Stem girdling indicates prioritized carbon allocation to the root system at the expense of radial stem growth in Norway spruce under drought conditions

•Girdling prioritized radial growth (RG) at the expense of carbon (C) storage.•RG increase above girdling (UZ) was significantly more intense under drought.•RG resumption in UZ suggests a distinct C requirement belowground under drought.•NSC content in dead girdled trees suggests C sequestration rather than storage.

The early culmination of maximum radial growth (RG) in late spring has been found in several coniferous species in a dry inner Alpine environment. We hypothesized that an early decrease in RG is an adaptation to cope with drought stress, which might require an early switch of carbon (C) allocation to belowground organs. To test this hypothesis, we experimentally subjected six-year-old Norway spruce saplings (tree height: 1.35 m; n = 80 trees) to two levels of soil water availability (watered versus drought conditions) and manipulated tree C status by physically blocking phloem transport at three girdling dates (GD). The influence of C availability and drought on tree growth (radial and shoot growth; root biomass) in response to girdling was analyzed in both treatments. Non-structural carbohydrates (NSCs, soluble sugars and starch) were measured in the stem, root and current leader to evaluate changes in tree C status due to girdling. The main finding was a significant increase in RG of the girdled trees compared to the controls above the girdling zone (UZ). At all girdling dates the RG increase was significantly more intense in the drought-stressed compared with watered trees (c. 3.3 and 1.9-fold higher compared with controls in the drought-stressed and watered trees, respectively), most likely indicating that an early switch of C allocation to belowground occurs as an adaptation to maintain tree water status under drought conditions. Reactivation of the cambium after the cessation of its regular activity was detected in UZ in drought-stressed trees, while below the girdling zone no xylem formation was found and the NSC content was strikingly reduced. Irrespective of water availability, girdling before growth onset significantly reduced the progression of bud break (P < 0.05) and the length of the current leader shoot by −47% (P < 0.01) indicating a reduction in xylem hydraulic conductance, which was corroborated by significantly reduced xylem sap flow (P < 0.001). Based on our findings, we conclude that during the growing season drought stress prioritizes an early switch of C allocation to the root system as an adaptation to maintain adequate tree water status in drought-prone environments.