Chapter 42 : Mycoparasitism

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Mycoparasitism, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555816636/9781555814731_Chap42-1.gif /docserver/preview/fulltext/10.1128/9781555816636/9781555814731_Chap42-2.gif


Mycoparasitism is considered a major contributor to fungus-fungus antagonism. The necrotrophs, primarily species, have a wider host range and less-specific mode of action, and perhaps for this reason more field and greenhouse trials have made use of these. species are focused in this chapter, because they have been the focus of the most work at the molecular and cellular levels. The interaction of with soilborne pathogenic fungi is an excellent example of necrotrophic mycoparasitism. Drastic reduction of intracellular cyclic AMP (cAMP) by knockout of adenylate cyclase leads to slow growth and loss of mycoparasitism in . In , mutants in the ortholog of the same mitogen-activated protein kinase (MAPK) gene, , showed increased coiling but reduced mycoparasitism in confrontation assays. A potentiation in the gene expression enables -treated plants to be more resistant to subsequent pathogen infection. Chytrids parasitizing vesicular arbuscular mycorrhizae were found in the fossil record of the Rhynie Chert, dating to more than 400 million years ago. There are theories that mycorrhizae themselves might have evolved from biotrophic fungal parasites of plants. Major features such as detection of the host, signal transduction, altered transcriptional patterns, and secretion of enzymes are likely to be shared, and this has provided working hypotheses to guide studies of mycoparasitism. Molecular mechanisms and genes manipulated to optimize biocontrol will be different for each type of interaction and for each niche within the complex web of fungus-fungus and fungus-root interactions.

Citation: Viterbo A, Horwitz B. 2010. Mycoparasitism, p 676-693. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch42
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of FIGURE 1

Basic mechanisms of antagonistic fungus-fungus interactions. (A) Antibiosis: culture filtrate from inhibits germination of conidia. Shown are culture filtrates from grown on 2% glucose (left) and on 0.5% colloidal chitin (right). Growth of on chitin induces production of soluble antagonistic factors, which could be enzymes or small metabolites. (Reprinted from , with permission of Blackwell Publishing Ltd.) (B) Necrotrophic mycoparasitic interactions: coiling of the mycoparasite around the host, shown here, is followed by destruction of the host. Upper panel, on (from ); lower panel, hyphae interacting with f. sp. . (Reprinted with permission from ) (C) Parasitism of sclerotia: an important interaction for biocontrol of soilborne disease. Upper four panels, SEM images (reprinted from Mukherjee et al., 1995b, with permission of Blackwell Publishing Ltd.). Lower two panels, fluorescence of GFP-expressing mycelia; fluorescent mycelia are indicated by arrows (reprinted from , with permission from Elsevier). (D) A biotrophic interaction: the parasite forms haustoria within the host cells, as in biotrophic fungus-plant interactions ( ). Image reprinted from ) (Fig. 12-1), courtesy of Jim Deacon, The University of Edinburgh.

Citation: Viterbo A, Horwitz B. 2010. Mycoparasitism, p 676-693. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch42
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2

Image of holes in host cell walls left by , evidence of digestion by secreted enzymes. (Reprinted with permission from .)

Citation: Viterbo A, Horwitz B. 2010. Mycoparasitism, p 676-693. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch42
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3

Modulation of mycoparasite gene expression by host-derived signals. Expression of chit36:GFP in a transgenic line (T) induced by interaction with (Rs). was grown on a dialysis membrane on minimal medium for 2 days and then transferred for 24 h onto a clean plate (panel 1); a plate where was previously grown for 2 days (panel 2); or a 2-day-old culture of (panel 3). (Reprinted from , with permission of Springer Science and Business Media.)

Citation: Viterbo A, Horwitz B. 2010. Mycoparasitism, p 676-693. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch42
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4

A model for how host signals are produced. Action of hydrolytic enzymes secreted by the mycoparasite releases diffusible products, and secondary metabolites of fungal origin (for example, 6-pentyl-2H-pyran-2-on3). These signals may, in turn, program the development of the mycoparasite. (Reprinted from , with permission from Elsevier.)

Citation: Viterbo A, Horwitz B. 2010. Mycoparasitism, p 676-693. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch42
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 5

Interactions with plant roots. (A) Left, interaction between (hypha indicated in SEM image by the arrow) and cucumber root. (Reprinted with permission from .) Right, interaction between tomato root and expressing GFP (fluorescent hyphae indicated by arrow). (Reprinted with permission from .) (B) Consequence of -root interactions: induction of systemic resistance in the plant. Bioassay for induced resistance in maize seedlings against . Left, symptoms on leaves of maize seedlings grown from untreated (NT) seeds, or seed treated with knockout strains (KO25 and KO46), wild-type strain (WT), or overexpression strains (OE38 and OE39) of . Lesions (indicated, for example, by black arrows in left-most leaf photo) appear dark in this grayscale image; see ) for original color image from which this figure was reprinted with permission. The gene disrupted or overexpressed in these strains encodes the secreted elicitor protein Sm1. Right, quantitative analysis of lesion size for the experiment shown in the left panel; different letters indicate significant differences ( ).

