Abstract
The objective of the present study was to assess the effects of exogenous application of 1 mM Jasmonic acid (JA), an endogenous plant growth regulator, on mitigation of oxidative and osmotic stresses caused by various levels of NaCl: none (0 mM), light (50 mM), moderate (150 mM), and severe (300 mM) in roselle (Hibiscus sabdariffa L.) seedlings. Salt stress without any change in leaf water content negatively affected seedlings growth from the aspect of plant height, root length, leaf morphological properties, plant biomass and levels of pigments, reducing sugars, starch, proteins and free amino acids, but accumulated higher levels of non-reducing sugars, total phenols, anthocyanins, flavonoids, proline and increased activities of both enzymatic and non-enzymatic antioxidants, such as ascorbate peroxidase (APX), pyrogallol peroxidase (PPX) and polyphenol oxidase (PPO). JA-treated seedlings exhibited a significant increase in growth parameters and activities of APX and PPX under salt stress, with hyper-accumulation of metabolite levels, but accumulated lower amounts of dry matter in roots and decreased the activity of PPO. These results clearly showed that exogenous JA treatment protected roselle seedlings against salt-induced damage through up-regulating the activity of H2O2-decomposing enzymes, osmoprotectants biosynthesis, and the accumulation of metabolites.
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Abdelgawad ZA, Khalafaallah AA, Abdallah MM (2014) Impact of methyl Jasmonate on antioxidant activity and some biochemical aspects of maize plant grown under water stress condition. Agri Sci 5:1077–1088. https://doi.org/10.4236/as.2014.512117
Ahanger MA, Agarwal RM (2017) Salinity stress induced alterations in antioxidant metabolism and nitrogen assimilation in wheat (Triticum aestivum L) as influenced by potassium supplementation. Plant Physiol Biochem 115:449–460. https://doi.org/10.1016/j.plaphy.2017.04.017
Ahanger MA, Tyagi SR, Wani MR, Ahmad P (2014) Drought tolerance: role of organic osmolytes, growth regulators, and mineral nutrients. In: Physiological mechanisms and adaptation strategies in plants under changing environment. Springer, New York, pp 25–55
Ahanger MA, Agarwal RM, Tomar NS, Shrivastava M (2015) Potassium induces positive changes in nitrogen metabolism and antioxidant system of oat (Avena sativa L cultivar Kent). J Plant Interact 10:211–223. https://doi.org/10.1080/17429145.2015.1056260
Ahanger MA, Tittal M, Mir RA, Agarwal RM (2017) Alleviation of water and osmotic stress-induced changes in nitrogen metabolizing enzymes in Triticum aestivum L. cultivars by potassium. Protoplasma 254:1953–1963. https://doi.org/10.1007/s00709-017-1086-z
Ahmad P, Jhon R (2005) Effect of salt stress on growth and biochemical parameters of Pisum sativum L. Arc Agro Soil Sci 51:665–672. https://doi.org/10.1080/03650340500274151
Ahmad P, Ozturk M, Sharma S, Gucel S (2014) Effect of sodium carbonate-induced salinity–alkalinity on some key osmoprotectants, protein profile, antioxidant enzymes, and lipid peroxidation in two mulberry (Morus alba L.) cultivars. J Plant Interact 9:460–467. https://doi.org/10.1080/17429145.2013.855271
Ahmad P, Hashem A, Abd-Allah EF, Alqarawi AA, John R, Egamberdieva D, Gucel S (2015) Role of Trichoderma harzianum in mitigating NaCl stress in Indian mustard (Brassica juncea L) through antioxidative defense system. Front Plant Sci 6:868. https://doi.org/10.3389/fpls.2015.00868
Ahmad P, Abdel Latef AA, Hashem A, Abd-Allah EF, Gucel S, Tran LSP (2016a) Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Front Plant Sci 7:347. https://doi.org/10.3389/fpls.2016.00347
Ahmad P, Rasool S, Gul A, Sheikh SA, Akram NA, Ashraf M, Kazi AM, Gucel S (2016b) Jasmonates: multifunctional roles in stress tolerance. Front Plant Sci 7:813. https://doi.org/10.3389/fpls.2016.00813
