Abstract
Transposons are usually present in multiple copies in their hosts’ genomes. Recombination between two transposon copies can result in chromosomal rearrangements. Here, we describe a recombination event between two copies of the retrotransposon ANiTa1 within the genome of the fungus Aspergillus niger (strain CBS513.88). The observed chromosomal rearrangement appears to be strain-specific, as the corresponding genomic region in another strain, ATCC1015, shows a different organization. Strain ATCC1015 actually seems to lack full-length ANiTa1 copies and possesses only solo LTR sequences. Presumably strain ATCC1015 was once colonized by ANiTa1, but then the genome subsequently lost the ANiTa1 copies. The striking genomic differences in ANiTa1 copy distribution leading to differences in the chromosomal structure between the two strains, ATTC1015 and CBS513.88, suggest that the activity of transposons may profoundly affect the evolution of different fungal strains.
Similar content being viewed by others
References
Anaya N, Roncero MIG (1996) Stress-induced rearrangement of Fusarium retrotransposon sequences. Mol Gen Genet 253:89–94
Asano Y, Nakazawa A, Kato Y, Kondo K (1989) Properties of a novel D-stereospecific aminopeptidase from Ochrobactrum anthropi. J Biol Chem 264:14233–14239
Baker SE (2006) Aspergillus niger genomics: past, present and into the future. Med Mycol 44(Suppl 1):S17–S21
Braumann I, van den Berg M, Kempken F (2007) Transposons in biotechnologically relevant strains of Aspergillus niger and Penicillium chrysogenum. Fungal Genet Biol 44:1399–1414
Braumann I, van den Berg M, Kempken F (2008) Repeat induced point mutation in two asexual fungi, Aspergillus niger and Penicillium chrysogenum. Curr Genet 53:287–297
Davière JM, Langin T, Daboussi MJ (2001) Potential role of transposable elements in the rapid reorganization of the Fusarium oxysporum genome. Fungal Genet Biol 34:177–192
de Lima Fávaro LC, de Araújo WL, de Azevedo JL, Pacolla-Meirelles LD (2005) The biology and potential for genetic research of transposable elements in filamentous fungi. Genet Mol Biol 28:804–813
Del Sorbo G, Andrade AC, Van Nistelrooy JGM, Van Kan JAL, Balzi E, De Waard MA (1997) Multidrug resistance in Aspergillus nidulans involves novel ATP-binding cassette transporters. Mol Gen Genet 254:417–426
Fierro F, Martín JF (1999) Molecular mechanisms of chromosomal rearrangement in fungi. Crit Rev Microbiol 25:1–17
Fierro F, Gutiérrez S, Díez B, Martín JF (1993) Resolution of four large chromosomes in penicillin-producing filamentous fungi: the penicillin gene cluster is located on chromosome II (9.6 Mb) in Penicillium notatum and chromosome I (10.4 Mb) in Penicillium chrysogenum. Mol Gen Genet 241:573–578
Flipphi MJ, Visser J, van der Veen P, de Graaff LH (1994) Arabinase gene expression in Aspergillus niger: indications for coordinated regulation. Microbiology 140:2673–2682
Hatamoto O, Watarai T, Kikuchi M, Mizusawa K, Sekine H (1996) Cloning and sequencing of the gene encoding tannase and a structural study of the tannase subunit from Aspergillus oryzae. Gene 175:215–221
Hua-Van A, Davière JM, Kaper F, Langin T, Daboussi MJ (2000) Genome organization in Fusarium oxysporum: clusters of class II transposons. Curr Genet 37:339–347
Itoh N, Kawanami T, Liu JQ, Dairi T, Miyakoshi M, Nitta C, Kimoto Y (2001) Cloning and biochemical characterization of Co(2+)-activated bromoperoxidase-esterase (perhydrolase) from Pseudomonas putida IF-3 strain. Biochim Biophys Acta 1545:53–66
Kaneko I, Tanaka A, Tsuge T (2000) REAL, an LTR retrotransposon from the plant pathogenic fungus Alternaria alternata. Mol Gen Genet 263:625–634
Kempken F (2003) Fungal transposable elements: inducers of mutations and molecular tools. In: Arora DK, Khachatourians GG (eds) Applied Mycology and Biotechnology vol 3. Fungal genomics. Elsevier Science Annual Review Series, pp 83–99
Kempken F, Windhofer F (2001) The hAT family: a versatile transposon group common to plants, fungi, animals, and man. Chromosoma 110:1–9
Kempken F, Jacobsen S, Kück U (1998) Distribution of the fungal transposon Restless: full-length and truncated copies in closely related strains. Fungal Genet Biol 25:110–118
