Interactive effect of potassium and spermidine protects growth, photosynthesis and chlorophyll biosynthesis in Vigna angularis from salinity induced damage by up-regulating the tolerance mechanisms
Pot experiments were conducted to evaluate the role of potassium (100 mg KCl / kg soil) and the spermidine (100 µM Spd) in regulation of growth, chlorophyll synthesis and photosynthesis in Vigna angularis under salinity stress (100 mM NaCl). Salinity declined chlorophyll synthesis by causing a significant decline in the synthesis of δ-amino levulinic acid (ALA), prototoporphyrin IX (Proto IX) and Mg-prototoporphyrin IX (Mg-Proto IX), however application of K and Spd alone as well as combinedly alleviated the decline to considerable extent. Further, K and Spd treated plants exhibited a significant decline in reactive oxygen species and the lipid peroxidation and such effects were also obvious under salinity stress. Photosynthetic rate, stomatal conductance, intercellular CO2 concentration, Fv/Fm and photochemical quenching increased significantly due to K and Spd application, and salinity induced alleviation of the decline was maximal due to combined K and Spd treatment. Up-regulation of antioxidant enzymes activity, increased content of ascorbic acid and glutathione (GSH), and the accumulation of compatible osmolytes due to K and Spd application strengthened the tolerance against the salinity stress thereby lessening the oxidative effects considerably. Accumulation of phenols and flavonoids increased significantly due to application of K and Spd. Salinity caused significant increase in Na however K and Spd application induced a significant decline concomitant with increase in K content reflecting in decreased Na/K. Results suggest that K and Spd application protect the growth and photosynthesis from salinity induced oxidative damage by up-regulating the ion homeostasis, antioxidant system, osmolyte accumulation and secondary metabolite synthesis.
Agnihotri A, Seth CS (2016). Exogenously applied nitrate improves the photosynthetic performance and nitrogen metabolism in tomato (Solanum lycopersicum L. cv Pusa Rohini) under arsenic (V) toxicity. Physiology and Molecular Biology of Plants 22(3):341-349. https://doi.org/10.1007/s12298-016-0370-2
Ahanger MA, Agarwal RM (2017a) Salinity stress induced alterations in antioxidant metabolism and nitrogen assimilation in wheat (Triticum aestivum L) as influenced by potassium supplementation. Plant Physiology and Biochemistry 115:449-460. https://doi.org/10.1016/j.plaphy.2017.04.017
Ahanger MA, Agarwal RM (2017b) Potassium up-regulates antioxidant metabolism and alleviates growth inhibition under water and osmotic stress in wheat (Triticum aestivum L). Protoplasma 254(4):1471-1486. https://doi.org/10.1007/s00709-016-1037-0
Ahanger MA, Aziz U, Alsahli AA, Alyemeni MN, Ahmad P (2020). Combined kinetin and spermidine treatments ameliorate growth and photosynthetic inhibition in Vigna angularis by up-regulating antioxidant and nitrogen metabolism under cadmium stress. Biomolecules 10:147. https://doi.org/10.3390/biom10010147
Ahanger MA, Qin C, Begum N, Maodong Q, Dong XX, El-Esawi M, … Zhang L. (2019a). Nitrogen availability prevents oxidative effects of salinity on wheat growth and photosynthesis by up-regulating the antioxidants and osmolytes metabolism, and secondary metabolite accumulation. BMC Plant Biology 19:479 https://doi.org/10.1186/s12870-019-2085-3
Ahanger MA, Qin C, Maodong Q, Dong XX, Ahmad P, Abd_Allah EF, Zhang L. (2019b). Spermine application alleviates salinity induced growth and photosynthetic inhibition in Solanum lycopersicum by modulating osmolyte and secondary metabolite accumulation and differentially regulating antioxidant metabolism. Plant Physiology and Biochemistry 144:1-13. https://doi.org/10.1016/j.plaphy.2019.09.021