Ahmad P, Alyemeni MN, Ahanger MA, Wijaya L, Alam P, Kumar A, Ashraf M (2018) Up-regulation of antioxidant and glyoxalase systems mitigates NaCl stress in Brassica juncea by supplementation of zinc and calcium. J Plant Interact 13:151–162. https://doi.org/10.1080/17429145.2018.1441452
Anjum SA, Wang L, Farooq M, Khan I, Xue L (2011) Methyl jasmonate-induced alteration in lipid peroxidation, antioxidative defence system and yield in soybean under drought. J Agron Crop Sci 197:296–301. https://doi.org/10.1111/j.1439-037X.2011.00468.x
Arnon D (1949) Copper enzymes in isolated chloroplasts: polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15. https://doi.org/10.1104/pp.24.1.1
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free Proline for water stress studies. Plant Soil 39:205–208. https://doi.org/10.1007/BF00018060
Bradford M (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. https://doi.org/10.1006/abio.1976.9999
Chang CC, Yang MH, Wen HM, Chern JC (2002) Estimation of total flavonoid content in propolis by two complementary colorimetric methods. J Food Drug Anal 10:178–182
Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560. https://doi.org/10.1093/aob/mcn125
Chen G, Asada K (1992) Inactivation of ascorbate peroxidase by thoils requires hydrogen peroxide. Plant Cell Physiol 33:117–123. https://doi.org/10.1093/oxfordjournals.pcp.a078229
Chung YC, Chen SJ, Hsu CK, Chang CT, Chou ST (2005) Studies on the antioxidative activity of Graptopetalum paraguayense E. Walther. Food Chem 91:419–424. https://doi.org/10.1016/j.foodchem.2004.06.022
Chutipaijit S, Cha-um S, Sompornpailin K (2009) Differential accumulations of proline and flavonoids in indica rice varieties against salinity. Pak J Bot 41:2497–2506
Creelman RA, Mullet JE (1997) Biosynthesis and action of jasmonates in plants. Annu Rev Plant Physiol Plant Mol Biol 48:355–381. https://doi.org/10.1146/annurev.arplant.48.1.355
Da-Costa-Rocha I, Bonnlaender B, Sievers H, Pischel I, Heinrich M (2014) Hibiscus sabdariffa L. a phytochemical and pharmacological review. Food Chem 165:424–443. https://doi.org/10.1016/j.foodchem.2014.05.002
Dar TA, Uddin M, Khan MMA, Hakeem KR, Jaleel H (2015) Jasmonates counter plant stress: a review. Environ Exp Bot 115:49–57. https://doi.org/10.1016/j.envexpbot.2015.02.010
De Costa W, Zeorb C, Hartung W, Schubert S (2007) Salt resistance is determined by osmotic adjustment and abscisic acid in newly developed maize hybrids in the first phase of salt stress. Physiol Plant 131:311–321. https://doi.org/10.1111/j.1399-3054.2007.00962.x
Doan AT, Ervin G, Felton G (2004) Temporal effects of jasmonate induction of anti-herbivore defense in Physalis angulata: seasonal and ontogenetic gradients. Biochem Systematics and Ecology 32:117–126. https://doi.org/10.1016/S0305-1978(03)00142-X
Einali A (2018) The induction of salt stress tolerance by propyl gallate treatment in green microalga Dunaliella bardawil, through enhancing ascorbate pool and antioxidant enzymes activity. Protoplasma 255:601–611. https://doi.org/10.1007/s00709-017-1173-1
Einali A, Valizadeh J (2017) Storage reserve mobilization, gluconeogenesis, and oxidative pattern in dormant pistachio (Pistacia vera L.) seeds during cold stratification. Trees 31:659–671. https://doi.org/10.1007/s00468-016-1498-y
Einali A, Azizian-Shermeh O, Ghasemi A (2018) Phytochemical screening and antimicrobial activities of Periploca aphylla Decne, Persian walnut (Juglans regia L.) and oleander (Nerium indicum mill.) leaf extracts. J Food Meas Charact 12:1350–1359. https://doi.org/10.1007/s11694-018-9749-9
El Khallal SM (2001) Some physiological roles of jasmonic acid in adaptation of pea seedlings to salt stress. Egypt J Biotechnol 10:249–271
Fedina IS, Benderliev KM (2000) Response of Scenedesmus incrassatulus to salt stress as affected by methyl jasmonate. Biol Plant 43:625–627. https://doi.org/10.1023/A:1002816502941
Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319. https://doi.org/10.1093/jxb/erh003
Goffman FD, Bergman CJ (2004) Rice kernel phenolic content and its relationship with antiradical efficiency. J Sci Food Agric 84:1235–1240. https://doi.org/10.1002/jsfa.1780
Gould KS, Markham KR, Smith RH, Goris JJ (2000) Functional role of anthocyanins in the leaves of Quintinia serrata a. Cunn J Exp Bot 51:1107–1115. https://doi.org/10.1093/jexbot/51.347.1107
Hanaka A, Maksymiec W, Bednarek W (2015) The effect of methyl jasmonate on selected physiological parameters of copper-treated Phaseolus coccineus plants. Plant Growth Regul 77:167–177. https://doi.org/10.1007/s10725-015-0048-8
Handel EV (1968) Direct micro determination of sucrose. Anal Biochem 22:280–283. https://doi.org/10.1016/0003-2697(68)90317-5
Henkes GJ, Thorpe MR, Minchin PEH, Schurr U, Rose USR (2008) Jasmonic acid treatment to part of the root system is consistent with simulated leaf herbivory, diverting recently assimilated carbon towards untreated roots within an hour. Plant Cell Environ 31:1229–1236. https://doi.org/10.1111/j.1365-3040.2008.01828.x
Hsu SY, Hsu YT, Kao CH (2003) The effect of polyethylene glycol on proline accumulation in rice leaves. Biol Plant 46:73–78. https://doi.org/10.1023/A:1022362117395
Huang H, Gao H, Liu B, Qi T, Tong J, Xiao L, Xie D, Song S (2017) Arabidopsis MYB24 regulates Jasmonate-mediated stamen development. Front Plant Sci 8:1525. https://doi.org/10.3389/fpls.2017.01525
Iqbal N, Umar S, Khan NA (2015) Nitrogen availability regulates proline and ethylene production and alleviates salinity stress in mustard (Brassica juncea). J Plant Physiol 178:84–91. https://doi.org/10.1016/j.jplph.2015.02.006
Kang DJ, Seo YJ, Lee JD, Ishii R, Kim KU, Shin DH, Park SK, Jang SW, Lee IJ (2005) Jasmonic acid differentially affects growth, ion uptake and abscisic acid concentration in salt tolerant and salt sensitive rice cultivars. J Agron Crop Sci 191:273–282. https://doi.org/10.1111/j.1439-037X.2005.00153.x
Kaur H, Sharma P, Sirhindi G (2013) Sugar accumulation and its regulation by jasmonic acid in Brassica napus L. under salt stress. J Stress Physiol Biochem 9:53–64
Khan MIR, Asgher M, Khan NA (2014) Alleviation of salt-induced photosynthesis and growth inhibition by salicylic acid involves glycinebetaine and ethylene in mungbean (Vigna radiata L.). Plant Physiol Biochem 80:67–74. https://doi.org/10.1016/j.plaphy.2014.03.026
Khan N, Bano A, Babar MA (2017) The root growth of wheat plants, the water conservation and fertility status of sandy soils influenced by plant growth promoting rhizobacteria. Symbiosis 72:195–205. https://doi.org/10.1007/s13199-016-0457-0
Kovacik J, Klejdus B, Stork F, Hedbavny J, Backor M (2011) Comparison of methyl jasmonate and cadmium effect on selected physiological parameters in Scenedesmus quadricauda (chlorophyta, chlorophyceae). J Phycol 47:1044–1049. https://doi.org/10.1111/j.1529-8817.2011.01027.x
Kukic J, Popovic V, Petrovic S, Mucaji P, Ciric A, Stojkovic D, Sokovic M (2008) Antioxidant and antimicrobial activity of Cynara cardunculus extracts. Food Chem 107:861–868. https://doi.org/10.1016/j.foodchem.2007.09.005
Kumari M, Asthir B (2016) Transformation of sucrose to starch and protein in Rice leaves and grains under two establishment methods. Rice Sci 23:255–265. https://doi.org/10.1016/j.rsci.2016.08.003
Li JT, Qiu ZB, Zhang XW, Wang LS (2011) Exogenous hydrogen peroxide can enhance tolerance of wheat seedlings to salt stress. Acta Physiol Plant 33:835–842. https://doi.org/10.1007/s11738-010-0608-5
Liao JL, Zhou HW, Zhang HY, Zhong PA, Huang YJ (2014) Comparative proteomic analysis of differentially expressed proteins in the early milky stage of rice grains during high temperature stress. J Exp Bot 65:655–671. https://doi.org/10.1093/jxb/ert435
Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. Curr Protoc Food Anal Chem:F4.3.1–F4.3.8. https://doi.org/10.1002/0471142913.faf0403s01
Lin J, Wang Y, Sun S, Mu C, Yan X (2017) Effects of arbuscular mycorrhizal fungi on the growth, photosynthesis and photosynthetic pigments of Leymus chinensis seedlings under salt-alkali stress and nitrogen deposition. Sci Total Environ 576:234–241. https://doi.org/10.1016/j.scitotenv.2016.10.091
Mahmood M, Bidabadi SS, Ghobadi C, Gray DJ (2012) Effect of methyl jasmonate treatments on alleviation of polyethyleneglycol-mediated water stress in banana (Musa acuminata cv. ‘Berangan’, AAA) shoot tip cultures. Plant Growth Regul 68:161–169. https://doi.org/10.1007/s10725-012-9702-6
Manan ACM, Pervez MA, Ahmad R (2016) Methyl jasmonate brings about resistance against salinity stressed tomato plants by altering biochemical and physiological processes. Pak J Agri Sci 53:35–41. https://doi.org/10.21162/PAKJAS/16.4441
Markwell MAK, Hass SM, Tolbert NE, Bieber LL (1981) Protein determination in membrane and lipoprotein samples: manual and automated procedures. Meth Enzymol 72:296–303. https://doi.org/10.1016/S0076-6879(81)72018-4
McCready RM, Guggolz J, Silviera V, Owens HS (1950) Determination of starch and amylose in vegetables. Anal Chem 22:1156–1158. https://doi.org/10.1021/ac60045a016
Meena RK, Verulkar SB, Chandel G (2012) Nutrient characters analysis in rice genotypes under different environmental conditions. Bull Environ Pharmacol Life Sci 1:61–64
Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugars. Anal Chem 31:426–428. https://doi.org/10.1021/acsbiomaterials.9b00796
Mishra A, Mandoli A, Jha B (2008) Physiological characterization and stress-induced metabolic responses of Dunaliella salina isolated from salt pan. J Ind Microbiol Biotechnol 35:1093–1101. https://doi.org/10.1007/s10295-008-0387-9
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498. https://doi.org/10.1016/j.tplants.2004.08.009
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Pattanagul W, Thitisaksakul M (2008) Effect of salinity stress on growth and carbohydrate metabolism in three rice (Oryza sativa L.) cultivars differing in salinity tolerance. Indian J Exp Biol 46:736–742
Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295. https://doi.org/10.1016/j.pbi.2011.02.001
Petridis A, Therios I, Samouris G, Tananaki C (2012) Salinity-induced changes in phenolic compounds in leaves and roots of four olive cultivars (Olea europaea L.) and their relationship to antioxidant activity. Environ Exp Bot 79:37–43. https://doi.org/10.1016/j.envexpbot.2012.01.007
Porra RJ, Schafer W, Cmiel E, Katheder I, Scheer H (1994) The derivation of the formyl-group oxygen of chlorophyll b in higher plants from molecular oxygen. Achievement of high enrichment of the 7-formyl-group oxygen from 18O2 in greening maize leaves. Eur J Biochem 219:671–679. https://doi.org/10.1111/j.1432-1033.1994.tb19983.x
Qiu Z, Guo J, Zhu A, Zhang L, Zhang M (2014) Exogenous jasmonic acid can enhance tolerance of wheat seedlings to salt stress. Ecotox Environ Safety 104:202–208. https://doi.org/10.1016/j.ecoenv.2014.03.014
Schmidt L, Hummel GM, Schöttner S, Schurr U, Walter A (2010) Jasmonic acid does not mediate root growth responses to wounding in Arabidopsis thaliana. Plant Cell Environ 33:104–116. https://doi.org/10.1111/j.1365-3040.2009.02062.x
Schubert S (2011) Salt resistance of crop plants: physiological characterization of a multigenic trait. In: Hawkesford MJ, Barraclough P (eds) The molecular and physiological basis of nutrient use efficiency in crops. Wiley-Blackwell, Oxford, pp 443–455
Shahzad AN, Pitann B, Ali H, Qayyum MF, Fatima A, Bakhat HF (2015) Maize genotypes differing in salt resistance vary in Jasmonic acid accumulation during the first phase of salt stress. J Agro Crop Sci:443–451. https://doi.org/10.1111/jac.12134
