The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
권호 표지
DOI QR코드

DOI QR Code

Salicylic Acid as a Safe Plant Protector and Growth Regulator

  • Koo, Young Mo (Department of Plant Medicals, Andong National University) ;
  • Heo, A Yeong (Department of Plant Medicals, Andong National University) ;
  • Choi, Hyong Woo (Department of Plant Medicals, Andong National University)
  • Received : 2019.12.16
  • Accepted : 2019.01.27
  • Published : 2020.02.01
Download PDF
⟨ Previous Next ⟩

Abstract

Since salicylic acid (SA) was discovered as an elicitor of tobacco plants inducing the resistance against Tobacco mosaic virus (TMV) in 1979, increasing reports suggest that SA indeed is a key plant hormone regulating plant immunity. In addition, recent studies indicate that SA can regulate many different responses, such as tolerance to abiotic stress, plant growth and development, and soil microbiome. In this review, we focused on the recent findings on SA's effects on resistance to biotic stresses in different plant-pathogen systems, tolerance to different abiotic stresses in different plants, plant growth and development, and soil microbiome. This allows us to discuss about the safe and practical use of SA as a plant defense activator and growth regulator. Crosstalk of SA with different plant hormones, such as abscisic acid, ethylene, jasmonic acid, and auxin in different stress and developmental conditions were also discussed.

Keywords

References

  1. Ali, S., Ganai, B. A., Kamili, A. N., Bhat, A. A., Mir, Z. A., Bhat, J. A., Tyagi, A., Islam, S. T., Mushtaq, M., Yadav, P., Rawat, S. and Grover, A. 2018. Pathogenesis-related proteins and peptides as promising tools for engineering plants with multiple stress tolerance. Microbiol. Res. 212-213:29-37. https://doi.org/10.1016/j.micres.2018.04.008
  2. Appu, M. and Muthukrishnan, S. 2014. Foliar application of salicylic acid stimulates flowering and induce defense related proteins in finger millet plants. Univers. J. Plant Sci. 2:14-18. https://doi.org/10.13189/ujps.2014.020102
  3. Audenaert, K., De Meyer, G. B. and Höfte, M. M. 2002. Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiol. 128:491-501. https://doi.org/10.1104/pp.010605
  4. Bandurska, H. and Stroiński, A. 2005. The effect of salicylic acid on barley response to water deficit. Acta Physiol. Plant. 27:379-386. https://doi.org/10.1007/s11738-005-0015-5
  5. Bulgarelli, D., Rott, M., Schlaeppi, K., Ver Loren van Themaat, E., Ahmadinejad, N., Assenza, F., Rauf, P., Huettel, B., Reinhardt, R., Schmelzer, E., Peplies, J., Gloeckner, F. O., Amann, R., Eickhorst, T. and Schulze-Lefert, P. 2012. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91-95. https://doi.org/10.1038/nature11336
  6. Castro-Torres, Y., Katholi, R. E. and Yar Khan, N. 2015. Aspirin for primary prevention of cardiovascular diseases: current concepts, unanswered questions and future directions. Hellenic J. Cardiol. 56:461-474.
  7. Chandrasekhar, B., Umesha, S. and Naveen Kumar, H. N. 2017. Proteomic analysis of salicylic acid enhanced disease resistance in bacterial wilt affected chilli (Capsicum annuum) crop. Physiol. Mol. Plant Pathol. 98:85-96. https://doi.org/10.1016/j.pmpp.2017.04.002
  8. Chang, C.-W., Horng, J.-T., Hsu, C.-C. and Chen, J.-M. 2016. Mean daily dosage of aspirin and the risk of incident alzheimer's dementia in patients with type 2 diabetes mellitus: a nationwide retrospective cohort study in Taiwan. J. Diabetes Res. 2016:9027484.
