Abstract
The beneficial roles of melatonin (Mel) and gibberellic acid (GA3) in the biosynthesis of photosynthetic pigments, osmoregulation, and methylglyoxal (MG) detoxification and antioxidant system were studied in tomato (Solanum lycopersicum L. cv. Five Star) seedlings under NaCl stress. The exogenous application of Mel (100 µM) and GA3 (1.4 µM) together more efficiently affected growth performance of seedlings under salt stress. The decreased chlorophyll (Chl) degradation and Chl-degrading enzyme (chlorophyllase) activity in seedlings receiving Mel plus GA3 resulted in increased Chl content by upregulating Chl synthesizing enzyme (δ-aminolevulinic acid dehydratase) under salinity. Exogenous Mel plus GA3 suppressed the overproduction of reactive oxygen species (ROS; superoxide and hydrogen peroxide) and activity of glycolate oxidase. Application of Mel with GA3 reduced MG content by enhancing the activity of enzymes (glyoxalase I and glyoxalase II) involved in the MG detoxification system. Both Mel and GA3 together protected seedlings from ROS induced damage by regulating Δ1-pyrroline-5-carboxylate synthetase activity, and content of proline (Pro) and glycine betaine (GB). Seedlings receiving Mel + GA3 exhibited a substantial upregulated activity of catalase, ascorbate peroxidase, glutathione reductase, dehydroascorbate reductase, monodehydroascorbate reductase, glutathione peroxidase, polyphenol oxidase and lipoxygenase, and redox homeostasis that reduced oxidative damage induced by salinity. These outcomes advocate that Mel and GA3 played beneficial roles in Chl, Pro and GB biosynthesis, and improved redox homeostasis, and MG detoxification and antioxidant system under salt stress.
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Alamri SA, Siddiqui MH, Al-Khaishany MY, Khan MN, Ali HM, Alakeel KA (2019) Nitric oxide-mediated cross-talk of proline and heat shock proteins induce thermotolerance in Vicia faba L. Environ Exp Bot 161:290–302. https://doi.org/10.1016/j.envexpbot.2018.06.012
Arnao MB, Hernández-Ruiz J (2018) Melatonin and its relationship to plant hormones. Ann Bot 121(2):195–207. https://doi.org/10.1093/aob/mcx114
Axelrod B, Cheesbrough TM, Laakso S (1981) Lipoxygenase from soybeans: EC 1.13.11.12 Linoleate:oxygen oxidoreductase. Methods Enzymol 71:441–451. https://doi.org/10.1016/0076-6879(81)71055-3
Babenko LM, Shcherbatiuk MM, Skaterna TD, Kosakivska IV (2017) Lipoxygenases and their metabolites in formation of plant stress tolerance. Ukr Biochem J 89(1):5–21. https://doi.org/10.15407/ubj89.01.005
Bates LS, Walden RP, Teare ID (1972) Rapid determination of free proline for water stress studies. Plant Soil 39(1):205–207
Bela K, Horvath E, Galle A, Szabados L, Tari I, Csiszar J (2015) Plant glutathione peroxidases: emerging role of the antioxidant enzymes in plant development and stress responses. J Plant Physiol 176:192–201. https://doi.org/10.1016/j.jplph.2014.12.014
Boeckx T, Winters AL, Webb KJ, Kingston-Smith AH (2015) Polyphenol oxidase in leaves: is there any significance to the chloroplastic localization? J Exp Bot 66(12):3571–3579. https://doi.org/10.1093/jxb/erv141
Bojović B, Đelić G, Topuzović M, Stanković M (2010) Effects of NaCl of on seed germiantion in some species from families Brassicaceae and Solanaceae. Kragujevac J Sci 32:83–87
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Campos CN, Avila RG, de Souza KRD, Azevedo LM, Alves JD (2019) Melatonin reduces oxidative stress and promotes drought tolerance in young Coffea arabica L. plants. Agric Water Manage 211:37–47. https://doi.org/10.1016/j.agwat.2018.09.025
Charest C, Phan CT (1990) Cold-acclimation of wheat (Triticum-Aestivum): properties of enzymes involved in proline metabolism. Physiol Plant 80(2):159–168. https://doi.org/10.1034/j.1399-3054.1990.800201.x
Çolak AM (2018) Effect of melatonin and gibberellic acid foliar application on the yield and quality of Jumbo blackberry species. Saudi J Biol Sci 25(6):1242–1246. https://doi.org/10.1016/j.sjbs.2018.06.008
