Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Exogenous salicylic acid-triggered changes in the glutathione transferases and peroxidases are key factors in the successful salt stress acclimation of Arabidopsis thaliana

Edit Horváth A C , Szilvia Brunner A , Krisztina Bela A , Csaba Papdi B , László Szabados B , Irma Tari A and Jolán Csiszár A
+ Author Affiliations
- Author Affiliations

A Department of Plant Biology, Faculty of Science and Informatics, University of Szeged, Közép fasor 52, 6726 Szeged, Hungary.

B Institute of Plant Biology, Biological Research Centre, Hungarian Academy of Sciences, Temesvári körút 62, 6726 Szeged, Hungary.

C Corresponding author. Email: horvathedo@yahoo.com

Functional Plant Biology 42(12) 1129-1140 https://doi.org/10.1071/FP15119
Submitted: 4 May 2015  Accepted: 10 September 2015   Published: 23 October 2015

Abstract

Salicylic acid (SA) applied exogenously is a potential priming agent during abiotic stress. In our experiments, the priming effect of SA was tested by exposing Arabidopsis thaliana (L.) Heynh. plants to 2-week-long 10−9–10−5 M SA pretreatments in a hydroponic medium, followed by 1 week of 100 mM NaCl stress. The levels of reactive oxygen species and H2O2, changes in antioxidant enzyme activity and the expression of selected glutathione transferase (GST) genes were investigated. Although 10−9–10−7 M SA pretreatment insufficiently induced defence mechanisms during the subsequent salt stress, 2-week pretreatments with 10−6 and 10−5 M SA alleviated the salinity-induced H2O2 and malondialdehyde accumulation, and increased superoxide dismutase, guaiacol peroxidase, GST and glutathione peroxidase (GPOX) activity. Our results indicate that long-term 10−6 and 10−5 M SA treatment mitigated the salt stress injury in this model plant. Enhanced expression of AtGSTU19 and AtGSTU24 may be responsible for the induced GST and GPOX activity, which may play an important role in acclimation. Modified GST expression suggested altered signalling in SA-hardened plants during salt stress. The hydroponic system applied in our experiments proved to be a useful tool for studying the effects of sequential treatments in A. thaliana.

Additional keywords: antioxidant enzyme activity, NaCl stress, priming, reactive oxygen species.


References

Abogadallah GM (2010) Antioxidative defense under salt stress. Plant Signaling & Behavior 5, 369–374.
Antioxidative defense under salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFemu73M&md5=4f04c21f4fa8a3100326f2d6a30d2bd2CAS |

Alonso-Ramírez A, Rodríguez D, Reyes D, Jiménez JA, Nicolás G, López-Climent M, Gómez-Cadenas A, Nicolás C (2009) Evidence for a role of gibberellins in salicylic acid-modulated early plant responses to abiotic stress in Arabidopsis seeds. Plant Physiology 150, 1335–1344.
Evidence for a role of gibberellins in salicylic acid-modulated early plant responses to abiotic stress in Arabidopsis seeds.Crossref | GoogleScholarGoogle Scholar | 19439570PubMed |

Ashraf M, Akram NA, Arteca RN, Foolad MR (2010) The physiological, biochemical and molecular roles of brassinosteroids and salicylic acid in plant processes and salt tolerance. Critical Reviews in Plant Sciences 29, 162–190.
The physiological, biochemical and molecular roles of brassinosteroids and salicylic acid in plant processes and salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtFKksrY%3D&md5=a537c41c8b75ddfb55504cb01b847c06CAS |

Attia H, Arnaud N, Karray N, Lachaa M (2008) Long-term effects of mild salt stress on growth, ion accumulation and superoxide dismutase expression of Arabidopsis rosette leaves. Physiologia Plantarum 132, 293–305.
Long-term effects of mild salt stress on growth, ion accumulation and superoxide dismutase expression of Arabidopsis rosette leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtlKmurc%3D&md5=5e3edc166f7344cde90983ad59807c7cCAS | 18275461PubMed |

