1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

Necrotrophic Mycoparasites and Their Genomes

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • HTML
    205.21 Kb
  • PDF
    12.78 MB
  • XML
    199.63 Kb
  • Authors: Magnus Karlsson1, Lea Atanasova2, Dan Funck Jensen3, Susanne Zeilinger4
  • Editors: Joseph Heitman5, Timothy Y. James6, Pedro W. Crous7
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Forest Mycology and Plant Pathology, Uppsala BioCenter, Swedish University of Agricultural Sciences, 75007, Uppsala, Sweden; 2: Institute of Microbiology, University of Innsbruck, 6020 Innsbruck, Austria; 3: Department of Forest Mycology and Plant Pathology, Uppsala BioCenter, Swedish University of Agricultural Sciences, 75007, Uppsala, Sweden; 4: Institute of Microbiology, University of Innsbruck, 6020 Innsbruck, Austria; 5: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 6: Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109-1048; 7: CBS-KNAW Fungal Diversity Centre, Royal Dutch Academy of Arts and Sciences, Utrecht, The Netherlands
    • Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0016-2016
  • Received 15 June 2016 Accepted 11 January 2017 Published 10 March 2017
  • Susanne Zeilinger, [email protected]
image of Necrotrophic Mycoparasites and Their Genomes
    Preview this microbiology spectrum article:
    Preview Magnify
    Zoom in
    Zoomout

    Necrotrophic Mycoparasites and Their Genomes, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/5/2/FUNK-0016-2016-1.gif /docserver/preview/fulltext/microbiolspec/5/2/FUNK-0016-2016-2.gif

  • Abstract:

    Mycoparasitism is a lifestyle where one fungus establishes parasitic interactions with other fungi. Species of the genus together with are among the most studied fungal mycoparasites. They have wide host ranges comprising several plant pathogens and are used for biological control of plant diseases. as well as mycoparasites efficiently overgrow and kill their fungal prey by using infection structures and by applying lytic enzymes and toxic metabolites. Most of our knowledge on the putative signals and signaling pathways involved in prey recognition and activation of the mycoparasitic response is derived from studies with . These fungi rely on G-protein signaling, the cAMP pathway, and mitogen-activated protein kinase cascades during growth and development as well as during mycoparasitism. The signals being recognized by the mycoparasite may include surface molecules and surface properties as well as secondary metabolites and other small molecules released from the prey. Their exact nature, however, remains elusive so far. Recent genomics-based studies of mycoparasitic fungi of the order , i.e., species, , and , revealed not only several gene families with a mycoparasitism-related expansion of gene paralogue numbers, but also distinct differences between the different mycoparasites. We use this information to illustrate the biological principles and molecular basis of necrotrophic mycoparasitism and compare the mycoparasitic strategies of as a “model” mycoparasite with the behavior and special features of , and .

  • Citation: Karlsson M, Atanasova L, Jensen D, Zeilinger S. 2017. Necrotrophic Mycoparasites and Their Genomes. Microbiol Spectrum 5(2):FUNK-0016-2016. doi:10.1128/microbiolspec.FUNK-0016-2016.

