Orchestration of Chlorophyll and Carotenoid Biosynthesis by ORANGE Family Proteins in Plant

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.