Effect of deletion of a trichothecene toxin regulatory gene on the secondary metabolism transcriptome of the saprotrophic fungus Trichoderma arundinaceum

Fungal Genetics and Biology

Volumn 119, Issue , 2018, Pages 29-46

  Lindo, Laura ^a   McCormick, Susan P ^b   Cardoza, Rosa E ^a   Brown, Daren W ^b   Kim, Hye Seon ^b   Alexander, Nancy J ^b   Proctor, Robert H ^b   Gutiérrez, Santiago ^a  

^a UNIVERSITY OF LEÓN   (Spain)

^b NATIONAL CENTER FOR AGRICULTURAL UTILIZATION RESEARCH   (United States)

Author keywords

Gene regulation; Metabolomics; Secondary metabolism; Transcriptomics; Trichoderma; Trichothecenes

Indexed keywords

ERGOSTEROL; FARNESYL DIPHOSPHATE; HARZIANUM; MEVALONIC ACID; RNA; TRANSCRIPTOME; TRICHOTHECENE; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; TRICHOTHECENE DERIVATIVE;

ARTICLE; CONTROLLED STUDY; ENZYME SYNTHESIS; FUNGAL GENE; FUNGAL PLANT DISEASE; FUNGUS GROWTH; GENE CLUSTER; GENE DELETION; GENE EXPRESSION REGULATION; GENE FUNCTION; GROWTH INHIBITION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; REGULATOR GENE; RNA SEQUENCE; SAPROTROPH; SECONDARY METABOLISM; TRI6 GENE; TRICHODERMA; TRICHODERMA ARUNDINACEUM; FUSARIUM; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE;

BASE SEQUENCE; ERGOSTEROL; FUSARIUM; GENE EXPRESSION REGULATION, FUNGAL; SECONDARY METABOLISM; SEQUENCE DELETION; TRANSCRIPTOME; TRICHODERMA; TRICHOTHECENES;

EID: 85052854665     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2018.08.002     Document Type: Article

References (64)

