Minos as a novel Tc1/mariner-type transposable element for functional genomic analysis in Aspergillus nidulans

Fungal Genetics and Biology

Volumn 81, Issue , 2015, Pages 1-11

  Evangelinos, Minoas ^a   Anagnostopoulos, Gerasimos ^a   Karvela Kalogeraki, Iliana ^a   Stathopoulou, Panagiota M ^a   Scazzocchio, Claudio ^b,c   Diallinas, George ^a  

^a UNIVERSITY OF ATHENS   (Greece)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

Author keywords

Class II transposons; Filamentous fungi; Gene tagging; Genetics

Indexed keywords

NITRATE; TRANSPOSASE; TRANSPOSON;

ARTICLE; ASPERGILLUS NIDULANS; CONIDIUM; DNA FLANKING REGION; DNA INTEGRATION; DNA TRANSPOSITION; FUNGAL GENOME; FUNGUS GROWTH; FUNGUS MUTANT; GENE; GENE LOCUS; GENE LOSS; GENE REARRANGEMENT; GENETIC TRANSCRIPTION; GENOME ANALYSIS; MINOS GENE; NIAD GENE; NKUA GENE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; REVERTANT; TEMPERATURE; TRANSPOSON; ULTRAVIOLET RADIATION; ANIMAL; DROSOPHILA; GENE EXPRESSION REGULATION; GENETICS; GENOMICS; MICROBIAL GENETICS; PROCEDURES;

AEPYCEROS MELAMPUS; DROSOPHILA HYDEI; EMERICELLA NIDULANS; FUNGI; FUSARIUM OXYSPORUM; METAZOA;

ANIMALS; ASPERGILLUS NIDULANS; DNA TRANSPOSABLE ELEMENTS; DROSOPHILA; GENETICS, MICROBIAL; GENOMICS; MUTAGENESIS, INSERTIONAL;

EID: 84931264127     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2015.05.007     Document Type: Article

References (61)

