MYCOPARASITISM: MODE OF ACTION

All living organisms require nutrient for their growth and so does the plant pathogen. Thus various soil microorganisms compete for limited resources like carbon, nitrogen, iron etc. which may result in biological control of plant pathogen. Mycoparasitism is a mechanisms where one fungus directly attack and parasitize another fungus for nutrient source. It may involve recognition, contact, attachment followed by penetration, and infection. The key factor is nutrient transfer from host to mycoparasite.

Mycoparasitism is initiated by directed growth toward the host on recognizing the host (Chet et al., 1981), recognition or sensing may be thigmotropism (response to touch stimulus) or chemotropism (chemical) i.e. interaction between the complementary molecule lectin-carbohydrate present on both the pathogen and the host surface. Isolation and characterization of novel lectins from S. rolfsii has been described by Inbar and Chet (1994).  After recognition, contact is made with the host surface and subsequently extracellular enzyme are secreted.  The mycoparasitic soil fungi attack another fungus by secreting cell wall degrading enzyme β-1,3 glucanases,  chitinases, cellulases and proteases (Haran et al., 1996; Vázquez-Garcidueñas et al., 1998; De Marco 2003). These lytic enzymes produced by the biocontrol agent are responsible for suppression of the plant pathogen by breaking down the polysaccharides, chitin, and β-glucans that are responsible for the rigidity of fungal cell walls, thereby destroying cell wall integrity.  Mycoparasitic fungus has the ability to   parasitize the macroconidia, chlamydopsore, hyphae (Davanlou et al., 1999), and sclerotia (van den Boogert and Deacon, 1994) the mechanism is correlated with biocontrol.  Pythium oligandrum produces hydrolytic enzymes and has the ability to utilize carbohydrates present in sclerotia (Madsen and de Neergaard 1999). Trichoderma virens is an aggressive mycoparasite of many plant pathogen (Howell 2006).

The plant pathogen and mycoparasite are characterized on the basis of the mode of nutrition. Fungus secrete bioactive molecules such as small peptide effectors, enzymes and secondary metabolites which facilitate colonization and contribute to both symbiotic and pathogenic relationships. The mycoparasitic relation based on mode of nutrition may be of following type:

  • Necrotrophic
  • Biotrophic

The necrotrophic and biotrophic mycoparasitism can be classified on the basis of the host-parasite interface as contact necrotrophs, invasive necrotroph, haustorial biotrophs, intracellular biotrophs and fusion biotrophs depending on the relationship (Jeffries 1995).

Necrotrophic: Necrotrophic mycoparasite, the fungus invades and kill their fungal prey followed by feeding on the dead cell content. Necrotroph have wide host range comprising of fungal plant pathogen and lack specialized infection structure. The antagonistic activity of necrotrophic mycoparasite is marked with the production of antibiotic, toxins and hydrolytic enzyme in proportion that causes the death of their host (Viterbo et al., 2007). Trichoderma as well as Clonostachys rosea mycoparasite overgrow and kill their fungal prey by using infection structure and by producing lytic enzymes and toxic metabolite (Karlsson et al., 2017).

Biotrophic:  Invades and feed on living cell.  Biotrophic pathogens derive nutrients from living cells and therefore must maintain host viability. Biotrophic mycoparasite have a more restricted host range and produce specialized structure to absorb nutrient from their host. Verticillium biguttatum  a biotrophic mycoparasite can grow on Rhizoctonia solani. From germinating spore it penetrated the hyphae of R.solani and formed haustorium without killing cell ( Van Den Boogert and Deacon 1994). Gliocephalis hyaline is a biotrophic contact parasite of Fusarium species. The fungus may penetrate the cells but has no apparent deleterious effect (Jacob et al., 2005).

There are some fungal species that may have both type of nutrition mode are referred to as hemibiotrophs, initially the fungal pathogen grows as a biotroph and at later stage becomes a necrotroph.  After initial biotrophic phase the hemibiotrophs like Colletotrichum lindemuthianum switch to destructive necrotrophic phase (González et al., 2015). These infection hyphae are surrounded by the host plant plasma membrane. Extra-haustorial membrane of haustoria differs biochemically and structurally from the normal membrane. An interfacial matrix separates haustoria and intracellular hyphae from the invaginated membrane and this seems to be characteristic of biotrophic interactions (Perfect and Green 2001). Upon the switch to necrotrophic growth the host plasma membrane surrounding the hyphae disintegrates and parasitic growth continues with narrower unsheathed hyphae. It therefore seems likely that this zone of separation plays an important role in the maintenance of the biotrophic lifestyle (Voegele and Mendgen 2003).

Biotrophic and hemibiotrophic fungi are successful groups of plant pathogen and most of these include rust fungi and powdery mildew (Koeck et al., 2011). Hyperparasitism is where parasite themselves are infected with parasite. Cucumber powdery mildew can be controlled by a mycoparasite Verticillium lecanii (Verhaar and Hijwegen 1994).  Soil fungi have the potential to control plant pathogen through mycoparasitic mechanism.

