Tolerance of citrus plants to the combination of high temperatures and drought is associated to the increase in transpiration modulated by a reduction in abscisic acid levels
Identifieur interne : 000018 ( Pmc/Checkpoint ); précédent : 000017; suivant : 000019Tolerance of citrus plants to the combination of high temperatures and drought is associated to the increase in transpiration modulated by a reduction in abscisic acid levels
Auteurs : Sara I. Zandalinas [Espagne] ; Rosa M. Rivero [Espagne] ; Vicente Martínez [Espagne] ; Aurelio G Mez-Cadenas [Espagne] ; Vicent Arbona [Espagne]Source :
- BMC Plant Biology [ 1471-2229 ] ; 2016.
Abstract
In natural environments, several adverse environmental conditions occur simultaneously constituting a unique stress factor. In this work, physiological parameters and the hormonal regulation of Carrizo citrange and Cleopatra mandarin, two citrus genotypes, in response to the combined action of high temperatures and water deprivation were studied. The objective was to characterize particular responses to the stress combination.
Experiments indicated that Carrizo citrange is more tolerant to the stress combination than Cleopatra mandarin. Furthermore, an experimental design spanning 24 h stress duration, heat stress applied alone induced higher stomatal conductance and transpiration in both genotypes whereas combined water deprivation partially counteracted this response. Comparing both genotypes, Carrizo citrange showed higher phostosystem-II efficiency and lower oxidative damage than Cleopatra mandarin. Hormonal profiling in leaves revealed that salicylic acid (SA) accumulated in response to individual stresses but to a higher extent in samples subjected to the combination of heat and drought (showing an additive response). SA accumulation correlated with the up-regulation of pathogenesis-related gene 2 (CsPR2), as a downstream response. On the contrary, abscisic acid (ABA) accumulation was higher in water-stressed plants followed by that observed in plants under stress combination. ABA signaling in these plants was confirmed by the expression of responsive to ABA-related gene 18 (CsRAB18). Modulation of ABA levels was likely carried out by the induction of 9-neoxanthin cis-epoxicarotenoid dioxygenase (CsNCED) and ABA 8’-hydroxylase (CsCYP707A) while conversion to ABA-glycosyl ester (ABAGE) was a less prominent process despite the strong induction of ABA O-glycosyl transferase (CsAOG).
Cleopatra mandarin is more susceptible to the combination of high temperatures and water deprivation than Carrizo citrange. This is likely a result of a higher transpiration rate in Carrizo that could allow a more efficient cooling of leaf surface ensuring optimal CO2 intake. Hence, SA induction in Cleopatra was not sufficient to protect PSII from photoinhibition, resulting in higher malondialdehyde (MDA) build-up. Inhibition of ABA accumulation during heat stress and combined stresses was achieved primarily through the up-regulation of CsCYP707A leading to phaseic acid (PA) and dehydrophaseic acid (DPA) production. To sum up, data indicate that specific physiological responses to the combination of heat and drought exist in citrus. In addition, these responses are differently modulated depending on the particular stress tolerance of citrus genotypes.
The online version of this article (doi:10.1186/s12870-016-0791-7) contains supplementary material, which is available to authorized users.
