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Berosich, C.M.; Lopez-Moya, F.; Lopez-Llorca, L.V. Modulation of the Host Defence System by Nematophagous Fungi and Chitosan. Encyclopedia. Available online: https://encyclopedia.pub/entry/55266 (accessed on 05 May 2024).
Berosich CM, Lopez-Moya F, Lopez-Llorca LV. Modulation of the Host Defence System by Nematophagous Fungi and Chitosan. Encyclopedia. Available at: https://encyclopedia.pub/entry/55266. Accessed May 05, 2024.
Berosich, Carla Mariel, Federico Lopez-Moya, Luis Vicente Lopez-Llorca. "Modulation of the Host Defence System by Nematophagous Fungi and Chitosan" Encyclopedia, https://encyclopedia.pub/entry/55266 (accessed May 05, 2024).
Berosich, C.M., Lopez-Moya, F., & Lopez-Llorca, L.V. (2024, February 21). Modulation of the Host Defence System by Nematophagous Fungi and Chitosan. In Encyclopedia. https://encyclopedia.pub/entry/55266
Berosich, Carla Mariel, et al. "Modulation of the Host Defence System by Nematophagous Fungi and Chitosan." Encyclopedia. Web. 21 February, 2024.
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Modulation of the Host Defence System by Nematophagous Fungi and Chitosan

Nematophagous fungi (NFs), which are responsible for soil suppression of plant-parasitic nematodes, are multitrophic biocontrol agents. This raises the question of the transition between lifestyles (e.g., endophytism vs. egg parasitism). The NF Pochonia chlamydosporia colonises food crops and promotes their growth and yield. When colonising the plant, P. chlamydosporia induces the plant immunity (PI). However, it also evades the PI. To do this, both endophytic NF and pathogenic fungi (PF) secrete LysM effectors (LysM-effs). LysM effectors have been shown to have diverse functions in different organisms, including the protection of fungal chitin from plant chitinases. P. chlamydosporia is resistant to chitosan, which modulates gene expression in fungi and plants and has antimicrobial properties. P. chlamydosporia chitin deacetylases (CDA) and chitosanases (CSN) also help P. chlamydosporia evade plant immunity, resist exogenous chitosan, and are induced during fungal infection of nematode eggs. NF-chitosan formulations are new biomanagement tools against plant parasitic nematodes, fungal wilt pathogens and insect pests that currently threaten food security crops. Furthermore, omics techniques are useful tools to elucidate the role of CDAs, CSNs, LysM-effs, adhesion proteins and carbohydrate-active enzymes in pathogen–BCA–plant interactions, adhesion and infection to nematode eggs and their modulation by chitosan.

nematophagous fungi Pochonia chlamydosporia plant immune system biocontrol agents chitosan chitin deacetylases chitosanases LysM effectors fungal host infection fungus–plant interactions
A plethora of nematophagous, mycoparasitic, plant- and insect-pathogenic, plant-endophytic, and saprophytic fungi belong to the order Hypocreales. Some of these fungi can switch between different lifestyles [1][2]. Nematophagous fungi (NFs), such as Pochonia chlamydosporia and Purpureocillium lilacinum, have been identified in nematode-suppressive soils [3][4]. P. chlamydosporia is a cosmopolitan biocontrol fungus which can parasitize females and eggs of cyst- and root-knot nematodes but also colonises endophytically the roots of many crops [5]. The multitrophic nature of these fungal biocontrol agents (BCAs) is paramount for their efficacy because, unlike conventional agrochemicals, they can be host-specific and persist in the environment. This leads to long-term host management [6] with low environmental impact and no damage to human health, unlike toxic agrochemicals.
Deacetylation of chitin results in the formation of chitosan (Figure 1). This occurs when the degree of deacetylation of chitin reaches approximately 50% due to solubilisation and protonation of the -NH2 functional group at the C-2 position of the D-glucosamine repeat unit [7]. Chitosan is thus a linear polymer of beta-(1-4)-linked N-acetyl-2-amino-2-deoxy-d-glucose and 2-amino-2-deoxy-d-glucose subunits [8]. It is also the only cationic biopolymer, with a wide range of applications, such as flocculant for protein recovery or decontamination [7]. The N-deacetylation of chitin and chitooligosaccharides is catalysed by chitin deacetylases (CDAs). These enzymes have different substrate specificities and give rise to fully or partially deacetylated products with various deacetylation patterns [9]. The main raw materials to obtain chitosan are marine crustacean exoskeletons [10]. Therefore, the multiple applications of this compound add value to the waste of the shellfish industry. As an alternative to toxic agrochemicals, chitosan may reduce current soil, marine, and freshwater pollution rates. Chitosan has antimicrobial properties and modulates the gene expression of plants and fungi [8]. It can be combined with fungal BCAs to protect global food security crops [11].
