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Jasmonic acid boosts the salt tolerance of kidney beans (Phaseolus vulgaris L.) by upregulating its osmolytes and antioxidant mechanism

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Abstract

As a lipid-derived compound, jasmonic acid (JA) regulates growth and defense against environmental stresses. An exogenous foliar JA application was investigated in our study (HA; 0.5 mM) on kidney bean plants (Phaseolus vulgaris L.) grown under different salinity stress concentrations (0, 75, and 150 mM NaCl). According to the results, salt concentrations were related to an increase in malondialdehyde (MDA) levels, whereas they declined the chlorophyll content index. In contrast, JA application decreased the level of MDA but increased the chlorophyll content index. Moreover, increasing salinity levels increased proline, phenolic compounds, flavonoids, free amino acid concentrations, and shikimic acid concentrations, as well as the activities of polyphenol oxidase (PPO), ascorbate peroxidase (APX), catalase (CAT), and peroxidase (POD). In addition, JA applications further increased their concentrations with increasing salinity stress levels. JA application increases salt-induced osmolytes and non-enzymatic antioxidants while increasing enzymatic antioxidant activity, suggesting kidney beans have a strong antioxidant mechanism, which can adapt to salinity stress. Our results showed that exogenous JA foliar applications could enhance the salt tolerance ability of kidney bean plants by upregulating their antioxidant mechanism and osmolytes.

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References

  • Abbas T, Fan R, Hussain S et al (2022) Protective effect of jasmonic acid and potassium against cadmium stress in peas (Pisum sativum L.). Saudi J Biol Sci 29:2626–2633

    Article  CAS  Google Scholar 

  • Abdel Latef AAH, Srivastava AK, Saber H et al (2017) Sargassum muticum and Jania rubens regulate amino acid metabolism to improve growth and alleviate salinity in chickpea. Sci Rep 7:1–12

    Article  CAS  Google Scholar 

  • Abdel Latef AAH, Srivastava AK, El-sadek MSA et al (2018) Titanium dioxide nanoparticles improve growth and enhance tolerance of broad bean plants under saline soil conditions. Land Degrad Dev 29:1065–1073

    Article  Google Scholar 

  • Abdel Latef AAH, Mostofa MG, Rahman MM et al (2019) Extracts from yeast and carrot roots enhance maize performance under seawater-induced salt stress by altering physio-biochemical characteristics of stressed plants. J Plant Growth Regul 38:966–979

    Article  CAS  Google Scholar 

  • Abdel-Fattah GM, Rabie GH, Lamis DS, Rabab AM (2016) The impact of the arbuscular mycorrhizal fungi on growth and physiological parameters of cowpea plants grown under salt stress conditions. Int J Appl Sci Biotechnol 4:372–379

    Article  CAS  Google Scholar 

  • Ahammed GJ, Li Y, Li X et al (2018) Epigallocatechin-3-gallate alleviates salinity-retarded seed germination and oxidative stress in tomato. J Plant Growth Regul 37:1349–1356

    Article  CAS  Google Scholar 

  • Ahmad P, Raja V, Ashraf M et al (2021) Jasmonic acid (JA) and gibberellic acid (GA3) mitigated Cd-toxicity in chickpea plants through restricted Cd uptake and oxidative stress management. Sci Rep 11:19768

    Article  CAS  Google Scholar 

  • Al-Elwany OA, Mohamed GF, Abdurrahman HA, Latef AAA (2020) Exogenous glutathione-mediated tolerance to deficit irrigation in salt-affected Capsicum frutescence (L.) plants is connected with higher antioxidant content and ionic homeostasis. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 48:1957–1979

    Article  CAS  Google Scholar 

  • Ali AYA, Ibrahim MEH, Zhou G et al (2022) Interactive impacts of soil salinity and jasmonic acid and humic acid on growth parameters, forage yield and photosynthesis parameters of sorghum plants. S Afr J Bot 146:293–303

    Article  CAS  Google Scholar 

  • Anuradha S, Ram Rao SS (2003) Application of brassinosteroids to rice seeds (Oryza sativa L.) reduced the impact of salt stress on growth, prevented photosynthetic pigment loss and increased nitrate reductase activity. Plant Growth Regul 40:29–32

