Chitosan and its derivatives as promising plant protection tools

In modern conditions, the increase in the yield of agricultural crops is provided not by expanding the areas of their cultivation, but mainly by introducing advanced technologies. The most effective strategy for this purpose is the development of genetically resistant and productive cultivars in combination with the use of a variety of plant protection products (PPPs). However, traditional, chemical PPPs, despite their effectiveness, have significant drawbacks, namely, pollution of environment, ecological damage, toxicity to humans. Recently, biological PPPs based on natural compounds have attracted more attention, since they do not have these disadvantages, but at the same time they can be no less effective. One of such agents is chitosan, a deacetylation product of chitin, one of the most common polysaccharides in nature. The high biological activity, biocompatibility, and safety of chitosan determine the breadth and effectiveness of its use in medicine, industry, and agrobiology. The review considers various mechanisms of action of chitosan as a biopesticide, including both a direct inhibitory effect on pathogens and the induction of plant internal defense systems as a result of chitosan binding to cell surface receptors. The effect of chitosan on the formation of resistance to the main classes of pathogens: fungi, bacteria, and viruses has been shown on a variety of plant objects. The review also discusses various ways of using chitosan: for the treatment of seeds, leaves, fruits, soil, as well as its specific biological effects corresponding to these ways. A separate chapter is devoted to protection products based on chitosan, obtained by its chemical modifications, or by means of combining of a certain molecular forms of chitosan with various substances that enhance its antipathogenic effect. The data presented in the review generally give an idea of chitosan and its derivatives as very effective and promising plant protection products and biostimulants.

1. Abd El-Kareem F., Haggag W. Chitosan and citral alone or in combination for controlling early blight disease of potato plants under field conditions. Res. J. Pharm. Biol. Chem. Sci. 2014;5(6):941-949

2. Abd El-Gawad H., Bondok A. Response of tomato plants to salicylic acid and chitosan under infection with tomato mosaic virus. Am. Eur. J. Agric. Environ. Sci. 2015;15(8):1520-1529. DOI 10.5829/idosi.aejaes.2015.15.8.12735

3. Algam S., Xie G., Li B., Yu S., Su T., Larsen J. Effects of Paenibacillus strains and chitosan on plant growth promotion and control of Ralstonia wilt in tomato. J. Plant Pathol. 2010;92(3):593-600. DOI 10.4454/JPP.V92I3.303

4. Amini J. Induced resistance in potato plants against verticillium wilt invoked by chitosan and Acibenzolar-S-methyl. Aust. J. Crop Sci. 2015;9(6):570-576

5. Appert C., Logemann E., Hahlbrock K., Schmid J., Amrhein N. Structural and catalytic properties of the four phenylalanine ammonia­lyase isoenzymes from parsley (Petroselinum crispum Nym.). Eur. J. Biochem. 1994;225(1):491-499. DOI 10.1111/j.1432-1033.1994.00491.x

6. Badanova E.G., Davletbaev I.M., Sirotkin A.S. Preparations based on chitosan for agriculture. Vestnik Tekhnologicheskogo Universi te ta = Herald of Technological University. 2016;19(16):89-95 (in Russian)

7. Badawy M.E., Rabea E.I. A biopolymer chitosan and its derivatives as promising antimicrobial agents against plant pathogens and their applications in crop protection. Int. J. Carbohydr. Chem. 2011;2011: 460381. DOI 10.1155/2011/460381

8. Badawy M.E., Rabea E.I., Taktak N.E. Antimicrobial and inhibitory enzyme activity of N-(benzyl) and quaternary N-(benzyl) chitosan derivatives on plant pathogens. Carbohydr. Polym. 2014;111:670-682. DOI 10.1016/j.carbpol.2014.04.098

9. Bautista-Baños S., Hernández-López M., Bosquez-Molina E., Wilson C. Effects of chitosan and plant extracts on growth of Colletot richum gloeosporioides, anthracnose levels and quality of papaya fruit. Crop Prot. 2003;22(9):1087-1092. DOI 10.1016/S0261-2194(03)00117-0

