Abstract
Plant hormones and antioxidant system changes occur during plants' exposure to stress conditions. Although the interactions of some plant hormones (abscisic acid, salicylic acid, jasmonic acid, nitric oxide, and ethylene) with the glutathione s-transferase (GST) enzyme, which is one of the antioxidant enzymes, have already been reported, the influence of gibberellic acid (GA3) on this enzyme under saline conditions has not yet been reported. Plant material for the experiments was obtained from M14G144 cultivar of maize (Zea mays L.) plants grown as a soil culture in growth chambers at 22 °C, 65–70% moisture, 16-h light/8-h dark conditions, and with full strength Hoagland solution for 8 days under controlled growth conditions. Then, the plants were exposed to salt stress (350 mM NaCl and 100, 300, and 500 ppm GA3) simultaneously. In maize leaves, GA3 treatment alleviated the physiological parameters under salt stress. Specifically, the treatments with 100 and 500 ppm of GA3 were able to trigger GST enzyme and isoenzyme activities as well as hydrogen sulfide accumulation and anthocyanin content, although the lowest malondialdehyde, hydrogen peroxide, and superoxide radical content were under the treatment of 300 ppm of GA3. Besides this, GST gene expression levels were found to be upregulated between 1.5 and fourfold higher in all the plants treated with GA3 at different concentrations in proportion to salt stress. These results first indicated that the reason for the changes in GA3-treated plants was the stimulating role of this hormone to maintain GST regulation in maize plants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahmad P (2010) Growth and antioxidant responses in mustard (Brassica juncea L.) plants subjected to combined effect of gibberellic acid and salinity. Arch Agronom Soil Sci 56(5):575–588. https://doi.org/10.1080/03650340903164231
Ahmad MZ, Nasir JA, Ahmed S, Ahmad B, Sana A, Salman S, Shah Z, Yang C (2020) Genome-wide analysis of glutathione s-transferase gene family in G. max. Biologia. https://doi.org/10.2478/s11756-020-00463-5
Ahmad P, Raja V, Ashraf M, Wijaya L, Bajguz A, Alyemeni MN (2021) Jasmonic acid (JA) and gibberellic acid (GA3) mitigated Cd-toxicity in chickpea plants through restricted cd uptake and oxidative stress management. Sci Rep 11(1):1–17. https://doi.org/10.1038/s41598-021-98753-8
Ali AYA, Ibrahim ME, Zhou G, Nimir NE, Elsiddig AM, Jiao X, Zhu G, Salih EG, Suliman MS, Elradi SB (2021) Gibberellic acid and nitrogen efficiently protect early seedlings growth stage from salt stress damage in Sorghum. Sci Rep 11(1):1–11. https://doi.org/10.1038/s41598-021-84713-9
Ben Rhouma M, Kriaa M, Ben Nasr Y, Mellouli L, Kammoun R (2020) A new endophytic Fusarium oxysporum gibberellic acid: Optimization of production using combined strategies of experimental designs and potency on tomato growth under stress condition. Biomed Res Int. https://doi.org/10.1155/2020/4587148
Benekos K, Kissoudis C, Nianiou-Obeidat I, Labrou N, Madesis P, Kalamaki M, Tsaftaris A (2010) Overexpression of a specific soybean GmGSTU4 isoenzyme improves diphenyl ether and chloroacetanilide herbicide tolerance of transgenic tobacco plants. J Biotec 150(1):195–201. https://doi.org/10.1016/j.jbiotec.2010.07.011
Bharath P, Gahir S, Raghavendra AS (2021) Abscisic acid-induced stomatal closure: an important component of plant defense against abiotic and biotic stress. Front Plant Sci 12:324. https://doi.org/10.3389/fpls.2021.615114
Bodeau JP, Walbot V (1996) Structure and regulation of the maize Bronze2 promoter. Plant Mol Biol. https://doi.org/10.1007/BF00020201
Chen W, Singh KB (1999) The auxin, hydrogen peroxide and salicylic acid induced expression of the Arabidopsis GST6 promoter is mediated in part by an ocs element. Plant J 19(6):667–677. https://doi.org/10.1046/j.1365-313x.1999.00560.x
Chen K, Fessehaie A, Arora R (2012) Selection of reference genes for normalizing gene expression during seed priming and germination using qPCR in Zea mays and Spinacia oleracea. Plant Mol Biol Rep 30:478–487. https://doi.org/10.1007/s11105-011-0354-x
