Eur. J. Entomol. 111 (3): 329-334, 2014 | 10.14411/eje.2014.052

Chromosomal mapping of two Mariner-like elements in the grasshopper Abracris flavolineata (Orthoptera: Acrididae) reveals enrichment in euchromatin

Octavio M. PALACIOS-GIMENEZ, Danilo BUENO, Diogo C. CABRAL-DE-MELLO*
UNESP - Univ. Estadual Paulista, Instituto de Biociências/IB, Departamento de Biologia, CEP 13506-900 Rio Claro, SP, Brazil; e-mails: mellodc@rc.unesp.br; opalacios7@gmail.com; danilo_riber@yahoo.com.br

The occurrence of transposable elements (TEs) is a ubiquitous characteristic of eukaryotic genomes, and these sequences are highly abundant in some species. Due to their large genomes, grasshoppers (Orthoptera) appear to be potentially good candidates in terms of having genomes that harbour considerable numbers of TEs. In the present study, we have investigated the occurrence of two Mariner-like elements (MLEs) within the genome of the grasshopper, Abracris flavolineata (De Geer, 1773), describing their distribution in both the A (i.e. standard or normal) complement and B chromosomes. PCR amplification followed by cloning and sequencing revealed two Mariner-like elements, which were named Afmar1 and Afmar2. Moreover, subsequent fluorescence in situ hybridization (FISH) assays indicated an abundance of these elements in the euchromatic regions of all the standard complement chromosomes and an absence of such sequences in heterochromatic regions. These sequences were also abundant in the euchromatic B chromosome: Afmar1 was distributed along the entire length of the chromosome, whereas Afmar2 was restricted to the proximal/interstitial regions of the chromosomal long arm. The general aspects of the distribution patterns of the two MLEs are discussed as well as their possible involvement in the origin and diversification of the B chromosome in A. flavolineata.

Keywords: Orthoptera, Acrididae, B chromosome, euchromatin, FISH, genome, grasshopper, repetitive DNA, transposable elements

Received: November 29, 2013; Accepted: March 6, 2014; Prepublished online: May 27, 2014; Published: July 14, 2014

