Combined Drought and Heat Activates Protective Responses in Eucalyptus globulus That Are Not Activated When Subjected to Drought or Heat Stress Alone

Aiming to mimic a more realistic field condition and to determine convergent and divergent responses of individual stresses in relation to their combination, we explored physiological, biochemical, and metabolomic alterations after drought and heat stress imposition (alone and combined) and recovery...

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Published inFrontiers in plant science Vol. 9; p. 819
Main Authors Correia, Barbara, Hancock, Robert D., Amaral, Joana, Gomez-Cadenas, Aurelio, Valledor, Luis, Pinto, Glória
Format Journal Article
LanguageEnglish
Published Switzerland Frontiers Media S.A 20.06.2018
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Abstract Aiming to mimic a more realistic field condition and to determine convergent and divergent responses of individual stresses in relation to their combination, we explored physiological, biochemical, and metabolomic alterations after drought and heat stress imposition (alone and combined) and recovery, using a drought-tolerant clone. When plants were exposed to drought alone, the main responses included reduced pre-dawn water potential (Ψ ) and gas exchange. This was accompanied by increases in malondialdehyde (MDA) and total glutathione, indicative of oxidative stress. Abscisic acid (ABA) levels increased while the content of jasmonic acid (JA) fell. Metabolic alterations included reductions in the levels of sugar phosphates accompanied by increases in starch and non-structural carbohydrates. Levels of α-glycerophosphate and shikimate were also reduced while free amino acids increased. On the other hand, heat alone triggered an increase in relative water content (RWC) and Ψ . Photosynthetic rate and pigments were reduced accompanied by a reduction in water use efficiency. Heat-induced a reduction of salicylic acid (SA) and JA content. Sugar alcohols and several amino acids were enhanced by the heat treatment while starch, fructose-6-phosphate, glucose-6-phosphate, and α-glycerophosphate were reduced. Contrary to what was observed under drought, heat stress activated the shikimic acid pathway. Drought-stressed plants subject to a heat shock exhibited a sharp decrease in gas exchange, Ψ and JA, no alterations in electrolyte leakage, MDA, starch, and pigments and increased glutathione pool in relation to control. Comparing this with drought stress alone, subjecting drought stressed plants to an additional heat stress alleviated Ψ and MDA, maintained an increased glutathione pool and reduced starch content and non-structural carbohydrates. A novel response triggered by the combined stress was the accumulation of cinnamate. Regarding recovery, most of the parameters affected by each stress condition reversed after re-establishment of control growing conditions. These results highlight that the combination of drought and heat provides significant protection from more detrimental effects of drought-stressed eucalypts, confirming that combined stress alter plant metabolism in a novel manner that cannot be extrapolated by the sum of the different stresses applied individually.
AbstractList Aiming to mimic a more realistic field condition and to determine convergent and divergent responses of individual stresses in relation to their combination, we explored physiological, biochemical, and metabolomic alterations after drought and heat stress imposition (alone and combined) and recovery, using a drought-tolerant clone. When plants were exposed to drought alone, the main responses included reduced pre-dawn water potential (Ψ ) and gas exchange. This was accompanied by increases in malondialdehyde (MDA) and total glutathione, indicative of oxidative stress. Abscisic acid (ABA) levels increased while the content of jasmonic acid (JA) fell. Metabolic alterations included reductions in the levels of sugar phosphates accompanied by increases in starch and non-structural carbohydrates. Levels of α-glycerophosphate and shikimate were also reduced while free amino acids increased. On the other hand, heat alone triggered an increase in relative water content (RWC) and Ψ . Photosynthetic rate and pigments were reduced accompanied by a reduction in water use efficiency. Heat-induced a reduction of salicylic acid (SA) and JA content. Sugar alcohols and several amino acids were enhanced by the heat treatment while starch, fructose-6-phosphate, glucose-6-phosphate, and α-glycerophosphate were reduced. Contrary to what was observed under drought, heat stress activated the shikimic acid pathway. Drought-stressed plants subject to a heat shock exhibited a sharp decrease in gas exchange, Ψ and JA, no alterations in electrolyte leakage, MDA, starch, and pigments and increased glutathione pool in relation to control. Comparing this with drought stress alone, subjecting drought stressed plants to an additional heat stress alleviated Ψ and MDA, maintained an increased glutathione pool and reduced starch content and non-structural carbohydrates. A novel response triggered by the combined stress was the accumulation of cinnamate. Regarding recovery, most of the parameters affected by each stress condition reversed after re-establishment of control growing conditions. These results highlight that the combination of drought and heat provides significant protection from more detrimental effects of drought-stressed eucalypts, confirming that combined stress alter plant metabolism in a novel manner that cannot be extrapolated by the sum of the different stresses applied individually.
