Unexpected Dual Function of Plant YUCCA Enzymes Links Chlorophyll Catabolism to Auxin Homeostasis

Chlorophyll (Chl) metabolism is pivotal to both photosynthesis and plant senescence and represents one of the most fundamental biological processes on Earth with an estimated annual turnover of 1 billion tons. During Chl degradation, only early catabolites and corresponding enzymes are well characterized, whereas for late-stage degradation products it remains often unclear if their formation involves specific enzymes. Here, we report that the ubiquitous YUCCA10 enzymes from the YUCCA flavin-containing monooxygenase (FMOs) family in land plants, normally implicated in the biosynthesis of indole-3-acetic acid (IAA) as the primary form of auxin, surprisingly catalyze the production of several predominant Chl catabolites via mechanistically distinct Baeyer-Villiger oxidation and subsequent hydrolytic γ-lactam-forming deformylation reactions. These historically postulated but hitherto undiscovered Chl degradation steps on several high molecular weight chl catabolites were verified for YUCCA10 from Vitis vinifera and Coffea arabica, while YUCCA10 from Arabidopsis thaliana lacked this activity. In contrast, all three homologs were able to catalyze the rate-limiting key step in IAA biosynthesis, akin to other YUCCA enzymes. Interestingly, Chl catabolites at physiological concentrations impaired IAA formation by YUCCA10 in vitro, suggesting a key role in leaf senescence through enzymatic feedback regulation of auxin levels.