Genetic transformation of Fusarium avenaceum by Agrobacterium tumefaciens mediated transformation and the development of a USER-Brick vector construction system

BMC Molecular Biology

Volumn 15, Issue 1, 2014, Pages

  Sørensen, Lisette Q ^a   Lysøe, Erik ^b   Larsen, Jesper E ^a   Khorsand Jamal, Paiman ^a   Nielsen, Kristian F ^a   Frandsen, Rasmus John N ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b NORWEGIAN INSTITUTE OF BIOECONOMY RESEARCH   (Norway)

Author keywords

Agrobacterium tumefaciens mediated transformation; ATMT; FaPKS6; Fusaristatin; Fusarium avenaceum; Genome modification; LC MS; MS MS; Mycotoxin; Nonribosomal peptide; Polyketide; Single step cloning; Transformation; USER Brick

Indexed keywords

ACETOSYRINGONE; ANTIBIOTIC G 418; DNA FRAGMENT; GENOMIC DNA; HYGROMYCIN; POLYKETIDE SYNTHASE; TYPE II SITE SPECIFIC DEOXYRIBONUCLEASE; DEPSIPEPTIDE; FUSARISTATIN A;

AGAR GEL ELECTROPHORESIS; AGROBACTERIUM TUMEFACIENS; ARTICLE; CHEMICAL ANALYSIS; COCULTURE; FUNGUS GROWTH; FUSARIUM AVENACEUM; GENE DELETION; GENETIC TRANSFORMATION; GENOME; GENOTYPE; HOMOLOGOUS RECOMBINATION; INOCULATION; NONHUMAN; POLYMERASE CHAIN REACTION; FUSARIUM; GENE TARGETING; GENE VECTOR; GENETICS; METABOLISM; MOLECULAR CLONING; NUCLEOTIDE SEQUENCE; PROCEDURES;

AGROBACTERIUM TUMEFACIENS; BASE SEQUENCE; CLONING, MOLECULAR; COCULTURE TECHNIQUES; DEPSIPEPTIDES; FUSARIUM; GENE TARGETING; GENETIC VECTORS; POLYKETIDE SYNTHASES; TRANSFORMATION, GENETIC;

EID: 84904527085     PISSN: None     EISSN: 14712199     Source Type: Journal    
DOI: 10.1186/1471-2199-15-15     Document Type: Article

References (60)

