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Journal of Integrative Agriculture  2025, Vol. 24 Issue (6): 2080-2095    DOI: 10.1016/j.jia.2024.03.009
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ORF138 causes abnormal lipid metabolism in the tapetum that leads to Ogu cytoplasmic male sterility in Brassica napus
Xiaoyu Ge, Junlin Chen, Ouqi Li, Min Zou, Baolong Tao, Lun Zhao, Jing Wen, Bin Yi, Jinxing Tu, Jinxiong Shen#
National Key Laboratory of Crop Genetic Improvement/Wuhan Research Branch, National Rapeseed Genetic Improvement Center/College of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, China
 Highlights 
Confirmed orf138 as the causal gene for Ogu cytoplasmic male sterility through genetic transformation.
Differentially expressed genes (DEGs) in aborted anthers are mainly enriched in glycerophospholipid pathways, with lipid metabolism genes like BnaGPAT1 down-regulated in the sterile line.
Abnormal lipid metabolism cause reactive oxygen species accumulation in an oxidative stress response, leading to microspore abortion.
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摘要  
植物细胞质雄性不育由线粒体基因重排和突变产生,是杂种优势利用以提升产量的重要途径。Ogu CMS是天然的细胞质雄性不育类型,目前已经成功被转育到油菜以及十字花科的蔬菜中应用。但是对其败育的分子机理的了解仍不够深入。本研究中,我们通过拟南芥中的遗传转化实验证实orf138是Ogu CMS的不育基因。花药的转录组分析结果表明差异基因主要集中在甘油磷脂代谢、精氨酸和脯氨酸代谢等通路上。进一步研究发现,脂质代谢通路上的关键基因如定位在绒毡层线粒体和内质网上的BnaGPAT1等在四分体形成时特异性下调表达,可能导致酰基甘油等物质代谢变化,引起绒毡层脂质代谢紊乱。这一结果与透射电镜中观察到的绒毡层和小孢子细胞形态和亚细胞结构变化相一致。脂质代谢异常导致花药中ROS特异性积累可能会进一步加剧氧化应激反应最终可以导致小孢子发育异常。基于转录水平上的研究加深了对Ogu CMS的分子机理的认识。


Abstract  

Mutations and rearrangements of mitochondrial genes cause plant cytoplasmic male sterility.   It is a significant way to utilize hybrid vigor to enhance crop yield.  Ogu cytoplasmic male sterility (CMS) is a natural cytoplasmic male sterility type discovered in radishes, being successfully transferred to rapeseed and cruciferous vegetables.  However, current studies lack depth in exploring the molecular mechanisms of its male sterility.  This study confirmed that orf138 is the causal gene for Ogu CMS through the genetic transformation in Arabidopsis.  Transcriptome analysis of aborted anthers in different stages suggested that differentially expressed genes (DEGs) are mainly enriched in pathways such as glycerophospholipid metabolism and arginine and proline metabolism.  It reveals that key genes involved in lipid metabolism pathways are significantly down-regulated in the sterile line (OguA), including BnaGPAT1, localized within the tapetum mitochondrial and endoplasmic reticulum.  This could lead to changes in the metabolism of substances like acylglycerols within the tapetum, causing disruptions in lipid metabolism.  This is consistent with morphological and subcellular structural changes in the tapetum and microspore cells, as observed in the transmission electron microscopy.  This abnormal lipid metabolism may trigger specific reactive oxygen species (ROS) accumulation in an oxidative stress response, ultimately leading to an aborted microspore.  Our study based on transcriptome has deepened our understanding of the molecular mechanisms in Ogu CMS.

Keywords:  orf138       cytoplasmic male sterility       mitochondria       tapetum       ROS  
Received: 18 October 2023   Online: 02 March 2024   Accepted: 23 January 2024
Fund: 
This project was supported by the National Natural Science Foundation of China (31930032).
About author:  Xiaoyu Ge, E-mail: 781082978@qq.com; #Correspondence Jinxiong Shen, Tel: +86-27-87281507, E-mail: jxshen@mail.hzau.edu.cn

Cite this article: 

Xiaoyu Ge, Junlin Chen, Ouqi Li, Min Zou, Baolong Tao, Lun Zhao, Jing Wen, Bin Yi, Jinxing Tu, Jinxiong Shen. 2025. ORF138 causes abnormal lipid metabolism in the tapetum that leads to Ogu cytoplasmic male sterility in Brassica napus. Journal of Integrative Agriculture, 24(6): 2080-2095.

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