β-1,3-glucan effect on the defence reaction of tomato leaves under fusarium wilt

  • Liudmila F. Kabashnikova Institute of Biophysics and Cell Engineering, National Academy of Sciences of Belarus
  • Sviataslau N. Shpileuski Institute of Biophysics and Cell Engineering, National Academy of Sciences of Belarus
  • Irina N. Domanskaya Institute of Biophysics and Cell Engineering, National Academy of Sciences of Belarus
  • Victoria I. Loucsha Institute of Biophysics and Cell Engineering, National Academy of Sciences of Belarus

Abstract

Objective reasons for a significant reduction in tomato crop yield include infection with pathogens of fungal diseases. In this regard, the study of the structural and functional characteristics of an infected plant represents an important step towards elucidating the mechanisms of resistance and creating a system of effective protection against diseases of fungal etiology. The effect of a drug containing β-1,3-glucan and a water-soluble polymer (WSP) based on a copolymer of acrylamide with sodium acrylate on the development of the pathogenic fungus Fusarium oxysporum sp. (Fus.oxy.) on solid Czapek medium was studied. The formation of protective reactions occurring in the leaves of 60-day-old tomato plants (Lycopersicon esculentum Mill., variety Tamara) during artificial Fusarium infection was studied under laboratory conditions. An assessment of the effect of β-1,3-glucan and WSP on the growth of fungal mycelium showed that the area of fungal colonies increases relative to the control variant by 4.0 and 4.7 times, respectively, therefore these compounds do not have antifungal activity and, moreover, stimulate the growth of fungal colonies in vitro. The protective effect of a preparation containing β-1,3-glucan and WSP was studied by pre-spraying tomato plants that were transferred from soil culture to tap water and infected with spores of the fungus Fus. oxy. through the root system. It was found that treatment of tomato plants with β-1,3-glucan induces protective
reactions, which are characterized by an increase in the content of reactive oxygen species, polyphenols and anthocyanins against the background of an increase in the expression of genes for PR proteins − β-1,3-glucanase (Glu) and chitinase (Chi) in tomato leaves during infection with Fus. oxy. Quantitative analysis of the content of photosynthetic pigments showed that the pathogenic fungus has a negative effect on the pigment apparatus, reducing the content of chlorophylls and carotenoids in tomato leaves, while pre-treatment of plants with a preparation including β-1,3-glucan and WSP contributes to a significant increase in the content of photosynthetic pigments. The results obtained provide a scientific basis for the use of β-1,3-glucan in crop production to improve the disease resistance of tomato plants.

Author Biographies

Liudmila F. Kabashnikova, Institute of Biophysics and Cell Engineering, National Academy of Sciences of Belarus

corresponding member of the National Academy of Sciences, Belarus; doctor of science (biology),
professor; head of the laboratory for applied biophysics and biochemistry.

Sviataslau N. Shpileuski, Institute of Biophysics and Cell Engineering, National Academy of Sciences of Belarus

researcher at the laboratory for applied biophysics and biochemistry.

Irina N. Domanskaya, Institute of Biophysics and Cell Engineering, National Academy of Sciences of Belarus

PhD (biology), docent; senior researcher at the laboratory for applied biophysics and biochemistry.

Victoria I. Loucsha, Institute of Biophysics and Cell Engineering, National Academy of Sciences of Belarus

PhD (biology); senior researcher at the laboratory for applied biophysics and biochemistry.

