Title: Fermentation‐mediated growth, signaling, and defense in plants

Journal Article · · New Phytologist
DOI: https://doi.org/10.1111/nph.19015 · OSTI ID:1984305
ORCiD logo [1];  [2]
  1. Climate and Ecosystem Sciences Division Lawrence Berkeley National Laboratory Berkeley CA 94720 USA, Ciências de Florestas Tropicais National Institute for Amazon Research Manaus 69067 Amazonas Brazil
  2. Atmospheric Sciences and Global Change Division Pacific Northwest National Lab Richland WA 99354 USA, School of Biological Sciences Washington State University Pullman WA 99164 USA

Summary 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.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science (BSS)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1984305
Report Number(s):
PNNL-SA-183144
Journal Information:
New Phytologist, Journal Name: New Phytologist Journal Issue: 3 Vol. 239; ISSN 0028-646X
Publisher:
Wiley-BlackwellCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (111)

Flooding-Driven Emissions from Trees book January 2013
Aerobic fermentation in tobacco pollen journal July 1995
The control of the production of lactate and ethanol by higher plants journal January 1974
Acetone production in solventogenic Clostridium species: new insights from non-enzymatic decarboxylation of acetoacetate journal April 2011
Use of cw-CRDS for studying the atmospheric oxidation of acetic acid in a simulation chamber journal June 2006
Simultaneous detection of ethanol, ether and acetone by mid-infrared cavity ring-down spectroscopy at 3.8 μm journal June 2016
Gas exchange and oxygen concentration in pneumatophores and prop roots of four mangrove species journal February 2002
Green leaf volatiles and oxygenated metabolite emission bursts from mesquite branches following light–dark transitions journal June 2012
Exogenous application of acetic acid improves the survival rate of cotton by increasing abscisic acid and jasmonic acid contents under drought stress journal January 2021
Root metabolism in the black mangrove (Avicennia germinans (L.) L): Response to hypoxia journal April 1987
Molecular genetics and physiology of alcohol dehydrogenase in woody plants journal October 1991
Enhancement of Submergence Tolerance in Transgenic Rice Overproducing Pyruvate Decarboxylase journal April 2000
Exchange of atmospheric formic and acetic acids with trees and crop plants under controlled chamber and purified air conditions journal May 1998
Factors controlling the emissions of volatile organic acids from leaves of Quercus ilex L. (Holm oak) journal April 1999
Production of hydrogen, ethanol and volatile fatty acids through co-fermentation of macro- and micro-algae journal April 2016
Field evaluation of mixed-seedlings with rice to alleviate flood stress for semi-arid cereals journal October 2016
Rapid flood-induced stomatal closure accompanies xylem sap transportation of root-derived acetaldehyde and ethanol in Forsythia journal November 2008
Aldehyde dehydrogenases in cellular responses to oxidative/electrophilicstress journal March 2013
Hydrodynamics in mangrove prop roots and their physical properties journal June 2015
Endogenous Hypoxia in Lateral Root Primordia Controls Root Architecture by Antagonizing Auxin Signaling in Arabidopsis journal April 2019
Root responses to flooding journal June 2013
A high affinity pyruvate decarboxylase is present in cottonwood leaf veins and petioles: A second source of leaf acetaldehyde emission? journal July 2009
The ALDH gene superfamily of Arabidopsis journal August 2004
Plant responses to hypoxia – is survival a balancing act? journal September 2004
Making sense of low oxygen sensing journal March 2012
Abundant Oxygenates in the Atmosphere:  A Biochemical Perspective journal December 2003
Gas Phase Measurements of Pyruvic Acid and Its Volatile Metabolites journal April 2010
A critical review on methods to measure apoplastic pH in plants journal March 2000
Biogenic Volatile Organic Compounds (VOC): An Overview on Emission, Physiology and Ecology journal January 1999
Exchange of Short-Chain Oxygenated Volatile Organic Compounds (VOCs) between Plants and the Atmosphere: A Compilation of Field and Laboratory Studies journal July 2001
Emissions of volatile organic compounds from Quercus ilex L. measured by Proton Transfer Reaction Mass Spectrometry under different environmental conditions journal August 2000
Spaceborne Measurements of Formic and Acetic Acids: A Global View of the Regional Sources journal February 2020