Colebrook EH, Thomas SG, Phillips AL, Hedden P (2014) The role of gibberellin signalling in plant responses to abiotic stress. J Exp Biol 217(1):67–75. https://doi.org/10.1242/jeb.089938
Conklin PL (2001) Recent advances in the role and biosynthesis of ascorbic acid in plants. Plant Cell Environ 24(4):383–394. https://doi.org/10.1046/j.1365-3040.2001.00686.x
Cui LL, Lu YS, Li Y, Yang C, Peng XX (2016) Overexpression of glycolate oxidase confers improved photosynthesis under high light and high temperature in rice. Front Plant Sci 7:1165. https://doi.org/10.3389/fpls.2016.01165
Dhindsa RS, Plumbdhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane-permeability and lipid-peroxidation, and decreased levels of superoxide-dismutase and catalase. J Exp Bot 32(126):93–101. https://doi.org/10.1093/jxb/32.1.93
Elstner EF, Heupel A (1976) Formation of hydrogen-peroxide by isolated cell-walls from horseradish (Armoracia-Lapathifolia Gilib). Planta 130(2):175–180. https://doi.org/10.1007/Bf00384416
Fahnenstich H, Flugge UI, Maurino VG (2008a) Arabidopsis thaliana overexpressing glycolate oxidase in chloroplasts: H(2)O(2)-induced changes in primary metabolic pathways. Plant Signal Behav 3(12):1122–1125
Fahnenstich H, Scarpeci TE, Valle EM, Flugge UI, Maurino VG (2008b) Generation of hydrogen peroxide in chloroplasts of Arabidopsis overexpressing glycolate oxidase as an inducible system to study oxidative stress. Plant Physiol 148(2):719–729. https://doi.org/10.1104/pp.108.126789
Fang ZY, Bouwkamp JC, Solomos T (1998) Chlorophyllase activities and chlorophyll degradation during leaf senescence in non-yellowing mutant and wild type of Phaseolus vulgaris L. J Exp Bot 49(320):503–510. https://doi.org/10.1093/jexbot/49.320.503
Foyer CH, Bloom AJ, Queval G, Noctor G (2009) Photorespiratory metabolism: genes, mutants, energetics, and redox signaling. Annu Rev Plant Biol 60:455–484. https://doi.org/10.1146/annurev.arplant.043008.091948
Gao W, Feng Z, Bai Q, He J, Wang Y (2019) Melatonin-mediated regulation of growth and antioxidant capacity in salt-tolerant naked oat under salt stress. Int J Mol Sci. https://doi.org/10.3390/ijms20051176
Giri J (2011) Glycinebetaine and abiotic stress tolerance in plants. Plant Signal Behav 6(11):1746–1751. https://doi.org/10.4161/psb.6.11.17801
Grieve CM, Grattan SR (1983) Rapid assay for determination of water-soluble quaternary ammonium-compounds. Plant Soil 70(2):303–307. https://doi.org/10.1007/Bf02374789
Gupta R, Chakrabarty SK (2013) Gibberellic acid in plant: still a mystery unresolved. Plant Signal Behav. https://doi.org/10.4161/psb.25504
Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genom 2014:701596. https://doi.org/10.1155/2014/701596
Hasanuzzaman M, Hossain MA, Fujita M (2011) Nitric oxide modulates antioxidant defense and the methylglyoxal detoxification system and reduces salinity-induced damage of wheat seedlings. Plant Biotechnol Rep 5(4):353–365. https://doi.org/10.1007/s11816-011-0189-9
Hossain MA, Nakano Y, Asada K (1984) Monodehydroascorbate reductase in spinach-chloroplasts and its participation in regeneration of ascorbate for scavenging hydrogen-peroxide. Plant Cell Physiol 25(3):385–395
Hossain MA, Hossain MZ, Fujita M (2009) Stress-induced changes of methylglyoxal level and glyoxalase I activity in pumpkin seedlings and cDNA cloning of glyoxalase I gene. Aust J Crop Sci 3(2):53–64
Hossain MA, Hasanuzzaman M, Fujita M (2010) Up-regulation of antioxidant and glyoxalase systems by exogenous glycinebetaine and proline in mung bean confer tolerance to cadmium stress. Physiol Mol Biol Plants 16(3):259–272. https://doi.org/10.1007/s12298-010-0028-4
Jain M, Gadre R (2004) Inhibition of chlorophyll biosynthesis by mercury in excised etiolated maize leaf segments during greening: effect of 2-oxoglutarate. Indian J Exp Biol 42(4):419–423
