Induction and expression of systemic resistance to downy mildew disease in grapevine by chitosan

Emad MAHMOUD; Zeinab N. HUSSIEN; Abou Ghanima S.F. SHEHATA; Najat MARRAIKI; Enas ALMANZALAWI; Tahani ALQAHTANI; Mohamed ABOU-ZEID; Mahmoud KAMHAWY

doi:10.15835/nbha53114265

Authors

Emad MAHMOUD Plant Pathology Research Institute, Agricultural Research Center, 12619, Giza (EG)
Zeinab N. HUSSIEN Plant Pathology Research Institute, Agricultural Research Center, 12619, Giza (EG)
Abou Ghanima S.F. SHEHATA Plant Pathology Research Institute, Agricultural Research Center, 12619, Giza (EG)
Najat MARRAIKI King Saud University, College of Science, Department of Botany and Microbiology, Riyadh, 11451 (SA)
Enas ALMANZALAWI King Abdulaziz University, Faculty of Science, Department of Biological Sciences, Jeddah 21589 (SA)
Tahani ALQAHTANI King Abdulaziz University, Faculty of Science, Department of Biological Sciences, Jeddah 21589 (SA)
Mohamed ABOU-ZEID Plant Pathology Research Institute, Agricultural Research Center, 12619, Giza (EG)
Mahmoud KAMHAWY Plant Pathology Research Institute, Agricultural Research Center, 12619, Giza (EG)

DOI:

https://doi.org/10.15835/nbha53114265

Keywords:

-1.3-glucanase, inducing resistance, peroxidase, phenols, Plasmopara viticola, polyphenol oxidase, salicylic

Abstract

Grapes represent a significant agricultural product globally. Despite their significance and value, grapes face numerous challenges, including disease. Grapevines are susceptible to various pathogens, with downy mildew caused by Plasmopara viticola, being the most damaging. In the twentieth century, contact and systemic fungicides were developed to combat plant pathogens, such as downy mildew. Recently, there has been a growing demand to minimize fungicide use and shift towards sustainability through implementing eco-friendly practices. Utilizing plant defense elicitors to stimulate disease resistance in grapevines is a crucial strategy. We conducted experiments in the field over two seasons, 2021 and 2022, at two different locations using two grape cultivars (‘Flame’ and ‘Crimson’). Four concentrations of chitosan (1, 2, 4, and 8 mM) were applied. The results indicated that chitosan could induce systemic resistance against downy mildew caused by P. viticola by activating the salicylic acid (SA) pathway, increasing the plant’s concentrations of SA and phenols, and augmenting the efficacy and activity of defense enzymes. The treatment also significantly enhanced the yield production of 1.3-glucanase, chitinase, peroxidase, and polyphenol oxidase. The present study assessed the efficacy of chitosan as a resistance inducer in managing grapevine downy mildew and examined its mechanism of action.

References

Abeles FB, Forrence LE (1970). Temporal and hormonal control of β-1,3-glucanase in Phaseolus vulgaris L. Plant Physiology 45:395-400. https://doi.org/10.1104/pp.45.4.395

Allam AI, Hollis SP (1972). Sulfide inhibition of oxidase in rice root. Phytopathology 62:634-639. https://doi.org/10.1094/Phyto-62-634

Ammar MM, Amer GA, Abd El-All AM, Badawy AE (2018). Effect of some plant extracts and oils on grape downy mildew disease. Menoufia Journal of Plant Protection 3(2):1-16. https://doi.org/10.21608/mjapam.2018.123337

Anonymous (2005). Co-Stat Program, version 6.4. Monterey, CA, USA: CoHort Software. http://www.cohort.com

Aziz A, Trotel-Aziz P, Dhuicq L, Jeandet P, Couderchet M, Vernet G (2006). Chitosan oligomers and copper sulfate induce grapevine defense reactions and resistance to gray mold and downy mildew. Phytopathology 96:1188-1194. https://doi.org/10.1094/PHYTO-96-1188

Chakraborty M, Hasanuzzaman M, Rahman M, Khan AR, Bhowmik P, Mahmud NU, … Islam T (2020). Mechanism of plant growth promotion and disease suppression by chitosan biopolymer. Agriculture 10(12):624. https://doi.org/10.3390/agriculture10120624

Chandrkrachang S (2002). The applications of chitin in agriculture in Thailand. Advances in Chitin Science 5:458-462.

