Transcriptional and metabolic profiling of sulfur starvation response in two monocots.

BACKGROUND: Sulfur (S) is a mineral nutrient essential for plant growth and development, which is incorporated into diverse molecules fundamental for primary and secondary metabolism, plant defense, signaling, and maintaining cellular homeostasis. Although, S starvation response is well documented in the dicot model Arabidopsis thaliana, it is not clear if the same transcriptional networks control the response also in the monocots. RESULTS: We performed series of physiological, expression, and metabolite analyses in two model monocot species, one representing the C3 plants, Oryza sativa cv. kitaake, and second representing the C4 plants, Setaria viridis. Our comprehensive transcriptomic analysis revealed twice as many differentially expressed genes (DEGs) in S. viridis than in O. sativa under S-deficiency, consistent with a greater loss of sulfur and S-containing metabolites under these conditions. Surprisingly, most of the DEGs and enriched gene ontology terms were species-specific, with an intersect of only 58 common DEGs. The transcriptional networks were different in roots and shoots of both species, in particular no genes were down-regulated by S-deficiency in the roots of both species. CONCLUSIONS: Our analysis shows that S-deficiency seems to have different physiological consequences in the two monocot species and their nutrient homeostasis might be under distinct control mechanisms.

Unique features of regulation of sulfate assimilation in monocots.

Sulfate assimilation is an essential pathway of plant primary metabolism, regulated by the demand for reduced sulfur (S). The S-containing tripeptide glutathione (GSH) is the key signal for such regulation in Arabidopsis, but little is known about the conservation of these regulatory mechanisms beyond this model species. Using two model monocot species, C3 rice (Oryza sativa) and C4Setaria viridis, and feeding of cysteine or GSH, we aimed to find out how conserved are the regulatory mechanisms described for Arabidopsis in these species. We showed that while in principle the regulation is similar, there are many species-specific differences. For example, thiols supplied by the roots are translocated to the shoots in rice but remain in the roots of Setaria. Cysteine and GSH concentrations are highly correlated in Setaria, but not in rice. In both rice and Setaria, GSH seems to be the signal for demand-driven regulation of sulfate assimilation. Unexpectedly, we observed cysteine oxidation to sulfate in both species, a reaction that does not occur in Arabidopsis. This reaction is dependent on sulfite oxidase, but the enzyme(s) releasing sulfite from cysteine still need to be identified. Altogether our data reveal a number of unique features in the regulation of S metabolism in the monocot species and indicate the need for using multiple taxonomically distinct models to better understand the control of nutrient homeostasis, which is important for generating low-input crop varieties.

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

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.

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

Global climate change is a challenge for efforts to ensure food security for future generations. It will affect crop yields through changes in temperature and precipitation, as well as the nutritional quality of crops. Increased atmospheric CO2 leads to a penalty in the content of proteins and micronutrients in most staple crops, with the possible exception of C4 crops. It is essential to understand the control of nutrient homeostasis to mitigate this penalty. However, despite the importance of mineral nutrition for plant performance, comparably less is known about the regulation of nutrient uptake and homeostasis in C4 plants than in C3 plants and mineral nutrition has not been a strong focus of the C4 research. Here we review what is known about C4 specific features of nitrogen and sulfur assimilation as well as of homeostasis of other essential elements. We identify the major knowledge gaps and urgent questions for future research. We argue that adaptations in mineral nutrition were an integral part of the evolution of C4 photosynthesis and should be considered in the attempts to engineer C4 photosynthetic mechanisms into C3 crops.