1. Alexander, N.J., Proctor, R.H., McCormick, S.P., Genes, gene clusters, and biosynthesis of trichothecenes and fumonisins. Toxin. Rev. 28 (2009), 198–215.
2. Asadollahi, M.A., Maury, J., Møller, K., Nielsen, K.F., Schalk, M., Clark, A., Nielsen, J., Production of plant sesquiterpenes in Saccharomyces cerevisiae: effect of ERG9 repression on sesquiterpene biosynthesis. Biotechnol. Bioeng. 99 (2008), 666–677.
3. Bo, L., Ruotti, V., Stewart, R.M., Thomson, J.A., Dewey, C.N., RNA-Seq gene expression estimation with read mapping uncertainty. Bioinformatics 26 (2010), 493–500.
4. Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976), 248–254.
5. Brown, D.W., McCormick, S.P., Alexander, N.J., Proctor, R.H., Desjardins, A.E., A genetic and biochemical approach to study trichothecene diversity in Fusarium sporotrichioides and Fusarium graminearum. Fungal Genet. Biol. 32 (2001), 121–133.
6. Brown, D.W., Proctor, R.H., Insights into natural products biosynthesis from analysis of 490 polyketide synthases from Fusarium. Fungal Genet. Biol. 89 (2016), 37–51.
7. Cardoza, R.E., Hermosa, M.R., Vizcaíno, J.A., González, F., Llobell, A., Monte, E., Gutiérrez, S., Partial silencing of a hydroxy-methylglutaryl-CoA reductase-encoding gene in Trichoderma harzianum CECT 2413 results in a lower level of resistance to lovastatin and lower antifungal activity. Fungal Genet. Biol. 44 (2007), 269–283.
8. Cardoza, R.E., Malmierca, M.G., Hermosa, M.R., Alexander, N.J., McCormick, S.P., Proctor, R.H., Tijerino, A.M., Rumbero, A., Monte, E., Gutiérrez, S., Identification of loci and functional characterization of trichothecene biosynthesis genes in filamentous fungi of the genus Trichoderma. Appl. Environ. Microbiol. 77 (2011), 4867–4877.
9. Cardoza, R.E., McCormick, S.P., Malmierca, M.G., Olivera, E.R., Alexander, N.J., Monte, E., Gutiérrez, S., Effects of trichothecene production on the plant defense response and fungal physiology: overexpression of the Trichoderma arundinaceum tri4 gene in T. harzianum. Appl. Environ. Microbiol. 81 (2015), 6355–6366.
10. Cardoza, R.E., Vizcaíno, J.A., Hermosa, M.R., Monte, E., Gutiérrez, S., A comparison of the phenotypic and genetic stability of recombinant Trichoderma spp. generated by protoplast- and Agrobacterium-mediated transformation. J. Microbiol. 44 (2006), 383–395.
11. Cardoza, R.E., Vizcaíno, J.A., Hermosa, M.R., Sousa, S., González, F.J., Llobell, A., Monte, E., Gutiérrez, S., Cloning and characterization of the erg1 gene of Trichoderma harzianum: effect of the erg1 sielencing on ergosterol biosynthesis and resistance to terbinafine. Fungal Genet. Biol. 43 (2006), 164–178.
12. Cole, R.J., Schweikert, M.A., Jarvis, B.B., Handbook of Secondary Fungal Metabolites, 3-Volume Set. 2003, Elsevier.
13. Conesa, A., Götz, S., García-Gómez, J.M., Terol, J., Talón, M., Robles, M., Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21 (2005), 3674–3676.
14. Dalmais, B., Schumacher, J., Moraga, J., LE Pêcheur, P., Tudzynski, B., Collado, I.G., Viaud, M., The Botrytis cinerea phytotoxin botcinic acid requires two polyketide synthases for production and has a redundant role in virulence with botrydial. Mol. Plant Pathol. 12 (2011), 564–579.
15. de Groot, M.J., Bundock, P., Hooykaas, P.J., Beijersbergen, A.G., Agrobacterium tumefaciens-mediated transformation of filamentous fungi. Nat. Biotechnol. 16 (1998), 839–842.
16. de Wit, P.J.G.M., van der Burgt, A., Ökmen, B., Stergiopoulos, I., Abd-Elsalam, K.A., Aerts, A.L., Bahkali, A.H., Beenen, H.G., Chettri, P., Cox, M.P., Datema, E., de Vries, R.P., Dhillon, B., Ganley, A.R., Griffiths, S.A., Guo, Y., Hamelin, R.C., Henrissat, B., Kabir, M.S., Jashni, M.K., Kema, G., Klaubauf, S., Lapidus, A., Levasseur, A., Lindquist, E., Mehrabi, R., Ohm, R.A., Owen, T.J., Salamov, A., Schwelm, A., Schijlen, E., Sun, H., van den Burg, H.A., van Ham, R.C.H.J., Zhang, S., Goodwin, S.B., Grigoriev, I.V., Collemare, J., Bradshaw, R.E., The genomes of the fungal plant pathogens Cladosporium fulvum and Dothistroma septosporum reveal adaptation to different hosts and lifestyles but also signatures of common ancestry. PLoS Genet., 8, 2012, e1003088.