    Article  CAS  Google Scholar 

  • Ashraf M, Harris P (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16

    Article  CAS  Google Scholar 

  • Ashraf M, Karim F, Rasul E (2002) Interactive effects of gibberellic acid (GA 3) and salt stress on growth, ion accumulation and photosynthetic capacity of two spring wheat (Triticum aestivum L.) cultivars differing in salt tolerance. Plant Growth Regul 36:49–59

    Article  CAS  Google Scholar 

  • Bates L, Waldren R, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Becerra-Moreno A, Redondo-Gil M, Benavides J et al (2015) Combined effect of water loss and wounding stress on gene activation of metabolic pathways associated with phenolic biosynthesis in carrot. Front Plant Sci 6:837

    Article  Google Scholar 

  • Berger AA, Völler J-S, Budisa N, Koksch B (2017) Deciphering the fluorine code—the many hats fluorine wears in a protein environment. Acc Chem Res 50:2093–2103

    Article  CAS  Google Scholar 

  • Calone R, Bregaglio S, Sanoubar R et al (2021) Physiological adaptation to water salinity in six wild halophytes suitable for Mediterranean agriculture. Plants 10:309

    Article  CAS  Google Scholar 

  • Chao WS, Gu Y-Q, Pautot V et al (1999) Leucine aminopeptidase RNAs, proteins, and activities increase in response to water deficit, salinity, and the wound signals systemin, methyl jasmonate, and abscisic acid. Plant Physiol 120:979–992

    Article  CAS  Google Scholar 

  • Chinnusamy V, Jagendorf A, Zhu J (2005) Understanding and improving salt tolerance in plants. Crop Sci 45:437–448

    Article  CAS  Google Scholar 

  • Creelman RA, Mullet JE (1995) Jasmonic acid distribution and action in plants: regulation during development and response to biotic and abiotic stress. Proc Natl Acad Sci 92:4114–4119

    Article  CAS  Google Scholar 

  • Davey M, Stals E, Panis B et al (2005) High-throughput determination of malondialdehyde in plant tissues. Anal Biochem 347:201–207

    Article  CAS  Google Scholar 

  • de Ollas C, Hernando B, Arbona V, Gómez-Cadenas A (2013) Jasmonic acid transient accumulation is needed for abscisic acid increase in citrus roots under drought stress conditions. Physiol Plant 147:296–306

    Article  Google Scholar 

  • Dewanto V, Wu X, Adom KK, Liu RH (2002) Thermal processing enhances the nutritional value of tomatoes by increasing total antioxidant activity. J Agric Food Chem 50:3010–3014

    Article  CAS  Google Scholar 

  • Ehnert S, Seehase J, Müller-Renno C et al (2021) Simultaneous quantification of total carbohydrate and protein amounts from aqueous solutions by the sulfuric acid ultraviolet absorption method (SA-UV method). Anal Chim Acta 1174:338712

    Article  CAS  Google Scholar 

  • El Moukhtari A, Cabassa-Hourton C, Farissi M, Savouré A (2020) How does proline treatment promote salt stress tolerance during crop plant development? Front Plant Sci 11:1127

    Article  Google Scholar 

  • El Nahhas N, AlKahtani MD, Abdelaal KA et al (2021) Biochar and jasmonic acid application attenuates antioxidative systems and improves growth, physiology, nutrient uptake and productivity of faba bean (Vicia faba L.) irrigated with saline water. Plant Physiol Biochem 166:807–817

    Article  Google Scholar 

  • Fancy NN, Bahlmann A, Loake GJ (2017) Nitric oxide function in plant abiotic stress. Plant Cell Environ 40:462–472

    Article  CAS  Google Scholar 

  • Ghassemi-Golezani K, Hosseinzadeh-Mahootchi A (2015) Improving physiological performance of safflower under salt stress by application of salicylic acid and jasmonic acid. WALIA J 31:104–109

    Google Scholar 

  • Ghorbel M, Brini F, Sharma A, Landi M (2021) Role of jasmonic acid in plants: the molecular point of view. Plant Cell Rep 40:1471–1494