Ahanger MA, Tittal M, Mir RA, Agarwal RM. (2017b) Alleviation of water and osmotic stress-induced changes in nitrogen metabolizing enzymes in Triticum aestivum L. cultivars by potassium. Protoplasma 254(5):1953-1963. https://doi.org/10.1007/s00709-017-1086-z
Ahanger MA, Tomar NS, Tittal M, Argal S, Agarwal RM. (2017a) Plant growth under water/ salt stress: ROS production; antioxidants and significance of added potassium under such conditions. Physiology and Molecular Biology of Plants 23(4):731-744. https://doi.org/10.1007/s12298-017-0462-7
Ahmad P, Abdel Latef AA, Abd_Allah EF, Hashem A, Sarwat M, Anjum NA, Gucel S (2016) Calcium and potassium supplementation enhanced growth, osmolyte secondary metabolite production, and enzymatic antioxidant machinery in cadmium-exposed chickpea (Cicer arietinum L.). Frontiers in Plant Science 7:513. https://doi.org/10.3389/fpls.2016.00513
Ahmad P, Ahanger MA, Alyemeni MN, Wijaya L, Alam P, Ashraf M (2018) Mitigation of sodium chloride toxicity in Solanum lycopersicum L. by supplementation of jasmonic acid and nitric oxide. Journal of Plant Interactions 13:64-72. https://doi.org/10.1080/17429145.2017.1420830
Ahmad P, Ahanger MA, Alam P, Alyemeni MN, Wijaya L, Ali S, Ashraf M (2019). Silicon (Si) supplementation alleviates NaCl toxicity in mung bean [Vigna radiata (L.) Wilczek] through the modifications of physio-biochemical attributes and key antioxidant enzymes. Journal of Plant Growth Regulation 38:70-82. https://doi.org/10.1007/s00344-018-9810-2
Amanullah Iqbal, Irfanullah A, Zeeshan H (2016). Potassium management for improving growth and grain yield of maize (Zea mays L.) under moisture stress condition. Scientific Reports 6:34627. https://doi.org/10.1038/srep34627
Anjitha KS, Sameena PP, Puthur JT (2021). Functional aspects of plant secondary metabolites in metal stress tolerance and their importance in pharmacology. Plant Stress 2:100038. https://doi.org/10.1016/j.stress.2021.100038
Arnon DI (1949). Copper enzymes in isolated chloroplast polyphenol oxidase in Beta vulgaris. Plant Physiology 24:1-15. https://doi.org/10.1104/pp.24.1.1
Asch F, Dingkuhn M, Dörffling K, Meizan K (2000). Leaf K/Na ratio predicts salinity induced yield loss in irrigated rice. Euphytica 113:109. https://doi.org/10.1023/A:1003981313160
Assaha DVM, Ueda A, Saneoka H, Al-Yahyai R, Yaish MW (2017). The role of Na+ and K+ transporters in salt stress adaptation in glycophytes. Frontiers in Physiology 8:509. https://doi.org/10.3389/fphys.2017.00509
Austen N, Walker HJ, Lake JA, Phoenix GK, Cameron DD (2019). The regulation of plant secondary metabolism in response to abiotic stress: interactions between heat shock and elevated CO2. Frontiers in Plant Science 14. https://doi.org/10.3389/fpls.2019.01463
Babar S, Siddiqi EH, Hussain I, Bhatti KH, Rasheed R (2014). Mitigating the effects of salinity by foliar application of salicylic acid in fenugreek. Physiology Journal. https://doi.org/10.1155/2014/869058
Bahrami-Rad S, Hajiboland R (2017). Effect of potassium application in drought-stressed tobacco (Nicotiana rustica L.) plants: Comparison of root with foliar application. Annals of Agricultural Sciences. 62(2):121-130. https://doi.org/10.1016/j.aoas.2017.08.001
Bano C, Amist N, Singh NB. (2020). Role of polyamines in plants abiotic stress tolerance: Advances and future prospects. In: Plant Life Under Changing Environment. Responses and Management 481-496.
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39:205-207. https://doi.org/10.1007/BF00018060
Bayer WF, Fridovich JL (1987). Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Annals of Biochemistry 161:559-566. https://doi.org/10.1016/0003-2697(87)90489-1
Begum N, Ahanger MA, Zhang L (2020). AMF inoculation and phosphorus supplementation alleviates drought induced growth and photosynthetic decline in Nicotiana tabacum by up-regulating antioxidant metabolism and osmolyte accumulation. Environmental and Experimental Botany. https://doi.org/10.1016/j.envexpbot.2020.104088.
