Non-structural carbohydrates constrain xylem formation of Picea crassifolia under drought year in the Qilian Mountains of Northwest China

Tree xylem formation is highly dependent on non-structural carbohydrates content and microenvironments. However, it is still less well understood how the key variables regulate cambial activity and xylem formation under different environmental conditions, or the specific contribution of each variable to the number of cells in different stages of xylogenesis. Here, we monitored the xylogenesis and xylem non-structural carbohydrates dynamics of Picea crassifolia during the growing seasons of 2021 and 2022 along an altitude gradient in the Qilian Mountains. We found that the date of maximum cell production rate was about a week later in 2021 than in 2022, and that was later at 2950 and 3200 m than at 2700 m. High altitude sites developed significantly more cambial cells, driving substantially higher cell production rates. Notably, non-structural carbohydrates remained stable early in the growing season before accumulating to peak levels in 2021, whereas 2022 showed a pronounced decrease followed by recovery. The altitude-independent contrast reveals seasonal non-structural carbohydrates dynamics, as the 2022 decline connects stored carbohydrates to sustained xylem formation under drought stress. Linear mixed-effects models showed that, in 2021, cambium cells were predominantly influenced by soil water content and tree individuality, enlargement cells primarily by air temperature (AT), wall-thickening cells by both air and soil temperatures, and the rates of cell production were most significantly affected by AT, soil temperature, and tree individuality. However, in 2022, the cambium cells enlargement cells, and cell production rates were constrained by starch and soluble sugars, while the wall-thickening cells were limited primarily by soluble sugars. Our findings demonstrate that drought triggers a physiological transition from environmental to non-structural carbohydrates mediated control of xylogenesis, highlighting the critical role of carbon reserves for tree resilience in arid regions.