Comparative transcriptomics reveals different strategies of Trichoderma mycoparasitism

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Atanasova, Lea ^a   Crom, Stephane Le ^b,c,d,e,f   Gruber, Sabine ^a   Coulpier, Fanny ^b,c,d   Seidl Seiboth, Verena ^a   Kubicek, Christian P ^a   Druzhinina, Irina S ^a  

^a VIENNA UNIVERSITY OF TECHNOLOGY   (Austria)

^b PSL RESEARCH UNIVERSITY   (France)

^c INSERM   (France)

^d CNRS   (France)

^e SORBONNE UNIVERSITÉ   (France)

^f Université René Descartes   (France)

Author keywords

Biocontrol; Gene expression; Hypocrea; Mycoparasitism; T. atroviride; T. reesei; T. virens; Transcriptomics

Indexed keywords

BETA GLUCAN HYDROLASE; BINDING PROTEIN; CELLULASE; CYSTEINE RICH PROTEIN; GLIOTOXIN; GLUTATHIONE; HEMICELLULASE; PROTEINASE; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN; FUNGUS HYPHAE; GENE CONTROL; GENE EXPRESSION; HYPOCREA JECORINA; HYPOCREA VIRENS; MYCOPARASITISM; NONHUMAN; ORGANISMAL INTERACTION; PREDATION; SAPROTROPH; THANATEPHORUS CUCUMERIS; TRANSCRIPTOMICS; TRICHODERMA; TRICHODERMA ATROVIRIDE;

DOWN-REGULATION; GENE EXPRESSION PROFILING; GENES, FUNGAL; MICROBIAL INTERACTIONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RHIZOCTONIA; TRICHODERMA; UP-REGULATION;

FUNGI; HYPOCREA; RHIZOCTONIA; TRICHODERMA; TRICHODERMA ATROVIRIDE;

EID: 84874041895     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-121     Document Type: Article

References (56)

1. Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Kenerley CM, Monte E, Mukherjee PK, Zeilinger S, Grigoriev IV, Kubicek CP. Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol 2011, 9(10):749-759. 10.1038/nrmicro2637, 21921934.
2. Benítez T, Rincón AM, Limón MC, Codón AC. Biocontrol mechanisms of Trichoderma strains. Int Microbiol 2004, 7:249-260.
3. Howell CR. Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis 2003, 87:4-10.
4. Kubicek CP, Herrera-Estrella A, Seidl-Seiboth V, Martinez DA, Druzhinina IS, Thon M, Zeilinger S, Casas-Flores S, Horwitz BA, Mukherjee PK, Mukherjee M, Kredics L, Alcaraz LD, Aerts A, Antal Z, Atanasova L, Cervantes-Badillo MG, Challacombe J, Chertkov O, McCluskey K, Coulpier F, Deshpande N, von Döhren H, Ebbole DJ, Esquivel-Naranjo EU, Fekete E, Flipphi M, Glaser F, Gómez-Rodríguez EY, Gruber S. Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol 2011, 12(4):R40. 10.1186/gb-2011-12-4-r40, 3218866, 21501500.
5. Reithner B, Ibarra-Laclette E, Mach RL, Herrera-Estrella A. Identification of mycoparasitism-related genes in Trichoderma atroviride. Appl Environ Microbiol 2011, 77(13):4361-4370. 10.1128/AEM.00129-11, 3127718, 21531825.
6. Omann MR, Lehner S, Escobar Rodríguez C, Brunner K, Zeilinger S. The seven-transmembrane receptor Gpr1 governs processes relevant for the antagonistic interaction of Trichoderma atroviride with its host. Microbiology 2012, 158(Pt 1):107-118. 3352357, 22075023.
7. Catalano V, Vergara M, Hauzenberger JR, Seiboth B, Sarrocco S, Vannacci G, Kubicek CP, Seidl-Seiboth V. Use of a non-homologous end-joining-deficient strain (delta-ku70) of the biocontrol fungus Trichoderma virens to investigate the function of the laccase gene lcc1 in sclerotia degradation. Curr Genet 2011, 57(1):13-23. 10.1007/s00294-010-0322-2, 3023040, 20872221.
8. Liu PG, Yang Q. Identification of genes with a biocontrol function in Trichoderma harzianum mycelium using the expressed sequence tag approach. Res Microbiol 2005, 156(3):416-423. 10.1016/j.resmic.2004.10.007, 15808946.
9. Vizcaíno JA, Redondo J, Suárez MB, Cardoza RE, Hermosa R, González FJ, Rey M, Monte E. Generation, annotation, and analysis of ESTs from four different Trichoderma strains grown under conditions related to biocontrol. Appl Microbiol Biotechnol 2007, 75(4):853-862. 10.1007/s00253-007-0885-0, 17333173.
10. Suárez MB, Vizcaíno JA, Llobell A, Monte E. Characterization of genes encoding novel peptidases in the biocontrol fungus Trichoderma harzianum CECT 2413 using the TrichoEST functional genomics approach. Curr Genet 2007, 51:331-342. 10.1007/s00294-007-0130-5, 17415567.
11. Samolski I, de Luis A, Vizcaíno JA, Monte E, Suárez MB. Gene expression analysis of the biocontrol fungus Trichoderma harzianum in the presence of tomato plants, chitin, or glucose using a high-density oligonucleotide microarray. BMC Microbiol 2009, 9:217. 10.1186/1471-2180-9-217, 2768740, 19825185.
12. Liu Z, Yang X, Sun D, Song J, Chen G, Juba O, Yang Q. Expressed sequence tags-based identification of genes in a biocontrol strain Trichoderma asperellum. Mol Biol Rep 2010, 37(8):3673-3681. 10.1007/s11033-010-0019-0, 20195770.
13. Rubio MB, Hermosa R, Reino JL, Collado IG, Monte E. Thctf1 transcription factor of Trichoderma harzianum is involved in 6-pentyl-2H-pyran-2-one production and antifungal activity. Fungal Genet Biol 2009, 46(1):17-27. 10.1016/j.fgb.2008.10.008, 19007898.
14. Ogoshi A. Ecology and pathogenicity of anastomosis and intraspecific groups of Rhizoctonia solani Kuhn. Annu Rev Phytopathol 1987, 25:125-143.
15. Dean R, VAN Kan JA, Pretorius ZA, Hammond-Kosack KE, DI Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD. The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 2012, 13(4):414-430. 10.1111/j.1364-3703.2011.00783.x, 22471698.
16. Smyth GK. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004, 3:Article 3.
17. Baker SE, Perrone G, Richardson NM, Gallo A, Kubicek CP. Phylogenomic analysis of polyketide synthase-encoding genes in Trichoderma. Microbiology 2012, 158(Pt 1):147-154.
18. Seiboth B, Aghcheh RK, Phatale PA, Linke R, Hartl L, Sauer DG, Smith KM, Baker SE, Freitag M, Kubicek CP. The putative protein methyltransferase LAE1 controls cellulase gene expression in Trichoderma reesei. Mol Microbiol 2012, 84(6):1150-1164. 10.1111/j.1365-2958.2012.08083.x, 3370264, 22554051.