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References

  1. Auge-Gouillou C., Bigot Y., Poller N., Hamelin M.H., Meunier-Rotival M. & Periquet G. 1995: Human and other mammalian genomes contain transposons of the mariner family. - FEBS Letters 368: 541-546 Go to original source...
  2. Biemont C. 2010: A brief history of the status of transposable elements: from junk DNA to major players in evolution. - Genetics 186: 1085-1093 Go to original source...
  3. Biemont C. & Vieira C. 2006: Genetics: Junk DNA as an evolutionary force. - Nature 443: 521-524 Go to original source...
  4. Boehne A., Brunet F., Galiana-Arnoux D., Schultheis C. & Volff J.N. 2008: Transposable elements as drivers of genomic and biological diversity in vertebrates. - Chromosome Res 16: 203-215 Go to original source...
  5. Bueno D., Palacios-Gimenez O.M. & Cabral-de-Mello D.C. 2013: Chromosomal mapping of repetitive DNAs in Abracris flavolineata reveal possible ancestry for the B chromosome and surprisingly H3 histone spreading. - PLoS ONE 8: e66532 Go to original source...
  6. Cabral-de-Mello D.C., Moura R.C. & Martins C. 2010: Chromosomal mapping of repetitive DNAs in the beetle Dichotomius geminatus provides the first evidence for an association of 5S rRNA and histone H3 genes in insects, and repetitive DNA similarity between the B chromosome and A complement. - Heredity 104: 393-400 Go to original source...
  7. Camacho J.P.M. 2005: B chromosomes. In Gregory T.R. (ed.): The Evolution of the Genome. Elsevier, Amsterdam, New York, pp. 223-286
  8. Castillo E.R., Taffarel A. & Marti D.A. 2011: Una tecnica alternativa para el caritiopado mitotico en saltamontes: bandeo C y fluorescente en Adimantus ornatissimus (Orthoptera: Acrididae). - Rev. Cienc. Tecnol. 16: 31-35
  9. Charles M., Belcram H., Just J., Huneau C., Viollet A., Couloux A., Segurens B., Carter M., Huteau V., Coriton O., Appels R., Samain S. & Chalhoub B. 2008: Dynamics and differential proliferation of transposable elements during the evolution of the B and A genomes of wheat. - Genetics 180: 1071-1086 Go to original source...
  10. Coleman J.J., Rounsley S.D., Rodriguez-Carres M., Kuo A., Wasmann C.C., Grimwood J., Schmutz J., Taga M., White G.J., Zhou Z., Schwartz D.C., Freitag M., Ma L., Danchin E.G.J., Henrissat B., Coutinho P.M., Nelson D.R., Straney D., Napoli C.A., Barker B.M., Gribskov M., Rep M., Kroken S., Molnar I., Rensing C., Kennell J.C., Zamora J., Farman M.L., Selker E.U., Salamov A., Shapiro H., Pangilinan J., Lindquist E., Lamers C., Grigoriev I.V., Geiser D.M., Covert S.F., Temporini E. & Van Etten H.D. 2009: The genome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. - PLoS Genet. 5: e1000618 Go to original source...
  11. Dimitri P., Jukanovic N. & Arca B. 2003: Colonization of heterochromatic genes by transposable elements in Drosophila. - Mol. Biol. Evol. 20: 503-512 Go to original source...
  12. Doolittle W.F. & Sapienza C. 1980: Selfish genes, the phenotype paradigm and genome evolution. - Nature 284: 601-603 Go to original source...
  13. Drummond A.J., Ashton B., Cheung M., Heled J., Kearse M. Moir R., Stones-Havas S., Sturrock S., Thierer T. & Wilson A. 2009: Geneious v4.8.5, Available from http://www.geneious.com
  14. Fantinatti B.E.A., Mazzuchelli J., Valente G.T., Cabral-de-Mello D.C. & Martins C. 2012: Genomic content and new insights on the origin of the B chromosome of the cichlid fish Astatotilapia latifasciata. - Genetica 139: 1273-1282 Go to original source...
  15. Feschotte C. & Pritham E.J. 2007: DNA transposons and the evolution of eukaryotic genomes. - Annu. Rev. Genet. 41: 331-368 Go to original source...
  16. Feschotte C. & Wessler S.R. 2002: Mariner-like transposases are widespread and diverse in flowering plants. - Proc. Natl. Acad. Sci. USA 99: 280-285 Go to original source...
  17. Green C.L. & Frommer M. 2001: The genome of the queensland fruit fly Bactrocera tryoni contains multiple representatives of the mariner family of transposable elements. - Insect Mol. Biol. 10: 371-386 Go to original source...
  18. Houben A., Banaei-Moghaddam A.M. & Klemme S. 2013: Biology and evolution of B chromosomes. In Leitch I.J., Greilhuber J., Dolezel J. & Wendel J. (eds): Plant Genome Diversity. Vol. 2. Physical Structure, Behaviour and Evolution of Plant Genomes. Springer, Wien, pp. 149-165