References

1. Barnett HL, Binder FL. 1973. The fungal host-parasite relationship. Annu Rev Phytopathol 11:273–292. http://dx.doi.org/10.1146/annurev.py.11.090173.001421
2. Kiss L, Russell JC, Szentivanyi O, Xu X, Jeffries P. 2004. Biology and biocontrol potential of Ampelomyces mycoparasites, natural antagonists of powdery mildew fungi. Biocontrol Sci Technol 14:635–651. http://dx.doi.org/10.1080/09583150410001683600
3. Jing Y, Liang C. 2016. Ampelomyces quisqualis HMLAC05119 v1.0. Joint Genome Institute. http://genome.jgi.doe.gov/Ampqui1/Ampqui1.home.html
4. Viterbo A, Inbar J, Hadar Y, Chet I. 2007. Plant disease biocontrol and induced resistance via fungal mycoparasites, p 127–146. In Kubicek CP, Druzhinina I (ed), The Mycota, vol IV. Springer, Berlin, Germany.
5. Jeffries P, Young TWK. 1994. Interfungal Parasitic Relationships. CAB International, UK.
6. Viterbo A, Horwitz BA. 2010. Mycoparasitism, p 676–693. In Borkovich KA, Ebbole DJ (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. http://dx.doi.org/10.1128/9781555816636.ch42
7. Chet I, Inbar J, Hadar Y. 1997. Fungal antagonists and mycoparasites, p 165–184. In Wicklow D, Söderström B (ed), The Mycota IV. Springer, Berlin, Germany.
8. Samuels GJ, Hebbar PK. 2015. Trichoderma: Identification and Agricultural Applications. APS Press, St. Paul, MN.
9. Weindling R. 1932. Trichoderma lignorum as a parasite of other soil fungi. Phytopathology 22:837–845. http://www.straininfo.net/publications/110032
10. Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Kenerley CM, Monte E, Mukherjee PK, Zeilinger S, Grigoriev IV, Kubicek CP. 2011. Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol 9:749–759. http://dx.doi.org/10.1038/nrmicro2637 [PubMed]
11. Schroers HJ, Samuels GJ, Seifert KA, Gams W. 1999. Classification of the mycoparasite Gliocladium roseum in Clonostachys as C. rosea, its relationship to Bionectria ochroleuca, and notes on other Gliocladium-like fungi. Mycologia 91:365–385. http://dx.doi.org/10.2307/3761383
12. Barnett HL, Lilly VG. 1962. A destructive mycoparasite, Gliocladium roseum. Mycologia 54:72–77. http://dx.doi.org/10.2307/3756600
13. Karlsson M, Durling MB, Choi J, Kosawang C, Lackner G, Tzelepis GD, Nygren K, Dubey MK, Kamou N, Levasseur A, Zapparata A, Wang J, Amby DB, Jensen B, Sarrocco S, Panteris E, Lagopodi AL, Pöggeler S, Vannacci G, Collinge DB, Hoffmeister D, Henrissat B, Lee YH, Jensen DF. 2015. Insights on the evolution of mycoparasitism from the genome of Clonostachys rosea. Genome Biol Evol 7:465–480. http://dx.doi.org/10.1093/gbe/evu292 [PubMed]
14. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M. 2004. Trichoderma species--opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56. http://dx.doi.org/10.1038/nrmicro797
15. Chatterton S, Punja ZK. 2010. Factors influencing colonization of cucumber roots by Clonostachys rosea f. catenulata, a biological disease control agent. Biocontrol Sci Technol 20:37–55. http://dx.doi.org/10.1080/09583150903350253
16. Dubey MK, Jensen DF, Karlsson M. 2014. Hydrophobins are required for conidial hydrophobicity and plant root colonization in the fungal biocontrol agent Clonostachys rosea. BMC Microbiol 14:18. http://dx.doi.org/10.1186/1471-2180-14-18
17. Shoresh M, Harman GE, Mastouri F. 2010. Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43. http://dx.doi.org/10.1146/annurev-phyto-073009-114450
18. Johansen A, Knudsen IMB, Binnerup SJ, Windinga A, Johansen JE, Jensen LE, Andersen KS, Svenning MM, Bonde TA. 2005. Non-target effects of the microbial control agents Pseudomonas fluorescens DR54 and Clonostachys rosea IK726 in soils cropped with barley followed by sugar beet: a greenhouse assessment. Soil Biol Biochem 37:2225–2239. http://dx.doi.org/10.1016/j.soilbio.2005.04.004
19. Roberti R, Veronesi AR, Cesari A, Cascone A, Di Berardino I, Bertini L, Caruso C. 2008. Induction of PR proteins and resistance by the biocontrol agent Clonostachys rosea in wheat plants infected with Fusarium culmorum. Plant Sci 175:339–347. http://dx.doi.org/10.1016/j.plantsci.2008.05.003
20. Mouekouba LD, Zhang L, Guan X, Chen X, Chen H, Zhang J, Zhang J, Li J, Yang Y, Wang A. 2014. Analysis of Clonostachys rosea-induced resistance to tomato gray mold disease in tomato leaves. PLoS One 9:e102690. http://dx.doi.org/10.1371/journal.pone.0102690
21. Lahlali R, Peng G. 2014. Suppression of clubroot by Clonostachys rosea via antibiosis and induced host resistance. Plant Pathol 63:447–455. http://dx.doi.org/10.1111/ppa.12112
22. Jensen DF, Karlsson M, Lindahl B. 2017. Fungal-fungal interactions: From natural ecosystems to managed plant production with emphasis on biological control of plant pathogens, p 549-562. In Dighton J, White JF (ed), The Fungal Community: Its Organization and Role in the Ecosystem, 4th ed. CRC Press, Boca Raton, FL.
23. Chet I, Harman GE, Baker R. 1981. Trichoderma hamatum: its hyphal interactions with Rhizoctonia solani and Pythium spp. Microb Ecol 7:29–38. http://dx.doi.org/10.1007/BF02010476 [PubMed]
24. Elad Y, Barak R, Chet I. 1983. Possible role of lectins in mycoparasitism. J Bacteriol 154:1431–1435. [PubMed]
25. Lu Z, Tombolini R, Woo S, Zeilinger S, Lorito M, Jansson JK. 2004. In vivo study of Trichoderma-pathogen-plant interactions, using constitutive and inducible green fluorescent protein reporter systems. Appl Environ Microbiol 70:3073–3081. http://dx.doi.org/10.1128/AEM.70.5.3073-3081.2004
26. Li GQH, Huang C, Kokko EG, Acharya SN. 2002. Ultrastructural study of mycoparasitism of Gliocladium roseum on Botrytis cinerea. Bot Bull Acad Sin 43:211–218.
27. Lübeck M, Knudsen IMB, Jensen B, Thrane U, Janvier C, Jensen DF. 2002. GUS and GFP transformation of the biocontrol strain Clonostachys rosea IK726 and the use of these marker genes in ecological studies. Mycol Res 106:815–826. http://dx.doi.org/10.1017/S095375620200607X [CrossRef]
28. Kubicek CP, et al. 2011. Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol 12:R40. http://dx.doi.org/10.1186/gb-2011-12-4-r40
29. de Man TJ, Stajich JE, Kubicek CP, Teiling C, Chenthamara K, Atanasova L, Druzhinina IS, Levenkova N, Birnbaum SS, Barribeau SM, Bozick BA, Suen G, Currie CR, Gerardo NM. 2016. Small genome of the fungus Escovopsis weberi, a specialized disease agent of ant agriculture. Proc Natl Acad Sci USA 113:3567–3572. http://dx.doi.org/10.1073/pnas.1518501113
30. Quandt CA, Bushley KE, Spatafora JW. 2015. The genome of the truffle-parasite Tolypocladium ophioglossoides and the evolution of antifungal peptaibiotics. BMC Genomics 16:553. http://dx.doi.org/10.1186/s12864-015-1777-9
31. Seidl V, Song L, Lindquist E, Gruber S, Koptchinskiy A, Zeilinger S, Schmoll M, Martínez P, Sun J, Grigoriev I, Herrera-Estrella A, Baker SE, Kubicek CP. 2009. Transcriptomic response of the mycoparasitic fungus Trichoderma atroviride to the presence of a fungal prey. BMC Genomics 10:567. http://dx.doi.org/10.1186/1471-2164-10-567
32. Atanasova L, Le Crom S, Gruber S, Coulpier F, Seidl-Seiboth V, Kubicek CP, Druzhinina IS. 2013. Comparative transcriptomics reveals different strategies of Trichoderma mycoparasitism. BMC Genomics 14:121. http://dx.doi.org/10.1186/1471-2164-14-121
33. Sun ZB, Sun MH, Li SD. 2015. Identification of mycoparasitism-related genes in Clonostachys rosea 67-1 active against Sclerotinia sclerotiorum. Sci Rep 5:18169. http://dx.doi.org/10.1038/srep18169 [PubMed]
34. Quandt CA, Di Y, Elser J, Jaiswal P, Spatafora JW. 2016. Differential expression of genes involved in host recognition, attachment, and degradation in the mycoparasite Tolypocladium ophioglossoides. G3 (Bethesda) 6:731–741. http://dx.doi.org/10.1534/g3.116.027045 [PubMed]
35. Sung GH, Poinar GO Jr, Spatafora JW. 2008. The oldest fossil evidence of animal parasitism by fungi supports a Cretaceous diversification of fungal-arthropod symbioses. Mol Phylogenet Evol 49:495–502. http://dx.doi.org/10.1016/j.ympev.2008.08.028
