1887

Abstract

genome harbours genes encoding 22 non-ribosomal peptide synthetases (NRPSs) with at least one complete module (containing adenylation, thiolation and condensation domains) and four PKS/NRPS (polyketide synthase/NRPS) hybrid enzymes. After a primary screen for expression of these 26 genes when mycelia of are in contact with maize roots, seven genes that are upregulated were selected for further study. Using homologous recombination, loss-of-function mutants in six of these were obtained (the seventh, , was acquired from our previous studies). Plant assays in a hydroponics system revealed that all seven mutants retained the ability to internally colonize maize roots. However, a mutation in one of the PKS/NRPS hybrid genes impaired the ability of to induce the defence response gene (phenylalanine ammonia lyase), suggesting a putative role for the associated metabolite product in induced systemic resistance. Interestingly, the mutant retained its ability to induce another defence response gene (allene oxide synthase). We thus provide evidence that a PKS/NRPS hybrid enzyme is involved in –plant interactions resulting in induction of defence responses.

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2012-01-01
2020-07-09
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References

  1. Aslam S. N., Erbs G., Morrissey K. L., Newman M. A., Chinchilla D., Boller T., Molinaro A., Jackson R. W., Cooper R. M.. ( 2009;). Microbe-associated molecular pattern (MAMP) signatures, synergy, size and charge: influences on perception or mobility and host defence responses. Mol Plant Pathol10:375–387 [CrossRef][PubMed]
    [Google Scholar]
  2. Bakker P. A., Pieterse C. M., van Loon L. C.. ( 2007;). Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology97:239–243 [CrossRef][PubMed]
    [Google Scholar]
  3. Balestrini R., Lanfranco L.. ( 2006;). Fungal and plant gene expression in arbuscular mycorrhizal symbiosis. Mycorrhiza16:509–524 [CrossRef][PubMed]
    [Google Scholar]
  4. Bent A. F., Mackey D.. ( 2007;). Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu Rev Phytopathol45:399–436 [CrossRef][PubMed]
    [Google Scholar]
  5. Bigirimana J., De Meyer G., Poppe J., Elad Y., Höfte M.. ( 1997;). Induction of systemic resistance on bean (Phaseolus vulgaris) by Trichoderma harzianum . Meded Fac Landbouww Toegep Biol Wet Univ Gent62:1001–1007
    [Google Scholar]
  6. Böhnert H. U., Fudal I., Dioh W., Tharreau D., Notteghem J. L., Lebrun M. H.. ( 2004;). A putative polyketide synthase/peptide synthetase from Magnaporthe grisea signals pathogen attack to resistant rice. Plant Cell16:2499–2513 [CrossRef][PubMed]
    [Google Scholar]
  7. Boller T., Felix G.. ( 2009;). A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol60:379–406 [CrossRef][PubMed]
    [Google Scholar]
  8. Brakhage A. A., Schroeckh V.. ( 2011;). Fungal secondary metabolites – strategies to activate silent gene clusters. Fungal Genet Biol48:15–22 [CrossRef][PubMed]
    [Google Scholar]
  9. Buensanteai N., Mukherjee P. K., Horwitz B. A., Cheng C., Dangott L. J., Kenerley C. M.. ( 2010;). Expression and purification of biologically active Trichoderma virens proteinaceous elicitor Sm1 in Pichia pastoris . Protein Expr Purif72:131–138 [CrossRef][PubMed]
    [Google Scholar]
  10. Bushley K. E., Turgeon B. G.. ( 2010;). Phylogenomics reveals subfamilies of fungal nonribosomal peptide synthetases and their evolutionary relationships. BMC Evol Biol10:26 [CrossRef][PubMed]
    [Google Scholar]
  11. Castresana J.. ( 2000;). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol17:540–552[PubMed][CrossRef]
    [Google Scholar]
