Nitric oxide enhances SlSPL10-mediated transcriptional repression of carotenoid synthesis genes to delay tomato fruit carotenoid accumulation.

Nitric oxide (NO) inhibits climacteric fruit ripening, but its mechanisms remain elusive. Here, S-nitrosoglutathione (GSNO, a NO donor) reduces carotenoid accumulation in tomato fruit, confirming NO's role as carotenoid biosynthesis suppressor. Transcriptome analysis identified SlSPL10 (SQUAMOSA promoter binding protein-like 10) as a key player during this process. Genetic evidence further revealed that SlSPL10 negatively regulates carotenoid synthesis. Moreover, GSNO fails to suppress carotenoid synthesis in slspl10 mutant fruit, in contrast to wild-type fruit, highlighting the involvement of SlSPL10 in NO-inhibited carotenoid synthesis. Transcriptomic profiling of slspl10 mutant fruit showed that both NO and SlSPL10 regulate key carotenoid synthesis genes (SlGPS, SlPDS, SlZDS, SlZISO, and SlCRTISO). SlSPL10 directly binds to the promoters of these genes to repress their transcription, and NO enhances the transcriptional inhibition of SlGPS, SlZISO, and SlCRTISO. These three genes are indispensable for SlSPL10's role in NO-mediated carotenoid suppression. Collectively, NO enhances SlSPL10-mediated repression of carotenoid biosynthesis gene expression, reducing carotenoid accumulation in tomato fruit.