1. Amutan M., Nyyssonen E., Stubbs J., Diaz-Torres M.R., Dunn-Coleman N. Identification and cloning of a mobile transposon from Aspergillus niger var. awamori. Curr. Genet. 1996, 29(5):468-473.
2. Arcà B., Zabalou S., Loukeris T.G., Savakis C. Mobilization of a Minos transposon in Drosophila melanogaster chromosomes and chromatid repair by heteroduplex formation. Genetics 1997, 145(2):267-279.
3. Beall E.L., Admon A., Rio D.C. A Drosophila protein homologous to the human p70 Ku autoimmune antigen interacts with the P transposable element inverted repeats. Proc. Natl. Acad. Sci. USA 1994, 91(26):12681-12685.
4. Bellen H.J., Levis R.W., He Y., Carlson J.W., Evans-Holm M., Bae E., et al. The Drosophila gene disruption project: progress using transposons with distinctive site specificities. Genetics 2011, 188(3):731-743. 10.1534/genetics.111.126995.
5. Bellen H.J., Levis R.W., Liao G., He Y., Carlson J.W., Tsang G., et al. The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes. Genetics 2004, 167(2):761-781. 10.1534/genetics.104.026427.
6. Buchon N., Vaury C. RNAi: a defensive RNA-silencing against viruses and transposable elements. Heredity 2006, 96(2):195-202. 10.1038/sj.hdy.6800789.
7. Carr P.D., Tuckwell D., Hey P.M., Simon L., d'Enfert C., Birch M., et al. The transposon impala is activated by low temperatures: use of a controlled transposition system to identify genes critical for viability of Aspergillus fumigatus. Eukaryot. Cell 2010, 9(3):438-448. 10.1128/EC.00324-09.
8. Cecchetto G., Amillis S., Diallinas G., Scazzocchio C., Drevet C. The AzgA purine transporter of Aspergillus nidulans. Characterization of a protein belonging to a new phylogenetic cluster. J. Biol. Chem. 2004, 279(5):3132-3141. 10.1074/jbc.M308826200.
9. Chang Y.C., Timberlake W.E. Identification of Aspergillus brlA response elements (BREs) by genetic selection in yeast. Genetics 1993, 133(1):29-38.
10. Chapman J.R., Taylor M.R., Boulton S.J. Playing the end game: DNA double-strand break repair pathway choice. Mol. Cell 2012, 47(4):497-510. 10.1016/j.molcel.2012.07.029.
11. Chun K.T., Edenberg H.J., Kelley M.R., Goebl M.G. Rapid amplification of uncharacterized transposon-tagged DNA sequences from genomic DNA. Yeast (Chichester, England) 1997, 13(3):233-240. 10.1002/(SICI)1097-0061(19970315)13:3<233::AID-YEA88>3.0.CO;2-E.
12. Daboussi M.-J., Capy P. Transposable elements in filamentous fungi. Annu. Rev. Microbiol. 2003, 57:275-299. 10.1146/annurev.micro.57.030502.091029.
13. Daboussi M.J. Fungal transposable elements and genome evolution. Genetica 1997, 100(1-3):253-260.
14. Daboussi M.J., Langin T. Transposable elements in the fungal plant pathogen Fusarium oxysporum. Genetica 1994, 93(1-3):49-59. 10.1007/BF01435239.
15. Daboussi M.J., Langin T., Brygoo Y. Fot1, a new family of fungal transposable elements. Mol. Gen. Genet.: MGG 1992, 232(1):12-16.
16. Daboussi M.J., Langin T., Deschamps F., Brygoo Y., Scazzocchio C., Burger G. Heterologous expression of the Aspergillus nidulans regulatory gene nirA in Fusarium oxysporum. Gene 1991, 109(1):155-160.
17. de Queiroz M.V., Daboussi M.J. Impala, a transposon from Fusarium oxysporum, is active in the genome of Penicillium griseoroseum. FEMS Microbiol. Lett. 2003, 218(2):317-321.
18. Deschamps F., Langin T., Maurer P., Gerlinger C., Felenbok B., Daboussi M.J. Specific expression of the Fusarium transposon Fot1 and effects on target gene transcription. Mol. Microbiol. 1999, 31(5):1373-1383.
19. Dufresne M., Daboussi M.-J. Development of impala-based transposon systems for gene tagging in filamentous fungi. Methods Mol. Biol. (Clifton, N.J.) 2010, 638:41-54. doi: 10.1007/978-1-60761-611-5_4.
20. Firon A., Villalba F., Beffa R., D'Enfert C. Identification of essential genes in the human fungal pathogen Aspergillus fumigatus by transposon mutagenesis. Eukaryot. Cell 2003, 2(2):247-255.
21. Franz G., Loukeris T.G., Dialektaki G., Thompson C.R., Savakis C. Mobile Minos elements from Drosophila hydei encode a two-exon transposase with similarity to the paired DNA-binding domain. Proc. Natl. Acad. Sci. USA 1994, 91(11):4746-4750.
