Comparative Transcriptome Analysis Reveals a Potential Regulatory Network for Ogura Cytoplasmic Male Sterility in Cabbage (<i>Brassica oleracea</i> L.)

Ogura cytoplasmic male sterility (CMS) lines are widely used breeding materials in cruciferous crops and play important roles in heterosis utilization; however, the sterility mechanism remains unclear. To investigate the microspore development process and gene expression changes after the introducti...

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Main Authors: Li Chen, Wenjing Ren, Bin Zhang, Huiling Guo, Zhiyuan Fang, Limei Yang, Mu Zhuang, Honghao Lv, Yong Wang, Jialei Ji, Xilin Hou, Yangyong Zhang
Format: Article
Language:English
Published: MDPI AG 2023-04-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/24/7/6703
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author Li Chen
Wenjing Ren
Bin Zhang
Huiling Guo
Zhiyuan Fang
Limei Yang
Mu Zhuang
Honghao Lv
Yong Wang
Jialei Ji
Xilin Hou
Yangyong Zhang
author_facet Li Chen
Wenjing Ren
Bin Zhang
Huiling Guo
Zhiyuan Fang
Limei Yang
Mu Zhuang
Honghao Lv
Yong Wang
Jialei Ji
Xilin Hou
Yangyong Zhang
author_sort Li Chen
collection DOAJ
description Ogura cytoplasmic male sterility (CMS) lines are widely used breeding materials in cruciferous crops and play important roles in heterosis utilization; however, the sterility mechanism remains unclear. To investigate the microspore development process and gene expression changes after the introduction of <i>orf138</i> and <i>Rfo</i>, cytological observation and transcriptome analysis were performed using a maintainer line, an Ogura CMS line, and a restorer line. Semithin sections of microspores at different developmental stages showed that the degradation of tapetal cells began at the tetrad stage in the Ogura CMS line, while it occurred at the bicellular microspore stage to the tricellular microspore stage in the maintainer and restorer lines. Therefore, early degradation of tapetal cells may be the cause of pollen abortion. Transcriptome analysis results showed that a total of 1287 DEGs had consistent expression trends in the maintainer line and restorer line, but were significantly up- or down-regulated in the Ogura CMS line, indicating that they may be closely related to pollen abortion. Functional annotation showed that the 1287 core DEGs included a large number of genes related to pollen development, oxidative phosphorylation, carbohydrate, lipid, and protein metabolism. In addition, further verification elucidated that down-regulated expression of genes related to energy metabolism led to decreased ATP content and excessive ROS accumulation in the anthers of Ogura CMS. Based on these results, we propose a transcriptome-mediated induction and regulatory network for cabbage Ogura CMS. Our research provides new insights into the mechanism of pollen abortion and fertility restoration in Ogura CMS.
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spelling doaj.art-c73f6f6d61544bfab0feb9b89cafdac42023-11-17T16:54:52ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-04-01247670310.3390/ijms24076703Comparative Transcriptome Analysis Reveals a Potential Regulatory Network for Ogura Cytoplasmic Male Sterility in Cabbage (<i>Brassica oleracea</i> L.)Li Chen0Wenjing Ren1Bin Zhang2Huiling Guo3Zhiyuan Fang4Limei Yang5Mu Zhuang6Honghao Lv7Yong Wang8Jialei Ji9Xilin Hou10Yangyong Zhang11State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural University, Nanjing 210095, ChinaState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural University, Nanjing 210095, ChinaState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural University, Nanjing 210095, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural University, Nanjing 210095, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaOgura cytoplasmic male sterility (CMS) lines are widely used breeding materials in cruciferous crops and play important roles in heterosis utilization; however, the sterility mechanism remains unclear. To investigate the microspore development process and gene expression changes after the introduction of <i>orf138</i> and <i>Rfo</i>, cytological observation and transcriptome analysis were performed using a maintainer line, an Ogura CMS line, and a restorer line. Semithin sections of microspores at different developmental stages showed that the degradation of tapetal cells began at the tetrad stage in the Ogura CMS line, while it occurred at the bicellular microspore stage to the tricellular microspore stage in the maintainer and restorer lines. Therefore, early degradation of tapetal cells may be the cause of pollen abortion. Transcriptome analysis results showed that a total of 1287 DEGs had consistent expression trends in the maintainer line and restorer line, but were significantly up- or down-regulated in the Ogura CMS line, indicating that they may be closely related to pollen abortion. Functional annotation showed that the 1287 core DEGs included a large number of genes related to pollen development, oxidative phosphorylation, carbohydrate, lipid, and protein metabolism. In addition, further verification elucidated that down-regulated expression of genes related to energy metabolism led to decreased ATP content and excessive ROS accumulation in the anthers of Ogura CMS. Based on these results, we propose a transcriptome-mediated induction and regulatory network for cabbage Ogura CMS. Our research provides new insights into the mechanism of pollen abortion and fertility restoration in Ogura CMS.https://www.mdpi.com/1422-0067/24/7/6703cabbageOgura CMSpollen developmentcomparative transcriptome analysis
spellingShingle Li Chen
Wenjing Ren
Bin Zhang
Huiling Guo
Zhiyuan Fang
Limei Yang
Mu Zhuang
Honghao Lv
Yong Wang
Jialei Ji
Xilin Hou
Yangyong Zhang
Comparative Transcriptome Analysis Reveals a Potential Regulatory Network for Ogura Cytoplasmic Male Sterility in Cabbage (<i>Brassica oleracea</i> L.)
International Journal of Molecular Sciences
cabbage
Ogura CMS
pollen development
comparative transcriptome analysis
title Comparative Transcriptome Analysis Reveals a Potential Regulatory Network for Ogura Cytoplasmic Male Sterility in Cabbage (<i>Brassica oleracea</i> L.)
title_full Comparative Transcriptome Analysis Reveals a Potential Regulatory Network for Ogura Cytoplasmic Male Sterility in Cabbage (<i>Brassica oleracea</i> L.)
title_fullStr Comparative Transcriptome Analysis Reveals a Potential Regulatory Network for Ogura Cytoplasmic Male Sterility in Cabbage (<i>Brassica oleracea</i> L.)
title_full_unstemmed Comparative Transcriptome Analysis Reveals a Potential Regulatory Network for Ogura Cytoplasmic Male Sterility in Cabbage (<i>Brassica oleracea</i> L.)
title_short Comparative Transcriptome Analysis Reveals a Potential Regulatory Network for Ogura Cytoplasmic Male Sterility in Cabbage (<i>Brassica oleracea</i> L.)
title_sort comparative transcriptome analysis reveals a potential regulatory network for ogura cytoplasmic male sterility in cabbage i brassica oleracea i l
topic cabbage
Ogura CMS
pollen development
comparative transcriptome analysis
url https://www.mdpi.com/1422-0067/24/7/6703
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