  9. Choi, H. W., Tian, M., Manohar, M., Harraz, M. M., Park, S.- W., Schroeder, F. C., Snyder, S. H. and Klessig, D. F. 2015a. Human GAPDH is a target of aspirin's primary metabolite salicylic acid and its derivatives. PLoS ONE 10:e0143447. https://doi.org/10.1371/journal.pone.0143447
  10. Choi, H. W., Tian, M., Song, F., Venereau, E., Preti, A., Park, S.-W., Hamilton, K., Swapna, G. V. T., Manohar, M., Moreau, M., Agresti, A., Gorzanelli, A., De Marchis, F., Wang, H., Antonyak, M., Micikas, R. J., Gentile, D. R., Cerione, R. A., Schroeder, F. C., Montelione, G. T., Bianchi, M. E. and Klessig, D. F. 2015b. Aspirin's active metabolite salicylic acid targets high mobility group box 1 to modulate inflammatory responses. Mol. Med. 21:526-535. https://doi.org/10.2119/molmed.2015.00148
  11. Choi, H. W., Wang, L., Powell, A. F., Strickler, S. R., Wang, D., Dempsey, D. A., Schroeder, F. C. and Klessig, D. F. 2019. A genome-wide screen for human salicylic acid (SA)-binding proteins reveals targets through which SA may influence development of various diseases. Sci. Rep. 9:13084. https://doi.org/10.1038/s41598-019-49234-6
  12. Connor, D. 2002. Climate change and global crop productivity. Crop Sci. 42:978.
  13. Daw, B. D., Zhang, L. H. and Wang, Z. Z. 2008. Salicylic acid enhances antifungal resistance to Magnaporthe grisea in rice plants. Australas. Plant Pathol. 37:637-644. https://doi.org/10.1071/AP08054
  14. Deenamo, N., Kuyyogsuy, A., Khompatara, K., Chanwun, T., Ekchaweng, K. and Churngchow, N. 2018. Salicylic acid induces resistance in rubber tree against Phytophthora palmivora. Int. J. Mol. Sci. 19:1883. https://doi.org/10.3390/ijms19071883
  15. Dempsey, D. A. and Klessig, D. F. 2017. How does the multifaceted plant hormone salicylic acid combat disease in plants and are similar mechanisms utilized in humans? BMC Biol. 15:23. https://doi.org/10.1186/s12915-017-0364-8
  16. El Oirdi, M., El Rahman, T. A., Rigano, L., El Hadrami, A., Rodriguez, M. C., Daayf, F., Vojnov, A. and Bouarab, K. 2011. Botrytis cinerea manipulates the antagonistic effects between immune pathways to promote disease development in tomato. Plant Cell 23:2405-2421. https://doi.org/10.1105/tpc.111.083394
  17. Erb, M., Meldau, S. and Howe, G. A. 2012. Role of phytohormones in insect-specific plant reactions. Trends Plant Sci. 17:250-259. https://doi.org/10.1016/j.tplants.2012.01.003
  18. Esmailzadeh, M., Soleimani, M. J. and Rouhani, H. 2008. Exogenous applications of salicylic acid for inducing systemic acquired resistance against tomato stem canker disease. J. Biol. Sci. 8:1039-1044. https://doi.org/10.3923/jbs.2008.1039.1044
  19. Ferrari, S., Plotnikova, J. M., De Lorenzo, G. and Ausubel, F. M. 2003. Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. Plant J. 35:193-205. https://doi.org/10.1046/j.1365-313X.2003.01794.x
  20. Glazebrook, J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43:205-227. https://doi.org/10.1146/annurev.phyto.43.040204.135923
  21. Guan, L. and Scandalios, J. G. 1995. Developmentally related responses of maize catalase genes to salicylic acid. Proc. Natl. Acad. Sci. U. S. A. 92:5930-5934. https://doi.org/10.1073/pnas.92.13.5930
  22. Gunes, A., Inal, A., Alpaslan, M., Eraslan, F., Bagci, E. G. and 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. J. Plant Physiol. 164:728-736. https://doi.org/10.1016/j.jplph.2005.12.009
  23. Gutierrez-Coronado, M. A., Trejo-Lopez, C. and Larque-Saavedra, A. 1998. Effects of salicylic acid on the growth of roots and shoots in soybean. Plant Physiol. Biochem. 36:563-565. https://doi.org/10.1016/S0981-9428(98)80003-X
  24. Hong, J. K. and Hwang, B. K. 2005. Induction of enhanced disease resistance and oxidative stress tolerance by overexpression of pepper basic PR-1 gene in Arabidopsis. Physiol. Plant. 124:267-277. https://doi.org/10.1111/j.1399-3054.2005.00515.x
  25. Horvath, E., Csiszar, J., Galle, A., Poor, P., Szepesi, A. and Tari, I. 2015. Hardening with salicylic acid induces concentrationdependent changes in abscisic acid biosynthesis of tomato under salt stress. J. Plant Physiol. 183:54-63. https://doi.org/10.1016/j.jplph.2015.05.010
  26. Horvath, E., Szalai, G. and Janda, T. 2007. Induction of abiotic stress tolerance by salicylic acid signaling. J. Plant Growth Regul. 26:290-300. https://doi.org/10.1007/s00344-007-9017-4
  27. Jendoubi, W., Harbaoui, K. and Hamada, W. 2017. Salicylic acidinduced resistance against Fusarium oxysporumf.s.pradicis lycopercisi in hydroponic grown tomato plants. J. New Sci. Agric. Biotechnol. 21:985-995.
