Adaptive Modifications in Plant Sulfur Metabolism over Evolutionary Time.

Sulfur (S) is an essential element for life on Earth. Plants are able to take up and utilize sulfate (SO42-), the most oxidized inorganic form of S compounds on Earth, through the reductive S assimilatory pathway that couples with the photosynthetic energy conversion. Organic S compounds are subsequently synthesized in plants and made accessible to animals, primarily as the amino acid methionine. Thus, the plant S metabolism clearly has nutritional importance in the global food chain. The S metabolites may be part of the redox regulation and drivers of essential metabolic pathways as cofactors and prosthetic groups, such as Fe-S centers, coenzyme A, thiamine, and lipoic acid. The evolution of the S metabolic pathways and enzymes reflects critical importance of the functional innovation and diversifications. Here we review the major evolutionary alterations that took place in the S metabolism across different scales and outline research directions that may take advantage of understanding the evolutionary adaptations.

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.

Psb34 protein modulates binding of high-light-inducible proteins to CP47-containing photosystem II assembly intermediates in the cyanobacterium Synechocystis sp. PCC 6803.

Assembly of photosystem II (PSII), a water-splitting catalyst in chloroplasts and cyanobacteria, requires numerous auxiliary proteins which promote individual steps of this sequential process and transiently associate with one or more assembly intermediate complexes. In this study, we focussed on the role of a PSII-associated protein encoded by the ssl1498 gene in the cyanobacterium Synechocystis sp. PCC 6803. The N-terminal domain of this protein, which is here called Psb34, is very similar to the N-terminus of HliA/B proteins belonging to a family of high-light-inducible proteins (Hlips). Psb34 was identified in both dimeric and monomeric PSII, as well as in a PSII monomer lacking CP43 and containing Psb28. When FLAG-tagged, the protein is co-purified with these three complexes and with the PSII auxiliary proteins Psb27 and Psb28. However, the preparation also contained the oxygen-evolving enhancers PsbO and PsbV and lacked HliA/B proteins even when isolated from high-light-treated cells. The data suggest that Psb34 competes with HliA/B for the same binding site and that it is one of the components involved in the final conversion of late PSII assembly intermediates into functional PSII complexes, possibly keeping them free of Hlips. Unlike HliA/B, Psb34 does bind to the CP47 assembly module before its incorporation into PSII. Analysis of strains lacking Psb34 indicates that Psb34 mediates the optimal equilibrium of HliA/B binding among individual PSII assembly intermediates containing CP47, allowing Hlip-mediated photoprotection at all stages of PSII assembly.

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.

Physiological and biochemical responses of sugar beet (Beta vulgaris L) to ultraviolet-B radiation.

Ultraviolet radiation can cause many serious problems for all living organisms. With a growing population, the UV sensitivity of crop plants presents a particular problem. To evaluate the suitability of growing in areas under UV irradiance, the influence of different doses of UV-B (3.042, 6.084 and 9.126 kJm-2d-1) on the sugar beet (Beta vulgaris L) plants was studied. UV-B induced a significant decrease in growth displayed as reduced height and fresh and dry weight. This reduction is not dose dependent and was associated with diminishing photosynthetic O2 evolution, relative chlorophyll content, photosynthetic pigments and chlorophyll fluorescence. On the other hand, antioxidant enzyme activities, total protein content, compatible solutes, total free amino acids and total betalain content were increased under 9.126 kJm-2d-1 UV-B treatments, representing mechanisms by which the plants coped with the stress. The oxidative stress upon UV-B treatment was evident by increased malondialdehyde (MDA) content, however, hydrogen peroxide (H2O2) was not affected in UV-B exposed plants. Thus, the studied sugar beet variety BR1seems to be suitable particularly for areas with high doses of UV-B irradiation.