De Bona GS, Vincenzi S, De Marchi F, Angelini E, Bertazzon N (2021). Chitosan induces delayed grapevine defense mechanisms and protects grapevine against Botrytis cinerea. Journal of Plant Diseases and Protection 128(5):715-724. https://doi.org/10.1007/s41348-021-00432-3

El Hadrami A, Adam LR, El Hadrami I, Daayf F (2010). Chitosan in crop protection. Marine Drugs 8(4):968-987. https://doi.org/10.3390/md8040968

Emami-Bistgani Z, Siadat SA, Bakhshandeh A, Ghasemi Pirbalouti A, Hashemi M (2017). Interactive effects of drought stress and chitosan application on physiological characteristics and essential oil yield of Thymus daenensis. The Crop Journal 5(5):407-415. https://doi.org/10.1016/j.cj.2017.04.003

Faoro F, Maffi D, Cantu D, Iriti M (2008). Chemical-induced resistance against powdery mildew in barley: The effects of chitosan and benzothiadiazole. BioControl 53(3):387-401. https://doi.org/10.1007/s10526-007-9146-2

Gao QM, Zhu S, Kachroo P, Kachroo A (2015). Signal regulators of systemic acquired resistance. Frontiers in Plant Science 6:228. https://doi.org/10.3389/fpls.2015.00228

Gessler C, Pertot I, Perazzolli M (2011). Plasmopara viticola: A review of knowledge on downy mildew of grapevine and effective disease management. Phytopathologia Mediterranea 50(1):3-44. https://doi.org/10.14601/Phytopathol_Mediterr-9360

Goldschmidt EE, Goren R, Monselise SP (1968). The IAA oxidase system of citrus roots. Planta 72(2):213-222.

Goy RC, Britto D, Assis OBG (2009). A review of the antimicrobial activity of chitosan. Polímeros: Ciência e Tecnologia 19(3):241-247. https://doi.org/10.1590/S0104-14282009000300008

Guan Y, Hu J, Wang X, Shao C (2009). Seed priming with chitosan improves maize germination and seedling growth in relation to physiological changes under low temperature stress. Journal of Zhejiang University Science B 10(6):427-433. https://doi.org/10.1631/jzus.B0920003

Hadwiger LA (2013). Multiple effects of chitosan on plant systems: Solid science or hype. Plant Science 208:42-49. https://doi.org/10.1016/j.plantsci.2013.03.001

Héloir MC, Adrian M, Brulé D, Claverie J, Cordelier S, Daire X (2019). Recognition of elicitors in grapevine: From MAMP and DAMP perception to induced resistance. Frontiers in Plant Science 10:1117. https://doi.org/10.3389/fpls.2019.01117

Kaku H, Shibuya N, Xu P, Aryan AP, Fincher GB (1997). N-acetylchitooligosaccharide elicitor induces expression of a single 1,3-β-glucanase gene in suspension-cultured cells from barley (Hordeum vulgare). Physiologia Plantarum 100(1):111-118. https://doi.org/10.1111/j.1399-3054.1997.tb02297.x

Koledenkova K, Esmaeel Q, Jacquard C, Nowak J, Clément C, Ait Barka E (2022). Plasmopara viticola the causal agent of downy mildew of grapevine: From its taxonomy to disease management. Frontiers in Microbiology 13:889472. https://doi.org/10.3389/fmicb.2022.889472

