Salicylic Acid Improves Tolerance Against Salt Stress Through Boosting Antioxidant Defense System in Black Bean

Abbaspour N, Babaee L. 2017. Effect of Salicylic Acid Application on Oxidative Damage and Antioxidant Activity of Grape (Vitis vinifera L.) Under Drought Stress Condition. International Journal of Horticultural Science and Technology 4(1), 29-50.
2. Afzal I, Basra S.M.A, Farooq M, Nawaz A. 2006. Alleviation of Salinity Stress in Spring Wheat by Hormonal Priming with ABA, Salicylic Acid and Ascorbic Acid. International Journal of Agriculture and Biology 8(1), 23-28.
3. Ahmad I, Khaliq T, Ahmad A, Basra SMA, Hasnain Z, Ali A. 2012. Effect of seed priming with ascorbic acid, salicylic acid and hydrogen peroxide on emergence, vigor and antioxidant
activities of maize. African Journal of Biotechnology 11(5), 1127-1132.
4. Anaya F, Fghire R, Wahbi S, Loutfi K. 2018. Influence of salicylic acid on seed germination of Vicia faba L. under salt stress. Journal of the Saudi Society of Agricultural Sciences 17, 1-8.
5. Ashraf M, Akram N.A, Arteca R.N, Foolad M.R. 2010. The physiological, biochemical and molecular roles of brassinosteroids and salicylic acid in plant processes and salt tolerance. Critical Review in Plant Science 29,162-190.
6. Bagheri M.Z. 2014. The effect of maize priming on germination characteristics, catalase and peroxidase enzyme activity, and total protein content under salt stress. International of Journal of Bioscience 4(2), 104-112.
7. Bahrani A, Pourreza J. 2012. Gibberlic Acid and Salicylic Acid Effects on Seed Germination and Seedlings Growth of Wheat (Triticum aestivum L.) Under Salt Stress Condition. World Applied Sciences Journal 18(5), 633-641.
8. Basra S.M.A, Farooq M, Rehman H, Saleem B.A. 2007. Improving the Germination and Early Seedling Growth in Melon (Cucumis melo L.) by Pre-sowing Salicylicate Treatments. International Journal of Agriculture and Biology 9(4), 550-554.
9. Borsani O, Valpuestan V, Botella M.A. 2001. Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiology 126, 1024-1030.
10. Boukraâ D, Benabdelli K, Belabid L and Bennabi F. 2013. Effect of salinity on chickpea seed germination pre-treated with salicylic acid. Scientific Journal of Biological Sciences 2(4), 86-93.
11. Boursiac Y, Chen S, Luu D.T, Sorieul M, Dries N, Maurel C. 2005. Early effects of salinity on water transport in Arabidopsis roots: molecular and cellular features of aquaporin expression. Plant Physiology 139, 790-805.
12. Bradford M. 1976. A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein–dye binding. Analytical Biochemistry 72, 248-254.
13. Buchanan B.B, Balmer Y. 2005. Redox regulation: a broadening horizon. Annual Review of Plant Biology 56, 187-220.
Fatemeh Heidarian & Parto Roshandel Int. J. Hort. Sci. Technol. 2021 8(2): 175-189
186
14. Bukhat S, Manzoor H, Zafar Z.U, Azeem F, Rasul S. 2020. Salicylic acid induced photosynthetic adaptability of Raphanus sativus to salt stress is associated with antioxidant capacity. Journal of Plant Growth Regulation 39(2), 809-822.
15. Chachoyan A.A, Oganesyan G.B. 1996. Antitumor of some species of family Lamiaceae. Rastitel 32(4), 59-64.
16. Chang C, Wang B, Shi L, Li Y, Duo L, Zhang W. 2010. Alleviation of salt stress-induced inhibition of seed germination in cucumber (Cucumis sativus L.) by ethylene and glutamate. Journal of Plant Physiology 167(14), 1152-1156.
17. Chen D.H, Ye H.C, Li G.F. 2000. Expression of a chimeric farnesyldiphosphate synthase gene in Artemisia annua L. transgenic plants via Agrobacterium tumefaciens-mediated transformation. Plant Science 155, 179-185.
18. Dallali H, Maalej E.M, Boughanmi N.G, Haouala R. 2012. Salicylic acid priming in Hedysarum carnosum and Hedysarum coronarium reinforces NaCl tolerance at germination and the seedling growth stage. Australian Journal of Crop Science 6(3), 407-414.