10. Bayrambekov B., Polyakova E.V., Mukatova M.D., Kirichko N.A. Biostimulator on the basis of low-molecular chitosan from the crayfish crust for preplant processing of tomato seeds. Vestnik Astrakhanskogo Gosudarstvennogo Tekhnicheskogo Universiteta. Seriya: Ryb noe Khozyaystvo = Vestnik of Astrakhan State Technical University. Series: Fishing Industry. 2012;1:181-184 (in Russian)

11. Bell A.A., Hubbard J.C., Liu L., Davis R.M., Subbarao K.V. Effects of chitin and chitosan on the incidence and severity of Fusarium yellows of celery. Plant Dis. 1998;82(3):322-328. DOI 10.1094/ PDIS.1998.82.3.322

12. Benhamou N., Lafontaine P., Nicole M. Induction of systemic resistance to Fusarium crown and root rot in tomato plants by seed treatment with chitosan. Phytopathology. 1994;84(12):1432-1444. DOI 10.1094/Phyto-84-1432.

13. Benhamou N., Bélanger R.R., Rey P., Tirilly Y. Oligandrin, the elicitinlike protein produced by the mycoparasite Pythium oligandrum, induces systemic resistance to Fusarium crown and root rot in tomato plants. Plant Physiol. Biochem. 2001;39(7-8):681-696. DOI 10.1016/S0981-9428(01)01283-9

14. Bhaskara Reddy M., Arul J., Angers P., Couture L. Chitosan treatment of wheat seeds induces resistance to Fusarium graminearum and improves seed quality. J. Agric. Food Chem. 1999;47(3):1208-1216. DOI 10.1021/jf981225k

15. Chen J., Zou X., Liu Q., Wang F., Feng W., Wan N. Combination effect of chitosan and methyl jasmonate on controlling Alternaria alternata and enhancing activity of cherry tomato fruit defense mechanisms. Crop Prot. 2014;56:31-36. DOI 10.1016/j.cropro.2013.10.007

16. Chen J., Edgar K.J., Frazier C.E. Photo-curable, double-crosslinked, in situ-forming hydrogels based on oxidized hydroxypropyl cellulose. Cellulose. 2021;28(7):3903-3915. DOI 10.1007/s10570-021-03788-9 Chirkov S. The antiviral activity of chitosan. Appl. Biochem. Micro biol. 2002;38(1):1-8. DOI 10.1023/A:1013206517442

17. Conrath U., Domard A., Kauss H. Chitosan-elicited synthesis of callose and of coumarin derivatives in parsley cell suspension cultures.

18. Plant Cell Rep. 1989;8(3):152-155. DOI 10.1007/BF00716829

19. Davydova V.N., Nagorskaya V.P., Gorbach V.I., Kalitnik A.A., Reunov A.V., Solov’eva T.F., Ermak I.M. Chitosan antiviral activity: dependence on structure and depolymerization method. Appl. Biochem. Microbiol. 2011;47(1):103-108. DOI 10.1134/S00036838110 10042

20. De Vega D., Holden N., Hedley P.E., Morris J., Luna E., Newton A. Chitosan primes plant defence mechanisms against Botrytis cinerea, including expression of Avr9/Cf-9 rapidly elicited genes. Plant Cell Environ. 2021;44(1):290-303. DOI 10.1111/pce.13921

21. Dobrokhotov S.A. Narcissus in greenhouses against root-knot ne matodes. Zashchita i Karantin Rasteniy = Plant Protection and Quarantine. 2000;4:21 (in Russian)

22. Dodgson J.L.A., Dodgson W. Comparison of effects of chitin and chitosan for control of Colletotrichum sp. оn cucumbers. J. Pure Appl. Microbiol. 2017;11(1):87-93. DOI 10.22207/JPAM.11.1.12

23. Eikemo H., Stensvand A., Tronsmo A. Induced resistance as a possible means to control diseases of strawberry caused by Phytophthor a spp. Plant Dis. 2003;87(4):345-350. DOI 10.1094/PDIS.2003.87.4.345

24. El-Sayed S., Mahdy M. Effect of chitosan on root-knot nematode, Meloidogyne javanica on tomato plants. Int. J. Chem. Tech. Res. 2015; 7(4):1985-1992

25. Elsharkawy M.M., Omara R.I., Mostafa Y.S., Alamri S.A., Hashem M., Alrumman S.A., Ahmad A.A. Mechanism of wheat leaf rust control using chitosan nanoparticles and salicylic acid. J. Fungi (Basel). 2022;8(3):304. DOI 10.3390/jof8030304