Aiming to mimic a more realistic field condition and to determine convergent and divergent responses of individual stresses in relation to their combination, we explored physiological, biochemical, and metabolomic alterations after drought and heat stress imposition (alone and combined) and recovery, using a drought-tolerant Eucalyptus globulus clone. When plants were exposed to drought alone, the main responses included reduced pre-dawn water potential (Ψ pd ) and gas exchange. This was accompanied by increases in malondialdehyde (MDA) and total glutathione, indicative of oxidative stress. Abscisic acid (ABA) levels increased while the content of jasmonic acid (JA) fell. Metabolic alterations included reductions in the levels of sugar phosphates accompanied by increases in starch and non-structural carbohydrates. Levels of α-glycerophosphate and shikimate were also reduced while free amino acids increased. On the other hand, heat alone triggered an increase in relative water content (RWC) and Ψ pd . Photosynthetic rate and pigments were reduced accompanied by a reduction in water use efficiency. Heat-induced a reduction of salicylic acid (SA) and JA content. Sugar alcohols and several amino acids were enhanced by the heat treatment while starch, fructose-6-phosphate, glucose-6-phosphate, and α-glycerophosphate were reduced. Contrary to what was observed under drought, heat stress activated the shikimic acid pathway. Drought-stressed plants subject to a heat shock exhibited a sharp decrease in gas exchange, Ψ pd and JA, no alterations in electrolyte leakage, MDA, starch, and pigments and increased glutathione pool in relation to control. Comparing this with drought stress alone, subjecting drought stressed plants to an additional heat stress alleviated Ψ pd and MDA, maintained an increased glutathione pool and reduced starch content and non-structural carbohydrates. A novel response triggered by the combined stress was the accumulation of cinnamate. Regarding recovery, most of the parameters affected by each stress condition reversed after re-establishment of control growing conditions. These results highlight that the combination of drought and heat provides significant protection from more detrimental effects of drought-stressed eucalypts, confirming that combined stress alter plant metabolism in a novel manner that cannot be extrapolated by the sum of the different stresses applied individually.
Aiming to mimic a more realistic field condition and to determine convergent and divergent responses of individual stresses in relation to their combination, we explored physiological, biochemical, and metabolomic alterations after drought and heat stress imposition (alone and combined) and recovery, using a drought-tolerant Eucalyptus globulus clone. When plants were exposed to drought alone, the main responses included reduced pre-dawn water potential (Ψpd) and gas exchange. This was accompanied by increases in malondialdehyde (MDA) and total glutathione, indicative of oxidative stress. Abscisic acid (ABA) levels increased while the content of jasmonic acid (JA) fell. Metabolic alterations included reductions in the levels of sugar phosphates accompanied by increases in starch and non-structural carbohydrates. Levels of α-glycerophosphate and shikimate were also reduced while free amino acids increased. On the other hand, heat alone triggered an increase in relative water content (RWC) and Ψpd. Photosynthetic rate and pigments were reduced accompanied by a reduction in water use efficiency. Heat-induced a reduction of salicylic acid (SA) and JA content. Sugar alcohols and several amino acids were enhanced by the heat treatment while starch, fructose-6-phosphate, glucose-6-phosphate, and α-glycerophosphate were reduced. Contrary to what was observed under drought, heat stress activated the shikimic acid pathway. Drought-stressed plants subject to a heat shock exhibited a sharp decrease in gas exchange, Ψpd and JA, no alterations in electrolyte leakage, MDA, starch, and pigments and increased glutathione pool in relation to control. Comparing this with drought stress alone, subjecting drought stressed plants to an additional heat stress alleviated Ψpd and MDA, maintained an increased glutathione pool and reduced starch content and non-structural carbohydrates. A novel response triggered by the combined stress was the accumulation of cinnamate. Regarding recovery, most of the parameters affected by each stress condition reversed after re-establishment of control growing conditions. These results highlight that the combination of drought and heat provides significant protection from more detrimental effects of drought-stressed eucalypts, confirming that combined stress alter plant metabolism in a novel manner that cannot be extrapolated by the sum of the different stresses applied individually.Aiming to mimic a more realistic field condition and to determine convergent and divergent responses of individual stresses in relation to their combination, we explored physiological, biochemical, and metabolomic alterations after drought and heat stress imposition (alone and combined) and recovery, using a drought-tolerant Eucalyptus globulus clone. When plants were exposed to drought alone, the main responses included reduced pre-dawn water potential (Ψpd) and gas exchange. This was accompanied by increases in malondialdehyde (MDA) and total glutathione, indicative of oxidative stress. Abscisic acid (ABA) levels increased while the content of jasmonic acid (JA) fell. Metabolic alterations included reductions in the levels of sugar phosphates accompanied by increases in starch and non-structural carbohydrates. Levels of α-glycerophosphate and shikimate were also reduced while free amino acids increased. On the other hand, heat alone triggered an increase in relative water content (RWC) and Ψpd. Photosynthetic rate and pigments were reduced accompanied by a reduction in water use efficiency. Heat-induced a reduction of salicylic acid (SA) and JA content. Sugar alcohols and several amino acids were enhanced by the heat treatment while starch, fructose-6-phosphate, glucose-6-phosphate, and α-glycerophosphate were reduced. Contrary to what was observed under drought, heat stress activated the shikimic acid pathway. Drought-stressed plants subject to a heat shock exhibited a sharp decrease in gas exchange, Ψpd and JA, no alterations in electrolyte leakage, MDA, starch, and pigments and increased glutathione pool in relation to control. Comparing this with drought stress alone, subjecting drought stressed plants to an additional heat stress alleviated Ψpd and MDA, maintained an increased glutathione pool and reduced starch content and non-structural carbohydrates. A novel response triggered by the combined stress was the accumulation of cinnamate. Regarding recovery, most of the parameters affected by each stress condition reversed after re-establishment of control growing conditions. These results highlight that the combination of drought and heat provides significant protection from more detrimental effects of drought-stressed eucalypts, confirming that combined stress alter plant metabolism in a novel manner that cannot be extrapolated by the sum of the different stresses applied individually.
