Wang Feibing, Wan Chenzhong, Wu Wenya, Yang Shasha, Chen Xinhong
Keywords:
MT, Okra, ROS, Salt tolerance
Melatonin (MT) is a ubiquitous molecule with pleiotropic roles in plant adaption to stress. However, physiological and biochemical mechanisms of enhancing salt tolerance of okra plants based on application of MT is poorly understood. In this study, the application of the investigated 100 µM MT significantly improved salt tolerance of okra plants based on the germination rates and culture pot experiment under salt stress. Based on optimal concentration of MT inducing salt tolerance of okra plants, application of 5 mM DPI and 100 µM MT + 5 mM DPI, respectively, significantly increased salt tolerance of okra plants. Assays on the content of component matter indicated the significant increases in proline, photosynthetic pigment, K+, relative water, glutathione (GSH) and ascorbic acid (AsA) content and the significant decreases in Na+, hydrogen peroxide (H2O2), superoxide radicals (O2−) and malondialdehyde (MDA) content and electrolyte leakage rates were observed in okra plants with 100 µM MT under salt stress. Enzymatic activities in terms of pyrroline-5-carboxylate synthase (P5CS), superoxide dismutase (SOD), glutathione peroxidase (GPX), catalase (CAT), glutathione reductase (GR), ascorbate peroxidase (APX) and peroxidase (POD) activities were significantly increased in okra plants by applied MT under salt stress. Furthermore, the marked decrease of H2O2, O2− and MDA content, and the significant increase of CAT, GR and APX activities and GSH and ASA content involved in ASA-GSH cycle were observed in MT-okra, DPI-okra and MT + DPI-okra plants under salt stress. H2O2 acted a toxic accumulation of ROS rather than as a second messenger for signal transduction in okra plants. These results demonstrate that exogenous MT increases the accumulation of proline and ratio of K+/Na+, which enhance salt tolerance of okra plants, by regulating osmotic balance and ion homeostasis, protecting membrane integrity and photosynthesis and activating ROS scavenging system. As a conclusion, treating okra plants with 100 µM MT could alleviate the harmful effects of salinity stress.
(*Only SPR Life Members can get full access.)
Ahmad S, Su W, Kamran M, Ahmad I, Meng X, Wu X, Javed T, Han Q (2020) Foliar application of melatonin delay leaf senescence in maize by improving the antioxidant defense system and enhancing photosynthetic capacity under semi-arid regions. Protoplasma 257:1079–1092
Ahmadi M, Souri MK (2018) Growth and mineral content of coriander (Coriandrum sativum L.) plants under mild salinity with different salts. Acta Physiol Plant 40:194
Ahmadi M, Souri MK (2019) Nutrient uptake, proline content and antioxidant enzymes activity of pepper (Capsicum annuum L.) under higher electrical conductivity of nutrient solution created by nitrate and chloride salts of potassium and calcium. Acta Sci Pol-Hortoru 18:113–122
Alia, Mohanty P, Matysik J (2001) Effect of proline on the production of singlet oxygen. Amino Acids 21:195–200
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
Azevedo Neto AD, Prisco JT, Eneas-Filho J, Abreu CD, Gomes-Filho E (2006) Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ Exp Bot 56:87–94
Csiszar J, Brunner S, Horvath E, Bela K, Kodmon P, Riyazuddin R, Galle A, Hurton A, Papdi C, Szabados L (2018) Exogenously applied salicylic acid maintains redox homeostasis in salt- stressed Arabidopsis gr1 mutants expressing cytosolic roGFP1. Plant Growth Regul 86:181–194
De Ronde JA, Cress WA, Krüger GHJ, Strasser RJ, Van Staden J (2004) Photosynthetic response of transgenic soybean plants, containing an Arabidopsis P5CR gene, during heat and drought stress. J Plant Physiol 161:1211–1224
Debnath B, Hussain M, Li M, Lu X, Sun Y, Qiu D (2018) Exogenous melatonin improves fruit quality features, health promoting antioxidant compounds and yield traits in tomato fruits under acid rain stress. Molecules 23:1868
