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.

Transcriptomic Study for Identification of Major Nitrogen Stress Responsive Genes in Australian Bread Wheat Cultivars

“…The 50 common DEGs between the second leaf and grain identified were mostly related to defense, amino acid metabolism, N metabolism, carbohydrate metabolism, and sulfate transport. It is known that in the plastid of the leaf, sulfate is converted to sulfide using the reducing power of photosynthesis and incorporated into amino acids that later remobilize to developing seeds (Gallardo et al, 2014;Jobe et al, 2019). Developing seeds requires sulfur amino acids to synthesize storage protein to secure germination for the next generation (Leustek et al, 2000;Saito, 2000).…”

Ensuring Nutritious Food Under Elevated CO2 Conditions: A Case for Improved C4 Crops

“…Nitrogen assimilation in C 4 plants differs from C 3 plants not only in PNUE but also in the intercellular compartmentalization of nitrogen assimilation enzymes (Figure 1; Kopriva, 2011;Jobe et al, 2019). Already at the onset of C 4 photosynthesis research, it was shown that the activity of nitrate reductase, the key enzyme of nitrate assimilation, is localized mainly in the MC of maize, Sorghum sudanense, and Gomphrena globosa (Mellor and Tregunna, 1971).…”

“…Compared to C 3 crops, such as rice, wheat, or oil-seed rape, less is known about specific alterations in mineral nutrition of C 4 plants, despite substantial differences in the organization of nitrate and sulfate assimilation (Jobe et al, 2019). Therefore, in this review, we summarize what is known about C 4 specific features of nitrogen and sulfur metabolism as well as of homeostasis of other essential elements.…”

Genetic encoding of complex traits

“…A large number of tools and resources have been obtained within the past decade, including genome and transcriptome sequences from numerous C 4 species (reviewed in Schlüter and Weber, 2020 ), a metabolic model of C 4 photosynthesis ( Bräutigam et al , 2014 ), and mathematical models describing the evolution of C 4 photosynthesis ( Heckmann et al , 2013 ; Mallmann et al , 2014 ; Blätke and Bräutigam, 2019 ). In addition, attention is starting to be given to other areas of C 4 biology, such as mineral nutrition ( Jobe et al , 2019 ). In this issue, Zamani-Nour et al (2021) address another key issue for C 4 photosynthesis, namely metabolite transport.…”