References:

Chet, I., Harman, G. E. and Baker, R. 1981 Trichoderma hamatum: Its Hyphal Interactions with Rhizoctonia solani and Pythium spp. Microb.  Ecol.  7(1): 29–38

doi: 10.1007/BF02010476

Davanlou, M., Madsen, A. M., Madsen, C. H. and Hockenhull, J. 1999 Parasitism of macroconidia, chlamydospores and hyphae of Fusarium culmorum by mycoparasitic Pythium species. Plant Pathol.   48: 352–359

De Marco, J. L., Valadares, M. C. and  Felix, C. R. 2003  Production of Hydrolytic Enzymes by Trichoderma Isolates with Antagonistic Activity Against Crinipellis perniciosa, the Causal Agent of Witches’ Broom of Cocoa. Braz. J.  Microbiol. 34: 33–38

González, A. M., Yuste-Lisbona,   F.  J., Rodiño,   A. P., De Ron, A. M., Capel, C., García-Alcázar, M., Lozano, R. and Santalla, M.  2015 Uncovering the Genetic Architecture of Colletotrichum lindemuthianum resistance through QTL mapping and epistatic interaction analysis in common bean. Front. Plant Sci. 6: 141

doi:  10.3389/fpls.2015.00141

Haran, S., Schickler, H. and  Chet, I. 1996  Molecular Mechanisms of Lytic Enzymes Involved in the Biocontrol Activity of Trichoderma harzianum. Microbiol.  142: 2321–2331

doi: 10.1099/00221287-142-9-2321

Howell, C. R. 2006 Understanding the Mechanisms Employed by Trichoderma virens to Effect Biological Control of Cotton Diseases. Phytopathol. 96 (2): 178 – 180

doi: 10.1094/PHYTO-96-0178

Inbar, J. and Chet, I. 1994 A Newly Isolated Lectin from the Plant Pathogenic Fungus Sclerotium rolfsii: Purification, Characterization and Role in Mycoparasitism. Microbiol.  140: 651–657

doi: 10.1099/00221287-140-3-651

Jacob, K., Holtzman, K. and Seifert, K. A. 2005  Morphology, Phylogeny and Biology of Gliocephalis hyalina, a Biotrophic Contact Mycoparasite of Fusarium species. Mycologia 97(1): 111-120

doi.org/10.1080/15572536.2006.11832844

Jeffries, P. 1995 Biology and Ecology of Mycoparasitism. Canadian J. Bot. 73(S1): 1284-1290

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Karlsson, M., Atanasova, L., Jensen, D. F. and Zeilinger, S. 2017 Necrotrophic Mycoparasites and Their Genomes. Microbiol Spectr. 5(2)

doi: 10.1128/microbiolspec.FUNK-0016-2016

Koeck, M., Hardham, A. R. and  Dodds, P. N. 2011 The Role of Effectors of Biotrophic and Hemibiotrophic Fungi In Infection. Cell Microbiol. 13(12):1849-57

doi: 10.1111/j.1462-5822.2011.01665.x

Madsen, A. M. and de Neergaard, E. 1999 Interactions Between the Mycoparasite Pythium oligandrum and Sclerotia of the Plant Pathogen Sclerotinia sclerotiorum. European J. Plant Pathol.  105(8):  761–768

Perfect, S. E. and Green, J. R. 2001 Infection Structures of Biotrophic and Hemibiotrophic Fungal Plant Pathogens.  Mol. Plant Pathol.  2(2): 101–108

Van den Boogert, P. H. J. F. and Deacon, J. W.  1994 Biotrophic Mycoparasitism by Verticillum biguttatum on Rhizoctonia solani. European J.  Plant Pathol.   100(2):  137–156

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Vázquez-Garcidueñas, S., Leal-Morales, C. A. and Herrera-Estrella, A. 1998 Analysis of the β-1, 3-Glucanolytic System of the Biocontrol Agent Trichoderma harzianum. Appl. Environ. Microbiol.  64(4): 1442–1446

Voegele, R. T. and Mendgen, K. 2003 Rust Haustoria: Nutrient Uptake and Beyond. New

Phytologist 159:  93-100.

Viterbo,A., Inbar, J.,  Hadar,Y. and Chet, I.  2007  Plant Disease Biocontrol and Induced Resistance via Fungal Mycoparasites in “Environmental and Microbial Relationships” Kubicek, C. and  Druzhinina, I. (eds). The Mycota, Vol 4. Springer, Berlin, Heidelberg. Pp: 127 – 146

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Verhaar M.A., Hijwegen T. (1994) Biological Control of Cucumber Powdery Mildew by Mycoparasites. In: Plant Production on the Threshold of a New Century. Struik P.C., Vredenberg W.J., Renkema J.A. and  Parlevliet J.E. (eds) Developments in Plant and Soil Sciences, vol 61. Springer, Dordrecht pp : 373 – 374

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