Multiomics analysis reveals the biochemical and genetic bases of Coffea arabica L. fruit color

Coffee is a remarkable source of bioactive compounds, including anthocyanins, proanthocyanidins, and carotenoids, with health benefits. To fully understand the biochemical and molecular regulation mechanisms behind Coffea arabica L. pigmentation, transcriptome profiling and metabolite quantitation were conducted on three varieties with significant color differences. A total of 40 anthocyanins, six proanthocyanidins, and 34 carotenoids were accumulated in three C. arabica fruits. The up-regulation and accumulation of most flavonoids, including anthocyanidin compounds, and the down-regulation and accumulation of proanthocyanidins were important factors in the purple pigmentation of C. arabica fruits, while the down-regulation and accumulation of anthocyanins and the up-regulation and accumulation of proanthocyanidins were important factors affecting the yellow pigmentation of C. arabica fruits. Cyanidins were major contributors to redness in the anthocyanins of C. arabica fruits, especially the cyanidin-3-O-glucoside compound. The accumulation of anthocyanin metabolites was the main factor affecting the purple pigmentation of C. arabica fruits, followed by the high proportion of cyanidin metabolites and the unique metabolites of petunidan. The accumulation of proanthocyanidins contributed to the yellow and pink pigmentation of C. arabica fruits, with Procyanidin B2 and Procyanidin C1 metabolites contributing specifically to yellow pigmentation. Lutein and lutein myristate were major contributors to carotenoids of C. arabica fruits, and lycopene and Zeaxanthin-laurate-myristate contributed to the red pigmentation of C. arabica fruits. CaCHSs, CaCHIs, Ca4CLs, and CaF3Hs could help enhance the synthesis of important compounds, including chalcone, naringenin, and dihydroflavonol, in the upstream pathway of anthocyanin synthesis. CaF3′Hs significantly promoted metabolic influx into cyanidin- and peonidin-related biosynthesis. CaANSs and CaDFRs were responsible for anthocyanin deposition in C. arabica fruits. CaPSYs, CaPDSs, CaZ-ISO, and CaZDS2 were important for the formation of lycopene in C. arabica fruits. The key structural gene expression of CaPSYs, CaPDSs, CaZ-ISO, CaZDS2, CaCHYE3, CaCHYE5, CaZEP9, and CaCRTISOs in C. arabica fruits contributed to carotenoid biosynthesis. This study provides a robust biochemical analysis, revealing target genes of C. arabica fruit pigment deposition, which have important implications for improving the nutritional quality of C. arabica fruits via molecular breeding.