Carotenoid sequestration protein fibrillin participates in CmOr-regulated B-carotene accumulation in melon

Authors: ZHOU, XUESONG - Cornell University; SUN, TIANHU - Cornell University; OWENS, LAUREN - Cornell University; Yang, Yong; Fish, Tara; LIU, ANDY - Cornell University; WRIGHTSTONE, EMALEE - Cornell University; YUAN, HUI - Cornell University; CHAYUT, NOAM - Newe Ya'Ar Research Center; BURGER, JOSEPH - Newe Ya'Ar Research Center; TADMOR, YAAKOV - Newe Ya'Ar Research Center; Thannhauser, Theodore - Ted; GUO, WANGZHEN - Nanjing Agricultural University; CHENG, LAILIANG - Cornell University; Li, Li

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/5/2023
Publication Date: 5/26/2023
Citation: Zhou, X., Sun, T., Owens, L., Yang, Y., Fish, T., Liu, A., Wrightstone, E., Yuan, H., Chayut, N., Burger, J., Tadmor, Y., Thannhauser, T.W., Guo, W., Cheng, L., Li, L. 2023. Carotenoid sequestration protein fibrillin participates in CmOr-regulated B-carotene accumulation in melon. Plant Physiology. 193:643-660. https://doi.org/10.1093/plphys/kiad312.
DOI: https://doi.org/10.1093/plphys/kiad312

Interpretive Summary: Carotenoids are essential to plants and crucial in human diets. Melon is an economically important crop, consumed globally. Orange flesh melon fruit is due to beta-carotene accumulation in chromoplasts, the site for carotenoid accumulation, induced by CmOr gene. However, the mechanism of the CmOr-induced chromoplast formation is unknown and the proteins associated with carotenoid accumulation in melon chromoplasts are not yet identified. Through proteomic analysis, we identified CmFBN1 as a potential protein involved. We showed that CmFBN1 physically associates with CmOR in a substructure of chromoplasts to enhance the OR-triggered chromoplast development and carotenoid accumulation.

Technical Abstract: Chromoplasts are organelles with unique ability to sequester and store carotenoids in pigment lipoprotein substructures, leading to carotenoid hyperproduction in many horticultural crops. In melon (Cucumismelo) fruit, ß-carotene accumulation in chromoplasts is governed by CmOr, the only known bona fide molecular switch for chromoplast formation. However, how CmOr regulates chromoplast development for carotenoid accumulation is not well understood. Quantitative proteome profiling of a high ß-carotene melon variety and its isogenic line low-ß mutant with impaired chromoplast formation revealed 309 proteins with different abundances. A fibrillin protein (CmFBN1) with a significant low level in the ripen fruit of low-ß was identified, which was investigated by protein-protein interaction, transgenic study, microscopic analysis, and subplastidial fractionation to analyze its impact on carotenoid sequestration and accumulation in melon fruit. CmFBN1 expresses highly in melon fruit tissue. Both in vitro and in vivo evidence showed that CmFBN1 physically interacts with CmOR and such interaction occurs in plastoglobules of plastids. Overexpression of CmFBN1 in a genetic background mimicking CmOr significantly enhances carotenoid accumulation, demonstrating its involvement in the CmOr-induced carotenoid accumulation. Noticeably, CmOR protein greatly stabilizes CmFBN1, which stimulates plastoglobule proliferation and enhances OR-triggered carotenoid accumulation in chromoplasts. Our findings suggest a fundamental role of CmFBN1 in facilitating plastoglobule proliferation in chromoplasts for carotenoid sequestration in orange melon fruit and reveal a genetic tool to further enhance the Or-induced carotenoid accumulation in crops.