Begum N, Akhtar K, Ahanger MA, Iqbal M, Wang P, Mustafa NS, Zhang L (2021). Arbuscular mycorrhizal fungi improve growth, essential oil, secondary metabolism, and yield of tobacco (Nicotiana tabacum L.) under drought stress conditions. Environmental Science and Pollution Research. https://doi.org/10.1007/s11356-021-13755-3
Berger A, Boscari A, Araújo NH, Maucourt M, Hanchi M, Bernillon S, Rolin D, Puppo A, Brouquisse R (2020). Plant nitrate reductases regulate nitric oxide production and nitrogen-fixing metabolism during the Medicago truncatula - Sinorhizobium meliloti symbiosis. Frontiers in Plant Science. https://doi.org/10.3389/fpls.2020.01313
Carlberg I, Mannervik B (1985). Glutathione reductase. In: Meister A (Ed). Methods in Enzymology. New York, Academic, pp 484-490.
Chatterjee J, Majumder AL. (2010). Salt-induced abnormalities on root tip mitotic cells of Allium cepa: prevention by inositol pretreatment. Protoplasma 245(1-4):165-72. https://doi.org/10.1007/s00709-010-0170-4
Dalal VK, Tripathy BC (2012). Modulation of chlorophyll biosynthesis by water stress in rice seedlings during chloroplast biogenesis. Plant Cell Environment 35:1685-1703. https://doi.org/10.1111/j.1365-3040.2012.02520.x
Dey N, Bhattacharjee S (2020). Accumulation of polyphenolic compounds and osmolytes under dehydration stress and their implication in redox regulation in four indigenous aromatic rice cultivars. Rice Science 27(4):329-344. https://doi.org/10.1016/j.rsci.2020.05.008
Elkelish EE, Soliman MH, Alhaithloul HA, El-Esawi MA (2019) Selenium protects wheat seedlings against salt stress-mediated oxidative damage by up-regulating antioxidants and osmolytes metabolism. Plant Physiology and Biochemistry 137:144-153. https://doi.org/10.1016/j.plaphy.2019.02.004
Ellman GL (1959) Tissue sulphydryl groups. Archives of Biochemistry and Biophysics 82:70‐77. https://doi.org/10.1016/0003-9861(59)90090-6
El-Taher AM, Abd El-Raouf HS, Osman NA, Azoz SN, Omar MA, Elkelish A, Abd El-Hady MAM (2022). Effect of salt stress and foliar application of salicylic acid on morphological, biochemical, anatomical, and productivity characteristics of cowpea (Vigna unguiculata L.) plants. Plants 11:115. https://doi.org/10.3390/plants11010115
Fariduddin Q, Zaid A, Mohammad F (2019). Plant growth regulators and salt stress: mechanism of tolerance trade-off. In: Akhtar M (Ed). Salt Stress, Microbes, and Plant Interactions: Causes and Solution. Springer, Singapore. https://doi.org/10.1007/978-981-13-8801-9_4
Fatma M, Masood A, Per TS and Khan NA (2016) Nitric oxide alleviates salt stress inhibited photosynthetic performance by interacting with sulfur assimilation in mustard. Frontiers in Plant Science 7:521. https://doi.org/10.3389/fpls.2016.00521
Foyer CH, Noctor G (2011). Ascorbate and glutathione: The Heart of the Redox Hub. Plant Physiology 155(1):2-18. https://doi.org/10.1104/pp.110.167569
Ghosh UK, Islam MN, Siddiqui MN, Khan MAR (2021). Understanding the roles of osmolytes for acclimatizing plants to changing environment: a review of potential mechanism. Plant Signalling and Behaviour 16(8):1913306. https://doi.org/10.1080/15592324.2021.1913306
Gill SS, Tuteja N (2010). Polyamines and abiotic stress tolerance in plants. Plant Signalling and Behaviour 5(1):26-33. https://doi.org/10.4161/psb.5.1.10291
Grieve CM, Grattan SR (1983) Rapid assay for determination of water-soluble quaternary ammonium compounds. Plant Soil 70:303. https://doi.org/10.1007/BF02374789
Harel E, Klein S (1972). Light dependent formation of 5-aminolevulinic acid in etiolated leaves of higher plants. Biochemical and Biophysical Research Communications 49:364-370. https://doi.org/10.1016/0006-291x(72)90419-6
Hasanuzzaman M, Bhuyan MHM, Nahar K, Hossain MS, Mahmud JA, Hossen MS, … Fujita M (2018). Potassium: a vital regulator of plant responses and tolerance to abiotic stresses. Agronomy 8:31 https://doi.org/10.3390/agronomy8030031
Hasanuzzaman M, Bhuyan MHM, Anee TI, Parvin K, Nahar K, Mahmud JA, Fujita M (2019). Regulation of ascorbate-glutathione pathway in mitigating oxidative damage in plants under abiotic stress. Antioxidants (Basel) 8(9):384. https://doi.org/10.3390/antiox8090384
