Abstract
Twenty-five repetitive elements are first described in the genomes of the arbuscular mycorrhizal (AM) fungi Gigaspora margarita, Gig. rosea and Glomus mosseae. Nineteen repetitive DNA sequences isolated by genomic library screening and four by self-priming PCR had no homology to known DNA sequences, except for two Gig. margarita sequences and one Gig. rosea sequence which showed amino acid similarity to retrotransposons. Part of the Gig. rosea sequence was also similar to a DNA transposon. Two other retrotransposon sequences were isolated using PCR targeting of reverse transcriptase and ribonuclease H domains. Evidence is provided for three gypsy-like LTR retrotransposon and two non-LTR retrotransposon sequences in the AM fungal genomes. Four contain stop codons indicating that they cannot be active. Expression of three retrotransposons was not detected in germinating spores or intraradical hyphae of Gig. margarita. Southern blot analyses indicated that these three sequences are dispersed in the genome and that two are methylated. Sequence analysis of different GmarLTR1 copies showed they have undergone mutations by transitions, which may have been induced by cytosine methylation. Transposable elements may have played a major role in shaping genome structure and size during evolution of the Glomeromycota.
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Abbreviations
- AM fungus:
-
Arbuscular mycorrhizal fungus
- EDTA:
-
Ethylenediaminetetraacetic acid
- EN:
-
Endonuclease
- GSP-PCR:
-
Genomic self-priming polymerase chain reaction
- INT:
-
Integrase
- LSU:
-
Large subunit
- LTR:
-
Long terminal repeat
- M-MLV:
-
Moloney murine leukemia virus
- rDNA:
-
Ribosomal DNA
- RNase H:
-
Ribonuclease H
- RT:
-
Reverse transcriptase
- SDS:
-
Sodium dodecyl sulfate
- SSC:
-
Sodium salt citrate
- SSU:
-
Small subunit
- TAE:
-
Tris/acetic acid/EDTA
References
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Attard A, Gout L, Ross S, Parlange F, Cattolico L, Balesdent MH, Rouxel T (2005) Truncated and RIP-degenerated copies of the LTR-retrotransposon Pholy are clustered in a pericentromeric region of the Leptosphaeria maculans genome. Fungal Genet Biol 42:30–41
Bennetzen JL (2000) Transposable element contributions to plant gene and genome evolution. Plant Mol Biol 42:251–269
Casacuberta JM, Santiago N (2003) Plant LTR-retrotransposons and MITEs: control of transposition and impact on the evolution of plant genes and genomes. Gene 311:1–11
Colot V, Rossignol JL (1999) Eukaryotic DNA methylation as an evolutionary device. BioEssays 21:402–411
Daboussi MJ, Capy P (2003) Transposable elements in filamentous fungi. Ann Rev Microbiol 57:275–299
Ferrol N, Azcon-Aguilar C, Bago B, Franken P, Gollotte A, Gonzalez-Guerrero M, Harrier LA, Lanfranco L, Van Tuinen D, Gianinazzi-Pearson V (2004) Genomics of arbuscular mycorrhizal fungi. In: Aroraand DK, Khachatourians GG (eds) Applied mycology and biotechnology: fungal genomics. Elsevier, pp 379–403
Fierro F, Martin JF (1999) Molecular mechanisms of chromosomal rearrangement in fungi. Crit Rev Microbiol 25:1–17
Flavell AJ, Pearce SR, Heslop-Harrison P, Kumar A (1997) The evolution of Ty1-copia group retrotransposons in eukaryote genomes. Genetica 100:185–195
Galagan JE, Selker EU (2004) RIP: the evolutionary cost of genome defense. Trends Genet 20:417–423
Galagan JE, Henn MR, Ma LJ, Cuomo CA, Birren B (2005) Genomics of the fungal kingdom: insights into eukaryotic biology. Genome Res 15:1620–1631
Gaut BS, Le Thierry D’Ennequin M, Peek AS, Sawkins MC (2000) Maize as a model for the evolution of plant nuclear genomes. Proc Natl Acad Sci USA 97:7008–7015
Gianinazzi-Pearson V, Azcon C, Becard G, Bonfante P, Ferrol N, Franken P, Gollotte A, Harrier LA, Lanfranco L, van Tuinen D (2004) Structural and functional genomics of symbiotic arbuscular mycorrhizal fungi. In: Tkaczand JS, Lange LE (eds) Advances in fungal biotechnology for industry, agriculture, and medicine. Kluwer, New York, pp 405–424
Grace C, Stribley DP (1991) A safer procedure for routine staining of vesicular-arbuscular mycorrhizal fungi. Mycol Res 95:1160–1162
