A Review on the Physicochemical and Biological Aspects of the Chitosan Antifungal Activity in Agricultural Applications

Cristóbal Lárez  Velásquez; Luz Rojas  Avelizapa

doi:10.6000/1929-5995.2020.09.07

Authors

Cristóbal Lárez Velásquez Grupo de Polímeros, Departamento de Química, Facultad de Ciencias, Universidad de Los Andes, Mérida 5101, Venezuela
Luz Rojas Avelizapa Facultad de Ciencias Biológicas y Agropecuarias, Universidad Veracruzana, Km 1 Camino Peñuela–Amatlán, S/N. Peñuela, C.P., 94945 Veracruz, México

DOI:

https://doi.org/10.6000/1929-5995.2020.09.07

Keywords:

Action mode, Radial growth inhibition, Membrane disruption, Fungal chitosan, Development stage., Download

Abstract

The antifungal activity of the chitosan biopolymer has been extensively studied for several decades. However, the mechanisms of action associated with this process have not been fully clarified yet. To a large extent, this situation is due to the lack of systematization with which, in general terms, the subject has been approached. However, it seems to have begun to change in recent years with the appearance of several papers reviewing the accumulated knowledge on the beneficial effects shown by chitosan in agricultural applications and putting forward it in a more systematic mode. In this work, the most relevant mechanisms of action proposed for chitosan regarding its antifungal activity will be briefly presented, i.e., disruption and changes in the fungal plasma membrane, alteration of gene expression, inhibition of RNA and protein synthesis, Ca²⁺ channel blocker, to then address the main factors that influence this antifungal activity, observed mainly in studies focused on phytopathogenic species, which have been grouped into three main blocks: those related exclusively to the chitosan molecules, those associated to the fungal itself and those having to do with the environment where the processes take place. Additionally, a brief section addressing some possibilities on which future studies on this topic should focus is also included.

References

Malerba M, Cerana R. Recent Applications of Chitin- and Chitosan-Based Polymers in Plants. Polymers 2019; 11: article number 839, 9 pages. https://doi.org/10.3390/polym11050839 DOI: https://doi.org/10.3390/polym11050839

Sharp R. A review of the applications of chitin and its derivatives in agriculture to modify plant-microbial interactions and improve crop yields. Agronomy 2013; 3: 757-793. https://doi.org/10.3390/agronomy3040757 DOI: https://doi.org/10.3390/agronomy3040757

Lárez-Velásquez C, Rojas-Pirela M. Biochemical Aspects of the Chitin Fungicidal Activity in Agricultural Uses. In: Chitosan in the Preservation of Agricultural Commodities. Academic Press, Oxford 2016; p. 277-298. https://doi.org/10.1016/B978-0-12-802735-6.00010-0 DOI: https://doi.org/10.1016/B978-0-12-802735-6.00010-0

Lárez-Velásquez C, Rojas Pirela M, Chirinos A, Rojas- Avelizapa L. Nuevos retos en agricultura para lós biopolímeros de quitina y quitosano. Parte 1: Efectos beneficiosos para lós cultivos. Rev Iberoam Polímeros y Materiales 2019; 20(3): 118–136. Available from: https://dialnet.unirioja.es/servlet/articulo? codigo=6996058

Shamshina JL, Kelly A, Oldham T, Rogers RD. Agricultural uses of chitin polymers. Environmental Chemistry Letters 2020; 18: 53-60. https://doi.org/10.1007/s10311-019-00934-5 DOI: https://doi.org/10.1007/s10311-019-00934-5

Bartinicki-García S. Cell wall composition and other biochemical markers in fungal phylogeny. In: Phytochemical Phylogeny. Academic Press, London 1970; p. 81-103. Available from: https://ci.nii.ac.jp/naid/10011584674/en/

Hadwiger LA, Kendra DF, Fristensky BW, Wagoner W. Chitosan both activates genes in plants and inhibits RNA synthesis in fungi. In: Chitin in Nature and Technology. Springer, Boston 1986; p. 209-214. https://doi.org/10.1007/978-1-4613-2167-5_28 DOI: https://doi.org/10.1007/978-1-4613-2167-5_28