Blanco F, Salinas P, Cecchini NM, Jordana X, Van Hummelen P, Alvarez ME, Holuigue L (2009) Early genomic responses to salicylic acid in Arabidopsis. Plant Molecular Biology 70, 79–102.
Early genomic responses to salicylic acid in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktFShs7g%3D&md5=d56d5c9365c9a1d0d015496895084c4cCAS | 19199050PubMed |

Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction. Analytical Biochemistry 162, 156–159.
Single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXitFSns7Y%3D&md5=ae5845494e3fde4b2c4d389f54f89ff9CAS | 2440339PubMed |

Cosio C, Dunand C (2009) Specific functions of individual class III peroxidase genes. Journal of Experimental Botany 60, 391–408.
Specific functions of individual class III peroxidase genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivFSmt74%3D&md5=9310b1a69b30b620a904e47417980fd0CAS | 19088338PubMed |

Csiszár J, Szabó M, Erdei L, Márton L, Horváth F, Tari I (2004) Auxin autotrophic tobacco callus tissue resist oxidative stress: the importance of the glutathione S-transferase and peroxidase activities in auxin heterotrophic and autotrophic calli. Journal of Plant Physiology 161, 691–699.
Auxin autotrophic tobacco callus tissue resist oxidative stress: the importance of the glutathione S-transferase and peroxidase activities in auxin heterotrophic and autotrophic calli.Crossref | GoogleScholarGoogle Scholar | 15266716PubMed |

Csiszár J, Gallé Á, Horváth E, Dancsó P, Gombos M, Váry ZS, Erdei L, Györgyey J, Tari I (2012) Different peroxidase activities and expression of abiotic stress-related peroxidases in apical root segments of wheat genotypes with different drought stress tolerance under osmotic stress. Plant Physiology and Biochemistry 52, 119–129.
Different peroxidase activities and expression of abiotic stress-related peroxidases in apical root segments of wheat genotypes with different drought stress tolerance under osmotic stress.Crossref | GoogleScholarGoogle Scholar | 22305075PubMed |

Csiszár J, Horváth E, Váry ZS, Gallé Á, Bela K, Brunner S, Tari I (2014) Glutathione transferase supergene family in tomato: salt stress-regulated expression of representative genes from distinct GST classes in plants primed with salicylic acid. Plant Physiology and Biochemistry 78, 15–26.
Glutathione transferase supergene family in tomato: salt stress-regulated expression of representative genes from distinct GST classes in plants primed with salicylic acid.Crossref | GoogleScholarGoogle Scholar | 24607575PubMed |

Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411, 826–833.
Plant pathogens and integrated defence responses to infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXksF2gu74%3D&md5=68eada5d8314c69d9050f90fd8236682CAS | 11459065PubMed |

De Gara L (2004) Class III peroxidases and ascorbate metabolism in plants. Phytochemistry Reviews 3, 195–205.
Class III peroxidases and ascorbate metabolism in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhsFehu7c%3D&md5=b8dcd73c36f4bd70bfd14422183000f8CAS |

Dixon DP, Lapthorn A, Edwards R (2002) Plant glutathione transferases. Genome Biology 3, REVIEWS3004

Dixon DP, Hawkins T, Hussey PJ, Edwards R (2009) Enzyme activities and subcellular localization of members of the Arabidopsis glutathione transferase superfamily. Journal of Experimental Botany 60, 1207–1218.
Enzyme activities and subcellular localization of members of the Arabidopsis glutathione transferase superfamily.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsFShsbs%3D&md5=593a859c142a7c99ce0f1d87161f8f52CAS | 19174456PubMed |

Dixon DP, Skipsey M, Edwards R (2010) Roles for glutathione transferases in plant secondary metabolism. Phytochemistry 71, 338–350.
Roles for glutathione transferases in plant secondary metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitVOnurc%3D&md5=8b9f313cdff734175572d163a8a1a8a1CAS | 20079507PubMed |