22. Franz G., Savakis C. Minos, a new transposable element from Drosophila hydei, is a member of the Tc1-like family of transposons. Nucl. Acids Res. 1991, 19(23). 6646-6646.
23. Galanopoulou K., Scazzocchio C., Galinou M.E., Liu W., Borbolis F., Karachaliou M., et al. Purine utilization proteins in the Eurotiales: cellular compartmentalization, phylogenetic conservation and divergence. Fungal Genet. Biol. 2014, 69:96-108. 10.1016/j.fgb.2014.06.005.
24. Glayzer D.C., Roberts I.N., Archer D.B., Oliver R.P. The isolation of Ant1, a transposable element from Aspergillus niger. Mol. Gen. Genet.: MGG 1995, 249(4):432-438.
25. Hamari Z., Amillis S., Drevet C., Apostolaki A., Vágvölgyi C., Diallinas G., Scazzocchio C. Convergent evolution and orphan genes in the Fur4p-like family and characterization of a general nucleoside transporter in Aspergillus nidulans. Mol. Microbiol. 2009, 73(1):43-57. 10.1111/j.1365-2958.2009.06738.x.
26. Han K.H., Han K.Y., Yu J.H., Chae K.S., Jahng K.Y., Han D.M. The nsdD gene encodes a putative GATA-type transcription factor necessary for sexual development of Aspergillus nidulans. Mol. Microbiol. 2001, 41(2):299-309.
27. Hey P., Robson G., Birch M., Bromley M. Characterisation of Aft1 a Fot1/Pogo type transposon of Aspergillus fumigatus. Fungal Genet. Biol.: FG & B 2008, 45(2):117-126. 10.1016/j.fgb.2007.10.009.
28. Ito H., Kakutani T. Control of transposable elements in Arabidopsis thaliana. Chromosome Res.: Int. J. Mol. Supramol. Evolut. Aspects Chromosome Biol. 2014, 22(2):217-223. 10.1007/s10577-014-9417-9.
29. Ivics Z., Izsvák Z. The expanding universe of transposon technologies for gene and cell engineering. Mobile DNA 2010, 1(1). 25-25. 10.1186/1759-8753-1-25.
30. Izsvák Z., Stüwe E.E., Fiedler D., Katzer A., Jeggo P.A., Ivics Z. Healing the wounds inflicted by sleeping beauty transposition by double-strand break repair in mammalian somatic cells. Mol. Cell 2004, 13(2):279-290. 10.1016/S1097-2765(03)00524-0.
31. Joly-Lopez Z., Bureau T.E. Diversity and evolution of transposable elements in Arabidopsis. Chromosome Res.: Int. J. Mol. Supramol. Evolut. Aspects Chromosome Biol. 2014, 22(2):203-216. 10.1007/s10577-014-9418-8.
32. Kempken F., Kück U. Transposons in filamentous fungi - facts and perspectives. BioEssays: News Rev. Mol. Cell. Develop. Biol. 1998, 20(8):652-659. 10.1002/(SICI)1521-1878(199808)20:8<652::AID-BIES8>3.0.CO;2-K.
33. Koukaki M., Giannoutsou E., Karagouni A., Diallinas G. A novel improved method for Aspergillus nidulans transformation. J. Microbiol. Methods 2003, 55(3):687-695.
34. Krypotou E., Evangelidis T., Bobonis J., Pittis A.A., Gabaldón T., Scazzocchio C., et al. Origin, diversification and substrate specificity in the family of NCS1/FUR transporters. Mol. Microbiol. 2015, 10.1111/mmi.12982.
35. Langin T., Capy P., Daboussi M.-J.e. The transposable element impala, a fungal member of the Tc1-mariner superfamily. Mgg Mol. Gen. Genet. 1995, 246(1):19-28. 10.1007/BF00290129.
36. Lee B.-Y., Han S.-Y., Choi H.G., Kim J.H., Han K.-H., Han D.-M. Screening of growth- or development-related genes by using genomic library with inducible promoter in Aspergillus nidulans. J. Microbiol. (Seoul, Korea) 2005, 43(6):523-528.
37. Li Destri Nicosia M.G., Brocard-Masson C., Demais S., Hua Van A., Daboussi M.J., Scazzocchio C. Heterologous transposition in Aspergillus nidulans. Mol. Microbiol. 2001, 39(5):1330-1344.
38. Loukeris T.G., Arcà B., Livadaras I., Dialektaki G., Savakis C. Introduction of the transposable element Minos into the germ line of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 1995, 92(21):9485-9489.
39. Macheda M.L., Hynes M.J., Davis M.A. The Aspergillus nidulans gltA gene encoding glutamate synthase is required for ammonium assimilation in the absence of NADP-glutamate dehydrogenase. Curr. Genet. 1999, 34(6):467-471.
40. Malavazi I., Semighini C.P., Kress M.R.v.Z., Harris S.D., Goldman G.H. Regulation of hyphal morphogenesis and the DNA damage response by the Aspergillus nidulans ATM homolog AtmA. Genetics 2006, 173(1):99-109. 10.1534/genetics.105.052704.
41. Min B., Weinert B.T., Rio D.C. Interplay between Drosophila Bloom's syndrome helicase and Ku autoantigen during nonhomologous end joining repair of P element-induced DNA breaks. Proc. Natl. Acad. Sci. USA 2004, 101(24):8906-8911. 10.1073/pnas.0403000101.
