Efficient sequential repetitive gene deletions in Neurospora crassa employing a self-excising β-recombinase/six cassette

Journal of Microbiological Methods

Volumn 92, Issue 3, 2013, Pages 236-243

  Szewczyk, Edyta ^a   Kasuga, Takao ^a,b   Fan, Zhiliang ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b United States Department of Agriculture Agricultural Research Service ^*  (United States)

Author keywords

Recombinase; Neurospora crassa; Recyclable self excising marker; Repetitive gene deletion

Indexed keywords

BETA RECOMBINASE; RECOMBINASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CRE 1 GENE; FUNGAL GENE; FUNGAL STRAIN; GENE CASSETTE; GENE DELETION; GENE SEQUENCE; GENETIC RECOMBINATION; MARKER GENE; MUS 51 GENE; NEUROSPORA CRASSA; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REPETITIVE GENE DELETION;

GENE DELETION; GENE TARGETING; GENETICS, MICROBIAL; MOLECULAR BIOLOGY; NEUROSPORA CRASSA; RECOMBINASES;

EID: 84873953188     PISSN: 01677012     EISSN: 18728359     Source Type: Journal    
DOI: 10.1016/j.mimet.2012.12.004     Document Type: Article

References (65)

1. Alonso J.C., Gutierrez C., Rojo F. The role of chromatin-associated protein Hbsu in beta-mediated DNA recombination is to facilitate the joining of distant recombination sites. Mol. Microbiol. 1995, 18:471-478.
2. Austin B., Hall R.M., Tyler B.M. Optimized vectors and selection for transformation of Neurospora crassa and Aspergillus nidulans to bleomycin and phleomycin resistance. Gene 1990, 93:157-162.
3. Avalos J., Geever R.F., Case M.E. Bialaphos resistance as a dominant selectable marker in Neurospora crassa. Curr. Genet. 1989, 16:369-372.
4. Borkovich K.A., Alex L.A., Yarden O., Freitag M., Turner G.E., Read N.D., Seiler S., Bell-Pedersen D., Paietta J., Plesofsky N., Plamann M., Goodrich-Tanrikulu M., Schulte U., Mannhaupt G., Nargang F.E., Radford A., Selitrennikoff C., Galagan J.E., Dunlap J.C., Loros J.J., Catcheside D., Inoue H., Aramayo R., Polymenis M., Selker E.U., Sachs M.S., Marzluf G.A., Paulsen I., Davis R., Ebbole D.J., Zelter A., Kalkman E.R., O'Rourke R., Bowring F., Yeadon J., Ishii C., Suzuki K., Sakai W., Pratt R. Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism. Microbiol. Mol. Biol. Rev. 2004, 68:1-108.
5. Brockman H.E., de Serres F.J. "Sorbose toxicity" in Neurospora. Am. J. Bot. 1963, 50:709-714.
6. Buxton F.P., Radford A. The transformation of mycelial spheroplasts of Neurospora crassa and the attempted isolation of an autonomous replicator. Mol. Gen. Genet. 1984, 196:339-344.
7. Canosa I., Rojo F., Alonso J.C. Site-specific recombination by the β protein from the streptococcal plasmid pSM19035: minimal recombination sequences and crossing over site. Nucleic Acids Res. 1996, 24:2712-2717.
8. Case M.E., Schweizer M., Kushner S.R., Giles N.H. Efficient transformation of Neurospora crassa by utilizing hybrid plasmid DNA. Proc. Natl. Acad. Sci. U. S. A. 1979, 76:5259-5263.
9. Colot H.V., Park G., Turner G.E., Ringelberg C., Crew C.M., Litvinkova L., Weiss R.L., Borkovich K.A., Dunlap J.C. A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:10352-10357.
10. Colot H.V., Park G., Collopy P.D., Krystofova S., Ringelberg C., Crew C., Litvinkova L., Curilla S., Altamirano L., Gorrochotegui-Escalante N., Wang W., Borkovich K.A., Dunlap J.C. How to create gene knockouts in Neurospora Fungal Genetics Stock Center website:. http://www.fgsc.net/neurosporaprotocols/How%20to%20create%20gene%20knockouts%20in%20Neurospora.pdf.