Citation: Viterbo A, Horwitz B. 2010. Mycoparasitism, p 676-693. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch42
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Abo-Foul, S.,, V. Raskin,, A. Sztejnberg, and, J. Marder. 1996. Disruption of chlorophyll organization and function in powdery mildew-diseased cucumber leaves and its control by the hyperparasite Ampelomyces quisqualis. Phytopathology 86: 195199.
2. Aguirre, J.,, M. Rios-Momberg,, D. Hewitt,and, W. Hansberg. 2005. Reactive oxygen species and development in microbial eukaryotes. Trends Microbiol. 13: 111118.
3. Alfano, G.,, M. L. Lewis Ivey,, C. Cakir,, J. I. B. Bos,, S. A. Miller,, L. V. Madden,, S. Kamoun,and, H. A. J. Hoitink. 2007. Systemic modulation of gene expression in tomato by Trichoderma hamatum 382. Phytopathology 97: 429437.
4. Andrews, J. H. 1992. Biological control in the phyllosphere. Annu. Rev. Phytopathol. 30: 603635.
5. Assante, G.,, D. Maffi,, M. Saracchi,, G. Farina,, S. Moricca,and, A. Ragazzi. 2004. Histological studies on the mycoparasitism of Cladosporium tenuissimum on urediniospores of Uromyces appendiculatus. Mycol. Res. 108: 170182.
6. Bagga, S.,, G. Hu,, S. E. Screen,and, R. J. St Leger. 2004. Reconstructing the diversification of subtilisins in the pathogenic fungus Metarhizium anisopliae. Gene 324: 159169.
7. Barnett, E. A.,and, W. A. Ayers. 1981. Nutritional and environmental factors affecting growth and sporulation of Sporidesmium sclerotivorum. Can. J. Microbiol. 27: 685691.
8. Barnett, H.,and, F. Binder. 1973. The fungal host-parasite relationship. Annu. Rev. Phytopathol. 11: 273292.
9. Bayon, C.,, Z. W. Yuan,, C. Ruiz,, M. Liesebach,and, M. H. Pei. 2006. Genetic diversity in the mycoparasite Sphaerellopsis filum inferred from AFLP analysis and ITS-5.8S sequences. Mycol. Res. 110: 12001206.
10. Benhamou, N.,and, I. Chet. 1993. Hyphal interactions between Trichoderma harzianum and Rhizoctonia solani: ultra-structure and cytochemistry of the antagonistic process. Phytopathology 83: 10621071.
11. Benhamou, N.,, P. Rey,, M. Chérif,, J. Hockenhull,and, Y. Tirilly. 1997. Treatment with the mycoparasite Pythium oligandrum triggers induction of defense-related reactions in tomato roots when challenged with Fusarium oxysporum f. sp. radicis-lycopersici. Phytopathology 87: 108122.
12. Benhamou, N.,, P. Rey,, K. Pichard,and, Y. Tirilly. 1999. Ultrastructural and cytochemical aspects of the interaction between the mycoparasite Pythium oligandrum and soilborne plant pathogens. Phytopathology 89: 506517.
13. Benitez, T.,, A. M. Rincon,, M. C. Limon,and, A. C. Codon. 2004. Biocontrol mechanisms of Trichoderma strains. Int. Microbiol. 7: 249260.
14. Bernardo, D.,, A. P. Cabo,, M. Novaes-Ledieu, and, C. G. Mendoza. 2004. Verticillium disease or “dry bubble” of cultivated mushrooms: the Agaricus bisporus lectin recognizes and binds the Verticillium fungicola cell wall glucogalactomannan. Can. J. Microbiol. 50: 729735.
15. Brozova, J. 2002. Exploitation of the mycoparasitic fungus Pythium oligandrum in plant protection. Plant Prot. Sci. 38: 2935.
16. Brunner, K.,, C. K. Peterbauer,, R. L. Mach,, M. Lorito,, S. Zeilinger,and, C. P. Kubicek. 2003. The Nag1 N-acetylglucosaminidase of Trichoderma atroviride is essential for chitinase induction by chitin and of major relevance to bio-control. Curr. Genet. 43: 289295.
17. Brunner, K.,, M. Omann,, M. E. Pucher,, M. Delic,, S. M. Lehner,, P. Domnanich,, K. Kratochwill,, I. Druzhinina,, D. Denk,and, S. Zeilinger. 2008. Trichoderma G protein-coupled receptors: functional characterisation of a cAMP receptor-like protein from Trichoderma atroviride. Curr. Genet. 54: 283299.
18. Brunner, K.,, S. Zeilinger,, R. Ciliento,, S. L. Woo,, M. Lorito,, C. P. Kubicek,and, R. L. Mach. 2005. Improvement of the fungal biocontrol agent Trichoderma atroviride to enhance both antagonism and induction of plant systemic disease resistance. Appl. Environ. Microbiol. 71: 39593965.
19. Cantarel, B. L.,, P. M. Coutinho,, C. Rancurel,, T. Bernard,, V. Lombard,and, B. Henrissat. 2009. The carbohydrate-active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37: D233D238.
20. Carpenter, M. A.,, H. J. Ridgway,, A. M. Stringer,, A. J. Hay,and, A. Stewart. 2008. Characterisation of a Trichoderma hamatum monooxygenase gene involved in antagonistic activity against fungal plant pathogens. Curr. Genet. 53: 193205.
21. Carpenter, M. A.,, A. Stewart,and, H. J. Ridgway. 2005. Identification of novel Trichoderma hamatum genes expressed during mycoparasitism using subtractive hybridisation. FEMS Microbiol. Lett. 251: 105112.
22. Carsolio, C.,, N. Benhamou,, S. Haran,, C. Cortes,, A. Gutierrez,, I. Chet,and, A. Herrera-Estrella. 1999. Role of the Trichoderma harzianum endochitinase gene, ech42, in mycoparasitism. Appl. Environ. Microbiol. 65: 929935.
