The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
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The Plant-Stress Metabolites, Hexanoic Aacid and Melatonin, Are Potential "Vaccines" for Plant Health Promotion

  • Anderson, Anne J. (Department of Biological Engineering, Utah State University) ;
  • Kim, Young Cheol (Department of Applied Biology, College of Agriculture & Life Sciences, Chonnam National University)
  • Received : 2021.01.28
  • Accepted : 2021.08.31
  • Published : 2021.10.01
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Abstract

A plethora of compounds stimulate protective mechanisms in plants against microbial pathogens and abiotic stresses. Some defense activators are synthetic compounds and trigger responses only in certain protective pathways, such as activation of defenses under regulation by the plant regulator, salicylic acid (SA). This review discusses the potential of naturally occurring plant metabolites as primers for defense responses in the plant. The production of the metabolites, hexanoic acid and melatonin, in plants means they are consumed when plants are eaten as foods. Both metabolites prime stronger and more rapid activation of plant defense upon subsequent stress. Because these metabolites trigger protective measures in the plant they can be considered as "vaccines" to promote plant vigor. Hexanoic acid and melatonin instigate systemic changes in plant metabolism associated with both of the major defense pathways, those regulated by SA- and jasmonic acid (JA). These two pathways are well studied because of their induction by different microbial triggers: necrosis-causing microbial pathogens induce the SA pathway whereas colonization by beneficial microbes stimulates the JA pathway. The plant's responses to the two metabolites, however, are not identical with a major difference being a characterized growth response with melatonin but not hexanoic acid. As primers for plant defense, hexanoic acid and melatonin have the potential to be successfully integrated into vaccination-like strategies to protect plants against diseases and abiotic stresses that do not involve man-made chemicals.

Keywords

Acknowledgement

This work was supported by Korea Institute of Planning and Evaluation for Technology in Food, Agriculture and Forestry (IPET) through Agricultural Machinery/Equipment Localization Technology Development Program, funded by Ministry of Agriculture, Food and Rural Affairs (MAFRA) (321055-05) and previous support from the USDA and NSF from grants to AJA.

References

  1. Agrios, G. 2005. Plant pathology. 5th ed. Academic Press, Amsterdam, The Netherlands. 953 pp.
  2. Ahammed, G. J., Wu, M., Wang, Y., Yan, Y., Mao, Q., Ren, J., Ma, R., Liu, A. and Chen, S. 2020. Melatonin alleviates iron stress by improving iron homeostasis, antioxidant defense and secondary metabolism in cucumber. Sci. Hortic. 265:109205. https://doi.org/10.1016/j.scienta.2020.109205
  3. Aranega-Bou, P., de la O. Leyva, M., Finiti, I., Garcia-Agustin, P. and Gonzalez-Bosch, C. 2014. Priming of plant resistance by natural compounds: hexanoic acid as a model. Front. Plant Sci. 5:488.
  4. Arnao, M. B. 2014. Phytomelatonin: discovery, content, and role in plants. Adv. Bot. 2014:815769.
  5. Arnao, M. B. and Hernandez-Ruiz, J. 2014. Melatonin: plant growth regulator and/or biostimulator during stress? Trends Plant Sci. 19:789-797. https://doi.org/10.1016/j.tplants.2014.07.006
  6. Arnao, M. B. and Hernandez-Ruiz, J. 2018. Melatonin in its relationship to plant hormones. Ann. Bot. 121:195-207. https://doi.org/10.1093/aob/mcx114
  7. Arnao, M. B. and Hernandez-Ruiz, J. 2019a. Melatonin: a new plant hormone and/or a plant master regulator? Trends Plant Sci. 24:38-48. https://doi.org/10.1016/j.tplants.2018.10.010
  8. Arnao, M. B. and Hernandez-Ruiz, J. 2019b. Melatonin and reactive oxygen and nitrogen species: a model for the plant redox network. Melatonin Res. 2:152-168. https://doi.org/10.32794/11250036
  9. Arnao, M. B. and Hernandez-Ruiz, J. 2020a. Is phytomelatonin a new plant hormone? Agronomy 10:95. https://doi.org/10.3390/agronomy10010095
  10. Arnao, M. B. and Hernandez-Ruiz, J. 2020b. Melatonin as a regulatory hub of plant hormone levels and action in stress situations. Plant Biol. 23:7-19.