  12. Chacón M. R., Rodríguez-Galán O., Benítez T., Sousa S., Rey M., Llobell A., Delgado-Jarana J.. ( 2007;). Microscopic and transcriptome analyses of early colonization of tomato roots by Trichoderma harzianum . Int Microbiol10:19–27[PubMed]
    [Google Scholar]
  13. Clay K., Schardl C.. ( 2002;). Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat160:Suppl. 4S99–S127 [CrossRef][PubMed]
    [Google Scholar]
  14. Collemare J., Billard A., Böhnert H. U., Lebrun M. H.. ( 2008a;). Biosynthesis of secondary metabolites in the rice blast fungus Magnaporthe grisea: the role of hybrid PKS-NRPS in pathogenicity. Mycol Res112:207–215 [CrossRef][PubMed]
    [Google Scholar]
  15. Collemare J., Pianfetti M., Houlle A. E., Morin D., Camborde L., Gagey M. J., Barbisan C., Fudal I., Lebrun M. H., Böhnert H. U.. ( 2008b;). Magnaporthe grisea avirulence gene ACE1 belongs to an infection-specific gene cluster involved in secondary metabolism. New Phytol179:196–208 [CrossRef][PubMed]
    [Google Scholar]
  16. De Meyer G., Capieau K., Audenaert K., Buchala A., Métraux J. P., Höfte M.. ( 1999;). Nanogram amounts of salicylic acid produced by the rhizobacterium Pseudomonas aeruginosa 7NSK2 activate the systemic acquired resistance pathway in bean. Mol Plant Microbe Interact12:450–458 [CrossRef][PubMed]
    [Google Scholar]
  17. Distefano G., La Malfa S., Vitale A., Lorito M., Deng Z., Gentile A.. ( 2008;). Defence-related gene expression in transgenic lemon plants producing an antimicrobial Trichoderma harzianum endochitinase during fungal infection. Transgenic Res17:873–879 [CrossRef][PubMed]
    [Google Scholar]
  18. Djonović S., Pozo M. J., Dangott L. J., Howell C. R., Kenerley C. M.. ( 2006;). Sm1, a proteinaceous elicitor secreted by the biocontrol fungus Trichoderma virens induces plant defense responses and systemic resistance. Mol Plant Microbe Interact19:838–853 [CrossRef][PubMed]
    [Google Scholar]
  19. Djonović S., Vargas W. A., Kolomiets M. V., Horndeski M., Wiest A., Kenerley C. M.. ( 2007;). A proteinaceous elicitor Sm1 from the beneficial fungus Trichoderma virens is required for induced systemic resistance in maize. Plant Physiol145:875–889 [CrossRef][PubMed]
    [Google Scholar]
  20. Eley K. L., Halo L. M., Song Z., Powles H., Cox R. J., Bailey A. M., Lazarus C. M., Simpson T. J.. ( 2007;). Biosynthesis of the 2-pyridone tenellin in the insect pathogenic fungus Beauveria bassiana . ChemBioChem8:289–297 [CrossRef][PubMed]
    [Google Scholar]
  21. Elliott C. E., Gardiner D. M., Thomas G., Cozijnsen A., VAN DE Wouw A., Howlett B. J.. ( 2007;). Production of the toxin sirodesmin PL by Leptosphaeria maculans during infection of Brassica napus . Mol Plant Pathol8:791–802 [CrossRef][PubMed]
    [Google Scholar]
  22. Fudal I., Collemare J., Böhnert H. U., Melayah D., Lebrun M. H.. ( 2007;). Expression of Magnaporthe grisea avirulence gene ACE1 is connected to the initiation of appressorium-mediated penetration. Eukaryot Cell6:546–554 [CrossRef][PubMed]
    [Google Scholar]
  23. Gressler M., Zaehle C., Scherlach K., Hertweck C., Brock M.. ( 2011;). Multifactorial induction of an orphan PKS-NRPS gene cluster in Aspergillus terreus . Chem Biol18:198–209 [CrossRef][PubMed]
    [Google Scholar]
  24. Harman G. E., Howell C. R., Viterbo A., Chet I., Lorito M.. ( 2004;). Trichoderma species – opportunistic, avirulent plant symbionts. Nat Rev Microbiol2:43–56 [CrossRef][PubMed]
    [Google Scholar]
  25. Harman G. E., Obregon M. A., Samuels G. J., Lorito M.. ( 2010;). Changing models for commercialization and implementation of biocontrol in the developing and developed world. Plant Dis94:928–939 [CrossRef]
    [Google Scholar]