42. Miskey C., Izsvák Z., Kawakami K., Ivics Z. DNA transposons in vertebrate functional genomics. Cell. Mol. Life Sci.: CMLS 2005, 62(6):629-641. 10.1007/s00018-004-4232-7.
43. Muñoz-López M., García-Pérez J.L. DNA transposons: nature and applications in genomics. Curr. Genom. 2010, 11(2):115-128. 10.2174/138920210790886871.
44. Nayak T., Szewczyk E., Oakley C.E., Osmani A., Ukil L., Murray S.L., et al. A versatile and efficient gene-targeting system for Aspergillus nidulans. Genetics 2006, 172(3):1557-1566. 10.1534/genetics.105.052563.
45. Nyyssönen E., Amutan M., Enfield L., Stubbs J., Dunn-Coleman N.S. The transposable element Tan1 of Aspergillus niger var. awamori, a new member of the Fot1 family. Mol. Gen. Genet.: MGG 1996, 253(1-2):50-56.
46. Ogasawara H., Obata H., Hata Y., Takahashi S., Gomi K. Crawler, a novel Tc1/mariner-type transposable element in Aspergillus oryzae transposes under stress conditions. Fungal Genet. Biol. 2009, 46(6-7):441-449. 10.1016/j.fgb.2009.02.007.
47. Pantazopoulou A., Diallinas G. Fungal nucleobase transporters. FEMS Microbiol. Rev. 2007, 31(6):657-675. 10.1111/j.1574-6976.2007.00083.x.
48. Pavlopoulos A., Berghammer A.J., Averof M., Klingler M. Efficient transformation of the beetle Tribolium castaneum using the Minos transposable element: quantitative and qualitative analysis of genomic integration events. Genetics 2004, 167(2):737-746. 10.1534/genetics.103.023085.
49. Pavlopoulos A., Oehler S., Kapetanaki M.G., Savakis C. The DNA transposon Minos as a tool for transgenesis and functional genomic analysis in vertebrates and invertebrates. Genome Biol. 2007, 8(Suppl. 1):S2. 10.1186/gb-2007-8-s1-s2.
50. Plasterk R.H., Izsvák Z., Ivics Z. Resident aliens: the Tc1/mariner superfamily of transposable elements. Trends Genet.: TIG 1999, 15(8):326-332.
51. Ruger-Herreros C., Rodríguez-Romero J., Fernández-Barranco R., Olmedo M., Fischer R., Corrochano L.M., Canovas D. Regulation of conidiation by light in Aspergillus nidulans. Genetics 2011, 188(4):809-822. 10.1534/genetics.111.130096.
52. Ryder E., Russell S. Transposable elements as tools for genomics and genetics in Drosophila. Briefings Funct. Genom. Proteom. 2003, 2(1):57-71.
53. Sambrook J., Fritsch E.F., Maniatis T. Molecular Cloning: A Laboratory Manual 1989, Cold Spring Harbor Laboratory, Cold Spring Harbor. second ed.
54. Sasakura Y., Awazu S., Chiba S., Kano S., Satoh N. Application of Minos, one of the Tc1/mariner superfamily transposable elements, to ascidian embryos as a tool for insertional mutagenesis. Gene 2003, 308:11-20. 10.1016/s0378-1119(03)00426-8.
55. She, W., Cambouris, C.B., Craig, N.L., 2015. Different DNA repair pathways are required following excision and integration of the DNA cut & paste transposon piggyBat in Saccharomyces cerevisiae.
56. Villalba F., Lebrun M.H., Hua-Van A., Daboussi M.J., Grosjean-Cournoyer M.C. Transposon impala, a novel tool for gene tagging in the rice blast fungus Magnaporthe grisea. Mol. Plant-microbe Interact.: MPMI 2001, 14(3):308-315. 10.1094/MPMI.2001.14.3.308.
57. Wang C.-L., Shim W.-B., Shaw B.D. Aspergillus nidulans striatin (StrA) mediates sexual development and localizes to the endoplasmic reticulum. Fungal Genet. Biol.: FG & B 2010, 47(10):789-799. 10.1016/j.fgb.2010.06.007.
58. Wood J.G., Helfand S.L. Chromatin structure and transposable elements in organismal aging. Front. Genet. 2013, 4. 274-274. 10.3389/fgene.2013.00274.
59. Yu J.-H., Hamari Z., Han K.-H., Seo J.-A., Reyes-Domínguez Y., Scazzocchio C. Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet. Biol.: FG & B 2004, 41(11):973-981. 10.1016/j.fgb.2004.08.001.
60. Yu J., Marshall K., Yamaguchi M., Haber J.E., Weil C.F. Microhomology-dependent end joining and repair of transposon-induced DNA hairpins by host factors in Saccharomyces cerevisiae. Mol. Cell Biol. 2004, 24(3):1351-1364.
61. Zagoraiou L., Drabek D., Alexaki S., Guy J.A., Klinakis A.G., Langeveld A., et al. In vivo transposition of Minos, a Drosophila mobile element, in mammalian tissues. Proc. Natl. Acad. Sci. USA 2001, 98(20):11474-11478. 10.1073/pnas.201392398.