  11. Back, K., Tan, D.-X. and Reiter, R. J. 2016. Melatonin biosynthesis in plants: multiple pathways catalyze tryptophan to melatonin in the cytoplasm or chloroplasts. J. Pineal Res. 61:426-437. https://doi.org/10.1111/jpi.12364
  12. Bektas, Y. and Eulgem, T. 2014. Synthetic plant defense elicitors. Front. Plant Sci. 5:804. https://doi.org/10.3389/fpls.2014.00804
  13. Buttar, Z. A., Wu, S. N., Arnao, M. B., Wang, C., Ullah, I. and Wang, C. 2020. Melatonin suppressed the heat stress-induced damage in wheat seedlings by modulating the antioxidant machinery. Plants 9:809. https://doi.org/10.3390/plants9070809
  14. Caarls, L., Pieterse, C. M. and Van Wees, S. C. 2015. How salicylic acid takes transcriptional control over jasmonic acid signaling. Front. Plant Sci. 6:170. https://doi.org/10.3389/fpls.2015.00170
  15. Cascales-Minana, B. and Cleal, C. J. 2014. The plant fossil record reflects just two great extinction events. Terra Nova 26:195-200. https://doi.org/10.1111/ter.12086
  16. Conrath, U. 2009. Chapter 9. Priming of induced plant defense responses. In: Advances in botanical research, ed. by L. C. V. Loon, pp. 361-395. Academic Press, Burlington, MA, USA.
  17. Conrath, U., Beckers, G. J. M., Langenbach, C. J. G. and Jaskiewicz, M. R. 2015. Priming for enhanced defense. Annu. Rev. Phytopathol. 53:97-119. https://doi.org/10.1146/annurev-phyto-080614-120132
  18. Crespo-Salvador, O., Escamilla-Aguilar, M., Lopez-Cruz, J., Lopez-Rodas, G. and Gonzalez-Bosch, C. 2018. Determination of histone epigenetic marks in Arabidopsis and tomato genes in the early response to Botrytis cinerea. Plant Cell Rep. 37:153-166. https://doi.org/10.1007/s00299-017-2218-9
  19. da Silva, A. C. R., Ferro, J. A., Reinach, F. C., Farah, C. S., Furlan, L. R., Quaggio, R. B., Monteiro-Vitorello, C. B., Van Sluys, M. A., Almeida, N. F., Alves, L. M. C., do Amaral, A. M., Bertolini, M. C., Camargo, L. E. A., Camarotte, G., Cannavan, F., Cardozo, J., Chambergo, F., Ciapina, L. P., Cicarelli, R. M. B., Coutinho, L. L., Cursino-Santos, J. R., El-Dorry, H., Faria, J. B., Ferreira, A. J. S., Ferreira, R. C. C., Ferro, M. I. T., Formighieri, E. F., Franco, M. C., Greggio, C. C., Gruber, A., Katsuyama, A. M., Kishi, L. T., Leite, R. P., Lemos, E. G. M., Lemos, M. V. F., Locali, E. C., Machado, M. A., Madeira, A. M. B. N., Martinez-Rossi, N. M., Martins, E. C., Meidanis, J., Menck, C. F. M., Miyaki, C. Y., Moon, D. H., Moreira, L. M., Novo, M. T. M., Okura, V. K., Oliveira, M. C., Oliveira, V. R., Pereira, H. A., Rossi, A., Sena, J. A. D., C. Silva, S., de Souza, R. F., Spinola, L. A. F., Takita, M. A., Tamura, R. E., Teixeira, E. C., Tezza, R. I. D., Trindade dos Santos, M., Truffi, D., Tsai, S. M., White, F. F., Setubal, J. C. and Kitajima, J. P. 2002. Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417:459-463. https://doi.org/10.1038/417459a
  20. Dai, L., Li, J., Harmens, H., Zheng, X. and Zhang, C. 2020. Melatonin enhances drought resistance by regulating leaf stomatal behaviour, root growth and catalase activity in two contrasting rapeseed (Brassica napus L.) genotypes. Plant Physiol. Biochem. 149:86-95. https://doi.org/10.1016/j.plaphy.2020.01.039
  21. Debnath, B., Islam, W., Li, M., Sun, Y., Lu, X., Mitra, S., Hussain, M., Liu, S. and Qiu, D. 2019. Melatonin mediates enhancement of stress tolerance in plants. Int. J. Mol. Sci. 20:1040. https://doi.org/10.3390/ijms20051040
  22. Ding, B. and Wang, G.-L. 2015. Chromatin versus pathogens: the function of epigenetics in plant immunity. Front. Plant Sci. 6:675. https://doi.org/10.3389/fpls.2015.00675