19. Lorito M, Woo SL, Harman GE, Monte E. Translational research on Trichoderma: from 'omics to the field. Annu Rev Phytopathol 2010, 48:395-417. 10.1146/annurev-phyto-073009-114314, 20455700.
20. Seidl V, Song LF, Lindquist EA, Gruber S, Koptchinskiy A, Zeilinger S, Schmoll M, Martinez P, Sun J, Grigoriev I, Herrera-Estrella A, Baker SE, Kubicek CP. Transcriptomic response of the mycoparasitic fungus Trichoderma atroviride to the close presence of a fungal prey. BMC Genomics 2009, 10:567. 10.1186/1471-2164-10-567, 2794292, 19948043.
21. Rossmann AY, Samuels GJ, Rogerson CT, Lowen R. Genera of Bionectriaceae, Hypocreaceae and Nectriaceae (Hypocreales, Ascomycetes). Stud Mycol 1999, 42:1-83.
22. Stricker AR, Grosstessner-Hain K, Würleitner E, Mach RL. Xyr1 (xylanase regulator 1) regulates both the hydrolytic enzyme system and D-xylose metabolism in Hypocrea jecorina. Eukaryot Cell 2006, 5(12):2128-2137. 10.1128/EC.00211-06, 1694815, 17056741.
23. Patron NJ, Waller RF, Cozijnsen AJ, Straney DC, Gardiner DM, Nierman WC, Howlett BJ. Origin and distribution of epipolythiodioxopiperazine (ETP) gene clusters in filamentous ascomycetes. BMC Evol Biol 2007, 7:174. 10.1186/1471-2148-7-174, 2045112, 17897469.
24. Wilhite SE, Lumsden RD, Straney DC. Mutational analysis of gliotoxin production by the biocontrol fungus Gliocladium virens in relation to suppression of Pythium damping-off. Phytopathology 1994, 84:816-821.
25. Lumsden RD, Locke JC. Biological control of damping-off caused by Pythium ultimum and Rhizoctonia solani with Gliocladium virens in soilless mix. Phytopathology 1989, 79:361-366.
26. Lumsden RD, Locke JC, Adkins ST, Walter JF, Ridout CJ. Isolation and localization of the antibiotic gliotoxin produced by Gliocladium virens from alginate prill in soil and soilless media. Phytopathology 1992, 82:230-235.
27. Wilhite SE, Straney DC. Timing of gliotoxin biosynthesis in the fungal biological control agent Gliocladium virens (Trichoderma virens). Appl Microbiol Biotechnol 1996, 45:513-518.
28. Kumar A, Paietta JV. The sulfur controller-2 negative regulatory gene of Neurospora crassa encodes a protein with beta-transducin repeats. Proc Natl Acad Sci U S A 1995, 92(8):3343-3347. 10.1073/pnas.92.8.3343, 42162, 7724564.
29. Helmstaedt K, Strittmatter A, Lipscomb WN, Braus GH. Evolution of 3-deoxy-D-arabino-heptulosonate-7-phosphate synthase-encoding genes in the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 2005, 102:9784-9789. 10.1073/pnas.0504238102, 1175010, 15987779.
30. Seidl V, Gamauf C, Druzhinina IS, Seiboth B, Hartl L, Kubicek CP. The Hypocrea jecorina (Trichoderma reesei) hypercellulolytic mutant RUT C30 lacks a 85 kb (29 gene-encoding) region of the wild-type genome. BMC Genomics 2008, 11(9):327.
31. Reino JL, Guerrero RF, Hernández-Galan R, Collado IG. Secondary metabolites from species of the biocontrol agent Trichoderma. Phytochem Rev 2008, 7:89-123.
32. Serrano-Carreon L, Hathout Y, Bensoussan M, Belin JM. Metabolism of Linoleic Acid or Mevalonate and 6-Pentyl-α-Pyrone Biosynthesis by Trichoderma Species. Appl Environ Microbiol 1993, 59:2945-2950. 182390, 16349040.
33. Mukherjee PK, Horwitz BA, Kenerley CM. Secondary metabolism in Trichoderma - a genomic perspective. Microbiol 2012, 158:35-45.
34. Kulkarni RD, Thon MR, Pan H, Dean RA. Novel G-protein-coupled receptor-like proteins in the plant pathogenic fungus Magnaporthe grisea. Genome Biol 2005, 6(3):R24. 10.1186/gb-2005-6-3-r24, 1088943, 15774025.
35. Muthumeenakshi S, Sreenivasaprasad S, Rogers CW, Challen MP, Whipps JM. Analysis of cDNA transcripts from Coniothyrium minitans reveals a diverse array of genes involved in key processes during sclerotial mycoparasitism. Fungal Genet Biol 2007, 44(12):1262-1284. 10.1016/j.fgb.2007.07.011, 17888694.
36. Gronover CS, Schumacher J, Hantsch P, Tudzynski B. A novel seven-helix transmembrane protein BTP1 of Botrytis cinerea controls the expression of GST-encoding genes, but is not essential for pathogenicity. Mol Plant Pathol 2005, 6(3):243-256. 10.1111/j.1364-3703.2005.00278.x, 20565654.