Url:
DOI: 10.1186/s12870-016-0791-7
PubMed: 27121193
PubMed Central: 4848825
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Tolerance of citrus plants to the combination of high temperatures and drought is associated to the increase in transpiration modulated by a reduction in abscisic acid levels</title><author><name sortKey="Zandalinas, Sara I" sort="Zandalinas, Sara I" uniqKey="Zandalinas S" first="Sara I." last="Zandalinas">Sara I. Zandalinas</name><affiliation wicri:level="2"><nlm:aff id="Aff1">Department Ciències Agràries i del Medi Natural, Universitat Jaume I, E-12071 Castelló de la Plana, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Department Ciències Agràries i del Medi Natural, Universitat Jaume I, E-12071 Castelló de la Plana</wicri:regionArea><placeName><region nuts="2" type="communauté">Communauté valencienne</region></placeName></affiliation></author><author><name sortKey="Rivero, Rosa M" sort="Rivero, Rosa M" uniqKey="Rivero R" first="Rosa M." last="Rivero">Rosa M. Rivero</name><affiliation wicri:level="2"><nlm:aff id="Aff2">Departament de Nutrición Vegetal, Centro de Edafología Aplicada del Segura, Consejo Superior de Investigaciones Científicas, 30100 Murcia, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Departament de Nutrición Vegetal, Centro de Edafología Aplicada del Segura, Consejo Superior de Investigaciones Científicas, 30100 Murcia</wicri:regionArea><placeName><region nuts="2" type="communauté">Région de Murcie</region></placeName></affiliation></author><author><name sortKey="Martinez, Vicente" sort="Martinez, Vicente" uniqKey="Martinez V" first="Vicente" last="Martínez">Vicente Martínez</name><affiliation wicri:level="2"><nlm:aff id="Aff2">Departament de Nutrición Vegetal, Centro de Edafología Aplicada del Segura, Consejo Superior de Investigaciones Científicas, 30100 Murcia, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Departament de Nutrición Vegetal, Centro de Edafología Aplicada del Segura, Consejo Superior de Investigaciones Científicas, 30100 Murcia</wicri:regionArea><placeName><region nuts="2" type="communauté">Région de Murcie</region></placeName></affiliation></author><author><name sortKey="G Mez Cadenas, Aurelio" sort="G Mez Cadenas, Aurelio" uniqKey="G Mez Cadenas A" first="Aurelio" last="G Mez-Cadenas">Aurelio G Mez-Cadenas</name><affiliation wicri:level="2"><nlm:aff id="Aff1">Department Ciències Agràries i del Medi Natural, Universitat Jaume I, E-12071 Castelló de la Plana, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Department Ciències Agràries i del Medi Natural, Universitat Jaume I, E-12071 Castelló de la Plana</wicri:regionArea><placeName><region nuts="2" type="communauté">Communauté valencienne</region></placeName></affiliation></author><author><name sortKey="Arbona, Vicent" sort="Arbona, Vicent" uniqKey="Arbona V" first="Vicent" last="Arbona">Vicent Arbona</name><affiliation wicri:level="2"><nlm:aff id="Aff1">Department Ciències Agràries i del Medi Natural, Universitat Jaume I, E-12071 Castelló de la Plana, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Department Ciències Agràries i del Medi Natural, Universitat Jaume I, E-12071 Castelló de la Plana</wicri:regionArea><placeName><region nuts="2" type="communauté">Communauté valencienne</region></placeName></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">27121193</idno><idno type="pmc">4848825</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4848825</idno><idno type="RBID">PMC:4848825</idno><idno type="doi">10.1186/s12870-016-0791-7</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000641</idno><idno type="wicri:Area/Pmc/Curation">000640</idno><idno type="wicri:Area/Pmc/Checkpoint">000018</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Tolerance of citrus plants to the combination of high temperatures and drought is associated to the increase in transpiration modulated by a reduction in abscisic acid levels</title><author><name sortKey="Zandalinas, Sara I" sort="Zandalinas, Sara I" uniqKey="Zandalinas S" first="Sara I." last="Zandalinas">Sara I. Zandalinas</name><affiliation wicri:level="2"><nlm:aff id="Aff1">Department Ciències Agràries i del Medi Natural, Universitat Jaume I, E-12071 Castelló de la Plana, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Department Ciències Agràries i del Medi Natural, Universitat Jaume I, E-12071 Castelló de la Plana</wicri:regionArea><placeName><region nuts="2" type="communauté">Communauté valencienne</region></placeName></affiliation></author><author><name sortKey="Rivero, Rosa M" sort="Rivero, Rosa M" uniqKey="Rivero R" first="Rosa M." last="Rivero">Rosa M. Rivero</name><affiliation wicri:level="2"><nlm:aff id="Aff2">Departament de Nutrición Vegetal, Centro de Edafología Aplicada del Segura, Consejo Superior de Investigaciones Científicas, 30100 