Glucose uptake to guard cells via STP transporters provides carbon sources for stomatal opening and plant growth

Abstract

Guard cells on the leaf epidermis regulate stomatal opening for gas exchange between plants and the atmosphere, allowing a balance between photosynthesis and transpiration. Given that guard cells possess several characteristics of sink tissues, their metabolic activities should largely depend on mesophyll-derived sugars. Early biochemical studies revealed sugar uptake into guard cells. However, the transporters that are involved and their relative contribution to guard cell function are not yet known. Here, we identified the monosaccharide/proton symporters Sugar Transport Protein 1 and 4 (STP1 and STP4) as the major plasma membrane hexose sugar transporters in the guard cells of Arabidopsis thaliana. We show that their combined action is required for glucose import to guard cells, providing carbon sources for starch accumulation and light-induced stomatal opening that are essential for plant growth. These findings highlight mesophyll-derived glucose as an important metabolite connecting stomatal movements with photosynthesis.

Light-Mediated Signaling and Metabolic Changes Coordinate Stomatal Opening and Closure

“…after white light illumination (Flütsch et al, 2020b). Collectively, Glc, either uptaken into GCs from mesophyll cells via STP transporters, or derived from blue light-induced starch degradation within GCs, contributes to rapid stomatal opening in response to light, highlighting the coordination of mesophyll and GC carbohydrate metabolism, and the tight connection between stomatal movement and photosynthesis.…”

Mesophyll‐derived sugars are positive regulators of light‐driven stomatal opening

“…This alternative transport route has long been overlooked. Fl€ utsch et al, (2020b) used a reverse genetic approach in Arabidopsis and demonstrated that Glc import to guard cells at dawn via the coordinated action of the monosaccharide-H + symporters Sugar Transport Protein 1 and 4 (STP1 and STP4) is essential for (white) light-induced stomatal opening and plant growth (Fl€ utsch et al, 2020b). Guard cells of stp1stp4 double mutants contained almost undetectable amounts of Glc at dawn and were nearly devoid of starch (Fl€ utsch et al, 2020b).…”

“…Flütsch et al ., (2020b) used a reverse genetic approach in Arabidopsis and demonstrated that Glc import to guard cells at dawn via the coordinated action of the monosaccharide‐H + symporters Sugar Transport Protein 1 and 4 (STP1 and STP4) is essential for (white) light‐induced stomatal opening and plant growth (Flütsch et al ., 2020b). Guard cells of stp1stp4 double mutants contained almost undetectable amounts of Glc at dawn and were nearly devoid of starch (Flütsch et al ., 2020b). Imported Glc via STPs likely joins the cytosolic pool of guard cell starch‐derived Glc and significantly contributes to maintaining homeostatic carbohydrate concentrations needed for stomatal opening.…”

Gluconeogenesis in Plants: A Key Interface between Organic Acid/Amino Acid/Lipid and Sugar Metabolism

“…Malate/citrate and sugars are abundant osmotica in stomata, and both can be important in turgor regulation associated with stomatal opening/closing [ 58 , 59 , 60 , 61 , 62 ]. Both PEPCK and PPDK could potentially play a role in converting malate/citrate, which is released from the vacuole, to sugars [ 15 , 17 , 58 , 60 ].…”