Leuba JL, Stossel P. Chitosan and other polyamines: antifungal activity and interaction with biological membranes. In: Chitin in nature and technology. Springer, Boston 1986; p. 215-222. https://doi.org/10.1007/978-1-4613-2167-5_29 DOI: https://doi.org/10.1007/978-1-4613-2167-5_29

Allan CR, Hadwiger LA. The fungicidal effect of chitosan on fungi of varying cell wall composition. Experimental Mycology 1979; 3(3): 285-287. https://doi.org/10.1016/S0147-5975(79)80054-7 DOI: https://doi.org/10.1016/S0147-5975(79)80054-7

Li M, Chen C, Xia X, Garba B, Shang L, Wang Y. Proteomic analysis of the inhibitory effect of chitosan on Penicillium expansum. Food Science and Technology 2020; 40(1): 250-257. https://doi.org/10.1590/fst.40418 DOI: https://doi.org/10.1590/fst.40418

Palma-Guerrero J, Jansson HB, Salinas J, Lopez-Llorca, LV. Effect of chitosan on hyphal growth and spore germination of plant pathogenic and biocontrol fungi. Journal of Applied Microbiology 2008; 104(2): 541-553. https://doi.org/10.1111/j.1365-2672.2007.03567.x DOI: https://doi.org/10.1111/j.1365-2672.2007.03567.x

Olicón-Hernández DR, Uribe-Alvarez C, Uribe-Carvajal S, Pardo JP, Guerra-Sánchez G. Response of Ustilago maydis against the stress caused by three polycationic chitin derivatives. Molecules 2017; 22(12): 1-11. https://doi.org/10.3390/molecules22121745 DOI: https://doi.org/10.3390/molecules22121745

Palma-Guerrero J, Huang IC, Jansson HB, Salinas J, Lopez-Llorca LV, Read ND. Chitosan permeabilizes the plasma membrane and kills cells of Neurospora crassa in an energy dependent manner. Fungal Genet Biol 2009; 46: 585–594. https://doi.org/10.1016/j.fgb.2009.02.010 DOI: https://doi.org/10.1016/j.fgb.2009.02.010

Palma-Guerrero J, Lopez-Jimenez JA, Pérez-Berná AJ, Huang IC, Jansson HB, Salinas J, Villalaín J, Read ND, Lopez-Llorca LV. Membrane fluidity determines sensitivity of filamentous fungi to chitosan. Mol Microbiol 2010; 75(4): 1021-1032. https://doi.org/10.1111/j.1365-2958.2009.07039.x DOI: https://doi.org/10.1111/j.1365-2958.2009.07039.x

Zakrzewska A, Boorsma A, Brul S, Hellingwerf KJ, Klis FM. Transcriptional response of Saccharomyces cerevisiae to the plasma membrane-perturbing compound chitosan. Eukaryot Cell 2005; 4: 703–715. https://doi.org/10.3390/molecules22121745 DOI: https://doi.org/10.1128/EC.4.4.703-715.2005

Gutiérrez-Martínez P, Chacón-López M, Xoca-Orozco L, Ramos-Guerrero A, Velázquez-Estrada R, Aguilera-Aguirre S. Chitosan and changes in gene expression during fruit-pathogen interaction at postharvest stage. In: Chitosan in the Preservation of Agricultural Commodities. Academic Press/Elsevier USA 2016; p. 299-311. https://doi.org/10.1016/B978-0-12-802735-6.00011-2 DOI: https://doi.org/10.1016/B978-0-12-802735-6.00011-2

Lee CG, Koo JC, Park JK. Antifungal effect of chitosan as Ca2+ channel blocker. The Plant Pathology Journal 2016; 32(3): 242-250. https://doi.org/10.5423/PPJ.OA.08.2015.0162 DOI: https://doi.org/10.5423/PPJ.OA.08.2015.0162

Kim KW, Park JK. Synergistic antimicrobial properties of active molecular chitosan with EDTA-divalent metal ion compounds. Journal of Phytopathology; 2017; 165(10): 641–651. https://doi.org/10.1111/jph.12603 DOI: https://doi.org/10.1111/jph.12603