19. Das K, Roychoudhury A. 2014. Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Frontiers in Environmental Science 2, 53-66.
20. Dolatabadian A, SanavyS, Chashmi N. 2008. The effects of foliar application of ascorbic acid (Vitamin C) on antioxidant enzymes activities, lipid peroxidation and proline accumulation of canola (Brassica napus L.) under conditions of salt stress. Journal of Agronomy and Crop Science 194, 206-213.
21. Dong M, He X, Liu R.H. 2007. Phytochemicals of black bean seed coats: isolation, structure elucidation, and their antiproliferative and antioxidative activities. Journal of Agricultural and Food Chemistry 55(15), 6044-6051.
22. El Tayeb M.A. 2005. Response of barley grains to the interactive effect of salinity and salicylic acid. Plant Growth Regulation 45, 215-224. 23. El-Khallal S.M, Hathout T.A, Ahsour A.E, Kerrit A.A. 2009. Brassinolide and salicylic acid induced antioxidant enzymes, hormonal balance and protein profile of maize plants grown under salt stress. Research Journal of Agriculture and Biological Sciences 5(4), 391-402.
24. El-Mergawi R.A, Abdel-Wahed M.S.A. 2004. Diversity in salicylic acid effects on growth criteria and different indol acetic acid forms among faba bean and maize. Egyptian Journal of Agronomy 26, 49-61.
25. Enteshari,M, Sharif-Zahed F, Zare S, Farhangfar M, Dashtaki M. 2012. Effects of seed priming on mung bean (Vigna radiate) cultivars with salicylic acid and potassium nitrate under salinity stress. International Journal of Agricultural Research and Reviews 2, 926-932.
26. Escobar H, Bustos R, Fernández F, Cárcamo H, Silva H, Frank N, Cardemil L. 2010. Mitigating effect of salicylic acid and nitrate on water relations and osmotic adjustment in maize, cv. Lluteño exposed to salinity. Cienciae Investigacion Agraria 37, 71-81. 27. Farhangi-Abriz S, Ghassemi-Golezani K. 2018. How can salicylic acid and jasmonic acid mitigate salt toxicity in soybean plants?. Ecotoxicology and environmental safety 1 (147), 1010-1016.
28. Farooq M, Basra S.M.A, Rehman H, Hussain M, Amanat Y. 2007. Pre-sowing salicylicate seed treatments improve the germination and early seedling growth in fine rice. Pakistan Journal of Agricultural Sciences 44(1), 1-8. 29. Gharoobi, B., Ghorbani, M, Ghasemi, N.M. 2012. Effects of different levels of osmotic potential on germination percentage and germination rate of barley, corn and canola. Iranian Journal of Plant Physiology 2(2), 413- 417.
30. Ghoohestani A, Gheisary H, Zahedi S.M, Dolatkhahi A. 2012. Effect of Seed Priming of Tomato with Salicylic Acid, Ascorbic Acid and Hydrogen Peroxideon Germination and Plantlet Growth in Saline Conditions. International journal of Agronomy and Plant Production 3(S), 700-704.
31. Guajardo-Flores D, Serna-Saldívar S.O, Gutiérrez-Uribe J.A. 2013. Evaluation of the antioxidant and antiproliferative activities of extracted saponins and flavonols from germinated black beans (Phaseolus vulgaris L.). Food chemistry 141(2), 1497-1503.
32. Gunes A, Inal A, Alpaslan M, Eraslan F, Bagci E.G, Cicek N. 2007. Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity. Journal of Plant Physiology 164, 728-736.
Fatemeh Heidarian & Parto Roshandel Int. J. Hort. Sci. Technol. 2021 8(2): 175-189
187
33. Haghshenas M, Nazarideljou M, Shokoohian A. 2020. Phytochemical and Quality Attributes of Strawberry Fruit under Osmotic Stress of Nutrient Solution and Foliar Application of Putrescine and Salicylic Acid. International Journal of Horticultural Science and Technology 7(3), 263-278.
34. Hamada A.M, Al-Hakimi M, 2001. Salicylic acid versus salinity-drought induced stress on wheat seedlings. Rostl Vyr 47, 444-450.