  23. Djami-Tchatchou, A. T., Ncube, E. N., Steenkamp, P. A. and Dubery, I. A. 2017. Similar, but different: structurally related azelaic acid and hexanoic acid trigger differential metabolomic and transcriptomic responses in tobacco cells. BMC Plant Biol. 17:227. https://doi.org/10.1186/s12870-017-1157-5
  24. Epstein, E. 1999. Silicon. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:641-664. https://doi.org/10.1146/annurev.arplant.50.1.641
  25. Fernandez-Crespo, E., Navarro, J. A., Serra-Soriano, M., Finiti, I., Garcia-Agustin, P., Pallas, V. and Gonzalez-Bosch, C. 2017. Hexanoic acid treatment prevents systemic MNSV movement in Cucumis melo plants by priming callose deposition correlating SA and OPDA accumulation. Front. Plant Sci. 8:1793. https://doi.org/10.3389/fpls.2017.01793
  26. Finiti, I., de la O. Leyva, M., Vicedo, B., Gomez-Pastor, R., Lopez-Cruz, J., Garcia-Agustin, P., Real, M. D. and GonzalezBosch, C. 2014. Hexanoic acid protects tomato plants against Botrytis cinerea by priming defence responses and reducing oxidative stress. Mol. Plant Pathol. 15:550-562. https://doi.org/10.1111/mpp.12112
  27. Gago-Zachert, S., Schuck, J., Weinholdt, C., Knoblich, M., Pantaleo, V., Grosse, I., Gursinsky, T. and Behrens, S.-E. 2019. Highly efficacious antiviral protection of plants by small interfering RNAs identified in vitro. Nucleic Acids Res. 47:9343-9357. https://doi.org/10.1093/nar/gkz678
  28. Gomez-Ariza, J., Campo, S., Rufat, M., Estopa, M., Messeguer, J., San Segundo, B. and Coca, M. 2007. Sucrose-mediated priming of plant defense responses and broad-spectrum disease resistance by overexpression of the maize pathogenesis-related PRms protein in rice plants. Mol. Plant-Microbe Interact. 20:832-842. https://doi.org/10.1094/MPMI-20-7-0832
  29. Guerriero, G., Stokes, I. and Exley, C. 2018. Is callose required for silicification in plants? Biol. Lett. 14:20180338. https://doi.org/10.1098/rsbl.2018.0338
  30. Han, W., He, P., Shao, L. and Lu, F. 2018. Metabolic interactions of a chain elongation microbiome. Appl. Environ. Microbiol. 84:e01614-18.
  31. Hardeland, R. 2016. Melatonin in plants: diversity of levels and multiplicity of functions. Front. Plant Sci. 7:198. https://doi.org/10.3389/fpls.2016.00198
  32. Hasan, M. K., Liu, C.-X., Pan, Y.-T., Ahammed, G. J., Qi, Z.- Y. and Zhou, J. 2018. Melatonin alleviates low-sulfur stress by promoting sulfur homeostasis in tomato plants. Sci. Rep. 8:10182. https://doi.org/10.1038/s41598-018-28561-0
  33. Hernandez-Ruiz, J. and Arnao, M. B. 2018. Relationship of melatonin and salicylic acid in biotic/abiotic plant stress responses. Agronomy 8:33. https://doi.org/10.3390/agronomy8040033
  34. Hu, Y., Dong, Q. and Yu, D. 2012. Arabidopsis WRKY46 coordinates with WRKY70 and WRKY53 in basal resistance against pathogen Pseudomonas syringae. Plant Sci. 185-186:288-297. https://doi.org/10.1016/j.plantsci.2011.12.003
  35. Isshiki, A., Akimitsu, K., Yamamoto, M. and Yamamoto, H. 2001. Endopolygalacturonase is essential for citrus black rot caused by Alternaria citri but not brown spot caused by Alternaria alternata. Mol. Plant-Microbe Interact. 14:749-757. https://doi.org/10.1094/MPMI.2001.14.6.749
  36. Jaskiewicz, M., Conrath, U. and Peterhansel, C. 2011. Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep. 12:50-55. https://doi.org/10.1038/embor.2010.186
  37. Kauss, H., Seehaus, K., Franke, R., Gilbert, S., Dietrich, R. A. and Kroger, N. 2003. Silica deposition by a strongly cationic proline-rich protein from systemically resistant cucumber plants. Plant J. 33:87-95. https://doi.org/10.1046/j.1365-313X.2003.01606.x
  38. Kong, H. G., Song, G. C., Sim, H.-J. and Ryu, C.-M. 2020. Achieving similar root microbiota composition in neighbouring plants through airborne signalling. ISME J. 15:397-408.