26. Falcón-Rodríguez A.B., Wégria G., Cabrera J.-C. Exploiting plant innate immunity to protect crops against biotic stress: chitosaccharides as natural and suitable candidates for this purpose. In: Ban dani A.R. (Ed.). New Perspectives in Plant Protection. InTech, 2012; 139-166. DOI 10.5772/36777

27. Faoro F., Maffi D., Cantu D., Iriti M. Chemical-induced resistance against powdery mildew in barley: the effects of chitosan and benzothiadiazole. BioControl. 2008;53(2):387-401. DOI 10.1007/s10526-007-9091-3

28. Fei Liu X., Lin Guan Y., Zhi Yang D., Li Z., De Yao K. Antibacterial action of chitosan and carboxymethylated chitosan. J. Appl. Polym. Sci. 2001;79(7):1324-1335. DOI 10.1002/1097-4628(20010214)79: 7<1324::AID-APP210>3.0.CO;2-L

29. Gaffney T., Friedrich L., Vernooij B., Negrotto D., Nye G., Uknes S., Ward E., Kessmann H., Ryals J. Requirement of salicylic acid for the induction of systemic acquired resistance. Science. 1993;261(5122): 754-756. DOI 10.1126/science.261.5122.754

30. Garibova L.V., Sidorova I.I. Mushrooms. Moscow: Prosveshche niye Publ., 1997 (in Russian)

31. Ghauoth A., Arul J., Grenier J., Benhamou N., Asselin A., Belanger G. Effect of chitosan on cucumber plants: suppression of Pythium aphanidermatum and induction of defense reaction. Phytopathology. 1994;84(3):313-320. DOI 10.1094/PHYTO-84-313

32. Ghaouth A.El., Arul J., Wilson C., Benhamou N. Biochemical and cytochemical aspects of the interactions of chitosan and Botrytis cinerea in bell pepper fruit. Postharvest Biol. Technol. 1997;12(2):183-194. DOI 10.1016/S0925-5214(97)00056-2

33. Gol’din E.B. The biological plant protection in the light of problems of XXI century. Geopolitika i Ekogeodinamika Regionov = Geopolitics and Ecogeodynamics of Regions. 2014;10(2):99-107 (in Russian)

34. Grant J.J., Loake G.J. Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiol. 2000; 124(1):21-29. DOI 10.1104/pp.124.1.21

35. El Hadrami A., Adam L.R., El Hadrami I., Daayf F. Chitosan in plant protection. Mar. Drugs. 2010;8(4):968-987. DOI 10.3390/ md8040968

36. Hadwiger L.A. Multiple effects of chitosan on plant systems: solid science or hype. Plant Sci. 2013;208:42-49. DOI 10.1016/j.plantsci.2013.03.007

37. Hassni M., El Hadrami A., El Hadrami I., Barka E.A., Daayf F.F. Chitosan, antifungal product against Fusarium oxysporum f. sp. albedinis and elicitor of defence reactions in date palm roots. Phytopathol. Mediterr. 2004;43(2):195-204. DOI 10.14601/Phytopathol_Mediterr-1743

38. Helander I.M., Nurmiaho-Lassila E.-L., Ahvenainen R., Rhoades J., Roller S. Chitosan disrupts the barrier properties of the outer membrane of Gram-negative bacteria. Int. J. Food Microbiol. 2001; 71(2-3):235-244. DOI 10.1016/s0168-1605(01)00609-2

39. Hirano S., Nakahira T., Nakagawa M., Kim S.K. The preparation and applications of functional fibres from crab shell chitin. J. Biotechnol. 1999;70(1-3):373-377. DOI 10.1016/S0168-1656(99)00090-5

40. Igbedioh S. Effects of agricultural pesticides on humans, animals, and higher plants in developing countries. Arch. Environ. Health. 1991; 46(4):218-224. DOI 10.1080/00039896.1991.9937452

41. Iriti M., Varoni E.M. Chitosan-induced antiviral activity and innate immunity in plants. Environ. Sci. Pollut. Res. 2015;22(4):2935-2944. DOI 10.1007/s11356-014-3571-7