  26. Hause B., Fester T.. ( 2005;). Molecular and cell biology of arbuscular mycorrhizal symbiosis. Planta221:184–196 [CrossRef][PubMed]
    [Google Scholar]
  27. Hoffmeister D., Keller N. P.. ( 2007;). Natural products of filamentous fungi: enzymes, genes, and their regulation. Nat Prod Rep24:393–416 [CrossRef][PubMed]
    [Google Scholar]
  28. Johnson R. D., Johnson L., Itoh Y., Kodama M., Otani H., Kohmoto K.. ( 2000;). Cloning and characterization of a cyclic peptide synthetase gene from Alternaria alternata apple pathotype whose product is involved in AM-toxin synthesis and pathogenicity. Mol Plant Microbe Interact13:742–753 [CrossRef][PubMed]
    [Google Scholar]
  29. Jones J. D., Dangl J. L.. ( 2006;). The plant immune system. Nature444:323–329 [CrossRef][PubMed]
    [Google Scholar]
  30. Kessler A., Halitschke R., Baldwin I. T.. ( 2004;). Silencing the jasmonate cascade: induced plant defenses and insect populations. Science305:665–668 [CrossRef][PubMed]
    [Google Scholar]
  31. Khaldi N., Collemare J., Lebrun M. H., Wolfe K. H.. ( 2008;). Evidence for horizontal transfer of a secondary metabolite gene cluster between fungi. Genome Biol9:R18 [CrossRef][PubMed]
    [Google Scholar]
  32. Kubicek C. P., Herrera-Estrella A., Seidl-Seiboth V., Martinez D. A., Druzhinina I. S., Thon M., Zeilinger S., Casas-Flores S., Horwitz B. A.. & other authors ( 2011;). Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma . Genome Biol12:R40 [CrossRef][PubMed]
    [Google Scholar]
  33. Leitgeb B., Szekeres A., Manczinger L., Vágvölgyi C., Kredics L.. ( 2007;). The history of alamethicin: a review of the most extensively studied peptaibol. Chem Biodivers4:1027–1051 [CrossRef][PubMed]
    [Google Scholar]
  34. Lorito M., Woo S. L., Harman G. E., Monte E.. ( 2010;). Translational research on Trichoderma: from ’omics to the field. Annu Rev Phytopathol48:395–417 [CrossRef][PubMed]
    [Google Scholar]
  35. Martin F., Kohler A., Duplessis S.. ( 2007;). Living in harmony in the wood underground: ectomycorrhizal genomics. Curr Opin Plant Biol10:204–210 [CrossRef][PubMed]
    [Google Scholar]
  36. Mastouri F., Björkman T., Harman G. E.. ( 2010;). Seed treatment with Trichoderma harzianum alleviates biotic, abiotic, and physiological stresses in germinating seeds and seedlings. Phytopathology100:1213–1221 [CrossRef][PubMed]
    [Google Scholar]
  37. Matsui K.. ( 2006;). Green leaf volatiles: hydroperoxide lyase pathway of oxylipin metabolism. Curr Opin Plant Biol9:274–280 [CrossRef][PubMed]
    [Google Scholar]
  38. Mauch-Mani B., Slusarenko A. J.. ( 1996;). Production of salicylic acid precursors is a major function of phenylalanine ammonia-lyase in the resistance of Arabidopsis to Peronospora parasitica . Plant Cell8:203–212 [CrossRef][PubMed]
    [Google Scholar]
  39. Mukherjee P. K., Kenerley C. M.. ( 2010;). Regulation of morphogenesis and biocontrol properties in Trichoderma virens by a VELVET protein, Vel1. Appl Environ Microbiol76:2345–2352 [CrossRef][PubMed]
    [Google Scholar]
  40. Mukherjee M., Hadar R., Mukherjee P. K., Horwitz B. A.. ( 2003a;). Homologous expression of a mutated β-tubulin gene does not confer benomyl resistance on Trichoderma virens . J Appl Microbiol95:861–867 [CrossRef][PubMed]
    [Google Scholar]
  41. Mukherjee P. K., Latha J., Hadar R., Horwitz B. A.. ( 2003b;). TmkA, a mitogen-activated protein kinase of Trichoderma virens, is involved in biocontrol properties and repression of conidiation in the dark. Eukaryot Cell2:446–455 [CrossRef][PubMed]
    [Google Scholar]
