Sensing Sulfur Conditions: Simple to Complex Protein Regulatory Mechanisms in Plant Thiol Metabolism

Abstract

Sulfur is essential for plant growth and development, and the molecular systems for maintaining sulfur and thiol metabolism are tightly controlled. From a biochemical perspective, the regulation of plant thiol metabolism highlights nature's ability to engineer pathways that respond to multiple inputs and cellular demands under a range of conditions. In this review, we focus on the regulatory mechanisms that form the molecular basis of biochemical sulfur sensing in plants by translating the intracellular concentration of sulfur-containing compounds into control of key metabolic steps. These mechanisms range from the simple (substrate availability, thermodynamic properties of reactions, feedback inhibition, and organelle localization) to the elaborate (formation of multienzyme complexes and thiol-based redox switches). Ultimately, the dynamic interplay of these regulatory systems is critical for sensing and maintaining sulfur assimilation and thiol metabolism in plants.

Impairment in Sulfite Reductase Leads to Early Leaf Senescence in Tomato Plants

“…Sulfide in plant cells can be generated either as the result of sulfite reduction by SiR in chloroplasts (Yi et al, 2010;Takahashi et al, 2011) or the release from degraded sulfur-containing biomolecules such as Cys (Alvarez et al, 2010;Álvarez et al, 2012). While sulfide was decreased with leaf age in wild-type leaves, in SIR Ri plants, it increased with leaf age.…”

“…The energy supply from the chloroplasts could be further significantly decreased by a futile cycle of sulfate reduction to sulfite followed by sulfite back oxidation to sulfate. Each round of this cycle would consume one ATP molecule for sulfate adenylation and two molecules of GSH for APS reduction to sulfite (Yi et al, 2010;Takahashi et al, 2011). Taking into account the simultaneous up-regulation of ATPS, APR, and SO in SiR-impaired leaves compared with wildtype plants, the futile cycle of sulfate reduction to sulfite followed by sulfite back oxidation to sulfate by SO in SiR-impaired plants could be an energetically costly process wasting ATP and GSH and enhancing the drop of glutathione levels in the mutant leaves ( Fig.…”

“…The further reductive assimilation of sulfite is catalyzed by sulfite reductase (SiR; EC 1.8.7.1) that contains one iron-sulfur cluster and one siroheme as prosthetic groups and uses reduced ferredoxin as the physiological donor of the six-electron reduction of sulfite to sulfide (Nakayama et al, 2000;Yonekura-Sakakibara et al, 2000). The latter is incorporated by O-acetyl-Ser (thiol) lyases (EC 2.5.1.47) into Cys that can be used for glutathione synthesis (Yi et al, 2010;Takahashi et al, 2011).…”

“…As with other nutrient metabolic pathways in plants, the enzymes required for sulfur assimilation and thiol metabolism are highly regulated and tightly coordinated at many levels (Yi et al, 2010). The flux of metabolites via the sulfate assimilation reductive pathway is controlled by APR enzymes whose expression is modulated by sulfate as well as nitrate availability and various stress factors (Leustek et al, 2000;Martin et al, 2005).…”

Exogenous salicylic acid improves photosynthesis and growth through increase in ascorbate-glutathione metabolism and S assimilation in mustard under salt stress

“…GSH has been shown to act as a signal molecule for S status of plants 14 and is sensitive to ATP-sulfurylase (ATPS), the first enzyme in S-assimilatory pathway. 15 Sulfur assimilation pathway enzymes have been found to be involved in the regulation of GSH synthesis. Therefore, the activity of ATP-sulfurylase (ATPS) may influence GSH and Cys content in plant cell as it is a constituent of sulfur.…”