Debouba M, Gouia H, Suzuki A, Ghorbel MH (2006) NaCl stress effects on enzymes involved in nitrogen assimilation pathway in tomato ‘Lycopersicon esculentum’ seedlings. J Plant Physiol 163:1247–1258
Feng Y, Chen X, He Y, Kou X, Xue Z (2019) Effects of exogenous trehalose on the metabolism of sugarand abscisic acid in tomato seedlings under salt stress. Trans Tianjin Univ 25:451–471
Gao S, Yuan L, Zhai H, Liu CL, He SZ, Liu QC (2011) Transgenic sweetpotato plants expressing an LOS5 gene are tolerant to salt stress. Plant Cell Tiss Org 107:205–213
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Bioch 48:909–930
Hatami E, Shokouhian AA, Ghanbari AR, Naseri LA (2018) Alleviating salt stress in almond rootstocks using of humic acid. Sci Hortic 237:296–230
Hayzer DJ, Leisinger T (1980) The gene-enzyme relationships of proline biosynthesis in Escherichia coli. J Gen Appl Microbiol 118:287–293
Hossain MS, Li J, Sikdar A, Hasanuzzaman M, Uzizerimana F, Muhammad I, Yuan Y, Zhang C, Wang C, Feng B (2020) Exogenous melatonin modulates the physiological and biochemical mechanisms of drought tolerance in Tartary Buckwheat (Fagopyrum tataricum (L.) Gaertn). Molecules 25:2828
Hosseini MS, Samsampour D, Zahedi SM, Zamanian K, Rahman MM, Mostofa MG, Tran LSP (2021) Melatonin alleviates drought impact on growth and essential oil yield of lemon verbena by enhancing antioxidant responses, mineral balance and abscisic acid content. Physiol Plant 172(2):1363–1375
Huang J, Sun S, Xu D, Lan H, Sun H, Wang Z, Bao Y, Wang J, Tang H, Zhang H (2012) A TFIIIA-type zinc finger protein confers multiple abiotic stress tolerances in transgenic rice (Oryza sativa L.). Plant Mol Biol 80:337–350
Hussain HA, Men S, Hussain S, Chen Y, Ali S, Zhang S, Zhang K, Li Y, Xu Q, Liao C, Wang L (2019) Interactive effects of drought and heat stresses on morpho-physiological attributes, yield, nutrient uptake and oxidative status in maize hybrids. Sci Rep 9:3890
James RA, Rivelli AR, Munns R, Caemmerer SV (2002) Factors affecting CO2 assimilation, leaf injury and growth in salt-stressed durum wheat. Funct Plant Biol 29:1393–1403
Jiang D, Lu B, Liu LT, Duan WJ, Meng YJ, Li J, Zhang K, Sun HC, Zhang YJ, Dong HZ, Bai ZY, Li CD (2021) Exogenous melatonin improves the salt tolerance of cotton by removing active oxygen and protecting photosynthetic organs. BMC Plant Biol 21:331
Jiang Y, Qiu Y, Hu Y, Yu D (2016) Heterologous expression of AtWRKY57 confers drought tolerance in Oryza sativa. Front Plant Sci 7:145
Kang C, He SZ, Zhai H, Li RJ, Zhao N, Liu QC (2018) A sweetpotato auxin response factor gene (IbARF5) is involved in carotenoid biosynthesis and salt and drought tolerance in transgenic Arabidopsis. Front Plant Sci 9:1307
Kang HM, Saltveit ME (2001) Activity of enzymatic antioxidant defense systems in chilled and heat shocked cucumber seedling radicles. Physiol Plant 113:548–556
Kostopoulou Z, Therios I, Roumeliotis E, Kanellis AK, Molassiotis A (2015) Melatonin combined with ascorbic acid provides salt adaptation in Citrus aurantium L. seedlings. Plant Physiol Biochem 86:155–165
Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608
Lang D, Yu X, Jia X, Li Z, Zhang X (2020) Methyl jasmonate improves metabolism and growth of NaCl-stressed Glycyrrhiza uralensis seedlings. Sci Hortic 266:109287
Lawlor DW (2002) Limitation to photosynthesis in water-stressed leaves: stomata vs. metabolism and the role of ATP. Ann Bot 89:871–885
Li G, Ye YX, Ren XQ, Qi MY, Zhao HY, Zhou Q, Chen XH, Wang J, Yuan CY, Wang FB (2020) The rice Aux/IAA transcription factor gene OsIAA18 enhances salt and osmotic tolerance in Arabidopsis. Biol Plant 64:454–464
Li J, Guo X, Zhang M, Wang X, Zhao Y, Yin Z, Zhang Z, Wang Y, Xiong H, Zhang H, Todorovskac E, Li Z (2018) OsERF71 confers drought tolerance via modulating aba signaling and proline biosynthesis. Plant Sci 270:131–139
Li J, Li Y, Yin Z, Jiang J, Zhang M, Guo X, Ye Z, Zhao Y, Xiong H, Zhang Z, Shao Y, Jiang C, Zhang H, An G, Paek NC, Ali J, Li Z (2017) OsASR5 enhances drought tolerance through a stomatal closure pathway associated with ABA and H2O2 signalling in rice. Plant Biotechnol J 15:183–196