Murcia, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Departament de Nutrición Vegetal, Centro de Edafología Aplicada del Segura, Consejo Superior de Investigaciones Científicas, 30100 Murcia</wicri:regionArea><placeName><region nuts="2" type="communauté">Région de Murcie</region></placeName></affiliation></author><author><name sortKey="Martinez, Vicente" sort="Martinez, Vicente" uniqKey="Martinez V" first="Vicente" last="Martínez">Vicente Martínez</name><affiliation wicri:level="2"><nlm:aff id="Aff2">Departament de Nutrición Vegetal, Centro de Edafología Aplicada del Segura, Consejo Superior de Investigaciones Científicas, 30100 Murcia, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Departament de Nutrición Vegetal, Centro de Edafología Aplicada del Segura, Consejo Superior de Investigaciones Científicas, 30100 Murcia</wicri:regionArea><placeName><region nuts="2" type="communauté">Région de Murcie</region></placeName></affiliation></author><author><name sortKey="G Mez Cadenas, Aurelio" sort="G Mez Cadenas, Aurelio" uniqKey="G Mez Cadenas A" first="Aurelio" last="G Mez-Cadenas">Aurelio G Mez-Cadenas</name><affiliation wicri:level="2"><nlm:aff id="Aff1">Department Ciències Agràries i del Medi Natural, Universitat Jaume I, E-12071 Castelló de la Plana, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Department Ciències Agràries i del Medi Natural, Universitat Jaume I, E-12071 Castelló de la Plana</wicri:regionArea><placeName><region nuts="2" type="communauté">Communauté valencienne</region></placeName></affiliation></author><author><name sortKey="Arbona, Vicent" sort="Arbona, Vicent" uniqKey="Arbona V" first="Vicent" last="Arbona">Vicent Arbona</name><affiliation wicri:level="2"><nlm:aff id="Aff1">Department Ciències Agràries i del Medi Natural, Universitat Jaume I, E-12071 Castelló de la Plana, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Department Ciències Agràries i del Medi Natural, Universitat Jaume I, E-12071 Castelló de la Plana</wicri:regionArea><placeName><region nuts="2" type="communauté">Communauté valencienne</region></placeName></affiliation></author></analytic><series><title level="j">BMC Plant Biology</title><idno type="eISSN">1471-2229</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p>In natural environments, several adverse environmental conditions occur simultaneously constituting a unique stress factor. In this work, physiological parameters and the hormonal regulation of Carrizo citrange and Cleopatra mandarin, two citrus genotypes, in response to the combined action of high temperatures and water deprivation were studied. The objective was to characterize particular responses to the stress combination.</p></sec><sec><title>Results</title><p>Experiments indicated that Carrizo citrange is more tolerant to the stress combination than Cleopatra mandarin. Furthermore, an experimental design spanning 24 h stress duration, heat stress applied alone induced higher stomatal conductance and transpiration in both genotypes whereas combined water deprivation partially counteracted this response. Comparing both genotypes, Carrizo citrange showed higher phostosystem-II efficiency and lower oxidative damage than Cleopatra mandarin. Hormonal profiling in leaves revealed that salicylic acid (SA) accumulated in response to individual stresses but to a higher extent in samples subjected to the combination of heat and drought (showing an additive response). SA accumulation correlated with the up-regulation of pathogenesis-related gene 2 (CsPR2), as a downstream response. On the contrary, abscisic acid (ABA) accumulation was higher in water-stressed plants followed by that observed in plants under stress combination. ABA signaling in these plants was confirmed by the expression of responsive to ABA-related gene 18 (CsRAB18). Modulation of ABA levels was likely carried out by the induction of 9-neoxanthin cis-epoxicarotenoid dioxygenase (CsNCED) and ABA 8’-hydroxylase (CsCYP707A) while conversion to ABA-glycosyl ester (ABAGE) was a less prominent process despite the strong induction of ABA O-glycosyl transferase (CsAOG).</p></sec><sec><title>Conclusions</title><p>Cleopatra mandarin is more susceptible to the combination of high temperatures and water deprivation than Carrizo citrange. This is likely a result of a higher transpiration rate in Carrizo that could allow a more efficient cooling of leaf surface ensuring optimal CO<sub>2</sub> intake. Hence, SA induction in Cleopatra was not sufficient to protect PSII from photoinhibition, resulting in higher malondialdehyde (MDA) build-up. Inhibition of ABA accumulation during heat stress and combined stresses was achieved primarily through the up-regulation of CsCYP707A leading to phaseic acid (PA) and dehydrophaseic acid (DPA) production. To sum up, data indicate that specific physiological responses to the combination of heat and drought exist in citrus. In addition, these responses are differently modulated depending on the particular stress tolerance of citrus genotypes.