36. Chenthamara K, Druzhinina I. 2016. Ecological genomics of mycotrophic fungi, p 215–246. In Druzhinina IS, Kubicek CP (ed), The Mycota IV, 3rd ed. Springer, Cham, Switzerland.
37. Sivan A, Chet I. 1986. Biological control of Fusarium spp. in cotton, wheat and muskmelon by Trichoderma harzianum. J Phytopathol 116:39–47. http://dx.doi.org/10.1111/j.1439-0434.1986.tb00892.x
38. Rodríguez MA, Cabrera G, Gozzo FC, Eberlin MN, Godeas A. 2011. Clonostachys rosea BAFC3874 as a Sclerotinia sclerotiorum antagonist:mechanisms involved and potential as a biocontrol agent. J Appl Microbiol 110:1177–1186. http://dx.doi.org/10.1111/j.1365-2672.2011.04970.x
39. Arroyo J, Sarfati J, Baixench MT, Ragni E, Guillén M, Rodriguez-Peña JM, Popolo L, Latgé JP. 2007. The GPI-anchored Gas and Crh families are fungal antigens. Yeast 24:289–296. http://dx.doi.org/10.1002/yea.1480 [PubMed]
40. Jensen DF, Knudsen IMB, Lübeck M, Mamarabadi M, Hockenhull JBJ, Jensen B. 2007. Development of a biocontrol agent for plant disease control with special emphasis on the near commercial fungal antagonist Clonostachys rosea strain IK726. Australas Plant Pathol 36:95–101. http://dx.doi.org/10.1071/AP07009
41. Reynolds HT, Currie CR. 2004. Pathogenicity of Escovopsis weberi: the parasite of the attine ant-microbe symbiosis directly consumes the ant-cultivated fungus. Mycologia 96:955–959. http://dx.doi.org/10.2307/3762079
42. Marfetán JA, Romero AI, Folgarait PJ. 2015. Pathogenic interaction between Escovopsis weberi and Leucoagaricus sp.: mechanisms involved and virulence levels. Fungal Ecol 17:52–61. http://dx.doi.org/10.1016/j.funeco.2015.04.002
43. Wapinski I, Pfeffer A, Friedman N, Regev A. 2007. Natural history and evolutionary principles of gene duplication in fungi. Nature 449:54–61. http://dx.doi.org/10.1038/nature06107 [PubMed]
44. Papp B, Pál C, Hurst LD. 2003. Dosage sensitivity and the evolution of gene families in yeast. Nature 424:194–197. http://dx.doi.org/10.1038/nature01771 [PubMed]
45. Studholme DJ, Harris B, Le Cocq K, Winsbury R, Perera V, Ryder L, Ward JL, Beale MH, Thornton CR, Grant M. 2013. Investigating the beneficial traits of Trichoderma hamatum GD12 for sustainable agriculture–insights from genomics. Front Plant Sci 4:258. http://dx.doi.org/10.3389/fpls.2013.00258
46. Xie BB, Qin QL, Shi M, Chen LL, Shu YL, Luo Y, Wang XW, Rong JC, Gong ZT, Li D, Sun CY, Liu GM, Dong XW, Pang XH, Huang F, Liu W, Chen XL, Zhou BC, Zhang YZ, Song XY. 2014. Comparative genomics provide insights into evolution of Trichoderma nutrition style. Genome Biol Evol 6:379–390. http://dx.doi.org/10.1093/gbe/evu018
47. Yang D, Pomraning K, Kopchinskiy A, Karimi Aghcheh R, Atanasova L, Chenthamara K, Baker SE, Zhang R, Shen Q, Freitag M, Kubicek CP, Druzhinina IS. 2015. Genome sequence and annotation of Trichoderma parareesei, the ancestor of the cellulase producer Trichoderma reesei. Genome Announc 3:e00885-15. http://dx.doi.org/10.1128/genomeA.00885-15
48. Sun Z-B, Sun M-H, Li S-D. 2015. Draft genome sequence of mycoparasite Clonostachys rosea strain 67-1. Genome Announc 3:e00546-15. http://dx.doi.org/10.1128/genomeA.00546-15 [PubMed]
49. Coleman JJ, Rounsley SD, Rodriguez-Carres M, Kuo A, Wasmann CC, Grimwood J, Schmutz J, Taga M, White GJ, Zhou S, Schwartz DC, Freitag M, Ma LJ, Danchin EG, Henrissat B, Coutinho PM, Nelson DR, Straney D, Napoli CA, Barker BM, Gribskov M, Rep M, Kroken S, Molnár I, Rensing C, Kennell JC, Zamora J, Farman ML, Selker EU, Salamov A, Shapiro H, Pangilinan J, Lindquist E, Lamers C, Grigoriev IV, Geiser DM, Covert SF, Temporini E, Vanetten HD. 2009. The genome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. PLoS Genet 5:e1000618. http://dx.doi.org/10.1371/journal.pgen.1000618
50. Ma LJ, et al. 2010. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464:367–373. http://dx.doi.org/10.1038/nature08850 [PubMed]
51. Inbar J, Chet I. 1992. Biomimics of fungal cell-cell recognition by use of lectin-coated nylon fibers. J Bacteriol 174:1055–1059. http://dx.doi.org/10.1128/jb.174.3.1055-1059.1992 [PubMed]
52. Cortés C, Gutierrez A, Olmedo V, Inbar J, Chet I, Herrera-Estrella A. 1998. The expression of genes involved in parasitism by Trichoderma harzianum is triggered by a diffusible factor. Mol Gen Genet 260:218–225. http://dx.doi.org/10.1007/s004380050889
53. Zeilinger S, Galhaup C, Payer K, Woo SL, Mach RL, Fekete C, Lorito M, Kubicek CP. 1999. Chitinase gene expression during mycoparasitic interaction of Trichoderma harzianum with its host. Fungal Genet Biol 26:131–140. http://dx.doi.org/10.1006/fgbi.1998.1111
54. Kullnig C, Mach RL, Lorito M, Kubicek CP. 2000. Enzyme diffusion from Trichoderma atroviride (= T. harzianum P1) to Rhizoctonia solani is a prerequisite for triggering of Trichoderma ech42 gene expression before mycoparasitic contact. Appl Environ Microbiol 66:2232–2234. http://dx.doi.org/10.1128/AEM.66.5.2232-2234.2000
55. Schmoll M, Dattenböck C, Carreras-Villaseñor N, Mendoza-Mendoza A, Tisch D, Alemán MI, Baker SE, Brown C, Cervantes-Badillo MG, Cetz-Chel J, Cristobal-Mondragon GR, Delaye L, Esquivel-Naranjo EU, Frischmann A, Gallardo-Negrete JJ, García-Esquivel M, Gomez-Rodriguez EY, Greenwood DR, Hernández-Oñate M, Kruszewska JS, Lawry R, Mora-Montes HM, Muñoz-Centeno T, Nieto-Jacobo MF, Nogueira Lopez G, Olmedo-Monfil V, Osorio-Concepcion M, Piłsyk S, Pomraning KR, Rodriguez-Iglesias A, Rosales-Saavedra MT, Sánchez-Arreguín JA, Seidl-Seiboth V, Stewart A, Uresti-Rivera EE, Wang CL, Wang TF, Zeilinger S, Casas-Flores S, Herrera-Estrella A. 2016. The genomes of three uneven siblings: footprints of the lifestyles of three Trichoderma species. Microbiol Mol Biol Rev 80:205–327. http://dx.doi.org/10.1128/MMBR.00040-15 [PubMed]
56. Li L, Wright SJ, Krystofova S, Park G, Borkovich KA. 2007. Heterotrimeric G protein signaling in filamentous fungi. Annu Rev Microbiol 61:423–452. http://dx.doi.org/10.1146/annurev.micro.61.080706.093432 [PubMed]
57. Rocha-Ramirez V, Omero C, Chet I, Horwitz BA, Herrera-Estrella A. 2002. Trichoderma atroviride G-protein alpha-subunit gene tga1 is involved in mycoparasitic coiling and conidiation. Eukaryot Cell 1:594–605. http://dx.doi.org/10.1128/EC.1.4.594-605.2002 [PubMed]
58. Mukherjee PK, Latha J, Hadar R, Horwitz BA. 2004. Role of two G-protein alpha subunits, TgaA and TgaB, in the antagonism of plant pathogens by Trichoderma virens. Appl Environ Microbiol 70:542–549. http://dx.doi.org/10.1128/AEM.70.1.542-549.2004
59. Reithner B, Brunner K, Schuhmacher R, Peissl I, Seidl V, Krska R, Zeilinger S. 2005. The G protein alpha subunit Tga1 of Trichoderma atroviride is involved in chitinase formation and differential production of antifungal metabolites. Fungal Genet Biol 42:749–760. http://dx.doi.org/10.1016/j.fgb.2005.04.009 [PubMed]
60. Zeilinger S, Reithner B, Scala V, Peissl I, Lorito M, Mach RL. 2005. Signal transduction by Tga3, a novel G protein alpha subunit of Trichoderma atroviride. Appl Environ Microbiol 71:1591–1597. http://dx.doi.org/10.1128/AEM.71.3.1591-1597.2005 [PubMed]
61. Gruber S, Omann M, Zeilinger S. 2013. Comparative analysis of the repertoire of G protein-coupled receptors of three species of the fungal genus Trichoderma. BMC Microbiol 13:108. http://dx.doi.org/10.1186/1471-2180-13-108
62. Brunner K, Omann M, Pucher ME, Delic M, Lehner SM, Domnanich P, Kratochwill K, Druzhinina I, Denk D, Zeilinger S. 2008. Trichoderma G protein-coupled receptors: functional characterisation of a cAMP receptor-like protein from Trichoderma atroviride. Curr Genet 54:283–299. http://dx.doi.org/10.1007/s00294-008-0217-7
63. Omann MR, Lehner S, Escobar Rodríguez C, Brunner K, Zeilinger S. 2012. The seven-transmembrane receptor Gpr1 governs processes relevant for the antagonistic interaction of Trichoderma atroviride with its host. Microbiology 158:107–118. http://dx.doi.org/10.1099/mic.0.052035-0
