Cell wall ester modifications and volatile emission signatures of plant response to abiotic stress

Abstract

Growth suppression and defence signalling are simultaneous strategies that plants invoke to respond to abiotic stress. Here, we show that the drought stress response of poplar trees (Populus trichocarpa) is initiated by a suppression in cell wall derived methanol (MeOH) emissions and activation of acetic acid (AA) fermentation defences. Temperature sensitive emissions dominated by MeOH (AA/MeOH <30%) were observed from physiologically active leaves, branches, detached stems, leaf cell wall isolations and whole ecosystems. In contrast, drought treatment resulted in a suppression of MeOH emissions and strong enhancement in AA emissions together with volatiles acetaldehyde, ethanol, and acetone. These drought‐induced changes coincided with a reduction in stomatal conductance, photosynthesis, transpiration, and leaf water potential. The strong enhancement in AA/MeOH emission ratios during drought (400%–3500%) was associated with an increase in acetate content of whole leaf cell walls, which became significantly 13C2‐labelled following the delivery of 13C2‐acetate via the transpiration stream. The results are consistent with both enzymatic and nonenzymatic MeOH and AA production at high temperature in hydrated tissues associated with accelerated primary cell wall growth processes, which are downregulated during drought. While the metabolic source(s) require further investigation, the observations are consistent with drought‐induced activation of aerobic fermentation driving high rates of foliar AA emissions and enhancements in leaf cell wall O‐acetylation. We suggest that atmospheric AA/MeOH emission ratios could be useful as a highly sensitive signal in studies investigating environmental and biological factors influencing growth‐defence trade‐offs in plants and ecosystems.

Fermentation‐mediated growth, signaling, and defense in plants

“…The high activity of fermentation metabolism in leaves under aerobic conditions (Fall, 2003) was proposed to explain large emission bursts of acetaldehyde lasting several minutes following light–dark transitions after a period of photosynthesis (Karl et al ., 2002). Subsequent studies found large emission bursts of not only acetaldehyde following light/dark transitions, but also ethanol, acetic acid, acetone, and methyl acetate (Jardine et al ., 2012, 2022a,b; Dewhirst et al ., 2021) with the magnitude of these bursts greatly increasing under hypoxia (Jardine et al ., 2012). While the biochemical origin of acetone biosynthesis in plants remains uncertain, one possibility is the decarboxylation of acetoacetate in a similar mechanism as in bacteria (Fall, 2003).…”

“…Using online mass spectrometry, temperature‐dependent emissions of acetaldehyde, ethanol, acetic acid, and methyl acetate were quantified in real‐time from individual leaves and branches during drought response in poplar trees (Dewhirst et al ., 2021; Jardine et al ., 2022a,b). Acetic acid emission has also been evaluated at the ecosystem scale using continuous vertical profiles of acetic acid ambient concentrations within and above a tropical forest canopy in South America (Jardine et al ., 2011) and in North America using the technique of eddy covariance where acetic acid emission fluxes are calculated every 30 min from the covariance between above canopy vertical wind speed and ambient acetic acid concentrations (Kim et al ., 2010; Park et al ., 2013).…”

“…Recently, acetaldehyde emission bursts following light–dark transitions was suggested to not derive from the decarboxylation of pyruvate mediated by PDC, but instead from an intermediate of the photosynthesis‐linked methylerythritol phosphate pathway (MEP) in chloroplasts (Jud et al ., 2016). Consistent with this idea, light/dark emission bursts of acetaldehyde, ethanol, acetic acid, and acetone were inhibited by drought (Jud et al ., 2016; Jardine et al ., 2022a,b), increased with cumulative photosynthesis (the total net amount of CO 2 assimilated during the light period, μmol CO 2 m −2 ), strongly suppressed by removing CO 2 from the atmosphere, and directly incorporated 13 CO 2 assimilated during the light period into 13 C 2 ‐acetyl‐CoA (Jardine et al ., 2012). However, as photosynthetic production of triosephosphates (glyceraldehyde‐3‐phosphate, G3P) can be exported to the cytosol and converted to pyruvate via glycolysis, the role of the pyruvate overflow mechanism in the emission bursts of volatile fermentation products (acetaldehyde, ethanol, acetic acid, acetone, and methyl acetate) following light–dark transitions, as originally proposed by Karl et al .…”

Transpiration Responses to Potential Volatile Signals and Hydraulic Failure in Single Leaves ofVitis Vinifera(CV. Shiraz) andArabidopsis Thaliana(Col 0) Utilising Sensitive Liquid Flow and Simultaneous Gas Exchange

“…Nevertheless, the non-specific sensors used were also able to detect volatiles emitted by the leaf but not to the resolution of specific molecules as used in other studies e.g. (Jardine et al, 2022; Jud et al, 2018). They were detected from V. vinifera leaves during the light-dark transition but not dark-light as observed in other studies (Jud et al, 2016) though for barley light-dark transitions appear to show a small peak in methanol emission (Jud et al, 2018).…”

“…Alternatively the sensitivity to methanol may be dependent on the transition phase or state of the stomata, that is, stomata may be less sensitive to methanol during the opening phase when methanol is normally released. Other alternatives exist to be further explored including that methanol may be part of a feedback system or that stomatal responses may depend on a combination of methanol with other VOCs, for example, acetic acid (Jardine et al, 2022).…”