35. Hayata Q, Hayata S, Irfan M, Ahmad A. 2010. Effect of exogenous salicylic acid under changing environment: A review. Environmental and Experimental Botany 68, 14-25.
36. Hopper N.W, Overholt J.R, Martin J.R. 1979. Effect of cultivar, temperature and seed size on the germination and emergence of soya beans (Glycine max (L.) Merr.). Annals of Botany 44(3), 301-308.
37. Hussain K, Nawaz K, Majeed A, Ilyas U, Lin F, Ali K, Nisar M.F. 2011. Role of exogenous salicylic acid applications for salt tolerance in violet. Sarhad Journal of Agriculture 27(2), 171-175.
38. ISTA., 2004. International Rules for Seed Testing. International Seed Testing Association. Zurich.
39. Jafar M.Z, Farooq M, Cheema M.A, Afzal I, Basra M.A, Wahid M.A, Aziz T, Shah M. 2012. Improving the Performance of Wheat by Seed Priming Under Saline Conditions. Journal of Agriculture and Crop Science 198, 38-45.
40. Javaheri M, Mashayekhi K, Dadkhah A, Tavallaee F.Z. 2012. Effects of salicylic acid on yield and quality characters of tomato fruit (Lycopersicum esculentum Mill.). International Journal of Agriculture and Crop Science 4(16), 1184-1187.
41. Jayakannan M, Bose J, Babourina O, Shabala S, Massart A, Poschenrieder C, Rengel Z. 2015. NPR1-dependent salicylic acid signalling pathway is pivotal for enhanced salt and oxidative stress tolerance in Arabidopsis. Journal of Experimental Botany 66, 1865-1875. 42. Jebara S, Jebara M, Limam F, Aouani M.E. 2005. Changes in ascorbate peroxidase, catalase, guaiacol peroxidase and superoxide dismutase activities in common bean (Phaseolus vulgaris) nodules under salt stress. Journal of plant physiology 162(8), 929-936. 43. Jiang L, Wang J, Li Y, Wang Z, Liang J, Wang R, Chen Y, Ma W, Qi B, Zhang M. 2014. Effects of ultrasound on the structure and physical properties of black bean protein isolates. Food Research International 62, 595-601.
44. Jini D, Joseph B. 2017. Physiological Mechanism of Salicylic Acid for Alleviation of Salt Stress in Rice. Rice Science 24(2), 97-108.
45. Joseph B, Jini D. 2010. Insight into the role of antioxidant enzymes for salt tolerance in plants. International Journal Botany 6, 456-464.
46. Kato M, Shimizu S. 1985. Chlorophyll metabolism in higher plants. Plant Cell Physiology 26, 1291-1301.
47. Kaydan D, Yagmur M and Okut N. 2007. Effects of Salicylic acid on the growth and some physiological characters in salt stressed wheat (Triticum aestivum L.). Tarim Bilimleri Dergisi 13(2), 114-119.
48. Ksouri R, Megdiche W, Debez A, Falleh H, Grignon C, Abdelly C. 2007. Salinity effects on polyphenol content and antioxidant activities in leaves of halophyte Cakile maritime. Plant Physiology Biochemistry 45, 44-49. 49. Li T, Hu Y, Du X, Tang H, Shen C, Wu J. 2014. Salicylic acid alleviates the adverse effects of salt stress in Torreya grandis cv. Merrillii seedlings by activating photosynthesis and enhancing antioxidant systems. PLOS one 9(10), e109492. 50. Li Z, Xu J, Gao Y, Wang C, Guo G, Luo Y, Huang Y, Hu W, Sheteiwy M.S, Guan Y, Hu J. 2017. The Synergistic Priming Effect of Exogenous Salicylic Acid and H2O2 on Chilling Tolerance Enhancement during Maize (Zea mays L.) Seed Germination. Frontier in Plant Science 8, 1153-1167. 51. Liu S, Dong Y, Xu L, Kong J. 2014. Effects of foliar applications of nitric oxide and salicylic acid on salt-induced changes in photosynthesis and antioxidative metabolism of cotton seedlings. Plant Growth Regulation 73(1), 67-78.
