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Journal of Integrative Agriculture
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The mitochondrial genes orf113b and orf146 from Xinjiang wild rapeseed cause pollen abortion in alloplasmic male sterility

Man Xing1, 2, Bo Hong1, 2, Chunyun Guan1, 2, 3, Mei Guan1, 2, 3#

1 College of Agronomy, Hunan Agricultural University, Changsha 410128, China

2 Hunan Branch of National Oilseed Crops Improvement Center, Changsha 410128, China

3 Southern Regional Collaborative Innovation Center for Grain and Oil Crops in China, Changsha 410128, China

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摘要  

利用远缘杂交技术,以新疆野生油菜(野芥,Sinapis arvensis)为母本,以甘蓝型油菜湘油15号(XY15Brassica napus L.)为父本,从杂交后代中选育出具有新疆野生油菜的细胞质雄性不育油菜Nsa CMS。其不育的因素及其潜在机制尚不清楚。本研究首次成功组装并分析了1258A (Nsa CMS)的线粒体基因组。该线粒体基因组全长263,010 bp,包含91个基因,包括33个蛋白质编码基因和36orf。一个新的线粒体基因orf113b和一个突变的、截断的基因orf146可能与1258A中观察到的雄性不育有关。ORF113bORF146抑制细胞生长,影响线粒体氧化磷酸化途径中与复合物IIIIV相关的基因表达,并触发活性氧ROS爆发。此外,转录组数据分析揭示了与orf113borf146共表达的关键核基因,表明它们的异常表达可能受到线粒体逆行信号的影响。该信号可导致绒毡层非典型程序性细胞死亡(PCD),导致花粉不育。总之,本研究不仅首次鉴定了远缘杂交而来的Nsa CMS线粒体基因组,明确orf113borf146对花粉不育至关重要。线粒体基因诱发的ROS可能是导致调控花粉发育关键核基因异常表达的主要触发因素,为探究Nsa CMS花粉败育的分子机制提供了新的思路。



Abstract  

Nsa CMS, a type of cytoplasmic male sterility (CMS) in rapeseed, originates from the cross between Xinjiang wild rapeseed (Sinapis arvensis) and Xiangyou 15 (Brassica napus L.).  Although this CMS variant shows promising applications, the factors contributing to its sterility and their underlying mechanisms remain unclear.  To the best of our knowledge, we successfully assembled and analyzed the mitochondrial genome of 1258A (Nsa CMS) for the first time.  This mitochondrial genome, spanning 263,010 bp, contains 91 genes, including 33 protein-coding and 36 orf genes.  Our analysis identified a novel mitochondrial gene, orf113b, and a mutated, truncated gene, orf146, both likely linked to the sterility observed in 1258A.  ORF113b and ORF146 were found to impede cell growth, disrupt gene expression associated with complexes I, III, and V of the mitochondrial oxidative phosphorylation pathway, and trigger reactive oxygen species (ROS) production.  Additionally, transcriptome data analysis revealed key nuclear genes co-expressed with orf113b and orf146, suggesting that their aberrant expression may be influenced by retrograde signaling from the mitochondria.  This signaling could lead to atypical programmed cell death (PCD) in the tapetum layer, resulting in pollen sterility.  In conclusion, our study not only provides the first characterization of the Nsa CMS mitochondrial genome but also identifies orf113b and orf146 as crucial to pollen sterility.  Furthermore, it suggests that ROS induced by these mitochondrial genes may play a central role in the abnormal regulation of nuclear genes essential for pollen development, offering new insights into the molecular mechanisms underlying Nsa CMS. 

Keywords:  Brassica napus L.       cytoplasmic male sterility        orf113b        orf146        ROS  
Received: 09 June 2024   Online: 24 September 2024  
Fund: 

This work was supported by the China Agriculture Research System of MOF and MARA (CARS-13), the National High Technology Research and Development Program of China (863 Program: 2011AA10A104) and the National Natural Science Foundation of China (3240150455).

About author:  Man Xing, E-mail: xingman18971@outlook.com; #Correspondence Mei Guan, E-mail: guanmei@hunau.edu.cn

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Man Xing, Bo Hong, Chunyun Guan, Mei Guan. 2024. The mitochondrial genes orf113b and orf146 from Xinjiang wild rapeseed cause pollen abortion in alloplasmic male sterility. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2024.09.018

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