Ederli L, Pasqualini S, Batini P, Antonielli M (1997) Photoinhibition and oxidative stress: effects on xanthophyll cycle, scavenger enzymes and abscisic content in tobacco plants. Journal of Plant Physiology 151, 422–428.
Photoinhibition and oxidative stress: effects on xanthophyll cycle, scavenger enzymes and abscisic content in tobacco plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmvVOms70%3D&md5=90e2484e06b713f9b0f75e064ba290ccCAS |

El-Tayeb MA (2005) Response of barley grains to the interactive effect of salinity and salicylic acid. Plant Growth Regulation 45, 215–224.
Response of barley grains to the interactive effect of salinity and salicylic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtVSgurw%3D&md5=cfb4e35ff2c61b95eb68ce5a26e84813CAS |

Ellouzi H, Ben Hamed K, Cela J, Munné-Bosch S, Abdelly C (2011) Early effects of salt stress on the physiological and oxidative status of Cakile maritima (halophyte) and Arabidopsis thaliana (glycophyte). Physiologia Plantarum 142, 128–143.
Early effects of salt stress on the physiological and oxidative status of Cakile maritima (halophyte) and Arabidopsis thaliana (glycophyte).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmvFeru7c%3D&md5=0e4cd83bab549557e13fcd6247038f10CAS | 21288246PubMed |

Gallé A, Csiszár J, Secenji M, Guóth A, Cseuz L, Tari I, Györgyey J, Erdei L (2009) Glutathione transferase activity and expression patterns during grain filling in flag leaves of wheat genotypes differing in drought tolerance: response to water deficit. Journal of Plant Physiology 166, 1878–1891.
Glutathione transferase activity and expression patterns during grain filling in flag leaves of wheat genotypes differing in drought tolerance: response to water deficit.Crossref | GoogleScholarGoogle Scholar | 19615785PubMed |

Gémes K, Poór P, Horváth E, Kolbert Z, Szopkó D, Szepesi Á, Tari I (2011) Cross-talk between salicylic acid and NaCl-generated reactive oxygen species and nitric oxide in tomato during acclimation to high salinity. Physiologia Plantarum 142, 179–192.
Cross-talk between salicylic acid and NaCl-generated reactive oxygen species and nitric oxide in tomato during acclimation to high salinity.Crossref | GoogleScholarGoogle Scholar | 21338371PubMed |

Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry 48, 909–930.
Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlKnu7fF&md5=d8466bc1f0ea5a1d21bd608636a35002CAS | 20870416PubMed |

Gunes A, Inal A, Alpaslan M, Eraslan F, Bagci EG, Cicek N (2007) Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity. Journal of Plant Physiology 164, 728–736.
Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmvFWqtbk%3D&md5=e46ed5455304833b1523e4c1a81aea35CAS | 16690163PubMed |

Gunning V, Tzafestas K, Sparrow H, Johnston EJ, Brentnall AS, Potts JR, Rylott EL, Bruce NC (2014) Arabidopsis glutathione transferases U24 and U25 exhibit a range of detoxification activities with the environmental pollutant and explosive, 2,4,6-trinitrotoluene. Plant Physiology 165, 854–865.
Arabidopsis glutathione transferases U24 and U25 exhibit a range of detoxification activities with the environmental pollutant and explosive, 2,4,6-trinitrotoluene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVWnurfM&md5=e0ff678258742bcabf3744103809718eCAS | 24733884PubMed |

Guo M, Gao W, Li L, Li H, Xu Y, Zhou C (2014) Proteomic and phosphoproteomic analyses of NaCl stress-responsive proteins in Arabidopsis roots. Journal of Plant Interactions 9, 396–401.
Proteomic and phosphoproteomic analyses of NaCl stress-responsive proteins in Arabidopsis roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsV2msbbN&md5=18bd8f3e1b4b39db6dfac3f5193494d9CAS |

