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.

/pdf/cell-wall-ester-modifications-and-volatile-emission-3fhtmnqz.pdf

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

While traditionally considered important mainly in hypoxic roots during flooding, upregulation of fermentation pathways in plants has recently been described as an evolutionarily conserved drought survival strategy, with acetate signaling mediating reprograming of transcription and cellular carbon and energy metabolism from roots to leaves. The amount of acetate produced directly correlates with survival through potential mechanisms including defense gene activation, biosynthesis of primary and secondary metabolites, and aerobic respiration. Here, we review root ethanolic fermentation responses to hypoxia during saturated soil conditions and summarize studies highlighting acetate fermentation under aerobic conditions coupled with respiration during growth and drought responses. Recent work is discussed demonstrating long-distance transport of acetate via the transpiration stream as a respiratory substrate. While maintenance and growth respiration are often modeled separately in terrestrial models, here we propose the concept of 'Defense Respiration' fueled by acetate fermentation in which upregulation of acetate fermentation contributes acetate substrate for alternative energy production via aerobic respiration, biosynthesis of primary and secondary metabolites, and the acetylation of proteins involved in defense gene regulation. Finally, we highlight new frontiers in leaf-atmosphere emission measurements as a potential way to study acetate fermentation responses of individual leaves, branches, ecosystems, and regions.

https://onlinelibrary.wiley.com/doi/pdfdirect/10.1111/nph.19015

Fermentation-mediated growth, signaling, and defense in plants.

Abstract Volatile organic compounds (VOCs) may communicate stress between plants. However little appears to be documented on how such VOCs affect transpiration. Changes in transpiration in response to some VOCs was examined by measurement of flow ( Q ) at high resolution into detached leaves of Vitis vinifera (cv. Shiraz) and Arabidopsis (Col 0). Sensors recorded arrival and decay of volatiles at the leaf lamina. Moderate xylem tensions were developed in V. vinifera leaves by incorporating a hydraulic resistance in the flow pathway. Simultaneous recording of leaf gas exchange (Assimilation, A , and Transpiration, E ) for both V. vinifera and Arabidopsis revealed that for Arabidopsis Q was stochastically restricted by the gas exchange cuvette but not E in the short term. Depending on the applied supply pressure cavitation could be controlled in V. vinifera evident from reduced Q , and leaf wilting. Stomatal closure occurred upon cavitation after a transitory increase in E and A , and after wilting began and was reversed by re-pressurization. VOCs were emitted from leaves corresponding to changes in flow rate, and light to dark transitions but not to cavitation. Volatile methanol but not ethanol or methyl salicylate induced a localised dose-dependent reversible stomatal closure in both V. vinifera and Arabidopsis. 

Transpiration Responses to Potential Volatile Signals and Hydraulic Failure in Single Leaves of<i>Vitis Vinifera</i>(CV. Shiraz) and<i>Arabidopsis Thaliana</i>(Col 0) Utilising Sensitive Liquid Flow and Simultaneous Gas Exchange

Growth suppression and defense signaling 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 defenses.
Temperature sensitive emissions dominated by meOH (AA/meOH <
30%) were observed from physiologically active 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 fermentation 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 (400-3,500%) was associated with
an increase in acetate content of whole leaf cell walls, which became
significantly C -labeled
following the delivery of C
-acetate via the transpiration stream. The results
are consistent with central roles of acetate fermentation in regulating
plant defense and metabolic responses to drought, and suggest that cell
wall O-acetylation may be reversible allowing plants to rapidly
respond to drought stresses by down-regulating methyl ester hydrolysis
and growth processes while enhancing O-acetylation. We suggest
that AA/meOH emission ratios could be used as a highly sensitive
non-destructive sensor to discriminate between thresholds of rapid plant
growth and drought stress responses.

/pdf/the-scent-of-senescence-cell-wall-ester-modifications-and-w7jx8pkk.pdf

Luping Su

Papers

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

The Scent of Senescence: Cell wall ester modifications and volatile emission signatures of plant responses to abiotic stress