52. Lutts S, Kinet J.M, Bouharmont J. 1996. NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Annals of Botany 78, 389-398. 53. Ma X, Zheng J, Zhang X, Hu Q, Qian R. 2017. Salicylic acid alleviates the adverse effects of salt stress on Dianthus superbus (Caryophyllaceae) by activating photosynthesis, protecting morphological structure, and enhancing the antioxidant system. Frontiers in plant science 8, 600-613.
Fatemeh Heidarian & Parto Roshandel Int. J. Hort. Sci. Technol. 2021 8(2): 175-189
188
54. Manaa A, Gharbi E, Mimouni H, Wasti S, Aschi-Smiti S, Lutts S, Ahmed H.B.2014. Simultaneous application of salicylic acid and calcium improves salt tolerance in two contrasting tomato (Solanum lycopersicum) cultivars. South African Journal of Botany 95, 32-39.
55. Mojica L, Meyer A, Berhow M.A, de Mejía E.G. 2015. Bean cultivars (Phaseolus vulgaris L.) have similar high antioxidant capacity, in vitro inhibition of α-amylase and α-glucosidase while diverse phenolic composition and concentration. Food Research International 69, 38-48.
56. Munns R. 2002. Comparative physiology of salt and water stress. Plant, Cell and Environment 25, 239-250.
57. Nag S, Saha K, Choudhuri A. 2000. A rapid and sensitive assay method for measuring amine oxidase based on hydrogen peroxide-titanium complex formation. Plant Science 157, 157-163.
58. Nazar R, Iqbal N, Syeed S, Khan N.A. 2011. Salicylic acid alleviates decreases in photosynthesis under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism differentially in two mung-bean cultivars. Journal of Plant Physiology 168, 807-815.
59. Nemat-Ala M.M, Hassan N.M. 2006. Changes of antioxidants levels in two maize lines following atrazine treatments. Plant Physiology and Biochemistry 44, 202-210.
60. Nonogaki H, Bassel G.W, Bewley J.D. 2010. Germination-still a mystery. Plant Science 179, 574-581.
61. Noreen S, Ashraf M. 2010. Modulation of salt (NaCl)-induced effects on oil composition and fatty acid profile of sunflower (Helianthus annuus L.) by exogenous application of salicylic acid. Journal of the Science of Food and Agriculture 90, 2608-2616.
62. Ondrasek G, Rengel Z, Veres S. 2011. Soil salinization and salt stress in crop production. In: Shanker A, Venkateswarlu B (eds) Abiotic stress in plants—mechanisms and adaptations. ISBN: 978-953-307-394-1, pp 171-190.
63. Qadir M, Quille´rou E, Nangia V, Murtaza G, Singh M, Thomas R.J, Drechsel P, Noble A.D. 2014. Economics of salt-induced land degradation and restoration. Natural Resources Forum 38(4), 282-295.
64. Radi A.A, Farghaly F.A, Hamada A.M. 2013. Physiological and biochemical responses of salt-
tolerant and salt-sensitive wheat and bean cultivars to salinity. Journal of Biology Earth Science 3(1), 72-88. 65. Rady M.M, Mohamed G.F. 2015.Modulation of salt stress effects on the growth, physio-chemical attributes and yields of Phaseolus vulgaris L. plants by the combined application of salicylic acid and Moringa oleifera leaf extract. Scientia Horticulturae 193, 105-113.
66. Rai VK. 2002. Role of amino acids in plant responses to stress. Biology Plantarum 45(4), 481-487.
67. Rajjou L, Belghazi M, Huguet R, Robin C, Moreau A, Job C, Job D. 2006. Proteomic investigation of the effect of salicylic acid on Arabidopsis seed germination and establishment of early defense mechanisms. Plant Physiology 141, 910-923.
68. Rehman H, Farooq M, Basra S.M.A, Afzal I. 2011. Hormonal Priming with Salicylic Acid Improves the Emergence and Early Seedling Growth in Cucumber. Journal of Agriculture and Social Sciences 7, 109-113
69. Sakhabutdinova A.R, Fatkhutdinova R., Bezrukova M.V, Shakirova F.M. 2003. Salicylic acid prevents the damaging action of stress factors on wheat plants. Bulgarian Journal of Plant Physiology, 314–319 (Special Issue).
70. Semida W.M, Rady M.M. 2014. Pre-soaking in 24-epibrassinolide or salicylicacid improves seed germination, seedling growth, and anti-oxidant capacity in Phaseolus vulgaris L. grown under NaCl stress. Journal of Horticulture Science and Biotechnology 89 (3), 338–344.