  39. Kroumova, A. B., Xie, Z. and Wagner, G. J. 1994. A pathway for the biosynthesis of straight and branched, odd- and evenlength, medium-chain fatty acids in plants. Proc. Natl. Acad. Sci. U. S. A. 91:11437-11441. https://doi.org/10.1073/pnas.91.24.11437
  40. Kuc, J. 1982. Induced immunity to plant disease. BioScience 32:854-860. https://doi.org/10.2307/1309008
  41. 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
  42. Laura, B., Silvia, P., Francesca, F., Benedetta, S. and Carla, C. 2018. Epigenetic control of defense genes following MeJAinduced priming in rice (O. sativa). J. Plant Physiol. 228:166-177. https://doi.org/10.1016/j.jplph.2018.06.007
  43. Lee, H. Y. and Back, K. 2017. Melatonin is required for H2O2-and NO-mediated defense signaling through MAPKKK3 and OXI1 in Arabidopsis thaliana. J. Pineal Res. 62:e12379. https://doi.org/10.1111/jpi.12379
  44. Lee, H. Y., Byeon, Y. and Back, K. 2014. Melatonin as a signal molecule triggering defense responses against pathogen attack in Arabidopsis and tobacco. J. Pineal Res. 57:262-268. https://doi.org/10.1111/jpi.12165
  45. Li, H., Chang, J., Zheng, J., Dong, Y., Liu, Q., Yang, X., Wei, C., Zhang, Y., Ma, J. and Zhang, X. 2017. Local melatonin application induces cold tolerance in distant organs of Citrullus lanatus L. via long distance transport. Sci. Rep. 7:40858. https://doi.org/10.1038/srep40858
  46. Li, S., Xu, Y., Bi, Y., Zhang, B., Shen, S., Jiang, T. and Zheng, X. 2019. Melatonin treatment inhibits gray mold and induces disease resistance in cherry tomato fruit during postharvest. Postharvest Biol. Technol. 157:110962. https://doi.org/10.1016/j.postharvbio.2019.110962
  47. Liang, D., Shen, Y., Ni, Z., Wang, Q., Lei, Z., Xu, N., Deng, Q., Lin, L., Wang, J., Lv, X. and Xia, H. 2018. Exogenous melatonin application delays senescence of kiwifruit leaves by regulating the antioxidant capacity and biosynthesis of flavonoids. Front. Plant Sci. 9:426. https://doi.org/10.3389/fpls.2018.00426
  48. Liu, C., Chen, L., Zhao, R., Li, R., Zhang, S., Yu, W., Sheng, J. and Shen, L. 2019. Melatonin induces disease resistance to Botrytis cinerea in tomato fruit by activating jasmonic acid signaling pathway. J. Agric. Food Chem. 67:6116-6124. https://doi.org/10.1021/acs.jafc.9b00058
  49. Llorens, E., Camanes, G., Lapena, L. and Garcia-Agustin, P. 2016. Priming by hexanoic acid induce activation of mevalonic and linolenic pathways and promotes the emission of plant volatiles. Front. Plant Sci. 7:495.