Graia F, Lespinet O, Rimbault B, Dequard-Chablat M, Coppin E, Picard M (2001) Genome quality control: RIP (repeat-induced point mutation) comes to Podospora. Mol Microbiol 40:586–595
Heslop-Harrison JS (2000) Comparative genome organization in plants: from sequence and markers to chromatin and chromosomes. Plant Cell 12:617–635
Hijri M, Sanders IR (2004) The arbuscular mycorrhizal fungus Glomus intraradices is haploid and has small genome size in the lower limit of eukaryotes. Fungal Genet Biol 41:253–261
Hijri M, Sanders IR (2005) Low gene copy number shows that arbuscular mycorrhizal fungi inherit genetically different nuclei. Nature 433:160–163
Hood ME, Katawczik M, Giraud T (2005) Repeat-induced point mutation and the population structure of transposable elements in Microbotryum violaceum. Genetics 170:1081–1089
Hosny M, De Barros JPP, Gianinazzi-Pearson V, Dulieu H (1997) Base composition of DNA from Glomalean fungi: high amounts of methylated cytosine. Fungal Genet Biol 22:103–111
Hosny M, Gianinazzi-Pearson V, Dulieu H (1998) Nuclear DNA content of 11 fungal species in Glomales. Genome 41:422–428
Hosny M, Hijri M, Passerieux E, Dulieu H 1999a rDNA units are highly polymorphic in Scutellospora castanea (Glomales, Zygomycetes). Gene 226:61–71
Hosny M, Van Tuinen D, Jacquin F, Fuller P, Zhao B, Gianinazzi-Pearson V, Franken P 1999b Arbuscular mycorrhizal fungi and bacteria: how to construct prokaryotic DNA-free genomic libraries from the Glomales. FEMS Microbiol Lett 170:425–430
Hsieh J, Fire A (2000) Recognition and silencing of repeated DNA. Annu Rev Genet 34:187–204
Hua-Van A, Hericourt F, Capy P, Daboussi MJ, Langin T (1998) Three highly divergent subfamilies of the impala transposable element coexist in the genome of the fungus Fusarium oxysporum. Mol Gen Genet 259:354–362
Jiang RH, Dawe AL, Weide R, van Staveren M, Peters S, Nuss DL, Govers F (2005) Elicitin genes in Phytophthora infestans are clustered and interspersed with various transposon-like elements. Mol Genet Genomics 273:20–32
Judelson HS (2002) Sequence variation and genomic amplification of a family of gypsy-like elements in the Oomycete genus Phytophthora. Mol Biol Evol 19:1313–1322
Judelson HS, Randall TA (1998) Families of repeated DNA in the oomycete Phytophthora infestans and their distribution within the genus. Genome 41:605–615
Kazazian HH (2004) Mobile elements: drivers of genome evolution. Science 303:1626–1632
Kempken F, Kuck U (1998) Transposons in filamentous fungi-facts and perspectives. BioEssays 20:652–659
Kordis D (2005) A genomic perspective on the chromodomain-containing retrotransposons: chromoviruses. Gene 347:161–173
Kricker MC, Drake JW, Radman M (1992) Duplication-targeted DNA methylation and mutagenesis in the evolution of eukaryotic chromosomes. Proc Natl Acad Sci USA 89:1075–1079
Kuhn G, Hijri M, Sanders IR (2001) Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi. Nature 414:745–748
Kumar A, Bennetzen JL (1999) Plant retrotransposons. Ann Rev Genet 33:479–532
Kumar A, Hirochika H (2001) Applications of retrotransposons as genetic tools in plant biology. Trends Plant Sci 6:127–134
Kuszala C, Gianinazzi S, Gianinazzi-Pearson V (2001) Storage conditions for the long-term survival of AM fungal propagules in wet sieved soil fractions. Symbiosis 30:287–299
Lammers P, Tuskan GA, Difazio SP, Podila GK, Martin F (2004) Mycorrhizal symbionts of Populus to be sequenced by the United States Department of Energy’s Joint Genome Institute. Mycorrhiza 14:63–64
Lanfranco L, Bolchi A, Ros EC, Ottonello S, Bonfante P (2002) Differential expression of a metallothionein gene during the presymbiotic versus the symbiotic phase of an arbuscular mycorrhizal fungus. Plant Physiol 130:58–67
Latijnhouwers M, de Wit PJGM, Govers F (2003) Oomycetes and fungi: similar weaponary to attack plants. Trends Microbiol 11:462–469
LloydMacgilp SA, Chambers SM, Dodd JC, Fitter AH, Walker C, Young JPW (1996) Diversity of the ribosomal internal transcribed spacers within and among isolates of Glomus mosseae and related mycorrhizal fungi. New Phytol 133:103–111
Marchler-Bauer A, Bryant SH (2004) CD-search: protein domain annotations on the fly. Nucleic Acids Res 32:327–331
