Comparative transcriptome analyses shed light on carotenoid production and plastid development in melon fruit

Authors: CHAYUT, NOAM - Volcani Center (ARO); YUAN, HUI - Cornell University; SAAR, YUVAL - Volcani Center (ARO); ZHENG, YI - Boyce Thompson Institute; SUN, TIANHU - Cornell University; ZHOU, XUESONG - Cornell University; HERMANNS, ANNA - Cornell University; OREN, ELAD - Volcani Center (ARO); FAIGENBOIM, ADI - Volcani Center (ARO); HUI, MAIXIA - Cornell University; FEI, ZHANGJUN - Boyce Thompson Institute; MAZOUREK, MICHAEL - Cornell University; BURGER, JOSEPH - Volcani Center (ARO); TADMOR, YAAKOV - Volcani Center (ARO); Li, Li

Submitted to: Horticulture Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/26/2021
Publication Date: 5/1/2021
Citation: Chayut, N., Yuan, H., Saar, Y., Zheng, Y., Sun, T., Zhou, X., Hermanns, A., Oren, E., Faigenboim, A., Hui, M., Fei, Z., Mazourek, M., Burger, J., Tadmor, Y., Li, L. 2021. Comparative transcriptome analyses shed light on carotenoid production and plastid development in melon fruit. Horticulture Research. 8:112. https://doi.org/10.1038/s41438-021-00547-6.
DOI: https://doi.org/10.1038/s41438-021-00547-6

Interpretive Summary: Carotenoid production is important to give fruit colors, aromas, and nutrients. By comparative analysis of developing fruit whole genome transcripts of orange-fleshed melon with its two mutants in the same genetic background, we found that melon fruit gene expression is primarily altered by changes in carotenoid metabolic flux, but minimally by the ripe fruit carotenoid composition. In addition, we showed an association between fruit carotenoid metabolic flux with the maintenance of the photosynthetic apparatus in fruit chloroplasts. Moreover, based on the transcriptome analysis, we identified a new role of CmOR in interacting with chlorophyll a-b binding (LHCB) proteins to maintain chloroplast development. This study brings more insights into the cellular and metabolic processes associated with carotenoid accumulation in melon fruit and reveals a new maintenance mechanism of the photosynthetic apparatus in chloroplasts.

Technical Abstract: Carotenoids, such as ß-carotene, accumulate in chromoplasts of various fleshy fruits, awarding them with colors, aromas, and nutrients. The Orange (CmOr) gene controls ß-carotene accumulation in melon fruit by posttranscriptionally enhancing carotenogenesis and repressing ß-carotene turnover in chromoplasts. Carotenoid isomerase (CRTISO) isomerizes yellow pro-lycopene into red lycopene, a prerequisite for further metabolism into ß-carotene. We comparatively analyzed the developing fruit transcriptomes of orange-colored melon and its two isogenic EMS-induced mutants, low-ß (Cmor) and yofi (Cmcrtiso). The Cmor mutation in low-ß caused a major transcriptomic change in the mature fruit. In contrast, the Cmcrtiso mutation in yofi significantly changed the transcriptome only in early fruit developmental stages. These findings indicate that melon fruit transcriptome is primarily altered by changes in carotenoid metabolic flux and plastid conversion, but minimally by carotenoid composition in the ripe fruit. Clustering of the differentially expressed genes into functional groups revealed an association between fruit carotenoid metabolic flux with the maintenance of the photosynthetic apparatus in fruit chloroplasts. Moreover, large numbers of thylakoid localized photosynthetic genes were differentially expressed in low-ß. CmOR family proteins were found to physically interact with light-harvesting chlorophyll a-b binding proteins, suggesting a new role of CmOR for chloroplast maintenance in melon fruit. This study brings more insights into the cellular and metabolic processes associated with fruit carotenoid accumulation in melon fruit and reveals a new maintenance mechanism of the photosynthetic apparatus for plastid development.