Indica Rice, the Ministry of Agriculture and Rural Affairs / Department of Genetics, College of Life Sciences, Wuhan University, Wuhan 430072, ChinaState Key Laboratory of Hybrid Rice, Key Laboratory for Research and Utilization of Heterosis in Indica Rice, the Ministry of Agriculture and Rural Affairs / Department of Genetics, College of Life Sciences, Wuhan University, Wuhan 430072, ChinaState Key Laboratory of Hybrid Rice, Key Laboratory for Research and Utilization of Heterosis in Indica Rice, the Ministry of Agriculture and Rural Affairs / Department of Genetics, College of Life Sciences, Wuhan University, Wuhan 430072, ChinaState Key Laboratory of Hybrid Rice, Key Laboratory for Research and Utilization of Heterosis in Indica Rice, the Ministry of Agriculture and Rural Affairs / Department of Genetics, College of Life Sciences, Wuhan University, Wuhan 430072, ChinaCorresponding author.; State Key Laboratory of Hybrid Rice, Key Laboratory for Research and Utilization of Heterosis in Indica Rice, the Ministry of Agriculture and Rural Affairs / Department of Genetics, College of Life Sciences, Wuhan University, Wuhan 430072, ChinaHonglian type-cytoplasmic male sterility (HL-CMS) is caused by the inter-communication between the nucleus and mitochondria. However, the mechanisms by which sterility genes regulate metabolic alterations and changes in mitochondrial morphology in the pollen of HL-CMS remain unclear. In this study, we compared the morphological differences between the pollen of the male sterile line YA and the near-isogenic line NIL-Rf6 using hematoxylin-eosin staining and 4ʹ,6-diamidino-2-phenylindole (DAPI) staining. HL-CMS is characterized by gametophytic sterility, where the aborted pollen grains are empty, and the tapetal layer remains intact. Transmission electron microscopy was employed to observe mitochondrial morphological changes at the microspore stage, revealing significant mitochondrial alterations, characterized by the formation of 'large spherical mitochondria', occurred at the binucleate stage in the YA line. Additionally, metabolomics analysis revealed decreased levels of metabolites associated with the carbohydrate and flavonoid pathways. Notably, the decrease in flavonoids was found to contribute to an elevation in reactive oxygen species (ROS) levels. Therefore, we propose a model in which rice fertility is modulated by the levels of pollen carbohydrates and flavonoid metabolites, with impaired mitochondrial energy production and reduced flavonoid biosynthesis as the main causes of ROS accumulation and pollen abortion in rice.http://www.sciencedirect.com/science/article/pii/S1672630824000891cytoplasmic male sterilitypollenreactive oxygen speciesricemitochondrial metabolite
spellingShingle Wang Mingyue
Zhao Weibo
Feng Xiaoya
Chen Yi
Li Junhao
Fu Jinmei
Yan Yingchun
Chu Zhaohui
Huang Wenchao
Disruption of Energy Metabolism and Reactive Oxygen Species Homeostasis in Honglian Type-Cytoplasmic Male Sterility (HL-CMS) Rice Pollen
Rice Science
cytoplasmic male sterility
pollen
reactive oxygen species
rice
mitochondrial metabolite
title Disruption of Energy Metabolism and Reactive Oxygen Species Homeostasis in Honglian Type-Cytoplasmic Male Sterility (HL-CMS) Rice Pollen
title_full Disruption of Energy Metabolism and Reactive Oxygen Species Homeostasis in Honglian Type-Cytoplasmic Male Sterility (HL-CMS) Rice Pollen
title_fullStr Disruption of Energy Metabolism and Reactive Oxygen Species Homeostasis in Honglian Type-Cytoplasmic Male Sterility (HL-CMS) Rice Pollen
title_full_unstemmed Disruption of Energy Metabolism and Reactive Oxygen Species Homeostasis in Honglian Type-Cytoplasmic Male Sterility (HL-CMS) Rice Pollen
title_short Disruption of Energy Metabolism and Reactive Oxygen Species Homeostasis in Honglian Type-Cytoplasmic Male Sterility (HL-CMS) Rice Pollen
title_sort disruption of energy metabolism and reactive oxygen species homeostasis in honglian type cytoplasmic male sterility hl cms rice pollen
topic cytoplasmic male sterility
pollen
reactive oxygen species
rice
mitochondrial metabolite
url http://www.sciencedirect.com/science/article/pii/S1672630824000891
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