37. Xiong S, Fan J, Kitazato K. The antiviral protein cyanovirin-N: the current state of its production and applications. Appl Microbiol Biotechnol 2010, 86(3):805-812. 10.1007/s00253-010-2470-1, 20162270.
38. Neethling D, Nevalainen H. Mycoparasitic species of Trichoderma produce lectins. Can J Microbiol 1996, 42(2):141-146. 10.1139/m96-022, 8742357.
39. Plett JM, Martin F. Poplar root exudates contain compounds that induce the expression of MiSSP7 in Laccaria bicolor. Plant Signal Behav 2012, 7(1):12-15. 10.4161/psb.7.1.18357, 3357351, 22301958.
40. Papapostolou I, Georgiou CD. Superoxide radical induces sclerotial differentiation in filamentous phytopathogenic fungi: a superoxide dismutase mimetics study. Microbiol 2010, 156:960-966.
41. Aliferis KA, Jabaji S. Metabolite composition and bioactivity of Rhizoctonia solani sclerotial exudates. J Agric Food Chem 2010, 58:7604-7615. 10.1021/jf101029a, 20527951.
42. Ruocco M, Lanzuise S, Vinale F, Marra R, Turrà D, Woo SL, Lorito M. 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 2009, 22:291-301. 10.1094/MPMI-22-3-0291, 19245323.
43. Basile LJ, Willson RC, Sewell BT, Benedik MJ. Genome mining of cyanide-degrading nitrilases from filamentous fungi. Appl Microbiol Biotechnol 2008, 80:427-435. 10.1007/s00253-008-1559-2, 18587571.
44. Michelsen CF, Stougaard P. Hydrogen cyanide synthesis and antifungal activity of the biocontrol strain Pseudomonas fluorescens In5 from Greenland is highly dependent on growth medium. Can J Microbiol 2011, 58:381-390.
45. Palmer JM, Keller NP. Secondary metabolism in fungi: does chromosomal location matter?. Curr Opin Microbiol 2010, 13:431-436. 10.1016/j.mib.2010.04.008, 2922032, 20627806.
46. Martinez D, Berka RM, Henrissat B, Saloheimo M, Arvas M, Baker SE, Chapman J, Chertkov O, Coutinho PM, Cullen D, Danchin EG, 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. Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat Biotechnol 2008, 26:553-560. 10.1038/nbt1403, 18454138.
47. Metz B, Seidl-Seiboth V, Haarmann T, Kopchinskiy A, Lorenz P, Seiboth B, Kubicek CP. Expression of biomass-degrading enzymes is a major event during conidium development in Trichoderma reesei. Eukaryot Cell 2011, 10(11):1527-1535. 10.1128/EC.05014-11, 3209057, 21890820.
48. Cuomo CA, Güldener U, Xu JR, Trail F, Turgeon BG, Di Pietro A, Walton JD, Ma LJ, Baker SE, Rep M, Adam G, Antoniw J, Baldwin T, Calvo S, Chang YL, Decaprio D, Gale LR, Gnerre S, Goswami RS, Hammond-Kosack K, Harris LJ, Hilburn K, Kennell JC, Kroken S, Magnuson JK, Mannhaupt G, Mauceli E, Mewes HW, Mitterbauer R, Muehlbauer G. The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 2007, 317:1400-1402. 10.1126/science.1143708, 17823352.
49. Kasuga T, Mannhaupt G, Glass NL. Relationship between phylogenetic distribution and genomic features in Neurospora crassa. PLoS One 2009, 4:e5286. 10.1371/journal.pone.0005286, 2684829, 19461939.
50. Strauss J, Reyes-Dominguez Y. Regulation of secondary metabolism by chromatin structure and epigenetic codes. Fungal Genet Biol 2011, 48:62-69. 10.1016/j.fgb.2010.07.009, 20659575.
51. Bayram O, Braus GH. Coordination of secondary metabolism and development in fungi: the velvet family of regulatory proteins. FEMS Microbiol Rev 2012, 36(1):1-24. 10.1111/j.1574-6976.2011.00285.x, 21658084.
52. Mukherjee PK, Kenerley CM. Regulation of morphogenesis and biocontrol properties in Trichoderma virens by a VELVET protein, Vel1. Appl Environ Microbiol 2010, 76(7):2345-2352. 10.1128/AEM.02391-09, 2849264, 20154111.
53. Chirgwin JM, Przybyla AE, MacDonald RJ, Rutter WJ. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 1979, 18(24):5294-5299. 10.1021/bi00591a005, 518835.
54. Jourdren L, Duclos A, Brion C, Portnoy T, Mathis H, Margeot A, Le Crom S. Teolenn: an efficient and customizable workflow to design high-quality probes for microarray experiments. Nucleic Acids Res 2010, 38:e117. 10.1093/nar/gkq110, 2879536, 20176570.
55. Lemoine S, Combes F, Servant N, Le Crom S. Goulphar: Rapid access and expertise for standard two-color microarray normalization methods. BMC Bioinformatics 2006, 7:467. 10.1186/1471-2105-7-467, 1626094, 17059595.
56. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25(4):402-408. 10.1006/meth.2001.1262, 11846609.