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

Abstract

The xylem is a complex system that includes a network of dead conduits ensuring long-distance water transport in plants. Under ongoing climate changes, xylem embolism is a major and recurrent cause of drought-induced tree mortality. Non-structural carbohydrates (NSC) play key roles in plant responses to drought and frost stress, and several studies putatively suggest their involvement in the regulation of xylem water transport. However, a clear picture on the roles of NSCs in plant hydraulics has not been drawn to date. We summarize the current knowledge on the involvement of NSCs during embolism formation and subsequent hydraulic recovery. Under drought, sugars are generally accumulated in xylem parenchyma and in xylem sap. At drought-relief, xylem functionality is putatively restored in an osmotically driven process involving wood parenchyma, xylem sap and phloem compartments. By analyzing the published data on stem hydraulics and NSC contents under drought/frost stress and subsequent stress relief, we found that embolism build-up positively correlated to stem NSC depletion, and that the magnitude of post-stress hydraulic recovery positively correlated to consumption of soluble sugars. These findings suggest a close relationship between hydraulics and carbohydrate dynamics. We call for more experiments on hydraulic and NSC dynamics in controlled and field conditions.

Keywords: NSC; PLC; drought; embolism; hydraulic recovery; pH; starch; stem; sugars; xylem sap.

Figure 1

Schematic representation of putative roles of stem NSCs in the hydraulic regulation in woody plants. (a) During drought, root-to-leaf water transport is reduced and NSC reserves (manly from roots ad stems) are mobilized. Stomata are closed and photosynthesis is reduced, and hence sugar export from leaves and transport through phloem is limited. Decreased xylem water potential (Ψ_x) induces embolism formation in xylem conduits and translocation of sugars to embolized vessels, putatively involving NSC metabolism in stem parenchyma cells and phloem unloading. (b) In the post-drought phase, restored water availability in the soil induces an increase in Ψ_x and a cascade of events leading to the refilling of previously embolized vessels. In the short term upon rehydration, stomata are still closed, transpiration is limited, sugars would still be loaded to the refilling vessels, and water would start to move in the direction of the refilling vessels, washing away the sugars accumulated in xylem sap. In the long term, stomata open and “normal” NSC metabolism and water relations are reestablished, and NSCs are invested for reactivation of cambial growth. Blue and red arrows indicate the direction of water and sugar fluxes, respectively, and their size indicates their magnitude. Question marks indicate putative processes. v = xylem vessel; p = wood parenchyma cells. < indicates low and > indicates high.

Figure 2

Relationships between stem hydraulics and non-structural carbohydrate (NSC) during drought/frost stress. Correlation between PLC at the end of stress (PLC_end) and total NSC concentration (a, ΔTotNSC_end) and starch (c, ΔStarch_end) difference between drought/winter-stressed and non-stressed trees. Correlation between drought/frost-induced PLC increase (ΔPLC_end) and the fraction of total NSC at the end of drought/winter stress with respect to control plants (b, TotNSC_end/TotNSC_c), and the soluble sugar difference between drought/winter-stressed and non-stressed trees (d, ΔSoluble_end). Spearman’s correlation coefficient (ρ), related p-value and regression lines are reported.

Figure 3

Relationship between percentage of recovered PLC (PLC_{rec_%}) and the difference in soluble sugar content between recovery and end-drought/frost phase (ΔSoluble_rec). Spearman’s correlation coefficient (ρ), related p-value and regression line are reported.