Unbalanced lipid metabolism in anther, especially the disorder of the alpha-linolenic acid metabolism pathway, leads to cotton male sterility

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.