Hajji S, Younes I, Rinaudo M, Jellouli K, Nasri M. Characterization and in vitro evaluation of cytotoxicity, antimicrobial and antioxidant activities of chitosans extracted from three different marine sources. Applied Biochemistry and Biotechnology 2015; 177(1): 18-35. https://doi.org/10.1007/s12010-015-1724-x DOI: https://doi.org/10.1007/s12010-015-1724-x

Sebastian J, Rouissi T, Brar SK. Fungal chitosan: prospects and challenges. In: Handbook of Chitin and Chitosan. Volume 1: Preparation and Properties. Chapter 14. Elsevier 2020; p. 419-452. https://doi.org/10.1016/B978-0-12-817970-3.00014-6 DOI: https://doi.org/10.1016/B978-0-12-817970-3.00014-6

RAA Muzzarelli. Chitins and Chitosans as Immuno-adjuvants and Non-Allergenic Drug Carriers. Mar Drugs 2010; 8: 292-312. https://doi.org/10.3390/md8020292 DOI: https://doi.org/10.3390/md8020292

Muzzarelli RA. Chitin nanostructures in living organisms. In: Chitin. Springer, Berlin 2011; p. 1–34. https://doi.org/10.1007/978-90-481-9684-5_1 DOI: https://doi.org/10.1007/978-90-481-9684-5_1

Darwesh OM, Sultan YY, Seif MM, Marrez DA. Bio-evaluation of crustacean and fungal nano-chitosan for applying as food ingredient. Toxicol Rep 2018; 5: 348-356. https://doi.org/10.1016/j.toxrep.2018.03.002 DOI: https://doi.org/10.1016/j.toxrep.2018.03.002

Lizardi-Mendoza J, Argüelles-Monal WM, Goycoolea-Valencia FM. Chemical Characteristics and Functional Properties of Chitosan. In. Chitosan in the Preservation of Agricultural Commodities. Academic Press, Oxford 2016; p. 3–31. https://doi.org/10.1016/B978-0-12-802735-6.00001-X DOI: https://doi.org/10.1016/B978-0-12-802735-6.00001-X

Kim YJ, Zhao Y, OH KT, Nguyen VN, Park RD. Enzymatic deacetylation of chitin by extracellular chitin deacetylase from a newly screened Mortierella sp. DY-52. J Microbiol Biotechnol 2008; 18: 759–66. Available from: https://pubmed.ncbi.nlm.nih.gov/18467873/

Zhu LF, Li JS, Mai J, Chang MW. Ultrasound-assisted synthesis of chitosan from fungal precursors for biomedical applications. Chemical Engineering Journal 2019; 357: 498-507. https://doi.org/10.1016/j.cej.2018.09.183 DOI: https://doi.org/10.1016/j.cej.2018.09.183

Delezuk JA, Cardoso MB, Domard A, Campana-Filho SP. Ultrasound-assisted deacetylation of beta-chitin: influence of processing parameters. Polymer International 2011; 60(6): 903–909. https://doi.org/10.1002/pi.3037 DOI: https://doi.org/10.1002/pi.3037

Gatto M, Ochi D, Pedroso-Yoshida CM, da Silva C. Study of chitosan with different degrees of acetylation as cardboard paper coating. Carbohydrate Polymers 2019; 210: 56–63. https://doi.org/10.1016/j.carbpol.2019.01.053 DOI: https://doi.org/10.1016/j.carbpol.2019.01.053

Younes I, Sellimi S, Rinaudo M, Jellouli K, Nasri M. Influence of acetylation degree and molecular weight of homogeneous chitosans on antibacterial and antifungal activities. Int J Food Microbiol 2014; 185: 57–63. https://doi.org/10.1016/j.ijfoodmicro.2014.04.029 DOI: https://doi.org/10.1016/j.ijfoodmicro.2014.04.029