Aiming to mimic a more realistic field condition and to determine convergent and divergent responses of individual stresses in relation to their combination, we explored physiological, biochemical, and metabolomic alterations after drought and heat stress imposition (alone and combined) and recovery, using a drought-tolerant Eucalyptus globulus clone. When plants were exposed to drought alone, the main responses included reduced pre-dawn water potential (Ψpd) and gas exchange. This was accompanied by increases in malondialdehyde (MDA) and total glutathione, indicative of oxidative stress. Abscisic acid (ABA) levels increased while the content of jasmonic acid (JA) fell. Metabolic alterations included reductions in the levels of sugar phosphates accompanied by increases in starch and non-structural carbohydrates. Levels of α-glycerophosphate and shikimate were also reduced while free amino acids increased. On the other hand, heat alone triggered an increase in relative water content (RWC) and Ψpd. Photosynthetic rate and pigments were reduced accompanied by a reduction in water use efficiency. Heat-induced a reduction of salicylic acid (SA) and JA content. Sugar alcohols and several amino acids were enhanced by the heat treatment while starch, fructose-6-phosphate, glucose-6-phosphate, and α-glycerophosphate were reduced. Contrary to what was observed under drought, heat stress activated the shikimic acid pathway. Drought-stressed plants subject to a heat shock exhibited a sharp decrease in gas exchange, Ψpd and JA, no alterations in electrolyte leakage, MDA, starch, and pigments and increased glutathione pool in relation to control. Comparing this with drought stress alone, subjecting drought stressed plants to an additional heat stress alleviated Ψpd and MDA, maintained an increased glutathione pool and reduced starch content and non-structural carbohydrates. A novel response triggered by the combined stress was the accumulation of cinnamate. Regarding recovery, most of the parameters affected by each stress condition reversed after re-establishment of control growing conditions. These results highlight that the combination of drought and heat provides significant protection from more detrimental effects of drought-stressed eucalypts, confirming that combined stress alter plant metabolism in a novel manner that cannot be extrapolated by the sum of the different stresses applied individually.
Author Valledor, Luis
Gomez-Cadenas, Aurelio
Pinto, Glória
Amaral, Joana
Correia, Barbara
Hancock, Robert D.
AuthorAffiliation 2 Cell and Molecular Sciences, The James Hutton Institute , Dundee , United Kingdom
4 Department of Organisms and Systems Biology, University of Oviedo , Oviedo , Spain
3 Departamento de Ciencias Agrarias y del Medio Natural, Universitat Jaume I , Castellón de la Plana , Spain
1 Department of Biology, Centre for Environmental and Marine Studies, University of Aveiro , Aveiro , Portugal
AuthorAffiliation_xml – name: 3 Departamento de Ciencias Agrarias y del Medio Natural, Universitat Jaume I , Castellón de la Plana , Spain
– name: 2 Cell and Molecular Sciences, The James Hutton Institute , Dundee , United Kingdom
– name: 1 Department of Biology, Centre for Environmental and Marine Studies, University of Aveiro , Aveiro , Portugal
– name: 4 Department of Organisms and Systems Biology, University of Oviedo , Oviedo , Spain
Author_xml – sequence: 1
  givenname: Barbara
  surname: Correia
  fullname: Correia, Barbara
– sequence: 2
  givenname: Robert D.
  surname: Hancock
  fullname: Hancock, Robert D.