</p></sec><sec><title>Electronic supplementary material</title><p>The online version of this article (doi:10.1186/s12870-016-0791-7) contains supplementary material, which is available to authorized users.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Mittler, R" uniqKey="Mittler R">R Mittler</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mittler, R" uniqKey="Mittler R">R Mittler</name></author><author><name sortKey="Blumwald, E" uniqKey="Blumwald E">E Blumwald</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Savin, R" uniqKey="Savin R">R Savin</name></author><author><name sortKey="Nicolas, M" uniqKey="Nicolas M">M Nicolas</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Jiang, Y" uniqKey="Jiang Y">Y 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<front><journal-meta><journal-id journal-id-type="nlm-ta">BMC Plant Biol</journal-id><journal-id journal-id-type="iso-abbrev">BMC Plant Biol</journal-id><journal-title-group><journal-title>BMC Plant Biology</journal-title></journal-title-group><issn pub-type="epub">1471-2229</issn><publisher><publisher-name>BioMed Central</publisher-name><publisher-loc>London</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">27121193</article-id><article-id pub-id-type="pmc">4848825</article-id><article-id pub-id-type="publisher-id">791</article-id><article-id pub-id-type="doi">10.1186/s12870-016-0791-7</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group></article-categories><title-group><article-title>Tolerance of citrus plants to the combination of high temperatures and drought is associated to the increase in transpiration modulated by a reduction in abscisic acid levels</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Zandalinas</surname><given-names>Sara I.</given-names></name><address><email>sizquier@camn.uji.es</email></address><xref ref-type="aff" rid="Aff1"></xref></contrib><contrib contrib-type="author"><name><surname>Rivero</surname><given-names>Rosa M.</given-names></name><address><email>rmrivero@cebas.csic.es</email></address><xref ref-type="aff" rid="Aff2"></xref></contrib><contrib contrib-type="author"><name><surname>Martínez</surname><given-names>Vicente</given-names></name><address><email>vicente@cebas.csic.es</email></address><xref ref-type="aff" rid="Aff2"></xref></contrib><contrib contrib-type="author"><name><surname>Gómez-Cadenas</surname><given-names>Aurelio</given-names></name><address><email>aurelio.gomez@camn.uji.es</email></address><xref ref-type="aff" rid="Aff1"></xref></contrib><contrib contrib-type="author" corresp="yes"><name><surname>Arbona</surname><given-names>Vicent</given-names></name><address><phone>+34 964 72 8101</phone><fax>+34 964 72 8116</fax><email>vicente.arbona@camn.uji.es</email></address><xref ref-type="aff" rid="Aff1"></xref></contrib><aff id="Aff1"><label></label>Department Ciències Agràries i del Medi Natural, Universitat Jaume I, E-12071 Castelló de la Plana, Spain</aff><aff id="Aff2"><label></label>Departament de Nutrición Vegetal, Centro de Edafología Aplicada del Segura, Consejo Superior de Investigaciones Científicas, 30100 Murcia, Spain</aff></contrib-group><pub-date pub-type="epub"><day>27</day><month>4</month><year>2016</year></pub-date><pub-date pub-type="pmc-release"><day>27</day><month>4</month><year>2016</year></pub-date><pub-date pub-type="collection"><year>2016</year></pub-date><volume>16</volume><elocation-id>105</elocation-id><history><date date-type="received"><day>25</day><month>11</month><year>2015</year></date><date date-type="accepted"><day>20</day><month>4</month><year>2016</year></date></history><permissions><copyright-statement>© Zandalinas et al. 2016</copyright-statement><license license-type="OpenAccess"><license-p><bold>Open Access</bold>This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/publicdomain/zero/1.0/">http://creativecommons.org/publicdomain/zero/1.0/</ext-link>) applies to the data made available in this article, unless otherwise stated.</license-p></license></permissions><abstract id="Abs1"><sec><title>Background</title><p>In natural environments, several adverse environmental conditions occur simultaneously constituting a unique stress factor. In this work, physiological parameters and the hormonal regulation of Carrizo citrange and Cleopatra mandarin, two citrus genotypes, in response to the combined action of high temperatures and water deprivation were studied. The objective was to characterize particular responses to the stress combination.