Abstract
Climate-induced forest die-off is widespread in multiple biomes, strongly affecting the species composition, function and primary production in forest ecosystems. Hydraulic failure and carbon starvation in xylem sapwood are major hypotheses to explain drought-induced tree mortality. Because it is difficult to obtain enough field observations on drought-induced mortality in adult trees, the current understanding of the physiological mechanisms for tree die-offs is still controversial. However, the simultaneous examination of water and carbon uses throughout dehydration and rehydration processes in adult trees will contribute to clarify the roles of hydraulic failure and carbon starvation in tree wilting. Here we show the processes of the percent loss of hydraulic conductivity (PLC) and the content of nonstructural carbohydrates (NSCs) of distal branches in woody plants with contrasting water use strategy. Starch was converted to soluble sugar during PLC progression under drought, and the hydraulic conductivity recovered following water supply. The conversion of NSCs is strongly associated with PLC variations during dehydration and rehydration processes, indicating that stored carbon contributes to tree survival under drought; further carbon starvation can advance hydraulic failure. We predict that even slow-progressing drought degrades forest ecosystems via carbon starvation, causing more frequent catastrophic forest die-offs than the present projection.
Highlights
Rates and NSCs content in sapwood have been reported to decrease during dehydration processes[28,29], whereas there are no reports of such changes during rehydration processes
Evaluation of carbon starvation and hydraulic failure hypotheses requires monitoring both of whole-plant carbon dynamics and hydraulic dynamics of xylem embolism and recovery during the dehydration and rehydration processes
We show that PLC can be a trigger of carbon dynamics between starch and soluble sugars within xylem sapwood in adult trees, and the amount of carbon dynamically transformed varies among tree species
Summary
Rates and NSCs content in sapwood have been reported to decrease during dehydration processes[28,29], whereas there are no reports of such changes during rehydration processes. To evaluate the relationship between the hydraulic failure and carbon use processes, we simultaneously measured daily time courses of the PLC (percent loss of conductivity) and NSCs content in the xylem sapwood of distal branches, in addition to the leaf water potential, leaf gas exchange and stem respiration rates, in drought-tolerant woody plants. To clarify the contribution of NSCs to hydraulic failure, we selected field-growing adult trees of two drought-tolerant woody plants, Hibiscus glaber Matsum. Xylem cavitation tolerance against dehydration in Hibiscus branches is lower than that in Ligustrum branches. These interspecific differences should reflect different physiological performance with respect to hydraulic failure and carbon use. We discuss the implications of our findings for global climate-induced forest die-offs and their influence on terrestrial ecosystems
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