Kalapos MP, Garzo T, Antoni F, Mandl J (1992) Accumulation of S-d-lactoylglutathione and transient decrease of glutathione level caused by methylglyoxal load in isolated hepatocytes. Biochim Biophys Acta 1135(2):159–164. https://doi.org/10.1016/0167-4889(92)90132-u
Kao WY, Tsai TT, Shih CN (2003) Photosynthetic gas exchange and chlorophyll a fluorescence of three wild soybean species in response to NaCl treatments. Photosynthetica 41(3):415–419. https://doi.org/10.1023/B:Phot.0000015466.22288.23
Kumar KB, Khan PA (1982) Peroxidase and polyphenol oxidase in excised ragi (Eleusine-Corcocana Cv Pr 202) leaves during senescence. Indian J Exp Biol 20(5):412–416
Kumar V, Shriram V, Hoque TS, Hasan MM, Burritt DJ, Hossain MA (eds) (2017) Glycinebetaine-mediated abiotic oxidative-stress tolerance in plants: physiological and biochemical mechanisms, vol 2. Stress signaling in plants: genomics and proteomics perspective. Springer, Cham. https://doi.org/10.1007/978-3-319-42183-4_5
Kuznetsov VV, Shevyakova NI (1999) Proline under stress: biological role, metabolism, and regulation. Russ J Plant Physiol 46(2):274–287
Li H, Teng RM, Liu JX, Yang RY, Yang YZ, Lin SJ, Han MH, Liu JY, Zhuang J (2019a) Identification and analysis of genes involved in auxin, abscisic acid, gibberellin, and brassinosteroid metabolisms under drought stress in tender shoots of tea plants. DNA Cell Biol. https://doi.org/10.1089/dna.2019.4896
Li JP, Liu J, Zhu TT, Zhao C, Li LY, Chen M (2019b) The role of melatonin in salt stress responses. Int J Mol Sci 20(7):1735. https://doi.org/10.3390/ijms20071735
Liang XW, Zhang L, Natarajan SK, Becker DF (2013) Proline mechanisms of stress survival. Antioxid Redox Sign 19(9):998–1011. https://doi.org/10.1089/ars.2012.5074
Liang CZ, Zheng GY, Li WZ, Wang YQ, Hu B, Wang HR, Wu HK, Qian YW, Zhu XG, Tan DX, Chen SY, Chu CC (2015) Melatonin delays leaf senescence and enhances salt stress tolerance in rice. J Pineal Res 59(1):91–101. https://doi.org/10.1111/jpi.12243
Lin YH, Pan KY, Hung CH, Huang HE, Chen CL, Feng TY, Huang LF (2013) Overexpression of ferredoxin, PETF, enhances tolerance to heat stress in Chlamydomonas reinhardtii. Int J Mol Sci 14(10):20913–20929. https://doi.org/10.3390/ijms141020913
Lu YS, Li Y, Yang QS, Zhang ZS, Chen Y, Zhang S, Peng XX (2014) Suppression of glycolate oxidase causes glyoxylate accumulation that inhibits photosynthesis through deactivating Rubisco in rice. Physiol Plant 150(3):463–476. https://doi.org/10.1111/ppl.12104
Magdah AG (2016) Impact of biostimulant and synthetic hormone gibberellic acid on molecular structure of Solanum melongena L. J Mol Biol Res 6(1):100–110. https://doi.org/10.5539/jmbr.v6n1p100
Matysik J, Alia BB, Mohanty P (2002) Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr Sci India 82(5):525–532
McFeeters RF, Chichester CO, Whitaker JR (1971) Purification and properties of chlorophyllase from Ailanthus altissima (tree-of-heaven). Plant Physiol 47(5):609–618
Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167(3):645–663. https://doi.org/10.1111/j.1469-8137.2005.01487.x
Nahar K, Hasanuzzaman M, Alam MM, Rahman A, Suzuki T, Fujita M (2016) Polyamine and nitric oxide crosstalk: antagonistic effects on cadmium toxicity in mung bean plants through upregulating the metal detoxification, antioxidant defense and methylglyoxal detoxification systems. Ecotoxicol Environ Saf 126:245–255. https://doi.org/10.1016/j.ecoenv.2015.12.026
Nakano Y, Asada K (1981) Hydrogen-peroxide is scavenged by ascorbate-specific peroxidase in spinach-chloroplasts. Plant Cell Physiol 22(5):867–880
Noctor G, Arisi ACM, Jouanin L, Foyer CH (1998) Manipulation of glutathione and amino acid biosynthesis in the chloroplast. Plant Physiol 118(2):471–482. https://doi.org/10.1104/pp.118.2.471
Okon OG (ed) (2019) Effect of salinity on physiological processes in plants, vol 56. Microorganisms in saline environments: strategies and functions. Soil biology. Springer, Cham. 10.1007/978-3-030-18975-4_10