Singh PK, Gautam S (2013) Role of salicylic acid on physiological and biochemical mechanism of salinity stress tolerance in plants. Acta Physiol Plant 35:2345–2353. https://doi.org/10.1007/s11738-013-1279-9
Singleton VL, Orthofer R, Lamuela-Raventos RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin–Ciocalteau reagent. Methods Enzymol 299:152–178. https://doi.org/10.1016/S0076-6879(99)99017-1
Sirhindi G, Mir MA, Abd-Allah EF, Ahmad P, Gucel S (2016) Jasmonic acid modulates the physio-biochemical attributes, antioxidant enzyme activity, and gene expression in glycine max under nickel toxicity. Front Plant Sci 7:591. https://doi.org/10.3389/fpls.2016.00591
Stone SL, Gifford DJ (1997) Structural and biochemical changes in loblolly pine (Pinus taeda L.) seeds during germination and early seedling growth: I. storage protein reserves. Int J Plant Sci 158:727–737. https://doi.org/10.1086/314158
Thakur M, Sharma AD (2005) Salt stress and phytohormone (ABA)-induced changes in germination, sugars and enzymes of carbohydrate metabolism in Sorghum bicolor L. Moench seeds J Agric Soc Sci 1:89–93
Thaler JS, Stout MJ, Karban R, Duffey SS (2001) Jasmonate-mediated induced plant resistance affects a community of herbivores. Ecol Entom 26:312–324. https://doi.org/10.1046/j.1365-2311.2001.00324.x
Triantaphylides C, Havaux M (2009) Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci 14:219–228. https://doi.org/10.1016/j.tplants.2009.01.008
Trivellini A, Gordillo B, Rodríguez-Pulido FJ, Borghesi E, Ferrante A, Vernieri P, Quijada-Morin N, González-Miret ML, Heredia FJ (2014) Effect of salt stress in the regulation of anthocyanins and color of hibiscus flowers by digital image analysis. Journal of Agricultural Food Chemistry 62:6966–6974. https://doi.org/10.1021/jf502444u
Velitcukova M, Fedina I (1998) Response of photosynthesis of Pisum sativum to salt stress as affected by methyl jasmonate. Photosynthetica 35:89–97. https://doi.org/10.1023/A:1006878016556
Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35:753–759. https://doi.org/10.1007/s00726-008-0061-6
Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Close TJ (2007) Large-scale expression profiling and physiological characterization of jasmonic acid-mediated adaptation of barley to salinity stress. Plant Cell Environ 30:410–421. https://doi.org/10.1111/j.1365-3040.2006.01628.x
Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697. https://doi.org/10.1093/aob/mcm079
Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in annals of botany. Ann Bot 111:1021–1058. https://doi.org/10.1093/aob/mct067
Xu G, Zhang Y, Sun J, Shao H (2016) Negative interactive effects between biochar and phosphorus fertilization on phosphorus availability and plant yield in saline sodic soil. Sci Total Environ 568:910–915. https://doi.org/10.1016/j.scitotenv.2016.06.079
Yang ZB, He C, Ma Y, Herde M, Ding Z (2017) Jasmonic acid enhances Al-induced root growth inhibition. Plant Physiol 173:1420–1433. https://doi.org/10.1104/pp.16.01756
Yemm EW, Cocking EC (1955) The determination of amino acids with Ninhydrin. Analyst 80:209–213. https://doi.org/10.1039/AN9558000209
Yoon JY, Hamayun M, Lee SK, Lee IJ (2009) Methyl jasmonate alleviated salinity stress in soybean. J Crop Sci Biotechnol 12:63–68. https://doi.org/10.1007/s12892-009-0060-5
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We would like to thank the USB Deputy of Research for financial support to Sh. Sheyhakinia in the form of grants for M.Sc. research project.
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Sheyhakinia, S., Bamary, Z., Einali, A. et al. The induction of salt stress tolerance by jasmonic acid treatment in roselle (Hibiscus sabdariffa L.) seedlings through enhancing antioxidant enzymes activity and metabolic changes. Biologia 75, 681–692 (2020). https://doi.org/10.2478/s11756-020-00444-8
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DOI: https://doi.org/10.2478/s11756-020-00444-8