11. Cox M.M. The FLP protein of the yeast 2-μμ plasmid: expression of a eukaryotic genetic recombination system in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 1983, 80:4223-4227.
12. Davis R.H. Neurospora: contributions of a Model Organism 2000, Oxford University Press, Oxford.
13. Davis R.H., Perkins D.D. Timeline: Neurospora: a model of model microbes. Nat. Rev. Genet. 2002, 3:397-403.
14. Díaz V., Rojo F., Martínez A.C., Alonso J.C., Bernad A. The prokaryotic β-recombinase catalyzes site-specific recombination in mammalian cells. J. Biol. Chem. 1999, 274:6634-6640.
15. Ebbole D.J. Vectors for construction of translational fusions to β-galactosidase. Fungal Genet. Newsl. 1990, 37:15.
16. Ebbole D.J., Sachs M.S. A rapid and simple method for isolation of Neurospora crassa homokaryons using microconidia. Fungal Genet. Newsl. 1990, 37:17-18.
17. Fan Z., Wu W., Hildebrand A., Kasuga T., Zhang R., Xiong X. A novel biochemical route for fuels and chemicals production from cellulosic biomass. PLoS One 2012, 7:e31693.
18. Florea S., Andreeva K., Machado C., Mirabito P.M., Schardl C.L. Elimination of marker genes from transformed filamentous fungi by unselected transient transfection with a Cre-expressing plasmid. Fungal Genet. Biol. 2009, 46:721-730.
19. Forment J.V., Ramón D., MacCabe A.P. Consecutive gene deletions in Aspergillus nidulans: application of the Cre/loxP system. Curr. Genet. 2006, 50:217-224.
20. Grant D.M., Lambowitz A.M., Rambosek J.A., Kinsey J.A. Transformation of Neurospora crassa with recombinant plasmids containing the cloned glutamate dehydrogenase (am) gene: evidence for autonomous replication of the transforming plasmid. Mol. Cell. Biol. 1984, 4:2041-2051.
21. Grønlund J.T., Stemmer C., Lichota J., Merkle T., Grasser K.D. Functionality of the β/six site-specific recombination system in tobacco and Arabidopsis: a novel tool for genetic engineering of plant genomes. Plant Mol. Biol. 2007, 63:545-556.
22. Hartmann T., Dümig M., Jaber B.M., Szewczyk E., Olbermann P., Morschhäuser J., Krappmann S. Validation of a self-excising marker in the human pathogen Aspergillus fumigatus by employing the β-rec/six site-specific recombination system. Appl. Environ. Microbiol. 2010, 76:6313-6317.
23. Honda S., Selker E.U. Tools for fungal proteomics: multifunctional Neurospora vectors for gene replacement, protein expression and protein purification. Genetics 2009, 182:11-23.
24. Ishibashi K., Suzuki K., Ando Y., Takakura C., Inoue H. Nonhomologous chromosomal integration of foreign DNA is completely dependent on MUS-53 (human Lig4 homolog) in Neurospora. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:14871-14876.
25. Khrunyk Y., Münch K., Schipper K., Lupas A.N., Kahmann R. The use of FLP-mediated recombination for the functional analysis of an effector gene family in the biotrophic smut fungus Ustilago maydis. New Phytol. 2010, 187:957-968.
26. Kinsey J.A., Rambosek J.A. Transformation of Neurospora crassa with the cloned am (glutamate dehydrogenase) gene. Mol. Cell. Biol. 1984, 4:117-122.
27. Kopke K., Hoff B., Kück U. Application of the Saccharomyces cerevisiae FLP/FRT recombination system in filamentous fungi for marker recycling and construction of knockout strains devoid of heterologous genes. Appl. Environ. Microbiol. 2010, 76:4664-4674.