Han Y, Chaouch S, Mhamdi A, Queval G, Zechmann B, Noctor GD (2013) Functional analysis of Arabidopsis mutants points to novel roles for glutathione in coupling H2O2 to activation of salicylic acid accumulation and signaling. Antioxidants & Redox Signalling 18, 2106–2121.
Functional analysis of Arabidopsis mutants points to novel roles for glutathione in coupling H2O2 to activation of salicylic acid accumulation and signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmtVyiu7g%3D&md5=4fa6b6dcdcc685f3146dc478474dac94CAS |

Hao L, Zhao Y, Jin D, Zhang L, Bi X, Chen H, Xu Q, Ma C, Li G (2012) Salicylic acid-altering Arabidopsis mutants response to salt stress. Plant and Soil 354, 81–95.
Salicylic acid-altering Arabidopsis mutants response to salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlvFWgtLw%3D&md5=e69c0d8a72d4918dcff08d616ff2fd89CAS |

Hayat Q, Hayat S, Irfan M, Ahmad A (2010) Effect of exogenous salicylic acid under changing environment: a review. Environmental and Experimental Botany 68, 14–25.
Effect of exogenous salicylic acid under changing environment: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1WitrbK&md5=9e02bfb278a5769be2d5bca94d486145CAS |

Horváth E, Szalai G, Janda T (2007) Induction of abiotic stress tolerance by salicylic acid signaling. Journal of Plant Growth Regulation 26, 290–300.
Induction of abiotic stress tolerance by salicylic acid signaling.Crossref | GoogleScholarGoogle Scholar |

Horváth E, Csiszár J, Gallé Á, Poór P, Szepesi Á, Tari I (2015) Hardening with salicylic acid induces concentration-dependent changes in abscisic acid biosynthesis of tomato under salt stress. Journal of Plant Physiology 183, 54–63.
Hardening with salicylic acid induces concentration-dependent changes in abscisic acid biosynthesis of tomato under salt stress.Crossref | GoogleScholarGoogle Scholar | 26086888PubMed |

Jayakannan M, Bose J, Babourina O, Rengel Z, Shabala S (2013) Salicylic acid improves salinity tolerance in Arabidopsis by restoring membrane potential and preventing salt-induced K+ loss via a GORK channel. Journal of Experimental Botany 64, 2255–2268.
Salicylic acid improves salinity tolerance in Arabidopsis by restoring membrane potential and preventing salt-induced K+ loss via a GORK channel.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnvV2nurs%3D&md5=68e458bd60ef7dbdf0655e90dd27be71CAS | 23580750PubMed |

Jayakannan M, Bose J, Babourina O, Rengel Z, Shabala S (2015) Salicylic acid in plant salinity stress signalling and tolerance. Plant Growth Regulation 76, 25–40.
Salicylic acid in plant salinity stress signalling and tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsVCrsL8%3D&md5=59e7cf32fc4af1ed4764fa766fdab383CAS |

Jiang Y, Yang B, Harris NS, Deyholos MK (2007) Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots. Journal of Experimental Botany 58, 3591–3607.
Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVWhurjP&md5=860f07cc71dc81bfbd34406a6b7c0602CAS | 17916636PubMed |

Joseph B, Jini D, Sujatha S (2010) Insight into the role of exogenous salicylic acid on plants grown under salt environment. Asian Journal of Crop Science 2, 226–235.
Insight into the role of exogenous salicylic acid on plants grown under salt environment.Crossref | GoogleScholarGoogle Scholar |

Khan NA, Syeed S, Masood A, Nazar R, Iqbal N (2010) Application of salicylic acid increases contents of nutrients and antioxidative metabolism in mungbean and alleviates adverse effects of salinity stress. International Journal of Plant Biology 1, e1
Application of salicylic acid increases contents of nutrients and antioxidative metabolism in mungbean and alleviates adverse effects of salinity stress.Crossref | GoogleScholarGoogle Scholar |

Kim SY, Lim JH, Park MR, Kim YJ, Park TI, Seo YW, Choi KG, Yun SJ (2005) Enhanced antioxidant enzymes are associated with reduced hydrogen peroxide in barley roots under saline stress. Journal of Biochemistry and Molecular Biology 38, 218–224.
Enhanced antioxidant enzymes are associated with reduced hydrogen peroxide in barley roots under saline stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjsVOqsLo%3D&md5=e0d827f9f052331c6d5cd8ae1166e0f8CAS | 15826500PubMed |