17. Degenkolb, T., Dieckmann, R., Nielsen, K.F., Gräfenhan, T., Theis, C., Zafari, D., Chaverri, P., Ismaiel, A., Brückner, H., von Döhren, H., Thrane, U., Petrini, O., Samuels, G.J., Trichoderma brevicompactum clade: a separate lineage with new species, new peptaibiotics, and mycotoxins. Mycol. Prog. 7 (2008), 179–219.
18. Desjardins, A.E., Fusarium mycotoxins, chemistry, genetics and biology. Am. Phytopathol. Soc., 2006.
19. Dyer, R.B., Plattner, R.D., Kendra, D.F., Brown, D.W., Fusarium graminearum TRI14 is required for high virulence and DON production on wheat but not for DON synthesis in vitro. J. Agric. Food Chem. 53 (2005), 9281–9287.
20. Emms, D.M., Kelly, S., OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol., 16, 2015, 157.
21. Fierro, F., Kosalková, K., Gutiérrez, S., Martin, J.F., Autonomously replicating plasmids carrying the AMA1 region in Penicillium chrysogenum. Curr. Genet. 29 (1996), 482–489.
22. Fisch, K.M., Biosynthesis of natural products by microbial iterative hybrid PKS-NRPS. RSC Adv., 3, 2013, 18228.
23. Ghimire, G.P., Lee, H.C., Sohng, J.K., Improved squalene production via modulation of the methylerythritol 4-phosphate pathway and heterologous expression of genes from Streptomyces peucetius ATCC 27952 in Escherichia coli. Appl. Environ. Microbiol. 75 (2009), 7291–7293.
24. Hansen, F.T., Gardiner, D.M., Lysøe, E., Fuertes, P.R., Tudzynski, B., Wiemann, P., Sondergaard, T.E., Giese, H., Brodersen, D.E., Sørensen, J.L., An update to polyketide synthase and non-ribosomal synthetase genes and nomenclature in Fusarium. Fungal Genet. Biol. 75 (2015), 20–29.
25. Hermosa, R., Viterbo, A., Chet, I., Monte, E., Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158 (2012), 17–25.
26. Hohn, T.M., Krishna, R., Proctor, R.H., Characterization of a transcriptional activator controlling trichothecene toxin biosynthesis. Fungal Genet. Biol. 26 (1999), 224–235.
27. Hulvová, H., Galuszka, P., Frébortová, J., Frébort, I., Parasitic fungus Claviceps as a source for biotechnological production of ergot alkaloids. Biotechnol. Adv. 31 (2013), 79–89.
28. Izquierdo-Bueno, I., Moraga, J., Cardoza, R.E., Lindo, L., Hanson, J.R., Gutiérrez, S., Collado, I.G., Relevance of the deletion of the Tatri4 gene in the secondary metabolome of Trichoderma arundinaceum. Org. Biomol. Chem. 16 (2018), 2955–2965.
29. Kikuchi, H., Miyagawa, Y., Sahashi, Y., Inatomi, S., Haganuma, A., Nakahata, N., Oshima, Y., Novel spirocyclic trichothecanes, spirotenuipesine A and B, isolated from entomopathogenic fungus, Paecilomyces tenuipes. J. Org. Chem. 69 (2004), 352–356.
30. Kimura, M., Todai, T., Takahashi-Ando, N., Ohsato, S., Fujimura, M., Molecular and genetic studies of Fusarium trichothecene biosynthesis: pathways, genes, and evolution. Biosci. Biotechnol. Biochem. 71 (2007), 2105–2123.
31. Malmierca, M.G., Barua, J., McCormick, S.P., Izquierdo-Bueno, I., Cardoza, R.E., Alexander, N.J., Hermosa, R., Collado, I.G., Monte, E., Gutiérrez, S., Novel aspinolide production by Trichoderma arundinaceum with a potential role in Botrytis cinerea antagonistic activity and plant defence priming. Environ. Microbiol. 17 (2015), 1103–1118.
32. Malmierca, M.G., Cardoza, R.E., Alexander, N.J., McCormick, S.P., Collado, I.G., Hermosa, R., Monte, E., Gutiérrez, S., Relevance of trichothecenes in fungal physiology: disruption of tri5 in Trichoderma arundinaceum. Fungal Genet. Biol. 53 (2013), 22–33.