Acetaldehyde emission by the leaves of trees - correlation with physiological and environmental parameters journal September 2001
Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants journal October 2011
Anaerobic microsites have an unaccounted role in soil carbon stabilization journal November 2017
An apical hypoxic niche sets the pace of shoot meristem activity journal May 2019
The modulation of acetic acid pathway genes in Arabidopsis improves survival under drought stress journal May 2018
Arabidopsis phenotyping reveals the importance of alcohol dehydrogenase and pyruvate decarboxylase for aerobic plant growth journal October 2020
Acetic-acid-induced jasmonate signaling in root enhances drought avoidance in rice journal March 2021
A hybrid inorganic–biological artificial photosynthesis system for energy-efficient food production journal June 2022
Mechanisms of woody-plant mortality under rising drought, CO2 and vapour pressure deficit journal March 2022
Transient releases of acetaldehyde from tree leaves − products of a pyruvate overflow mechanism?: Acetaldehyde emissions from tree leaves journal August 2002
Anoxia tolerance in tobacco roots: effect of overexpression of pyruvate decarboxylase journal May 1998
The ethanolic fermentation pathway supports respiration and lipid biosynthesis in tobacco pollen journal May 2002
Aerenchyma formation: Tansley review journal October 2003
Interaction of Flooding with Carbon Metabolism of Forest Trees journal May 2004
Low-oxygen response is triggered by an ATP-dependent shift in oleoyl-CoA in Arabidopsis journal December 2018
Intermediate-scale horizontal isoprene concentrations in the near-canopy forest atmosphere and implications for emission heterogeneity journal September 2019
Presence of acetone and acetoacetate decarboxylase in soybean moot nodules journal December 1993
Fermentative and Photochemical Production of Hydrogen in Algae journal November 1942
Ethanol Accumulation in Drought‐Stressed Conifer Seedlings journal March 2008
Regulation of Photosynthesis of C3 Plants in Response to Progressive Drought: Stomatal Conductance as a Reference Parameter journal June 2002
The crucial role of plant mitochondria in orchestrating drought tolerance journal June 2008
Submerged in darkness: adaptations to prolonged submergence by woody species of the Amazonian floodplains journal November 2008
Stem hypertrophic lenticels and secondary aerenchyma enable oxygen transport to roots of soybean in flooded soil journal August 2010
Metabolic origin of acetaldehyde emitted by poplar (Populus tremula x (P. alba) trees journal June 1999
Effects of carbon dioxide and oxygen on sapwood respiration in five temperate tree species journal March 2007
Conservation of ethanol fermentation and its regulation in land plants journal February 2019
Xylan O-Acetylation Impacts Xylem Development and Enzymatic Recalcitrance as Indicated by the Arabidopsis Mutant tbl29 journal July 2013
Plant Adaptations to Anaerobic Stress journal January 1997
Ethanol-Mediated Novel Survival Strategy against Drought Stress in Plants journal August 2022
The Four Arabidopsis REDUCED WALL ACETYLATION Genes are Expressed in Secondary Wall-Containing Cells and Required for the Acetylation of Xylan journal June 2011
Exogenous application of acetic acid enhances drought tolerance by influencing the MAPK signaling pathway induced by ABA and JA in apple plants journal March 2022
Metabolism of Transpired Ethanol by Eastern Cottonwood (Populus deltoides Bartr.) journal May 1993
Enhanced Low Oxygen Survival in Arabidopsis through Increased Metabolic Flux in the Fermentative Pathway journal July 2003
Hypoxic Induction of Anoxia Tolerance in Roots of Adh1 Null Zea mays L journal May 1994
The Role of Acetyl-Coenzyme A Synthetase in Arabidopsis journal June 2008
Regulation of Respiration and Fermentation to Control the Plant Internal Oxygen Concentration journal December 2008
Reduced Wall Acetylation Proteins Play Vital and Distinct Roles in Cell Wall O -Acetylation in Arabidopsis journal September 2013
ATP Production by Respiration and Fermentation, and Energy Charge during Aerobiosis and Anaerobiosis in Twelve Fatty and Starchy Germinating Seeds journal November 1985
Acetaldehyde and Ethanol Biosynthesis in Leaves of Plants journal August 1987
Alcohol Dehydrogenase and Pyruvate Decarboxylase Activity in Leaves and Roots of Eastern Cottonwood (Populus deltoides Bartr.) and Soybean (Glycine max L.) journal August 1987
Alcohol Dehydrogenase and Ethanol in the Stems of Trees journal July 1988
Hypoxic Stress-Induced Changes in Ribosomes of Maize Seedling Roots journal November 1990
