Integration of sulfate assimilation with carbon and nitrogen metabolism in transition from C3 to C4 photosynthesis

Abstract

The first product of sulfate assimilation in plants, cysteine, is a proteinogenic amino acid and a source of reduced sulfur for plant metabolism. Cysteine synthesis is the convergence point of the three major pathways of primary metabolism: carbon, nitrate, and sulfate assimilation. Despite the importance of metabolic and genetic coordination of these three pathways for nutrient balance in plants, the molecular mechanisms underlying this coordination, and the sensors and signals, are far from being understood. This is even more apparent in C4 plants, where coordination of these pathways for cysteine synthesis includes the additional challenge of differential spatial localization. Here we review the coordination of sulfate, nitrate, and carbon assimilation, and show how they are altered in C4 plants. We then summarize current knowledge of the mechanisms of coordination of these pathways. Finally, we identify urgent questions to be addressed in order to understand the integration of sulfate assimilation with carbon and nitrogen metabolism particularly in C4 plants. We consider answering these questions to be a prerequisite for successful engineering of C4 photosynthesis into C3 crops to increase their efficiency.

Keywords: Flaveria; C4 photosynthesis; cysteine; evolution; primary metabolism; sulfate assimilation.

Fig. 1.

Conceptualized plant cell showing the convergence of carbon assimilation through the Calvin cycle, nitrate assimilation through reduction and the GS–GOGAT cycle, and sulfate assimilation. These three pathways converge at cysteine synthesis, making cysteine a keystone metabolite connecting primary metabolism.

Fig. 2.

Carbon and nitrogen metabolism impact sulfur signaling. Red lines signify repression or down-regulation, while blue lines represent activation or up-regulation. Black lines represent biochemical pathways

Fig. 3.

Model showing separation of enzymes between the M and BS in carbon assimilation (a), nitrogen assimilation (b), and sulfate assimilation (c) in C₄ plants.