  42. Mukherjee P. K., Wiest A., Ruiz N., Keightley A., Moran-Diez M. E., McCluskey K., Pouchus Y. F., Kenerley C. M.. ( 2011;). Two classes of new peptaibols are synthesized by a single non-ribosomal peptide synthetase of Trichoderma virens . J Biol Chem286:4544–4554 [CrossRef][PubMed]
    [Google Scholar]
  43. Park Y. H., Kenerley C. M., Stack J. P.. ( 1992;). Inoculum dynamics of Gliocladium virens associated with roots of cotton seedlings. Microb Ecol23:169–179 [CrossRef]
    [Google Scholar]
  44. Porras-Alfaro A., Bayman P.. ( 2011;). Hidden fungi, emergent properties: endophytes and microbiomes. Annu Rev Phytopathol49:291–315 [CrossRef][PubMed]
    [Google Scholar]
  45. Pozo M. J., Azcón-Aguilar C.. ( 2007;). Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol10:393–398 [CrossRef][PubMed]
    [Google Scholar]
  46. Reino J. L., Guerrero R. F., Hernandez-Galan R., Collado I. G.. ( 2008;). Secondary metabolites from species of the biocontrol agent Trichoderma . Phytochem Rev7:89–123 [CrossRef]
    [Google Scholar]
  47. Schümann J., Hertweck C.. ( 2007;). Molecular basis of cytochalasan biosynthesis in fungi: gene cluster analysis and evidence for the involvement of a PKS-NRPS hybrid synthase by RNA silencing. J Am Chem Soc129:9564–9565 [CrossRef][PubMed]
    [Google Scholar]
  48. Shank E. A., Kolter R.. ( 2009;). New developments in microbial interspecies signaling. Curr Opin Microbiol12:205–214 [CrossRef][PubMed]
    [Google Scholar]
  49. Shoresh M., Harman G. E.. ( 2008;). The molecular basis of shoot responses of maize seedlings to Trichoderma harzianum T22 inoculation of the root: a proteomic approach. Plant Physiol147:2147–2163 [CrossRef][PubMed]
    [Google Scholar]
  50. Shoresh M., Yedidia I., Chet I.. ( 2005;). Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203 . Phytopathology95:76–84 [CrossRef][PubMed]
    [Google Scholar]
  51. Shoresh M., Gal-On A., Leibman D., Chet I.. ( 2006;). Characterization of a mitogen-activated protein kinase gene from cucumber required for Trichoderma-conferred plant resistance. Plant Physiol142:1169–1179 [CrossRef][PubMed]
    [Google Scholar]
  52. Shoresh M., Harman G. E., Mastouri F.. ( 2010;). Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol48:21–43 [CrossRef][PubMed]
    [Google Scholar]
  53. Sims J. W., Fillmore J. P., Warner D. D., Schmidt E. W.. ( 2005;). Equisetin biosynthesis in Fusarium heterosporum . Chem Commun (Camb)2:186–188 [CrossRef][PubMed]
    [Google Scholar]
  54. Smith J. L., De Moraes C. M., Mescher M. C.. ( 2009;). Jasmonate- and salicylate-mediated plant defense responses to insect herbivores, pathogens and parasitic plants. Pest Manag Sci65:497–503 [CrossRef][PubMed]
    [Google Scholar]
  55. Song Z., Cox R. J., Lazarus C. M., Simpson T. J.. ( 2004;). Fusarin C biosynthesis in Fusarium moniliforme and Fusarium venenatum . ChemBioChem5:1196–1203 [CrossRef][PubMed]
    [Google Scholar]
  56. Swofford D. L.. ( 2002;). paup*: Phylogenetic analysis using parsimony (and other methods), version 4. Sunderland, MA: Sinauer Associates;
  57. Thomas M. D., Kenerley C. M.. ( 1989;). Transformation of the mycoparasite Gliocladium . Curr Genet15:415–420 [CrossRef]
    [Google Scholar]
  58. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G.. ( 1997;). The clustal_x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res25:4876–4882 [CrossRef][PubMed]
    [Google Scholar]
  59. Van der Ent S., Verhagen B. W., Van Doorn R., Bakker D., Verlaan M. G., Pel M. J., Joosten R. G., Proveniers M. C., Van Loon L. C.. & other authors ( 2008;). MYB72 is required in early signaling steps of Rhizobacteria-induced systemic resistance in Arabidopsis . Plant Physiol146:1293–1304 [CrossRef][PubMed]
    [Google Scholar]