42. Iriti M., Sironi M., Gomarasca S., Casazza A., Soave C., Faoro F. Cell death-mediated antiviral effect of chitosan in tobacco. Plant Physiol. Biochem. 2006;44(11-12):893-900. DOI 10.1016/j.plaphy.2006.10.009

43. Ishiguro S., Kawai-Oda A., Ueda J., Nishida I., Okada K. The DEFECTIVE IN ANTHER DEHISCIENCE1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell. 2001;13(10):2191-2209. DOI 10.1105/tpc.010192

44. Je J.Y., Kim S.K. Chitosan derivatives killed bacteria by disrupting the outer and inner membrane. J. Agric. Food Chem. 2006;54(18): 6629-6633. DOI 10.1021/jf061310p

45. Jiang X., Lin H., Lin M., Chen Y., Wang H., Lin Y., Shi J., Lin Y. A novel chitosan formulation treatment induces disease resistance of harvested litchi fruit to Peronophythora litchii in association with ROS metabolism. Food Chem. 2018;266:299-308. DOI 10.1016/ j.foodchem.2018.06.010

46. Karimi K., Zamani A. Mucor indicus: biology and industrial application perspectives: a review. Biotechnol. Adv. 2013;31(4):466-481. DOI 10.1016/j.biotechadv.2013.01.009

47. Katiyar D., Hemantaranjan A., Singh B., Bhanu A.N. A future perspective in crop protection: chitosan and its oligosaccharides. Adv. Plants Agric. Res. 2014;1(1):23-30. DOI 10.15406/APAR.2014.01.00006

48. Khalil M.S., Badawy M.E. Nematicidal activity of a biopolymer chitosan at different molecular weights against root-knot nematode, Meloidogyne incognita. Plant Prot. Sci. 2012;48(4):170-178. DOI 10.17221/46/2011-PPS

49. Kheiri A., Moosawi Jorf S.A., Malihipour A., Saremi H., Nikkhah M. Application of chitosan and chitosan nanoparticles for the control of Fusarium head blight of wheat (Fusarium graminearum) in vitro and greenhouse. Int. J. Biol. Macromol. 2016;93(Pt. A):1261-1272. DOI 10.1016/j.ijbiomac.2016.09.072

50. Kim K.D., Nemec S., Musson G. Control of phytophthora root and crown rot of bell pepper with composts and soil amendments in the greenhouse. Appl. Soil Ecol. 1997;5(2):169-179. DOI 10.1016/ S0929-1393(96)00138-2

51. Kirillova O.S. Semiochemical interactions and induced defense responses in cucumber plants damaged by phytophages. Сand. Sci. (Biol.) Dissertation. St. Petersburg; Pushkin, 2015 (in Russian)

52. Köhle H., Jeblick W., Poten F., Blaschek W., Kauss H. Chitosan-elicited callose synthesis in soybean cells as a Ca2+-dependent process. Plant Physiol. 1985;77(3):544-551. DOI 10.1104/pp.77.3.544.

53. Kong M., Chen X.G., Xing K., Park H.J. Antimicrobial properties of chitosan and mode of action: a state of the art review. Int. J. Food Microbiol. 2010;144(1):51-63. DOI 10.1016/j.ijfoodmicro.2010.09.012

54. Krivtsov G.G., Loskutova N.A., Konyukhova N.S., Khor’kov E.I., Kononenko N.V., Vanyushin B.F. Effect of chitosan elicitors on wheat plants. Biol. Bull. 1996;23(1):16-21

55. Kulikov S., Chirkov S., Il’ina A., Lopatin S., Varlamov V. Effect of the molecular weight of chitosan on its antiviral activity in plants. Appl. Biochem. Microbiol. 2006;42(2):200-203. DOI 10.1134/S0003683806020165

56. Kumaraswamy R.V., Kumari S., Choudhary R.C., Pal A., Raliya R., Biswas P., Saharan V. Engineered chitosan based nanomaterials: bioactivities, mechanisms and perspectives in plant protection and growth. Int. J. Biol. Macromol. 2018;113:494-506. DOI 10.1016/j.ijbiomac.2018.02.130