Wang Y, Li B, Zhang X, Peng N, Mei Y, Liang Y. Low molecular weight chitosan is an effective antifungal agent against Botryosphaeria sp. and preservative agent for pear (Pyrus) fruits. Int J Biol Macromol 2017; 95: 1135-1143. https://doi.org/10.1016/j.ijbiomac.2016.10.105 DOI: https://doi.org/10.1016/j.ijbiomac.2016.10.105

Guo ZY, Xing RE, Liu S, Zhong ZM, Ji X, Wang L, Li PC. The influence of molecular weight of quaternized chitosan on antifungal activity. Carbohydrate Polymers 2008; 71: 694–697. https://doi.org/10.1016/j.carbpol.2007.06.027 DOI: https://doi.org/10.1016/j.carbpol.2007.06.027

Oliveira-Junior EN, Gueddari N, Moerschbacher BM, Franco T. Growth rate inhibition of phytopathogenic fungi by characterized chitosans. Brazilian Journal of Microbiology 2012; 43(2): 800–809. https://doi.org/10.1590/S1517-83822012000200046 DOI: https://doi.org/10.1590/S1517-83822012000200046

Lárez-Velásquez C, Sánchez J, Millán-Barrios E. Vis-cosimetric studies of chitosan nitrate and chitosan chlorhydrate in acid free NaCl aqueous solution. epolymers 2008; 014; 22 pages. https://doi.org/10.1515/epoly.2008.8.1.137 DOI: https://doi.org/10.1515/epoly.2008.8.1.137

Chung Y, Wang HL, Chen YM, Li SL. 2003. Effect of abiotic factors on the antibacterial activity of chitosan against waterborne pathogens. Bioresource Technology 2003; 88: 179–184. https://doi.org/10.1016/S0960-8524(03)00002-6 DOI: https://doi.org/10.1016/S0960-8524(03)00002-6

Al-Hetar MY, Zainal-Abidin MA, Sariah M, Wong MY. Antifungal Activity of Chitosan against Fusarium oxysporum f. sp. Cubense. J App Polym Sci 2011; 120: 2434–2439. https://doi.org/10.1002/app.33455 DOI: https://doi.org/10.1002/app.33455

Rodríguez-Pedroso AT, Plascencia-Jatomea M, Bautista-Baños S, Cortez-Rocha MO, Ramírez-Arrebato, MA. Actividad antifúngica in vitro de quitosanos sobre Bipolaris oryzae patógeno del arroz. Acta Agronómica 2016; 65(1): 98-103. https://doi.org/10.15446/acag.v65n1.48235 DOI: https://doi.org/10.15446/acag.v65n1.48235

Živković S, Stevanović M, Đurović S, Ristić D, Stošić S. Antifungal activity of chitosan against Alternaria alternata and Colletotrichum gloeosporioides. Pestic Phytomed (Belgrade) 2018; 33(3-4): 197–204. https://doi.org/10.2298/PIF1804197Z DOI: https://doi.org/10.2298/PIF1804197Z

Li XF, Feng XQ, Yang S, Wang TP, Su ZX.. Effects of molecular weight and concentration of chitosan on antifungal activity against Aspergillus niger. Iranian Polymer Journal 2008; 17: 843-852. Available from: https://www.sid.ir/ FileServer/JE/81320 081104.pdf

Wang J, Zhou W, Yuan H, Wang Y. Characterization of a novel fungal chitosanase Csn2 from Gongronella sp. JG. Carboh Res 2008; 343: 2583-2588. https://doi.org/10.1016/j.carres.2008.08.004 DOI: https://doi.org/10.1016/j.carres.2008.08.004

Gaikwad HD, Hasabnis SN, Kadam MB, Dalvi SG. Antifungal activity of oligochitosan against purple blotch pathogen (Alternaria porri (Ellis) Cif) of onion. International Journal of Chemical Studies 2019; 7(6): 2425-2429. Available from: https://www.chemijournal.com/archives/20 19/vol7issue6/PartAN/7-6-270-811.pdf

da Silva L, Bitencourt T, Saltoratto A, Seleghim M, Assis O. Antifungal activity of chitosan and its quaternized derivative in gel form and as an edible coating on cut cherry tomatoes. Journal of Agricultural Sciences (Belgrade) 2018; 63(3): 271-285. https://doi.org/10.2298/JAS1803271S DOI: https://doi.org/10.2298/JAS1803271S