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125:189-198. https://doi.org/10.1016/0003-9861(68)90654-1
Hodgins RR, Huystee RBV (1986) Rapid simultaneous estimation of protoporphyrin and Mg-porphyrins in higher plants. Journal of Plant Physiology 125:311-323. https://doi.org/10.1016/s0176-1617(86)80153-5
Hu L, Xiang L, Li S, Zou Z, Hu XH (2016a). Beneficial role of spermidine in chlorophyll metabolism and D1 protein content in tomato seedlings under salinity–alkalinity stress. Physiologia Plantarum 156:468-477. https://doi.org/10.1111/ppl.12398
Huang H, Ullah F, Zhou DX, Yi M, Zhao Y (2019). Mechanisms of ROS regulation of plant development and stress responses. Frontiers in Plant Science. https://doi.org/10.3389/fpls.2019.00800
Ibrahim MH, Jaafar HZE, Karimi E, Ghasemzadeh A (2014). Allocation of secondary metabolites, photosynthetic capacity, and antioxidant activity of kacip fatimah (Labisia pumila Benth) in response to CO2 and light intensity. The Scientific World Journal. https://doi.org/10.1155/2014/360290
Isah T (2019). Stress and defense responses in plant secondary metabolites production. Biology Research 52:39. https://doi.org/10.1186/s40659-019-0246-3
Islam MJ, Ryu BR, Azad MOK, Rahman MH, Rana MS, Lim J-D, Lim Y-S (2021). Exogenous putrescine enhances salt tolerance and ginsenosides content in Korean ginseng (Panax ginseng Meyer) Sprouts. Plants 10:1313. https://doi.org/10.3390/plants10071313
Islam S, Zaid A, Mohammad F (2021). Role of triacontanol in counteracting the Ill effects of salinity in plants: a review. Journal of Plant Growth Regulation 40:1-10. https://doi.org/10.1007/s00344-020-10064-w
Jan R, Asaf S, Numan M, Kim KM (2021). Plant secondary metabolite biosynthesis and transcriptional regulation in response to biotic and abiotic stress conditions. Agronomy 11(5):968. https://doi.org/10.3390/agronomy11050968
Jan S, Alyemeni MN, Wijaya L, Alam P, Siddique KH, Ahmad P (2018). Interactive effect of 24-epibrassinolide and silicon alleviates cadmium stress via the modulation of antioxidant defense and glyoxalase systems and macronutrient content in Pisum sativum L. seedlings. BMC Plant Biology 18(1):146. https://doi.org/10.1186/s12870-018-1359-5
Jaworski EG (1971) Nitrate reductase assay in intact plant tissue. Biochemical and Biophysical Research Communications 43:1274-1279.
Jiang D, Hou J, Gao W Tong X, Li M, Chu X, Chen G (2021). Exogenous spermidine alleviates the adverse effects of aluminum toxicity on photosystem II through improved antioxidant system and endogenous polyamine contents. Ecotoxicology and Environmental Safety 207(1):111265. https://doi.org/10.1016/j.ecoenv.2020.111265
Khan MIR, Asgher M, Khan NA. (2014). Alleviation of salt-induced photosynthesis and growth inhibition by salicylic acid involves glycine betaine and ethylene in mungbean (Vigna radiata L.). Plant Physiology and Biochemistry 80:67-74. https://doi.org/10.1016/j.plaphy.2014.03.026
Khan MIR, Nazir F, Asgher M, Per TS, Khan NA (2015). Selenium and sulfur influence ethylene formation and alleviate cadmium-induced oxidative stress by improving proline and glutathione production in wheat. Journal of Plant Physiology 173:9-18. https://doi.org/10.1016/j.jplph.2014.09.011
Liaqat S, Umar S, Saffeullah P, Iqbal N, Siddiqi TO, Khan MIR (2020). Protective Effect of 24-epibrassinolide on barley plants growing under combined stress of salinity and potassium deficiency. Journal of Plant Growth Regulation 39:1543-1558. https://doi.org/10.1007/s00344-020-10163-8
Liu B, Peng X, Han L, Hou L, Li B (2020). Effects of exogenous spermidine on root metabolism of cucumber seedlings under salt stress by GC-MS. Agronomy 459. https://doi.org/10.3390/agronomy10040459
Liu M, Chu M, Ding Y, Wang S, Liu Z, Tang S, Ding C, Li G (2015). Exogenous spermidine alleviates oxidative damage and reduce yield loss in rice submerged at tillering stage. Frontiers in Plant Science. https://doi.org/10.3389/fpls.2015.00919
Lowry OH, Rosebrough, NS, Farrand AL, Randall RJ (1951). Protein measurement with Folin phenol reagent. Journal of Biological Chemistry 193:263-275.