    Article  CAS  Google Scholar 

  • Ghouri F, Ali Z, Naeem M et al (2022) Effects of silicon and selenium in alleviation of drought stress in rice. Silicon 14:5453–5461

    Article  CAS  Google Scholar 

  • Guo Q, Major IT, Howe GA (2018) Resolution of growth–defense conflict: mechanistic insights from jasmonate signaling. Curr Opin Plant Biol 44:72–81

    Article  CAS  Google Scholar 

  • Hernández-Montes G, Díaz-Mejía JJ, Pérez-Rueda E, Segovia L (2008) The hidden universal distribution of amino acid biosynthetic networks: a genomic perspective on their origins and evolution. Genome Biol 9:1–15

    Article  Google Scholar 

  • Hossain MN, Sarker U, Raihan MS et al (2022) Influence of salinity stress on color parameters, leaf pigmentation, polyphenol and flavonoid contents, and antioxidant activity of Amaranthus lividus leafy vegetables. Molecules 27:1821

    Article  CAS  Google Scholar 

  • Hoyos ME, Zhang S (2000) Calcium-independent activation of salicylic acid-induced protein kinase and a 40-kilodalton protein kinase by hyperosmotic stress. Plant Physiol 122:1355–1364

    Article  CAS  Google Scholar 

  • Ibrahim MEH, Zhou G, Nimir NEA et al (2020) Exogenous jasmonic acid and humic acid increased salinity tolerance of sorghum. Agro J 112(2):871–884

    Article  Google Scholar 

  • Ismail H, Maksimović JD, Maksimović V et al (2015) Rutin, a flavonoid with antioxidant activity, improves plant salinity tolerance by regulating K+ retention and Na+ exclusion from leaf mesophyll in quinoa and broad beans. Funct Plant Biol 43:75–86

    Article  Google Scholar 

  • Jacobo-Velázquez D, Cisneros-Zevallos L (2009) Correlations of antioxidant activity against phenolic content revisited: a new approach in data analysis for food and medicinal plants. J Food Sci 74:R107–R113

    Article  Google Scholar 

  • Jin S, Chen C, Plant A (2000) Regulation by ABA of osmotic-stress-induced changes in protein synthesis in tomato roots. Plant Cell Environ 23:51–60

    Article  CAS  Google Scholar 

  • Kataria S, Jain M (2019) Magnetopriming alleviates adverse effects of abiotic stresses in plants. In: Plant tolerance to environmental stress. CRC Press, pp 427–442

    Chapter  Google Scholar 

  • Kaur G, Asthir B (2015) Proline: a key player in plant abiotic stress tolerance. Biol Plant 59:609–619

    Article  CAS  Google Scholar 

  • Kim H, Seomun S, Yoon Y, Jang G (2021) Jasmonic acid in plant abiotic stress tolerance and interaction with abscisic acid. Agronomy 11:1886

    Article  CAS  Google Scholar 

  • Machado RMA, Serralheiro RP (2017) Soil salinity: effect on vegetable crop growth. Management practices to prevent and mitigate soil salinization. Horticulturae 3:30

    Article  Google Scholar 

  • Mansour M (2000) Nitrogen containing compounds and adaptation of plants to salinity stress. Biol Plant 43:491–500

    Article  CAS  Google Scholar 

  • Matallo M, Almeida S, Franco D et al (2014) Glyphosate as a tool to produce shikimic acid in plants. Planta Daninha 32:601–608

    Article  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  Google Scholar 

  • Pereira A (2016) Plant abiotic stress challenges from the changing environment. Front Plant Sci 7:1123

    Article  Google Scholar 

  • Qadir M, Quillérou E, Nangia V et al (2014) Economics of salt-induced land degradation and restoration. Wiley Online Library, pp 282–295

    Google Scholar 

  • Qiu Z, Guo J, Zhu A et al (2014) Exogenous jasmonic acid can enhance tolerance of wheat seedlings to salt stress. Ecotoxicol Environ Saf 104:202–208