23. Carsolio, C.,, A. Gutierrez,, B. Jimenez,, M. Van Montagu, and, A. Herrera-Estrella. 1994. Characterization of ech-42, a Trichoderma harzianum endochitinase gene expressed during mycoparasitism. Proc. Natl. Acad. Sci. USA 91: 1090310907.
24. Casas-Flores, S.,, M. Rios-Momberg,, T. Rosales-Saavedra,, P. Martinez-Hernandez,, V. Olmedo-Monfil, and, A. Herrera-Estrella. 2006. Cross talk between a fungal blue-light perception system and the cyclic AMP signaling pathway. Eukaryot. Cell 5: 499506.
25. Chacon, M. R.,, O. Rodriguez-Galan,, T. Benitez,, S. Sousa,, M. Rey,, A. Llobell,and, J. Delgado-Jarana. 2007. Microscopic and transcriptome analyses of early colonization of tomato roots by Trichoderma harzianum. Int. Microbiol. 10: 1927.
26. Chet, I. 1993. Biotechnology in Plant Disease Control. Wiley-Liss, New York, NY.
27. Chet, I. 1987. Innovative Approaches to Plant Disease Control. Wiley, New York, NY.
28. Chet, I.,and, J. Inbar. 1994. Biological control of fungal pathogens. Appl. Biochem. Biotechnol. 48: 3743.
29. Chet, I.,and, R. Baker. 1981. Isolation and biocontrol potential of Trichoderma hamatum from soil naturally suppressive to Rhizoctonia solani. Phytopathology 71: 286290.
30. Cook, R.,and, K. Baker. 1983. The Nature and Practice of Biological Control of Plant Pathogens. The American Phytopathological Society, St Paul, MN.
31. Cooper, R. M.,, D. Longman,, A. Campbell,, M. Henry,and, P. E. Lees. 1988. Enzymatic adaptation of cereal pathogens to the monocotyledonous primary wall. Physiol. Mol. Plant Pathol. 32: 3348.
32. Cortes, C.,, A. Gutierrez,, V. Olmedo,, J. Inbar,, I. Chet,and, A. Herrera-Estrella. 1998. The expression of genes involved in parasitism by Trichoderma harzianum is triggered by a diffusible factor. Mol. Gen. Genet. 260: 218225.
33. Deacon, J. W. 2005. Fungal Biology. Wiley, New York, NY.
34. DeBach, P.,and, D. Rosen. 1991. Biological Control by Natural Enemies, 2nd ed. Cambridge University Press, Cambridge, England.
35. de la Cruz, J.,, J. A. Pintor-Toro,, T. Benitez,and, A. Llobell. 1995. Purification and characterization of an endo-beta-1,6-glucanase from Trichoderma harzianum that is related to its mycoparasitism. J. Bacteriol. 177: 18641871.
36. Delgado-Jarana, J.,, S. Sousa,, F. Gonzalez,, M. Rey,and, A. Llo-bell. 2006. ThHog1 controls the hyperosmotic stress response in Trichoderma harzianum. Microbiology 152: 16871700.
37. Del Rio, L., C. Martinson,and, X. Yang. 2002. Biological control of Sclerotinia stem rot of soybean with Sporidesmium sclerotivorum. Plant Dis. 86: 9991004.
38. Djonovic, S.,, W. A. Vargas,, M. V. Kolomiets,, M. Horn-deski,, A. Wiest,and, C. M. Kenerley. 2007. A proteinaceous elicitor Sm1 from the beneficial fungus Trichoderma virens is required for induced systemic resistance in maize. Plant Physiol. 145: 875889.
39. Egan, M. J.,, Z. Y. Wang,, M. A. Jones,, N. Smirnoff,and, N. J. Talbot. 2007. Generation of reactive oxygen species by fungal NADPH oxidases is required for rice blast disease. Proc. Natl. Acad. Sci. USA 104: 1177211777.
40. Elad, Y.,, R. Barak,and, I. Chet. 1983a. Possible role of lectins in mycoparasitism. J. Bacteriol. 154: 14311435.
41. Elad, Y.,, I. Chet,, P. Boyle,and, Y. Henis. 1983b. Parasitism of Trichoderma spp. on Rhizoctonia solani and Sclerotium rolfsii—scanning electron microscopy and fluorescence microscopy. Phytopathology 73: 8588.
42. Elad, Y.,, R. Lisfshitz,and, R. Baker. 1985. Enzymatic activity of the mycoparasite Pythium nunn during interaction with host and non-host fungi. Physiol. Plant Pathol. 27: 131148.
43. El Bassam, S.,, N. Benhamou,and, O. Carisse. 2002. The role of melanin in the antagonistic interaction between the apple scab pathogen Venturia inaequalis and Microsphaeropsis ochracea. Can. J. Microbiol. 48: 349358.
44. el-Gogary, S.,, A. Leite,, O. Crivellaro,, D. E. Eveleigh,and, H. el-Dorry. 1989. Mechanism by which cellulose triggers cellobiohydrolase I gene expression in Trichoderma reesei. Proc. Natl. Acad. Sci. USA 86: 61386141.
45. Fahima, T.,and, Y. Henis. 1990. Interaction between pathogen, host and biocontrol agent: multiplication of Trichoderma hamatum and Talaromyces flavus on roots of diseased and healthy hosts, p. 165. In D. Horny (ed.), Biological Control of Soil-Borne Pathogens. CAB International, Wallingford, United Kingdom.
46. Falk, S. P.,, D. M. Gadoury,, R. C. Pearson,and, R. C. Seem. 1995. Partial control of grape powdery mildew by the myco-parasite Ampelomyces quisqualis. Plant Dis. 79: 483490.
47. Flores, A.,, I. Chet,and, A. Herrera-Estrella. 1997. Improved biocontrol activity of Trichoderma harzianum by over-expression of the proteinase-encoding gene prb1. Curr. Genet. 31: 3037.
48. Fravel, D. R.,, W. J. Connick, Jr.,, C. C. Grimm,and, S. W. Lloyd. 2002. Volatile compounds emitted by sclerotia of Sclerotinia minor, Sclerotinia sclerotiorum, and Sclerotium rolfsii. J. Agric. Food Chem. 50: 37613764.