1. Desjardins AE. Gibberella from A (venaceae) to Z (eae). Annu Rev Phytopathol 2003, 41:177-198.
2. Uhlig S, Jestoi M, Parikka P. Fusarium avenaceum - the North European situation. Int J Food Microbiol 2007, 119:17-24.
3. Peters Rick D, Barasubiye Tharcisse DJ. Dry rot of rutabaga caused by Fusarium avenaceum. Hortoscience 2007, 42:737-739.
4. Sørensen JL, Phipps RK, Nielsen KF, Schroers H-J, Frank J, Thrane U. Analysis of Fusarium avenaceum metabolites produced during wet apple core rot. J Agric Food Chem 2009, 57:1632-1639.
5. Mercier J, Markhlouf JMR. Fusarium avenaceum, a pathogen of stored broccoli. Can Plant Dis Surv 1991, 71:161-162.
6. Aprasad KS, Bateman GL, Read PJ. Variation in pathogenicity on potato tubers and sensitivity to thiabendazole of the dry rot fungus Fusarium avenaceum. Potato Res 1997, 40(4):357-365.
7. Kulik T, Pszczółkowska A, Łojko M. Multilocus Phylogenetics show high intraspecific variability within Fusarium avenaceum. Int J Mol Sci 2011, 12(9):5626-5640.
8. Sørensen JL, Giese H. Influence of carbohydrates on secondary metabolism in Fusarium avenaceum. Toxins (Basel) 2013, 5:1655-1663.
9. Herrmann M, Zocher R, Haese A. Effect of disruption of the enniatin synthetase gene on the virulence of Fusarium avenaceum. Mol Plant Microbe Interact 1996, 9:226-232.
10. Frandsen RJN. A guide to binary vectors and strategies for targeted genome modification in fungi using Agrobacterium tumefaciens-mediated transformation. J Microbiol Methods 2011, 87(3):247-262.
11. Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning: A Laboratory Manual 1989, 931-957. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
12. Frandsen RJN, Frandsen M, Giese H. Targeted gene replacement in Fungal Pathogens via Agrobacterium tumefaciens-mediated transformation. Methods Mol Biol 2012, 835:17-45.
13. Yoder WT, Christianson LM. Species-specific primers resolve members of Fusarium section Fusarium. Taxonomic status of the edible " Quorn" fungus reevaluated. Fungal Genet Biol 1998, 23:68-80.
14. Nørholm MHH. A mutant Pfu DNA polymerase designed for advanced uracil-excision DNA engineering. BMC Biotechnol 2010, 10:21.
15. Frandsen RJN, Andersson JA, Kristensen MB, Giese H. Efficient four fragment cloning for the construction of vectors for targeted gene replacement in filamentous fungi. BMC Mol Biol 2008, 9:70.
16. Covert SF, Kapoor P, Lee M, Briley A, Nairn CJ. Agrobacterium tumefaciens-mediated transformation of Fusarium circinatum. Mycol Res 2001, 105(3):259-264.
17. Fulton TR, Ibrahim N, Losada MC, Grzegorski D, Tkacz JS. A melanin polyketide synthase (PKS) gene from Nodulisporium sp. that shows homology to the pks1 gene of Colletotrichum lagenarium. Mol Gen Genet 1999, 262:714-720.
18. Punt PJ, Oliver RP, Dingemanse MA, Pouwels PH, van den Hondel CA. Transformation of Aspergillus based on the hygromycin B resistance marker from Escherichia coli. Gene 1987, 56:117-124.
19. Flaherty JE, Pirttilä AM, Bluhm BH, Woloshuk CP. PAC1, a pH-regulatory gene from Fusarium verticillioides. Appl Environ Microbiol 2003, 69:5222-5227.
20. Pall ML, Brunelli JP. A series of six compact fungal transformation vectors containing polylinkers with multiple unique restriction sites. Fungal Genet Newsl 1993, 40:59-62.
21. Lisby M, Mortensen UH, Rothstein R. Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nat Cell Biol 2003, 5:572-577.
22. Campbell RE, Tour O, Palmer AE, Steinbach PA, Baird GS, Zacharias DA, Tsien RY. A monomeric red fluorescent protein. Proc Natl Acad Sci U S A 2002, 99:7877-7882.
23. Frandsen RJN, Nielsen NJ, Maolanon N, Sørensen JC, Olsson S, Nielsen J, Giese H. The biosynthetic pathway for aurofusarin in Fusarium graminearum reveals a close link between the naphthoquinones and naphthopyrones. Mol Microbiol 2006, 61:1069-1080.
24. Smedsgaard J. Micro-scale extraction procedure for standardization screening of fungal metabolite production in cultures. J Chromatogr A 1997, 760:264-270.
