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Journal of Integrative Agriculture  2026, Vol. 25 Issue (2): 610-623    DOI: 10.1016/j.jia.2024.07.036
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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 Improvement/College 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, Chinese Academy of Agricultural Sciences, Anyang 455000, China

 Highlights 
Imbalanced lipid profiles in male sterile cotton anthers, featuring over-accumulation of free fatty acids (FFAs), phosphatidic acid (PA), mono-galactosyldiacylglycerol (MGDG), and di-galactosyldiacylglycerol (DGDG), alongside reduced triacylglycerol (TAG), disrupt normal pollen development.
alpha-Linolenic acid (C18:3) metabolism disruption is central to sterility, with excess MGDG/DGDG elevating jasmonic acid (JA) levels, which feedback-inhibits GhFAD3 and further reduces C18:3.
CRISPR/Cas9 knockout of GhFAD3 confirms its essential role in anther development, as mutants show no pollen, reduced TAG/C18:3, and male sterility.
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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 (DEGs) 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 jasmonic acid (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  
Received: 25 April 2024   Accepted: 13 June 2024 Online: 22 July 2024  
Fund: 
This work was supported by the Science and Technology Major Program of Bingtuan, China (2023AA008), the National Natural Science Foundation of China (31960369), the Bingtuan Science and Technology Program, China (2025DA001), 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, QianHao Zhu, Xinqi Cheng, Tao Zhang, Xinyu Zhang, Huaguo Zhu, Zuoren Yang, Jie Sun, Feng Liu. 2026. Unbalanced lipid metabolism in anther, especially the disorder of the alpha-linolenic acid metabolism pathway, leads to cotton male sterility. Journal of Integrative Agriculture, 25(2): 610-623.

Ali U, Lu S, Fadlalla T, Iqbal S, Yue H, Yang B, Hong Y, Wang X, Guo L. 2022. The functions of phospholipases and their hydrolysis products in plant growth, development and stress responses. Progress in Lipid Research86, 101158.

Bailey A P, Koster G, Guillermier C, Hirst E M, MacRae J I, Lechene C P, Postle A D, Gould A P. 2015. Antioxidant role for lipid droplets in a stem cell niche of drosophila. Cell163, 340–353.

Bates P D. 2016. Understanding the control of acyl flux through the lipid metabolic network of plant oil biosynthesis. Biochimica et Biophysica Acta1861, 1214–1225.

Bell E, Creelman R A, Mullet J E. 1995. A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in ArabidopsisProceedings of the National Academy of Sciences of the United States of America92, 8675–8679.

Benning C. 2009. Mechanisms of lipid transport involved in organelle biogenesis in plant cells. Annual Review of Cell and Developmental Biology25, 71–91.

Block M A, Dorne A J, Joyard J, Douce R. 1983. Preparation and characterization of membrane fractions enriched in outer and inner envelope membranes from spinach chloroplasts. I. Electrophoretic and immunochemical analyses. Journal of Biological Chemistry258, 13273–13280.

Browse J, Warwick N, Somerville C R, Slack C R. 1986. Fluxes through the prokaryotic and eukaryotic pathways of lipid synthesis in the ‘16:3’ plant Arabidopsis thalianaThe Biochemical Journal235, 25–31.

Caldelari D, Wang G, Farmer E E, Dong X. 2011. Arabidopsis lox3 lox4 double mutants are male sterile and defective in global proliferative arrest. Plant Molecular Biology75, 25–33.

Cheng X Q, Zhang X Y, Xue F, Zhu S H, Li Y J, Zhu Q H, Liu F, Sun J. 2020. Characterization and transcriptome analysis of a dominant genic male sterile cotton mutant. BMC Plant Biology20, 312.

Ding Y, Ma Y, Liu N, Xu J, Hu Q, Li Y, Wu Y, Xie S, Zhu L, Min L, Zhang X. 2017. microRNAs involved in auxin signalling modulate male sterility under high-temperature stress in cotton (Gossypium hirsutum). The Plant Journal91, 977–994.