Li ZJ, Fu XY, Tian YS, Xu J, Gao JJ, Wang B, Han HJ, Wang LJ, Zhang FJ, Zhu YM, Huang YN, Peng RH, Yao QH (2019) Overexpression of a trypanothione synthetase gene from Trypanosoma cruzi, TcTrys, confers enhanced tolerance to multiple abiotic stresses in rice. Gene 710:279–290
Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscop. Current Protocols in Food Analytical Chemistry1
Liu DG, He SZ, Zhai H, Wang LJ, Zhao Y, Wang B, Li RJ, Liu QC (2014) Overexpression of IbP5CR enhances salt tolerance in transgenic sweetpotato. Plant Cell Tiss Org 117:1–16
Liu Y, Ji X, Nie X, Qu M, Zheng L, Tan Z, Zhao H, Huo L, Liu S, Zhang B, Wang Y (2015) Arabidopsis AtbHLH112 regulates the expression of genes involved in abiotic stress tolerance by binding to their E-box and GCG-box motifs. New Phytol 207:692–709
Ma XH, Zhang J, Zhang HW, Chen B, Wen XY, Xu ZC (2019) Exogenous MeJA improves cold tolerance of tobacco by inhibiting H2O2 accumulation. Acta Agron Sinica 45:411
Martinez V, Nieves-Cordones M, Lopez-Delacalle M, Rodenas R, Mestre TC, Garcia- Sanchez F, Rubio F, Nortes PA, Mittler R, Rivero RM (2018) Tolerance to stress combination in tomato plants: new insights in the protective role of melatonin. Molecules 23:53
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Moradi F, Ismail AM (2007) Responses of photosynthesis, chlorophyll fluorescence and ROS-scavenging systems to salt stress during seedling and reproductive stages in rice. Ann Bot 99:1161–1173
Mostofa MG, Hossain MA, Fujita M (2015) Trehalose pretreatment induces salt tolerance in rice (Oryza sativa L.) seedlings: oxidative damage and co-induction of antioxidant defense and glyoxalase systems. Protoplasma 252:461–475
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681
Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349
Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295
Penna S (2003) Building stress tolerance through over-producing trehalose in transgenic plants. Trends Plant Sci 8:353–357
Poor P, Gemes K, Horvath F, Szepesi A, 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 Biol 13:105–114
Qin J, Dong WY, He KN, Yu Y, Tan GD, Han L, Dong M, Zhang YY, Zhang D, Li AZ, Wang ZL (2010) NaCl salinity-induced changes in water status, ion contents and photosynthetic properties of Shepherdia argentea (Pursh) Nutt. Seedlings. Plant Soil Environ 56:325–332
Ren CG, Kong CC, Xie ZH (2018) Role of abscisic acid in strigolactone-induced salt stress tolerance in arbuscular mycorrhizal Sesbania cannabina seedlings. BMC Plant Biol 18:74
Ren S, Rutto L, Katuuramu D (2019) Melatonin acts synergistically with auxin to promote lateral root development through fine tuning auxin transport in Arabidopsis thaliana. PLoS ONE 14(8):e0221687
Saha P, Chatterjee P, Biswas AK (2010) NaCl pretreatment alleviates salt stress by enhancement of antioxidant defense system and osmolyte accumulation in mungbean (Vigina radiate L.Wilczek). Indian J Exp Biol 48:593–600
Salimi F, Shekari F, Hamzei J (2016) Methyl jasmonate improves salinity resistance in german chamomile (Matricaria chamomilla L.) by increasing activity of antioxidant enzymes. Acta Physiol Plan 38:1
Sevengor S, Yasar F, Kusvuran S, Ellialtioglu S (2011) The effect of salt stress on growth, chlorophyll content, lipid peroxidation and antioxidative enzymes of pumpkin seedling. Afr J Agric Res 6:4920–4924
Souri MK, Tohidloo G (2019) Effectiveness of different methods of salicylic acid application on growth characteristics of tomato seedlings under salinity. Chem Biol Technol Ag 6:26
Tanveer M, Shahzad B, Sharma A, Biju S, Bhardwaj R (2018) 24-Epibrassinolide; an active brassinolide and its role in salt stress tolerance in plants: a review. Plant Physiol Biochem 130:69–79
Teng XX, Cao WL, Lan HX, Tang HJ, Bao YM, Zhang HS (2017) OsNHX2, an Na+/H+ antiporter gene, can enhance salt tolerance in rice plants through more effective accumulation of toxic Na+ in leaf mesophyll and bundle sheath cells. Acta Physiol Plant 39:113
Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in high plants. Ann Bot 91:503–527