49. Galagan, J. E.,, S. E. Calvo,, K. A. Borkovich,, E. U. Selker,, N. D. Read,, D. Jaffe,, W. FitzHugh,, L. J. Ma,, S. Smirnov,, S. Purcell,, B. Rehman,, T. Elkins,, R. Engels,, S. Wang,, C. B. Nielsen,, J. Butler,, M. Endrizzi,, D. Qui,, P. Ianakiev,, D. Bell-Pedersen,, M. A. Nelson,, M. Werner-Washburne,, C. P. Selitrennikoff,, J. A. Kinsey,, E. L. Braun,, A. Zelter,, U. Schulte,, G. O. Kothe,, G. Jedd,, W. Mewes,, C. Staben,, E. Marcotte,, D. Greenberg,, A. Roy,, K. Foley,, J. Naylor,, N. Stange-Thomann,, R. Barrett,, S. Gnerre,, M. Kamal,, M. Kamvysselis,, E. Mauceli,, C. Bielke,, S. Rudd,, D. Frishman,, S. Krystofova,, C. Rasmussen,, R. L. Metzenberg,, D. D. Perkins,, S. Kroken,, C. Cogoni,, G. Macino,, D. Catcheside,, W. Li,, R. J. Pratt,, S. A. Osmani,, C. P. DeSouza,, L. Glass,, M. J. Orbach,, J. A. Berglund,, R. Voelker,, O. Yarden,, M. Plamann,, S. Seiler,, J. Dunlap,, A. Radford,, R. Aramayo,, D. O. Natvig,, L. A. Alex,, G. Mannhaupt,, D. J. Ebbole,, M. Freitag,, I. Paulsen,, M. S. Sachs,, E. S. Lander,, C. Nusbaum,and, B. Birren. 2003. The genome sequence of the filamentous fungus Neurospora crassa. Nature 422: 859868.
50. Gao, K.,, X. Liu,, Z. Kang,and, K. Mendgen. 2005. Mycoparasitism of Rhizoctonia solani by endophytic Chaetomium spirale ND35: ultrastructure and cytochemistry of the interaction. J. Phytopathol. 153: 280290.
51. Geremia, R. A.,, G. H. Goldman,, D. Jacobs,, W. Ardiles,, S. B. Vila,, M. Van Montagu, and, A. Herrera-Estrella. 1993. Molecular characterization of the proteinase-encoding gene, prb1, related to mycoparasitism by Trichoderma harzianum. Mol. Microbiol. 8: 603613.
52. Giesbert, S.,, T. Schurg,, S. Scheele,and, P. Tudzynski. 2008. The NADPH oxidase Cpnox1 is required for full pathogenicity of the ergot fungus Claviceps purpurea. Mol. Plant Pathol. 9: 317327.
53. Govrin, E. M.,and, A. Levine. 2000. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr. Biol. 10: 751757.
54. Harman, G. E.,, C. R. Howell,, A. Viterbo,, I. Chet,and, M. Lorito. 2004. Trichoderma species—opportunistic, avirulent plant symbionts. Nat. Rev. Microbiol. 2: 4356.
55. Harman, G. E.,and, C. P. Kubicek. 1998. Enzymes, Biological Control and Commercial Applications, vol. 2. Taylor and Francis, Bristol, PA.
56. Hass, H.,, T. N. Taylor,and, W. Remy. 1994. Fungi from the lower Devonian Rhynie chert—mycoparasitism. Am. J. Bot. 81: 2937.
57. Herrera-Estrella, A.,and, I. Chet. 1998. Biocontrol of bacteria and phytopathogenic fungi, p. 263–282. In A. Altman (ed.), Agricultural Biotechnology. Marcel Dekker, Inc., New York, NY.
58. Hoopen, G. M.,, R. Rees,, P. Aisa,, T. Stirrup,and, U. Krauss. 2003. Population dynamics of epiphytic mycoparasites of the genera Clonostachys and Fusarium for the control of black pod ( Phytophthora palmivora) and moniliasis ( Moniliophthora roreri) on cocoa ( Theobroma cacao). Mycol. Res. 107: 587596.
59. Howell, C. 1998. The role of antibiosis in biocontrol, p. 173–184. In G. Harmanand, C. Kubicek (ed.), Trichoderma & Gliocladium, vol. 2. Taylor & Francis, Padstow, United Kingdom.
60. Howell, C.,, R. Stipanovic,and, R. Lumsden. 1993. Antibiotic production by strains of Gliocladium virens and its relation to biocontrol of cotton seedling diseases. Biocontrol Sci. Technol. 3: 435441.
61. Igbaria, A.,, S. Lev,, M. S. Rose,, B. N. Lee,, R. Hadar,, O. Degani,and, B. A. Horwitz. 2008. Distinct and combined roles of the MAP kinases of Cochliobolus heterostrophus in virulence and stress responses. Mol. Plant-Microbe Interact. 21: 769780.
62. Inbar, J.,and, I. Chet. 1992. Biomimics of fungal cell-cell recognition by use of lectin-coated nylon fibers. J. Bacteriol. 174: 10551059.
63. Inbar, J.,and, I. Chet. 1994. A newly isolated lectin from the plant pathogenic fungus Sclerotium rolfsii: purification, characterization and role in mycoparasitism. Microbiology 140: 651657.
64. Jacobs, K.,, K. Holtzman,and, K. A. Seifert. 2005. Morphology, phylogeny and biology of Gliocephalis hyalina, a biotrophic contact mycoparasite of Fusarium species. Mycologia 97: 111120.
65. Joshi, B. K.,, J. B. Gloer,and, D. T. Wicklow. 1999. New verticillin and glisoprenin analogues from Gliocladium catenulatum, a mycoparasite of Aspergillus flavus sclerotia. J. Nat. Prod. 62: 730733.
66. Kavkova, M.,and, V. Curn. 2005. Paecilomyces fumosoroseus (Deuteromycotina: Hyphomycetes) as a potential mycopara-site on Sphaerotheca fuliginea (Ascomycotina: Erysiphales). Mycopathologia 159: 5363.
67. Kawasaki, L.,, O. Sanchez,, K. Shiozaki,and, J. Aguirre. 2002. SakA MAP kinase is involved in stress signal transduction, sexual development and spore viability in Aspergillus nidulans. Mol. Microbiol. 45: 11531163.
68. Kays, A. M.,, P. S. Rowley,, R. A. Baasiri,and, K. A. Borkovich. 2000. Regulation of conidiation and adenylyl cyclase levels by the Gα protein GNA-3 in Neurospora crassa. Mol. Cell. Biol. 20: 76937705.