Fan J, Yan C, Xu C. 2013. Phospholipid: Diacylglycerol acyltransferase-mediated triacylglycerol biosynthesis is crucial for protection against fatty acid-induced cell death in growing tissues of ArabidopsisThe Plant Journal76, 930–942.

Fu W, Shen Y, Hao J, Wu J, Ke L, Wu C, Huang K, Luo B, Xu M, Cheng X, Zhou X, Sun J, Xing C, Sun Y. 2015. Acyl-CoA N-acyltransferase influences fertility by regulating lipid metabolism and jasmonic acid biogenesis in cotton. Scientific Reports5, 11790.

Gao Y, Chen G, Weselake R J. 2014. A rapid nile red fluorescence-based method for triacylglycerol content in microspore-derived cell suspension cultures of Brassica napusLipids49, 1161–1168.

Han G S, Carman G M. 2010. Characterization of the human LPIN1-encoded phosphatidate phosphatase isoforms. The Journal of Biological Chemistry285, 14628–14638.

He M, Ding N Z. 2020. Plant unsaturated fatty acids: Multiple roles in stress response. Frontiers in Plant Science11, 562785.

Heinz E, Roughan P G. 1983. Similarities and differences in lipid metabolism of chloroplasts isolated from 18:3 and 16:3 plants. Plant Physiology72, 273–279.

Hyun Y, Choi S, Hwang H J, Yu J, Nam S J, Ko J, Park J Y, Seo Y S, Kim E Y, Ryu S B, Kim W T, Lee Y H, Kang H, Lee I. 2008. Cooperation and functional diversification of two closely related galactolipase genes for jasmonate biosynthesis. Developmental Cell14, 183–192.

Ishiguro S, Kawai-Oda A, Ueda J, Nishida I, Okada K. 2001. The DEFECTIVE IN ANTHER DEHISCIENCE1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in ArabidopsisThe Plant Cell, 13, 2191–2209.

Jiang P, Zhang X, Zhu Y, Zhu W, Xie H, Wang X. 2007. Metabolism of reactive oxygen species in cotton cytoplasmic male sterility and its restoration. Plant Cell Reports26, 1627–1634.

Khan A H, Min L, Ma Y, Wu Y, Ding Y, Li Y, Xie S, Ullah A, Shaban M, Manghwar H, Shahid M, Zhao Y, Wang C, Zhang X. 2020. High day and night temperatures distinctively disrupt fatty acid and jasmonic acid metabolism, inducing male sterility in cotton. Journal of Experimental Botany71, 6128–6141.

Kohlwein S D. 2010. Triacylglycerol homeostasis: Insights from yeast. The Journal of Biological Chemistry285, 15663–15667.

Lavell A A, Benning C. 2019. Cellular organization and regulation of plant glycerolipid metabolism. Plant Cell Physiology60, 1176–1183.

Li L O, Klett E L, Coleman R A. 2010. Acyl-CoA synthesis, lipid metabolism and lipotoxicity. Biochimica et Biophysica Acta1801, 246–251.

Li M, Hong Y, Wang X. 2009. Phospholipase D- and phosphatidic acid-mediated signaling in plants. Biochimica et Biophysica Acta1791, 927–935.

Li-Beisson Y, Shorrosh B, Beisson F, Andersson M X, Arondel V, Bates P D, Baud S, Bird D, Debono A, Durrett T P, Franke R B, Graham I A, Katayama K, Kelly A A, Larson T, Markham J E, Miquel M, Molina I, Nishida I, Rowland O, et al. 2013. Acyl-lipid metabolism. The Arabidopsis Book11, e0161.

Liu F, Ma L, Wang Y, Li Y, Zhang X, Xue F, Nie X, Zhu Q, Sun J. 2019. GhFAD2-3 is required for anther development in Gossypium hirsutumBMC Plant Biology19, 393.

Liu F, Zhao Y P, Zhu H G, Zhu Q H, Sun J. 2017. Simultaneous silencing of GhFAD2-1 and GhFATB enhances the quality of cottonseed oil with high oleic acid. Journal of Plant Physiology215, 132–139.