Olmos E, Hernandez JA, Sevilla F, Hellin E (1994) Induction of several antioxidant enzymes in the selection of a salt-tolerant cell-line of pisum-sativum. J Plant Physiol 144(4–5):594–598. https://doi.org/10.1016/S0176-1617(11)82142-5
Paradiso A, Berardino R, de Pinto MC, Sanita di Toppi L, Storelli MM, Tommasi F, De Gara L (2008) Increase in ascorbate-glutathione metabolism as local and precocious systemic responses induced by cadmium in durum wheat plants. Plant Cell Physiol 49(3):362–374. https://doi.org/10.1093/pcp/pcn013
Principato GB, Rosi G, Talesa V, Giovannini E, Norton SJ (1987) A comparative study on glyoxalase II from vertebrata. Enzyme 37(3):164–168. https://doi.org/10.1159/000469255
Queiros F, Rodrigues JA, Almeida JM, Almeida DP, Fidalgo F (2011) Differential responses of the antioxidant defence system and ultrastructure in a salt-adapted potato cell line. Plant Physiol Biochem 49(12):1410–1419. https://doi.org/10.1016/j.plaphy.2011.09.020
Reiter RJ, Tan DX, Zhou Z, Cruz MHC, Fuentes-Broto L, Galano A (2015) Phytomelatonin: assisting plants to survive and thrive. Molecules 20(4):7396–7437. https://doi.org/10.3390/molecules20047396
Ronen R, Galun M (1984) Pigment extraction from lichens with dimethylsulfoxide (DMSO) and estimation of chlorophyll degradation. Environ Exp Bot 24(3):239–245. https://doi.org/10.1016/0098-8472(84)90004-2
Shahid SA, Zaman M, Heng L (eds) (2018) Soil salinity: historical perspectives and a world overview of the problem. Guideline for salinity assessment, mitigation and adaptation using nuclear and related techniques. Springer, Cham. https://doi.org/10.1007/978-3-319-96190-3_2
Shrivastava P, Kumar R (2015) Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci 22(2):123–131. https://doi.org/10.1016/j.sjbs.2014.12.001
Siddiqui MH, Khan MN, Mohammad F, Khan MMA (2008a) Role of nitrogen and gibberellin (GA3) in the regulation of enzyme activities and in osmoprotectant accumulation in Brassica juncea L. under salt stress. J Agron Crop Sci 194(3):214–224. https://doi.org/10.1111/j.1439-037X.2008.00308.x
Siddiqui MH, Mohammad F, Khan MN (2009) Morphological and physio-biochemical characterization of Brassica juncea L. Czern. & Coss. genotypes under salt stress. J Plant Interact 4(1):67–80. https://doi.org/10.1080/17429140802227992
Siddiqui MH, Mohammad F, Khan MN, Al-Whaibi MH, Bahkali AHA (2010) Nitrogen in relation to photosynthetic capacity and accumulation of osmoprotectant and nutrients in brassica genotypes grown under salt stress. Agric Sci China 9(5):671–680. https://doi.org/10.1016/S1671-2927(09)60142-5
Siddiqui MH, Al-Whaibi MH, Basalah MO (2011) Interactive effect of calcium and gibberellin on nickel tolerance in relation to antioxidant systems in Triticum aestivum L. Protoplasma 248(3):503–511. https://doi.org/10.1007/s00709-010-0197-6
Siddiqui MH, Mohammad F, Khan MM, Al-Whaibi MH (2012) Cumulative effect of nitrogen and sulphur on Brassica juncea L. genotypes under NaCl stress. Protoplasma 249(1):139–153. https://doi.org/10.1007/s00709-011-0273-6
Siddiqui MH, Alamri SA, Al-Khaishany MY, Al-Qutami MA, Ali HM, Al-Rabiah H, Kalaji HM (2017) Exogenous application of nitric oxide and spermidine reduces the negative effects of salt stress on tomato. Hortic Environ Biotechnol 58(6):537–547. https://doi.org/10.1007/s13580-017-0353-4
Siddiqui MH, Alamri SA, Al-Khaishany MYY, Al-Qutami MA, Ali HM, Al-Whaibi MH, Al-Wahibi MS, Alharby HF (2018) Mitigation of adverse effects of heat stress on Vicia faba by exogenous application of magnesium. Saudi J Biol Sci 25(7):1393–1401. https://doi.org/10.1016/j.sjbs.2016.09.022
Siddiqui MH, Alamri S, Al-Khaishany MY, Khan MN, Al-Amri A, Ali HM, Alaraidh IA, Alsahli AA (2019a) Exogenous melatonin counteracts NaCl-induced damage by regulating the antioxidant system, proline and carbohydrates metabolism in tomato seedlings. Int J Mol Sci. https://doi.org/10.3390/ijms20020353