64. Dickman MB, Yarden O. 1999. Serine/threonine protein kinases and phosphatases in filamentious fungi. Fungal Genet Biol 26:99–117. http://dx.doi.org/10.1006/fgbi.1999.1118 [PubMed]
65. Mukherjee M, Mukherjee PK, Kale SP. 2007. cAMP signalling is involved in growth, germination, mycoparasitism and secondary metabolism in Trichoderma virens. Microbiology 153:1734–1742. http://dx.doi.org/10.1099/mic.0.2007/005702-0 [PubMed]
66. Silva RN, da Silva SP, Brandão RL, Ulhoa CJ. 2004. Regulation of N-acetyl-beta-D-glucosaminidase produced by Trichoderma harzianum: evidence that cAMP controls its expression. Res Microbiol 155:667–671. http://dx.doi.org/10.1016/j.resmic.2004.05.012
67. Seger R, Krebs EG. 1995. The MAPK signaling cascade. FASEB J 9:726–735. [PubMed]
68. Mendoza-Mendoza A, Pozo MJ, Grzegorski D, Martínez P, García JM, Olmedo-Monfil V, Cortés C, Kenerley C, Herrera-Estrella A. 2003. Enhanced biocontrol activity of Trichoderma through inactivation of a mitogen-activated protein kinase. Proc Natl Acad Sci USA 100:15965–15970. http://dx.doi.org/10.1073/pnas.2136716100
69. Mukherjee PK, Latha J, Hadar R, Horwitz BA. 2003. TmkA, a mitogen-activated protein kinase of Trichoderma virens, is involved in biocontrol properties and repression of conidiation in the dark. Eukaryot Cell 2:446–455. http://dx.doi.org/10.1128/EC.2.3.446-455.2003
70. Reithner B, Schuhmacher R, Stoppacher N, Pucher M, Brunner K, Zeilinger S. 2007. Signaling via the Trichoderma atroviride mitogen-activated protein kinase Tmk 1 differentially affects mycoparasitism and plant protection. Fungal Genet Biol 44:1123–1133. http://dx.doi.org/10.1016/j.fgb.2007.04.001 [PubMed]
71. Zhao X, Xu JR. 2007. A highly conserved MAPK-docking site in Mst7 is essential for Pmk1 activation in Magnaporthe grisea. Mol Microbiol 63:881–894. http://dx.doi.org/10.1111/j.1365-2958.2006.05548.x [PubMed]
72. Gruber S, Zeilinger S. 2014. The transcription factor Ste12 mediates the regulatory role of the Tmk1 MAP kinase in mycoparasitism and vegetative hyphal fusion in the filamentous fungus Trichoderma atroviride. PLoS One 9:e111636. http://dx.doi.org/10.1371/journal.pone.0111636
73. Kumar A, Scher K, Mukherjee M, Pardovitz-Kedmi E, Sible GV, Singh US, Kale SP, Mukherjee PK, Horwitz BA. 2010. Overlapping and distinct functions of two Trichoderma virens MAP kinases in cell-wall integrity, antagonistic properties and repression of conidiation. Biochem Biophys Res Commun 398:765–770. http://dx.doi.org/10.1016/j.bbrc.2010.07.020
74. Wang M, Dong Y, Zhao Q, Wang F, Liu K, Jiang B, Fang X. 2014. Identification of the role of a MAP kinase Tmk2 in Hypocrea jecorina ( Trichoderma reesei). Sci Rep 4:6732. http://dx.doi.org/10.1038/srep06732 [PubMed]
75. Hohmann S, Krantz M, Nordlander B. 2007. Yeast osmoregulation. Methods Enzymol 428:29–45. http://dx.doi.org/10.1016/S0076-6879(07)28002-4 [PubMed]
76. Delgado-Jarana J, Sousa S, González F, Rey M, Llobell A. 2006. ThHog1 controls the hyperosmotic stress response in Trichoderma harzianum. Microbiology 152:1687–1700. http://dx.doi.org/10.1099/mic.0.28729-0
77. Esquivel-Naranjo EU, García-Esquivel M, Medina-Castellanos E, Correa-Pérez VA, Parra-Arriaga JL, Landeros-Jaime F, Cervantes-Chávez JA, Herrera-Estrella A. 2016. A Trichoderma atroviride stress-activated MAPK pathway integrates stress and light signals. Mol Microbiol 100:860–876. http://dx.doi.org/10.1111/mmi.13355
78. Bayram O, Krappmann S, Ni M, Bok JW, Helmstaedt K, Valerius O, Braus-Stromeyer S, Kwon NJ, Keller NP, Yu JH, Braus GH. 2008. VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science 320:1504–1506. http://dx.doi.org/10.1126/science.1155888 [PubMed]
79. Mukherjee PK, Kenerley CM. 2010. Regulation of morphogenesis and biocontrol properties in Trichoderma virens by a VELVET protein, Vel1. Appl Environ Microbiol 76:2345–2352. http://dx.doi.org/10.1128/AEM.02391-09 [PubMed]
80. Karimi Aghcheh R, Druzhinina IS, Kubicek CP. 2013. The putative protein methyltransferase LAE1 of Trichoderma atroviride is a key regulator of asexual development and mycoparasitism. PLoS One 8:e67144. http://dx.doi.org/10.1371/journal.pone.0067144
81. Bowman SM, Free SJ. 2006. The structure and synthesis of the fungal cell wall. BioEssays 28:799–808. http://dx.doi.org/10.1002/bies.20441 [PubMed]
82. Latgé JP. 2007. The cell wall: a carbohydrate armour for the fungal cell. Mol Microbiol 66:279–290. http://dx.doi.org/10.1111/j.1365-2958.2007.05872.x [PubMed]
83. Druzhinina IS, Shelest E, Kubicek CP. 2012. Novel traits of Trichoderma predicted through the analysis of its secretome. FEMS Microbiol Lett 337:1–9. http://dx.doi.org/10.1111/j.1574-6968.2012.02665.x
84. Karlsson M, Stenlid J. 2009. Evolution of family 18 glycoside hydrolases: diversity, domain structures and phylogenetic relationships. J Mol Microbiol Biotechnol 16:208–223. http://dx.doi.org/10.1159/000151220
85. Karlsson M, Stenlid J. 2008. Comparative evolutionary histories of the fungal chitinase gene family reveal non-random size expansions and contractions due to adaptive natural selection. Evol Bioinform Online 4:47–60. [PubMed]
86. Seidl V, Huemer B, Seiboth B, Kubicek CP. 2005. A complete survey of Trichoderma chitinases reveals three distinct subgroups of family 18 chitinases. FEBS J 272:5923–5939. http://dx.doi.org/10.1111/j.1742-4658.2005.04994.x
87. Karlsson M, Stenlid J, Lindahl B. 2016. Functional differentiation of chitinases in the white-rot fungus Phanerochaete chrysosporium. Fungal Ecol 22:52–60. http://dx.doi.org/10.1016/j.funeco.2016.04.004
88. Ihrmark K, Asmail N, Ubhayasekera W, Melin P, Stenlid J, Karlsson M. 2010. Comparative molecular evolution of Trichoderma chitinases in response to mycoparasitic interactions. Evol Bioinform Online 6:1–26. [PubMed]
89. Seidl-Seiboth V, Ihrmark K, Druzhinina IS, Karlsson M. 2014. Molecular evolution of Trichoderma chitinases, p 67–78. In Gupta VK, Schmoll M, Herrera-Estrella A, Upadhyay RS, Druzhinina I, Tuohy MG (ed), Biotechnology and Biology of Trichoderma. Elsevier, Oxford, UK. http://dx.doi.org/10.1016/B978-0-444-59576-8.00005-9
90. Tzelepis G, Dubey M, Jensen DF, Karlsson M. 2015. Identifying glycoside hydrolase family 18 genes in the mycoparasitic fungal species Clonostachys rosea. Microbiology 161:1407–1419. http://dx.doi.org/10.1099/mic.0.000096 [PubMed]
91. Boer H, Simolin H, Cottaz S, Söderlund H, Koivula A. 2007. Heterologous expression and site-directed mutagenesis studies of two Trichoderma harzianum chitinases, Chit33 and Chit42, in Escherichia coli. Protein Expr Purif 51:216–226. http://dx.doi.org/10.1016/j.pep.2006.07.020
92. Hoell IA, Klemsdal SS, Vaaje-Kolstad G, Horn SJ, Eijsink VG. 2005. Overexpression and characterization of a novel chitinase from Trichoderma atroviride strain P1. Biochim Biophys Acta 1748:180–190. http://dx.doi.org/10.1016/j.bbapap.2005.01.002 [PubMed]
93. Klemsdal SS, Clarke JL, Hoell IA, Eijsink VG, Brurberg MB. 2006. Molecular cloning, characterization, and expression studies of a novel chitinase gene (ech30) from the mycoparasite Trichoderma atroviride strain P1. FEMS Microbiol Lett 256:282–289. http://dx.doi.org/10.1111/j.1574-6968.2006.00132.x
94. Seidl V. 2008. Chitinases of filamentous fungi: a large group of diverse proteins with multiple physiological functions. Fungal Biol Rev 22:36–42. http://dx.doi.org/10.1016/j.fbr.2008.03.002
95. Kim DJ, Baek JM, Uribe P, Kenerley CM, Cook DR. 2002. Cloning and characterization of multiple glycosyl hydrolase genes from Trichoderma virens. Curr Genet 40:374–384. http://dx.doi.org/10.1007/s00294-001-0267-6
96. Limón MC, Lora JM, García I, de la Cruz J, Llobell A, Benítez T, Pintor-Toro JA. 1995. Primary structure and expression pattern of the 33-kDa chitinase gene from the mycoparasitic fungus Trichoderma harzianum. Curr Genet 28:478–483. http://dx.doi.org/10.1007/BF00310819
97. Viterbo A, Montero M, Ramot O, Friesem D, Monte E, Llobell A, Chet I. 2002. Expression regulation of the endochitinase chit36 from Trichoderma asperellum ( T. harzianum T-203). Curr Genet 42:114–122. http://dx.doi.org/10.1007/s00294-002-0345-4 [PubMed]