Ma TL, Wu WH, Wang Y (2012). Transcriptome analysis of rice root responses to potassium deficiency. BMC Plant Biology 12:161. https://doi.org/10.1186/1471-2229-12-161
Mahajan M, Sharma S, Kumar P, Pal PK (2020). Foliar application of KNO3 modulates the biomass yield, nutrient uptake and accumulation of secondary metabolites of Stevia rebaudiana under saline conditions. Industrial Crops and Products 145:112102 https://doi.org/10.1016/j.indcrop.2020.112102
Marschner H (2012). Marschner’s Mineral Nutrition of Higher Plants. Cambridge, MA: Academic press.
Mattioli R, Marchese D, D’Angeli S, Altamura MM, Costantino P, Trovato M (2008). Modulation of intracellular proline levels affects flowering time and inflorescence architecture in Arabidopsis. Plant Molecular Biology 66(3):277-288. https://doi.org/10.1007/s11103-007-9269-1
Mbambalala N, Panda SK, van der Vyver C (2021). Overexpression of AtBBX29 improves drought tolerance by maintaining photosynthesis and enhancing the antioxidant and osmolyte capacity of sugarcane plants. Plant Molecular Biology Reporter 39:419-433. https://doi.org/10.1007/s11105-020-01261-8
Miranda JA, Avonce N, Suárez R, Thevelein JM, Van Dijck P, Iturriaga GA (2007). Bifunctional TPS–TPP enzyme from yeast confers tolerance to multiple and extreme abiotic-stress conditions in transgenic Arabidopsis. Planta 226(6):1411-1421. https://doi.org/10.1007/s00425-007-0579-y
Mukherjee SP, Choudhuri MA (1983) Implications of water stress-induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Physiologia Plantarum 58:166-170. https://doi.org/10.1111/j.1399-3054.1983.tb04162.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 up-regulating the metal detoxification, antioxidant defense and methylglyoxal detoxification systems. Ecotoxicology and Environmental Safety 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 Physiology 22:867-880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Nasizadeh S, Myhre L, Thiman L, Alm K, Oredsson S, Persson L (2005). Importance of polyamines in cell cycle kinetics as studied in a transgenic system. Experimental Cell Research 308(2):254-64. https://doi.org/10.1016/j.yexcr.2005.04.027
Nguyen QH, Vu LTK, Nguyen LTN, Le SV, Chu MH (2019). Overexpression of the GmDREB6 gene enhances proline accumulation and salt tolerance in genetically modified soybean plants. Science Reports 9:19663. https://doi.org/10.1038/s41598-019-55895-0
Pandey P, Singh J, Achary VMM, Reddy MK (2015). Redox homeostasis via gene families of ascorbate-glutathione pathway. Frontiers in Environmental Science. https://doi.org/10.3389/fenvs.2015.00025
Pathak MR, da Silva JAT, Wani SH (2014). Polyamines in response to abiotic stress tolerance through transgenic approaches. GM Crops Food 5(2):87-96. https://doi.org/10.4161/gmcr.28774
Patra B, Schluttenhofer C, Wu Y, Pattanaik S, Yuan L (2013). Transcriptional regulation of secondary metabolite biosynthesis in plants. Biochimica et Biophysica Acta 1829(11):1236-1247. https://doi.org/10.1016/j.bbagrm.2013.09.006
Naliwajski M, Skłodowska M (2021). The relationship between the antioxidant system and proline metabolism in the leaves of cucumber plants acclimated to salt stress. Cells 10(3):609. https://doi.org/10.3390/cells10030609