    Article  CAS  Google Scholar 

  • Qureshi M, Abdin M, Qadir S, Iqbal M (2007) Lead-induced oxidative stress and metabolic alterations in Cassia angustifolia Vahl. Biol Plant 51:121–128

    Article  CAS  Google Scholar 

  • Rabab AM, Reda EA (2019) Impact of Ridomil, Bavistin and Agrothoate on arbuscular mycorrhizal fungal colonization, biochemical changes and potassium content of cucumber plants. Ecotoxicology 28:487–498

    Article  CAS  Google Scholar 

  • Raza A, Charagh S, Zahid Z et al (2021) Jasmonic acid: a key frontier in conferring abiotic stress tolerance in plants. Plant Cell Rep 40:1513–1541

    Article  CAS  Google Scholar 

  • Rezazadeh A, Ghasemnezhad A, Barani M, Telmadarrehei T (2012) Effect of salinity on phenolic composition and antioxidant activity of artichoke (Cynara scolymus L.) leaves. Res J Med Plant 6:245–252

    Article  CAS  Google Scholar 

  • Rosa M, Prado C, Podazza G et al (2009) Soluble sugars: metabolism, sensing and abiotic stress: a complex network in the life of plants. Plant Signal Behav 4:388–393

    Article  CAS  Google Scholar 

  • Ruan J, Zhou Y, Zhou M et al (2019) Jasmonic acid signaling pathway in plants. Int J Mol Sci 20:2479

    Article  CAS  Google Scholar 

  • Saeed S, Ullah A, Ullah S et al (2022) Validating the impact of water potential and temperature on seed germination of wheat (Triticum aestivum L.) via hydrothermal time model. Life 12:983

    Article  Google Scholar 

  • Sami F, Yusuf M, Faizan M et al (2016) Role of sugars under abiotic stress. Plant Physiol Biochem 109:54–61

    Article  CAS  Google Scholar 

  • Sané AK, Diallo B, Kane A et al (2021) In vitro germination and early vegetative growth of five tomato (Solanum lycopersicum L.) varieties under salt stress conditions. Am J Plant Sci 12:796–817

    Article  Google Scholar 

  • Sharma A, Kumar V, Shahzad B et al (2020) Photosynthetic response of plants under different abiotic stresses: a review. J Plant Growth Regul 39:509–531

    Article  CAS  Google Scholar 

  • Silla F, González-Gil A, González-Molina ME et al (2010) Estimation of chlorophyll in Quercus leaves using a portable chlorophyll meter: effects of species and leaf age. Ann For Sci 67:108

    Article  Google Scholar 

  • Sirhindi G, Mir MA, Abd-Allah EF et al (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

    Article  Google Scholar 

  • Ullah S, Afzal I, Shumaila S, Shah W (2021) Effect of naphthyl acetic acid foliar spray on the physiological mechanism of drought stress tolerance in maize (Zea Mays L.). Plant Stress 2:100035

    Article  CAS  Google Scholar 

  • 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 151:59–66

    Article  CAS  Google Scholar 

  • Waheed A, Haxim Y, Islam W et al (2022a) Impact of cadmium stress on growth and physio-biochemical attributes of Eruca sativa Mill. Plants 11:2981

    Article  CAS  Google Scholar 

  • Waheed A, Haxim Y, Kahar G et al (2022b) Jasmonic acid boosts physio-biochemical activities in Grewia asiatica L. under Drought Stress. Plants 11:2480

    Article  CAS  Google Scholar 

  • Wang J, Song L, Gong X et al (2020) Functions of jasmonic acid in plant regulation and response to abiotic stress. Int J Mol Sci 21:1446

    Article  CAS  Google Scholar 

  • Wang Y, Mostafa S, Zeng W, Jin B (2021) Function and mechanism of jasmonic acid in plant responses to abiotic and biotic stresses. Int J Mol Sci 22:8568

    Article  CAS  Google Scholar 

  • Warren CR, Aranda I, Cano FJ (2012) Metabolomics demonstrates divergent responses of two Eucalyptus species to water stress. Metabolomics 8:186–200

    Article  CAS  Google Scholar 

  • Woodward AJ, Bennett IJ (2005) The effect of salt stress and abscisic acid on proline production, chlorophyll content and growth of in vitro propagated shoots of Eucalyptus camaldulensis. Plant Cell Tissue Organ Cult 82:189–200