98. Mamarabadi M, Jensen B, Jensen DF, Lübeck M. 2008. Real-time RT-PCR expression analysis of chitinase and endoglucanase genes in the three-way interaction between the biocontrol strain Clonostachys rosea IK726, Botrytis cinerea and strawberry. FEMS Microbiol Lett 285:101–110. http://dx.doi.org/10.1111/j.1574-6968.2008.01228.x
99. Mamarabadi M, Jensen B, Lübeck M. 2008. Three endochitinase-encoding genes identified in the biocontrol fungus Clonostachys rosea are differentially expressed. Curr Genet 54:57–70. http://dx.doi.org/10.1007/s00294-008-0199-5
100. Magliani W, Conti S, Gerloni M, Bertolotti D, Polonelli L. 1997. Yeast killer systems. Clin Microbiol Rev 10:369–400. [PubMed]
101. Tzelepis GD, Melin P, Stenlid J, Jensen DF, Karlsson M. 2014. Functional analysis of the C-II subgroup killer toxin-like chitinases in the filamentous ascomycete Aspergillus nidulans. Fungal Genet Biol 64:58–66. http://dx.doi.org/10.1016/j.fgb.2013.12.009
102. Gruber S, Vaaje-Kolstad G, Matarese F, López-Mondéjar R, Kubicek CP, Seidl-Seiboth V. 2011. Analysis of subgroup C of fungal chitinases containing chitin-binding and LysM modules in the mycoparasite Trichoderma atroviride. Glycobiology 21:122–133. http://dx.doi.org/10.1093/glycob/cwq142
103. Gruber S, Kubicek CP, Seidl-Seiboth V. 2011. Differential regulation of orthologous chitinase genes in mycoparasitic Trichoderma species. Appl Environ Microbiol 77:7217–7226. http://dx.doi.org/10.1128/AEM.06027-11
104. Carsolio C, Benhamou N, Haran S, Cortés C, Gutiérrez A, Chet I, Herrera-Estrella A. 1999. Role of the Trichoderma harzianum endochitinase gene, ech42, in mycoparasitism. Appl Environ Microbiol 65:929–935. [PubMed]
105. Baek JM, Howell CR, Kenerley CM. 1999. The role of an extracellular chitinase from Trichoderma virens Gv29-8 in the biocontrol of Rhizoctonia solani. Curr Genet 35:41–50. http://dx.doi.org/10.1007/s002940050431 [PubMed]
106. Woo SL, Donzelli B, Scala F, Mach R, Harman GE, Kubicek CP, Del Sorbo G, Lorito M. 1999. Disruption of the ech42 (endochitinase-encoding) gene affects biocontrol activity in Trichoderma harzianum P1. Mol Plant Microbe Interact 12:419–429. http://dx.doi.org/10.1094/MPMI.1999.12.5.419
107. Gruber S, Seidl-Seiboth V. 2012. Self versus non-self: fungal cell wall degradation in Trichoderma. Microbiology 158:26–34. http://dx.doi.org/10.1099/mic.0.052613-0 [PubMed]
108. López-Mondéjar R, Catalano V, Kubicek CP, Seidl V. 2009. The beta-N-acetylglucosaminidases NAG1 and NAG2 are essential for growth of Trichoderma atroviride on chitin. FEBS J 276:5137–5148. http://dx.doi.org/10.1111/j.1742-4658.2009.07211.x [PubMed]
109. Tzelepis G, Hosomi A, Hossain TJ, Hirayama H, Dubey M, Jensen DF, Suzuki T, Karlsson M. 2014. Endo-β- N-acetylglucosamidases (ENGases) in the fungus Trichoderma atroviride: possible involvement of the filamentous fungi-specific cytosolic ENGase in the ERAD process. Biochem Biophys Res Commun 449:256–261. http://dx.doi.org/10.1016/j.bbrc.2014.05.017
110. Stals I, Samyn B, Sergeant K, White T, Hoorelbeke K, Coorevits A, Devreese B, Claeyssens M, Piens K. 2010. Identification of a gene coding for a deglycosylating enzyme in Hypocrea jecorina. FEMS Microbiol Lett 303:9–17. http://dx.doi.org/10.1111/j.1574-6968.2009.01849.x
111. Dubey MK, Ubhayasekera W, Sandgren M, Jensen DF, Karlsson M. 2012. Disruption of the Eng18B ENGase gene in the fungal biocontrol agent Trichoderma atroviride affects growth, conidiation and antagonistic ability. PLoS One 7:e36152. http://dx.doi.org/10.1371/journal.pone.0036152
112. Wang SL, Lin TY, Yen YH, Liao HF, Chen YJ. 2006. Bioconversion of shellfish chitin wastes for the production of Bacillus subtilis W-118 chitinase. Carbohydr Res 341:2507–2515. http://dx.doi.org/10.1016/j.carres.2006.06.027 [PubMed]
113. da Silva LC, Honorato TL, Cavalcante RS, Franco TT, Rodrigues S. 2012. Effect of pH and temperature on enzyme activity of chitosanase produced under solid stated fermentation by Trichoderma spp. Indian J Microbiol 52:60–65. http://dx.doi.org/10.1007/s12088-011-0196-0
114. Ike M, Ko Y, Yokoyama K, Sumitani J-I, Kawaguchi T, Ogasawara W, Okada H, Morikawa Y. 2007. Cellobiohydrolase I (Cel7A) from Trichoderma reesei has chitosanase activity. J Mol Catal B Enzym 47:159–163. http://dx.doi.org/10.1016/j.molcatb.2007.05.004
115. de la Cruz J, Pintor-Toro JA, Benítez T, Llobell A. 1995. Purification and characterization of an endo-beta-1,6-glucanase from Trichoderma harzianum that is related to its mycoparasitism. J Bacteriol 177:1864–1871. http://dx.doi.org/10.1128/jb.177.7.1864-1871.1995 [PubMed]
116. Cohen-Kupiec R, Broglie KE, Friesem D, Broglie RM, Chet I. 1999. Molecular characterization of a novel beta-1,3-exoglucanase related to mycoparasitism of Trichoderma harzianum. Gene 226:147–154. http://dx.doi.org/10.1016/S0378-1119(98)00583-6
117. Chatterton S, Punja ZK. 2009. Chitinase and beta-1,3-glucanase enzyme production by the mycoparasite Clonostachys rosea f. catenulata against fungal plant pathogens. Can J Microbiol 55:356–367. http://dx.doi.org/10.1139/W08-156
118. Montero M, Sanz L, Rey M, Monte E, Llobell A. 2005. BGN16.3, a novel acidic beta-1,6-glucanase from mycoparasitic fungus Trichoderma harzianum CECT 2413. FEBS J 272:3441–3448. http://dx.doi.org/10.1111/j.1742-4658.2005.04762.x [PubMed]
119. Djonović S, Pozo MJ, Kenerley CM. 2006. Tvbgn3, a beta-1,6-glucanase from the biocontrol fungus Trichoderma virens, is involved in mycoparasitism and control of Pythium ultimum. Appl Environ Microbiol 72:7661–7670. http://dx.doi.org/10.1128/AEM.01607-06 [PubMed]
120. Montero M, Sanz L, Rey M, Llobell A, Monte E. 2007. Cloning and characterization of bgn16.3, coding for a beta-1,6-glucanase expressed during Trichoderma harzianum mycoparasitism. J Appl Microbiol 103:1291–1300. http://dx.doi.org/10.1111/j.1365-2672.2007.03371.x
121. Inglis GD, Kawchuk LM. 2002. Comparative degradation of oomycete, ascomycete, and basidiomycete cell walls by mycoparasitic and biocontrol fungi. Can J Microbiol 48:60–70. http://dx.doi.org/10.1139/w01-130 [PubMed]
122. Monteiro VN, Steindorff AS, dos Reis Almeida FB, Lopes FAC, Ulhoa CJ, Félix CR, Silva RN. 2015. Trichoderma reesei mycoparasitism against Pythium ultimum is coordinated by G-alpha protein GNA1 signaling. Microb Biochem Technol 7:1–7.
123. Thrane C, Tronsmo A, Jensen DF. 1997. Endo-1,3-β-glucanase and cellulase from Trichoderma harzianum: purification and partial characterization, induction of and biological activity against plant pathogenic Pythium spp. Eur J Plant Pathol 103:331–344.
124. Seidl V, Schmoll M, Scherm B, Balmas V, Seiboth B, Migheli Q, Kubicek CP. 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 257:145–151. http://dx.doi.org/10.1111/j.1574-6968.2006.00157.x
125. Viterbo A, Harel M, Chet I. 2004. Isolation of two aspartyl proteases from Trichoderma asperellum expressed during colonization of cucumber roots. FEMS Microbiol Lett 238:151–158. [PubMed]
126. Troian RF, Steindorff AS, Ramada MH, Arruda W, Ulhoa CJ. 2014. Mycoparasitism studies of Trichoderma harzianum against Sclerotinia sclerotiorum: evaluation of antagonism and expression of cell wall-degrading enzymes genes. Biotechnol Lett 36:2095–2101. http://dx.doi.org/10.1007/s10529-014-1583-5 [PubMed]
127. Demain AL, Fang A. 2000. The natural functions of secondary metabolites. Adv Biochem Eng Biotechnol 69:1–39. http://dx.doi.org/10.1007/3-540-44964-7_1
128. Keller NP, Turner G, Bennett JW. 2005. Fungal secondary metabolism - from biochemistry to genomics. Nat Rev Microbiol 3:937–947. http://dx.doi.org/10.1038/nrmicro1286 [PubMed]
129. Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Barbetti MJ, Li H, Woo SL, Lorito M. 2008. A novel role for Trichoderma secondary metabolites in the interactions with plants. Mol Plant Pathol 72:80–86. http://dx.doi.org/10.1016/j.pmpp.2008.05.005
