Advertisement

Chromosoma

, Volume 124, Issue 3, pp 353–365 | Cite as

Neo-sex chromosomes of Ronderosia bergi: insight into the evolution of sex chromosomes in grasshoppers

  • O. M. Palacios-Gimenez
  • D. A. Marti
  • D. C. Cabral-de-Mello
Research Article

Abstract

Sex chromosomes have evolved many times from morphologically identical autosome pairs, most often presenting several recombination suppression events, followed by accumulation of repetitive DNA sequences. In Orthoptera, most species have an X0♂ sex chromosome system. However, in the subfamily Melanoplinae, derived variants of neo-sex chromosomes (neo-XY♂ or neo-X1X2Y♂) emerged several times. Here, we examined the differentiation of neo-sex chromosomes in a Melanoplinae species with a neo-XY♂/XX♀ system, Ronderosia bergi, using several approaches: (i) classical cytogenetic analysis, (ii) mapping via fluorescent in situ hybridization of some selected repetitive DNA sequences and microdissected sex chromosomes, and (iii) immunolocalization of distinct histone modifications. The microdissected sex chromosomes were also used as sources for Polymerase chain reaction (PCR) amplification of RNA-coding multigene families, to study variants related to the sex chromosomes. Our data suggest that the R. bergi neo-Y has become differentiated after its formation by a Robertsonian translocation and inversions, and has accumulated repetitive DNA sequences. Interestingly, the ex autosomes incorporated into the neo-sex chromosomes retain some autosomal post-translational histone modifications, at least in metaphase I, suggesting that the establishment of functional modifications in neo-sex chromosomes is slower than their sequence differentiation.

Keywords

Rb-translocation Neo-sex chromosomes FISH Repetitive DNA Histone modification 

Abbreviations

2n

Diploid number

♀gDNA

Female genomic DNA

BSA

Bovine serum albumin

C0t-1 DNA

C 0 is the initial concentration of single-stranded DNA in moles per liter and t is the reannealing time in seconds

DAPI

4′,6-Diamidine-2′-phenylindole

FISH

Fluorescence in situ hybridization

mya

Million years ago

PBS

Phosphate-buffered saline

PCR

Polymerase chain reaction

Rb-translocation

Robertsonian translocation

rDNA

Ribosomal DNA

rRNA

Ribosomal RNA

snRNA

Small nuclear RNA

μX-DNA

X chromosome DNA obtained by microdissection

μY-DNA

Y chromosome DNA obtained by microdissection

Notes

Acknowledgments

The authors are grateful to Frantisek Marec for critical reading of the manuscript and to the anonymous reviewers for their substantial contributions, and to “Parque Estadual Edmundo Navarro de Andrade” administration for sample collecting authorization. OMPG acknowledges scholarship obtained from Fundação de Amparo a Pesquisa do Estado de São Paulo-FAPESP (process number 2012/01421-7). This study was partly supported by FAPESP (process number 2014/11763-8), Coordenadoria de Aperfeiçoamento de Pessoal de Nível Superior-CAPES, Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq, and the Programa Primeiros Projetos-PROPE/UNESP from Brazil. DAM was supported by Consejo Nacional de Investigaciones Científicas y Técnicas-CONICET from Argentina. The authors are grateful to Antonio Sergio Pascon for technical assistance in obtaining embryos.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

412_2015_505_Fig7_ESM.gif (466 kb)
Supplementary material 1

FISH analysis for the C 0 t-1 and C 0 t-100 DNA fractions and three multigene families in the male mitotic metaphase complements of Ronderosia bergi. Each probe that was used and the neo-XY sex chromosome are indicated directly on the images. Note the absence of signals for multigene families in the sex chromosomes and the propagation of highly and moderately repetitive DNA sequences throughout the long arm of neo-Y chromosome; however, no differences in the distribution of the hybridization signals were observed with the distinct probes. Bar = 5 μm. (GIF 466 kb)

412_2015_505_MOESM1_ESM.tif (6.8 mb)
High resolution image (TIFF 6925 kb)
412_2015_505_Fig8_ESM.gif (510 kb)
Supplementary material 2

FISH of the microsatellite probes in the male mitotic metaphase complements of Ronderosia bergi. Each probe that was used is indicated directly on the images. Note the specific and dispersed signals of the microsatellite arrays. The sex chromosomes are indicated. Bar = 5 μm. (GIF 509 kb)