  50. Llorens, E., Fernandez-Crespo, E., Vicedo, B., Lapena, L. and Garcia-Agustin, P. 2013. Enhancement of the citrus immune system provides effective resistance against Alternaria brown spot disease. J. Plant Physiol. 170:146-154. https://doi.org/10.1016/j.jplph.2012.09.018
  51. Llorens, E., Vicedo, B., Lopez, M. M., Lapena, L., Graham, J. H. and Garcia-Agustin, P. 2015. Induced resistance in sweet orange against Xanthomonas citri subsp. citri by hexanoic acid. Crop Prot. 74:77-84. https://doi.org/10.1016/j.cropro.2015.04.008
  52. Lopez-Galiano, M. J., Ruiz-Arroyo, V. M., Fernandez-Crespo, E., Rausell, C., Real, M. D., Garcia-Agustin, P., Gonzalez-Bosch, C. and Garcia-Robles, I. 2017. Oxylipin mediated stress response of a miraculin-like protease inhibitor in hexanoic acid primed eggplant plants infested by Colorado potato beetle. J. Plant Physiol. 215:59-64. https://doi.org/10.1016/j.jplph.2017.04.013
  53. Luna, E. 2016. Using green vaccination to brighten the agronomic future. Outlooks Pest Manag. 27:136-140. https://doi.org/10.1564/v27_jun_10
  54. Luna, E., Bruce, T. J. A., Roberts, M. R., Flors, V. and Ton, J. 2012. Next-generation systemic acquired resistance. Plant Physiol. 158:844-853. https://doi.org/10.1104/pp.111.187468
  55. Martinez-Medina, A., Flors, V., Heil, M., Mauch-Mani, B., Pieterse, C. M. J., Pozo, M. J., Ton, J., van Dam, N. M. and Conrath, U. 2016. Recognizing plant defense priming. Trends Plant Sci. 21:818-822. https://doi.org/10.1016/j.tplants.2016.07.009
  56. Martinez, V., Nieves-Cordones, M., Lopez-Delacalle, M., Rodenas, R., Mestre, T. C., Garcia-Sanchez, F., Rubio, F., Nortes, P. A., Mittler, R. and Rivero, R. M. 2018. Tolerance to stress combination in tomato plants: new insights in the protective role of melatonin. Molecules 23:535. https://doi.org/10.3390/molecules23030535
  57. Mauch-Mani, B., Baccelli, I., Luna, E. and Flors, V. 2017. Defense priming: an adaptive part of induced resistance. Annu. Rev. Plant Biol. 68:485-512. https://doi.org/10.1146/annurev-arplant-042916-041132
  58. McElwain, J. C. and Punyasena, S. W. 2007. Mass extinction events and the plant fossil record. Trends Ecol. Evol. 22:548-557. https://doi.org/10.1016/j.tree.2007.09.003
  59. Moustafa-Farag, M., Almoneafy, A., Mahmoud, A., Elkelish, A., Arnao, M. B., Li, L. and Ai, S. 2019. Melatonin and its protective role against biotic stress impacts on plants. Biomolecules 10:54. https://doi.org/10.3390/biom10010054
  60. Moustafa-Farag, M., Elkelish, A., Dafea, M., Khan, M., Arnao, M. B., Abdelhamid, M. T., El-Ezz, A. A., Almoneafy, A., Mahmoud, A., Awad, M., Li, L., Wang, Y., Hasanuzzaman, M. and Ai, S. 2020. Role of melatonin in plant tolerance to soil stressors: salinity, pH and heavy metals. Molecules 25:5359. https://doi.org/10.3390/molecules25225359
  61. Niehl, A., Soininen, M., Poranen, M. M. and Heinlein, M. 2018. Synthetic biology approach for plant protection using dsRNA. Plant Biotechnol. J. 16:1679-1687. https://doi.org/10.1111/pbi.12904
  62. Osbourn, A. E. 1996. Preformed antimicrobial compounds and plant defense against fungal attack. Plant Cell 8:1821-1831. https://doi.org/10.2307/3870232
  63. Park, S.-W., Li, W., Viehhauser, A., He, B., Kim, S., Nilsson, A. K., Andersson, M. X., Kittle, J. D., Ambavaram, M. M. R., Luan, S., Esker, A. R., Tholl, D., Cimini, D., Ellerstrom, M., Coaker, G., Mitchell, T. K., Pereira, A., Dietz, K.-J. and Lawrence, C. B. 2013. Cyclophilin 20-3 relays a 12-oxo-phytodienoic acid signal during stress responsive regulation of cellular redox homeostasis. Proc. Natl. Acad. Sci. U. S. A. 110:9559-9564. https://doi.org/10.1073/pnas.1218872110