130. Weindling R. 1934. Studies on a lethal principle effective in the parasitic action of Trichoderma lignorum on Rhizoctonia solani and other soil fungi. Phytopathology 24:1153–1179.
131. Weindling R, Emerson OH. 1936. The isolation of a toxic substance from the culture filtrate of Trichoderma. Phytopathology 26:1068–1070.
132. Keller NP. 2015. Translating biosynthetic gene clusters into fungal armor and weaponry. Nat Chem Biol 11:671–677. http://dx.doi.org/10.1038/nchembio.1897 [PubMed]
133. Strieker M, Tanović A, Marahiel MA. 2010. Nonribosomal peptide synthetases: structures and dynamics. Curr Opin Struct Biol 20:234–240. http://dx.doi.org/10.1016/j.sbi.2010.01.009 [PubMed]
134. Neumann NK, Stoppacher N, Zeilinger S, Degenkolb T, Brückner H, Schuhmacher R. 2015. The peptaibiotics database--a comprehensive online resource. Chem Biodivers 12:743–751. http://dx.doi.org/10.1002/cbdv.201400393 [PubMed]
135. Stoppacher N, Neumann NK, Burgstaller L, Zeilinger S, Degenkolb T, Brückner H, Schuhmacher R. 2013. The comprehensive peptaibiotics database. Chem Biodivers 10:734–743. http://dx.doi.org/10.1002/cbdv.201200427 [PubMed][CrossRef]
136. Ooka T, Shimojima Y, Akimoto T, Takeda I, Senoh S, Abe J. 1966. A new antibacterial peptide “suzukacillin”. Agric Biol Chem 30:700–702. http://dx.doi.org/10.1080/00021369.1966.10858667
137. Meyer CE, Reusser F. 1967. A polypeptide antibacterial agent isolated from Trichoderma viride. Experientia 23:85–86. http://dx.doi.org/10.1007/BF02135929 [PubMed]
138. Chugh JK, Wallace BA. 2001. Peptaibols: models for ion channels. Biochem Soc Trans 29:565–570. http://dx.doi.org/10.1042/bst0290565 [PubMed]
139. Bortolus M, De Zotti M, Formaggio F, Maniero AL. 2013. Alamethicin in bicelles: orientation, aggregation, and bilayer modification as a function of peptide concentration. Biochim Biophys Acta 1828:2620–2627. http://dx.doi.org/10.1016/j.bbamem.2013.07.007
140. Schirmböck M, Lorito M, Wang YL, Hayes CK, Arisan-Atac I, Scala F, Harman GE, Kubicek CP. 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 60:4364–4370. [PubMed]
141. Lorito M, Farkas V, Rebuffat S, Bodo B, Kubicek CP. 1996. Cell wall synthesis is a major target of mycoparasitic antagonism by Trichoderma harzianum. J Bacteriol 178:6382–6385. http://dx.doi.org/10.1128/jb.178.21.6382-6385.1996 [PubMed]
142. Shi M, Chen L, Wang XW, Zhang T, Zhao PB, Song XY, Sun CY, Chen XL, Zhou BC, Zhang YZ. 2012. Antimicrobial peptaibols from Trichoderma pseudokoningii induce programmed cell death in plant fungal pathogens. Microbiology 158:166–175. http://dx.doi.org/10.1099/mic.0.052670-0
143. Engelberth J, Koch T, Schüler G, Bachmann N, Rechtenbach J, Boland W. 2001. Ion channel-forming alamethicin is a potent elicitor of volatile biosynthesis and tendril coiling. Cross talk between jasmonate and salicylate signaling in lima bean. Plant Physiol 125:369–377. http://dx.doi.org/10.1104/pp.125.1.369
144. Viterbo A, Wiest A, Brotman Y, Chet I, Kenerley C. 2007. The 18mer peptaibols from Trichoderma virens elicit plant defence responses. Mol Plant Pathol 8:737–746. http://dx.doi.org/10.1111/j.1364-3703.2007.00430.x [PubMed]
145. Mukherjee PK, Wiest A, Ruiz N, Keightley A, Moran-Diez ME, McCluskey K, Pouchus YF, Kenerley CM. 2011. Two classes of new peptaibols are synthesized by a single non-ribosomal peptide synthetase of Trichoderma virens. J Biol Chem 286:4544–4554. http://dx.doi.org/10.1074/jbc.M110.159723 [PubMed]
146. Gardiner DM, Waring P, Howlett BJ. 2005. The epipolythiodioxopiperazine (ETP) class of fungal toxins: distribution, mode of action, functions and biosynthesis. Microbiology 151:1021–1032. http://dx.doi.org/10.1099/mic.0.27847-0 [PubMed]
147. Howell CR, Stipanovic RD, Lumsden RD. 1993. Antibiotic production by strains of Gliocladium virens and its relation to the biocontrol of cotton seedling diseases. Biocontrol Sci Technol 3:435–441. http://dx.doi.org/10.1080/09583159309355298
148. Lorito M, Peterbauer C, Hayes CK, Harman GE. 1994. Synergistic interaction between fungal cell wall degrading enzymes and different antifungal compounds enhances inhibition of spore germination. Microbiology 140:623–629. http://dx.doi.org/10.1099/00221287-140-3-623
149. Mukherjee PK, Horwitz BA, Kenerley CM. 2012. Secondary metabolism in Trichoderma--a genomic perspective. Microbiology 158:35–45. http://dx.doi.org/10.1099/mic.0.053629-0 [PubMed]
150. Vargas WA, Mukherjee PK, Laughlin D, Wiest A, Moran-Diez ME, Kenerley CM. 2014. Role of gliotoxin in the symbiotic and pathogenic interactions of Trichoderma virens. Microbiology 160:2319–2330. http://dx.doi.org/10.1099/mic.0.079210-0
151. Dong JY, He HP, Shen YM, Zhang KQ. 2005. Nematicidal epipolysulfanyldioxopiperazines from Gliocladium roseum. J Nat Prod 68:1510–1513. http://dx.doi.org/10.1021/np0502241 [PubMed]
152. Bansal R, Mukherjee PK. 2016. Identification of novel gene clusters for secondary metabolism in Trichoderma genomes. Microbiology 85:185–190. http://dx.doi.org/10.1134/S002626171602003X
153. Atanasova L, Knox BP, Kubicek CP, Druzhinina IS, Baker SE. 2013. The polyketide synthase gene pks4 of Trichoderma reesei provides pigmentation and stress resistance. Eukaryot Cell 12:1499–1508. http://dx.doi.org/10.1128/EC.00103-13
154. Zhai MM, Qi FM, Li J, Jiang CX, Hou Y, Shi YP, Di DL, Zhang JW, Wu QX. 2016. Isolation of secondary metabolites from the soil-derived fungus Clonostachys rosea YRS-06, a biological control agent, and evaluation of antibacterial activity. J Agric Food Chem 64:2298–2306. http://dx.doi.org/10.1021/acs.jafc.6b00556
155. Okuda T, Kohno J, Kishi N, Asai Y, Nishio M, Komatsubara S. 2000. Production of TMC-151, TMC-154 and TMC-171, a new class of antibiotics, is specific to ‘ Gliocladium roseum’ group. Mycoscience 41:239–253. http://dx.doi.org/10.1007/BF02489678
156. Cardoza RE, Malmierca MG, Hermosa MR, Alexander NJ, McCormick SP, Proctor RH, Tijerino AM, Rumbero A, Monte E, Gutiérrez S. 2011. Identification of loci and functional characterization of trichothecene biosynthesis genes in filamentous fungi of the genus Trichoderma. Appl Environ Microbiol 77:4867–4877. http://dx.doi.org/10.1128/AEM.00595-11 [PubMed]
157. Stoppacher N, Kluger B, Zeilinger S, Krska R, Schuhmacher R. 2010. Identification and profiling of volatile metabolites of the biocontrol fungus Trichoderma atroviride by HS-SPME-GC-MS. J Microbiol Methods 81:187–193. http://dx.doi.org/10.1016/j.mimet.2010.03.011
158. Malmierca MG, Cardoza RE, Alexander NJ, McCormick SP, Collado IG, Hermosa R, Monte E, Gutiérrez S. 2013. Relevance of trichothecenes in fungal physiology: disruption of tri5 in Trichoderma arundinaceum. Fungal Genet Biol 53:22–33. http://dx.doi.org/10.1016/j.fgb.2013.02.001
159. Malmierca MG, Cardoza RE, Alexander NJ, McCormick SP, Hermosa R, Monte E, Gutiérrez S. 2012. Involvement of Trichoderma trichothecenes in the biocontrol activity and induction of plant defense-related genes. Appl Environ Microbiol 78:4856–4868. http://dx.doi.org/10.1128/AEM.00385-12 [PubMed]
160. Vinale F, Marra R, Scala F, Ghisalberti EL, Lorito M, Sivasithamparam K. 2006. Major secondary metabolites produced by two commercial Trichoderma strains active against different phytopathogens. Lett Appl Microbiol 43:143–148. http://dx.doi.org/10.1111/j.1472-765X.2006.01939.x
161. Serrano-Carreon L, Hathout Y, Bensoussan M, Belin JM. 1993. Metabolism of linoleic acid or mevalonate and 6-pentyl-alpha-pyrone biosynthesis by Trichoderma Species. Appl Environ Microbiol 59:2945–2950. [PubMed]
162. Cooney JM, Lauren DR. 1998. Trichoderma/pathogen interactions: measurement of antagonistic chemicals produced at the antagonist/pathogen interface using a tubular bioassay. Lett Appl Microbiol 27:283–286. http://dx.doi.org/10.1046/j.1472-765X.1998.00437.x
163. Cooney JM, Lauren DR, di Menna ME. 2001. Impact of competitive fungi on trichothecene production by Fusarium graminearum. J Agric Food Chem 49:522–526. http://dx.doi.org/10.1021/jf0006372