71. Shabala S. 2013. Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Annals of Botany 112, 1209-1221.
72. Shah J. 2003. The salicylic acid loop in plant defense. Current Opinion in Plant Biology 6(4), 365-371.
73. Shahmoradi H, Naderi D. 2018. Improving Effects of Salicylic Acid on Morphological, Physiological and Biochemical Responses of Salt-imposed Winter Jasmine. International Journal of Horticultural Science and Technology 5(2), 219-230.
74. Shakirova F.M, Sakhabutdinova A.R, Bezrukova M.V, Fatkhutdinova R.A, Fatkhutdinova DR. 2003. Changes in the hormonal status of wheat seedlings induced by salicylic acid and salinity. Plant Science 164, 317-322.
Fatemeh Heidarian & Parto Roshandel Int. J. Hort. Sci. Technol. 2021 8(2): 175-189
189
75. Shi Q, Zhu Z. 2008. Effects of exogenous salicylic acid on manganese toxicity, element contents and antioxidative system in cucumber. Environmental and Experimental of Botany 63, 317-326. 76. Syeed S, Anjum N.A, Nazar R, Iqbal N, Masood A, Khan N.A. 2011. Salicylic acid-mediated changes in photosynthesis, nutrients content and antioxidant metabolism in two mustard (Brassica juncea L.) cultivars differing in salt tolerance. Acta physiologiae plantarum 33(3), 877-886.
77. Szalai G, Páldi E, Janda T. 2005. Effect of salt stress on the endogenous salicylic acid content in maize (Zea mays L.) plants. Acta Biologica Szegediensis 49, 47-48.
78. Szepesi A, Csiszar J, Bajkan S.z, Gemes K, Horvath F, Erdei L, Deer A, Simon LM, Tari I. 2005. Role of salicylic acid pre-treatment on the acclimation of tomato plants to salt- and osmotic stress. Acta Biological Szegediensi 49, 123-125.
79. Szepesi A, Csiszár J, Gémes K, Horváth E, Horváth F, Simon M.L. 2009. Salicylic acid improves acclimation to salt stress by stimulating abscisic aldehyde oxidase activity and abscisic acid accumulation, and increases Na+ content in leaves without toxicity symptoms in Solanum lycopersicum L. Journal of Plant Physiology 166, 914-925. 80. Tahjib-Ul-Arif M, Siddiqui M.N, Sohag A.A, Sakil M.A, Rahman M.M, Polash M.A, Mostofa M.G, Tran L.S. 2018. Salicylic acid-mediated enhancement of photosynthesis attributes and antioxidant capacity contributes to yield improvement of maize plants under salt stress. Journal of Plant Growth Regulation 37(4), 1318-1330. 81. Taïbi K, Taïbi F, Abderrahim L.A, Ennajah A, Belkhodja M, Mulet J.M. 2016. Effect of salt stress on growth, chlorophyll content, lipid peroxidation and antioxidant defence systems in Phaseolus vulgaris L. South African Journal of Botany 105, 306-312.
82. Tammam A.A, Alhamd M.F.A, Hemeda M.M. 2008. Study of salt tolerance in wheat (Triticum aestivum L.) cultivar Banysoif 1. Australian Journal of Crop Science 1(3), 115-125.
83. Tari I, Csiszar J, Gabriella S, Horvath F, Pecsvaradi A, Kiss G, Szepsi A, Szabo M, Erdei L. 2002. Acclimation of tomato plants to salinity stress after a salicylic acid pre-treatment. Acta Biologica Szegediensis 46, 55–56.
84. Tari I, Simon LM, Deer KA, Csiszar J, Bajkan Sz, Kis GY, Szepesi A. 2004. Influence of salicylic acid on salt stress acclimation of tomato plants: oxidative stress responses and osmotic adaptation. Acta Physiologia Plantarum 265S, 237.
85. Tufail A, Arfan M, Gurmani AR, Khan A, Bano A. 2013. Salicylic acid induced salinity tolerance in maize (Zea mays). Pakistani Journal of Botany 45, 75-82.
86. Verdoucq L, Grondin A, Maurel C. 2008. Structure-function analysis of plant aquaporin AtPIP2; 1 gating by divalent cations and protons. Biochemistry Journal 415, 409-416.