Kocsy G, Tari I, Vanková R, Zechmann B, Gulyás Z, Poór P, Galiba G (2013) Redox control of plant growth and development. Plant Science 211, 77–91.
Redox control of plant growth and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlGqt7%2FK&md5=5c4a5f245b953e1f4a42405f95de0609CAS | 23987814PubMed |

Kuai X, MacLeod BJ, Després C (2015) Integrating data on the Arabidopsis NPR1/NPR3/NPR4 salicylic acid receptors; a differentiating argument. Frontiers in Plant Science 6, 235
Integrating data on the Arabidopsis NPR1/NPR3/NPR4 salicylic acid receptors; a differentiating argument.Crossref | GoogleScholarGoogle Scholar | 25914712PubMed |

Lee S, Park CM (2010) Modulation of reactive oxygen species by salicylic acid in Arabidopsis seed germination under high salinity. Plant Signaling & Behavior 5, 1534–1536.
Modulation of reactive oxygen species by salicylic acid in Arabidopsis seed germination under high salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1GqsbfI&md5=bd417087c5d1c32b9e082ef24a9a9e39CAS |

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods (San Diego, Calif.) 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=322bb6fd44685e306f8210cd65b59997CAS |

Marrs KA (1996) The function and regulation of glutathione S-transferases in plants. Annual Review of Plant Physiology 47, 127–158.
The function and regulation of glutathione S-transferases in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjtlWgsbo%3D&md5=b370c311c73b7d92a464513b66702672CAS |

Masclaux-Daubresse C, Purdy S, Lemaitre T, Pourtau N, Taconnat L, Renou JP, Wingler A (2007) Genetic variation suggests interaction between cold acclimation and metabolic regulation of leaf senescence. Plant Physiology 143, 434–446.
Genetic variation suggests interaction between cold acclimation and metabolic regulation of leaf senescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpt1Olsw%3D%3D&md5=8fffc849efe6ef0523200cf7ff3c254cCAS | 17098848PubMed |

Métrauxs JP (2001) Systemic acquired resistance and salicylic acid: current state of knowledge. European Journal of Plant Pathology 107, 13–18.
Systemic acquired resistance and salicylic acid: current state of knowledge.Crossref | GoogleScholarGoogle Scholar |

Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113, 935–944.
Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlsVSjur8%3D&md5=0fa4e28787e94dcc4949042bbe58d751CAS | 12837250PubMed |

Munns R (2005) Genes and salt tolerance: bringing them together. New Phytologist 167, 645–663.
Genes and salt tolerance: bringing them together.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVGisbfP&md5=1fcd1863a904ebf12f79ac52eb165eabCAS | 16101905PubMed |

Munns M, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681.
Mechanisms of salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqtrw%3D&md5=e2ba555e0946a244ab5e98e4f2e7cc4dCAS |

Noreen S, Ashraf M, Hussain M, Jamil A (2009) Exogenous application of salicylic acid enhances antioxidative capacity in salt stressed sunflower (Helianthus annuus L.) plants. Pakistan Journal of Botany 41, 473–479.

Palma F, Lluch C, Iribarne C, García-Garrido JM, Tejera García NA (2009) Combined effect of salicylic acid and salinity on some antioxidant activities, oxidative stress and metabolite accumulation in Phaseolus vulgaris. Plant Growth Regulation 58, 307–316.
Combined effect of salicylic acid and salinity on some antioxidant activities, oxidative stress and metabolite accumulation in Phaseolus vulgaris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlKntb8%3D&md5=adb300cf2c54b29320208ad9a77caeb5CAS |