57. Lee S., Choi H., Suh S., Doo I.-S., Oh K.-Y., Choi E.J., Schroeder Taylor A.T., Low P.S., Lee Y. Oligogalacturonic acid and chitosan reduce stomatal aperture by inducing the evolution of reactive oxygen species from guard cells of tomato and Commelina communis. Plant Physiol. 1999;121(1):147-152. DOI 10.1104/pp.121.1.147

58. Li B., Wang X., Chen R., Huangfu W., Xie G. Antibacterial activity of chitosan solution against Xanthomonas pathogenic bacteria isolated from Euphorbia pulcherrima. Carbohydr. Polym. 2008;72(2):287-292. DOI 10.3390/molecules17067028

59. Li B., Liu B., Shan C., Ibrahim M., Lou Y., Wang Y., Xie G., Li H.Y., Sun G. Antibacterial activity of two chitosan solutions and their effect on rice bacterial leaf blight and leaf streak. Pest Manag. Sci. 2013a;69(2):312-320. DOI 10.1002/ps.3399

60. Li B., Shi Y., Shan C., Zhou Q., Ibrahim M., Wang Y., Wu G., Li H., Xie G., Sun G. Effect of chitosan solution on the inhibition of Acidovorax citrulli causing bacterial fruit blotch of watermelon. J. Sci. Food Agric. 2013b;93(5):1010-1015. DOI 10.1002/jsfa.5812

61. Li H., Yu T. Effect of chitosan on incidence of brown rot, quality and physiological attributes of postharvest peach fruit. J. Sci. Food Agric. 2001;81(2):269-274. DOI 10.1002/1097-0010(20010115)81: 2<269::AID-JSFA806>3.0.CO;2-F

62. Liu J., Tian S., Meng X., Xu Y. Effects of chitosan on control of postharvest diseases and physiological responses of tomato fruit. Postharvest Biol. Technol. 2007;44(3):300-306. DOI 10.1016/j.postharv bio.2006.12.019

63. Lou M.-M., Zhu B., Muhammad I., Li B., Xie G.-L., Wang Y.-L., Li H.Y., Sun G.C. Antibacterial activity and mechanism of action of chitosan solutions against apricot fruit rot pathogen Burkholderia seminalis. Carbohydr. Res. 2011;346(11):1294-1301. DOI 10.1016/j.carres.2011.04.042

64. Ma Z., Yang L., Yan H., Kennedy J.F., Meng X. Chitosan and oligochitosan enhance the resistance of peach fruit to brown rot. Carbohydr. Polym. 2013;94(1):272-277. DOI 10.1016/j.carbpol.2013.01.012 Malerba M., Cerana R. Chitosan effects on plant systems. Int. J. Mol. Sci. 2016;17(7):996. DOI 10.3390/ijms17070996

65. Manjunatha G., Roopa K., Prashanth G.N., Shetty H. Chitosan enhances disease resistance in pearl millet against downy mildew caused by Sclerospora graminicola and defence-related enzyme activation. Pest Manag. Sci. 2008;64(12):1250-1257. DOI 10.1002/ps.1626

66. Manjunatha G., Niranjan-Raj S., Prashanth G.N., Deepak S., Amruthesh K.N., Shetty H.S. Nitric oxide is involved in chitosan-induced systemic resistance in pearl millet against downy mildew disease. Pest Manag. Sci. 2009;65(7):737-743. DOI 10.1002/ps.1710

67. Mansilla A.Y., Albertengo L., Rodríguez M.S., Debbaudt A., Zúñiga A., Casalongué C.A. Evidence on antimicrobial properties and mode of action of a chitosan obtained from crustacean exoskeletons on pseudomonas Syringae pv. tomato DC3000. Appl. Microbiol. Biotechnol. 2013;97(15):6957-6966. DOI 10.1007/s00253-013-4993-8

68. Meng X., Yang L., Kennedy J.F., Tian S. Effects of chitosan and oligochitosan on growth of two fungal pathogens and physiological properties in pear fruit. Carbohydr. Polym. 2010;81(1):70-75. DOI 10.1016/j.carbpol.2010.01.057

69. Morin-Crini N., Lichtfouse E., Torri G., Crini G. Applications of chitosan in food, pharmaceuticals, medicine, cosmetics, agriculture, textiles, pulp and paper, biotechnology, and environmental chemistry. Environ. Chem. Lett. 2019;17:1667-1692. DOI 10.1007/s10311-019-00904-x