Kumar RR, Sharma SK, Goswami S, Verma P, Singh K, Dixit N, Rai RD (2015). Salicylic acid alleviates the heat stress-induced oxidative damage of starch biosynthesis pathway by modulating the expression of heat-stable genes and proteins in wheat (Triticum aestivum). Acta Physiologiae Plantarum 37:143. https://doi.org/10.1007/s11738-015-1861-8

Kurita K (2006). Chitin and chitosan: Functional biopolymers from marine crustaceans. Marine Biotechnology 8(3):203-226. https://doi.org/10.1007/s10126-005-0237-9

Li P, Cao Z, Wu Z, Wang X, Li X (2016). The effect and action mechanisms of oligochitosan on control of stem dry rot of Zanthoxylum bungeanum. International Journal of Molecular Sciences 17(7):1044. https://doi.org/10.3390/ijms17071044

Liu T, Li T, Zhang L, Li H, Liu S, Yang S, … Zou N (2020). Exogenous salicylic acid alleviates the accumulation of pesticides and mitigates pesticide-induced oxidative stress in cucumber plants (Cucumis sativus L.). Ecotoxicology and Environmental Safety 208:111654. https://doi.org/10.1016/j.ecoenv.2020.111654

Mahmoud EY, Hussien-Zinab N, Ibrahim MM, Risk-Heba Y (2021). Using of some biotic and abiotic inducers on controlling peanut Cercospora leaf spot. Current Sciences International 10(1):18-28. https://doi.org/10.28941/csi/2021/10/1/18-28

Manjunatha G, Niranjan Raj S, Prashanth GN, Deepak S, Amruthesh KN, Shetty HS (2009). Nitric oxide is involved in chitosan-induced systemic resistance in pearl millet against downy mildew disease. Pest Management Science 65(7):737-743. https://doi.org/10.1002/ps.1748

Matta A, Dimond AE (1963). Symptoms of Fusarium wilt in relation to quantity of fungus and enzyme activity in tomato stems. Phytopathology 53:574–587.

Miao Y, Luo X, Gao X, Wang W, Li B, Hou L (2020). Exogenous salicylic acid alleviates salt stress by improving leaf photosynthesis and root system architecture in cucumber seedlings. Scientia Horticulturae 272:109577. https://doi.org/10.1016/j.scienta.2020.109577

Monreal J, Reese ET (1969). The chitinase of Serratia marcescens. Canadian Journal of Microbiology 15(7):689-696.

Moreau S, Van Aubel G, Janky R, Van Cutsem P (2020). Chloroplast electron chain, ROS production, and redox homeostasis are modulated by COS-OGA elicitation in tomato (Solanum lycopersicum) leaves. Frontiers in Plant Science 11:597589. https://doi.org/10.3389/fpls.2020.597589

Nahar SJ, Kazuhiko S, Haque SM (2012). Effect of polysaccharides including elicitors on organogenesis in protocorm-like body (PLB) of Cymbidium insigne in vitro. Journal of Agricultural Science and Technology 2(11):1029-1033. https://doi.org/10.1007/s10012-012-0043-6

Nishizawa Y, Kawakami A, Hibi T, He DY, Shibuya N, Minami E (1999). Regulation of the chitinase gene expression in suspension-cultured rice cells by N-acetylchitooligosaccharides: Differences in the signal transduction pathways leading to the activation of elicitor-responsive genes. Plant Molecular Biology 39(5):907-914. https://doi.org/10.1023/A:1006040304860

Omar HS, Al Mutery A, Osman NH, Reyad NE, Abou-Zeid MA (2021). Molecular marker analysis of stem and leaf rust resistance in Egyptian wheat genotypes and interpretation of the antifungal activity of chitosan-copper nanoparticles by molecular docking analysis. Plos One 16(11):e0257959. https://doi.org/10.1371/journal.pone.0257959