69. Kellner, M., A. Burmester,, A. Wostemeyer,and, J. Woste-meyer. 1993. Transfer of genetic information from the mycoparasite Parasitella parasitica to its host Absidia glauca. Curr. Genet. 23: 334337.
70. Kim, D. J.,, J. M. Baek,, P. Uribe,, C. M. Kenerley,and, D. R. Cook. 2002. Cloning and characterization of multiple glycosyl hydrolase genes from Trichoderma virens. Curr. Genet. 40: 374384.
71. Klemsdal, S. S.,, J. L. Clarke,, I. A. Hoell,, V. G. Eijsink,and, M. B. Brurberg. 2006. Molecular cloning, characterization, and expression studies of a novel chitinase gene (ech30) from the mycoparasite Trichoderma atroviride strain P1. FEMS Microbiol. Lett. 256: 282289.
72. Kojima, K.,, Y. Takano,, A. Yoshimi,, C. Tanaka,, T. Kikuchi,and, T. Okuno. 2004. Fungicide activity through activation of a fungal signalling pathway. Mol. Microbiol. 53: 17851796.
73. Kulkarni, R. D.,, M. R. Thon,, H. Pan,and, R. A. Dean. 2005. Novel G-protein-coupled receptor-like proteins in the plant pathogenic fungus Magnaporthe grisea. Genome Biol. 6: R24.
74. Kullnig, C.,, R. L. Mach,, M. Lorito,and, C. P. Kubicek. 2000. Enzyme diffusion from Trichoderma atroviride (= T. harzianum P1) to Rhizoctonia solani is a prerequisite for triggering of Trichoderma ech42 gene expression before myco-parasitic contact. Appl. Environ. Microbiol. 66: 22322234.
75. Lafon, A.,, K. H. Han,, J. A. Seo,, J. H. Yu,and, C. d’Enfert. 2006. G-protein and cAMP-mediated signaling in aspergilli: a genomic perspective. Fungal Genet. Biol. 43: 490502.
76. Lin, C.,, J. Yang,, H. Sun,, X. Huang,, R. Wang,and, K. Q. Zhang. 2007. Purification and characterization of a beta-1,3-glucanase from the novel mycoparasite Periconia byssoides. Biotechnol. Lett. 29: 617622.
77. Liu, P. G.,and, Q. Yang. 2005. Identification of genes with a biocontrol function in Trichoderma harzianum mycelium using the expressed sequence tag approach. Res. Microbiol. 156: 416423.
78. Lora, J. M.,, J. De La Cruz,, T. Benitez,, A. Llobell,and, J. A. Pintor-Toro. 1995. Molecular characterization and heterologous expression of an endo-b-1,6-glucanase gene from the mycoparasitic fungus Trichoderma harzianum. Mol. Gen. Genet. 247: 639645.
79. Lorito, M.,, V. Farkas,, S. Rebuffat,, B. Bodo,and, C. P. Kubicek. 1996. Cell wall synthesis is a major target of mycoparasitic antagonism by Trichoderma harzianum. J. Bacteriol. 178: 63826385.
80. Mach, R. L.,, C. K. Peterbauer,, K. Payer,, S. Jaksits,, S. L. Woo,, S. Zeilinger,, C. M. Kullnig,, M. Lorito,and, C. P. Kubicek. 1999. Expression of two major chitinase genes of Trichoderma atroviride ( T. harzianum P1) is triggered by different regulatory signals. Appl. Environ. Microbiol. 65: 18581863.
81. Manocha, M. 1990. Cell-cell interaction in fungi. J. Plant Dis. Prot. 97: 655669.
82. Manocha, M. 1981. Host specificity and mechanism of resistance in a mycoparasitic system. Physiol. Plant Pathol. 18: 257267.
83. Manocha, M.,, D. Xiong,and, V. Govindsamy. 1997. Isolation and partial characterization of a complementary protein from the mycoparasite Piptocephalis virginiana that specifically binds to two glycoproteins at the host cell surface. Can. J. Microbiol. 43: 625632.
84. Marahiel, M. A. 1997. Protein templates for the biosynthesis of peptide antibiotics. Chem. Biol. 4: 561567.
85. Marra, R.,, P. Ambrosino,, V. Carbone,, F. Vinale,, S. L. Woo,, M. Ruocco,, R. Ciliento,, S. Lanzuise,, S. Ferraioli,, I. Soriente,, S. Gigante,, D. Turra,, V. Fogliano,, F. Scala,and, M. Lorito. 2006. Study of the three-way interaction between Trichoderma atroviride, plant and fungal pathogens by using a proteomic approach. Curr. Genet. 50: 307321.
86. Martinez, D.,, R. M. Berka,, B. Henrissat,, M. Saloheimo,, M. Arvas,, S. E. Baker,, J. Chapman,, O. Chertkov,, P. M. Coutinho,, D. Cullen,, E. G. Danchin,, I. V. Grigoriev,, P. Harris,, M. Jackson,, C. P. Kubicek,, C. S. Han,, I. Ho,, L. F. Larrondo,, A. L. de Leon,, J. K. Magnuson,, S. Merino,, M. Misra,, B. Nelson,, N. Putnam,, B. Robbertse,, A. A. Salamov,, M. Schmoll,, A. Terry,, N. Thayer,, A. Wester-holm-Parvinen,, C. L. Schoch,, J. Yao,, R. Barbote,, M. A. Nelson,, C. Detter,, D. Bruce,, C. R. Kuske,, G. Xie,, P. Richardson,, D. S. Rokhsar,, S. M. Lucas,, E. M. Rubin,, N. Dunn-Coleman,, M. Ward,and, T. S. Brettin. 2008. Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat. Biotechnol. 26: 553560.
87. Mathivanan, N.,, V. Kabilan,and, K. Murugesan. 1998. Purification, characterization, and antifungal activity of chitinase from Fusarium chlamydosporum, a mycoparasite to groundnut rust, Puccinia arachidis. Can. J. Microbiol. 44: 646651.
88. McQuilken, M. P.,and, J. Gemmell. 2004. Enzyme production by the mycoparasite Verticillium biguttatum against Rhizoctania solani. Mycopathologia 157: 201205.
89. McQuilken, M. P.,, J. Gemmell,, R. A. Hill,and, J. M. Whipps. 2003. Production of macrosphelide A by the mycoparasite Coniothyrium minitans. FEMS Microbiol. Lett. 219: 2731.