70. Mulawarman, Hallmann J., Bell D., Kopp-Holtwiesche B., Sikora R. Effects of natural products on soil organisms and plant health enhancement. Meded. Rijksuniv. Gent. Fak. Landbouwkd. Toegep. Biol. Wet. 2001;66(2b):609-617

71. Muzzarelli R.A. Chitins and chitosans as immunoadjuvants and nonallergenic drug carriers. Mar. Drugs. 2010;8(2):292-312. DOI 10.3390/md8020292

72. Nagorskaya V., Reunov A., Lapshina L., Davydova V., Yermak I. Effect of chitosan on tobacco mosaic virus (TMV) accumulation, hydrolase activity, and morphological abnormalities of the viral particles in leaves of N. tabacum L. cv. Samsun. Virol. Sin. 2014;29(4):250256. DOI 10.1007/s12250-014-3452-8

73. Nandeeshkumar P., Sudisha J., Ramachandra K.K., Prakash H., Niranjana S., Shekar S.H. Chitosan induced resistance to downy mildew in sunflower caused by Plasmopara halstedii. Physiol. Mol. Plant Pathol. 2008;72(4-6):188-194. DOI 10.1016/j.pmpp.2008.09.001.

74. No H.K., Park N.Y., Lee S.H., Meyers S.P. Antibacterial activity of chitosans and chitosan oligomers with different molecular weights. Int. J. Food Microbiol. 2002;74(1-2):65-72. DOI 10.1016/S01681605(01)00717-6

75. Orzali L., Forni C., Riccioni L. Effect of chitosan seed treatment as elicitor of resistance to Fusarium graminearum in wheat. Seed Sci. Technol. 2014;42(2):132-149. DOI 10.15258/sst.2014.42.2.03

76. Orzali L., Corsi B., Forni C., Riccioni L. Chitosan in Agriculture: A New Challenge for Managing Plant Disease. In: Shalaby E.A. (Ed.). Biological Activities and Application of Marine Polysaccharides. InTech, 2017;87-96. DOI 10.5772/66840

77. Palma-Guerrero J., Huang I.-C., Jansson H.-B., Salinas J., LopezLlorca L., Read N. Chitosan permeabilizes the plasma membrane and kills cells of Neurospora crassa in an energy dependent manner. Fungal Genet. Biol. 2009;46(8):585-594. DOI 10.1016/j.fgb.2009. 02.010

78. Park K.-C., Chang T.-H. Effect of chitosan on microbial community in soils planted with cucumber under protected cultivation. Hort. Sci. Technol. 2012;30(3):261-269. DOI 10.7235/hort.2012.11148

79. Peña-Cortes H., Sanchez-Serrano J., Rocha-Sosa M., Willmitzer L. Systemic induction of proteinase-inhibitor-II gene expression in potato plants by wounding. Planta. 1988;174(1):84-89. DOI 10.1007/BF00394877

80. Photchanachai S., Singkaew J., Thamthong J. Effects of chitosan seed treatment on Colletotrichum sp. and seedling growth of chili cv. Jinda. In: IV International Conference on Managing Quality in ChainsThe Integrated View on Fruits and Vegetables Quality. Bangkok, 2006;712:585-590. DOI 10.17660/ActaHortic.2006.712.70

81. Popova E.V., Domnina N.S., Kovalenko N.M., Sokornova S.V., Tyuterev S.L. Influence of chitosan hybrid derivatives on induced wheat resistance to pathogens with different nutrition strategies. Applied Biochemistry and Microbiology. 2018;54(5):535-539. DOI 10.1134/S0003683818050150

82. Qing W., Zuo J.-H., Qian W., Yang N., Gao L.-P. Inhibitory effect of chitosan on growth of the fungal phytopathogen, Sclerotinia sclerotiorum, and sclerotinia rot of carrot. J. Integr. Agric. 2015;14(4): 691-697. DOI 10.1016/S2095-3119(14)60800-5

83. Rabea E.I., Badawy M.E.-T., Stevens C.V., Smagghe G., Steurbaut W. Chitosan as antimicrobial agent: applications and mode of action. Biomacromolecules. 2003;4(6):1457-1465. DOI 10.1021/bm034130m