Figure 1. Effects of chitosan on biocontrol fungi and plants. Responses of nematophagous fungi (NFs, red) to chitosan (completely deacetylated as portrayed) and plants to NF combined with Chitosan (purple) are displayed. Abbreviations: RF—chitosan-resistant fungi; SF—chitosan-sensitive fungi; NFs—nematophagous fungi; Pc—Pochonia chlamydosporia [12]; Negg—nematode eggs; GE—gene expression; PD—plant defences; JA—jasmonic acid; ROS—reactive oxygen species; Ta—Trichoderma atroviride.
Polysaccharide deacetylases are widely distributed in fungi and other organisms [13][14][15]. They have been reported to have diverse functions in developmental processes other than virulence [9][16][17][18][19][20][21][22]. For instance, the fungal pathogen Magnaporthe oryzae expresses CDAs during appressorium development. Additionally, chitosan is a cell wall component of germ tubes and appressoria of M. oryzae [17]. Alternatively, chitosan could promote the avoidance of plant immunity (PI) and fitness/virulence of fungal pathogens, including BCAs such as P. chlamydosporia [8]. Moreover, fungal effectors (F-effs) prevent pathogen recognition by plants, suppressing host immune responses (IR), and manipulating host cell physiology to facilitate colonisation [23]. Many effectors and their modes of action have been well identified and characterized as LysM domains effectors (LysM-effs) in fungi [23]. Analysing fungi with different lifestyles, our research group has shown that LysM-effs, CDAs, chitosanases (CSNs), and other hydrolases contribute to fungal lifestyle [24][25][26][27][28][29].
This article describes recent advances in NF gene expression in relation to their multi-trophic lifestyles and their relevance as BCAs. The importance of their combination with natural elicitors, such as chitosan, and their modulatory and regulatory potential on fungi and plants is highlighted. The mechanisms of action and effects of NFs, PFs, and chitosan on plants are discussed in a cross-sectional and integrative manner, considering the relevance of F-effs, CDAs, CSNs, and plant cell wall-degrading enzymes in the evolution of NFs to evade PI.

References

  1. Bushley, K.E.; Raja, R.; Jaiswal, P.; Cumbie, J.S.; Nonogaki, M.; Boyd, A.E.; Owensby, C.A.; Knaus, B.J.; Elser, J.; Miller, D.; et al. The Genome of Tolypocladium inflatum: Evolution, Organization, and Expression of the Cyclosporin Biosynthetic Gene Cluster. PLoS Genet. 2013, 9, e1003496.
  2. Sung, G.-H.; Poinar, G.O.; Spatafora, J.W. The oldest fossil evidence of animal parasitism by fungi supports a Cretaceous diversification of fungal–arthropod symbioses. Mol. Phylogenet. Evol. 2008, 49, 495–502.
  3. Bent, E.; Loffredo, A.; McKenry, M.V.; Becker, J.O.; Borneman, J. Detection and Investigation of Soil Biological Activity against Meloidogyne incognita. J. Nematol. 2008, 40, 109–118.
  4. Lamovsek, J.; Urek, G.; Trdan, S. Biological control of root-knot nematodes (Meloidogyne spp.): Microbes against the pests. Acta Agron. Slov. 2013, 101, 263–275.
  5. Bordallo, J.J.; Lopez-Llorca, L.V.; Jansson, H.B.; Salinas, J.; Persmark, L.; Asensio, L. Colonization of plant roots by egg-parasitic and nematode-trapping fungi. New Phytol. 2002, 154, 491–499.
  6. Singh, S.; Sharma, A. Fungi as Biological Control Agents. In Biofertilizers for Sustainable Agriculture and Environment; Giri, B., Prasad, R., Wu, Q.S., Varma, A., Eds.; Springer: Cham, The Netherlands, 2019; Volume 55.
  7. Rinaudo, M. Chitin and chitosan: Properties and applications. Prog. Polym. Sci. 2006, 31, 603–632.
  8. Lopez-Moya, F.; Suarez-Fernandez, M.; Lopez-Llorca, L.V. Molecular Mechanisms of Chitosan Interactions with Fungi and Plants. Int. J. Mol. Sci. 2019, 20, 332.
  9. Grifoll-Romero, L.; Pascual, S.; Aragunde, H.; Biarnés, X.; Planas, A. Chitin Deacetylases: Structures, Specificities, and Biotech Applications. Polymer 2018, 10, 352.
  10. Younes, I.; Rinaudo, M. Chitin and Chitosan Preparation from Marine Sources. Structure, Properties and Applications. Mar. Drugs 2015, 13, 1133–1174.
  11. Escudero, N.; Ferreira, S.R.; Lopez-Moya, F.; Naranjo-Ortiz, M.A.; Marin-Ortiz, A.I.; Thornton, C.R.; Lopez-Llorca, L.V. Chitosan enhances parasitism of Meloidogyne javanica eggs by the nematophagous fungus Pochonia chlamydosporia. Fungal Biol. 2016, 120, 572–585.