25. Klitgaard A, Iversen A, Andersen MR, Larsen TO, Frisvad JC, Nielsen KF. Aggressive dereplication using UHPLC-DAD-QTOF: screening extracts for up to 3000 fungal secondary metabolites. Anal Bioanal Chem 2014, in press.
26. Broecker S, Herre S, Wüst B, Zweigenbaum J, Pragst F. Development and practical application of a library of CID accurate mass spectra of more than 2,500 toxic compounds for systematic toxicological analysis by LC-QTOF-MS with data-dependent acquisition. Anal Bioanal Chem 2011, 400:101-117.
27. Nielsen KF, Månsson M, Rank C, Frisvad JC, Larsen TO. Dereplication of microbial natural products by LC-DAD-TOFMS. J Nat Prod 2011, 74:2338-2348.
28. Gardiner DM, Jarvis RS, Howlett BJ. The ABC transporter gene in the sirodesmin biosynthetic gene cluster of Leptosphaeria maculans is not essential for sirodesmin production but facilitates self-protection. Fungal Genet Biol 2005, 42:257-263.
29. Sleight SC, Bartley BA, Lieviant JA, Sauro HM. In-Fusion BioBrick assembly and re-engineering. Nucleic Acids Res 2010, 38:2624-2636.
30. Aslanidis C, de Jong PJ. Ligation-independent cloning of PCR products (LIC-PCR). Nucleic Acids Res 1990, 18:6069-6074.
31. Gibson DG, Young L, Chuang R-Y, Venter JC, Hutchison CA, Smith HO. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods 2009, 6:343-345.
32. Nisson PE, Rashtchian A, Watkins PC. Rapid and efficient cloning of Alu-PCR products using uracil DNA glycosylase. PCR Methods Appl 1991, 1:120-123.
33. Nour-Eldin HH, Hansen BG, Nørholm MHH, Jensen JK, Halkier BA. Advancing uracil-excision based cloning towards an ideal technique for cloning PCR fragments. Nucleic Acids Res 2006, 34:e122.
34. Geu-Flores F, Nour-Eldin HH, Nielsen MT, Halkier BA. USER fusion: a rapid and efficient method for simultaneous fusion and cloning of multiple PCR products. Nucleic Acids Res 2007, 35:e55.
35. Olsen LR, Hansen NB, Bonde MT, Genee HJ, Holm DK, Carlsen S, Hansen BG, Patil KR, Mortensen UH, Wernersson R. PHUSER (Primer Help for USER): a novel tool for USER fusion primer design. Nucleic Acids Res 2011, 39(Suppl 2):W61-W67.
36. Hansen BG, Salomonsen B, Nielsen MT, Nielsen JB, Hansen NB, Nielsen KF, Regueira TB, Nielsen J, Patil KR, Mortensen UH. Versatile enzyme expression and characterization system for Aspergillus nidulans, with the Penicillium brevicompactum polyketide synthase gene from the mycophenolic acid gene cluster as a test case. Appl Environ Microbiol 2011, 77:3044-3051.
37. Michielse CB, Hooykaas PJJ, van den Hondel CAMJJ, Ram AFJ. Agrobacterium-mediated transformation as a tool for functional genomics in fungi. Curr Genet 2005, 48:1-17.
38. Abuodeh RO, Orbach MJ, Mandel MA, Das A, Galgiani JN. Genetic transformation of Coccidioides immitis facilitated by Agrobacterium tumefaciens. J Infect Dis 2000, 181:2106-2110.
39. Michielse CB, Ram AFJ, van den Hondel CAMJJ. The Aspergillus nidulans amdS gene as a marker for the identification of multicopy T-DNA integration events in Agrobacterium-mediated transformation of Aspergillus awamori. Curr Genet 2004, 45:399-403.
40. Leclerque A, Wan H, Abschütz A, Chen S, Mitina GV, Zimmermann G, Schairer HU. Agrobacterium-mediated insertional mutagenesis (AIM) of the entomopathogenic fungus Beauveria bassiana. Curr Genet 2004, 45:111-119.
41. Morioka LRI, Furlaneto MC, Bogas AC, Pompermayer P, Duarte RTD, Vieira MLC, Watanabe MAE, Fungaro MHP. Efficient genetic transformation system for the ochratoxigenic fungus Aspergillus carbonarius. Curr Microbiol 2006, 52:469-472.
42. Rho HS, Kang S, Lee YH. Agrobacterium tumefaciens-mediated transformation of the plant pathogenic fungus, Magnaporthe grisea. Mol Cells 2001, 12:407-411.
43. Mullins ED, Chen X, Romaine P, Raina R, Geiser DM, Kang S. Agrobacterium-mediated transformation of Fusarium oxysporum: An Efficient Tool for Insertional Mutagenesis and Gene Transfer. Phytopathology 2001, 91:173-180.