Kaur P, Thakur R, Choudhary A. An In vitro Study of The Antifungal Activity of Silver/Chitosan Nanoformulations Against Important Seed Borne Pathogens. International Journal of Scientific and Technology Research 2012; 1(7): 83-86. Available from: https://www.ijstr.org/finalprint/August2012 /An-In-Vitro-Study-of-The-Antifungal-Activity-of-SilverChit osan-Nanoformulations-Against-Important-Seed-Borne-Pa thogens.pdf

Alghuthaymi MA, Abd-Elsalam KA, Shami A, Said-Galive E, Shtykova EV, Naumkin AV. Silver/Chitosan Nano-composites: Preparation and Characterization and Their Fungicidal Activity against Dairy Cattle Toxicosis Penicillium expansum. J Fungi 2020; 6: 51, 18 pages. https://doi.org/10.3390/jof6020051 DOI: https://doi.org/10.3390/jof6020051

Mujeeb RP, Muraleedaran K ,Mujeeb AV. Applications of chitosan powder with in situ synthesized nano ZnO particles as an antimicrobial agent. Int J Biol Macromol 2015; 77: 266–272. https://doi.org/10.1016/j.ijbiomac.2015.03.058 DOI: https://doi.org/10.1016/j.ijbiomac.2015.03.058

Ziani K, Fernández-Pan I, Royo M, Maté JI. Antifungal activity of films and solutions based on chitosan against typical seed fungi. Food Hydrocolloids 2009; 23(8): 2309-2314. https://doi.org/10.1016/j.foodhyd.2009.06.005 DOI: https://doi.org/10.1016/j.foodhyd.2009.06.005

Feofilova EP, Nemtsev DV, Tereshina VM, Memorskaya AS. Developmental Change of the Composition and Content of the Chitin–Glucan Complex in the Fungus Aspergillus niger. App Biochem Microbiol 2006; 42(6): 545–549. https://doi.org/10.1134/S0003683806060032 DOI: https://doi.org/10.1134/S0003683806060032

Liu J, Tian S, Meng X, Xu Y. Effects of chitosan on control of postharvest diseases and physiological responses of tomato fruit. Postharvest Biology and Technology 2007; 44(3): 300-306. https://doi.org/10.1016/j.postharvbio.2006.12.019 DOI: https://doi.org/10.1016/j.postharvbio.2006.12.019

Everett KR, Owen SG, Cutting JG. Testing efficacy of fungicides against postharvest pathogens of avocado (Persea Americana cv. Hass). New Zeland Plant Prot 2005; 58: 89–95. https://doi.org/10.30843/nzpp.2005.58.4260 DOI: https://doi.org/10.30843/nzpp.2005.58.4260

Wang QZ, Chen XG, Liu N, Wang SX, Liu CS, Meng SH, Liu CG. Protonation constants of chitosan with different molecular weight and degree of deacetylation. Carbohydr Polymers 2006; 65: 194–201. https://doi.org/10.1016/j.carbpol.2006.01.001 DOI: https://doi.org/10.1016/j.carbpol.2006.01.001

Roller S, Covill N. The antifungal properties of chitosan in laboratory media and apple juice. Int J Food Microbiol 1999; 47: 67–77. https://doi.org/10.1016/s0168-1605(99)00006-9 DOI: https://doi.org/10.1016/S0168-1605(99)00006-9

Rinaudo M, Milas M, Dung P. Characterization of chitosan. Influence of ionic strength and degree of acetylation on chain expansion. Int J Biol Macromol 1993; 15: 281-285. https://doi.org/10.1016/0141-8130(93)90027-J DOI: https://doi.org/10.1016/0141-8130(93)90027-J

Vårurm KM, Ottϕy MH, Smisrϕd O. Acid hydrolysis of chitosan. Carbohydr Polym 2001; 46: 89–98. https://doi.org/10.1016/S0144-8617(00)00288-5 DOI: https://doi.org/10.1016/S0144-8617(00)00288-5