Puyang X, An M, Xu L, Han L, Zhang X (2016). Protective effect of exogenous spermidine on ion and polyamine metabolism in Kentucky bluegrass under salinity stress. Horticulture, Environment, and Biotechnology 57:11-19. https://doi.org/10.1007/s13580-016-0113-x
Qi D, Xin-Hua Z, Le X, Chun-Ji J, Xiao-Guang W, Yi H, Jing W, Hai-Qiu Y (2019). Effects of potassium deficiency on photosynthesis, chloroplast ultrastructure, ROS, and antioxidant activities in maize (Zea mays L.) Journal of Integrative Agriculture 18(2):395-406 https://doi.org/10.1016/S2095-3119(18)61953-7
Qin C, Ahanger MA, Lin B, Huang Z, Zhou J, Ahmed N, Ai S, Mustafa NSA, Ashraf M, Zhang L (2021). Comparative transcriptomic analysis reveals the regulatory effects of acetylcholine on salt tolerance of Nicotiana benthamiana. Phytochemistry 181:112582. https://doi.org/10.1016/j.phytochem.2020.112582
Qin C, Ahanger MA, Zhou J, Ahmed N, Wei C, Yuan S, Ashraf M, Zhang L (2020). Beneficial role of acetylcholine in chlorophyll metabolism and photosynthetic gas exchange in Nicotiana benthamiana seedlings under salinity stress. Plant Biology 22(3):357-365 https://doi.org/10.1111/plb.13079
Rad PB, Roozban, MR, Karimi S, Ghahremani R, Vahdati K (2021). Osmolyte accumulation and sodium compartmentation has a key role in salinity tolerance of pistachios rootstocks. Agriculture 11:708. https://doi.org/10.3390/agriculture11080708
Rakesh B, Sudheer WN, Nagella P (2021). Role of polyamines in plant tissue culture: An overview. Plant Cell, Tissue and Organ Culture 145:487-506. https://doi.org/10.1007/s11240-021-02029-y
Roychoudhury A, Basu S, Sengupta DN (2011). Amelioration of salinity stress by exogenously applied spermidine or spermine in three varieties of indica rice differing in their level of salt tolerance. Journal of Plant Physiology 168:317-328. https://doi.org/10.1016/j.jplph.2010.07.009.
Sano T, Becker D, Ivashikina N, Wegner LH, Zimmermann U, Roelfsema MRG, Nagata T, Hedrich R (2007). Plant cells must pass a K+ threshold to re-enter the cell cycle. The Plant Journal 50(3):401-413. https://doi.org/10.1111/j.1365-313X.2007.03071.x
Sardans J, Peñuelas J (2021). Potassium control of plant functions: ecological and agricultural implications. Plants 10:419. https://doi.org/10.3390/plants10020419
Schields R, Burnett W (1960). Determination of protein-bound carbohydrate in serum by a modified anthrone method. Annals of Chemistry 32:885-886.
Singleton VL, Rossi Jr JA (1965) Colorimetry of total phenolics with phosphor-molybdic-phosphotungstic acid reagents. American Journal of Enology and Viticulture 16:144-153.
Smart RE, Bihgham GE, (1974). Rapid estimates of relative water content. Plant Physiology 53:258-260. https://doi.org/10.1104/pp.53.2.258
Soliman M, Alhaithloul HA, Hakeem KR, Alharbi BM, El-Esawi M, Elkelish A (2019). Exogenous nitric oxide mitigates nickel-induced oxidative damage in eggplant by upregulating antioxidants, osmolyte metabolism, and glyoxalase systems. Plants 8:562. https://doi.org/10.3390/plants8120562
Soliman M, Elkelish A, Souad T, Alhaithloul H, Farooq M (2020). Brassinosteroid seed priming with nitrogen supplementation improves salt tolerance in soybean. Physiology and Molecular Biology of Plants 26(3):501-511. https://doi.org/10.1007/s12298-020-00765-7
Sudhir P, Murthy S (2004). Effects of salt stress on basic processes of photosynthesis. Photosynthetica 42:481-486.
