Aerobic fermentation in plant drought response
The upregulation of aerobic fermentation in plants is now recognized as
an evolutionarily conserved drought survival strategy in plants, with
the amount of acetate produced directly correlating to survival
(Kimet al., 2017). Drought-induced acetate accumulation promotesde novo synthesis of the potent phytohormone jasmonic acid (JA)
and the acetylation of histone H4, which influences the priming of the
JA signaling pathway for plant drought tolerance
(Kimet al., 2017). Thus, acetate regulates an epigenetic switch of
metabolic flux conversion and hormone signaling by which plants adapt to
drought. However, destructive measurements are required to evaluate
acetate-linked drought responses, limiting the temporal and spatial
scales that can be studied. As a consequence, few studies have reported
aerobic fermentation rates in plants during drought due to the current
method requirements of destructive sampling followed by offline tissue
analysis of acetate content
(Dewhirstet al., 2021b). In this study, by directly quantifying real-time
leaf emissions rates of MeOH together with volatiles intermediates of
aerobic fermentation (acetaldehyde, AA, ethanol, acetone), we suggest
that growth and aerobic fermentation responses to drought can be studied
in real-time from individual leaves to whole ecosystems. At the onset of
drought in poplar, large increases in the fermentation volatiles
acetaldehyde, acetic acid, ethanol, and acetone were consistently
emitted from poplar branches despite reduced stomatal conductance.
This suggests that
drought-activation of the aerobic fermentation pathway occurred
(Kim
et al., 2017; Rasheed et al., 2018), with foliar emissions of methyl
acetate (Dewhirst et al. , 2021b) and acetone (Fall 2003, Jardineet al. , 2010) associated with acetate activation to acetyl-CoA
(Millerd et al. , 1954).
During aerobic fermentation,
acetate formed from the oxidation of acetaldehyde does not lead to
Nicotinamide adenine dinucleotide+(NAD+) regeneration, as in the case of ethanol
production in anoxic tissues like flooded roots (Kreuzwieser et
al. ,1999). However, while NAD+ regeneration is
considered a critical aspect of fermentation under anoxia, it may be
less important during aerobic fermentation where acetate may be a key
respiratory substrate, effectively coupling aerobic fermentation with
mitochondrial respiration to help meet high energy demands of the cell
(Tadege 1997). However, non-fermentative sources of acetaldehyde may be
possible during stress, such as the peroxidation of membranes associated
with irreversible damage (Jardine et al. , 2009).
Our study suggests that there are at least two distinct plant sources of
atmospheric AA emissions; hydrolysis of O -acetyl groups on the
cell wall (Figure 6 ) and the aerobic fermentation pathway
(Figures 3, 7 ). AA and MeOH emission patterns of hydrated leaf
cell wall isolations (AIR) showed similar temperature sensitivities when
compared with physiologically active poplar leaves and branches.
Emissions of AA and MeOH increased with temperature, with AA/MeOH
tending to slightly increase with temperature but generally remaining
below 30%. Similar results were observed at the ecosystem scale, for
example in Alabama, where ambient AA and MeOH concentrations and AA/MeOH
ratio above a mixed hardwood forest increased with air temperature with
AA/MeOH ranging from < 5% during early mornings to high
values of 25% in the afternoon. The striking similarities in
temperature sensitivities of AA, MeOH, and AA/MeOH emissions from
hydrated leaf cell wall material (AIR), leaves, branches, and whole
ecosystems provides direct evidence for the cell wall as the main source
of foliar MeOH and AA emissions during normal physiological activities.
In contrast, drought stress activates a second source of AA emissions
via aerobic fermentation, which overwhelms cell wall sources. Together
with the decreased MeOH emissions, AA/MeOH ratios increased dramatically
(400-3,500%). However, we caution that the use of the AA/MeOH emission
ratio as a plant and ecosystem growth and stress indicator is only
realistic if net emissions of AA and MeOH occur under natural
conditions. While net uptake of atmospheric MeOH has not been
demonstrated to our knowledge, limited studies on AA exchange between
plants and the atmosphere suggests that under polluted atmospheres with
high AA concentrations in the lower troposphere, net uptake of
atmospheric AA can occur (Jardine et al ., 2011).