References

  1. Shakirova FM. Nespecificheskaya ustoychivost’ rasteniy k stressovym faktoram i yeyo regulyatsiya [Nonspecific resistance of plants to stress factors and its regulation]. Ufa: Gilem; 2001. 160 p. Russian.
  2. Peresypkin VF, editor. Bolezni sel’skokhozyaystvennykh kul’tur [Diseases of agricultural crops]. Kiev: Urozhay; 1991. T. 3. 512 p. Russian.
  3. Sidorova SF. Vertitsilleznoe i fuzarioznoe uvyanie odnoletnikh sel’skokhozyaystvennykh kul’tur [Verticillous and fusarium wilting of annual crops]. Moscow: Kolos; 1983. 157 p. Russian.
  4. Leubner-Metzger G. Functions and regulation of β-1,3-glucanase during seed germination, dormancy release and afterripening. Seed Science Research. 2003;13(1):17–34.
  5. Leclercq J, Fliegmann J, Tellstroem V. Identification of a multigene family encoding putative beta-glucan-binding proteins in Medicago truncatula. Journal of Plant Physiology. 2008;165(7):766–776.
  6. Sriram S, Misra RS, Sahu AK, Maheswari SK. A cell wall glucan elicitor induces resistance in taro against Phytophthora leaf blight. Journal of Plant Diseases and Protection. 2003;110(1):17–26.
  7. Klarzynski O, Plesse B, Joubert JM, Yvin JC, Kopp M, Kloareg B, et al. Linear β-1,3 glucans are elicitors of defense responses in tobacco. Plant Physiology. 2000;124(3):1027–1038.
  8. Mélida H, Sopeña-Torres S, Bacete L, Garrido-Arandia M, Jordá L, López G, et al. Non-branched β-1,3-glucan oligosaccharides trigger immune responses in Arabidopsis. The Plant Journal. 2018;93(1):34–49.
  9. Inui H, Yamaguchi Y, Hirano S. Elicitor actions of N-acetylchitooligosaccharides and laminarioligosaccharides for chitinase and L-phenylalanine ammonia-lyase induction in rice suspension culture. Bioscience, Biotechnology and Biochemistry. 1997;61(6):975–978.
  10. Cosio EG, Feger M, Miller CJ, Antelo L, Ebel J. High-affinity binding of fungal β-glucan elicitors to cell membranes of species of the plant family Fabaceae. Planta. 1996;200(1):92–99.
  11. Aziz A, Poinssot B, Daire X, Adrian M, Bézier A, Lambert B, et al. Laminarin elicits defense responses in grapevine and induces protection against Botrytis cinerea and Plasmopara viticola. Molecular Plant-Microbe Interactions. 2003;16(12):1118–1128.
  12. Kabashnikova L, Abramchik L, Domanskaya I, Savchenko G, Shpileuski S. β-1,3-glucan effect on the photosynthetic apparatus and oxidative stress parameters of tomato leaves under fusarium wilt. Functional Plant Biology. 2020;47(11):988–997.
  13. Rodrigues-Amaya DB, Kimura M. Handbook for Carotenoid Analysis. Washington, D. C.: HarvestPlus; 2004. 63 p.
  14. LeBel CP, Ischiropoulos H, Bondy SC. Evaluation of probe 2,’7’-dichlorfluorescin as an indicator of oxygen species formation and oxidative stress. Chemical Research in Toxicology. 1992;9:304–307.
  15. Mabry TJ, Markham KR, Thomas MB. The Systematic Identification of Flavonoids. Berlin: Springer; 1970. 354 p.
  16. Nikolaeva TN, Lapshin PV, Zagoskina NV. Metod opredeleniya summarogo soderzhaniya fenol’nykh soedineniy v rastitel’nykh ekstraktakh s reaktivom Folina-Denisa i reaktivom Folina-Chokal’teu: modifikatsiya i sravnenie [Method for determining the total content of phenolic compounds in plant extracts with Folin-Denis reagent and Folin-Chocalteu reagent: modification and comparison]. Khimiya Rastitel’nogo Syr’ya [Chemistry of Plant Raw Material]. 2021;(2):291–299. Russian.
  17. Rebrikov DV, Samatov GA, Trofimov DY, Semenov PA. PTsR v real’nom vremeni [Real-time PCR]. Moscow: GEOTARMedia; 2015. 233 p. Russian.
  18. Cao J, Tan X. Comprehensive Analysis of the Chitinase Family Genes in Tomato (Solanum lycopersicum). Plants. 2019;8(3):52.
  19. Milling A, Babujee L, Allen C. Ralstonia solanacearum extracellular polysaccharide is a specific elicitor of defense responses in wilt-resistant tomato plants. PLoS One. 2011;6(1). DOI: 10.1371/journal.pone.0015853.
  20. Ren Z, Li Z, Miao Q, Yang Y, Deng W, Hao Y. The auxin receptor homologue in Solanum lycopersicum stimulates tomato fruit set and leaf morphogenesis. Journal of Experimental Botany. 2011; 62(8):2815–2826.
  21. Du B, Meenu M, Liu H, Xu B. A Concise Review on the Molecular Structure and Function Relationship of β-Glucan. International Journal of Molecular Sciences. 2019;20(16):4032.
  22. Melo TA, Serra IMRS, Nascimento ITVS. Ascophyllum nodosum seaweed extract effect on morphology and cellulolytic ability of the fungus Fusarium oxysporum f. sp. vasinfectum. Research, Society and Development. 2020;9(11). DOI: https://doi.org/10.33448/rsd-v9i11.991322.
