Abstract
We analyze here the presence and abundance of three types of transposable elements (TEs), i.e. Gypsy, RTE and Mariner, in the genome of the grasshopper Eyprepocnemis plorans. PCR experiments allowed amplification, cloning and sequencing of these elements (EploGypI, EploRTE5, EploMar20) from the E. plorans genome. Fluorescent in situ hybridization (FISH) showed that all three elements are restricted to euchromatic regions, thus being absent from the pericentromeric region of all A chromosomes, which contain a satellite DNA (satDNA) and ribosomal DNA (rDNA), and being very scarce in B chromosomes mostly made up of these two types of repetitive DNA. FISH suggested that EploGypI is the most abundant and EploMar20 is the least abundant, with EploRTE5 showing intermediate abundance. An estimation of copy number, by means of quantitative PCR, showed that EploGypI is, by far, the most abundant element, followed by EploRTE5 and EploMar20, in consistency with FISH results. RNA isolation and PCR experiments on complementary DNA (cDNA) showed the presence of transcripts for the three TE elements. The implications of the preferential location of these TE elements into euchromatin, the significance of TE abundance in the giant genome of this species, and a possible relationship between TEs and B chromosome mutability, are discussed.
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References
Baker RJ, Kass DH (1994) Comparison of chromosomal distribution of a retrotransposon (LINE) and a retrovirus-like element mys in Peromyscus maniculatus and P. leucopus. Chromosom Res 2:185–189
Bakkali M, Camacho JPM (2004) The B chromosome polymorphism of the grasshopper Eyprepocnemis plorans in North Africa: III mutation rate of B chromosomes. Heredity 92:428–433
Belyayev A, Raskina O, Nevo E (2001) Chromosomal distribution of reverse transcriptase-containing retroelements in two Triticeae species. Chromosom Res 9:129–136
Bureau TE, Wessler SR (1994) Stowaway: a new family of inverted repeat elements associated to genes of both monocotyledonous abs dicotyledonous plants. Plant Cell 6:907–916
Burke WD, Eickbush DG, Xiong Y, Jakubczak J, Eickbush TH (1993) Sequence relationship of retrotransposable elements R1 and R2 within and between divergent insect species. Mol Biol Evol 10:163–185
Cabrero J, López-León MD, Bakkali M, Camacho JPM (1999) Common origin of B chromosomes variants in the grasshopper Eyprepocnemis plorans. Heredity 83:435–439
Cabrero J, Bugrov A, Warchałowska-Sliwa E, López-León MD, Perfectti F, Camacho JPM (2003a) Comparative FISH analysis in five species of Eyprepocnemidine grasshoppers. Heredity 90:377–381
Cabrero J, Perfectti F, Gómez R, Camacho JPM, López-León MD (2003b) Population variation in the A chromosome distribution of satellite DNA and ribosomal DNA in the grasshopper Eyprepocnemis plorans. Chromosom Res 11:375–381
Camacho JPM (2005) B chromosomes. In: Gregory TR (ed) The evolution of the genome. Elsevier, San Diego, pp 223–286
Camacho JPM, Cabrero J, Viseras E, López-León ND, Navas-Castillo J, Alché JD (1991) G banding in two species of grasshopper and its relationships to C, N and fluorescence banding techniques. Genome 34:638–643
Cermak T, Kubat Z, Hobza R et al (2008) Survey of repetitive sequences in Selene latifolia with respect to their distribution on sex chromosomes. Chromosom Res 16:961–976
Charles M, Belcram H, Just J, Huneau C, Viollet A, Couloux A et al (2008) Dynamics and differential proliferation of transposable elements during the evolution of the B and A genomes of wheat. Genetics 180:1071–1086
Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215–220
Dimitri P, Jukanovic N, Arcà B (2003) Colonization of heterochromatic genes by transposable elements in Drosophila. Mol Biol Evol 20:503–512