  28. Jiang, C.-J., Shimono, M., Sugano, S., Kojima, M., Yazawa, K., Yoshida, R., Inoue, H., Hayashi, N., Sakakibara, H. and Takatsuji, H. 2010. Abscisic acid interacts antagonistically with salicylic acid signaling pathway in rice-Magnaporthe grisea interaction. Mol. Plant-Microbe Interact. 23:791-798. https://doi.org/10.1094/MPMI-23-6-0791
  29. Ju, C. and Chang, C. 2015. Mechanistic insights in ethylene perception and signal transduction. Plant Physiol. 169:85-95. https://doi.org/10.1104/pp.15.00845
  30. Kalachova, T., Puga-Freitas, R., Kravets, V., Soubigou-Taconnat, L., Repellin, A., Balzergue, S., Zachowski, A. and Ruelland, E. 2016. The inhibition of basal phosphoinositide-dependent phospholipase C activity in Arabidopsis suspension cells by abscisic or salicylic acid acts as a signalling hub accounting for an important overlap in transcriptome remodelling induced by these hormones. Environ. Exp. Bot. 123:37-49. https://doi.org/10.1016/j.envexpbot.2015.11.003
  31. Kazemi, M. 2013. Foliar application of salicylic acid and calcium on yield, yield component and chemical properties of strawberry. Bull. Environ. Pharmacol. Life Sci. 2:19-23.
  32. Khan, M. I. R., Fatma, M., Per, T. S., Anjum, N. A. and Khan, N. A. 2015. Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Front. Plant Sci. 6:462.
  33. Khanam, N. N., Ueno, M., Kihara, J., Honda, Y. and Arase, S. 2005. Suppression of red light-induced resistance in broad beans to Botrytis cinerea by salicylic acid. Physiol. Mol. Plant Pathol. 66:20-29. https://doi.org/10.1016/j.pmpp.2005.03.006
  34. Klessig, D. F., Choi, H. W. and Dempsey, D. A. 2018. Systemic acquired resistance and salicylic acid: past, present, and future. Mol. Plant-Microbe Interact. 31:871-888. https://doi.org/10.1094/MPMI-03-18-0067-CR
  35. Kobeasy, M. I., El-Beltagi, H. S., El-Shazly, M. A. and Khattab, E. A. H. 2011. Induction of resistance in Arachis hypogaea L. against Peanut mottle virus by nitric oxide and salicylic acid. Physiol. Mol. Plant Pathol. 76:112-118. https://doi.org/10.1016/j.pmpp.2011.07.005
  36. Korver, R. A., Koevoets, I. T. and Testerink, C. 2018. Out of shape during stress: a key role for auxin. Trends Plant Sci. 23:783-793. https://doi.org/10.1016/j.tplants.2018.05.011
  37. Kovacik, J., Klejdus, B., Hedbavny, J. and Backor, M. 2009. Salicylic acid alleviates NaCl-induced changes in the metabolism of Matricaria chamomilla plants. Ecotoxicology 18:544-554. https://doi.org/10.1007/s10646-009-0312-7
  38. Krantev, A., Yordanova, R., Janda, T., Szalai, G. and Popova, L. 2008. Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. J. Plant Physiol. 165:920-931. https://doi.org/10.1016/j.jplph.2006.11.014
  39. Kundu, S., Chakraborty, D. and Pal, A. 2011. Proteomic analysis of salicylic acid induced resistance to Mungbean Yellow Mosaic India Virus in Vigna mungo. J. Proteomics 74:337-349. https://doi.org/10.1016/j.jprot.2010.11.012
  40. Kunkel, B. N. and Brooks, D. M. 2002. Cross talk between signaling pathways in pathogen defense. Curr. Opin. Plant Biol. 5:325-331. https://doi.org/10.1016/S1369-5266(02)00275-3
  41. Le Thanh, T., Thumanu, K., Wongkaew, S., Boonkerd, N., Teaumroong, N., Phansak, P. and Buensanteai, N. 2017. Salicylic acid-induced accumulation of biochemical components associated with resistance against Xanthomonas oryzae pv. oryzae in rice. J. Plant Interact. 12:108-120. https://doi.org/10.1080/17429145.2017.1291859
  42. Lebeis, S. L., Paredes, S. H., Lundberg, D. S., Breakfield, N., Gehring, J., McDonald, M., Malfatti, S., Glavina del Rio, T., Jones, C. D., Tringe, S. G. and Dangl, J. L. 2015. Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349:860-864. https://doi.org/10.1126/science.aaa8764
  43. Li, L. and Zou, Y. 2017. Induction of disease resistance by salicylic acid and calcium ion against Botrytis cinerea in tomato (Lycopersicon esculentum). Emir. J. Food Agric. 29:78-82. https://doi.org/10.9755/ejfa.2016-10-1515