  60. van Wees S. C., Luijendijk M., Smoorenburg I., van Loon L. C., Pieterse C. M.. ( 1999;). Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis is not associated with a direct effect on expression of known defense-related genes but stimulates the expression of the jasmonate-inducible gene Atvsp upon challenge. Plant Mol Biol41:537–549 [CrossRef][PubMed]
    [Google Scholar]
  61. Vargas W. A., Djonović S., Sukno S. A., Kenerley C. M.. ( 2008;). Dimerization controls the activity of fungal elicitors that trigger systemic resistance in plants. J Biol Chem283:19804–19815 [CrossRef][PubMed]
    [Google Scholar]
  62. Vargas W. A., Mandawe J. C., Kenerley C. M.. ( 2009;). Plant-derived sucrose is a key element in the symbiotic association between Trichoderma virens and maize plants. Plant Physiol151:792–808 [CrossRef][PubMed]
    [Google Scholar]
  63. Vargas W. A., Crutcher F. K., Kenerley C. M.. ( 2011;). Functional characterization of a plant-like sucrose transporter from the beneficial fungus Trichoderma virens. Regulation of the symbiotic association with plants by sucrose metabolism inside the fungal cells. New Phytol189:777–789 [CrossRef][PubMed]
    [Google Scholar]
  64. Velázquez-Robledo R., Contreras-Cornejo H., Macías-Rodríguez L. I., Hernández-Morales A., Aguirre J., Casas-Flores S., López-Bucio J., Herrera-Estrella A.. ( 2011;). Role of the 4-phosphopantetheinyl transferase of Trichoderma virens in secondary metabolism, and induction of plant defense responses. Mol Plant Microbe Interact24:1459–1471 [CrossRef]
    [Google Scholar]
  65. Vergne E., Ballini E., Marques S., Sidi Mammar B., Droc G., Gaillard S., Bourot S., DeRose R., Tharreau D.. & other authors ( 2007;). Early and specific gene expression triggered by rice resistance gene Pi33 in response to infection by ACE1 avirulent blast fungus. New Phytol174:159–171 [CrossRef][PubMed]
    [Google Scholar]
  66. Verma M., Brar S. K., Tyagi R. D., Surampalli R. Y., Val'ero J. R.. ( 2007;). Antagonistic fungi, Trichoderma spp.: panoply of biological control. Biochem Eng J37:1–20 [CrossRef]
    [Google Scholar]
  67. Viterbo A., Harel M., Horwitz B. A., Chet I., Mukherjee P. K.. ( 2005;). Trichoderma mitogen-activated protein kinase signaling is involved in induction of plant systemic resistance. Appl Environ Microbiol71:6241–6246 [CrossRef][PubMed]
    [Google Scholar]
  68. Viterbo A., Wiest A., Brotman Y., Chet I., Kenerley C. M.. ( 2007;). The 18mer peptaibols from Trichoderma virens elicit plant defence responses. Mol Plant Pathol8:737–746 [CrossRef][PubMed]
    [Google Scholar]
  69. Walters D. R.. ( 2010;). Induced resistance: destined to remain on the sidelines of crop protection?. Phytoparasitica38:1–4 [CrossRef]
    [Google Scholar]
  70. Walton J. D.. ( 2006;). HC-toxin. Phytochem67:1406–1413 [CrossRef]
    [Google Scholar]
  71. Walton J. D., Panaccione D. G., Hallen H. E.. ( 2004;). Peptide synthesis without ribosomes. Advances in Fungal Biotechnology for Industry, Agriculture, and Medicine127–162 Tkacz J., Lange L.. New York: Kluwer Academic;[CrossRef]
    [Google Scholar]
  72. Wiest A., Grzegorski D., Xu B. W., Goulard C., Rebuffat S., Ebbole D. J., Bodo B., Kenerley C. M.. ( 2002;). Identification of peptaibols from Trichoderma virens and cloning of a peptaibol synthetase. J Biol Chem277:20862–20868 [CrossRef][PubMed]
    [Google Scholar]
  73. Yedidia I., Shoresh M., Kerem Z., Benhamou N., Kapulnik Y., Chet I.. ( 2003;). Concomitant induction of systemic resistance to Pseudomonas syringae pv. lachrymans in cucumber by Trichoderma asperellum (T-203) and accumulation of phytoalexins. Appl Environ Microbiol69:7343–7353 [CrossRef][PubMed]
    [Google Scholar]
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