Priming xylem for stress recovery depends on coordinated activity of sugar metabolic pathways and changes in xylem sap pH

Abstract

Some plant species are capable of significant reduction of xylem embolism during recovery from drought despite stem water potential remains negative. However, the functional biology underlying this process is elusive. We subjected poplar trees to drought stress followed by a period of recovery. Water potential, hydraulic conductivity, gas exchange, xylem sap pH, and carbohydrate content in sap and woody stems were monitored in combination with an analysis of carbohydrate metabolism, enzyme activity, and expression of genes involved in sugar metabolic and transport pathways. Drought resulted in an alteration of differential partitioning between starch and soluble sugars. Upon stress, an increase in the starch degradation rate and the overexpression of sugar symporter genes promoted the efflux of disaccharides (mostly maltose and sucrose) to the apoplast. In turn, the efflux activity of the sugar‐proton cotransporters caused a drop in xylem pH. The newly acidic environment induced the activity of apoplastic invertases leading to the accumulation of monosaccharides in the apoplast, thus providing the main osmoticum necessary for recovery. During drought and recovery, a complex network of coordinated molecular and biochemical signals was activated at the interface between xylem and parenchyma cells that appeared to prime the xylem for hydraulic recovery.

Defoliation-induced compensatory transpiration is compromised in SUT4-RNAi Populus

“…This contrasts with large PtaSUT4 expression decreases that occur in poplar plants grown under chronic, mild water deficit conditions (Frost et al 48 2012). Consistent with the notion of functional versatility in Populus, PtaSUT4 expression has been found to respond differently to chronic and acute water stress (Frost et al 2012;Xue et al 50 2016; Pagliarani et al 2019). In addition, aquaporin expression differs between droughtstressed wild-type (WT) and SUT4-RNAi poplars, consistent with a link between sucrose 52 trafficking and changes in water flux (Xue et al 2016).…”

The Possible Role of Non-Structural Carbohydrates in the Regulation of Tree Hydraulics

“…Multiple studies conducted in the last decade in different poplar species have demonstrated that severe drought triggers a cascade of metabolic processes in xylem parenchyma cells [63,64]. These are supposed to be early events involved in hydraulic restoration when water is again available to the plant [42,64] (see the following section). These events, for which we provide the sequence and related experimental proof below, apparently culminate in the accumulation of low molecular weight sugars in the xylem apoplast ( Figure 1a).…”

“…In xylem parenchyma of Populus tremula x alba, glucose, fructose and maltose derived from starch hydrolysis, while sucrose derived from long distance transport through the phloem-to-parenchyma rays pathway. All these sugars accumulated in the xylem apoplast and sap during drought, possibly due to the activation of plasma membrane sugar transporters in VACs [64]. In fact, sugar (especially maltose and sucrose) symporter genes were overexpressed parallel to starch degradation [64], likely sustaining the efflux of disaccharides to the cell walls in contact with xylem conduits.…”

“…All these sugars accumulated in the xylem apoplast and sap during drought, possibly due to the activation of plasma membrane sugar transporters in VACs [64]. In fact, sugar (especially maltose and sucrose) symporter genes were overexpressed parallel to starch degradation [64], likely sustaining the efflux of disaccharides to the cell walls in contact with xylem conduits. This was accompanied by a decrease in xylem sap pH [64,68], suggesting the involvement of sucrose-proton co-transporters.…”

“…In fact, sugar (especially maltose and sucrose) symporter genes were overexpressed parallel to starch degradation [64], likely sustaining the efflux of disaccharides to the cell walls in contact with xylem conduits. This was accompanied by a decrease in xylem sap pH [64,68], suggesting the involvement of sucrose-proton co-transporters. Indeed, acidification of xylem sap has been documented in several tree species during dry or prolonged frost periods [69,70].…”