33. Malmierca, M.G., Cardoza, R.E., Alexander, N.J., McCormick, S.P., Hermosa, R., Monte, E., Gutiérrez, S., Involvement of Trichoderma trichothecenes in the biocontrol activity and induction of plant defense-related genes. Appl. Environ. Microbiol. 78 (2012), 4856–4868.
34. Malmierca, M.G., Cardoza, R.E., Gutiérrez, S., Trichoderma transformation methods. Genetic Transformation Systems in Fungi, 2015, Springer, 41–48.
35. McCormick, S.P., Stanley, A.M., Stover, N.A., Alexander, N.J., Trichothecenes: from simple to complex mycotoxins. Toxins 3 (2011), 802–814.
36. Medema, M.H., Blin, K., Cimermancic, P., de Jager, V., Zakrzewski, P., Fischbach, M.A., Weber, T., Takano, E., Breitling, R., antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nucleic Acids Res. 39 (2011), W339–W346.
37. Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L., Wold, B., Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5 (2008), 621–628.
38. Nasmith, C.G., Walkowiak, S., Wang, L., Leung, W.W.Y., Gong, Y., Johnston, A., Harris, L.J., Guttman, D.S., Subramaniam, R., Tri6 is a global transcription regulator in the phytopathogen Fusarium graminearum. PLoS Pathog., 7, 2011, e1002266.
39. Niehaus, E.-M., Münsterkötter, M., Proctor, R.H., Brown, D.W., Sharon, A., Idan, Y., Oren-Young, L., Sieber, C.M., Novák, O., Pěnčík, A., Tarkowská, D., Hromadová, K., Freeman, S., Maymon, M., Elazar, M., Youssef, S.A., El-Shabrawy, E.S.M., Shalaby, A.B.A., Houterman, P., Brock, N.L., Burkhardt, I., Tsavkelova, E.A., Dickschat, J.S., Galuszka, P., Güldener, U., Tudzynski, B., Comparative “Omics” of the Fusarium fujikuroi species complex highlights differences in genetic potential and metabolite synthesis. Genome Biol. Evol. 8 (2016), 3574–3599.
40. Penttilä, M., Nevalainen, H., Rättö, M., Salminen, E., Knowles, J., A versatile transformation system for the cellulolytic filamentous fungus Trichoderma reesei. Gene 61 (1987), 155–164.
41. Peplow, A.W., Tag, A.G., Garifullina, G.F., Beremand, M.N., Identification of new genes positively regulated by Tri10 and a regulatory network for trichothecene mycotoxin production. Appl. Environ. Microbiol. 69 (2003), 2731–2736.
42. Pestka, J.J., Yike, I., Dearborn, D.G., Ward, M.D.W., Harkema, J.R., Stachybotrys chartarum, trichothecene mycotoxins, and damp building-related illness: new insights into a public health enigma. Toxicol. Sci. Off. J. Soc. Toxicol. 104 (2008), 4–26.
43. Pfaffl, M.W., Horgan, G.W., Dempfle, L., Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res., 30, 2002, e36.
44. Pinedo, C., Wang, C.-M., Pradier, J.-M., Dalmais, B., Choquer, M., Le Pêcheur, P., Morgant, G., Collado, I.G., Cane, D.E., Viaud, M., Sesquiterpene synthase from the botrydial biosynthetic gene cluster of the phytopathogen Botrytis cinerea. ACS Chem. Biol. 3 (2008), 791–801.
45. Pitt, J.I., Lange, L., Lacey, A.E., Vuong, D., Midgley, D.J., Greenfield, P., Bradbury, M.I., Lacey, E., Busk, P.K., Pilgaard, B., Chooi, Y.-H., Piggott, A.M., Aspergillus hancockii sp. nov., a biosynthetically talented fungus endemic to southeastern Australian soils. PloS One, 12, 2017, e0170254.
46. Proctor, R.H., Desjardins, A.E., Plattner, R.D., Hohn, T.M., A polyketide synthase gene required for biosynthesis of fumonisin mycotoxins in Gibberella fujikuroi mating population A. Fungal Genet. Biol. 27 (1999), 100–112.
47. Proctor, R.H., Hohn, T.M., McCormick, S.P., Desjardins, A.E., Tri6 encodes an unusual zinc finger protein involved in regulation of trichothecene biosynthesis in Fusarium sporotrichioides. Appl. Environ. Microbiol. 61 (1995), 1923–1930.
48. Proctor, R.H., McCormick, S.P., Kim, H.-S., Cardoza, R.E., Stanley, A.M., Lindo, L., Kelly, A., Brown, D.W., Lee, T., Vaughan, M.M., Alexander, N.J., Busman, M., Gutiérrez, S., Evolution of structural diversity of trichothecenes, a family of toxins produced by plant pathogenic and entomopathogenic fungi. PLoS Pathog., 14, 2018, e1006946.
