Cargando…

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

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 a...

Descripción completa

Detalles Bibliográficos
Autores principales: Jardine, Kolby J., Dewhirst, Rebecca A., Som, Suman, Lei, Joseph, Tucker, Eliana, Young, Robert P., Portillo‐Estrada, Miguel, Gao, Yu, Su, Luping, Fares, Silvano, Castanha, Cristina, Scheller, Henrik V., Mortimer, Jenny C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9828120/
https://www.ncbi.nlm.nih.gov/pubmed/36222152
http://dx.doi.org/10.1111/pce.14464
_version_ 1784867200394330112
author Jardine, Kolby J.
Dewhirst, Rebecca A.
Som, Suman
Lei, Joseph
Tucker, Eliana
Young, Robert P.
Portillo‐Estrada, Miguel
Gao, Yu
Su, Luping
Fares, Silvano
Castanha, Cristina
Scheller, Henrik V.
Mortimer, Jenny C.
author_facet Jardine, Kolby J.
Dewhirst, Rebecca A.
Som, Suman
Lei, Joseph
Tucker, Eliana
Young, Robert P.
Portillo‐Estrada, Miguel
Gao, Yu
Su, Luping
Fares, Silvano
Castanha, Cristina
Scheller, Henrik V.
Mortimer, Jenny C.
author_sort Jardine, Kolby J.
collection PubMed
description 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 (13)C(2)‐labelled following the delivery of (13)C(2)‐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.
format Online
Article
Text
id pubmed-9828120
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher John Wiley and Sons Inc.
record_format MEDLINE/PubMed
spelling pubmed-98281202023-01-10 Cell wall ester modifications and volatile emission signatures of plant response to abiotic stress Jardine, Kolby J. Dewhirst, Rebecca A. Som, Suman Lei, Joseph Tucker, Eliana Young, Robert P. Portillo‐Estrada, Miguel Gao, Yu Su, Luping Fares, Silvano Castanha, Cristina Scheller, Henrik V. Mortimer, Jenny C. Plant Cell Environ Original Articles 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 (13)C(2)‐labelled following the delivery of (13)C(2)‐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. John Wiley and Sons Inc. 2022-10-20 2022-12 /pmc/articles/PMC9828120/ /pubmed/36222152 http://dx.doi.org/10.1111/pce.14464 Text en © 2022 The Authors. Plant, Cell & Environment published by John Wiley & Sons Ltd. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
spellingShingle Original Articles
Jardine, Kolby J.
Dewhirst, Rebecca A.
Som, Suman
Lei, Joseph
Tucker, Eliana
Young, Robert P.
Portillo‐Estrada, Miguel
Gao, Yu
Su, Luping
Fares, Silvano
Castanha, Cristina
Scheller, Henrik V.
Mortimer, Jenny C.
Cell wall ester modifications and volatile emission signatures of plant response to abiotic stress
title Cell wall ester modifications and volatile emission signatures of plant response to abiotic stress
title_full Cell wall ester modifications and volatile emission signatures of plant response to abiotic stress
title_fullStr Cell wall ester modifications and volatile emission signatures of plant response to abiotic stress
title_full_unstemmed Cell wall ester modifications and volatile emission signatures of plant response to abiotic stress
title_short Cell wall ester modifications and volatile emission signatures of plant response to abiotic stress
title_sort cell wall ester modifications and volatile emission signatures of plant response to abiotic stress
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9828120/
https://www.ncbi.nlm.nih.gov/pubmed/36222152
http://dx.doi.org/10.1111/pce.14464
work_keys_str_mv AT jardinekolbyj cellwallestermodificationsandvolatileemissionsignaturesofplantresponsetoabioticstress
AT dewhirstrebeccaa cellwallestermodificationsandvolatileemissionsignaturesofplantresponsetoabioticstress
AT somsuman cellwallestermodificationsandvolatileemissionsignaturesofplantresponsetoabioticstress
AT leijoseph cellwallestermodificationsandvolatileemissionsignaturesofplantresponsetoabioticstress
AT tuckereliana cellwallestermodificationsandvolatileemissionsignaturesofplantresponsetoabioticstress
AT youngrobertp cellwallestermodificationsandvolatileemissionsignaturesofplantresponsetoabioticstress
AT portilloestradamiguel cellwallestermodificationsandvolatileemissionsignaturesofplantresponsetoabioticstress
AT gaoyu cellwallestermodificationsandvolatileemissionsignaturesofplantresponsetoabioticstress
AT suluping cellwallestermodificationsandvolatileemissionsignaturesofplantresponsetoabioticstress
AT faressilvano cellwallestermodificationsandvolatileemissionsignaturesofplantresponsetoabioticstress
AT castanhacristina cellwallestermodificationsandvolatileemissionsignaturesofplantresponsetoabioticstress
AT schellerhenrikv cellwallestermodificationsandvolatileemissionsignaturesofplantresponsetoabioticstress
AT mortimerjennyc cellwallestermodificationsandvolatileemissionsignaturesofplantresponsetoabioticstress