– sequence: 3
  givenname: Joana
  surname: Amaral
  fullname: Amaral, Joana
– sequence: 4
  givenname: Aurelio
  surname: Gomez-Cadenas
  fullname: Gomez-Cadenas, Aurelio
– sequence: 5
  givenname: Luis
  surname: Valledor
  fullname: Valledor, Luis
– sequence: 6
  givenname: Glória
  surname: Pinto
  fullname: Pinto, Glória
BackLink https://www.ncbi.nlm.nih.gov/pubmed/29973941$$D View this record in MEDLINE/PubMed
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Keywords isolated stress
combined stress
network analysis
recovery
plant metabolism
Language English
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This article was submitted to Plant Systems and Synthetic Biology, a section of the journal Frontiers in Plant Science
Reviewed by: Ernani Pinto, Universidade de São Paulo, Brazil; Carlos Alberto Labate, Universidade de São Paulo, Brazil; Kris Morreel, Flemish Institute for Technological Research, Belgium
Edited by: Atsushi Fukushima, RIKEN, Japan
These authors have contributed equally to this work.
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24372529 - Plant Cell Environ. 2014 Jul;37(7):1598-613
23986766 - Front Plant Sci. 2013 Aug 23;4:315
27121193 - BMC Plant Biol. 2016 Apr 27;16:105
17288982 - Anal Biochem. 2007 Apr 1;363(1):58-69
19083153 - Plant Mol Biol. 2009 Mar;69(4):473-88
15377388 - BMC Plant Biol. 2004 Sep 17;4:17
12102516 - Ann Bot. 2002 Jun;89 Spec No:907-16
20417989 - J Plant Physiol. 2010 Sep 15;167(14):1157-64
24954071 - Plant Physiol Biochem. 2014 Sep;82:151-60
16359910 - Trends Plant Sci. 2006 Jan;11(1):15-9
12242399 - Plant Cell. 1995 Jul;7(7):1085-1097
26442037 - Front Plant Sci. 2015 Sep 16;6:723
23889235 - Plant Cell Environ. 2014 Feb;37(2):439-50
16040710 - Science. 2005 Jul 22;309(5734):630-3
27001437 - Mol Cell Proteomics. 2016 Jun;15(6):1921-37
23677117 - Tree Physiol. 2013 May;33(5):447-50
15923322 - Plant Physiol. 2005 Jun;138(2):882-97
14513379 - Planta. 2003 Nov;218(1):1-14
23525156 - Tree Physiol. 2013 May;33(5):451-63
22467407 - J Exp Bot. 2012 Jun;63(10):3523-43
28042678 - Physiol Plant. 2018 Jan;162(1):2-12
26764270 - Tree Physiol. 2016 Jan;36(1):63-77
26442017 - Front Plant Sci. 2015 Sep 10;6:701
26371234 - Plant Physiol. 2015 Nov;169(3):1499-511
26902148 - Sci Rep. 2016 Feb 23;6:21843
20554469 - Trends Plant Sci. 2010 Aug;15(8):462-70
16248534 - J Agric Food Chem. 2005 Nov 2;53(22):8437-42
20619485 - J Plant Physiol. 2010 Nov 1;167(16):1360-70
24256338 - BMC Plant Biol. 2013 Nov 20;13:184
22776350 - Plant Biol (Stuttg). 2013 Jan;15 Suppl 1:169-76
22167807 - Proc Natl Acad Sci U S A. 2012 Jan 3;109(1):233-7
26424159 - Plant Physiol. 2015 Dec;169(4):2665-83
12427981 - Plant Physiol. 2002 Nov;130(3):1143-51
16773557 - Plant Biol (Stuttg). 2006 Sep;8(5):556-71
21692813 - Plant Cell Environ. 2011 Oct;34(10):1609-29
28456836 - Planta. 2017 Jun;245(6):1067
19011001 - Plant Physiol. 2009 Jan;149(1):575-84
20192746 - Annu Rev Plant Biol. 2010;61:443-62
25502480 - Planta. 2015 Apr;241(4):803-22
18662937 - Ann Bot. 2009 Feb;103(4):551-60
24117924 - Physiol Plant. 2014 Apr;150(4):580-92
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Snippet Aiming to mimic a more realistic field condition and to determine convergent and divergent responses of individual stresses in relation to their combination,...
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pubmedcentral
proquest
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crossref
SourceType Open Website
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Aggregation Database
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StartPage 819
SubjectTerms combined stress
isolated stress
network analysis
plant metabolism
Plant Science
recovery
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Title Combined Drought and Heat Activates Protective Responses in Eucalyptus globulus That Are Not Activated When Subjected to Drought or Heat Stress Alone
URI https://www.ncbi.nlm.nih.gov/pubmed/29973941
https://www.proquest.com/docview/2064766523
https://pubmed.ncbi.nlm.nih.gov/PMC6019450
https://doaj.org/article/473c0d8dad5d42aa9c21030bac8f84b8
Volume 9
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