49. Schumacher, J., Gautier, A., Morgant, G., Studt, L., Ducrot, P.-H., Le Pêcheur, P., Azeddine, S., Fillinger, S., Leroux, P., Tudzynski, B., Viaud, M., A functional bikaverin biosynthesis gene cluster in rare strains of Botrytis cinerea is positively controlled by VELVET. PloS One, 8, 2013, e53729.
50. Semeiks, J., Borek, D., Otwinowski, Z., Grishin, N.V., Comparative genome sequencing reveals chemotype-specific gene clusters in the toxigenic black mold Stachybotrys. BMC Genom., 15, 2014, 590.
51. Seong, K.-Y., Pasquali, M., Zhou, X., Song, J., Hilburn, K., McCormick, S., Dong, Y., Xu, J.-R., Kistler, H.C., Global gene regulation by Fusarium transcription factors Tri6 and Tri10 reveals adaptations for toxin biosynthesis. Mol. Microbiol. 72 (2009), 354–367.
52. Stanke, M., Steinkamp, R., Waack, S., Morgenstern, B., AUGUSTUS: a web server for gene finding in eukaryotes. Nucl. Acids Res. 32 (2004), W309–W312.
53. Stanke, M., Keller, O., Gunduz, I., Hayes, A., Waack, S., Morgenstern, B., AUGUSTUS: ab initio prediction of alternative transcripts. Nucl. Acids Res. 34 (2006), W435–W439.
54. Surup, F., Medjedović, A., Szczygielski, M., Schroers, H.-J., Stadler, M., Production of trichothecenes by the apple sooty blotch fungus Microcyclospora tardicrescens. J. Agric. Food Chem. 62 (2014), 3525–3530.
55. Susca, A., Proctor, R.H., Butchko, R.A.E., Haidukowski, M., Stea, G., Logrieco, A., Moretti, A., Variation in the fumonisin biosynthetic gene cluster in fumonisin-producing and nonproducing black aspergilli. Fungal Genet. Biol. 73 (2014), 39–52.
56. Tag, A.G., Garifullina, G.F., Peplow, A.W., Ake, C., Phillips, T.D., Hohn, T.M., Beremand, M.N., A novel regulatory gene, Tri10, controls trichothecene toxin production and gene expression. Appl. Environ. Microbiol. 67 (2001), 5294–5302.
57. Tanaka, M., Fujimori, T., Nabeta, K., Biosynthesis of depudecin, a metabolite of Nimbya scirpicola. Biosci. Biotechnol. Biochem. 64 (2000), 244–247.
58. Trapp, S.C., Hohn, T.M., McCormick, S., Jarvis, B.B., Characterization of the gene cluster for biosynthesis of macrocyclic trichothecenes in Myrothecium roridum. Mol. Gen. Genet. 257 (1998), 421–432.
59. Tudzynski, B., Hölter, K., Gibberellin biosynthetic pathway in Gibberella fujikuroi: evidence for a gene cluster. Fungal Genet. Biol. 25 (1998), 157–170.
60. Venkatasubbaiah, P., Sutton, T.B., Chilton, W.S., The structure and biological properties of secondary metabolites produced by Peltaster fructicola, a fungus associated with apple sooty blotch disease. Plant Dis. 79 (1995), 1157–1160.
61. von Bargen, K.W., Niehaus, E.-M., Krug, I., Bergander, K., Würthwein, E.-U., Tudzynski, B., Humpf, H.-U., Isolation and structure elucidation of fujikurins A-D: products of the PKS19 gene cluster in Fusarium fujikuroi. J. Nat. Prod. 78 (2015), 1809–1815.
62. Wiemann, P., Sieber, C.M.K., von Bargen, K.W., Studt, L., Niehaus, E.-M., Espino, J.J., Huß, K., Michielse, C.B., Albermann, S., Wagner, D., Bergner, S.V., Connolly, L.R., Fischer, A., Reuter, G., Kleigrewe, K., Bald, T., Wingfield, B.D., Ophir, R., Freeman, S., Hippler, M., Smith, K.M., Brown, D.W., Proctor, R.H., Münsterkötter, M., Freitag, M., Humpf, H.-U., Güldener, U., Tudzynski, B., Deciphering the cryptic genome: genome-wide analyses of the rice pathogen Fusarium fujikuroi reveal complex regulation of secondary metabolism and novel metabolites. PLoS Pathog., 9, 2013, e1003475.
63. Wight, W.D., Kim, K.-H., Lawrence, C.B., Walton, J.D., Biosynthesis and role in virulence of the histone deacetylase inhibitor depudecin from Alternaria brassicicola. Mol. Plant. Microbe Interact. 22 (2009), 1258–1267.
64. Xu, Y., Sheng, F., Zhao, J., Chen, L., Li, C., ERG11 mutations and expression of resistance genes in fluconazole-resistant Candida albicans isolates. Arch. Microbiol. 197 (2015), 1087–1093.