Discussion
Fast growing poplar trees are increasingly being utilized as a sustainable source of bioproducts and biofuels as well as carbon farming, urban greening, hillslope stabilization, and marginal land restoration and re-forestation (Ragauskaset al., 2006; Furtado et al., 2014). Field observations have consistently shown that non-water limited poplar plantations have high growth and productivity rates, but are highly sensitive to drought (Ji et al., 2020). Understanding the biological mechanisms and environmental thresholds that determine plant responses to drought stress is critical for predicting how the structure and function of managed ecosystems will respond to environmental change (McDowellet al., 2008). Previous studies have characterized the sequence of plant hydraulic, physiological, biochemical, and structural changes associated with reversible and irreversible responses to drought stress. For example, leaf dehydration responses of ten angiosperm species showed stomatal closure and a decrease in xylem conductance occurring first as a reversible response (Truebaet al., 2019). This was followed by reaching the turgor loss point, xylem embolism, and the cessation of transpiration as a critical irreversible threshold following which further irreversible damage occurred including to the membranes, pigments, and other components of the photochemical system in the chloroplast (Truebaet al., 2019). While ecosystem response to water deficit can be detected by current remote sensing methods such as solar induced fluorescence (SIF) (Sunet al., 2015), and various normalized vegetation indices such as the Normalized Difference Vegetation Index (NDVI) (Peterset al., 2002) and Enhanced Vegetation Index (EVI) (Auliaet al., 2016), these generally only identify extreme drought and the associated irreversible loss of major leaf function such as transpiration and net carbon assimilation. For example, in 2-yr oldPopulus deltoides individuals, while strong responses of net photosynthesis and stomatal conductance to initial water stress were observed at the leaf level, SIF showed relatively minimal changes (Helmet al., 2020). It was concluded that the value of SIF as an accurate estimator of net photosynthesis may decrease during mild stress events of short duration, especially when the response is primarily stomatal and not fully coupled with the degradation of photosynthetic capacity. This highlights the need for new methods to better understand the biochemical, physiological, and ecological mechanisms in situassociated with the onset of drought stress including processes that alter plant growth and defense balances and their associated changes in leaf CO2 and H2O gas exchange fluxes.
In this study, we present foliar AA/MeOH emission ratios as non-invasive gas-phase chemical observational method providing insights into the dynamics of growth and defense processes during abiotic stress from cell wall leaf isolations, individual leaves, branches, and whole ecosystems. We observed 4 potentially distinct phases during the drought response in poplar trees, with unique CO2/H2O gas exchange, volatile emissions (MeOH and AA), and cell wall characteristics including:
1) Growth Phase: Well hydrated leaves characterized by high rates of net photosynthesis (Anet), transpiration (E) and stomatal conductance (gs), and less negative leaf water potential (LWP) values. MeOH and AA emissions increase with temperature, with AA/MeOH emission ratios low with values below 30%. 2) Methanol Suppression Phase: Characterized by high rates ofA, E and gs. Leaf MeOH emissions are suppressed and AA emissions remain low. The ratio of AA/MeOH may increase relative to the growth phase but remain below 30%. Drought effects reversible. 3) Aerobic fermentation Phase Reduction inAnet, E, gs, and MeOH emissions, with high and sustained emissions of the fermentation volatiles acetaldehyde, acetic acid (AA), ethanol, and acetone. Cell wall O-acetylation increases and the ratio of AA/MeOH greatly increases to 400-3,500%. Drought effects may or may not be reversible. 4) Senescence Phase: Anet, E,gs close to zero indicating a loss of functional photosynthetic capacity and irreversible degradation of cellular structural integrity. The ratio of AA/MeOH emissions begins to decline from the aerobic fermentation phase, but remains high (e.g. 50-100%).