Shade‐induced reduction of stem nonstructural carbohydrates increases xylem vulnerability to embolism and impedes hydraulic recovery in Populus nigra

Abstract

 Non-structural carbohydrates (NSCs) have been suggested to affect xylem transport under fluctuating water availability, but conclusive evidence is still lacking. We tested the effect of shade-induced NSC depletion on xylem vulnerability to embolism and hydraulic recovery on Populus nigra saplings.  Vulnerability was assessed in light-exposed (L) and shaded (S) plants with the hydraulic method, and in-vivo with the optical method and X-ray MicroCT. Plants were stressed to 80% loss of hydraulic conductance (PLC) and re-irrigated to check for possible recovery. We measured PLC, bark and wood NSC content, as well as xylem sap pH, surface tension ( sap ) and sugar concentration, before, during and after drought.  Shading induced depletion of stem NSC (mainly starch) reserves. All methods converged in indicating higher xylem vulnerability in S than in L plants. This difference was not explained by xylem vessel and pit anatomy or by  sap . Shading impeded sap acidification and sugar accumulation during drought in S plants and prevented hydraulic recovery, which was observed in L plants.  Our results highlight the importance of stem NSCs to sustain xylem hydraulic functioning during drought and suggest that light and/or adequate stem NSC thresholds are required to trigger xylem sap chemical changes involved in embolism recovery.

Limited plasticity in embolism resistance in response to light in leaves and stems in species with considerable vulnerability segmentation

“…Cochard et al (1999), Lemoine et al (2002), and Herbette et al (2010) also found similar results by air injection or the cavitron, measuring losses in hydraulic conductivity in 2–3 cm long stems in Fagus sylvatica acclimated to sun and shade, although vessel length was not determined. More recently, Populus nigra plants grown under shade conditions had stem P 50 values, measured both hydraulically and optically, which were up to 0.3 MPa less negative than those of stems grown under sun conditions (Tomasella et al, 2021). In this recent work, no anatomical differences in the xylem could explain this shift in P 50 , instead, differences in nonstructural carbohydrates were implicated in this variation (Tomasella et al, 2021).…”

“…More recently, Populus nigra plants grown under shade conditions had stem P 50 values, measured both hydraulically and optically, which were up to 0.3 MPa less negative than those of stems grown under sun conditions (Tomasella et al, 2021). In this recent work, no anatomical differences in the xylem could explain this shift in P 50 , instead, differences in nonstructural carbohydrates were implicated in this variation (Tomasella et al, 2021). Most of these species used to assess variation in embolism resistance in response to light environment are characterized by relatively vulnerable xylem to embolism.…”

“…In conifers, Schoonmaker et al, 2010 found increased vulnerability in shade acclimated stems paralleling alterations in pit membrane structure. A recent study in Populus nigra has found that changes in non‐structural carbohydrates drive increased xylem resistance to embolism, up to 0.3 MPa, in plants grown under high light conditions compared to those adapted to shaded conditions (Tomasella et al, 2021).…”

Stem Photosynthesis Affects Hydraulic Resilience in the Deciduous Populusalba but Not in the Evergreen Laurus nobilis

“…Soluble NSCs derived from photosynthesis or by starch hydrolysis are also necessary for osmoregulation processes and/or ROS scavenging [46][47][48]90]. Sugars lead to generation of local positive pressures to drive water inflow into embolized conduits when water potential rises upon re-irrigation, leading to hydraulic recovery, i.e., [61,[91][92][93]. In accordance, L. nobilis plants under drought showed a significant increase in soluble NSC content, and a parallel decrease in starch concentration in both C and S samples, compared to well-watered plants.…”

“…Based on the above, stem-level photosynthesis might play a primary role not only in the production of NSCs contributing to the whole plant carbon gain but also in the modulation and regulation of xylem hydraulic function. Indeed, some recent studies have reported experimental evidence for a role of stem photosynthesis in reducing xylem vulnerability to embolism and improving the capacity for xylem embolism reversal [59][60][61][62][63].…”