</p></sec><sec><title>Results</title><p>Experiments indicated that Carrizo citrange is more tolerant to the stress combination than Cleopatra mandarin. Furthermore, an experimental design spanning 24 h stress duration, heat stress applied alone induced higher stomatal conductance and transpiration in both genotypes whereas combined water deprivation partially counteracted this response. Comparing both genotypes, Carrizo citrange showed higher phostosystem-II efficiency and lower oxidative damage than Cleopatra mandarin. Hormonal profiling in leaves revealed that salicylic acid (SA) accumulated in response to individual stresses but to a higher extent in samples subjected to the combination of heat and drought (showing an additive response). SA accumulation correlated with the up-regulation of pathogenesis-related gene 2 (CsPR2), as a downstream response. On the contrary, abscisic acid (ABA) accumulation was higher in water-stressed plants followed by that observed in plants under stress combination. ABA signaling in these plants was confirmed by the expression of responsive to ABA-related gene 18 (CsRAB18). Modulation of ABA levels was likely carried out by the induction of 9-neoxanthin cis-epoxicarotenoid dioxygenase (CsNCED) and ABA 8’-hydroxylase (CsCYP707A) while conversion to ABA-glycosyl ester (ABAGE) was a less prominent process despite the strong induction of ABA O-glycosyl transferase (CsAOG).</p></sec><sec><title>Conclusions</title><p>Cleopatra mandarin is more susceptible to the combination of high temperatures and water deprivation than Carrizo citrange. This is likely a result of a higher transpiration rate in Carrizo that could allow a more efficient cooling of leaf surface ensuring optimal CO<sub>2</sub> intake. Hence, SA induction in Cleopatra was not sufficient to protect PSII from photoinhibition, resulting in higher malondialdehyde (MDA) build-up. Inhibition of ABA accumulation during heat stress and combined stresses was achieved primarily through the up-regulation of CsCYP707A leading to phaseic acid (PA) and dehydrophaseic acid (DPA) production. To sum up, data indicate that specific physiological responses to the combination of heat and drought exist in citrus. In addition, these responses are differently modulated depending on the particular stress tolerance of citrus genotypes.</p></sec><sec><title>Electronic supplementary material</title><p>The online version of this article (doi:10.1186/s12870-016-0791-7) contains supplementary material, which is available to authorized users.</p></sec></abstract><kwd-group xml:lang="en"><title>Keywords</title><kwd>Carrizo citrange</kwd><kwd>Cleopatra mandarin</kwd><kwd>Combined stress conditions</kwd><kwd>Heat</kwd><kwd>Hormone regulation</kwd><kwd>Salicylic acid</kwd></kwd-group><funding-group><award-group><funding-source><institution-wrap><institution-id institution-id-type="FundRef">http://dx.doi.org/10.13039/501100003329</institution-id><institution>Ministerio de Economía y Competitividad</institution></institution-wrap></funding-source><award-id>AGL2013-42038-R</award-id><principal-award-recipient><name><surname>Gómez-Cadenas</surname><given-names>Aurelio</given-names></name></principal-award-recipient></award-group><award-group><funding-source><institution-wrap><institution-id institution-id-type="FundRef">http://dx.doi.org/10.13039/501100004834</institution-id><institution>Universitat Jaume I</institution></institution-wrap></funding-source></award-group><award-group><funding-source><institution-wrap><institution-id institution-id-type="FundRef">http://dx.doi.org/10.13039/501100004834</institution-id><institution>Universitat Jaume I</institution></institution-wrap></funding-source><award-id>P1IB2013-23</award-id><principal-award-recipient><name><surname>Gómez-Cadenas</surname><given-names>Aurelio</given-names></name></principal-award-recipient></award-group></funding-group><custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name><meta-value>© The Author(s) 2016</meta-value></custom-meta></custom-meta-group></article-meta></front></pmc><affiliations><list><country><li>Espagne</li></country><region><li>Communauté valencienne</li><li>Région de Murcie</li></region></list><tree><country name="Espagne"><region name="Communauté valencienne"><name sortKey="Zandalinas, Sara I" sort="Zandalinas, Sara I" uniqKey="Zandalinas S" first="Sara I." last="Zandalinas">Sara I. Zandalinas</name></region><name sortKey="Arbona, Vicent" sort="Arbona, Vicent" uniqKey="Arbona V" first="Vicent" last="Arbona">Vicent Arbona</name><name sortKey="G Mez Cadenas, Aurelio" sort="G Mez Cadenas, Aurelio" uniqKey="G Mez Cadenas A" first="Aurelio" last="G Mez-Cadenas">Aurelio G Mez-Cadenas</name><name sortKey="Martinez, Vicente" sort="Martinez, Vicente" uniqKey="Martinez V" first="Vicente" last="Martínez">Vicente Martínez</name><name sortKey="Rivero, Rosa M" sort="Rivero, Rosa M" uniqKey="Rivero R" first="Rosa M." last="Rivero">Rosa M. Rivero</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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