84. Rabea E.I., Badawy M.E., Rogge T.M., Stevens C.V., Höfte M., Steurbaut W., Smagghe G. Insecticidal and fungicidal activity of new synthesized chitosan derivatives. Pest Manag. Sci. 2005;61(10): 951-960. DOI 10.1002/ps.1085

85. Rabea E.I., Steurbaut W. Chemically modified chitosans as antimicrobial agents against some plant pathogenic bacteria and fungi. Plant Prot. Sci. 2010;46(4):149-158. DOI 10.17221/9/2009-PPS

86. Ramos-García M., Bosquez-Molina E., Hernández-Romano J., Zavala-Padilla G., Terrés-Rojas E., Alia-Tejacal I., Barrera-Necha L., Hernández-López M., Bautista-Baños S. Use of chitosan-based edible coatings in combination with other natural compounds, to control Rhizopus stolonifer and Escherichia coli DH5α in fresh tomatoes. Crop Prot. 2012;38:1-6. DOI 10.1016/j.cropro.2012.02.016

87. Reglinski T., Elmer P., Taylor J., Wood P., Hoyte S. Inhibition of Botrytis cinerea growth and suppression of botrytis bunch rot in grapes using chitosan. Plant Pathol. 2010;59(5):882-890. DOI 10.1111/j.1365-3059.2010.02312.x

88. Reinbothe C., Springer A., Samol I., Reinbothe S. Plant oxylipins: role of jasmonic acid during programmed cell death, defence and leaf senescence. FEBS J. 2009;276(17):4666-4681. DOI 10.1111/j.1742-4658.2009.07193.x

89. Rinaudo M. Chitin and chitosan: properties and applications. Prog. Polym. Sci. 2006;31(7):603-632. DOI 10.1016/j.progpolymsci.2006.06.001

90. Romanazzi G., Nigro F., Ippolito A. Short hypobaric treatments potentiate the effect of chitosan in reduction storage decay of sweet cherries. Postharvest Biol. Technol. 2003;29(1):73-80. DOI 10.1016/S0925-5214(02)00239-9

91. Rouphael Y., Colla G. Editorial: Biostimulants in Agriculture. Front. Plant Sci. 2020;11:40. DOI 10.3389/fpls.2020.00040

92. Saberi Riseh R., Skorik Y.A., Thakur V.K., Moradi Pour M., Tamanadar E., Shahidi Noghabi S. Encapsulation of plant biocontrol bacteria with alginate as a main polymer material. Int. J. Mol. Sci. 2021; 22(20):11165. DOI 10.3390/ijms222011165

93. Sathiyabama M., Bernstein N., Anusuya S. Chitosan elicitation for increased curcumin production and stimulation of defence response in turmeric (Curcuma longa L.). Ind. Crop. Prod. 2016;89:87-94. DOI 10.1016/j.indcrop.2016.05.007

94. Sembdner G., Parthier B. The biochemistry and the physiological and molecular actions of jasmonates. Annu. Rev. Plant Biol. 1993; 44(1):569-589. DOI 10.1146/annurev.pp.44.060193.003033

95. Sharathchandra R., Raj S.N., Shetty N., Amruthesh K., Shetty H.S. A chitosan formulation Elexa™ induces downy mildew disease resistance and growth promotion in pearl millet. Crop Prot. 2004; 23(10):881-888. DOI 10.1016/j.cropro.2003.12.008

96. Singh R.P., Hodson D.P., Huerta-Espino J., Jin Y., Bhavani S., Njau P., Herrera-Foessel S., Singh P.K., Singh S., Govindan V. The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. Annu. Rev. Phytopathol. 2011;49:465-481. DOI 10.1146/annurev-phyto-072910-095423

97. Skryabin K.G., Vikhoreva G.A., Varlamov V.P. Chitin and Chitosan: Obtaining, Properties and Application. Moscow: Nauka Publ., 2002 (in Russian)

98. Stanley-Raja V., Senthil-Nathan S., Chanthini K.M.-P., Sivanesh H., Ramasubramanian R., Karthi S., Shyam-Sundar N., Vasantha-Srinivasan P., Kalaivani K. Biological activity of chitosan inducing resistance efficiency of rice (Oryza sativa L.) after treatment with fungal based chitosan. Sci. Rep. 2021;11(1):20488. DOI 10.1038/s41598-021-99391-w