Siddiqui MH, Alamri S, Alsubaie QD, Ali HM, Ibrahim AA, Alsadon A (2019b) Potential roles of melatonin and sulfur in alleviation of lanthanum toxicity in tomato seedlings. Ecotoxicol Environ Saf 180:656–667. https://doi.org/10.1016/j.ecoenv.2019.05.043
Takahama U, Oniki T (1992) Regulation of peroxidase-dependent oxidation of phenolics in the apoplast of spinach leaves by ascorbate. Plant Cell Physiol 33(4):379–387
Tnay G (2019) Too much salt: the growing threat that salinity poses to global food production. Future Directions International Pty Ltd., Dalkeith
Turcsányi E, Lyons T, Plochl M, Barnes J (2000) Does ascorbate in the mesophyll cell walls form the first line of defence against ozone? Testing the concept using broad bean (Vicia faba L.). J Exp Bot 51(346):901–910. https://doi.org/10.1093/jexbot/51.346.901
Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151(1):59–66. https://doi.org/10.1016/S0168-9452(99)00197-1
Wang P, Yin LH, Liang D, Li C, Ma FW, Yue ZY (2012) Delayed senescence of apple leaves by exogenous melatonin treatment: toward regulating the ascorbate-glutathione cycle. J Pineal Res 53(1):11–20. https://doi.org/10.1111/j.1600-079X.2011.00966.x
War AR, Paulraj MG, War MY, Ignacimuthu S (2011) Role of salicylic acid in induction of plant defense system in chickpea (Cicer arietinum L.). Plant Signal Behav 6(11):1787–1792. https://doi.org/10.4161/psb.6.11.17685
Wheeler AW, Humphries EC (1963) Effect of gibberellic acid on growth, gibberellin content, and chlorophyll content of leaves of potato (Solanum Tuberosum). J Exp Bot 14(40):132. https://doi.org/10.1093/jxb/14.1.132
Yamaguchi K, Nishimura M (2000) Reduction to below threshold levels of glycolate oxidase activities in transgenic tobacco enhances photoinhibition during irradiation. Plant Cell Physiol 41(12):1397–1406. https://doi.org/10.1093/pcp/pcd074
Yang XH, Wen XG, Gong HM, Lu QT, Yang ZP, Tang YL, Liang Z, Lu CM (2007) Genetic engineering of the biosynthesis of glycinebetaine enhances thermotolerance of photosystem II in tobacco plants. Planta 225(3):719–733. https://doi.org/10.1007/s00425-006-0380-3
Yu CW, Murphy TM, Lin CH (2003) Hydrogen peroxide-induced chilling tolerance in mung beans mediated through ABA-independent glutathione accumulation. Funct Plant Biol 30(9):955–963. https://doi.org/10.1071/Fp03091
Zhang N, Zhao B, Zhang HJ, Weeda S, Yang C, Yang ZC, Ren S, Guo YD (2013) Melatonin promotes water-stress tolerance, lateral root formation, and seed germination in cucumber (Cucumis sativus L.). J Pineal Res 54(1):15–23. https://doi.org/10.1111/j.1600-079X.2012.01015.x
Zhao HB, Su T, Huo LQ, Wei HB, Jiang Y, Xu LF, Ma FW (2015) Unveiling the mechanism of melatonin impacts on maize seedling growth: sugar metabolism as a case. J Pineal Res 59(2):255–266. https://doi.org/10.1111/jpi.12258
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The authors extend their appreciation to the Deanship of Scientific Research at King Saud University for funding this work through Research Group No. RG-1439-041. The authors thank the Deanship of Scientific Research and RSSU at King Saud University for their technical support
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MHS conceived and designed experiment and made important contributions to the discussion and also prepared first draft of manuscript. QDA and HMA participated in the preparation of experimental pots and reagents, and also in morpho-physiological and biochemical analysis. SA helped in statistical calculation and data analysis. SA provided intellectual input, critical reading and editing of the manuscript.
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Siddiqui, M.H., Alamri, S., Alsubaie, Q.D. et al. Melatonin and Gibberellic Acid Promote Growth and Chlorophyll Biosynthesis by Regulating Antioxidant and Methylglyoxal Detoxification System in Tomato Seedlings Under Salinity. J Plant Growth Regul 39, 1488–1502 (2020). https://doi.org/10.1007/s00344-020-10122-3
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DOI: https://doi.org/10.1007/s00344-020-10122-3