Tuteja N (2007) Abscisic acid and abiotic stress signaling. Plant Signal Behav 2:135–138
Wang FB, Kong WL, Wong G, Fu LF, Peng RH, Li ZJ, Yao QH (2016) AtMYB12 regulates flavonoids accumulation and abiotic stress tolerance in transgenic Arabidopsis thaliana. Mol Genet Genomics 291:1545–1559
Wang FB, Ren GL, Li FS, Qi ST, Xu Y, Wang BW, Yang YL, Ye YX, Zhou Q, Chen XH (2018) A chalcone synthase gene AeCHS from Abelmoschus esculentus regulates flavonoids accumulation and abiotic stress tolerance in transgenic Arabidopsis. Acta Physiol Plant 40:97
Wei W, Li QT, Chu YN, Reiter RJ, Yu XM, Zhu DH, Zhang WK, Ma B, Lin Q, Zhang JS, Chen SY (2015) Melatonin enhances plant growth and abiotic stress tolerance in soybean plants. J Exp Bot 66:695–707
Xiong H, Li J, Liu P, Duan J, Zhao Y, Guo X, Li Y, Zhang H, Ali J, Li Z (2014) Overexpression of OsMYB48-1, a novel MYB-related transcription factor, enhances drought and salinity tolerance in rice. PLoS ONE 9:e92913
Yang YF, Guan SK, Zhai H, He SZ, Liu QC (2009) Development and evaluation of a storage root-bearing sweetpotato somatic hybrid between Ipomoea batatas (L.) Lam. and I. triloba L. Plant Cell Tiss Org 99: 83–89
Yasar S, Ellialtioglu F, Yildiz K (2008) Effect salt stress on antioxidant defense systems, lipid peroxidation, and chlorophyll content in green bean. Russ J Plant Physl 55:782–786
Yokoi S, Quintero FJ, Cubero B, Ruiz MT, Bressan RA, Hasegawa PM, Pardo JM (2002) Differential expression and function of Arabidopsis thaliana NHX Na+/H+ antiporters in the salt stress response. Plant J 30:529–539
Yoon JY, Hamayun M, Lee SK, Lee IJ (2009) Methyl jasmonate alleviated salinity stress in soybean. J Crop Sci Biotech 12:63–68
Yue K, Liu H, Liu D, Liu Y, Han W (2020) An ultralow dose of the NADPH oxidase inhibitor diphenyleneiodonium (DPI) is an economical and effective therapeutic agent for the treatment of colitis-associated colorectal cancer. Theranostics 10:6743–6757
Yue Y, Zhang MC, Zhang JC, Duan LS, Li ZH (2012) SOS1 gene overexpression increased salt tolerance in transgenic tobacco by maintaining a higher K+/Na+ ratio. J Plant Physiol 169:255–261
Zahedi SM, Hosseini MS, Abadia J, Marjani M (2020) Melatonin foliar sprays elicit salinity stress tolerance and enhance fruit yield and quality in strawberry (Fragaria × ananssa Duch.). Plant Physiol Biochem 149:313–323
Zhai H, Wang FB, Si ZZ, Huo JX, Xing L, An YY, He SZ, Liu QC (2016) A myo-inositol-1-phosphate synthase gene, IbMIPS1, enhances salt and drought tolerance and stem nematode resistance in transgenic sweetpotato. Plant Biotechnol J 14:592–602
Zhan Y, Wu T, Zhao X, Wang Z, Chen Y (2021) Comparative physiological and full-length transcriptome analyses reveal the molecular mechanism of melatonin-mediated salt tolerance in okra (Abelmoschus esculentus L.). BMC Plant Biol 21:180
Zhang H, Gao XR, Zhi YH, Li X, Zhang Q, Niu JB, Wang J, Zhai H, Zhao N, Li JG, Liu QC, He SZ (2019) A non-tandem CCCH-type zinc-finger protein, IbC3H18, functions as a nuclear transcriptional activator and enhances abiotic stress tolerance in sweet potato. New Phytol 223:1918–1936
Zhang WJ, Xie ZC, Wang LH, Li M, Lang DY, Zhang XH (2017) Silicon alleviates salt and drought stress of Glycyrrhiza uralensis seedling by altering antioxidant metabolism and osmotic adjustment. J Plant Res 130:611–662
Zhao Q, Zhou L, Liu J, Du X, Asad MA, Huang F, Pan G, Cheng F (2018) Relationship of ROS accumulation and superoxide dismutase isozymes in developing anther with floret fertility of rice under heat stress. Plant Physiol Bioch 122:90–101
Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324
Zhu MD, Zhang M, Gao DJ, Zhou K, Lv YM (2020) Rice OsHSFA3 gene improves drought tolerance by modulating polyamine biosynthesis depending on abscisic acid and ROS levels. Int J Mol Sci 21:1857
Zuo YT, Dong L, Ren XS, Liu ZY, Zuo SY, Li J (2021) Effects of exogenous melatonin on seed germination, seedling growth and antioxidant ability of triticale under saline-alkali stress. J Triticeae Crops 41(8):1–10