Martienssen RA, Colot V (2001) DNA methylation and epigenetic inheritance in plants and filamentous fungi. Science 293:1070–1074
McClintock B (1984) The significance of responses of the genome to challenge. Science 226:792–801
Nakayashiki H, Nishimoto N, Ikeda K, Tosa Y, Mayama S (1999) Degenerate MAGGY elements in a subgroup of Pyricularia grisea: a possible example of successful capture of a genetic invader by a fungal genome. Mol Gen Genet 261:958–966
Neumann P, Nouzova M, Macas J (2001) Molecular and cytogenetic analysis of repetitive DNA in pea (Pisum sativum L.). Genome 716–728
Neuveglise C, Sarfati J, Latge JP, Paris S (1996) Afut1, a retrotransposable-like element from Aspergillus fumigatus. Nucleic Acids Res 24:1428–1434
Neuveglise C, Feldmann H, Bon E, Gaillarfin C, Casaregola S (2002) Genomic evolution of the long terminal repeat retrotransposons in hemiascomycetous yeasts. Genome Res 12:930–943
Nielsen ML, Hermanson TD, Aleksenko A (2001) A family of DNA repeats in Aspergillus nidulans has assimilated degenerated retrotransposons. Mol Genet Genomics 265:883–887
Pawlowska TE (2005) Genetic processes in arbuscular mycorrhizal fungi. FEMS Microbiol Lett 251:185–192
Pawlowska TE, Taylor JW (2004) Organization of genetic variation in individuals of arbuscular mycorrhizal fungi. Nature 427:733–737
Queen RA, Gribbon BM, James C, Jack P, Flavell AJ (2004) Retrotransposon-based molecular markers for linkage and genetic diversity analysis in wheat. Mol Gen Genomics 271:91–97
Redecker D, Kodner R, Graham LE (2000) Glomalean fungi from the Ordovician. Science 289:1920–1921
Rodriguez A, Clapp JP, Robinson L, Dodd JC (2005) Studies on the diversity of the distinct phylogenetic lineage encompassing Glomus claroideum and Glomus etunicatum. Mycorrhiza 15:33–46
Sambrook J, Russel DW (2001) Molecular cloning: a laboratory manual, 3rd edn. CSHL Press, New York
San Miguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20:43–45
Schussler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421
Selker EU, Stevens JN (1985) DNA methylation at asymetric sites is associated with numerous transition mutations. Proc Natl Acad Sci USA 82:8114–8118
Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic Press, San Diego
Taylor EJA, Konstantinova P, Leigh F, Bates JA, Lee D (2004) Gypsy-like retrotransposons in Pyrenophora: an abundant and informative class of molecular markers. Genome 47:519–525
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment though sequence weighing, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d’un système radiculaire. Recherche de méthodes d’estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA-Presse, Paris, pp 217–221
van Tuinen D, Jacquot E, Zhao B, Gollotte A, Gianinazzi-Pearson V (1998) Characterization of root colonization profiles by a microcosm community of arbuscular mycorrhizal fungi using 25S rDNA-targeted nested PCR. Mol Ecol 7:879–887
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR protocols: a guide to methods and applications, Academic Press (eds) San Diego, pp 315–322
Wostemeyer J, Kreibich A (2002) Repetitive DNA elements in fungi (Mycota): impact on genomic architecture and evolution. Curr Genet 41:189–198
Young CA, Bryant MK, Christensen MJ, Tapper BA, Bryan GT, Scott B (2005) Molecular cloning and genetic analysis of a symbiosis-expressed gene cluster for lolitrem biosynthesis from a mutualistic endophyte of perennial ryegrass. Mol Gen Genomics 274:13–29
Zeze A, Hosny M, Gianinazzi-Pearson V, Dulieu H (1996) Characterization of a highly repeated DNA sequence (SC1) from the arbuscular mycorrhizal fungus Scutellospora castanea and its detection in planta. Appl Environ Microbiol 62:2443–2448
Zeze A, Hosny M, Van Tuinen D, Gianinazzi-Pearson V, Dulieu H (1999) MYCDIRE, a dispersed repetitive DNA element in arbuscular mycorrhizal fungi. Mycol Res 103:572–576
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Gollotte, A., L’Haridon, F., Chatagnier, O. et al. Repetitive DNA sequences include retrotransposons in genomes of the Glomeromycota. Genetica 128, 455–469 (2006). https://doi.org/10.1007/s10709-006-0019-0
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DOI: https://doi.org/10.1007/s10709-006-0019-0