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Unbalanced lipid metabolism in anther, especially the disorder of the alpha-linolenic acid metabolism pathway, leads to cotton male sterility
Lihong Ma1, Pengtao Wang2, Qian-Hao Zhu3, Xinqi Cheng4, Tao Zhang1, Xinyu Zhang1, Huaguo Zhu4, Zuoren Yang5, Jie Sun1#, Feng Liu1#

1 Key Laboratory of Oasis Eco-agriculture, College of Agriculture, Shihezi University, Shihezi 832000, China

2 State Key Laboratory of Crop Stress Adaptation and ImprovementCollege of Life Sciences, Henan University, Kaifeng 475000, China

3 CSIRO Agriculture and Food, GPO Box 1700, Canberra 2601, Australia

4 College of Biology and Agricultural Resources, Huanggang Normal University, Huanggang 438000, China

5 State Key Laboratory of Cotton Biology, Institute of Cotton Research of Chinese Academy of Agricultural Sciences, Anyang 455000, China

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摘要  

最近的研究表明,植物脂质代谢是影响花药发育和雄性育性的关键因素。然而,植物是如何调节多种脂质的代谢平衡以确保花药正常发育和雄性育性仍不清楚。分析与花药育性相关的脂质分子及其生物途径合成的关键基因对于理解脂质代谢在作物育性中的生理学意义至关重要。在本研究中,我们比较分析了两种陆地棉(Gossypium hirsutum)材料石大98WT)及其近等基因雄性不育系石大98AMS)花药的转录组及花药脂质的组成和含量。转录组学分析鉴定了两种材料之间的许多差异表达基因,而其中α-亚麻酸代谢途径的基因与雄性不育表型显著相关。脂质代谢研究表明,MS花药中游离脂肪酸(FFAs)、磷脂酸(PA)、单半乳糖和双半乳糖二酰基甘油(MGDGDGDG)过量积累,以及三酰基甘油(TAG)含量的显著降低等,与花药中α -亚麻酸(C18:3)代谢的异常密切相关。在花药脂质PAMGDGDGDGTAG中,含有C18:3-酰基链的脂质分子可能在棉花花药发育中发挥重要作用。结果还表明,过量的MGDGDGDG会导致茉莉酸在MS花药中过度积累,并可能是通过反馈调节机制进而抑制GhFAD3的表达,进一步降低C18:3的含量,最终影响花药的育性。总之,我们的研究结果揭示了平衡的脂质代谢在调节棉花花药发育以及雄性育性方面的重要性。



Abstract  

Recent studies have shown that lipid metabolism is a key factor affecting anther development and male fertility. However, how plants regulating the metabolic balance of multiple lipids to ensure proper anther development and male fertility remains unclear. Analyzing lipid molecules related to anther fertility and genes responsible for their biosynthesis is crucial for understanding the physiological significance of lipid metabolism in crop fertility. In this study, we compared the transcriptome and the composition and content of lipids in anthers of two Upland cotton (Gossypium hirsutum) materials, Shida 98 (WT) and its nearly-isogenic male sterile line Shida 98A (MS). Transcriptomics analysis identified many differentially expressed genes between the two materials, with the genes of the alpha-linolenic acid metabolism pathway being the most significantly associated with the male sterility phenotype. Investigations on lipids revealed that the MS anthers over-accumulated free fatty acids (FFAs), phosphatidic acid (PA), mono- and di-galactosyldiacylglycerol (MGDG and DGDG), and had a decreased content of triacylglycerol (TAG), which was closely related to the abnormal metabolism of alpha-linolenic acid (C18:3); therefore, the major lipids containing C18:3-acyl chains, such as PA, MGDG, DGDG and TAG, are proposed to play a major role in cotton anther development. We also showed that an excessive level of MGDG and DGDG caused JA overaccumulation in MS anthers, which in turn inhibited the expression of GhFAD3 and consequently reduced the C18:3 content, presumably via a feedback regulation mechanism, ultimately affecting plant fertility. Together, our results revealed the importance of a balanced lipid metabolism in regulating the development of cotton anther and pollen and consequently male fertility.

Keywords:  cotton       anther              male sterility              lipid metabolism              alpha-linolenic acid  
Online: 22 July 2024  
Fund: 
This work was supported by the National Biotechnology Breeding Program of China (2023ZD04039-3), the Natural Science Foundation of China (31960369), the Science and Technology Major Program of BINGTUAN (2023AA008), BTNYGG (NYHXGG, 2023AA102) and the Henan Provincial Science and Technology Research Project, China (222102110200).
About author:  #Correspondence Jie Sun, E-mail: sunjie@shzu.edu.cn; Feng Liu, E-mail: liufeng@shzu.edu.cn

Cite this article: 

Lihong Ma, Pengtao Wang, Qian-Hao Zhu, Xinqi Cheng, Tao Zhang, Xinyu Zhang, Huaguo Zhu, Zuoren Yang, Jie Sun, Feng Liu. 2024. Unbalanced lipid metabolism in anther, especially the disorder of the alpha-linolenic acid metabolism pathway, leads to cotton male sterility. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2024.07.036

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