  44. Lu, H. 2009. Dissection of salicylic acid-mediated defense signaling networks. Plant Signal. Behav. 4:713-717. https://doi.org/10.4161/psb.4.8.9173
  45. Lundberg, D. S., Lebeis, S. L., Paredes, S. H., Yourstone, S., Gehring, J., Malfatti, S., Tremblay, J., Engelbrektson, A., Kunin, V., Del Rio, T. G., Edgar, R. C., Eickhorst, T., Ley, R. E., Hugenholtz, P., Tringe, S. G. and Dangl, J. L. 2012. Defining the core Arabidopsis thaliana root microbiome. Nature 488:86-90. https://doi.org/10.1038/nature11237
  46. Manzoor, K., Ilyas, N., Batool, N., Ahmad, B. and Arshad, M. 2015. Effect of salicylic acid on the growth and physiological characteristics of maize under stress conditions. J. Chem. Soc. Pakistan 37:588-593.
  47. Metwally, A., Finkemeier, I., Georgi, M. and Dietz, K.-J. 2003. Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiol. 132:272-281. https://doi.org/10.1104/pp.102.018457
  48. Mohan Babu, R., Sajeena, A., Vijaya Samundeeswari, A., Sreedhar, A., Vidhyasekaran, P., Seetharaman, K. and Reddy, M. S. 2003. Induction of systemic resistance to Xanthomonas oryzae pv. oryzae by salicylic acid in Oryza sativa (L.). J. Plant Dis. Prot. 110:419-431. https://doi.org/10.1007/BF03356119
  49. Ng, L. M., Melcher, K., Teh, B. T. and Xu, H. E. 2014. Abscisic acid perception and signaling: structural mechanisms and applications. Acta Pharmacol. Sin. 35:567-584. https://doi.org/10.1038/aps.2014.5
  50. Ngullie, C. R., Tank, R. V. and Bhanderi, D. R. 2014. Effect of salicylic acid and humic acid on flowering, fruiting, yield and quality of mango (Mangifera indica L.) cv. KESAR. Adv. Res. J. Crop Improv. 5:136-139. https://doi.org/10.15740/HAS/ARJCI/5.2/136-139
  51. Pasternak, T., Groot, E. P., Kazantsev, F. V., Teale, W., Omelyanchuk, N., Kovrizhnykh, V., Palme, K. and Mironova, V. V. 2019. Salicylic acid affects root meristem patterning via auxin distribution in a concentration-dependent manner. Plant Physiol. 180:1725-1739. https://doi.org/10.1104/pp.19.00130
  52. Perez-Llorca, M., Munoz, P., Muller, M. and Munne-Bosch, S. 2019. Biosynthesis, metabolism and function of auxin, salicylic acid and melatonin in climacteric and non-climacteric fruits. Front. Plant Sci. 10:136. https://doi.org/10.3389/fpls.2019.00136
  53. Radwan, D. E. M., Fayez, K. A., Mahmoud, S. Y., Hamad, A. and Lu, G. 2007. Physiological and metabolic changes of Cucurbita pepo leaves in response to zucchini yellow mosaic virus (ZYMV) infection and salicylic acid treatments. Plant Physiol. Biochem. 45:480-489. https://doi.org/10.1016/j.plaphy.2007.03.002
  54. Rivas-San Vicente, M. and Plasencia, J. 2011. Salicylic acid beyond defence: its role in plant growth and development. J. Exp. Bot. 62:3321-3338. https://doi.org/10.1093/jxb/err031
  55. Robert-Seilaniantz, A., Grant, M. and Jones, J. D. G. 2011. Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu. Rev. Phytopathol. 49:317-343. https://doi.org/10.1146/annurev-phyto-073009-114447
  56. Rothwell, P. M., Wilson, M., Elwin, C.-E., Norrving, B., Algra, A., Warlow, C. P. and Meade, T. W. 2010. Long-term effect of aspirin on colorectal cancer incidence and mortality: 20-year follow-up of five randomised trials. Lancet 376:1741-1750. https://doi.org/10.1016/S0140-6736(10)61543-7
  57. Saikia, R., Singh, T., Kumar, R., Srivastava, J., Srivastava, A. K., Singh, K. and Arora, D. K. 2003. Role of salicylic acid in systemic resistance induced by Pseudomonas fluorescens against Fusarium oxysporum f. sp. ciceri in chickpea. Microbiol. Res. 158:203-213. https://doi.org/10.1078/0944-5013-00202
  58. Sakhabutdinova, A. R., Fatkhutdinova, D. R., Bezrukova, M. V. and Shakirova, F. M. 2003. Salicylic acid prevents the damaging action of stress factors on wheat plants. Bulg. J. Plant Physiol. 29(3-4 Spec issue):314-319.