412_2015_505_MOESM2_ESM.tif (4.1 mb)
High resolution image (TIFF 4247 kb)
412_2015_505_Fig9_ESM.gif (169 kb)
Supplementary material 3

Alignment of the multigene family sequences that were isolated from the autosomes and sex chromosomes of Ronderosia bergi and Drosophila virilis. (GIF 169 kb)

412_2015_505_MOESM3_ESM.tif (2.3 mb)
High resolution image (TIFF 2404 kb)

References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefPubMedGoogle Scholar
  2. Bachtrog D (2006) A dynamic view of sex chromosome evolution. Curr Opin Genetic Dev 16:578–585CrossRefGoogle Scholar
  3. Bergero R, Forrest A, Kamau E, Charlesworth D (2007) Evolutionary strata on the X chromosomes of the dioecious plant Silene latifolia: evidence from new sex-linked genes. Genetics 175:1945–1954PubMedCentralCrossRefPubMedGoogle Scholar
  4. Bidau CJ, Martí DA (2001) Meiosis and the Neo-XY of Dichroplus vittatus (Melanoplinae, Acrididae): a comparison between sexes. Genetica 110:185–194CrossRefGoogle Scholar
  5. Bidau CJ, Martí DA, Castillo ER (2011) Inexorable spread: inexorable death? The fate of neo-XY chromosomes of grasshoppers. J Genet 90:397–400CrossRefPubMedGoogle Scholar
  6. Bueno D, Palacios-Gimenez OM, Cabral-de-Mello DC (2013) Chromosomal mapping of repetitive DNAs in Abracris flavolineata reveal possible ancestry for the B chromosome and surprisingly H3 histone spreading. PLoS One 8:e66532PubMedCentralCrossRefPubMedGoogle Scholar
  7. Bull JJ (1983) Evolution of sex determining mechanisms. Benjamin Cummings, Menlo ParkGoogle Scholar
  8. Cabral-de-Mello DC, Moura RC, 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 104:393–400CrossRefPubMedGoogle Scholar
  9. Cabral-de-Mello DC, Valente GT, Nakajima RT, Martins C (2012) Genomic organization and comparative chromosome mapping of the U1 snRNA gene in cichlid fish, with an emphasis in Oreochromis niloticus. Chromosome Res 20:279–292CrossRefPubMedGoogle Scholar
  10. Cabrero J, Teruel M, Carmona FD, Camacho JPM (2007) Histone H2AX phosphorylation is associated with most meiotic events in grasshopper. Cytogenet Genome Res 116:311–315CrossRefPubMedGoogle Scholar
  11. Carbonell CS, Mesa A (2006) Ronderosia ommexechoides: a new species of Brazilian Dichroplini (Orthoptera: Acrididae, Melanoplinae). Neotrop Entomol 35:632–637CrossRefPubMedGoogle Scholar
  12. Cardoso H, Dutra A (1979) The Neo-X Neo-Y sex pair in Acrididae, its structure and association. Chromosoma 70:323–336CrossRefGoogle Scholar
  13. Carvalho AB (2002) Origin and evolution of the Drosophila Y chromosome. Curr Opin Genet Dev 12:664–668CrossRefPubMedGoogle Scholar
  14. Castillo ER, Martí DA, Bidau CJ (2010a) Sex and neo-sex chromosomes in Orthoptera: a review. J Orthopt Res 19:213–231CrossRefGoogle Scholar
  15. Castillo ERD, Bidau CJ, Martí DA (2010b) Neo-sex chromosome diversity in neotropical melanopline grasshoppers (Melanoplinae, Acrididae). Genetica 138:775–786CrossRefPubMedGoogle Scholar
  16. Castillo ERD, Tafarel A, Martí DA (2014) The early evolutionary history of neo-sex chromosomes in Neotropical grasshoppers, Boliviacris noroestensis (Orthoptera: Acrididae: Melanoplinae). Eur J Entomol 111:321–327CrossRefGoogle Scholar
  17. Charlesworth D, Mank JE (2010) The birds and the bees and the flowers and the trees: lessons from genetic mapping of sex determination in plants and animals. Genetics 186:9–31PubMedCentralCrossRefPubMedGoogle Scholar
  18. Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215–220CrossRefPubMedGoogle Scholar