Kim JM, Vanguri S, Boeke JD, Gabriel A, Voytas DF (1998) Transposable elements and genome organization: a comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence. Genome Res 8:464–478
Larrondo LF, Canessa P, Vicuna R, Stewart P, Vanden Wymelenberg A, Cullen D (2007) Structure and transcriptional impact of divergent repetitive elements inserted within Phanerochaete chrysosporium strain RP-78 genes. Mol Genet Genomics 277:43–55
Marín S, Sanchis V, Arnau F, Ramos AJ, Magan N (1998) Colonisation and competitiveness of Aspergillus and Penicillium species on maize grain in the presence of Fusarium moniliforme and Fusarium proliferatum. Int J Food Microbiol 45:107–117
Mieczkowski PA, Lemoine FJ, Petes TD (2006) Recombination between retrotransposons as a source of chromosome rearrangements in the yeast Saccharomyces cerevisiae. DNA Repair (Amst) 5:1010–1020
Moore SP, Liti G, Stefanisko KM, Nyswaner KM, Chang C, Louis EJ, Garfinkel DJ (2004) Analysis of a Ty1-less variant of Saccharomyces paradoxus: the gain and loss of Ty1 elements. Yeast 21:649–660
Nitta N, Farman ML, Leong SA (1997) Genome organization of Magnaporthe grisea: integration fo genetic maps, clustering of transposable elements and identification of genome duplications and rearrangements. Theor Appl Genet 95:20–32
Pel HJ, de Winde JH, Archer DB, Dyer PS, Hofmann G, Schaap PJ, Turner G, de Vries RP, Albang R, Albermann K, Andersen MR, Bendtsen JD, Benen JAE, van den Berg M, Breestraat S, Caddick MX, Contreras R, Cornell M, Coutinho PM, Danchin EGJ, Debets AJM, Dekker P, van Dijck PWM, van Dijk A, Dijkhuizen L, Driessen AJM, d‘Enfert C, Geysens S, Goosen C, Groot GSP, de Groot PWJ, Guillemette T, Henrissat B, Herweijer M, van den Hombergh JPTW, van den Hondel CAMJJ, van der Heijden RTJM, van der Kaaij RM, Klis FM, Kools HJ, Kubicek CP, van Kuyk PA, Lauber J, Lu X, van der Maarel MJEC, Meulenberg R, Menke H, Mortimer MA, Nielsen J, Oliver SG, Olsthoorn M, Pal K, van Peij NNME, Ram AFJ, Rinas U, Roubos JA, Sagt CMJ, Schmoll M, Sun J, Ussery D, Varga J, Vervecken W, van de Vondervoort PJJ, Wedler H, Wosten HAB, Zeng A-P, van Ooyen AJJ, Visser J, Stam H (2007) Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat Biotech 25:221–231
Pöggeler S, Kempken F (2004) Mobile genetic elements in mycelial fungi. In: Kück U (ed) The Mycota II, genetics and biotechnology, 2nd edn. Springer, Heidelberg
Selker EU, Cambareri EB, Jensen BC, Haack KR (1987) Rearrangement of duplicated DNA in specialized cells of Neurospora. Cell 51:741–752
Sharma N, Tripathi A (2006) Effects of Citrus sinensis (L.) Osbeck epicarp essential oil on growth and morphogenesis of Aspergillus niger (L.) Van Tieghem. Microbiol Res doi:10.1016/j.micres.2006.06.009
Wöstemeyer J, Kreibich A (2002) Repetitive DNA elements in fungi (Mycota): impact on genomic architecture and evolution. Curr Genet 41:189–198
Xiao H, Jiang N, Schaffner E, Stockinger EJ, van der Knaap E (2008) A retrotransposon-mediated gene duplication underlies morphological variation of tomato fruit. Science 319:1527–1530
Yagawa Y, Kawakami K, Nagano K (1990) Cloning and analysis of the 5′-flanking region of rat Na+/K(+)-ATPase alpha 1 subunit gene. Biochim Biophys Acta 1049:286–292
Young CA, Felliti S, Shields K, Spangenberg G, Johnson RD, Bryan GT, Saika S, Scott B (2006) A complex gene cluster for indole-diterpene biosynthesis in the grass endophyte Netyphodium lolii. Fungal Genet Biol 43:679–693
Zhong S, Steffenson BJ (2007) Molecular karyotyping and chromosome length polymorphism in Cochliobolus sativus. Mycol Res 111:78–86
Acknowledgments
This work was funded in part by DSM Anti-Infectives, Delft. We thank the US Department of Energy, Joint Genome Institute for access to the A. niger ATCC1015 sequence. English language editing of the manuscript was performed by “San Francisco Editing”. Ilka Braumann received a grant of the Max-Buchner-Stiftung.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by J. Perez-Martin.
Rights and permissions
About this article
Cite this article
Braumann, I., van den Berg, M.A. & Kempken, F. Strain-specific retrotransposon-mediated recombination in commercially used Aspergillus niger strain. Mol Genet Genomics 280, 319–325 (2008). https://doi.org/10.1007/s00438-008-0367-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-008-0367-9