90. Mendoza-Mendoza, A.,, M. J. Pozo,, D. Grzegorski,, P. Martinez,, J. M. Garcia,, V. Olmedo-Monfil,, C. Cortes,, C. Kenerley,and, A. Herrera-Estrella. 2003. Enhanced biocontrol activity of Trichoderma through inactivation of a mitogen-activated protein kinase. Proc. Natl. Acad. Sci. USA 100: 1596515970.
91. Moreno-Mateos, M. A.,, J. Delgado-Jarana,, A. C. Codon,and, T. Benitez. 2007. pH and Pac1 control development and antifungal activity in Trichoderma harzianum. Fungal Genet. Biol. 44: 13551367.
92. Morissette, D. C.,, P. Seguin,and, S. H. Jabaji-Hare. 2006. Expression regulation of the endochitinase-encoding gene sechi44 from the mycoparasite Stachybotris elegans. Can. J. Microbiol. 52: 11031109.
93. Morissette, D. C.,, A. Dauch,, R. Beech,, L. Masson,, R. Brousseau,and, S. Jabaji-Hare. 2008. Isolation of mycoparasitic-related transcripts by SSH during interaction of the mycoparasite Stachybotrys elegans with its host Rhizoctonia solani. Curr. Genet. 53: 6780.
94. Mueller, O.,, R. Kahmann,, G. Aguilar,, B. Trejo-Aguilar,, A. Wu,and, R. P. de Vries. 2008. The secretome of the maize pathogen Ustilago maydis. Fungal Genet. Biol. 45(Suppl. 1): S63S70.
95. Mukherjee, M.,, B. A. Horwitz,, P. D. Sherkhane,, R. Hadar,and, P. K. Mukherjee. 2006. A secondary metabolite biosynthesis cluster in Trichoderma virens: evidence from analysis of genes underexpressed in a mutant defective in morphogenesis and antibiotic production. Curr. Genet. 50: 193202.
96. Mukherjee, M.,, P. K. Mukherjee,and, S. P. Kale. 2007. cAMP signalling is involved in growth, germination, mycoparasitism and secondary metabolism in Trichoderma virens. Microbiology 153: 17341742.
97. Mukherjee, P. K.,, J. Latha,, R. Hadar,and, B. A. Horwitz. 2003. TmkA, a mitogen-activated protein kinase of Trichoderma virens, is involved in biocontrol properties and repression of conidiation in the dark. Eukaryot. Cell 2: 446455.
98. Mukherjee, P. K.,, A. N. Mukhopadhyay,, D. K. Sarmah,and, S. M. Shreshtha. 1995. Comparative antagonistic properties of Gliocladium virens and Trichoderma harzianum on Sclerotium rolfsii and Rhizoctonia solani—its relevance to understanding the mechanisms of biocontrol. J. Phytopathol. 143: 275279.
99. Nelson, E. B. 2004. Microbial dynamics and interactions in the spermosphere. Annu. Rev. Phytopathol. 42: 271309.
100. Nischwitz, C.,, G. Newcombe,and, C. L. Anderson. 2005. Host specialization of the mycoparasite Eudarluca caricis and its evolutionary relationship to Ampelomyces. Mycol. Res. 109: 421428.
101. Olmedo-Monfil, V.,, A. Mendoza-Mendoza,, I. Gomez,, C. Cortes,and, A. Herrera-Estrella. 2002. Multiple environmental signals determine the transcriptional activation of the mycoparasitism related gene prb1 in Trichoderma atroviride. Mol. Genet. Genomics 267: 703712.
102. Omero, C.,, J. Inbar,, V. Rocha-Ramirez,, A. Herrera-Estrella,, I. Chet,and, B. A. Horwitz. 1999. G protein activators and cAMP promote mycoparasitic behaviour in Trichoderma harzianum. Mycol. Res. 103: 16371642.
103. Papavizas, G. 1985. Trichoderma and Gliocladium: biology, ecology and the potential for biocontrol. Annu. Rev. Phytopathol. 23: 2354.
104. Paul, B. 1999. Pythium periplocum, an aggressive mycoparasite of Botrytis cinerea causing the gray mould disease of grapevine. FEMS Microbiol. Lett. 181: 277280.
105. Pei, M. H.,, T. Hunter,, C. Ruiz,, C. Bayon,and, J. Harris. 2003. Quantitative inoculation of willow rust Melampsora larici-epitea with the mycoparasite Sphaerellopsis filum (teleomorph Eudarluca caricis). Mycol. Res. 107: 5763.
106. Picard, K.,, M. Ponchet,, J. P. Blein,, P. Rey,, Y. Tirilly,and, N. Benhamou. 2000. Oligandrin. A proteinaceous molecule produced by the mycoparasite Pythium oligandrum induces resistance to Phytophthora parasitica infection in tomato plants. Plant Physiol. 124: 379395.
107. Prados-Rosales, R. C.,, C. Serena,, J. Delgado-Jarana,, J. Guarro,and, A. Di Pietro. 2006. Distinct signalling pathways coordinately contribute to virulence of Fusarium oxysporum on mammalian hosts. Microbes Infect. 8: 28252831.
108. Reino, J.,, R. Guerrero,, R. Hernandez-Galan, and, I. Collado. 2008. Secondary metabolites from species of the biocontrol agent Trichoderma. Phytochem. Rev. 7: 89123.
109. Reithner, B.,, K. Brunner,, R. Schuhmacher,, I. Peissl,, V. Seidl,, R. Krska,and, S. Zeilinger. 2005. The G protein alpha subunit Tga1 of Trichoderma atroviride is involved in chitinase formation and differential production of antifungal metabolites. Fungal Genet. Biol. 42: 749760.
110. Reithner, B.,, R. Schuhmacher,, N. Stoppacher,, M. Pucher,, K. Brunner,and, S. Zeilinger. 2007. Signaling via the Trichoderma atroviride mitogen-activated protein kinase Tmk 1 differentially affects mycoparasitism and plant protection. Fungal Genet. Biol. 44: 11231133.
111. Remy, W.,, T. N. Taylor,, H. Hass,and, H. Kerp. 1994. Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc. Natl. Acad. Sci. USA 91: 1184111843.