  64. Quintana-Rodriguez, E., Duran-Flores, D., Heil, M. and Camacho-Coronel, X. 2018. Damage-associated molecular patterns (DAMPs) as future plant vaccines that protect crops from pests. Sci. Hortic. 237:207-220. https://doi.org/10.1016/j.scienta.2018.03.026
  65. Ramirez-Prado, J. S., Abulfaraj, A. A., Rayapuram, N., Benhamed, M. and Hirt, H. 2018. Plant immunity: from signaling to epigenetic control of defense. Trends Plant Sci. 23:833-844. https://doi.org/10.1016/j.tplants.2018.06.004
  66. Riemann, M., Dhakarey, R., Hazman, M., Miro, B., Kohli, A. and Nick, P. 2015. Exploring jasmonates in the hormonal network of drought and salinity responses. Front. Plant Sci. 6:1077. https://doi.org/10.3389/fpls.2015.01077
  67. Ryan, C. A. and Farmer, E. E. 1991. Oligosaccharide signals in plants: a current assessment. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42:651-674. https://doi.org/10.1146/annurev.pp.42.060191.003251
  68. Scalschi, L., Vicedo, B., Camanes, G., Fernandez-Crespo, E., Lapena, L., Gonzalez-Bosch, C. and Garcia-Agustin, P. 2013. Hexanoic acid is a resistance inducer that protects tomato plants against Pseudomonas syringae by priming the jasmonic acid and salicylic acid pathways. Mol. Plant Pathol. 14:342-355. https://doi.org/10.1111/mpp.12010
  69. Sharif, R., Xie, C., Zhang, H., Arnao, M. B., Ali, M., Ali, Q., Muhammad, I., Shalmani, A., Nawaz, M. A., Chen, P. and Li, Y. 2018. Melatonin and its effects on plant systems. Molecules 23:2352. https://doi.org/10.3390/molecules23092352
  70. Sharma, A. and Zheng, B. 2019. Melatonin mediated regulation of drought stress: physiological and molecular aspects. Plants 8:190. https://doi.org/10.3390/plants8070190
  71. Shi, H., Chen, K., Wei, Y. and He, C. 2016. Fundamental issues of melatonin-mediated stress signaling in plants. Front. Plant Sci. 7:1124.
  72. Siddiqui, M. H., Alamri, S., Al-Khaishany, M. Y., Khan, M. N., Al-Amri, A., Ali, H. M., Alaraidh, I. A. and Alsahli, A. A. 2019. Exogenous melatonin counteracts NaCl-induced damage by regulating the antioxidant system, proline and carbohydrates metabolism in tomato seedlings. Int. J. Mol. Sci. 20:353. https://doi.org/10.3390/ijms20020353
  73. Simlat, M., Ptak, A., Skrzypek, E., Warchol, M., Moranska, E. and Piorkowska, E. 2018. Melatonin significantly influences seed germination and seedling growth of Stevia rebaudiana Bertoni. PeerJ 6:e5009. https://doi.org/10.7717/peerj.5009
  74. Soukup, M., Martinka, M., Bosnic, D., Caplovicova, M., Elbaum, R. and Lux, A. 2017. Formation of silica aggregates in sorghum root endodermis is predetermined by cell wall architecture and development. Ann. Bot. 120:739-753. https://doi.org/10.1093/aob/mcx060
  75. Tan, D.-X., Manchester, L. C., Esteban-Zubero, E., Zhou, Z. and Reiter, R. J. 2015. Melatonin as a potent and inducible endogenous antioxidant: synthesis and metabolism. Molecules 20:18886-188906. https://doi.org/10.3390/molecules201018886
  76. Tan, D.-X., Manchester, L. C., Liu, X., Rosales-Corral, S. A., Acuna-Castroviejo, D. and Reiter, R. J. 2013. Mitochondria and chloroplasts as the original sites of melatonin synthesis: a hypothesis related to melatonin's primary function and evolution in eukaryotes. J. Pineal Res. 54:127-138. https://doi.org/10.1111/jpi.12026
  77. Tan, D.-X. and Reiter, R. J. 2020. An evolutionary view of melatonin synthesis and metabolism related to its biological functions in plants. J. Exp. Bot. 71:4677-4689. https://doi.org/10.1093/jxb/eraa235
  78. Tauzin, A. S. and Giardina, T. 2014. Sucrose and invertases, a part of the plant defense response to the biotic stresses. Front. Plant Sci. 5:293.
