Plastid Sulfate Transporters Open Doors to Abiotic Stress Resistance

Climate change is causing more extreme weather patterns and increasing challenges for agriculture. The unusually dry European summer of 2018 caused an 8% drop in cereal production (https://ec.europa.eu/info/sites/info/files/food-farming-fisheries/farming/documents/short-term-outlook-autumn-2018_en.pdf). Plants need water for photosynthesis and to maintain turgor pressure; drought-stressed plants wilt, turn yellow, and eventually die. Stomata quickly close during drought stress, limiting water loss by transpiration. Since drought is first perceived by roots, this response requires a signal to move rapidly upward to the leaves, where stomata are localized.

The anion sulfate (SO₄⁻²) quickly accumulates in the xylem upon drought stress and is therefore thought to fulfill this role as a signaling molecule (Malcheska et al., 2017). Several classes of SO₄⁻² transporters (SULTRs) are responsible for SO₄⁻² uptake from the soil (root-localized SULTR1;1 and SULTR1;2) and transport into the xylem and toward the shoot (SULTR2;1 and SULTR2;2) or into the phloem and back to the roots (SULTR1;3; Fig. 1). At the cellular level, SULTR4;1 and SULT4;2 mediate SO₄⁻² efflux from the vacuole, where it is stored. The SULTR3 class of transporters has been less well studied, although SULTR3;1 was shown to localize to the chloroplast membrane and import SO₄⁻² 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 SO₄⁻² into the plastids (Fig. 1).

Figure 1.

Sulfate transport is essential for drought stress responses in plants. Different classes of SULTR transporters facilitate the transport of SO₄⁻² throughout the plant. During drought, SO₄⁻² accumulates in the xylem and moves toward the green tissues. The SULTR3 class of transporters, localized at the plastid membrane, brings SO₄⁻² into the chloroplasts. There, the sulfur is metabolized into Cys, which is essential for ABA synthesis, the hormone that induces stomatal closure. Sulfur metabolism produces a by-product, PAP, which acts as a retrograde signal that moves toward the nucleus to induce the expression of stress-response genes.

SO₄⁻² 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. SO₄⁻² is the main source of sulfur, which is incorporated into the amino acids Cys and Met via a plastid-localized metabolic process. Cys is essential for abscisic acid (ABA) biosynthesis (Fig. 1). Despite the limited nutrient uptake from the soil during drought, SO₄⁻² 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 wild-type plants.

SO₄⁻² uptake into the chloroplasts also contributes to drought stress tolerance in an ABA-independent pathway. During secondary sulfur metabolism in the plastids, an important by-product accumulates: 3′-phosphoadenosine 5′-phosphate (PAP). PAP can be degraded to AMP by the Arabidopsis 3′(2′),5′-bisphosphate nucleotidase (SAL1) enzyme, but it can also move out of the chloroplast. PAP is a retrograde signal, able to enter the nucleus, where it inhibits the RNA-degrading ability of several 5′ to 3′ exoribonucleases. This results in the accumulation of drought-related gene products and increased stress tolerance (Fig. 1). As a proof of concept, sal1 mutants of Arabidopsis accumulate PAP and are able to withstand 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. Chloroplasts are the photosynthetic and metabolic factories but, as supported by an increasing number of studies, also act as abiotic stress signaling modules.