Jasmonic acid-mediated starch degradation regulates male fertility in cucumber.

Abstract

Cucumbers (Cucumis sativus L.) are typically monoecious, with both male and female flowers developing on the same plant. Successful fertilization relies on the synchronized release of pollen from the anthers of male flowers and its subsequent germination on the stigma of female flowers. However, the coordinated regulatory mechanisms underlying these processes remain largely unknown. Here, we show that treatment with the JA biosynthesis inhibitor dihydrocoumarin significantly suppresses both anther dehiscence and pollen germination, indicating that JA signaling may regulate male fertility in cucumber. Loss-of-function mutations in the JA receptor COI1 or the JA-signaling transcription factors MYC2a/MYC2b completely abolish anther dehiscence, resulting in complete male sterility. Mechanistic analyses reveal that MYC2a and MYC2b directly bind to the promoters of multiple amylases, including BAM1, BAM5, and AMY3, and activate their transcription. Consistently, loss-of-function alleles of BAM1, BAM5, and AMY3 severely compromise anther dehiscence. Starch degradation in the anther produces substantial quantities of soluble sugars, which are actively transported out from anther; the osmotic potential triggers water outflow from anther, ultimately resulting in anther dehydration and precise dehiscence, as well as pollen release. Collectively, these results demonstrate that JA-mediated starch catabolism serves as a dual-functional regulatory hub: it supplies both the osmotic driving force for anther dehiscence and the metabolic substrates essential for early pollen development. This pathway thus coordinately governs male fertility in cucumber. Our findings identify COI1, MYC2a/MYC2b, and the amylases BAM1, BAM5, and AMY3 as high-priority genetic targets for engineering male sterility and optimizing hybrid seed production in Cucurbitaceae crops.