112. Rey, P.,, G. Le Floch,, N. Benhamou,, M. I. Salermo,, E. Thuillier,and, Y. Tirilly. 2005. Interactions between the mycoparasite Pythium oligandrum and two types of sclerotia of plant-pathogenic fungi. Mycol. Res. 109: 779788.
113. Rocha-Ramirez, V.,, C. Omero,, I. Chet,, B. A. Horwitz,and, A. Herrera-Estrella. 2002. Trichoderma atroviride G-protein alpha-subunit gene tga1 is involved in mycoparasitic coiling and conidiation. Eukaryot. Cell 1: 594605.
114. Rogers, C. W.,, M. P. Challen,, J. R. Green,and, J. M. Whipps. 2004. Use of REMI and Agrobacterium-mediated transformation to identify pathogenicity mutants of the bio-control fungus, Coniothyrium minitans. FEMS Microbiol. Lett. 241: 207214.
115. Sarrocco, S.,, L. Mikkelsen,, M. Vergara,, D. F. Jensen,, M. Lubeck,and, G. Vannacci. 2006. Histopathological studies of sclerotia of phytopathogenic fungi parasitized by a GFP transformed Trichoderma virens antagonistic strain. Mycol. Res. 110: 179187.
116. Schirmbock, M.,, M. Lorito,, Y. L. Wang,, C. K. Hayes,, I. Arisan-Atac,, F. Scala,, G. E. Harman,and, C. P. Kubicek. 1994. Parallel formation and synergism of hydrolytic enzymes and peptaibol antibiotics, molecular mechanisms involved in the antagonistic action of Trichoderma harzianum against phytopathogenic fungi. Appl. Environ. Microbiol. 60: 43644370.
117. Schultze, K.,, C. Schimek,, J. Wostemeyer,and, A. Burmester. 2005. Sexuality and parasitism share common regulatory pathways in the fungus Parasitella parasitica. Gene 348: 3344.
118. Segmueller, N.,, U. Ellendorf,, B. Tudzynski,and, P. Tudzynski. 2007. BcSAK1, a stress-activated mitogen-activated protein kinase, is involved in vegetative differentiation and pathogenicity in Botrytis cinerea. Eukaryot. Cell 6: 211221.
119. Segmueller, N.,, L. Kokkelink,, S. Giesbert,, D. Odinius,, J. van Kan, and, P. Tudzynski. 2008. NADPH oxidases are involved in differentiation and pathogenicity in Botrytis cinerea. Mol. Plant-Microbe Interact. 21: 808819.
120. Seidl, V.,, B. Huemer,, B. Seiboth,and, C. P. Kubicek. 2005. A complete survey of Trichoderma chitinases reveals three distinct subgroups of family 18 chitinases. FEBS J. 272: 59235939.
121. Seidl, V.,, M. Schmoll,, B. Scherm,, V. Balmas,, B. Seiboth,, Q. Migheli,and, C. P. Kubicek. 2006. Antagonism of Pythium blight of zucchini by Hypocrea jecorina does not require cellulase gene expression but is improved by carbon catabolite derepression. FEMS Microbiol. Lett. 257: 145151.
122. Sestak, S.,and, V. Farkas. 1993. Metabolic regulation of endoglucanase synthesis in Trichoderma reesei: participation of cyclic AMP and glucose-6-phosphate. Can. J. Microbiol. 39: 342347.
123. Shoresh, M.,, I. Yedidia,and, I. Chet. 2005. Involvement of the jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. Phytopathology 95: 7684.
124. Silva, R. N.,, S. P. da Silva,, R. L. Brandao,and, C. J. Ulhoa. 2004. Regulation of N-acetyl-beta-D-glucosaminidase produced by Trichoderma harzianum: evidence that cAMP controls its expression. Res. Microbiol. 155: 667671.
125. Steyaert, J.,, H. J. Ridgway,, Y. Elad,and, A. Stewart. 2003. Genetic basis of mycoparasitism: a mechanism of biological control by species of Trichoderma. N. Z. J. Crop Hortic. Sci. 31: 281291.
126. Steyaert, J.,, A. Stewart,, M. Jaspers,, M. A. Carpenter,and, H. J. Ridgway. 2004. Co-expression of two genes, a chitinase ( chit42) and proteinase ( prb1), implicated in mycoparasitism by Trichoderma harzianum. Mycologia 96: 12451252.
127. St Leger, R. J.,, L. Joshi,and, D. W. Roberts. 1997. Adaptation of proteases and carbohydrates of saprophytic, phytopathogenic and entomopathogenic fungi to the requirements of their ecological niches. Microbiology 143(Pt. 6): 19831992.
128. Suarez, M. B.,, J. A. Vizcaino,, A. Llobell,and, E. Monte. 2007. Characterization of genes encoding novel peptidases in the biocontrol fungus Trichoderma harzianum CECT 2413 using the TrichoEST functional genomics approach. Curr. Genet. 51: 331342.
129. Sullivan, R. F.,and, J. F. White,, Jr. 2000. Phoma glomerata as a mycoparasite of powdery mildew. Appl. Environ. Microbiol. 66: 425427.
130. Takemoto, D.,, A. Tanaka,and, B. Scott. 2007. NADPH oxidases in fungi: diverse roles of reactive oxygen species in fungal cellular differentiation. Fungal Genet. Biol. 44: 10651076.
131. Tekaia, F.,and, J. P. Latge. 2005. Aspergillus fumigatus: saprophyte or pathogen? Curr. Opin. Microbiol. 8: 385392.
132. Tu, J. C. 1984. Mycoparasitism by Coniothyrium minitans and its effects on sclerotia germination. Phytopathol. Z. 109: 261268.
133. Tzean, S. S.,and, R. H. Esty. 1978. Schizophyllum commune Fr. as a destructive mycoparasite. Can. J. Microbiol. 24: 780784.
134. Van Den Boogert, P. H. J. F.,and, J. W. Deacon. 1994. Biotrophic mycoparasitism by Verticillium biguttatum on Rhizoctonia solani. Eur. J. Plant Pathol. 100: 137156.
135. van Loon, L. 2007. Plant responses to plant growth-promoting rhizobacteria. Eur. J. Plant Pathol. 119: 243254.