  12. Zare, R.; Gams, W.; Evans, H.C. A revision of Verticillium section Prostrata. V. The genus Pochonia, with notes on Rotiferophthora. Nova Hedwig. 2001, 73, 51–86.
  13. Berlemont, R. Distribution and diversity of enzymes for polysaccharide degradation in fungi. Sci. Rep. 2017, 7, 222.
  14. Andreou, A.; Giastas, P.; Christoforides, E.; Eliopoulos, E.E. Structural and Evolutionary Insights within the Polysaccharide Deacetylase Gene Family of Bacillus anthracis and Bacillus cereus. Genes 2018, 9, 386.
  15. Sun, H.; Gao, L.; Xue, C.; Mao, X. Marine-polysaccharide degrading enzymes: Status and prospects. Compr. Rev. Food Sci. Food Saf. 2020, 19, 2767–2796.
  16. Baker, L.G.; Specht, C.A.; Donlin, M.J.; Lodge, J.K. Chitosan, the deacetylated form of chitin, is necessary for cell wall integrity in Cryptococcus neoformans. Eukaryot. Cell 2007, 6, 855–867.
  17. Geoghegan, I.A.; Gurr, S.J. Chitosan Mediates Germling Adhesion in Magnaporthe oryzae and Is Required for Surface Sensing and Germling Morphogenesis. PLoS Pathog. 2016, 12, e1005703.
  18. Christodoulidou, A.; Bouriotis, V.; Thireos, G. Two Sporulation-specific Chitin Deacetylase-encoding Genes Are Required for the Ascospore Wall Rigidity of Saccharomyces cerevisiae. J. Biol. Chem. 1996, 271, 31420–31425.
  19. Sánchez-Vallet, A.; Mesters, J.R.; Thomma, B.P. The battle for chitin recognition in plant-microbe interactions. FEMS Microbiol. Rev. 2015, 39, 171–183.
  20. White, S.; McIntyre, M.; Berry, D.R.; McNeil, B. The autolysis of industrial filamentous fungi. Crit. Rev. Biotechnol. 2002, 22, 1–14.
  21. Zhao, Y.; Park, R.-D.; Muzzarelli, R.A. Chitin deacetylases: Properties and applications. Mar. Drugs 2010, 8, 24–46.
  22. Cord-Landwehr, S.; Melcher, R.L.; Kolkenbrock, S.; Moerschbacher, B.M. A chitin deacetylase from the endophytic fungus Pestalotiopsis sp. efficiently inactivates the elicitor activity of chitin oligomers in rice cells. Sci. Rep. 2016, 6, 38018.
  23. Liu, T.; Chen, Y.; Tian, S.; Li, B. Crucial Roles of Effectors in Interactions between Horticultural Crops and Pathogens. Horticulturae 2023, 9, 250.
  24. Lopez-Llorca, L.V.; Gómez-Vidal, S.; Monfort, E.; Larriba, E.; Casado-Vela, J.; Elortza, F.; Jansson, H.B.; Salinas, J.; Martín-Nieto, J. Expression of serine proteases in egg-parasitic nematophagous fungi during barley root colonization. Fungal Genet. Biol. 2010, 47, 342–351.
  25. Larriba, E.; Jaime, M.D.; Carbonell-Caballero, J.; Conesa, A.; Dopazo, J.; Nislow, C.; Martín-Nieto, J.; Lopez-Llorca, L.V. Sequencing and functional analysis of the genome of a nematode egg-parasitic fungus, Pochonia chlamydosporia. Fungal Genet. Biol. 2014, 65, 69–80.
  26. Aranda-Martinez, A.; Lenfant, N.; Escudero, N.; Zavala-Gonzalez, E.A.; Henrissat, B.; Lopez-Llorca, L.V. CAZyme content of Pochonia chlamydosporia reflects that chitin and chitosan modification are involved in nematode parasitism. Environ. Microbiol. 2016, 18, 4200–4215.
  27. Aranda-Martinez, A.; Grifoll-Romero, L.; Aragunde, H.; Sancho-Vaello, E.; Biarnés, X.; Lopez- Llorca, L.V.; Planas, A. Expression and specificity of a chitin deacetylase from the nematophagous fungus Pochonia chlamydosporia potentially involved in pathogenicity. Sci. Rep. 2018, 8, 2170.
  28. Suarez-Fernandez, M.; Sambles, C.; Lopez-Moya, F.; Nueda, M.J.; Studholme, D.J.; Lopez-Llorca, L.V. Chitosan modulates Pochonia chlamydosporia gene expression during nematode egg parasitism. Environ. Microbiol. 2021, 23, 4980–4997.
  29. Suarez-Fernandez, M.; Aragon-Perez, A.; Lopez-Llorca, L.V.; Lopez-Moya, F. Putative LysM Effectors Contribute to Fungal Lifestyle. Int. J. Mol. Sci. 2021, 22, 3147.
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