The BCM1-EGY1 module balances chlorophyll biosynthesis and breakdown to confer chlorophyll homeostasis in land plants

Chlorophyll metabolism has evolved during plant evolution. The strictly light-dependent nature of chlorophyll biosynthesis found in angiosperms requires tight coordination of chlorophyll biosynthesis and breakdown to achieve chlorophyll homeostasis. However, the specific control mechanisms remain largely unclear. Here, we demonstrate that the scaffold protein BALANCE OF CHLOROPHYLL METABOLISM1 (BCM1) has co-evolved with the carboxy-terminal domains of specific enzymes involved in chlorophyll biosynthesis and breakdown, including GENOMES UNCOUPLED 4 (GUN4) and Mg-dechelatase 1 (SGR1). We found that the land plant-specific interaction of BCM1 with the carboxy-terminal domains of GUN4 and SGR1 is indispensable for concurrent stimulation of chlorophyll biosynthesis and suppression of chlorophyll breakdown. The land plant-specific carboxy-terminal domain is essential for the membrane docking and turnover of GUN4, whereas it is key for proteolysis of SGR1. More importantly, we identified the metallopeptidase Gravitropism-deficient and Yellow-green 1 (EGY1) as the proteolytic machinery responsible for BCM1-mediated proteolysis of SGR1. In summary, this study reveals the BCM1-EGY1 module has evolved to maintain chlorophyll homeostasis by the post-translational control of the balance between chlorophyll biosynthesis and breakdown. This mechanism thus represents an evolutionary response to the metabolic demands imposed on plants in terrestrial environments.