136. Vasseur, V.,, M. Van Montagu, and, G. H. Goldman. 1995. Trichoderma harzianum genes induced during growth on Rhizoctonia solani cell walls. Microbiology 141: 767774.
137. Vinale, F.,, K. Sivasithamparam,, E. Ghisalberti,, R. Marra,, S. Woo,and, M. Lorito. 2008. Trichoderma–plant–pathogen interactions. Soil Biol. Biochem. 40: 110.
138. Viterbo, A.,, S. Haran,, D. Friesem,, O. Ramot,and, I. Chet. 2001. Antifungal activity of a novel endochitinase gene (chit36) from Trichoderma harzianum Rifai TM. FEMS Microbiol. Lett. 200: 169174.
139. Viterbo, A.,, M. Montero,, O. Ramot,, D. Friesem,, E. Monte,, A. Llobell,and, I. Chet. 2002. Expression regulation of the endochitinase chit36 from Trichoderma asperellum( T. harzianum T-203). Curr. Genet. 42: 114122.
140. Viterbo, A.,, M. Harel,, B. A. Horwitz,, I. Chet,and, P. K. Mukherjee. 2005. Trichoderma mitogen-activated protein kinase signaling is involved in induction of plant systemic resistance. Appl. Environ. Microbiol. 71: 62416246.
141. Viterbo, A.,, J. Inbar,, Y. Hadar and, I. Chet. 2007a. Plant disease biocontrol and induced resistance via fungal myco-parasites, p. 127–146. In C. P. Kubicekand, I. S. Druzhinina (ed.), The Mycota, vol. 4. Springer, Berlin, Germany.
142. Viterbo, A.,, A. Wiest,, Y. Brotman,, I. Chet,and, C. Kenerley. 2007b. The 18mer peptaibols from Trichoderma virens elicit plant defense responses. Mol. Plant Pathol. 8: 737764.
143. Vizcaino, J. A.,, F. J. Gonzalez,, M. B. Suarez,, J. Redondo,, J. Heinrich,, J. Delgado-Jarana,, R. Hermosa,, S. Gutierrez,, E. Monte,, A. Llobell,and, M. Rey. 2006. Generation, annotation and analysis of ESTs from Trichoderma harzianum CECT 2413. BMC Genomics 7: 193.
144. Vizcaino, J. A.,, J. Redondo,, M. B. Suarez,, R. E. Cardoza,, R. Hermosa,, F. J. Gonzalez,, M. Rey,and, E. Monte. 2007. Generation, annotation, and analysis of ESTs from four different Trichoderma strains grown under conditions related to biocontrol. Appl. Microbiol. Biotechnol. 75: 853862.
145. Vizcaino, J. A.,, L. Sanz,, R. E. Cardoza,, E. Monte,and, S. Gutierrez. 2005. Detection of putative peptide synthetase genes in Trichoderma species: application of this method to the cloning of a gene from T. harzianum CECT 2413. FEMS Microbiol. Lett. 244: 139148.
146. Wiest, A.,, D. Grzegorski,, B. W. Xu,, C. Goulard,, S. Rebuffat,, D. J. Ebbole,, B. Bodo,and, C. Kenerley. 2002. Identification of peptaibols from Trichoderma virens and cloning of a peptaibol synthetase. J. Biol. Chem. 277: 2086220868.
147. Woo, S.,, F. Scala,, M. Ruocco,and, M. Lorito. 2006. The molecular biology of the interactions between Trichoderma spp., phytopathogenic fungi, and plants. Phytopathology 96: 181185.
148. Xu, J.,and, J. Hamer. 1996. MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Dev. 10: 26962706.
149. Xue, C.,, Y. S. Bahn,, G. M. Cox,and, J. Heitman. 2006. G protein-coupled receptor Gpr4 senses amino acids and activates the cAMP-PKA pathway in Cryptococcus neoformans. Mol. Biol. Cell 17: 667679.
150. Yedidia, I.,, N. Benhamou,, Y. Kapulnik,and, I. Chet. 2000. Induction and accumulation of PR proteins activity during early stages of root colonization by the mycoparasite Trichoderma harzianum strain T-203. Plant Physiol. Biochem. 38: 863873.
151. Yedidia, I.,, M. Shoresh,, Z. Kerem,, N. Benhamou,, Y. Kapulnik,and, I. Chet. 2003. Concomitant induction of systemic resistance to Pseudomonas syringae pv. lachrymans in cucumber by Trichoderma asperellum (T-203) and accumulation of phytoalexins. Appl. Environ. Microbiol. 69: 73437353.
152. Zeilinger, S.,, C. Galhaup,, K. Payer,, S. L. Woo,, R. L. Mach,, C. Fekete,, M. Lorito,and, C. P. Kubicek. 1999. Chitinase gene expression during mycoparasitic interaction of Trichoderma harzianum with its host. Fungal Genet. Biol. 26: 131140.
153. Zeilinger, S.,, B. Reithner,, V. Scala,, I. Peissl,, M. Lorito,and, R. L. Mach. 2005. Signal transduction by Tga3, a novel G protein alpha subunit of Trichoderma atroviride. Appl. Environ. Microbiol. 71: 15911597.
154. Zelakowska-Komon, M.,, T. Neuhof,, R. Dieckmann,, H. von Dohren,, A. Herrera-Estrella,, C. P. Kubicek,and, I. S. Druzhinina. 2007. Formation of atroviridin by Hypocrea atroviridis is conidiation-associated and positively regulated by blue light and the G-protein GNA3. Eukaryot. Cell 6: 23322342.
155. Zhang, Y.,, R. Lamm,, C. Pillonel,, S. Lam,and, J. R. Xu. 2002. Osmoregulation and fungicide resistance: the Neurospora crassa os-2 gene encodes a HOG1 mitogen-activated protein kinase homologue. Appl. Environ. Microbiol. 68: 532538.


Generic image for table

Summary of some mycoparasitic fungi applied in biocontrol or with potential as biocontrol agents

Citation: Viterbo A, Horwitz B. 2010. Mycoparasitism, p 676-693. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch42

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error