Szymańska E, Winnicka K. Stability of Chitosan — A Challenge for Pharmaceutical and Biomedical Applications. Marine Drugs 2015; 13:1 819-1846. https://doi.org/10.3390/md13041819 DOI: https://doi.org/10.3390/md13041819

Nguyen TT, Hein S, Ng CH, Stevens WF. Molecular stability of chitosan in acid solutions stored at various conditions. J Appl Polym Sci 2008; 107: 2588–2593. https://doi.org/10.1002/app.27376 DOI: https://doi.org/10.1002/app.27376

Tsai GJ, Su WH. Antibacterial Activity of Shrimp Chitosan against Escherichia coli. J Food Protection 1999; 62(3): 239–243. https://doi.org/10.4315/0362-028x-62.3.239 DOI: https://doi.org/10.4315/0362-028X-62.3.239

Kim SW, Park JK, Lee CH, Hahn BS, Koo JC. Comparison of the Antimicrobial Properties of Chitosan Oligo-saccharides (COS) and EDTA against Fusarium fujikuroi Causing Rice Bakanae Disease. Current Microbiology 2016; 72(4): 496-502. https://doi.org/10.1007/s00284-015-0973-9 DOI: https://doi.org/10.1007/s00284-015-0973-9

Abd-Elsalam KA, Al-Dhabaan FA, Alghuthaymi M, Njobeh PB, Almoammar H. Nanobiofungicides: Present concept and future perspectives in fungal control. In: Nano-Biopesticides

Today and Future Perspectives 2019; Elsevier Inc. 2019; p. 315–351. https://doi.org/10.1016/B978-0-12-815829-6.00014-0 DOI: https://doi.org/10.1016/B978-0-12-815829-6.00014-0

Tan W, Zhang J, Mi Y, Dong F, Li Q, Guo Z. Synthesis, characterization, and evaluation of antifungal and anti-oxidant properties of cationic chitosan derivative via azide-alkyne click reaction. Int J Biol Macromol 2018; 120: 318-324. https://doi.org/10.1016/j.ijbiomac.2018.08.111 DOI: https://doi.org/10.1016/j.ijbiomac.2018.08.111

Kritchenkov AS, Egorov AR, Volkova OV, Kritchenkov IS, Kurliuk AV, Shakola TV, Khrustalev VN. Ultrasound-assisted catalyst-free phenol-yne reaction for the synthesis of new water-soluble chitosan derivatives and their nano-particles with enhanced antibacterial properties. Int J Biol Macromol 2019; 139: 103-113. https://doi.org/10.1016/j.ijbiomac.2019.07.203 DOI: https://doi.org/10.1016/j.ijbiomac.2019.07.203

Singh R, Tiamereen N, Dahio L, Banik S, Kanaujia SP, Neok P. Role of the Agro nanotechnology on the Plant Protection. Nagaland University Research Journal 2017; 10: 64-82. Available from: http://nurj.nagalanduniversity.ac.in/sites/ default/files/nurj/2017Vol10/NURJVolume10.pdf

Boddula R, Trivedi U, Pothu R, Rajput MS, Saran A. Nanopesticides and Nanosensors in Agriculture. In: Plant Nanobionics, Nanotechnology in the Life Sciences. Springer, Cham 2019; p. 165-181. https://doi.org/10.1007/978-3-030-12496-0_8 DOI: https://doi.org/10.1007/978-3-030-12496-0_8

Shawon ZBZ, Hoque ME, Chowdhury SR. Nanosensors and nanobiosensors: Agricultural and food technology aspects. In: Nanofabrication for Smart Nanosensor Applications. Elsevier 2020; p. 135-161. https://doi.org/10.1016/B978-0-12-820702-4.00006-4 DOI: https://doi.org/10.1016/B978-0-12-820702-4.00006-4

Tripathi M, Kumar S, Kumar A, Tripathi P, Kumar S. Agro-nanotechnology: A Future Technology for Sustainable Agriculture. Int J Curr Microbiol App Sci 2018; Especial Issue 7: 196-200. Available from: https://www.ijcmas.com/special/ 7/Manikant %20Tripathi,%20et%20al.pdf