Lock Y Y, Snyder C L, Zhu W, Siloto R M, Weselake R J, Shah S. 2009. Antisense suppression of type 1 diacylglycerol acyltransferase adversely affects plant development in Brassica napusPhysiologia Plantarum137, 61–71.

Lohden I, Frentzen M. 1988. Role of plastidial acyl-acyl carrier protein: Glycerol 3-phosphate acyltransferase and acyl-acyl carrier protein hydrolase in channelling the acyl flux through the prokaryotic and eukaryotic pathway. Planta176, 506–512.

Ma H, Wu Y, Lv R, Chi H, Zhao Y, Li Y, Liu H, Ma Y, Zhu L, Guo X, Kong J, Wu J, Xing C, Zhang X, Min L. 2022. Cytochrome P450 mono-oxygenase CYP703A2 plays a central role in sporopollenin formation and ms5ms6 fertility in cotton. Journal of Integrative Plant Biology64, 2009–2025.

von Malek B, van der Graaff E, Schneitz K, Keller B. 2002. The Arabidopsis male-sterile mutant dde2-2 is defective in the ALLENE OXIDE SYNTHASE gene encoding one of the key enzymes of the jasmonic acid biosynthesis pathway. Planta216, 187–192.

Maraschin F, Kulcheski F R, Segatto A, Trenz T S, Barrientos-Diaz O, Margis-Pinheiro M, Margis R, Turchetto-Zolet A C. 2019. Enzymes of glycerol-3-phosphate pathway in triacylglycerol synthesis in plants: Function, biotechnological application and evolution. Progress in Lipid Research73, 46–64.

McConn M, Browse J. 1996. The critical requirement for linolenic acid is pollen development, not photosynthesis, in an Arabidopsis mutant. The Plant Cell8, 403–416.

Min L, Li Y, Hu Q, Zhu L, Gao W, Wu Y, Ding Y, Liu S, Yang X, Zhang X. 2014. Sugar and auxin signaling pathways respond to high-temperature stress during anther development as revealed by transcript profiling analysis in cotton. Plant Physiology164, 1293–1308.

Mittler R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science7, 405–410.

Ohlrogge J, Browse J. 1995. Lipid biosynthesis. The Plant Cell7, 957–970.

Park J H, Halitschke R, Kim H B, Baldwin I T, Feldmann K A, Feyereisen R. 2002. A knock-out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis. The Plant Journal31, 1–12.

Piffanelli P, Ross J H, Murphy D. 1998. Biogenesis and function of the lipidic structures of pollen grains. Sexual Plant Reproduction11, 65–80.

Pressman E, Shaked R, Shen S, Altahan L, Firon N. 2012. Variations in carbohydrate content and sucrose-metabolizing enzymes in tomato (Solanum lycopersicum L.) stamen parts during pollen maturation. American Journal of Plant Sciences3, 252–260.

Rong H, Yang W, Xie T, Wang Y, Wang X, Jiang J, Wang Y. 2022. Transcriptional profiling between yellow- and black-seeded Brassica napus reveals molecular modulations on flavonoid and fatty acid content. Journal of Integrative Agriculture21, 22112226.

Sawhney V K, Shukla S A. 1994. Male sterility in flowering plants: Are plant growth substances involved. American Journal of Botany81, 1640–1647.

Schilmiller A L, Koo A J, Howe G A. 2007. Functional diversification of acyl-coenzyme A oxidases in jasmonic acid biosynthesis and action. Plant Physiology143, 812–824.

Stenzel I, Hause B, Miersch O, Kurz T, Maucher H, Weichert H, Ziegler J, Feussner I, Wasternack C. 2003. Jasmonate biosynthesis and the allene oxide cyclase family of Arabidopsis thalianaPlant Molecular Biology51, 895–911.

Stintzi A, Browse J. 2000. The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proceedings of the National Academy of Sciences of the United States of America97, 10625–10630.

Taguchi R, Ishikawa M. 2010. Precise and global identification of phospholipid molecular species by an Orbitrap mass spectrometer and automated search engine lipid search. Journal of Chromatography A1217, 4229–4239.