Papdi C, Ábrahám E, Joseph MP, Popescu C, Koncz C, Szabados L (2008) Functional identification of Arabidopsis stress regulatory genes using the controlled cDNA overexpression system. Plant Physiology 147, 528–542.
Functional identification of Arabidopsis stress regulatory genes using the controlled cDNA overexpression system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnsVyhsbk%3D&md5=919396b76756f61b45e2b1657c3df09aCAS | 18441225PubMed |

Passardi F, Longet D, Penel C, Dunand C (2004) The class III peroxidase multigenic family in rice and its evolution in land plants. Phytochemistry 65, 1879–1893.
The class III peroxidase multigenic family in rice and its evolution in land plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtVCjtrc%3D&md5=f91647b1175b38066ce4ee88ba0ac1acCAS | 15279994PubMed |

Pető A, Lehotai N, Feigl G, Tugyi N, Ördög A, Gémes K, Tari I, Erdei L, Kolbert ZS (2013) Nitric oxide contributes to copper tolerance by influencing ROS metabolism in Arabidopsis. Plant Cell Reports 32, 1913–1923.
Nitric oxide contributes to copper tolerance by influencing ROS metabolism in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 24013762PubMed |

Poór P, Gémes K, Horváth F, Szepesi Á, Simon ML, Tari I (2011) Salicylic acid treatment via the rooting medium interferes with stomatal response, CO2 fixation rate and carbohydrate metabolism in tomato, and decreases harmful effects of subsequent salt stress. Plant Biology 13, 105–114.
Salicylic acid treatment via the rooting medium interferes with stomatal response, CO2 fixation rate and carbohydrate metabolism in tomato, and decreases harmful effects of subsequent salt stress.Crossref | GoogleScholarGoogle Scholar | 21143731PubMed |

Raskin I (1992) Role of salicylic acid in plants. Annual Review of Plant Physiology 43, 439–463.
Role of salicylic acid in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xks1Knu74%3D&md5=134b88a07a18ecf3039ff86adfdf2520CAS |

Rivas-San Vicente M, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. Journal of Experimental Botany 62, 3321–3338.
Salicylic acid beyond defence: its role in plant growth and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXoslOmtbc%3D&md5=e2279777bbfbc531ab496f3f6ba68f9dCAS | 21357767PubMed |

Roxas VP, Lodhi SA, Garrett DK, Mahan JR, Allen RD (2000) Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidase. Plant & Cell Physiology 41, 1229–1234.
Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXosVKgurs%3D&md5=236e0e1e9b824c2f8ac4ace61ab04333CAS |

Sappl PG, Onate-Sanchez L, Singh KB, Millar AH (2004) Proteomic analysis of glutathione S-transferases ofArabidopsis thaliana reveals differential salicylic acid-induced expression of the plant-specific phi and tau classes. Plant Molecular Biology 54, 205–219.
Proteomic analysis of glutathione S-transferases ofArabidopsis thaliana reveals differential salicylic acid-induced expression of the plant-specific phi and tau classes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkt1Squ74%3D&md5=6204d4fe6075d6d3a3a21ede515366f4CAS | 15159623PubMed |

Sappl PG, Carroll AJ, Clifton R, Lister R, Whelan J, Millar AH, Singh KB (2009) The Arabidopsis glutathione transferase gene family displays complex stress regulation and co-silencing multiple genes results in altered metabolic sensitivity to oxidative stress. The Plant Journal 58, 53–68.
The Arabidopsis glutathione transferase gene family displays complex stress regulation and co-silencing multiple genes results in altered metabolic sensitivity to oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXks1Cnsrg%3D&md5=e4852ff40b1e2a15e5eff685ba146d3bCAS | 19067976PubMed |

Shirasu K, Nakajima H, Rajashekar K, Dixon RA, Lamb C (1997) Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signal in the activation of defense mechanisms. The Plant Cell 9, 261–270.
Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signal in the activation of defense mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhslGrtbs%3D&md5=d41cce20ef346194797f0238215564a8CAS | 9061956PubMed |

Stevens J, Senaratna T, Sivasithamparam K (2006) Salicylic acid induces salinity tolerance in tomato (Lycopersicon esculentum cv. Roma): associated changes in gas exchange, water relations and membrane stabilisation. Plant Growth Regulation 49, 77–83.