Todorov D, Karanov E, Smith A, Hall MA (2003). Chlorophyllase activity and chlorophyll content in wild type and Eti 5 Mutant of Arabidopsis thaliana subjected to low and high temperatures. Biologia Plantarum 46:633-636 https://doi.org/ 10.1023/A:1024896418839
Ugarte RM, Escudero A, Gavilán RG (2021). Assessing the role of selected osmolytes in Mediterranean high-mountain specialists Frontiers in Ecology and Evolution 31. https://doi.org/10.3389/fevo.2021.576122
Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Plant Science 151:59-66. https://doi.org/10.1016/S0168-9452(99)00197-1
Vuosku J, Karppinen K, Muilu-Mäkelä R, Kusano T, Sagor GHM, Avia K (2018). Scot’s pine amino propyltransferases shed new light on evolution of the polyamine biosynthesis pathway in seed plants. Annals of Botany 121:1243-1256. https://doi.org/10.1093/aob/mcy012
West G, Inzé D, Beemster GTS (2004). Cell cycle modulation in the response of the primary root of Arabidopsis to salt stress. Plant Physiology 135(2):050-1058. https://doi.org/10.1104/pp.104.040022
White PJ, Karley AJ (2010). Potassium Cell Biology of Metals and Nutrients. Springer, Berlin, pp 199-224.
Wink M (2018). Plant secondary metabolites modulate insect behavior-steps toward addiction? Frontiers in Physiology. https://doi.org/10.3389/fphys.2018.00364
Wu Y, Jin X, Liao W, Hu L, Dawuda MM, Zhao X, Tang Z, Gong T, Yu J (2018). 5-aminolevulinic acid (ALA) alleviated salinity stress in cucumber seedlings by enhancing chlorophyll synthesis pathway. Frontiers in Plant Science 9:635. https://doi.org/10.3389/fpls.2018.00635
Xu X, Du X, Wang F, Sha J, Chen Q, Tian G, Zhu Z, Ge S, Jiang Y (2020). Effects of potassium levels on plant growth, accumulation and distribution of carbon, and nitrate metabolism in apple dwarf rootstock seedlings. Frontiers in Plant Science 11:904. https://doi.org/10.3389/fpls.2020.00904
Yadav B, Jogawat A, Rahman MS, Narayan OP (2021) Secondary metabolites in the drought stress tolerance of crop plants: A review. Gene Reports 23:101040 https://doi.org/10.1016/j.genrep.2021.101040
Yang H, Wu F, Cheng J (2011). Reduced chilling injury in cucumber by nitric oxide and the antioxidant response. Food Chemistry 127:1237-1242. https://doi.org/10.1016/j.foodchem.2011.02.011
Zaid A, Mohammad F, Fariduddin Q (2020). Plant growth regulators improve growth, photosynthesis, mineral nutrient and antioxidant system under cadmium stress in menthol mint (Mentha arvensis L.). Physiology and Molecular Biology of Plants 26:25-39. https://doi.org/10.1007/s12298-019-00715-y
Zaid A, Wani SH (2019). Reactive oxygen species generation, scavenging and signaling in plant defense responses. In: Jogaiah S, Abdelrahman M (Eds). Bioactive Molecules in Plant Defense. Springer, Cham. https://doi.org/10.1007/978-3-030-27165-7_7
Zhang Y, Fang J, Wu X, Dong L (2018). Na+/K+ balance and transport regulatory mechanisms in weedy and cultivated rice (Oryza sativa L.) under salt stress. BMC Plant Biology 18:375. https://doi.org/10.1186/s12870-018-1586-9
Zhao D, Gao S, Zhang X, Zhang Z, Zheng H, Rong K, Zhao W, Khan SA (2021). Impact of saline stress on the uptake of various macro and micronutrients and their associations with plant biomass and root traits in wheat. Plant, Soil and Environment 67(2):61-70. https://doi.org/10.3389/fagro.2021.661932
Zhao S, Zhang Q, Liu M, Zhou H, Ma C, Wang P (2021). Regulation of plant responses to salt stress. International Journal of Molecular Sciences 22(9):4609. https://doi.org/10.3390/ijms22094609
Zhishen J, Mengcheng T, Jianming W (1999a). The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chemistry 64:555-559. https://doi.org/10.1016/S0308-8146(98)00102-2
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