  19. Charlesworth D, Charlesworth B, Marais G (2005) Steps in the evolution of heteromorphic sex chromosomes. Heredity 95:118–128CrossRefPubMedGoogle Scholar
  20. Chintauan-Marquier IC, Jordan S, Berthier P, Amédégnato C, Pompanon F (2011) Evolutionary history and taxonomy of a short-horned grasshopper subfamily: The Melanoplinae (Orthoptera: Acrididae). Mol Phyl Evol 58:22–32CrossRefGoogle Scholar
  21. Cigliano MM (1997) Ronderosia, a new genus of South American Melanoplinae (Orthoptera: Acrididae). J Orthoptera Res 6:1–19CrossRefGoogle Scholar
  22. Cobb J, Cargile B, Handel MA (1999a) Acquisition of competence to condense metaphase I chromosomes during spermatogenesis. Dev Biol 205:49–64CrossRefPubMedGoogle Scholar
  23. Cobb J, Miyaike M, Kikuchi A, Handel MA (1999b) Meiotic events at the centromeric heterochromatin: histone H3 phosphorylation, topoisomerase IIα localization and chromosome condensation. Chromosoma 108:412–425CrossRefPubMedGoogle Scholar
  24. Colgan DJ, McLauchlan A, Wilson GDF, Livingston SP, Edgecombe GD, Macaranas J, Cassis G, Gray MR (1998) Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution. Austral J Zool 46:419–437CrossRefGoogle Scholar
  25. Díaz MO, Sáez FA (1968) DNA synthesis in the neo-X neo-Y sex determination system of Dichroplus bergi (Orthoptera: Acrididae). Chromosoma 24:10–16CrossRefPubMedGoogle Scholar
  26. Drummond AJ, Ashton B, Cheung M, Heled J, Kearse M, Moir R et al. (2009) Geneious v4.8.5, Available from. http://www.geneious.com
  27. Filatov DA, Moneger F, Negrutiu I, Charlesworth D (2000) Low variability in a Y linked plant gene and its implications for Y-chromosome evolution. Nature 404:388–390CrossRefPubMedGoogle Scholar
  28. Fuchs J, Schubert I (2012) Chromosomal distribution and functional interpretation of epigenetic histone marks in plants. In: Bass HW, Birchler JA (ed.). Plant cytogenetics, plant genetics and genomics: crops and models 4. Springer Science+Business Media, LLC, pp 231–253Google Scholar
  29. Hewitt GM (1979) Grasshoppers and crickets. Animal Cytogenetics. vol 3: Insecta 1. Orthoptera. Gebrüder Borntraeger, BerlinGoogle Scholar
  30. Hobza R, Kejnovsky E, Vyskot B, Widmer A (2007) The role of chromosome rearrangements in the evolution of Silene latifolia sex chromosomes. Mol Genet Genomics 278:633–638CrossRefPubMedGoogle Scholar
  31. Houben A, Demidov D, Gernand D, Meister A, Leach CR, Schubert I (2003) Methylation of histone H3 in euchromatin of plant chromosomes depends on basic nuclear DNA content. Plant J 33:967–973CrossRefPubMedGoogle Scholar
  32. Houben A, Demidov D, Karimi-Ashtiyani R (2013) Epigenetic control of cell division. Springer, BerlinCrossRefGoogle Scholar
  33. Ijdo JW, Wells RA, Baldini A, Reeders ST (1991) Improved telomere detection using a telomere repeat probe (TTAGGG)n generated by PCR. Nucleic Acids Res 19:4780PubMedCentralCrossRefPubMedGoogle Scholar
  34. Kaiser VB, Bachtrog D (2010) Evolutions of sex chromosome in insects. Annu Rev Genet 44:91–112PubMedCentralCrossRefPubMedGoogle Scholar
  35. Kejnovsky E, Hobza R, Cermak T, Kubat Z, Vyskot B (2009) The role of repetitive DNA in structure and evolution of sex chromosomes in plants. Heredity 102:533–541CrossRefPubMedGoogle Scholar
  36. Kejnovský E, Michalovova M, Steflova P, Kejnovska I, Manzano S, Hobza R, Kubat Z, Kovarik J, Jamilena M, Vyskot B (2013) Expansion of microsatellites on evolutionary young Y chromosome. PLoS One 8:e45519PubMedCentralCrossRefPubMedGoogle Scholar
  37. Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693–705CrossRefPubMedGoogle Scholar