Syeed S, Anjum NA, Nazar R, Iqbal N, Masood A, Khan NA (2011) Salicylic acid-mediated changes in photosynthesis, nutrients content and antioxidant metabolism in two mustard (Brassica juncea L.) cultivars differing in salt tolerance. Acta Physiologiae Plantarum 33, 877–886.
Salicylic acid-mediated changes in photosynthesis, nutrients content and antioxidant metabolism in two mustard (Brassica juncea L.) cultivars differing in salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkslWqsbo%3D&md5=db45da34337e390f26352253d5f6d49bCAS |

Szepesi Á, Csiszár J, Gallé Á, Gémes K, Poór P, Tari I (2008) Effects of long-term salicylic acid pre-treatment on tomato (Lycopersicon esculentum Mill. L.) salt stress tolerance: changes in glutathione S-transferase activities and anthocyanin contents. Acta Agronomica Hungarica 56, 129–138.
Effects of long-term salicylic acid pre-treatment on tomato (Lycopersicon esculentum Mill. L.) salt stress tolerance: changes in glutathione S-transferase activities and anthocyanin contents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpsFOqtL0%3D&md5=194810b6b08e9c8a29aacd85b562228cCAS |

Szepesi Á, Csiszár J, Gémes K, Horváth E, Horváth F, Simon ML, Tari I (2009) Salicylic acid improves acclimation to salt stress by stimulating abscisic aldehyde oxidase activity and abscisic acid accumulation, and increases Na+ content in leaves without toxicity symptoms in Solanum lycopersicum L. Journal of Plant Physiology 166, 914–925.
Salicylic acid improves acclimation to salt stress by stimulating abscisic aldehyde oxidase activity and abscisic acid accumulation, and increases Na+ content in leaves without toxicity symptoms in Solanum lycopersicum L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmslartbk%3D&md5=3283a936ddc0caddf57738bf45f2b25aCAS | 19185387PubMed |

Tari I, Csiszár J, Szalai G, Horváth F, Pécsváradi A, Kiss G, Szepesi Á, Szabó M, Erdei L (2002) Acclimation of tomato plants to salinity stress after a salicylic acid pre-treatment. Acta Biologica Szegediensis 46, 55–56.

Tian M, von Dahl CC, Liu P-P, Friso G, van Wijk KJ, Klessig DF (2012) The combined use of photoaffinity labeling and surface plasmon resonance-based technology identifies multiple salicylic acid-binding proteins. The Plant Journal 72, 1027–1038.

Vlot AC, Dempsey DMA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annual Review of Phytopathology 47, 177–206.
Salicylic acid, a multifaceted hormone to combat disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1Gjt73P&md5=99619e9bf46d7add6e970eb7a90d63fbCAS | 19400653PubMed |

Wagner U, Edwards R, Dixon DP, Mauch F (2002) Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Molecular Biology 49, 515–532.
Probing the diversity of the Arabidopsis glutathione S-transferase gene family.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvVWrurY%3D&md5=6a32e9b2ec5822d79d8f35b315df9028CAS | 12090627PubMed |

Wu Y, Zhang D, Chu JY, Boyle P, Wang Y, Brindle ID, De Luca V, Després C (2012) The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Reports 1, 639–647.
The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVOrsrvK&md5=fb2ebcbd3eeb4ab489b8b336f0617784CAS | 22813739PubMed |

Xia XJ, Zhou YH, Shi K, Zhou J, Foyer CH, Yu JQ (2015) Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance. Journal of Experimental Botany 66, 2839–2856.
Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance.Crossref | GoogleScholarGoogle Scholar | 25788732PubMed |

Zhang H, Han B, Wang T, Chen S, Li H, Zhang Y, Dai S (2012) Mechanisms of plant salt response: insights from proteomics. Journal of Proteome Research 11, 49–67.
Mechanisms of plant salt response: insights from proteomics.Crossref | GoogleScholarGoogle Scholar | 22017755PubMed |