28. Krappmann S., Bayram O., Braus G.H. Deletion and allelic exchange of the Aspergillus fumigatus veA locus via a novel recyclable marker module. Eukaryot. Cell 2005, 4:1298-1307.
29. Kück U., Hoff B. New tools for the genetic manipulation of filamentous fungi. Appl. Microbiol. Biotechnol. 2010, 86:51-62.
30. Lee S.B., Taylor J.W. Isolation of DNA from fungal mycelia and single spores. PCR Protocols: A Guide to Methods and Applications 1990, Academic Press, Orlando, Florida. M. Innis, D. Gelfand, J. Sninsky, T. White (Eds.).
31. Lee S.B., Milgroom M.G., Taylor J.W. A rapid, high yield mini-prep method for isolation of total genomic DNA from fungi. Fungal Genet. Newsl. 1988, 35:23-24.
32. Lee D.W., Haag J.R., Aramayo R. Construction of strains for rapid homokaryon purification after integration of constructs at the histidine-3 (his-3) locus of Neurospora crassa. Curr. Genet. 2003, 43:17-23.
33. Low W., Jedd G. An improved plasmid for transformation of Neurospora crassa using the pan-2 gene as a selectable marker. Fungal Genet. Rep. 2008, 55:44-45.
34. Mach R.L., Strauss J., Zeilinger S., Schindler M., Kubicek C.P. Carbon catabolite repression of xylanase I (xyn1) gene expression in Trichoderma reesei. Mol. Microbiol. 1996, 21:1273-1281.
35. Mach-Aigner A.R., Pucher M.E., Steiger M.G., Bauer G.E., Preis S.J., Mach R.L. Transcriptional regulation of xyr1, encoding the main regulator of the xylanolytic and cellulolytic enzyme system in Hypocrea jecorina. Appl. Environ. Microbiol. 2008, 74:6554-6562.
36. Margolin B.S., Freitag M., Selker E.U. Improved plasmids for gene targeting at the his-3 locus of Neurospora crassa by electroporation. Fungal Genet. Newsl. 1997, 44:34-36.
37. Margolin B.S., Freitag M., Selker E.U. Improved plasmids for gene targeting at the his-3 locus of Neurospora crassa by electroporation: correction. Fungal Genet. Newsl. 2000, 47:112.
38. McCluskey K., Wiest A., Plamann M. The Fungal Genetics Stock Center: a repository for 50 years of fungal genetics research. J. Biosci. 2010, 35:119-126.
39. McNally M.T., Free S.J. Isolation and characterization of a Neurospora glucose-repressible gene. Curr. Genet. 1988, 14:545-551.
40. Mizutani O., Masaki K., Gomi K., Iefuji H. Modified Cre-loxP recombination in Aspergillus oryzae by direct introduction of Cre recombinase for marker gene rescue. Appl. Environ. Microbiol. 2012, 78:4126-4133.
41. Mylyk O.M., Barry E.G., Galeazzi D.R. New isogenic wild types in N. crassa. Neurospora Newsl. 1974, 21:24.
42. Navarro-Sampedro L., Olmedo M., Corrochano L.M. How to transform Neurospora crassa by electroporation http://www.fgsc.net/neurosporaprotocols/How%20to%20transform%20Nc%20by%20electroporation.pdf.
43. Ninomiya Y., Suzuki K., Ishii C., Inoue H. Highly efficient gene replacements in Neurospora strains deficient for nonhomologous end-joining. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:12248-12253.
44. Paietta J.V., Marzluf G.A. Gene disruption by transformation in Neurospora crassa. Mol. Cell. Biol. 1985, 5:1554-1559.
45. Pall M.L. The use of Ignite (Basta;glufosinate;phosphinothricin) to select transformants of bar-containing plasmids in Neurospora crassa. Fungal Genet. Newsl. 1993, 40:58.