  59. Sallam, A. M. and Ibrahim, H. I. M. 2015. Effect of grain priming with salicylic acid on germination speed, seedling characters, anti-oxidant enzyme activity and forage yield of teosinte. Am. Eurasian J. Agric. Environ. Sci. 15:744-753.
  60. Sarowar, S., Kim, Y. J., Kim, E. N., Kim, K. D., Hwang, B. K., Islam, R. and Shin, J. S. 2005. Overexpression of a pepper basic pathogenesis-related protein 1 gene in tobacco plants enhances resistance to heavy metal and pathogen stresses. Plant Cell Rep. 24:216-224. https://doi.org/10.1007/s00299-005-0928-x
  61. Senaratna, T., Touchell, D., Bunn, E. and Dixon, K. 2000. Acetyl salicylic acid (Aspirin) and salicylic acid induce multiple stress tolerance in bean and tomato plants. Plant Growth Regul. 30:157-161. https://doi.org/10.1023/A:1006386800974
  62. Shaaban, M. M., Abd El-Aal, A. M. K. and Ahmed, F. F. 2011. Insight into the effect of salicylic acid on apple trees growing under sandy saline soil. Res. J. Agric. Biol. Sci. 7:150-156.
  63. Steinberg, G. R., Dandapani, M. and Hardie, D. G. 2013. AMPK: mediating the metabolic effects of salicylate-based drugs? Trends Endocrinol. Metab. 24:481-487. https://doi.org/10.1016/j.tem.2013.06.002
  64. Stella de Freitas, T. F., Stout, M. J. and Sant'Ana, J. 2019. Effects of exogenous methyl jasmonate and salicylic acid on rice resistance to Oebalus pugnax. Pest Manag. Sci. 75:744-752. https://doi.org/10.1002/ps.5174
  65. Szalai, G., Pal, M. and Janda, T. 2011. Abscisic acid may alter the salicylic acid-related abiotic stress response in maize. Acta Biol. Szeged. 55:155-157.