Claussen W (2002) Growth, water use efficiency, and proline content of hydroponically grown tomato plants as affected by nitrogen source and nutrient concentration. Plant Soil 247(2):199–209. https://doi.org/10.1023/A:1021453432329
Csiszár J, Horváth E, Váry Z, 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 Physiol Biochem 78:15–26. https://doi.org/10.1016/j.plaphy.2014.02.010
da Silva CJ, Mollica DC, Vicente MH, Peres LE, Modolo LV (2018) NO, hydrogen sulfide does not come first during tomato response to high salinity. Nitric Oxide 76:164–173. https://doi.org/10.1016/j.niox.2017.09.008
Dinler BS, Antoniou C, Fotopoulos V (2014) Interplay between GST and nitric oxide in the early response of soybean (Glycine max L.) plants to salinity stress. J Plant Physiol 171(18):1740–1747. https://doi.org/10.1016/j.jplph.2014.07.026
Dinler BS, Cetinkaya H, Akgun M, Korkmaz K (2021) Simultaneous treatment of different gibberellic acid doses induces ion accumulation and response mechanisms to salt damage in maize roots. J Plant Biochem Physiol. https://doi.org/10.35248/2329-9029.21.9.258
Dixon DP, Skipsey M, Edwards R (2010) Roles for glutathione transferases in plant secondary metabolism. Phytochem 71(4):338–350. https://doi.org/10.1016/j.phytochem.2009.12.012
Edwards R, Dixon DP (2005) Plant Glutathione transferases. Meth Enzymol 401:169–186. https://doi.org/10.1016/S0076-6879(05)01011-6
Edwards R, Dixon DP, Walbot V (2000) Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci 5(5):193–198. https://doi.org/10.1016/S1360-1385(00)01601-0
Estévez IH, Hernández MR (2020) Plant glutathione S-transferases: an overview. Plant Gene 23:100233. https://doi.org/10.1016/j.plgene.2020.100233
Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase inchloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25. https://doi.org/10.1007/BF00386001
Gallé Á, Bela K, Hajnal Á, Faragó N, Horváth E, Horváth M, Csiszár J (2021) Crosstalk between the redox signalling and the detoxification: GSTs under redox control? Plant Physiol Biochem. https://doi.org/10.1016/j.plaphy.2021.11.009
Gantait S, Rani Sinniah U, Ali N, Chandra Sahu N (2015) Gibberellins-a multifaceted hormone in plant growth regulatory network. Curr Protein Pept Sci 16(5):406–412
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48(12):909–930. https://doi.org/10.1016/j.plaphy.2010.08.016
Gomi K, Matsuoka M (2003) Gibberellin signalling pathway. Curr Opin Plant Biol 6(5):489–493. https://doi.org/10.1016/S1369-5266(03)00079-7
Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases: the first enzymatic step in mercapturic acid formation. J Biol Chem 249(22):7130–7139. https://doi.org/10.1016/S0021-9258(19)42083-8
Iftikhar A, Ali S, Yasmeen T, Arif MS, Zubair M, Rizwan M, Soliman MH (2019) Effect of gibberellic acid on growth, photosynthesis and antioxidant defense system of wheat under zinc oxide nanoparticle stress. Environ Poll 254:113109. https://doi.org/10.1016/j.envpol.2019.113109
Jiao X, Zhi W, Liu G, Zhu G, Feng G, Eltyb Ahmed Nimir N, Zhou G et al (2019) Responses of foreign GA3 application on seedling growth of castor bean (Ricinus communis L.) under salinity stress conditions. Agronomy 9(6):274. https://doi.org/10.3390/agronomy9060274
Kamran M, Wang D, Alhaithloul HAS, Alghanem SM, Aftab T, Xie K, Soliman MH (2021) Jasmonic acid-mediated enhanced regulation of oxidative, glyoxalase defense system and reduced chromium uptake contributes to alleviation of chromium (VI) toxicity in choysum (Brassica parachinensis L.). Ecotoxicol Environ Safe 208:111758. https://doi.org/10.1016/j.ecoenv.2020.111758
Kaur S, Gupta AK, Kaur N (2000) Effect of GA3, kinetin and indole acetic acid on carbohydrate metabolism in chickpea seedlings germinating under water stress. Plant Grow Regul 30(1):61–70. https://doi.org/10.1023/A:1006371219048