99. Su X., Zivanovic S., D’Souza D.H. Effect of chitosan on the infectivity of murine norovirus, feline calicivirus, and bacteriophage MS2. J. Food Prot. 2009;72(12):2623-2628. DOI 10.4315/0362-028x-72.12.2623

100. Suarez-Fernandez M., Marhuenda-Egea F.C., Lopez-Moya F.F., Arnao M.B., Cabrera-Escribano F., Nueda M.J., Gunsé B., LopezLlorca L.V. Chitosan induces plant hormones and defenses in tomato root exudates. Front. Plant Sci. 2020;11:572087. DOI 10.3389/fpls.2020.572087

101. Tang D., Kang R., Coyne C.B., Zeh H.J., Lotze M.T. PAMPs and DAMPs: signal 0s that spur autophagy and immunity. Immunol. Rev. 2012;249(1):158-175. DOI 10.1111/j.1600-065X.2012.01146

102. Tayel A.A., Moussa S., Opwis K., Knittel D., Schollmeyer E., Nickisch-Hartfiel A. Inhibition of microbial pathogens by fungal chitosan. Int. J. Biol. Macromol. 2010;47(1):10-14. DOI 10.1016/j.ijbiomac.2010.04.005

103. Teplyakova O.I., Fomenko V.V., Salakhutdinov N.F., Vlasenko N.G. Novochizol™ seed treatment: effects on germination, growth and development in soft spring wheat. Nat. Prod. Chem. Res. 2022;10(5): 1-4. DOI 10.35248/naturalproducts.10.5.1-04

104. Tyuterev S.L. Scientific bases of induced disease resistance of plants. St. Petersburg: VIZR Publ., 2002 (in Russian)

105. Tyuterev S.L. Natural and synthetic inducers of plant resistance to diseases. St. Petersburg: Rodnyye Prostory Publ., 2014 (in Russian)

106. Tyuterev S.L. Ecologically safe inducers of plant resistance to dis eases and physiological stresses. Vestnik Zashchity Rasteniy = Plant Protection News. 2015;1(83):3-13 (in Russian)]

107. Wang Z., Zheng L., Li C., Zhang D., Xiao Y., Guan G., Zhu W. Modification of chitosan with monomethyl fumaric acid in an ionic liquid solution. Carbohydr. Polym. 2015;117:973-979. DOI 10.1016/j.carbpol.2014.10.021

108. Wiśniewska-Wrona M., Niekraszewicz A., Ciechańska D., Pospieszny H., Orlikowski L.B. Biological properties of chitosan degradation products. Prog. Chem. Applic. Chitin Derivatives. 2007;7:149-156

109. Xing K., Zhu X., Peng X., Qin S. Chitosan antimicrobial and eliciting properties for pest control in agriculture: a review. Agron. Sustain. Dev. 2015;35(2):569-588. DOI 10.1007/s13593-014-0252-3

110. Yasmin S., D’Souza D. Effects of pesticides on the growth and reproduction of earthworm: a review. Appl. Environ. Soil Sci. 2010; 2010:678360. DOI 10.1155/2010/678360

111. Yu J., Hu N., Hou L., Hang F., Li K., Xie C. Effect of deacetylation of chitosan on the physicochemical, antioxidant and antibacterial pro perties activities of chitosan­mannose derivatives. J. Sci. Food Agric. 2023. DOI 10.1002/jsfa.12715

112. Zhang X., Li K., Xing R., Liu S., Li P. Metabolite profiling of wheat seedlings induced by chitosan: revelation of the enhanced carbon and nitrogen metabolism. Front Plant Sci. 2017;8:2017. DOI 10.3389/fpls.2017.02017

113. Zheng K., Lu J., Li J., Yu Y., Zhang J., He Z., Ismail O.M., Wu J., Xie X., Li X., Xu G., Dou D., Wang X. Efficiency of chitosan application against Phytophthora infestans and the activation of defence mechanisms in potato. Int. J. Biol. Macromol. 2021;182:1670-1680. DOI 10.1016/j.ijbiomac.2021.05.097