Better safe than sorry: Non-stomatal mechanisms delay drought stress and hydraulic failure in Scots pine saplings

Daniel Nadal-Sala, Ruediger Grote, Benjamin Birami, Martha Lutzenberger, Romy Rehschuh, Selina Schwarz and Nadine K. Ruehr, Institute of Meteorology and Climate Research - Atmospheric Environmental Research (IMK-IFU), Karlsruhe Institute of Technology, Garmisch-Partenkirchen, Germany, Timo Knüver, Department of Botany, University of Innsbruck, Innsbruck, Austria

Background/Question/Methods
There is no more vital connection than the tight linkage between water and organic carbon, and there is no more paradigmatic example for that than plant photosynthesis. In plants, carbon uptake is done at elevated expenses in terms of water transport from soil to the atmosphere. Under limited water supply, transpiration increases the tension of the within-tree water column. This will eventually lead to emboli formation and loss of hydraulic conductivity, and may result in tree death. The main mechanism by which trees slow down such tension increases is by actively closing their stomata. However, even if stomata are fully closed, some water loss can still occur through cuticular evaporation. Therefore, non-stomatal mechanisms exist that additionally reduce water losses, and hence increase hydraulic safety. Among these, leaf shedding as well as non-stomatal limitations over photosynthesis (NSL, combining increases in mesophyll conductance and biochemical down-regulation on photosynthesis), are well-known but poorly quantified mechanisms that trees may trigger to save water under drought stress. In order to better describe such mechanisms quantitatively, we conducted a severe two-month-long dry-down experiment on potted Scots pine (Pinus sylvestris L.) saplings (n = 6) and under controlled conditions. We measured tree transpiration, photosynthesis and leaf shedding. Based on our observations we trained a state-of-the-art tree hydraulic model and we quantified the impact of the above-mentioned processes on whole-tree percent loss of conductance.
Results/Conclusions
We found that NSL play a key role in tree drought response by further reducing conductance, which subsequently reduces transpiration and delays dehydration. If sap flow was reduced below a given threshold, saplings responded by shedding leaves. Noteworthy, this threshold was uncorrelated to soil water content. Leaf shedding buffered reductions in xylem water potential and loss of whole-tree conductance in the mid-term. This indicates a hierarchy of active acclimation processes involving a continuous NSL response, and a threshold-based leaf area reduction when P. sylvestris is in danger to lose water to dangerous degrees without any counterpart in form of photosynthetic gain. Combined, both mechanisms reduce whole-plant C uptake, but contribute to tree survival under drought stress.