  79. Tepper, C. S. and Anderson, A. J. 1990. Interactions between pectic fragments and extracellular components from the fungal pathogen, Colletotrichum lindemuthianum. Physiol. Mol. Plant Pathol. 36:147-158. https://doi.org/10.1016/0885-5765(90)90103-5
  80. Thaler, J. S., Fidantsef, A. L. and Bostock, R. M. 2002. Antagonism between jasmonate- and salicylate-mediated induced plant resistance: effects of concentration and timing of elicitation on defense-related proteins, herbivore, and pathogen performance in tomato. J. Chem. Ecol. 28:1131-1159. https://doi.org/10.1023/A:1016225515936
  81. Ton, J. and Mauch-Mani, B. 2004. Beta-amino-butyric acidinduced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. Plant J. 38:119-130. https://doi.org/10.1111/j.1365-313X.2004.02028.x
  82. Wan, J., Zhang, P., Wang, R., Sun, L., Ju, Q. and Xu, J. 2018. Comparative physiological responses and transcriptome analysis reveal the roles of melatonin and serotonin in regulating growth and metabolism in Arabidopsis. BMC Plant Biol. 18:362. https://doi.org/10.1186/s12870-018-1548-2
  83. Wang, N., Wang, L., Zhu, K., Hou, S., Chen, L., Mi, D., Gui, Y., Qi, Y., Jiang, C. and Guo, J.-H. 2019. Plant root exudates are involved in Bacillus cereus AR156 mediated biocontrol against Ralstonia solanacearum. Front. Microbiol. 10:98. https://doi.org/10.3389/fmicb.2019.00098
  84. Weeda, S., Zhang, N., Zhao, X., Ndip, G., Guo, Y., Buck, G. A., Fu, C. and Ren, S. 2014. Arabidopsis transcriptome analysis reveals key roles of melatonin in plant defense systems. PLoS ONE 9:e93462. https://doi.org/10.1371/journal.pone.0093462
  85. Wei, J., Li, D.-X., Zhang, J.-R., Shan, C., Rengel, Z., Song, Z.- B. and Chen, Q. 2018. Phytomelatonin receptor PMTR1- mediated signaling regulates stomatal closure in Arabidopsis thaliana. J. Pineal Res. 65:e12500. https://doi.org/10.1111/jpi.12500
  86. Wingler, A. 2018. Transitioning to the next phase: the role of sugar signaling throughout the plant life cycle. Plant Physiol. 176:1075-1084. https://doi.org/10.1104/pp.17.01229
  87. Yang, X. L., Xu, H., Li, D., Gao, X., Li, T. L. and Wang, R. 2018. Effect of melatonin priming on photosynthetic capacity of tomato leaves under low-temperature stress. Photosynthetica 56:884-892. https://doi.org/10.1007/s11099-017-0748-6
  88. Yin, H., Zhao, X. and Du, Y. 2010. Oligochitosan: a plant diseases vaccine-a review. Carbohydr. Polym. 82:1-8. https://doi.org/10.1016/j.carbpol.2010.03.066
  89. Zdor, R. E. and Anderson, A. J. 1992. Influence of root colonizing bacteria on the defense responses of bean. Plant Soil 140:99-107. https://doi.org/10.1007/BF00012811
  90. Zhang, N., Zhang, H.-J., Zhao, B., Sun, Q.-Q., Cao, Y.-Y., Li, R., Wu, X.-X., Weeda, S., Li, L., Ren, S., Reiter, R. J. and Guo, Y.-D. 2014. The RNA-seq approach to discriminate gene expression profiles in response to melatonin on cucumber lateral root formation. J. Pineal Res. 56:39-50. https://doi.org/10.1111/jpi.12095
  91. Zhao, D., Yu, Y., Shen, Y., Liu, Q., Zhao, Z., Sharma, R. and Reiter, R. J. 2019. Melatonin synthesis and function: evolutionary history in animals and plants. Front. Endocrinol. 10:249. https://doi.org/10.3389/fendo.2019.00249
  92. Zhao, H., Xu, L., Su, T., Jiang, Y., Hu, L. and Ma, F. 2015. Melatonin regulates carbohydrate metabolism and defenses against Pseudomonas syringae pv. tomato DC3000 infection in Arabidopsis thaliana. J. Pineal Res. 59:109-119. https://doi.org/10.1111/jpi.12245