  23. Krul LP, Nareyko EI, Matusevich YuI, Yakimtsova LV, Matusevich V. Superabsorbenty na osnove sopolimerov akrilamida s akrilatom natriya [Superabsorbents based on copolymers of acrylamide with sodium acrylate]. Polymer Bulletin. 2000;45(2):159–165.
  24. Fesel PH, Zuccaro A. β-glucan: Crucial component of the fungal cell wall and elusive MAMP in plants. Fungal Genetics and Biology. 2016;90:53-60.
  25. Khan M, Ali S, Al Azzawi TNI, Saqib S, Ullah F, Ayaz A, et al. The Key Roles of ROS and RNS as a Signaling Molecule in Plant-Microbe Interactions. Antioxidants (Basel). 2023;12(2):268.
  26. Vincenzo L, Veronica MT, Cardinali L, Cardinali A. Role of phenolics in the resistance mechanisms of plants against fungal pathogens and insects. In: Imperato F, editor. Phytochemistry: Advances in Research. Kerala, India: Research Signpost; 2006:23–67.
  27. Skadhauge B, Thomsen KK, Wettstein DV. The role of the barley testa layer and its flavonoid content in resistance to Fusarium infections. Hereditas. 1977;126:147–160.
  28. López-Zapata SP, García-Jaramillo DJ, López WR, Ceballos-Aguirre N. Tomato (Solanum lycopersicum L.) and Fusarium oxysporum f. sp. lycopersici interaction. A review. Revista UDCA Actualidad & Divulgación Científica. 2021;24(1). DOI: https://doi.org/10.31910/rudca.v24.n1.2021.1713.
  29. Srinivas C, Nirmala D, Narasimha Murthy K, Mohan CD, Lakshmeesha TR, Singh B, et al. Fusarium oxysporum f. sp. lycopersici causal agent of vascular wilt disease of tomato: biology to diversity – A review. Saudi Journal of Biological Sciences. 2019;26(7):1315–1324.
  30. Pshibitko NL, Zenevich LA, Kabashnikova LF. Izmeneniya v fotosinteticheskom apparate pri fuzarioznom uvyanie tomata [Changes in the photosynthetic apparatus during fusarium wilt of tomatoes]. Fiziologiya Rasteniy [Russian Journal of Plant Physiology]. 2006;53(1):25–31. Russian.
  31. Kabashnikova LF. Fotosinteticheskiy apparat i stress u rasteniy [Photosynthetic apparatus and stress in plants]. Minsk: Belaruskaya navuka; 2014. 267 p. Russian.
  32. Sen S, Mukherji S. Season-controlled changes in biochemical constituents and oxidase enzyme activities in tomato (Lycopersicon esculentum Mill.). Journal of Environmental Biology. 2009;30(4):479–483.
  33. Balasubramanian V, Vashisht D, Cletus J, Sakthivel N. Plant beta-1,3-glucanases: their biological functions and transgenic expression against phytopathogenic fungi. Biotechnology Letters. 2012;34(11):1983–1990.
  34. Sela-Buurlage MB, Ponstein AS, Bres-Vloemans SA, Melchers LS, Van Den Elzen PJM, Cornelissen BJC. Only Specific Tobacco (Nicotiana tabacum) Chitinases and β-1,3-Glucanases Exhibit Antifungal Activity. Plant Physiology. 1993;101:857–863.
  35. Wen X, Tengsheng Z, Dandan L, Sufang A, Jinna H, Genyi L. Evolution and Expression Divergence of the Chitinase Gene Family against Leptosphaeria maculans and Sclerotinia sclerotiorum Infection in Brassica napus. Journal of Henan Agricultural Sciences. 2020;49:89–103.
  36. Li J, Zhang R, Qi X, Xie Q, Chen X. A Preliminary Study on Cloning of Chitinase Gene and Relationships to Resistance of Powdery Mildew in Cucumber (Cucumis sativus L.). Molecular Plant Breeding. 2015;13:1584–1591.
  37. Xu J, Xu X, Tian L, Wang G, Zhang X, Wang X, et al. Discovery and identification of candidate genes from the chitinase gene family for Verticillium dahliae resistance in cotton. Scientific Reports. 2016;6:29022.
Published
2024-10-31
Keywords: tomato, reactive oxygen species, polyphenols, chlorophyll, carotenoids, glucanase, chitinase, Fusarium oxysporum sp.
Supporting Agencies The authors thanks Sushchevich Yuliya, − PhD (аgriculture), Head of the Immunity Laboratory, the Republican Unitary Enterprise «Research and Practical Centre for Arable Farming of the National Academy of Sciences of Belarus» for the fungus culture Fus. oxy. and consultation with respect to its cultivation and the tomato plant inoculation procedure. The work was funded by the State Program «High Technology and Technic» for 2016–2020.
How to Cite
Kabashnikova, L., Shpileuski, S., Domanskaya, I., & Loucsha, V. (2024). β-1,3-glucan effect on the defence reaction of tomato leaves under fusarium wilt. Journal of the Belarusian State University. Ecology, 3, 49-58. Retrieved from https://journals.bsu.by/index.php/ecology/article/view/6589
Issue
No 3 (2024): Journal of the Belarusian State University. Ecology
Section
The Study and Rehabilitation of Ecosystems