Stimulation of isoprene emissions and electron transport rates as key mechanisms of thermal tolerance in the tropical species Vismia guianensis journal July 2020
Assimilation exceeds respiration sensitivity to drought: A FLUXNET synthesis journal February 2010
Flooding induced emissions of volatile signalling compounds in three tree species with differing waterlogging tolerance journal April 2010
The plant ADH gene family: The plant ADH gene family journal March 2011
Emerging concept for the role of photorespiration as an important part of abiotic stress response journal March 2013
Response of Sorghum to Abiotic Stresses: A Review journal December 2012
High temperature causes negative whole-plant carbon balance under mild drought journal July 2013
Core principles which explain variation in respiration across biological scales journal December 2018
Molecular oxygen as a signaling component in plant development journal February 2020
Phytogenic biosynthesis and emission of methyl acetate: Phytogenic methyl acetate journal August 2013
The future of isoprene emission from leaves, canopies and landscapes: The future of isoprene emission journal March 2014
Molecular and physiological responses of trees to waterlogging stress: Responses of tree to waterlogging journal April 2014
Effects of heat and drought stress on post-illumination bursts of volatile organic compounds in isoprene-emitting and non-emitting poplar: Post-illumination bursts in poplar journal January 2016
Cell wall ester modifications and volatile emission signatures of plant response to abiotic stress journal October 2022
Analysis of the role of the pyruvate decarboxylase gene family inArabidopsis thalianaunder low-oxygen conditions journal April 2013
Stem metabolism under drought stress – a paradox of increasing respiratory substrates and decreasing respiratory rates journal July 2020
Acetic acid improves drought acclimation in soybean: an integrative response of photosynthesis, osmoregulation, mineral uptake and antioxidant defense journal October 2020
Acetone-butanol fermentation revisited. journal January 1986
Organization and Regulation of Mitochondrial Respiration in Plants journal June 2011
The roles of aldehyde dehydrogenases (ALDHs) in the PDH bypass of Arabidopsis journal March 2009
Cell wall O-acetyl and methyl esterification patterns of leaves reflected in atmospheric emission signatures of acetic acid and methanol journal May 2020
Fermentation metabolism and its evolution in algae journal January 2013
Acetic Acid Treatment Enhances Drought Avoidance in Cassava (Manihot esculenta Crantz) journal April 2019
Histone Acetylation Dynamics Integrates Metabolic Activity to Regulate Plant Response to Stress journal October 2019
Balanced Xylan Acetylation is the Key Regulator of Plant Growth and Development, and Cell Wall Structure and for Industrial Utilization journal October 2020
Plant Morphological, Physiological and Anatomical Adaption to Flooding Stress and the Underlying Molecular Mechanisms journal January 2021
Are Methanol-Derived Foliar Methyl Acetate Emissions a Tracer of Acetate-Mediated Drought Survival in Plants? journal February 2021
Light-Dependence of Formate (C1) and Acetate (C2) Transport and Oxidation in Poplar Trees journal August 2022
Green Leaf Volatile Emissions during High Temperature and Drought Stress in a Central Amazon Rainforest journal September 2015
What Makes Adventitious Roots? journal July 2019
Vertical Profile of Ozone and Accompanying Air Pollutant Concentrations Observed at a Downwind Foothill Site of Industrial and Urban Areas journal January 2009
Volatile organic compound emissions from Larrea tridentata (creosotebush) journal January 2010
Emissions and ambient distributions of Biogenic Volatile Organic Compounds (BVOC) in a ponderosa pine ecosystem: interpretation of PTR-MS mass spectra journal January 2010
Eddy covariance emission and deposition flux measurements using proton transfer reaction – time of flight – mass spectrometry (PTR-TOF-MS): comparison with PTR-MS measured vertical gradients and fluxes journal January 2013
A multi-purpose, multi-rotor drone system for long-range and high-altitude volcanic gas plume measurements journal June 2021
The effect of flooding on the exchange of the volatile C2-compounds ethanol, acetaldehyde and acetic acid between leaves of Amazonian floodplain tree species and the atmosphere journal January 2008
Ecosystem-scale compensation points of formic and acetic acid in the central Amazon journal January 2011