SULTR3s Function in Chloroplast Sulfate Uptake and Affect ABA Biosynthesis and the Stress Response

Abstract

Plants are major sulfur reducers in the global sulfur cycle. Sulfate, the major natural sulfur source in soil, is absorbed by plant roots and transported into plastids, where it is reduced and assimilated into Cys for further metabolic processes. Despite its importance, how sulfate is transported into plastids is poorly understood. We previously demonstrated using single Arabidopsis (Arabidopsis thaliana) genetic mutants that each member of the sulfate transporter (SULTR) subfamily 3 was able to transport sulfate across the chloroplast envelope membrane. To resolve the function of SULTR3s, we constructed a sultr3 quintuple mutant completely knocking out all five members of the subfamily. Here we report that all members of the SULTR3 subfamily show chloroplast membrane localization. Sulfate uptake by chloroplasts of the quintuple mutant is reduced by more than 50% compared with the wild type. Consequently, Cys and abscisic acid (ABA) content are reduced to ;67 and ;20% of the wildtype level, respectively, and strong positive correlations are found among sulfate, Cys, and ABA content. The sultr3 quintuple mutant shows obvious growth retardation with smaller rosettes and shorter roots. Seed germination of the sultr3 quintuple mutant is hypersensitive to exogenous ABA and salt stress, but is rescued by sulfide supplementation. Furthermore, sulfateinduced stomatal closure is abolished in the quintuple mutant, strongly suggesting that chloroplast sulfate is required for stomatal closure. Our genetic analyses unequivocally demonstrate that sulfate transporter subfamily 3 is responsible for more than half of the chloroplast sulfate uptake and influences downstream sulfate assimilation and ABA biosynthesis.

Plastid Sulfate Transporters Open Doors to Abiotic Stress Resistance

“…drought much better than wild-type plants (Wilson et al, 2009;Estavillo et al, 2011;Chan et al, 2013). The data provided by Chen et al (2019) confirm that chloroplasts play a key role during drought stress adaptation. Although far away from the source of the stress, chloroplasts gather information and release the signals to undertake action.…”

“…Despite the limited nutrient uptake from the soil during drought, SO 4 22 quickly accumulates in the xylem sap, is transported toward green tissues, is imported into the chloroplasts, and ultimately causes an increase in ABA and stomatal closure (Malcheska et al, 2017;Batool et al, 2018). Chen et al (2019) now show that this rapid drought response depends on all five SULTR3 transporters, resulting in an 80% reduction in ABA levels in the quintuple mutant compared with wildtype plants.…”

“…1). SO 4 22 accumulation in the chloroplasts is essential, as is supported by the impaired-growth phenotype of the sultr3-quintuple mutant that Chen et al (2019) created for their study. SO 4 22 is the main source of sulfur, which is incorporated into the amino acids Cys and Met via a plastid-localized metabolic process.…”

“…The SULTR3 class of transporters has been less well studied, although SULTR3;1 was shown to localize to the chloroplast membrane and import SO 4 22 into these organelles (Cao et al, 2014). In this issue of Plant Physiology, Chen et al (2019) characterize the function of all five SULTR3 transporters in Arabidopsis (Arabidopsis thaliana). They confirm that all are localized to the chloroplast membrane and facilitate the import of SO 4 22 into the plastids (Fig.…”

MADS-box factor AGL16 negatively regulates drought resistance via stomatal density and stomatal movement

“…The ABA content is significantly decreased in Arabidopsis aba2 and aao3 mutants, which show enhanced sensitivity to drought (Nambara et al, 1998; Seo et al, 2000; Wang et al, 2018). Recently, the essential nutrient sulfate has been confirmed to induce stomatal closure (Batool et al, 2018; Chen et al, 2019), probably by affecting ABA biosynthesis via cysteine as sulfur donor for MoCo modification by ABA3.…”