  19. Hua-Van A., Le Rouzic A., Boutin T.S., Filee J. & Capy P. 2011: The struggle for life of the genome's selfish architects. - Biology Dir 6: 19 Go to original source...
  20. Hurst G.D.D. & Werren J.H. 2001: The role of selfish genetic elements in eukaryotic. - Nature Rev. Genet. 2: 597-606 Go to original source...
  21. Jacobs G., Dechyeva D., Menzel G., Dombrowski C. & Schmidt T. 2004: Molecular characterization of Vulmar1, a complete mariner transposon of sugar beet and diversity of mariner and En/Spm-like sequences in the genus Beta. - Genome 47: 1192-1201 Go to original source...
  22. Jurka J., Kapitonov V.V., Pavlicek A., Klonowski P., Kohany O. &Walichiewicz J. 2005: Repbase update, a database of eukaryotic repetitive elements. - Cytogenet. Gen. Res. 110: 462-467 Go to original source...
  23. Kapitonov V.V. & Jurka J. 2008: A universal classification of eukaryotic transposable elements implemented in Repbase. - Nature Rev. Genet. 9: 411-412 Go to original source...
  24. Kazazian Jr H.H. 2004: Mobile elements: drivers of genome evolution. - Science 303: 1625-1632 Go to original source...
  25. Kidwell M.G. 2002: Transposable elements and the evolution of genome size in eukaryotes. - Genetica 115: 49-63 Go to original source...
  26. Kumaresan G. & Mathavan S. 2004: Molecular diversity and phylogenetic analysis of mariner-like transposons in the genome of the silkworm Bombyx mori. - Insect Mol. Biol. 3: 259-271 Go to original source...
  27. Lamb J.C., Riddle N.C., Cheng Y.M., Theuri J. & Birchler J.A. 2007: Location and transcription of a retrotransposon-derived element on the maize B chromosome. - Chromosome Res 15: 383-398 Go to original source...
  28. Lander E.S., Linton L.M., Birren B., Nusbaum C., Zody M.C., Baldwin J., Devon K., Dewar K., Doyle M., FitzHugh W., Funke R., Gage D., Harris K., Heaford A., Howland J., Kann L., Lehoczky J., LeVine R., McEwan P., McKernan K., Meldrim J., Mesirov J.P., Miranda C., Morris W., Naylor J., Raymond C., Rosetti M., Santos R., Sheridan A., Sougnez C., Stange-Thomann N., Stojanovic N., Subramanian A., Wyman D., Rogers J., Sulston J., Ainscough R., Beck S., Bentley D., Burton J., Clee C., Carter N., Coulson A., Deadman R., Deloukas P., Dunham A., Dunham I., Durbin R., French L., Grafham D., Gregory S., Hubbard T., Humphray S., Hunt A., Jones M., Lloyd C., McMurray A., Matthews L., Mercer S., Milne S., Mullikin J.C., Mungall A., Plumb R., Ross M., Shownkeen R., Sims S., Waterston R.H., Wilson R.K., Hillier L.W., McPherson J.D., Marra M.A., Mardis E.R., Fulton L.A., Chinwalla A.T., Pepin K.H., Gish W.R., Chissoe S.L., Wendl M.C., Delehaunty K.D., Miner T.L., Delehaunty A., Kramer J.B., Cook L.L., Fulton R.S., Johnson D.L., Minx P.J., Clifton S.W., Hawkins T., Branscomb E., Predki P., Richardson P., Wenning S., Slezak T., Doggett N., Cheng J.F., Olsen A., Lucas S., Elkin C., Uberbacher E., Frazier M., Gibbs R.A., Muzny D.M., Scherer S.E., Bouck J.B., Sodergren E.J., Worley K.C., Rives C.M., Gorrell J.H., Metzker M.L., Naylor S.L., Kucherlapati R.S., Nelson D.L., Weinstock G.M., Sakaki Y., Fujiyama A., Hattori M., Yada T., Toyoda A., Itoh T., Kawagoe C., Watanabe H., Totoki Y., Taylor T., Weissenbach J., Heilig R., Saurin W., Artiguenave F., Brottier P., Bruls T., Pelletier E., Robert C., Wincker P., Smith D.R., Doucette-Stamm L., Rubenfield M., Weinstock K., Lee H.M., Dubois J., Rosenthal A., Platzer M., Nyakatura G., Taudien S., Rump A., Yang H., Yu J., Wang J., Huang G., Gu J., Hood L., Rowen L., Madan A., Qin S., Davis R.W., Federspiel N.A., Abola A.P., Proctor M.J., Myers R.M., Schmutz J., Dickson M., Grimwood J., Cox D.R., Olson M.V., Kaul R., Raymond C., Shimizu N., Kawasaki K., Minoshima S., Evans G.A., Athanasiou M. & Schultz R. 2001: Initial sequencing and analysis of the human genome. - Nature 409: 860-921 Go to original source...
  29. Langin T., Capy P. & Daboussi M.J. 1995: The transposable element impala, a fungal member of the Tc1-mariner superfamily. - Mol. Gen. Genet. 246: 19-28 Go to original source...
  30. Lampe D.J., Churchill M.E.A. & Robertson H.M. 1996: A purified mariner transposase is sufficient to mediate transposition in vitro. - EMBO J. 15: 5470-5479
