Introduction
Terrestrial ecosystem dynamics are dramatically changing in response to
trends in surface warming and drought
(Palut
and Canziani, 2007). Increased magnitude, frequency, and spatial
distribution of abiotic stress anomalies threaten the ability of natural
and managed ecosystems to produce sustainable food, wood, biofuels, and
other bioproducts as well as to mitigate increased atmospheric
CO2 by photosynthetic conversion to biomass. Driven by
increasing leaf-atmosphere vapor pressure deficits and soil moisture
limitations
(Eamus
et al., 2013), partial stomatal closure in response to high temperature
and drought stress reduces leaf gas exchange including net
photosynthesis and transpiration fluxes
(Dewhirst
et al., 2021a). This phenomenon is well documented on diurnal time
scales in numerous ecosystems, where a mid-day depression of net
photosynthesis, transpiration, and stomatal conductance are associated
with high vapor pressure deficits and leaf temperatures above their
optimal values
(Pathre
et al., 1998).
Prolonged excessive water loss via transpiration not replaced by water
uptake from the soil can result in drought-induced tissue senescence and
mortality, thereby converting individual plants and ecosystems from net
sinks of CO2 to net sources
(McDowell
et al., 2008; Jardine et al., 2015; Liu et al., 2021). In northern
China, trees of the fast growing genus poplar, which are actively being
investigated for afforestation efforts and as renewable sources of
biofuels and bioproducts globally, have experienced large-scale dieback
and mortality in recent years
(Ji
et al., 2020). An estimated 79.5% of the area of the poplar forests
have experienced severe degradation with an observed trend of narrower
tree-ring widths of intact trees together with reduced soil moisture.
These observations highlight the need to understand the mechanisms of
poplar forest growth suppression and die-back in response to drought
stress
(Ji
et al., 2020).
A common thread among many of the biochemical and physiological
processes that determine ecosystem dynamic responses to climate change
variables are alterations in plant cell wall chemical composition,
structure, and function
(Dewhirst
et al., 2020a). A large proportion of the plant cell wall polymers can
be heavily modified with methyl and O -acetyl ester groups which
may play important roles in cell growth and tissue development
(Peaucelle
et al., 2012), proper xylem
(Yuan
et al., 2016) and stomatal functioning
(Amsbury
et al., 2016), central carbon and energy metabolism
(Jardine
et al., 2017), and stress communication and signaling
(Novaković
et al., 2018). For example, wood of hybrid poplar trees, one of the
fastest growing temperate trees in the world, is composed of lignin
(22%), cellulose (40%), hemicellulose (20%) dominated by theO -acetylated polysaccharide glucuronoxylan, and other
polysaccharides such as pectins (18%), which can be both heavilyO -acetylated and methyl-esterified
(Sannigrahi
et al., 2010). The two main components of the plant primary cell wall,
the
pectin
matrix and the cellulose/xyloglucan network, are constantly being
remodeled to support dynamic morphological and physiological processes
from daily growth and stress response patterns, to developmental changes
over longer time scales
(Chebli
and Geitmann, 2017). This remodeling is regulated, in part, by a number
of loosening and stiffening agents including pectin and xylan methyl and
acetyl esterases which catalyze the hydrolysis of cell wall esters on
the wall. The hydrolysis of methyl and O -acetyl esters leads to
rapid physicochemical changes in the cell wall and the release of
methanol
(Fall,
2003) and acetic acid
(Scheller,
2017). Given that cell wall methyl and O -acetyl esters are known
to modify cell wall elasticity/rigidity
(Peaucelle
et al., 2011), and previous observations have shown links between bulk
cell wall elasticity and water relations
(Roig-Oliver
et al., 2020), they may play important roles in the response to drought
(Ganie
and Ahammed, 2021). However, how the degree of cell wall esterification
varies with abiotic stress is largely unknown
(Pauly
and Keegstra, 2010; Gille and Pauly, 2012).
One evolutionarily conserved, but poorly understood survival strategy in
plants is drought-induced activation of aerobic fermentation, resulting
in the formation of acetate
(Kim
et al., 2017). The degree of acetate accumulation in plants predicts
survivability, in part by mediating protein acetylation and jasmonate
defense signaling. In this study, we hypothesize that due to hydraulic
limitations to growth during drought, cell wall-derived MeOH production
is inhibited. Moreover, although cell wall-derived AA may be an
important source of foliar AA emission to the atmosphere
(Dewhirst
et al., 2020b), we hypothesize that aerobic fermentation becomes the
dominant source of leaf AA emissions during drought, as a central
component of the plant drought response. We aimed to define real-time
patterns in MeOH and AA emissions together with the fermentation
volatiles acetaldehyde, ethanol, and acetone in parallel with leaf gas
exchange (net photosynthesis, transpiration, stomatal conductance) and
leaf water potential during experimental drought stress in 2-year old
potted California poplar (Populus trichocarpa ) trees and
complementary MeOH and AA gas exchange studies on leaf bulk cell wall
preparations and physiologically active leaves, branches and whole
ecosystems.
We define the AA/MeOH emission ratio as a potentially sensitive
atmospheric indicator of environmental and biological conditions that
favor rapid plant growth versus reduced growth and defense activation.
Using detached branches and whole plant xylem delivery of a 10 mM13C2-acetate
solution via the transpiration stream followed by analysis of13C2-acetate content of leaf cell
walls preparations, we evaluate the hypothesis that aerobic fermentation
signaling can impact the acetylation of numerous biopolymers including
cell wall carbohydrates.