164. Utermark J, Karlovsky P. 2007. Role of zearalenone lactonase in protection of Gliocladium roseum from fungitoxic effects of the mycotoxin zearalenone. Appl Environ Microbiol 73:637–642. http://dx.doi.org/10.1128/AEM.01440-06 [PubMed]
165. El-Sharkawy S, Abul-Hajj YJ. 1988. Microbial cleavage of zearalenone. Xenobiotica 18:365–371. http://dx.doi.org/10.3109/00498258809041672
166. Takahashi-Ando N, Kimura M, Kakeya H, Osada H, Yamaguchi I. 2002. A novel lactonohydrolase responsible for the detoxification of zearalenone: enzyme purification and gene cloning. Biochem J 365:1–6. http://dx.doi.org/10.1042/bj20020450
167. Kosawang C, Karlsson M, Vélëz H, Rasmussen PH, Collinge DB, Jensen B, Jensen DF. 2014. Zearalenone detoxification by zearalenone hydrolase is important for the antagonistic ability of Clonostachys rosea against mycotoxigenic Fusarium graminearum. Fungal Biol 118:364–373. http://dx.doi.org/10.1016/j.funbio.2014.01.005
168. Popiel D, Koczyk G, Dawidziuk A, Gromadzka K, Blaszczyk L, Chelkowski J. 2014. Zearalenone lactonohydrolase activity in Hypocreales and its evolutionary relationships within the epoxide hydrolase subset of a/b-hydrolases. BMC Microbiol 14:82. http://dx.doi.org/10.1186/1471-2180-14-82
169. Kosawang C, Karlsson M, Jensen DF, Dilokpimol A, Collinge DB. 2014. Transcriptomic profiling to identify genes involved in Fusarium mycotoxin Deoxynivalenol and Zearalenone tolerance in the mycoparasitic fungus Clonostachys rosea. BMC Genomics 15:55. http://dx.doi.org/10.1186/1471-2164-15-55
170. Kovalchuk A, Driessen AJ. 2010. Phylogenetic analysis of fungal ABC transporters. BMC Genomics 11:177. http://dx.doi.org/10.1186/1471-2164-11-177 [PubMed]
171. Abou Ammar G, Tryono R, Döll K, Karlovsky P, Deising HB, Wirsel SG. 2013. Identification of ABC transporter genes of Fusarium graminearum with roles in azole tolerance and/or virulence. PLoS One 8:e79042. http://dx.doi.org/10.1371/journal.pone.0079042
172. Dubey MK, Jensen DF, Karlsson M. 2014. An ATP-binding cassette pleiotropic drug transporter protein is required for xenobiotic tolerance and antagonism in the fungal biocontrol agent Clonostachys rosea. Mol Plant Microbe Interact 27:725–732. http://dx.doi.org/10.1094/MPMI-12-13-0365-R
173. Dubey M, Jensen DF, Karlsson M. 2016. The ABC transporter ABCG 29 is involved in H 2O 2 tolerance and biocontrol traits in the fungus Clonostachys rosea. Mol Genet Genomics 291:677–686. http://dx.doi.org/10.1007/s00438-015-1139-y [PubMed]
174. Ruocco M, Lanzuise S, Vinale F, Marra R, Turrà D, Woo SL, Lorito M. 2009. Identification of a new biocontrol gene in Trichoderma atroviride: the role of an ABC transporter membrane pump in the interaction with different plant-pathogenic fungi. Mol Plant Microbe Interact 22:291–301. http://dx.doi.org/10.1094/MPMI-22-3-0291
175. Rosado IV, Rey M, Codón AC, Govantes J, Moreno-Mateos MA, Benítez T. 2007. QID74 Cell wall protein of Trichoderma harzianum is involved in cell protection and adherence to hydrophobic surfaces. Fungal Genet Biol 44:950–964. http://dx.doi.org/10.1016/j.fgb.2007.01.001
176. Seidl-Seiboth V, Gruber S, Sezerman U, Schwecke T, Albayrak A, Neuhof T, von Döhren H, Baker SE, Kubicek CP. 2011. Novel hydrophobins from Trichoderma define a new hydrophobin subclass: protein properties, evolution, regulation and processing. J Mol Evol 72:339–351. http://dx.doi.org/10.1007/s00239-011-9438-3
177. Kubicek CP, Baker S, Gamauf C, Kenerley CM, Druzhinina IS. 2008. Purifying selection and birth-and-death evolution in the class II hydrophobin gene families of the ascomycete Trichoderma/Hypocrea. BMC Evol Biol 8:4. http://dx.doi.org/10.1186/1471-2148-8-4
178. Frischmann A, Neudl S, Gaderer R, Bonazza K, Zach S, Gruber S, Spadiut O, Friedbacher G, Grothe H, Seidl-Seiboth V. 2013. Self-assembly at air/water interfaces and carbohydrate binding properties of the small secreted protein EPL1 from the fungus Trichoderma atroviride. J Biol Chem 288:4278–4287. http://dx.doi.org/10.1074/jbc.M112.427633
179. Gomes EV, Costa MN, de Paula RG, de Azevedo RR, da Silva FL, Noronha EF, Ulhoa CJ, Monteiro VN, Cardoza RE, Gutiérrez S, Silva RN. 2015. The Cerato-Platanin protein Epl-1 from Trichoderma harzianum is involved in mycoparasitism, plant resistance induction and self cell wall protection. Sci Rep 5:17998. http://dx.doi.org/10.1038/srep17998
180. de Jonge R, van Esse HP, Kombrink A, Shinya T, Desaki Y, Bours R, van der Krol S, Shibuya N, Joosten MH, Thomma BP. 2010. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329:953–955. http://dx.doi.org/10.1126/science.1190859
181. Olmedo-Monfil V, Casas-Flores S. 2014. Molecular mechanisms of biocontrol in Trichderma spp. and their applications in agriculture, p 429–453. In Gupta VKS, Schmoll M, Herrera-Estrella A, Upadhyay RS, Druzhinina I, Tuohy MG (ed), Biotechnology and Biology of Trichoderma. Elsevier, Oxford, UK. http://dx.doi.org/10.1016/B978-0-444-59576-8.00032-1
182. Montero-Barrientos M, Hermosa R, Cardoza RE, Gutiérrez S, Monte E. 2011. Functional analysis of the Trichoderma harzianum nox1 gene, encoding an NADPH oxidase, relates production of reactive oxygen species to specific biocontrol activity against Pythium ultimum. Appl Environ Microbiol 77:3009–3016. http://dx.doi.org/10.1128/AEM.02486-10
183. Angelova MB, Pashova SB, Spasova BK, Vassilev SV, Slokoska LS. 2005. Oxidative stress response of filamentous fungi induced by hydrogen peroxide and paraquat. Mycol Res 109:150–158. http://dx.doi.org/10.1017/S0953756204001352 [PubMed]
184. Yang CA, Cheng CH, Lo CT, Liu SY, Lee JW, Peng KC. 2011. A novel L-amino acid oxidase from Trichoderma harzianum ETS 323 associated with antagonism of Rhizoctonia solani. J Agric Food Chem 59:4519–4526. http://dx.doi.org/10.1021/jf104603w [CrossRef]
185. Yang CA, Cheng CH, Lee JW, Lo CT, Liu SY, Peng KC. 2012. Monomeric L-amino acid oxidase-induced mitochondrial dysfunction in Rhizoctonia solani reveals a novel antagonistic mechanism of Trichoderma harzianum ETS 323. J Agric Food Chem 60:2464–2471. http://dx.doi.org/10.1021/jf203883u
186. Sun CB, Suresh A, Deng YZ, Naqvi NI. 2006. A multidrug resistance transporter in Magnaporthe is required for host penetration and for survival during oxidative stress. Plant Cell 18:3686–3705. http://dx.doi.org/10.1105/tpc.105.037861 [PubMed]
187. Zou CG, Tao N, Liu WJ, Yang JK, Huang XW, Liu XY, Tu HH, Gan ZW, Zhang KQ. 2010. Regulation of subtilisin-like protease prC expression by nematode cuticle in the nematophagous fungus Clonostachys rosea. Environ Microbiol 12:3243–3252. http://dx.doi.org/10.1111/j.1462-2920.2010.02296.x [PubMed]
188. Schumacher J, Pradier JM, Simon A, Traeger S, Moraga J, Collado IG, Viaud M, Tudzynski B. 2012. Natural variation in the VELVET gene bcvel1 affects virulence and light-dependent differentiation in Botrytis cinerea. PLoS One 7:e47840. http://dx.doi.org/10.1371/journal.pone.0047840
189. Zeilinger S, Gupta VK, Dahms TE, Silva RN, Singh HB, Upadhyay RS, Gomes EV, Tsui CK, Nayak S C. 2016. Friends or foes? Emerging insights from fungal interactions with plants. FEMS Microbiol Rev 40:182–207. http://dx.doi.org/10.1093/femsre/fuv045 [PubMed]
190. Martinez D, Berka RM, Henrissat B, Saloheimo M, Arvas M, Baker SE, Chapman J, Chertkov O, Coutinho PM, Cullen D, Danchin EGJ, Grigoriev IV, Harris P, Jackson M, Kubicek CP, Han CS, Ho I, Larrondo LF, de Leon AL, Magnuson JK, Merino S, Misra M, Nelson B, Putnam N, Robbertse B, Salamov AA, Schmoll M, Terry A, Thayer N, Westerholm-Parvinen A, Schoch CL, Yao J, Barabote R, Nelson MA, Detter C, Bruce D, Kuske CR, Xie G, Richardson P, Rokhsar DS, Lucas SM, Rubin EM, Dunn-Coleman N, Ward M, Brettin TS. 2008. Corrigendum: Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat Biotechnol 26:1193. http://dx.doi.org/10.1038/nbt1008-1193a
Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016
2017-03-10
2021-04-19