Orzali L, Corsi B, Forni C, Riccioni L (2017). Chitosan in agriculture: A new challenge for managing plant disease. In: Shalaby EA (Ed). Biological Activities and Application of Marine Polysaccharides. London: IntechOpen, pp 83-98. https://doi.org/10.5772/66723

Orzali L, Forni C, Riccioni L (2014). Effect of chitosan seed treatment as elicitor of resistance to Fusarium graminearum in wheat. Seed Science and Technology 42(1):132-149. https://doi.org/10.15258/sst.2014.42.1.12

Prakongkha I, Sompong M, Wongkaew S, Athinuwat D, Buensanteai N (2013). Foliar application of systemic acquired resistance (SAR) inducers for controlling grape anthracnose caused by Sphaceloma ampelinum de Bary in Thailand. African Journal of Biotechnology 12(33):5148-5156. https://doi.org/10.5897/AJB2013.12459

Raskin I, Turner IM, Melander WR (1989). Regulation of heat production in the inflorescences of an Arum lily by endogenous salicylic acid. Proceedings of the National Academy of Sciences 86(6):2214-2218. https://doi.org/10.1073/pnas.86.6.2214

Roby D, Gadelle A, Toppan A (1987). Chitin oligosaccharides as elicitors of chitinase activity in melon plants. Biochemical and Biophysical Research Communications 143(3):885-892. https://doi.org/10.1016/0006-291X(87)92299-3

Romanazzi G (2010). Chitosan treatment for the control of postharvest decay of table grapes, strawberries, and sweet cherries. Fresh Produce 4:111–115. https://doi.org/10.1055/s-0030-1255085

Snell FD, Snell CT (1953). Colorimetric Methods of Analysis, Vol. III. New York: D. Van Nostrand Co. Inc.

Taibi O, Bardelloni V, Bove F, Scaglia F, Caffi T, Rossi V (2022). Activity of resistance inducers against Plasmopara viticola in vineyard. BIO Web of Conferences 50:03003. https://doi.org/10.1051/bioconf/20225003003

Toffolatti SL, Russo G, Campia P, Bianco PA, Borsa P, Coatti M (2018). A time-course investigation of resistance to the carboxylic acid amide mandipropamid in field populations of Plasmopara viticola treated with anti-resistance strategies. Pest Management Science 74(12):2822-2834. https://doi.org/10.1002/ps.5072

Tripathi D, Raikhy G, Kumar D (2019). Chemical elicitors of systemic acquired resistance—Salicylic acid and its functional analogs. Current Plant Biology 17:48-59. https://doi.org/10.1016/j.cpb.2019.03.002

Tuzun S, Rao MN, Vogeli U, Schardl CL, Kuc J (1989). Induced systemic resistance to blue mold: Early induction and accumulation of β-1,3-glucanase, chitinase, and other pathogenesis-related proteins (b-proteins) in immunized tobacco plants. Phytopathology 79(9):979-983.

Xing K, Zhu X, Peng X, Qin S (2015). Chitosan antimicrobial and eliciting properties for pest control in agriculture: A review. Agronomy for Sustainable Development 35(2):569-588. https://doi.org/10.1007/s13593-014-0252-3

Xoca-Orozco LA, Cuellar-Torres EA, González-Morales S, Gutiérrez-Martínez P, López-García U, Herrera-Estrella L, … Chacón-López A (2017). Transcriptomic analysis of avocado hass (Persea americana Mill) in the interaction system fruit-chitosan-Colletotrichum. Frontiers in Plant Science 8:956. https://doi.org/10.3389/fpls.2017.00956

Zhang D, Wang H, Hu Y, Liu Y (2015). Chitosan controls postharvest decay on cherry tomato fruit possibly via the mitogen-activated protein kinase signaling pathway. Journal of Agricultural and Food Chemistry 63(31):7399-7404. https://doi.org/10.1021/acs.jafc.5b01760