Kavas M, Baloğlu MC, Atabay ES, Ziplar UT, Daşgan HY, Ünver T (2016) Genome-wide characterization and expression analysis of common bean bHLH transcription factors in response to excess salt concentration. Mol Genet Genom 291:129–143. https://doi.org/10.1007/s00438-015-1095-6
Kaya C, Sarıoğlu A, Ashraf M, Alyemeni MN, Ahmad P (2020) Gibberellic acid-induced generation of hydrogen sulfide alleviates boron toxicity in tomato (Solanum lycopersicum L.) plants. Plant Physiol Biochem 153:53–63. https://doi.org/10.1016/j.plaphy.2020.04.038
Ke D, Sun G (2004) The effect of reactive oxygen species on ethylene production induced by osmotic stress in etiolated mungbean seedling. Plant Grow Regul 44(3):199–206. https://doi.org/10.1007/s10725-004-5575-7
Khan MA, Asaf S, Khan AL, Ullah I, Ali S, Kang SM, Lee IJ (2019) Alleviation of salt stress response in soybean plants with the endophytic bacterial isolate Curtobacterium sp. SAK1. Annal Microbiol 69(8):797–808. https://doi.org/10.1007/s13213-019-01470-x
Kishor PK, Sangam S, Amrutha RN, Laxmi PS, Naidu KR, Rao KS, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci 10:424–438
Kundu S, Gantait S (2017) Abscisic acid signal crosstalk during abiotic stress response. Plant Gene 11:61–69. https://doi.org/10.1016/j.plgene.2017.04.007
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259):680–685. https://doi.org/10.1038/227680a0
Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79(4):583–593. https://doi.org/10.1016/0092-8674(94)90544-4
Li W, Wu J, Weng S, Zhang Y, Zhang D, Shi C (2010) Identification and characterization of dwarf 62, a loss-of-function mutation in DLT/OsGRAS-32 affecting gibberellin metabolism in rice. Planta 232(6):1383–1396. https://doi.org/10.1007/s00425-010-1263-1
Liang Y, Farooq MU, Hu Y, Tang Z, Zhang Y, Zeng R, Zhu J (2018) Study on stability and antioxidant activity of red anthocyanidin glucoside rich hybrid rice, its nutritional and physicochemical characteristics. Food Sci Technol 24(4):687–696. https://doi.org/10.3136/fstr.24.687
Lieberherr D, Wagner U, Dubuis PH, Métraux JP, Mauch F (2003) The rapid induction of glutathione S-transferases AtGSTF2 and AtGSTF6 by avirulent Pseudomonas syringae is the result of combined salicylic acid and ethylene signaling. Plant Cell Physiol 44(7):750–757. https://doi.org/10.1093/pcp/pcg093
Liu K, Zhang L, Lin X, Chen L, Shi H, Magaye R, Zhao J et al (2013) Association of GST genetic polymorphisms with the susceptibility to hepatocellular carcinoma (HCC) in Chinese population evaluated by an updated systematic meta-analysis. PLoS One 8(2):e57043. https://doi.org/10.1371/journal.pone.0057043
Liu L, Xia W, Li H, Zeng H, Wei B, Han S, Yin C (2018) Salinity inhibits rice seed germination by reducing α-amylase activity via decreased bioactive gibberellin content. Front Plant Sci 9:275. https://doi.org/10.3389/fpls.2018.00275
Liu Y, Qi Y, Zhang A, Wu H, Liu Z, Ren X (2019) Molecular cloning and functional characterization of AcGST1, an anthocyanin-related glutathione S-transferase gene in kiwifruit (Actinidia chinensis). Plant Mol Biol 100(4):451–465. https://doi.org/10.1007/s11103-019-00870-6
Liu Z, Wang X, Li L, Wei G, Zhao M (2020) Hydrogen sulfide protects against paraquat-induced acute liver injury in rats by regulating oxidative stress, mitochondrial function, and inflammation. Oxid Med Cell. https://doi.org/10.1155/2020/6325378
Mancinelli AL, Yang CPH, Lindquist P, Anderson OR, Rabino I (1975) Photocontrol of anthocyanin synthesis: III. The action of streptomycin on the synthesis of chlorophyll and anthocyanin. Plant Physiol 55(2):251–257. https://doi.org/10.1104/pp.55.2.251
Marrs KA (1996) The functions and regulation of glutathione S-transferases in plants. Ann Rev Plant Biol 47(1):127–158. https://doi.org/10.1146/annurev.arplant.47.1.127
McGonigle B, Keeler SJ, Lau SMC, Koeppe MK, O’Keefe DP (2000) A genomics approach to the comprehensive analysis of the glutathione s-transferase gene family in soybean and maize. Plant Physiol 124(3):1105–1120. https://doi.org/10.1104/pp.124.3.1105