Abstract:

Mycoparasitism is a lifestyle where one fungus establishes parasitic interactions with other fungi. Species of the genus together with are among the most studied fungal mycoparasites. They have wide host ranges comprising several plant pathogens and are used for biological control of plant diseases. as well as mycoparasites efficiently overgrow and kill their fungal prey by using infection structures and by applying lytic enzymes and toxic metabolites. Most of our knowledge on the putative signals and signaling pathways involved in prey recognition and activation of the mycoparasitic response is derived from studies with . These fungi rely on G-protein signaling, the cAMP pathway, and mitogen-activated protein kinase cascades during growth and development as well as during mycoparasitism. The signals being recognized by the mycoparasite may include surface molecules and surface properties as well as secondary metabolites and other small molecules released from the prey. Their exact nature, however, remains elusive so far. Recent genomics-based studies of mycoparasitic fungi of the order , i.e., species, , and , revealed not only several gene families with a mycoparasitism-related expansion of gene paralogue numbers, but also distinct differences between the different mycoparasites. We use this information to illustrate the biological principles and molecular basis of necrotrophic mycoparasitism and compare the mycoparasitic strategies of as a “model” mycoparasite with the behavior and special features of , and .

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

/deliver/fulltext/microbiolspec/5/2/FUNK-0016-2016.html?itemId=/content/journal/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016&mimeType=html&fmt=ahah

Figures

Necrotrophic Mycoparasites and Their Genomes
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016-1,webId=/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016-1,properties={foaf_givenname=Magnus, foaf_name=Magnus Karlsson, foaf_surname=Karlsson, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016-2,webId=/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016-2,properties={foaf_givenname=Lea, foaf_name=Lea Atanasova, foaf_surname=Atanasova, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016-aff2]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016-3,webId=/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016-3,properties={foaf_givenname=Dan Funck, foaf_name=Dan Funck Jensen, foaf_surname=Jensen, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016-aff3]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016-4,webId=/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016-4,properties={foaf_givenname=Susanne, foaf_name=Susanne Zeilinger, foaf_surname=Zeilinger, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016-aff4]]}]]
Citation: Karlsson M, Atanasova L, Jensen D, Zeilinger S. 2017. Necrotrophic mycoparasites and their genomes. microbiolspec 5(2): doi:10.1128/microbiolspec.FUNK-0016-2016
/content/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016.fig1
FIGURE 1
Interaction between hyphae of the mycoparasite and the fungal plant pathogen . Before attack of (expressing cytoplasmic GFP) ( 188 ) by , the apical cell wall extends quickly and is only weakly stained with Congo red, a chitin-specific red fluorescent dye (arrows). Mycoparasitic attack induces tip growth arrest in the prey hyphae, leading to tip swelling and increased chitin deposition in the apical cell wall (arrows). Tip lysis of the prey hyphae results in cytoplasmic leakage (asterisks and inset) and use as nutrient substrate by the mycoparasite. GFP, green fluorescent protein. Scale bars: 20 μm (reprinted from [ 189 ]).
microbiolspec/5/2/FUNK-0016-2016-fig1_thmb.gif
microbiolspec/5/2/FUNK-0016-2016-fig1.gif
Image of FIGURE 1

Click to view

FIGURE 1

Interaction between hyphae of the mycoparasite and the fungal plant pathogen . Before attack of (expressing cytoplasmic GFP) ( 188 ) by , the apical cell wall extends quickly and is only weakly stained with Congo red, a chitin-specific red fluorescent dye (arrows). Mycoparasitic attack induces tip growth arrest in the prey hyphae, leading to tip swelling and increased chitin deposition in the apical cell wall (arrows). Tip lysis of the prey hyphae results in cytoplasmic leakage (asterisks and inset) and use as nutrient substrate by the mycoparasite. GFP, green fluorescent protein. Scale bars: 20 μm (reprinted from [ 189 ]).

Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0016-2016
Permissions and Reprints Request Permissions
Download as Powerpoint

Tables

Necrotrophic Mycoparasites and Their Genomes
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016-1,webId=/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016-1,properties={foaf_givenname=Magnus, foaf_name=Magnus Karlsson, foaf_surname=Karlsson, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016-2,webId=/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016-2,properties={foaf_givenname=Lea, foaf_name=Lea Atanasova, foaf_surname=Atanasova, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016-aff2]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016-3,webId=/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016-3,properties={foaf_givenname=Dan Funck, foaf_name=Dan Funck Jensen, foaf_surname=Jensen, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016-aff3]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016-4,webId=/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016-4,properties={foaf_givenname=Susanne, foaf_name=Susanne Zeilinger, foaf_surname=Zeilinger, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016-aff4]]}]]
Citation: Karlsson M, Atanasova L, Jensen D, Zeilinger S. 2017. Necrotrophic mycoparasites and their genomes. microbiolspec 5(2): doi:10.1128/microbiolspec.FUNK-0016-2016
/content/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016.T1
TABLE 1
Genome sizes and gene numbers of mycoparasites in the Hypocreales order
Generic image for table

Click to view

TABLE 1

Genome sizes and gene numbers of mycoparasites in the Hypocreales order

Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0016-2016
/content/microbiolspec/10.1128/microbiolspec.FUNK-0016-2016.T2
TABLE 2
Predicted number of glycoside hydrolase family 18 genes in mycoparasitic and nonmycoparasitic ascomycete fungi
Generic image for table

Click to view

TABLE 2

Predicted number of glycoside hydrolase family 18 genes in mycoparasitic and nonmycoparasitic ascomycete fungi

Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0016-2016

Supplemental Material

No supplementary material available for this content.

Back to top
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