  38. Kubat Z, Hobza R, Vyskot B, Kejnovsky E (2008) Microsatellite accumulation on the Y chromosome in Silene latifolia. Genome 51:350–356CrossRefPubMedGoogle Scholar
  39. Librado P, Rozas J (2009) DnaSP v5: A software a comprehensive analysis of DNA polymorphism data. Biogeosciences 25:1451–1452Google Scholar
  40. Manzanero S, Arana P, Puertas MJ, Houben A (2000) The chromosomal distribution of phosphorylated histone H3 differs between plants and animals at meiosis. Chromosoma 109:308–317CrossRefPubMedGoogle Scholar
  41. Manzanero S, Rutten T, Kotseruba V, Houben A (2002) Alterations in the distribution of histone H3 phosphorylation in mitotic plant chromosomes in response to cold treatment and the protein phosphatase inhibitor cantharidin. Chromosome Res 10:467–476CrossRefPubMedGoogle Scholar
  42. Matsubara K, Knopp T, Sarre SD, Georges A, Ezaz T (2013) Karyotypic analysis and FISH mapping of microsatellite motifs reveal highly differentiated XX/XY sex chromosomes in the pink-tailed worm-lizard (Aprasia parapulchella, Pygopodidae, Squamata). Mol Cytogenet 6:60PubMedCentralCrossRefPubMedGoogle Scholar
  43. Matsunaga S (2009) Junk DNA promotes sex chromosome evolution. Heredity 102:525–526CrossRefPubMedGoogle Scholar
  44. Mesa A, de Mesa RS (1967) Complex sex-determining mechanisms in thre species of South American grasshoppers (Orthoptera, Acridoidea). Chromosoma 21:163–180CrossRefGoogle Scholar
  45. Navajas-Pérez R, de la Herrán R, Jamilena M, Lozano R, Ruiz Rejón C, Ruiz Rejón M, Garrido-Ramos MA (2005) Reduced rates of sequence evolution of Y-linked satellite DNA in Rumex (Polygonaceae). J Mol Evol 60:391–399CrossRefPubMedGoogle Scholar
  46. Navajas-Pérez R, Quesada del Bosque ME, Garrido-Ramos MA (2009) Effect of location, organization, and repeat-copy number in satellite-DNA evolution. Mol Genet Genomics 282:395–406CrossRefPubMedGoogle Scholar
  47. Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39:121–152PubMedCentralCrossRefPubMedGoogle Scholar
  48. Nicolas M, Marais G, Hykelova V, Janousek B, Laporte V, Byskot V, Mouchiroud D, Negrutiu I, Charlesworth D, Monéger F (2005) A gradual process of recombination restriction in the evolutionary history of the sex chromosomes in dioecious plants. PLoS Biol 3:e4PubMedCentralCrossRefPubMedGoogle Scholar
  49. Ohno S (1967) Sex chromosomes and sex linked genes. Springer, BerlinCrossRefGoogle Scholar
  50. Oliver C, Pradillo M, Corredor E, Cuñado N (2013) The dynamics of histone H3 modifications is species-specific in plant meiosis. Planta 238:23–33CrossRefPubMedGoogle Scholar
  51. Page J, de la Fuente R, Manterola M, Parra MT, Viera A, Berríos S, Fernández-Donoso R, Rufas JS (2012) Inactivation or non-reactivation: what accounts better for the silence of sex chromosomes during mammalian male meiosis? Chromosoma 121:307–326CrossRefPubMedGoogle Scholar
  52. Palacios-Gimenez OM, Castillo ER, Martí DA, Cabral-de-Mello DC (2013) Tracking the evolution of sex chromosome systems in Melanoplinae grasshoppers through chromosomal mapping of repetitive DNA sequences. BMC Evol Biol 13:167PubMedCentralCrossRefPubMedGoogle Scholar
  53. Pinkel D, Straume T, Gray JW (1986) Cytogenetic analysis using quantitative, high sensitivity, fluorescence hybridization. Proc Natl Acad Sci U S A 83:2934–2938PubMedCentralCrossRefPubMedGoogle Scholar
  54. Pokorná M, Giovannotti M, Kratochvíl L, Kasai F, Trifonov VA, O’Brien PCM, Caputo C, Olmo E, Ferguson-Smith MA, Rens W (2011a) Strong conservation of the bird Z chromosome in reptilian genomes is revealed by comparative painting despite 275 million years divergence. Chromosoma 120:455–468CrossRefPubMedGoogle Scholar