Moons A (2003) Osgstu3 and osgtu4, encoding tau class glutathione S-transferases, are heavy metal-and hypoxic stress-induced and differentially salt stress-responsive in rice roots. FEBS Lett 553(3):427–32. https://doi.org/10.1016/S0014-5793(03)01077-9
Mukarram M, Firoz Mohammad M, Naeem MM, Khan A (2021) Exogenous gibberellic acid supplementation renders growth and yield protection against salinity induced oxidative damage through upregulating antioxidant metabolism in Fenugreek (Trigonella foenum-graceum L.). In: Naeem M, Tariq Aftab M, Khan MA (eds) Fenugreek: biology and applications. Springer Singapore, Singapore, pp 99–117. https://doi.org/10.1007/978-981-16-1197-1_6
Nashef AS, Osuga DT, Feeney RE (1977) Determination of hydrogen sulfide with 5, 5′-dithiobis-(2-nitrobenzoic acid), N-ethylmaleimide, and parachloromercuribenzoate. Anal Biochem 79(1–2):394–405. https://doi.org/10.1016/0003-2697(77)90413-4
Nehela Y, Hijaz F, Elzaawely AA, El-Zahaby HM, Killiny N (2016) Phytohormone profiling of the sweet orange (Citrus sinensis (L.) Osbeck) leaves and roots using GC–MS-based method. J Plant Physiol 199:12–17. https://doi.org/10.1016/j.jplph.2016.04.005
Nutricati E, Miceli A, Blando F, De Bellis L (2006) Characterization of two Arabidopsis thaliana glutathione S-transferases. Plant Cell Rep 25(9):997–1005. https://doi.org/10.1007/s00299-006-0146-1
Polidoros AN, Scandalios JG (1999) Role of hydrogen peroxide and different classes of antioxidants in the regulation of catalase and glutathione S-transferase gene expression in maize (Zea mays L.). Physiol Plant 106(1):112–20. https://doi.org/10.1093/jxb/erl292
Rao KM, Sresty TVS (2000) Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Sci 157(1):113–128. https://doi.org/10.1016/S0168-9452(00)00273-9
Ricci G, Bello ML, Caccuri AM, Galiazzo F, Federici G (1984) Detection of glutathione transferase activity on polyacrylamide gels. Anal Biochem 143(2):226–230. https://doi.org/10.1016/0003-2697(84)90657-2
Sahoo S, Awasthi JP, Sunkar R, Panda SK (2017) Determining glutathione levels in plants. In: Sunkar R (ed) Plant stress tolerance. Springer New York, New York, pp 273–277. https://doi.org/10.1007/978-1-4939-7136-7_16
Seo M, Hanada A, Kuwahara A, Endo A, Okamoto M, Yamauchi Y, Nambara E et al (2006) Regulation of hormone metabolism in Arabidopsis seeds: phytochrome regulation of abscisic acid metabolism and abscisic acid regulation of gibberellin metabolism. Plant J 48(3):354–366. https://doi.org/10.1111/j.1365-313X.2006.02881.x
Shahzad K, Hussain S, Arfan M, Hussain S, Waraich EA, Zamir S, El-Esawi MA (2021) Exogenously applied gibberellic acid enhances growth and salinity stress tolerance of Maize through modulating the morpho-physiological. Biochem Mol Attrib Biomol 11(7):1005. https://doi.org/10.3390/biom11071005
Sharma R, Sahoo A, Devendran R, Jain M (2014) Over-expression of a rice tau class glutathione s-transferase gene improves tolerance to salinity and oxidative stresses in Arabidopsis. PLoS one 9(3):e92900. https://doi.org/10.1371/journal.pone.0092900
Smart RE, Bingham GE (1974) Rapid estimates of relative water content. Plant Physiol 53(2):258–260. https://doi.org/10.1104/pp.53.2.258
Sofy MR (2016) Effect of gibberellic acid, paclobutrazol and zinc on growth, physiological attributes and the antioxidant defense system of soybean (Glycine max L.) under salinity stress. Int J Plant Res 6:64–87. https://doi.org/10.5923/j.plant.20160603
Tasci E, Dinler BS (2020) Dehydroabietic acid mediated WRKY71 gene expressions and reactive oxygen species regulation in soybean under salinity. Acta Biol Crac Ser Bot. https://doi.org/10.24425/abcsb.2020.131664
Timmerman KP (1989) Molecular characterization of corn glutathione S-transferase isozymes involved in herbicide detoxication. ASPB 77(3):465–471. https://doi.org/10.1111/j.1399-3054.1989.tb05668.x
Toh S, Imamura A, Watanabe A, Nakabayashi K, Okamoto M, Jikumaru Y, Kawakami N (2008) High temperature-induced abscisic acid biosynthesis and its role in the inhibition of gibberellin action in Arabidopsis seeds. Plant Physiol 146(3):1368–1385. https://doi.org/10.1104/pp.107.113738