46. Pall M.L., Brunelli J.P. A series of six compact fungal transformation vectors containing polylinkers with multiple unique restriction sites. Fungal Genet. Newsl. 1993, 40:59-62.
47. Pandit A., Maheshwari R. A simple method of obtaining pure microconidia in Neurospora crassa. Fungal Genet. Newsl. 1993, 40:64-65.
48. Perkins D.D. Hints and precautions for the care, feeding and breeding of Neurospora. Fungal Genet. Newsl. 1986, 33:35.
49. Perkins D.D. How to make a cross Fungal Genetics Stock Center website:. http://www.fgsc.net/neurosporaprotocols/How%20to%20make%20a%20cross-2.pdf.
50. Perkins D.D. How to convert wild-type spreading growth to colonial http://www.fgsc.net/neurosporaprotocols/How%20to%20convert%20wild-type%20spreading%20growth%20to%20colonial.pdf.
51. Rojo F., Alonso J.C. A novel site-specific recombinase encoded by the Streptococcus pyogenes plasmid pSM19035. J. Mol. Biol. 1994, 238:159-172.
52. Rojo F., Alonso J.C. The beta recombinase of plasmid pSM19035 binds to two adjacent sites, making different contacts at each of them. Nucleic Acids Res. 1995, 23:3181-3188.
53. Sambrook J., Fritsch E.F., Maniatis T. Molecular Cloning: A Laboratory Manual 1989, Cold Spring harbor Laborotory Press, New York.
54. Shaikh A.C., Sadowski P.D. The Cre recombinase cleaves the lox site in trans. J. Biol. Chem. 1997, 272:5695-5702.
55. Southern E. Southern blotting. Nat. Protoc. 2006, 1:518-525.
56. Staben C., Jensen B.C., Singer M., Pollock J., Schechtman M., Kinsey J.A., Selker E.U. Use of bacterial hygromycin B resistance gene as a dominant selectable marker in Neurospora crassa transformation. Fungal Genet. Newsl. 1989, 36:79-81.
57. Steiger M.G., Vitikainen M., Uskonen P., Brunner K., Adam G., Pakula T., Penttila M., Saloheimo M., Mach R.L., Mach-Aigner A.R. Transformation system for Hypocrea jecorina (Trichoderma reesei) that favors homologous Integration and mmploys reusable didirectionally selectable markers. Appl. Environ. Microbiol. 2011, 77:114-121.
58. Stohl L.L., Akins R.A., Lambowitz A.M. Characterization of deletion derivatives of an autonomously replicating Neurospora plasmid. Nucleic Acids Res. 1984, 12:6169-6178.
59. Straubinger B., Straubinger E., Wirsel S., Turgeon B.G., Yoder O.C. Versatile transformation vectors carrying the bar gene of Streptomyces hygroscopicus. Fungal Genet. Newsl. 1992, 39:82-83.
60. Suzci A., Radford A. ARS8 sequences in the Neurospora genome. Neurospora Newsl. 1983, 30:13.
61. Szewczyk E., Nayak T., Oakley C.E., Edgerton H., Xiong Y., Taheri-Talesh N., Osmani S.A., Oakley B.R. Fusion PCR and gene targeting in Aspergillus nidulans. Nat. Protoc. 2006, 1:3111-3120.
62. Turner G.E., Jimenez T.J., Chae S.K., Baasiri R.A., Borkovich K.A. Utilization of the Aspergillus nidulans pyrG gene as a selectable marker for transformation and electroporation of Neurospora crassa. Fungal Genet. Newsl. 1997, 44:57-59.
63. Vogel H.J. A convenient growth medium for Neurospora. Microbiol. Genet. Bull. 1956, 13:42-46.
64. Zadra I., Abt B., Parson W., Haas H. xylP promoter-based expression system and its use for antisense downregulation of the Penicillium chrysogenum nitrogen regulator NRE. Appl. Environ. Microbiol. 2000, 66:4810-4816.
65. Znameroski E.A., Coradetti S.T., Roche C.M., Tsai J.C., Iavarone A.T., Cate J.H., Glass N.L. Induction of lignocellulose-degrading enzymes in Neurospora crassa by cellodextrins. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:6012-6017.