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,...
Saved in:
Main Authors: | , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Elsevier
2025-01-01
|
Series: | Rice Science |
Subjects: | |
Online Access: | http://www.sciencedirect.com/science/article/pii/S1672630824000891 |
Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
_version_ | 1823856817256529920 |
---|---|
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. |
format | Article |
id | doaj-art-45fa6d1a897a4c20b9cfcc6e38a69f32 |
institution | Kabale University |
issn | 1672-6308 |
language | English |
publishDate | 2025-01-01 |
publisher | Elsevier |
record_format | Article |
series | Rice Science |
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 |
work_keys_str_mv | AT wangmingyue disruptionofenergymetabolismandreactiveoxygenspecieshomeostasisinhongliantypecytoplasmicmalesterilityhlcmsricepollen AT zhaoweibo disruptionofenergymetabolismandreactiveoxygenspecieshomeostasisinhongliantypecytoplasmicmalesterilityhlcmsricepollen AT fengxiaoya disruptionofenergymetabolismandreactiveoxygenspecieshomeostasisinhongliantypecytoplasmicmalesterilityhlcmsricepollen AT chenyi disruptionofenergymetabolismandreactiveoxygenspecieshomeostasisinhongliantypecytoplasmicmalesterilityhlcmsricepollen AT lijunhao disruptionofenergymetabolismandreactiveoxygenspecieshomeostasisinhongliantypecytoplasmicmalesterilityhlcmsricepollen AT fujinmei disruptionofenergymetabolismandreactiveoxygenspecieshomeostasisinhongliantypecytoplasmicmalesterilityhlcmsricepollen AT yanyingchun disruptionofenergymetabolismandreactiveoxygenspecieshomeostasisinhongliantypecytoplasmicmalesterilityhlcmsricepollen AT chuzhaohui disruptionofenergymetabolismandreactiveoxygenspecieshomeostasisinhongliantypecytoplasmicmalesterilityhlcmsricepollen AT huangwenchao disruptionofenergymetabolismandreactiveoxygenspecieshomeostasisinhongliantypecytoplasmicmalesterilityhlcmsricepollen |