Interorganelle Communication: Peroxisomal MALATE DEHYDROGENASE 2 Connects Lipid Catabolism to Photosynthesis through Redox Coupling in Chlamydomonas

International audiencePlants and algae must tightly coordinate photosynthetic electron transport and metabolic activities given that they often face fluctuating light and nutrient conditions. The exchange of metabolites and signaling molecules between organelles is thought to be central to this regulation but evidence for this is still fragmentary. Here we show that knocking out the peroxisome-located MALATE DEHYDROGENASE 2 (MDH2) of Chlamydomonas reinhardtii results in dramatic alterations not only in peroxisomal fatty acid breakdown but also in chloroplast starch metabolism and photosynthesis. mdh2 mutants accumulated 50% more storage lipid and twofold more starch than wild type during nitrogen deprivation. In parallel, mdh2 showed increased PSII yield and photosynthetic CO 2 fixation. Metabolite analyses revealed a >60% reduction in malate, together with increased levels of NADPH and H 2 O 2 in mdh2. Similar phenotypes were found upon high light exposure. Furthermore, based on the lack of starch accumulation in a knockout mutant of the H 2 O 2-producing peroxisomal ACYL-COA OXIDASE 2 and on the effects of H 2 O 2 supplementation, we propose that peroxisome-derived H 2 O 2 acts as a regulator of chloroplast metabolism. We conclude that peroxisomal MDH2 helps photoautotrophs cope with nitrogen scarcity and high light by transmitting the redox state of the peroxisome to the chloroplast by means of malate shuttle-and H 2 O 2-based redox signaling