Feng J, Zeng R, Chen J (2008) Accurate and efficient data processing for quantitative real-time PCR using a tripartite plant virus as a model. Biotechniques 44:901–912
Feschotte C, Pritham EJ (2007) DNA Transposons and the evolution of eukaryotic Genomes. Annu Rev Genet 41:331–368
Fujiwara H, Osanai M, Matsumoto T, Kojima KK (2005) Telomere-specific non-LTR retrotransposon and telomere maintenance in the silkworm, Bombyx mori. Chromosom Res 13:455–467
Gao D, Gill N, Kim HR et al (2009) A lineage-specific centromere retrotransposon in Oryza brachyantha. Plant J 60:820–831
Gerlach WL, Bedbrook JR (1979) Cloning and characterization of ribosomal RNA genes from wheat and barley. Nucl Acids Res 7:1869–1885
Grandbastien MA (1998) Activation of plant retrotranposons under stress conditions. Trends Plant Sci 3:181–187
Haberer G, Young S, Bharti AK, Gundlach H, Raymond C et al (2005) Structure and architecture of the Maiz genome. Plant Physiol 139:1612–1624
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98
Henriques-Gil N, Arana P (1990) Origin and substitution of B chromosomes in the grasshopper Eyprepocnemis plorans. Evolution 44:747–753
Hsieh J, Fire A (2000) Recognition and silencing of repeated DNA. Annu Rev Genet 34:187–204
Jacobs G, Dechyeva D, Menzel G, Dombrowski C, Schmidt T (2004) Molecular characterization of Vulmar 1, a complete mariner transposon of sugar beet and diversity of mariner and En/Spm like sequences in the genus Beta. Genome 47:1192–1201
Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J (2005) Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110:462–467
Kapitonov VV, Jurka J (2005) RAGI core and V(D)J recombination signal sequences were derived from Transib transposons. PLoS Biol 3:e181
Kasschau KD, Fahlgren N, Chapman EJ et al (2007) Genome-wide profiling and analysis of arabidopsis siRNA. PLoS Biol 5:e57
Kazazian HH (1999) An estimated frequency of endogenous insertional mutations in humans. Nat Genet 22:130
Kidwell MG (2002) Transposable elements and the evolution of genome size in eukaryotes. Genetica 115:49–63
Kidwell MG (2005) Transposable elements. In: Gregory TR (ed) The evolution of the genome. Elsevier, San Diego, pp 165–221
Kidwell MG, Lish D (1997) Transposable elements as sources of variation animals and plants. Proc Natl Acad Sci USA 94:7704–7711
Kidwell MG, Lish D (2000) Transposable elements and genome evolution. TREE 15:95–99
Lamb JC, Riddle NC, Cheng YM, Theuri J, Birchler JA (2007) Location and transcription of a retrotransposon-derived element on the maize B chromosome. Chromosom Res 15:383–398
Lander ES, Linton LM, Birren B et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921
Lipatov M, Lenko K, Petrov DA, Bergman CM (2005) Paucity of chimeric gene-transposable element transcripts in the Drosophila melanogaster genome. BMC Biol 3:24
López-León MD, Cabrero J, Pardo MC, Viseras E, Camacho JPM, Santos JL (1993) Generating high variability of B chromosomes in Eyprepocnemis plorans (grasshopper). Heredity 71:352–362
López-León MD, Neves N, Schwarzacher T, Heslop-Harrison JS, Hewitt GM, Camacho JPM (1994) Possible origin of B chromosome deduced from its DNA composition using double FISH technique. Chromosom Res 2:87–92
López-León MD, Vázquez P, Hewitt GM, Camacho JPM (1995) Cloning and sequence analysis of an extremely homogeneous tandemly repeated DNA in the grasshopper Eyprepocnemis plorans. Heredity 75:370–375
Mariño-Ramírez L, Lewis KC, Landsman D, Jordan IK (2005) Transposable elements donate lineage-specific regulatory sequences to host genomes. Cytogenet Genome Res 110:333–341
