Multiomics analyses reveal high temperature-induced molecular regulation of ascorbic acid and capsaicin biosynthesis in pepper fruits

Heat stress (HS) is one of the most severe abiotic stressors that affects pepper fruit development, coloration, nutritional quality and yield. However, the molecular basis of pepper fruit response to HS has not been extensively studied. In this study, we performed integrated transcriptomic, proteomic and metabolomic analyses in pepper fruits subjected to HS (36 ℃) for 6 h, 12 h and 24 h. A total of 14513 differentially expressed genes (DEGs), 1999 differentially abundant proteins (DAPs), and 39 differentially accumulated metabolites (DAMs) were identified in response to heat treatments. Molecular function, regulatory network, and metabolic pathway analyses revealed that the DEGs and DAPs in heat-stressed fruits were mainly attributed to photosynthesis, response to stimulus, carbohydrate metabolic process, and protein folding process. Interestingly, among the DAMs, the content of capsaicin and ascorbic acid (Vitamin C), which are important phytochemical substances of pepper as food, was substantially impaired by HS. By integrated analysis of the genes, proteins and intermediate metabolites related to the biosynthesis pathway of capsaicin and ascorbic acid, we found that transcripts of most of the capsaicin biosynthesis genes are positively correlated to capsaicin content, while there is no obvious correlation between the biosynthesis genes and the content of ascorbic acid. Furthermore, by analyzing the promoter sequence, we found 3 transcription factors that could potentially regulate the expression of key genes in the capsaicin biosynthesis pathway in response to HS. Our research here provides a better understanding of the molecular mechanism of pepper fruit response to HS, and also provides a theoretical basis for the pre-harvest temperature management to harvest high-quality pepper fruits.