A photorespiratory cycle that regulates plant responses to atmospheric CO2

Abstract

Abstract Rubisco (ribulose-1,5-bisphosphate carboxylase-oxygenase), the most prevalent protein on the planet 1,2, catalyzes two competing chemical reactions. One reaction is the carboxylation of ribulose 1,5-bisphosphate (RuBP), which initiates plant carbohydrate synthesis. The other is the oxygenation of RuBP, which initiates photorespiration 3. The common assumption is that photorespiration is a futile cycle that dissipates more than 25% of a plant’s energy as waste heat 4–6, but inhibiting photorespiration decreases shoot protein synthesis 7–11. Here is evidence for a previously unrecognized photorespiratory cycle in which rubisco converts RuBP into pyruvate, malic enzyme carboxylates pyruvate into malate, and malate dehydrogenase oxidizes malate, generating reductants that convert nitrate into amino acids (Fig. 1). This cycle becomes prominent only when rubisco or malic enzyme are associated with manganese, but prior experiments replaced the manganese bound to these enzymes with magnesium 3,12,13. The proposed cycle coordinates photorespiration with several other processes including C3 carbon fixation, pentose phosphate shunt, malate valve, and nitrogen metabolism. It thereby balances plant organic carbon and nitrogen as atmospheric CO2 fluctuates daily, seasonally, and over millennia 14. This carbon:nitrogen homeostasis improves photosynthetic efficiency 3 and explains why C3 species, plants that photorespire at substantial rates, remain dominant in most habitats.