Co-chaperoning of chlorophyll and carotenoid biosynthesis by orange family proteins in plant

Authors: SUN, TIAN - Cornell University; WANG, PENG - Humboldt University; LU, SHAN - Nanjing University; YUAN, HUI - Cornell University; Yang, Yong; Fish, Tara; Thannhauser, Theodore - Ted; Liu, Jiping; MAZOUREK, MICHAEL - Cornell University; GRIMM, BERNHARD - Humboldt University; Li, Li

Submitted to: Molecular Plant
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/15/2023
Publication Date: 5/18/2023
Citation: Sun, T., Wang, P., Lu, S., Yuan, H., Yang, Y., Fish, T., Thannhauser, T.W., Liu, J., Mazourek, M., Grimm, B., Li, L. 2023. Co-chaperoning of chlorophyll and carotenoid biosynthesis by orange family proteins in plant. Molecular Plant. 16:1048-1065. https://doi.org/10.1016/j.molp.2023.05.006.
DOI: https://doi.org/10.1016/j.molp.2023.05.006

Interpretive Summary: Plants must coordinately regulate chlorophyll and carotenoid pigment biosynthesis to efficiently and precisely adjust photosynthesis and plant fitness in response to various cues. However, little is known about the molecular mechanisms underlying this highly coordinated process. The common regulators that orchestrate chlorophyll and carotenoid biosynthesis, particularly at posttranslational level to allow rapid regulation of these two pathways, are unknown. In this study, we report the discovery of the evolutionarily conserved OR family proteins as the common regulators of both chlorophyll and carotenoid biosynthesis. We show that OR proteins regulate the first committed enzyme in each pathway to safeguard photosynthetic pigment biosynthesis and enhance plant thermotolerance under heat stress. This study establishes a novel conserved mechanism of green plant to coordinate photosynthetic pigment biosynthesis and provides a potential genetic target to generate climate-resilient crops.

Technical Abstract: Chlorophyll and carotenoid are essential photosynthetic pigments. Plants must spatiotemporally coordinate the needs of chlorophyll and carotenoid for optimal photosynthesis and plant fitness in response to diverse environmental and developmental cues. However, how these two biosynthesis pathways are orchestrated remains largely unknown. Here, we report that the highly conserved ORANGE (OR) family proteins are the common regulators of both pathways via posttranslationally regulating the first committed enzyme in each pathway. We demonstrate that OR family proteins physically interact with magnesium chelatase subunit I (CHLI) in addition to phytoene synthase (PSY) and concurrently regulate CHLI and PSY protein stability and activity. We show that loss of OR genes hinders both chlorophyll and carotenoid biosynthesis, limits light-harvesting complex assembly, and impairs thylakoid grana stacking in chloroplast. OR overexpression safeguards photosynthetic pigment biosynthesis and enhances thermotolerance in both Arabidopsis and tomato plants. Our findings establish a conserved mechanism of green plant to coordinate chlorophyll and carotenoid biosynthesis and provide a potential genetic target to generate climate-resilient crops.