  31. Lampe D.J., Witherspoon D.J., Soto-Adames F.N. & Robertson H.M. 2003: Recent horizontal transfer of mellifera subfamily Mariner transposons into insect lineages representing four different orders shows that selection acts only during horizontal transfer. - Mol. Biol. Evol. 20: 554-562 Go to original source...
  32. Mandrioli M. 2003: Identification and chromosomal localization of mariner-like elements in the cabbage moth Mamestra brassicae (Lepidoptera). - Chromosome Res. 11: 319-322 Go to original source...
  33. Marques A., Banaei-Moghaddam A.M., Klemme S., Blattner F.R., Niwa K., Guerra M. & Houben A. 2013: B chromosomes of rye are highly conserved and accompanied the development of early agriculture. - Ann. Bot. 112: 527-534 Go to original source...
  34. Montiel E.E., Cabrero J., Camacho J.P.M. & Lopez-Leon M.A. 2012: Gypsy, RTE and Mariner transposable elements populate Eyprepocnemis plorans genome. - Genetica 140: 365-374 Go to original source...
  35. Oliveira S.G., Moura R.C. & Martins C. 2012: B chromosome in the beetle Coprophanaeus cyanescens (Scarabaeidae): emphasis in the organization of repetitive DNA sequences. - BMC Genet. 13: 96 Go to original source...
  36. Orgel L.E. & Crick F.H.C. 1980: Selfish DNA: the ultimate parasite. - Nature 284: 604-607 Go to original source...
  37. Osanai-Futahashi M., Suetsugub Y., Mita K. & Fujiwara H. 2008: Genome-wide screening and characterization of transposable elements and their distribution analysis in the silkworm Bombyx mori. - Insect Mol. Biol. 38: 1046-1057 Go to original source...
  38. Plasterk R.H.A., Izsvak Z. & Ivics Z. 1999: Resident aliens: the Tc1/mariner superfamily of transposable elements. - Trends Genet. 15: 326-332 Go to original source...
  39. Rezende-Teixeira P., Siviero F., Andrade A., Santelli R.V. & Machado-Santelli G.M. 2008: Mariner-like elements in Rhynchosciara americana (Sciaridae) genome: molecular and cytological aspects. - Genetica 133: 137-145 Go to original source...
  40. Ruiz-Ruano F.J., Ruiz-Estevez M., Rodriguez-Perez J., Lopez-Pino J.L., Cabrero J. & Camacho J.P.M. 2011: DNA amount of X and B chromosomes in the grasshoppers Eyprepocnemis plorans and Locusta migratoria. - Cytogenet. Gen. Res. 134: 120-126 Go to original source...
  41. Sambrook J. & Russel D.W. 2001: Molecular Cloning. A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 999 pp
  42. Sinzelle L., Chesneau A., Bigot Y., Mazabraud A. & Pollet N. 2006: The mariner transposons belonging to the irritans subfamily were maintained in Chordate genomes by vertical transmission. - J. Mol. Evol. 62: 53-65 Go to original source...
  43. Smit A.F. 2002: Initial survey of interspersed repeats in Takifugu rubripes. - Repbase Reports 2: 56-56
  44. Wang X., Fang X., Yang P., Jiang X., Jiang F., Zhao D., Li B., Cui F., Wei J., Ma C., Wang Y., He J., Luo Y., Wang Z., Guo X., Guo W., Wang X., Zhang Y.,Yang M., Hao S., Chen B., Ma Z., Yu D., Xiong Z., Zhu Y., Fan D., Han L., Wang B., Chen Y., Wang J., Yang L., Zhao W., Feng Y., Chen G., Lian J., Li Q., Huang Z., Yao X., Lv N., Zhang G., Li Y., Wang J., Wang J., Zhu B. & Kang L. 2014: The locust genome provides insight into swarm formation and long-distance flight. - Nature Commun 5: 2957 Go to original source...
  45. Westerman M., Barton N.H. & Hewitt G.M. 1987: Differences in DNA content between two chromosomal races of the grasshopper Podisma pedestris. - Heredity 58: 221-228 Go to original source...
  46. Wicker T., Sabot F., Hua-Van A., Bennetzen J.L., Capy P., Chalhoub B., Flavell A., Leroy P., Morgante M., Panaud O., Paux E., SanMiguel P. & Schulman A.H. 2007: A unified classification system for eukaryotic transposable elements. - Nature Rev. Genet. 8: 973-982 Go to original source...
  47. Witherspoon D.J. & Robertson H.M. 2003: Neutral evolution of ten types of mariner transposons in the genomes of Caenorhabditis elegans and Caenorhabditis briggsae. - J. Mol. Evol. 56: 751-769 Go to original source...
  48. Zhang L., Dawson A. & Finnegan D.J. 2001: DNA-binding activity and subunit interaction of the mariner tranposase. - Nucl. Acid Res. 29: 3566-3575 Go to original source...
  49. Ziegler C.G., Lamatsch D.K., Steinlein C., Engel W., Schartl M. & Schmid M. 2003: The giant B chromosome of the cyprinid fish Alburnus alburnus harbours a retrotransposon-derived repetitive DNA sequence. - Chromosome Res 11: 23-35 Go to original source...