Miller K, Lynch C, Martin J, Herniou E, Tristem M (1999) Identification of multiple Gypsy LTR-retrotransposon lineages in vertebrate genomes. J Mol Evol 49:358–366
Mukabayire O, Besansky NJ (1996) Distribution of T1, Q, Pegasus and mariner transposable elements on the polytene chromosomes of PEST, a standard strain of Anopheles gambiae. Chromosoma 104:585–595
Muñoz-López M, Siddique A, Bischerour J et al (2008) Transposition of Mboumar-9: identification of a new naturally active mariner-family transposon. J Mol Biol 382:567–572
Nekrutenko A, Li WH (2001) Transposable elements are found in a large number of human protein-coding genes. Trends Genet 17:619–621
Pardue ML (1995) Drosophila telomeres: another way to end it all. In: Blackbum EH, Graider CW (eds) Telomeres. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 339–370
Paux ED, Roger D, Badaeva E, Gay G, Bernard M et al (2006) Characterizing the composition and evolution of homoeologous genomes in hexaploid wheat through BAC-end sequencing on chromosome 3B. Plan J 48:463–478
Rebuzzini P, Castiglia R, Nergadze G et al (2009) Quantitative variation of LINE-1 sequences in five species and three subspecies of the subgenus Mus and in five Robertsonian races of Mus musculus domesticus. Chromosom Res 17:65–76
Rose T (2003) CODEHOP (COnsensus-DEgenerate hybrid oligonucleotide Primer) PCR primer design. Nucl Acids Res 31:3763–3766
Ruiz-Ruano FJ, Ruiz-Estévez M, Rodríguez-Pérez J, López-Pino JL, Cabrero J, Camacho JPM (2011) DNA amount of X and B chromosomes in the grasshoppers Eyprepocnemis plorans and Locusta migratoria. Cytogenet Genome Res 134:120–126
Santiago M, Hérraiz C, Goñi JR, Messeguer X, Casacuberta JM (2002) Genome wide analysis of the Emigrant family of MITEs of Arabidopsis thaliana. Mol Biol Evol 19:2285–2293
Tenaillon MI, Hufford MB, Gaut BS, Ross-Ibarra J (2011) Genome size and transposable element content as determined by high-throughput sequencing in Maize and Zea luxurians. Genome Biol Evol 3:219–229
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680
Torti C, Ludvik M, Gomulski M, Maralli D, Raimondi E, Robertson HM (2000) Evolution of different subfamilies of mariner elements within mdfly genome inferred from abundance and chromosomal distribution. Chromosoma 108:523–532
Vicient C (2010) Transcriptional activity of transposable elements in maize. BMC Genom 11:601–610
Vieira C, Lepetit D, Dumont S, Biemont C (1999) Wake up of transposable elements following Drosophila simulans worldwide colonization. Mol Biol Evol 16:1251–1255
Vitte C, Bennetzen JL (2006) Analysis of retrotransposon structural diversity uncovers properties and propensities in angiosperm genome evolution. Proc Natl Acad Sci USA 103:17638–17643
Wessler S, Bureau T, White SE (1995) LTR-retrotransposons and MITE: important players in the evolution of plant genomes. Curr Opin Gent Dev 5:814–821
Wicker T, Sabot F, Hua-Van A et al (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8:973–982
Zurita S, Cabrero J, López-León MD, Camacho JPM (1998) Polymorphism regeneration for a neutralized selfish B chromosome. Evolution 52:274–277
Acknowledgments
This study was supported by grants from the Spanish Ministerio de Ciencia e Innovación (CGL2009-11917) and Junta de Andalucía (CVI-6649), and was partially performed by FEDER funds. E. E. Montiel was supported by a Junta de Andalucía fellowship. We thank David Martinez for English corrections.
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Montiel, E.E., Cabrero, J., Camacho, J.P.M. et al. Gypsy, RTE and Mariner transposable elements populate Eyprepocnemis plorans genome. Genetica 140, 365–374 (2012). https://doi.org/10.1007/s10709-012-9686-1
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DOI: https://doi.org/10.1007/s10709-012-9686-1