Tuna AL, Kaya C, Dikilitas M, Higgs D (2008) The combined effects of gibberellic acid and salinity on some antioxidant enzyme activities, plant growth parameters and nutritional status in maize plants. Environ Exp Bot 62(1):1–9. https://doi.org/10.1016/j.envexpbot.2007.06.007
Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E, Kobayashi M, Matsuoka M et al (2005) GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437(7059):693–698. https://doi.org/10.1038/nature04028
Uzal O, Yasar F (2017) Effects of GA3 hormone treatments on ion uptake and growth of pepper plants under cadmium stress. Appl Ecol Environ Res 15(4):1347–1357. https://doi.org/10.15666/aeer/1504_13471357
Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous poly-amines. Plant Sci 151:59–66. https://doi.org/10.1016/S0168-9452(99)00197-1
Wang H, Zhang G, Chen Y, Gao J, Sun YR, Sun MF, Chen JP (2019a) Exogenous application of gibberellic acid and ascorbic acid improved tolerance of okra seedlings to NaCl stress. Act Physiol Plant 41(6):93. https://doi.org/10.1007/s11738-019-2869-y
Wang R, Ma J, Zhang Q, Wu C, Zhao H, Wu Y, He G (2019) Genome-wide identification and expression profiling of glutathione transferase gene family under multiple stresses and hormone treatments in wheat (Triticum aestivum L.). BMC Genom 20(1):1–15. https://doi.org/10.1186/s12864-019-6374-x
Wilce MC, Feil SC, Board PG, Parker MW (1994) Crystallization and preliminary X-ray diffraction studies of a glutathione S-transferase from the Australian sheep blowfly. Lucilia Cuprina J Mol Biol 236(5):1407–1409. https://doi.org/10.1016/0022-2836(94)90067-1
Xu J, Xing XJ, Tian YS, Peng RH, Xue Y, Zhao W, Yao QH (2015) Transgenic Arabidopsis plants expressing tomato glutathione S-transferase showed enhanced resistance to salt and drought stress. PLOS ONE 10(9):e0136960. https://doi.org/10.1371/journal.pone.0136960
Yang G, Chen S, Li D, Gao X, Su L, Peng S, Zhai M (2019) Multiple transcriptional regulation of walnut JrGSTTau1 gene in response to osmotic stress. Physiol Plant 166(3):748–761. https://doi.org/10.1111/ppl.12833
Younesi O, Moradi A (2014) Effect of priming of seeds of Medicago sativa “Bami” with gibberellic acid on germination, seedlings growth and antioxidant enzymes activity under salinity stress. J Hortic Res. https://doi.org/10.2478/johr-2014-0034
Yu Q, Powles S (2014) Metabolism-based herbicide resistance and cross-resistance in crop weeds: a threat to herbicide sustainability and global crop production. Plant Physiol 166(3):1106–1118. https://doi.org/10.1104/pp.114.242750
Yuan K, Rashotte AM, Wysocka-Diller JW (2011) ABA and GA signaling pathways interact and regulate seed germination and seedling development under salt stress. Acta Physiol Plant 33(2):261–271. https://doi.org/10.1007/s11738-010-0542-6
Zettl R, Schell J, Palme K (1994) Photoaffinity labeling of Arabidopsis thaliana plasma membrane vesicles by 5-azido-[7-3H] indole-3-acetic acid: identification of a glutathione S-transferase. PNAS 91(2):689–693. https://doi.org/10.1073/pnas.91.2.689
Zhao C, Yang M, Wu X, Wang Y, Zhang R (2021) Physiological and transcriptomic analyses of the effects of exogenous melatonin on drought tolerance in maize (Zea mays L.). Plant Physiol Biochem 168:128–142. https://doi.org/10.1016/j.plaphy.2021.09.044
Funding
This work was also supported by the Sinop University Research Foundation (FEF-1901–21-004).
Author information
Authors and Affiliations
Contributions
BSD and HC designed the research. BSD, HC and ZS performed the analysis and wrote the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Seckin Dinler, B., Cetinkaya, H. & Secgin, Z. The regulation of glutathione s-transferases by gibberellic acid application in salt treated maize leaves. Physiol Mol Biol Plants 29, 69–85 (2023). https://doi.org/10.1007/s12298-022-01269-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12298-022-01269-2