Leaf Shedding and Non-Stomatal Limitations of Photosynthesis Mitigate Hydraulic Conductance Losses in Scots Pine Saplings During Severe Drought Stress

During drought, trees reduce water loss and hydraulic failure by closing their stomata, which also limits photosynthesis. Under severe drought stress, other acclimation mechanisms are trigged to further reduce transpiration to prevent irreversible conductance loss. Here, we investigate two of them: the reversible impacts on the photosynthetic apparatus, lumped as non-stomatal limitations (NSL) of photosynthesis, and the irreversible effect of premature leaf shedding. We integrate NSL and leaf shedding with a state-of-the-art tree hydraulic simulation model (SOX+) and parameterize them with example field measurements to demonstrate the stress-mitigating impact of these processes. We measured xylem vulnerability, transpiration, and leaf litter fall dynamics in Pinus sylvestris (L.) saplings grown for 54 days under severe dry-down. The observations showed that, once transpiration stopped, the rate of leaf shedding strongly increased until about 30% of leaf area was lost on average. We trained the SOX+ model with the observations and simulated changes in root-to-canopy conductance with and without including NSL and leaf shedding. Accounting for NSL improved model representation of transpiration, while model projections about root-to-canopy conductance loss were reduced by an overall 6%. Together, NSL and observed leaf shedding reduced projected losses in conductance by about 13%. In summary, the results highlight the importance of other than purely stomatal conductance-driven adjustments of drought resistance in Scots pine. Accounting for acclimation responses to drought, such as morphological (leaf shedding) and physiological (NSL) adjustments, has the potential to improve tree hydraulic simulation models, particularly when applied in predicting drought-induced tree mortality

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

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