    Article  CAS  Google Scholar 

  • Yang Y, Han C, Liu Q et al (2008) Effect of drought and low light on growth and enzymatic antioxidant system of Picea asperata seedlings. Acta Physiol Plant 30:433–440

    Article  CAS  Google Scholar 

  • Yoon JY, Hamayun M, Lee S-K, Lee I-J (2009) Methyl jasmonate alleviated salinity stress in soybean. J Crop Sci Biotechnol 12:63–68

    Article  Google Scholar 

  • Zhang W, Xie Z, Lang D et al (2017) Beneficial effects of silicon on abiotic stress tolerance in legumes. J Plant Nutr 40:2224–2236

    Article  CAS  Google Scholar 

  • Zlatić N, Jakovljević D, Stanković M (2019) Temporal, plant part, and interpopulation variability of secondary metabolites and antioxidant activity of Inula helenium L. Plants 8:179

    Article  Google Scholar 

  • Zhang Z, Chai X, Tariq A et al (2021) Coordinated patterns in the allocation, composition, and variability of multiple elements among organs of two desert shrubs under nitrogen addition and drought. J Soil Sci Plant Nutr:1–12

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Acknowledgements

The authors acknowledge the Deanship of Scientific Research, King Khalid University for funding this work through the research groups program under grant number R.G.P.2/205/44.

Funding

This work was supported by Leading Talents in Technological Innovation program, 2022TSYCLJ0049, Xinjiang Key Project of Research and Development Plan, 2022B03020, and CAS-PIFI postdoctoral fellowship (2020PB0027) at the Xinjiang Institute of Ecology & Geography, Chinese Academy of Sciences, Urumqi, Xinjiang, China. 

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Authors and Affiliations

  1. National Key Laboratory of Ecological Security and Resource Utilization in Arid Areas, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi, 830011, China

    Abdul Waheed, Yakupjan Haxim, Gulnaz Kahar, Waqar Islam & Zhang Daoyuan

  2. Xinjiang Key Laboratory of Desert Plant Roots Ecology and Vegetation Restoration, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi, 830011, China

    Abdul Waheed, Yakupjan Haxim, Gulnaz Kahar, Waqar Islam & Zhang Daoyuan

  3. Department of Zoology, Islamia College University, Peshawar, 24420, Pakistan

    Mushtaq Ahmad

  4. Unit of Bee Research and Honey Production, Research Center for Advanced Materials Science (RCAMS), King Khalid University, P.O. Box 9004, Abha, 61413, Saudi Arabia

    Khalid Ali Khan & Hamed A. Ghramh

  5. Applied College, King Khalid University, P. O. Box 9004, Abha, 61413, Saudi Arabia

    Khalid Ali Khan

  6. Biology Department, Faculty of Science, King Khalid University, P. O. Box 9004, Abha, 61413, Saudi Arabia

    Hamed A. Ghramh

  7. Department of Biology, College of Science, King Khalid University, Abha, 61413, Saudi Arabia

    Fatmah M. Alqahtani & Mohamed Hashemand

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  1. Abdul Waheed
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Contributions

This manuscript reflects the contributions of all authors. Conceptualization and investigation, A.W. and D.Z; methodology, A.W.; Y.H.; software, G.K., W.I.; validation and formal analysis, M.A., K.A.K., and H.A.G.; data curation and visualization, F.M.A. and M.H.; writing original draft preparation, A.W.; review and editing, Y.H. and Z.D.; supervision, Z.D.; project administration, Z.D.; funding acquisition, K.A.K., H.A.G., M.H., and Z.D. A final version of the manuscript has been approved by all the authors.

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Correspondence to Zhang Daoyuan.

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Waheed, ., Haxim, Y., Kahar, G. et al. Jasmonic acid boosts the salt tolerance of kidney beans (Phaseolus vulgaris L.) by upregulating its osmolytes and antioxidant mechanism. Environ Sci Pollut Res 30, 91237–91246 (2023). https://doi.org/10.1007/s11356-023-28632-4

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