44. Fang W, Zhang Y, Yang X, Zheng X, Duan H, Li Y, Pei Y. Agrobacterium tumefaciens-mediated transformation of Beauveria bassiana using an herbicide resistance gene as a selection marker. J Invertebr Pathol 2004, 85:18-24.
45. Tsuji G, Fujii S, Fujihara N, Hirose C, Tsuge S, Shiraishi T, Kubo Y. Agrobacterium tumefaciens -mediated transformation for random insertional mutagenesis in Colletotrichum lagenarium. J Gen Plant Pathol 2003, 69:230-239.
46. McClelland CM, Chang YC, Kwon-Chung KJ. High frequency transformation of Cryptococcus neoformans and Cryptococcus gattii by Agrobacterium tumefaciens. Fungal Genet Biol 2005, 42:904-913.
47. Michielse CB, Ram AFJ, Hooykaas PJJ, van den Hondel CAMJJ. Role of bacterial virulence proteins in Agrobacterium-mediated transformation of Aspergillus awamori. Fungal Genet Biol 2004, 41:571-578.
48. Leslie JF, Summerell BA. The Fusarium Laboratory Manual 2006, Ames IA, US: Blackwell Publishing, 132 and 176.
49. Rolland S, Jobic C, Fèvre M, Bruel C. Agrobacterium-mediated transformation of Botrytis cinerea, simple purification of monokaryotic transformants and rapid conidia-based identification of the transfer-DNA host genomic DNA flanking sequences. Curr Genet 2003, 44:164-171.
50. Ando A, Sumida Y, Negoro H, Suroto DA, Ogawa J, Sakuradani E, Shimizu S. Establishment of Agrobacterium tumefaciens-mediated transformation of an oleaginous fungus, Mortierella alpina 1S-4, and its application for eicosapentaenoic acid producer breeding. Appl Environ Microbiol 2009, 75:5529-5535.
51. Combier J-P, Melayah D, Raffier C, Gay G, Marmeisse R. Agrobacterium tumefaciens-mediated transformation as a tool for insertional mutagenesis in the symbiotic ectomycorrhizal fungus Hebeloma cylindrosporum. FEMS Microbiol Lett 2003, 220:141-148.
52. Lima IGP, Duarte RTD, Furlaneto L, Baroni CH, Fungaro MHP, Furlaneto MC. Transformation of the entomopathogenic fungus Paecilomyces fumosoroseus with Agrobacterium tumefaciens. Lett Appl Microbiol 2006, 42:631-636.
53. Miyagawa H, Inoue M, Yamanaka H, Tsurushima Tetsu UT. Chemistry of Spore Germination Self-Inhibitors from the Plant Pathogenic Fungus Colletotrichum fragariae. Agrochem Discov Chapter 6, Volume 774 2000, 62-71. Washington, DC: American Chemical Society, Baker DR, Umetsu NK, [ACS Symposium Series (Series editor)].
54. Gaffoor I, Brown DW, Plattner R, Proctor RH, Qi W, Trail F. Functional analysis of the polyketide synthase genes in the filamentous fungus Gibberella zeae (anamorph Fusarium graminearum). Eukaryot Cell 2005, 4:1926-1933.
55. Gauthier GM, Sullivan TD, Gallardo SS, Brandhorst TT, Vanden Wymelenberg AJ, Cuomo CA, Suen G, Currie CR, Klein BS. SREB, a GATA transcription factor that directs disparate fates in Blastomyces dermatitidis including morphogenesis and siderophore biosynthesis. PLoS Pathog 2010, 6:e1000846.
56. Duyvesteijn RGE, van Wijk R, Boer Y, Rep M, Cornelissen BJC, Haring MA. Frp1 is a Fusarium oxysporum F-box protein required for pathogenicity on tomato. Mol Microbiol 2005, 57:1051-1063.
57. Malz S, Grell MN, Thrane C, Maier FJ, Rosager P, Felk A, Albertsen KS, Salomon S, Bohn L, Schäfer W, Giese H. Identification of a gene cluster responsible for the biosynthesis of aurofusarin in the Fusarium graminearum species complex. Fungal Genet Biol 2005, 42:420-433.
58. Ola ARB, Thomy D, Lai D, Brötz-Oesterhelt H, Proksch P. Inducing secondary metabolite production by the endophytic fungus Fusarium tricinctum through coculture with Bacillus subtilis. J Nat Prod 2013, 76:2094-2099.
59. Shiono Y, Tsuchinari M, Shimanuki K, Miyajima T, Murayama T, Koseki T, Laatsch H, Funakoshi T, Takanami K, Suzuki K. Fusaristatins A and B, two new cyclic lipopeptides from an endophytic Fusarium sp. J Antibiot (Tokyo) 2007, 60:309-316.
60. Lim C, Kim J, Choi JN, Ponnusamy K, Jeon Y, Kim S-U, Kim JG, Lee C. Identification, fermentation, and bioactivity against Xanthomonas oryzae of antimicrobial metabolites isolated from Phomopsis longicolla S1B4. J Microbiol Biotechnol 2010, 20:494-500.