Vance J E, Vance D E. 2004. Phospholipid biosynthesis in mammalian cells. Biochemistry and Cell Biology82, 113–128.

Wan X, Wu S, Li Z, An X, Tian Y. 2020. Lipid metabolism: Critical roles in male fertility and other aspects of reproductive development in plants. Molecular Plant13, 955–983.

Wasternack C, Hause B. 2013. Jasmonates: Biosynthesis, perception, signal transduction and action in plant stress response, growth and development. Annals of Botany111, 1021–1058.

Wasternack C, Song S. 2017. Jasmonates: Biosynthesis, metabolism, and signaling by proteins activating and repressing transcription. Journal of Experimental Botany68, 1303–1321.

Weber H. 2002. Fatty acid-derived signals in plants. Trends in Plant Science7, 217–224.

Wu Y, Li Y, Li Y, Ma Y, Zhao Y, Wang C, Chi H, Chen M, Ding Y, Guo X, Min L, Zhang X. 2019. Proteomic analysis reveals that sugar and fatty acid metabolisms play a central role in sterility of the male-sterile line 1355A of cotton. The Journal of Biological Chemistry294, 7057–7067.

Wu Y, Min L, Wu Z, Yang L, Zhu L, Yang X, Yuan D, Guo X, Zhang X. 2015. Defective pollen wall contributes to male sterility in the male sterile line 1355A of cotton. Scientific Reports5, 9608.

Xie H T, Wan Z Y, Li S, Zhang Y. 2014. Spatiotemporal production of reactive oxygen species by NADPH oxidase is critical for tapetal programmed cell death and pollen development in ArabidopsisThe Plant Cell26, 2007–2023.

Xu C, Fan J, Shanklin J. 2020. Metabolic and functional connections between cytoplasmic and chloroplast triacylglycerol storage. Progress in Lipid Research80, 101069.

Yang J. 2001. Hormonal changes in the grains of rice subjected to water stress during grain fifilling. Plant Physiology127, 315–323.

Yen C L, Stone S J, Koliwad S, Harris C, Farese Jr R V. 2008. Thematic review series: Glycerolipids. DGAT enzymes and triacylglycerol biosynthesis. Journal of Lipid Research49, 2283–2301.

Yu C W, Lin Y T, Li H M. 2020. Increased ratio of galactolipid MGDG: DGDG induces jasmonic acid overproduction and changes chloroplast shape. The New Phytologist228, 1327–1335.

Yurchenko O P, Park S, Ilut D C, Inmon J J, Millhollon J C, Liechty Z, Page J T, Jenks M A, Chapman K D, Udall J A, Gore M A, Dyer J M. 2014. Genome-wide analysis of the omega-3 fatty acid desaturase gene family in GossypiumBMC Plant Biology14, 312.

Zegarlińska J, Piaścik M, Sikorski A F, Czogalla A. 2018. Phosphatidic acid - A simple phospholipid with multiple faces. Acta Biochimica Polonica65, 163–171.

Zhang T, Hu Y, Jiang W, Fang L, Guan X, Chen J, Zhang J, Saski C A, Scheffler B E, Stelly D M, Hulse-Kemp A M, Wan Q, Liu B, Liu C, Wang S, Pan M, Wang Y, Wang D, Ye W, Chang L, et al. 2015. Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement. Nature Biotechnology33, 531–537.

Zhang Y, Zhu H, Zhang Q, Li M, Yan M, Wang R, Wang L, Welti R, Zhang W, Wang X. 2009. Phospholipase dalpha1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in ArabidopsisThe Plant Cell21, 2357–2377.

Zhu Y, Wang K, Wu C, Zhao Y, Yin X, Zhang B, Grierson D, Chen K, Xu C. 2019. Effect of ethylene on cell wall and lipid metabolism during alleviation of postharvest chilling injury in peach. Cells8, 1612.

Zhu Y, Yuan G, Jia S, An G, Li W, Sun D, Liu J. 2022. Transcriptomic profiling of watermelon (Citrullus lanatus) provides insights into male flowers development. Journal of Integrative Agriculture21, 407421.

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