The Roles of Organic Acids in C(4) Photosynthesis

Organic acids are involved in numerous metabolic pathways in all plants. The finding that some plants, known as C(4) plants, have four-carbon dicarboxylic acids as the first product of carbon fixation showed these organic acids play essential roles as photosynthetic intermediates. Oxaloacetate (OAA), malate, and aspartate (Asp) are substrates for the C(4) acid cycle that underpins the CO(2) concentrating mechanism of C(4) photosynthesis. In this cycle, OAA is the immediate, short-lived, product of the initial CO(2) fixation step in C(4) leaf mesophyll cells. The malate and Asp, resulting from the rapid conversion of OAA, are the organic acids delivered to the sites of carbon reduction in the bundle-sheath cells of the leaf, where they are decarboxylated, with the released CO(2) used to make carbohydrates. The three-carbon organic acids resulting from the decarboxylation reactions are returned to the mesophyll cells where they are used to regenerate the CO(2) acceptor pool. NADP-malic enzyme-type, NAD-malic enzyme-type, and phosphoenolpyruvate carboxykinase-type C(4) plants were identified, based on the most abundant decarboxylating enzyme in the leaf tissue. The genes encoding these C(4) pathway-associated decarboxylases were co-opted from ancestral C(3) plant genes during the evolution of C(4) photosynthesis. Malate was recognized as the major organic acid transferred in NADP-malic enzyme-type C(4) species, while Asp fills this role in NAD-malic enzyme-type and phosphoenolpyruvate carboxykinase-type plants. However, accumulating evidence indicates that many C(4) plants use a combination of organic acids and decarboxylases during CO(2) fixation, and the C(4)-type categories are not rigid. The ability to transfer multiple organic acid species and utilize different decarboxylases has been suggested to give C(4) plants advantages in changing and stressful environments, as well as during development, by facilitating the balance of energy between the two cell types involved in the C(4) pathway of CO(2) assimilation. The results of recent empirical and modeling studies support this suggestion and indicate that a combination of transferred organic acids and decarboxylases is beneficial to C(4) plants in different light environments.