  66. Tschanz, J. T., Norton, M. C., Zandi, P. P. and Lyketsos, C. G. 2013. The Cache County Study on Memory in Aging: factors affecting risk of Alzheimer's disease and its progression after onset. Int. Rev. Psychiatry 25:673-685. https://doi.org/10.3109/09540261.2013.849663
  67. Ulferts, S., Delventhal, R., Splivallo, R., Karlovsky, P. and Schaffrath, U. 2015. Abscisic acid negatively interferes with basal defence of barley against Magnaporthe oryzae. BMC Plant Biol. 15:7. https://doi.org/10.1186/s12870-014-0409-x
  68. Vlot, A. C., Dempsey, D. A. and Klessig, D. F. 2009. Salicylic Acid, a multifaceted hormone to combat disease. Annu. Rev. Phytopathol. 47:177-206. https://doi.org/10.1146/annurev.phyto.050908.135202
  69. Wang, C., Liu, Y., Li, S. S. and Han, G. Z. 2015a. Insights into the origin and evolution of the plant hormone signaling machinery. Plant Physiol. 167:872-886. https://doi.org/10.1104/pp.114.247403
  70. Wang, J., Chen, S.-H., Huang, Y.-F. and Sun, S. 2006. Induced resistance to anthracnose of Camelia oleifera by salicylic acid. For. Res. 19:629-632. https://doi.org/10.3321/j.issn:1001-1498.2006.05.017
  71. Wang, K. L.-C., Li, H. and Ecker, J. R. 2002. Ethylene biosynthesis and signaling networks. Plant Cell 14 Suppl: S131-S151. https://doi.org/10.1105/tpc.001768
  72. Wang, W., Wang, X., Huang, M., Cai, J., Zhou, Q., Dai, T., Cao, W. and Jiang, D. 2018. Hydrogen peroxide and abscisic acid mediate salicylic acid-induced freezing tolerance in wheat. Front. Plant Sci. 9:1137. https://doi.org/10.3389/fpls.2018.01137
  73. Wang, Y. and Liu, J.-H. 2012. Exogenous treatment with salicylic acid attenuates occurrence of citrus canker in susceptible navel orange (Citrus sinensis Osbeck). J. Plant Physiol. 169:1143-1149. https://doi.org/10.1016/j.jplph.2012.03.018
  74. Wang, Z., Jia, C., Li, J., Huang, S., Xu, B. and Jin, Z. 2015b. Activation of salicylic acid metabolism and signal transduction can enhance resistance to Fusarium wilt in banana (Musa acuminata L. AAA group, cv. Cavendish). Funct. Integr. Genomics 15:47-62. https://doi.org/10.1007/s10142-014-0402-3
  75. Wasternack, C. and Song, S. 2017. Jasmonates: biosynthesis, metabolism, and signaling by proteins activating and repressing transcription. J. Exp. Bot. 68:1303-1321.
  76. Went, F. W. and Thimann, K. V. 1937. Phytohormones. Macmillan, New York, NY, USA. 294 pp.
  77. Wu, J., Kim, S. G., Kang, K. Y., Kim, J.-G., Park, S.-R., Gupta, R., Kim, Y. H., Wang, Y. and Kim, S. T. 2016. Overexpression of a pathogenesis-related protein 10 enhances biotic and abiotic stress tolerance in rice. Plant Pathol. J. 32:552-562. https://doi.org/10.5423/PPJ.OA.06.2016.0141
  78. Wu, W., Ding, Y., Wei, W., Davis, R. E., Lee, I.-M., Hammond, R. W. and Zhao, Y. 2012. Salicylic acid-mediated elicitation of tomato defence against infection by potato purple top phytoplasma. Ann. Appl. Biol. 161:36-45. https://doi.org/10.1111/j.1744-7348.2012.00550.x
  79. Xie, Z., Zhang, Z.-L., Hanzlik, S., Cook, E. and Shen, Q. J. 2007. Salicylic acid inhibits gibberellin-induced alpha-amylase expression and seed germination via a pathway involving an abscisic-acid-inducible WRKY gene. Plant Mol. Biol. 64:293-303. https://doi.org/10.1007/s11103-007-9152-0
  80. Xiong, L. and Zhu, J.-K. 2003. Regulation of abscisic acid biosynthesis. Plant Physiol. 133:29-36. https://doi.org/10.1104/pp.103.025395
  81. Yan, S. and Dong, X. 2014. Perception of the plant immune signal salicylic acid. Curr. Opin. Plant Biol. 20:64-68. https://doi.org/10.1016/j.pbi.2014.04.006
  82. Yildirim, E., Ekinci, M., Turan, M., Dursun, A., Kul, R. and Parlakova, F. 2015. Roles of glycine betaine in mitigating deleterious effect of salt stress on lettuce (Lactuca sativa L.). Arch. Agron. Soil Sci. 61:1673-1689. https://doi.org/10.1080/03650340.2015.1030611
  83. Yildirim, E., Turan, M. and Guvenc, I. 2008. Effect of foliar salicylic acid applications on growth, chlorophyll, and mineral content of cucumber grown under salt stress. J. Plant Nutr. 31:593-612. https://doi.org/10.1080/01904160801895118
  84. Yousif, D. Y. M. 2018. Effects sprayed solution of salicylic acid to prevent of wilt disease caused by Fussarium oxysporium. J. Phys. Conf. Ser. 1003:012001. https://doi.org/10.1088/1742-6596/1003/1/012001
  85. Zhang, Y. and Li, X. 2019. Salicylic acid: biosynthesis, perception, and contributions to plant immunity. Curr. Opin. Plant Biol. 50:29-36. https://doi.org/10.1016/j.pbi.2019.02.004