Journal of Integrative Agriculture ›› 2025, Vol. 24 ›› Issue (3): 1092-1107.DOI: 10.1016/j.jia.2024.07.046

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有丝分裂花粉发育异常与大白菜Ogura细胞质雄性不育相关

  

  • 收稿日期:2023-10-30 接受日期:2024-07-08 出版日期:2025-03-20 发布日期:2025-02-28

Mitotic pollen abnormalities are linked to Ogura cytoplasmic male sterility in Chinese cabbage (Brassica rapa L. ssp. pekinensis)

Xiaochun Wei1, 2*, Yuanlin Zhang1, 2*, Yanyan Zhao1, Weiwei Chen2, Ujjal Kumar Nath3, Shuangjuan Yang1, Henan Su1, Zhiyong Wang1, Wenjing Zhang1, Baoming Tian2, Fang Wei1, 2#, Yuxiang Yuan1#, Xiaowei Zhang1, 2#   

  1. 1 Institute of Vegetables, Henan Academy of Agricultural Sciences, Zhengzhou 450002, China

    2 School of Agricultural Sciences, Zhengzhou University, Zhengzhou 450001, China

    3 Department of Genetics and Plant Breeding, Bangladesh Agricultural University, Mymensingh 2202, Bangladesh

  • Received:2023-10-30 Accepted:2024-07-08 Online:2025-03-20 Published:2025-02-28
  • About author:#Correspondence Fang Wei, E-mail: fangwei@zzu.edu.cn; Yuxiang Yuan, E-mail: yuxiangyuan126@126.com; Xiaowei Zhang, E-mail: xiaowei5737@163.com *These authors contributed equally to this study.
  • Supported by:
    This work was supported by the China Agricultural Research System (CARS-23-G15), the Innovation Team of Henan Academy of Agricultural Sciences, China (2024TD06), the Autonomous Innovation Project of Henan Academy of Agricultural Sciences, China (2024ZC034), the Joint Research on Agricultural Variety Improvement of Henan Province, China (2022010504), and the Key Research & Development Project of Henan Province, China (221111110100).

摘要:

Ogura细胞质雄性不育(Ogura CMS)最初在野生萝卜中被鉴定,其特征为花粉完全败育。但Ogura CMS在大白菜中的分子机制尚不清楚。细胞学分析证实,细胞核降解发生在花粉发育的单核后期,在三核期几乎消失,而绒毡层细胞从四分体时期开始异常增大并出现空泡化。花粉壁存在严重的发育缺陷。在花粉发育早期,与细胞色素c和程序性细胞死亡(PCD)相关的基因在Ogura CMS系中上调表达。相反,与花粉壁有丝分裂相关的基因表达下调。在花粉发育后期,Ogura CMS系中过氧化物酶体和自噬相关基因上调表达。线粒体orf138基因突变刺激绒毡层细胞PCD过程,导致其内容物异常增大和降解,直至三核期绒毡层细胞空泡化。由于绒毡层缺陷,其不能为小孢子提供足够的孢粉素和营养物质,从而导致花粉壁发育异常和小孢子有丝分裂异常。综上所述,核弥散与自噬发生在花粉发育后期导致大白菜Ogura CMS系不能产生功能性花粉,表现出雄性不育。

Abstract:

Ogura cytoplasmic male sterility (Ogura CMS) was first identified in wild radish (Raphanus sativus) and resulted in complete pollen abortion.  However, the molecular mechanism of Ogura CMS in Chinese cabbage remains unclear.  A cytological analysis confirmed nuclear degradation during the late uninucleate stage of pollen development, which diminished by the tricellular stage.  Concurrently, tapetal cells exhibited abnormal enlargement and vacuolation starting from the tetrad stage.  Serious developmental defects were observed in the pollen wall.  During early pollen development, genes associated with cytochrome c and programmed cell death (PCD) were upregulated in the Ogura CMS line, while genes involved in pollen wall mitosis were downregulated.  Conversely, at the late stage of pollen development, peroxisome and autophagy-related genes in the Ogura CMS line were upregulated.  The mitochondrial orf138 gene mutation triggered the PCD process in tapetal cells, leading to their abnormal enlargement and the degradation of their contents, eventually resulting in vacuolation at the tricellular stage.  These tapetal defects hindered the provision of adequate sporopollenin and nutrients to the microspores, consequently leading to abnormal pollen wall development and abnormal mitosis in the microspores.  Ultimately, nuclear dispersion commenced during the late uninucleate stage, and autophagy occurred in the late stage of pollen development.  Consequently, the plant could not produce functional pollen, resulting in male sterility in Chinese cabbage.  Studies of Ogura CMS can promote the production and application of male sterile materials and enrich male sterile resources, which is of great significance for hybrid breeding.


Key words: Ogura CMS , Chinese cabbage ,  cytology ,  transcriptome ,  PCD ,  pollen abortion