  55. Pokorná M, Kratochvíl L, Kejnovský E (2011b) Microsatellite distribution on sex chromosomes at different stages of heteromorphism and heterochromatinization in two lizard species (Squamata: Eublepharidae: Coleonyx elegans and Lacertidae: Eremias velox). BMC Genet 12:90PubMedCentralCrossRefPubMedGoogle Scholar
  56. Rice WR (1996) Evolution of the Y sex chromosome in animals. Bioscience 46:331–343CrossRefGoogle Scholar
  57. Sambrook J, Russel DW (2001) Molecular cloning. A laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  58. Skaletsky H, Kuroda-Kawaguchi T, Minx PJ et al (2003) The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423:825–837CrossRefPubMedGoogle Scholar
  59. Sotero-Caio CG, de Souza MJ, Cabral-de-Mello DC, Brasileiro-Vidal AC, Guerra M (2011) Phosphorylation of histone H3S10 in animal chromosomes: is there a uniform pattern? Cytogenet Genome Res 135:111–117CrossRefPubMedGoogle Scholar
  60. Steinemann M, Steinemann S (1997) The enigma of Y chromosome degeneration: TRAM, a novel retrotransposon is preferentially located on the neo-Y chromosome of Drosophila miranda. Genetics 145:261–266PubMedCentralPubMedGoogle Scholar
  61. Steinemann S, Steinemann M (2005) Retroelements: tools for sex chromosome evolution. Cytogenet Genome Res 110:134–143CrossRefPubMedGoogle Scholar
  62. Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306CrossRefPubMedGoogle Scholar
  63. Tamura K, Peterson D, Stecher G, Nei M, Kumar S (2011) Molecular evolutionary genetics using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCentralCrossRefPubMedGoogle Scholar
  64. Traut W, Sahara K, Marec F (2007) Sex chromosomes and sex determination in Lepidoptera. Sex Dev 1:332–346CrossRefPubMedGoogle Scholar
  65. Turner BM, Birley AJ, Lavender J (1992) Histone H4 isoforms acetylated at specific lysine residues define individual chromosomes and chromatin domains in Drosophila polytene nuclei. Cell 69:375–384CrossRefPubMedGoogle Scholar
  66. Turner JMA, Shantha K, Mahadevaiah RB, Offenberg HH, Heyting C, Burgoyne PS (2000) Analysis of male meiotic “sex-body” proteins during XY female meiosis provides new insights into their functions. Chromosoma 109:426–432CrossRefPubMedGoogle Scholar
  67. Vítková M, Fukova I, Kubíčková S, Marec F (2007) Molecular divergence of the W chromosomes in pyralid moths (Lepidoptera). Chromosome Res 15:917–930CrossRefPubMedGoogle Scholar
  68. Webb GC, White MJD, Contreras N, Cheney J (1978) Cytogenetics of the parthogenetic grasshopper Warramaba (formely Moraba) virgo and its bisexual relatives. IV. Chromosome banding studies. Chromosoma 67:309–339CrossRefGoogle Scholar
  69. White MJD (1973) Animal cytology and evolution. Cambridge University Press, CambridgeGoogle Scholar
  70. Yoshido A, Šíchová J, Kubíčková S, Marec F, Sahara K (2013) Rapid turnover of the W chromosome in geographical populations of wild silkmoths, Samia cynthia ssp. Chromosome Res 21:149–164CrossRefPubMedGoogle Scholar
  71. Zhou Q, Ellison CE, Kaiser VB, Alekseyenko AA, Gorchakov AA, Bachtrog D (2013) The epigenome of evolving Drosophila neo-sex chromosomes: dosage compensation and heterochromatin formation. PLoS Biol 11:e1001711PubMedCentralCrossRefPubMedGoogle Scholar
  72. Zwick MS, Hanson RE, McKnight TD, Nurul-Islam-Faridi M, Stelly DM (1997) A rapid procedure for the isolation of C 0 t–1 DNA from plants. Genome 40:138–142CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • O. M. Palacios-Gimenez
    • 1
  • D. A. Marti
    • 2
  • D. C. Cabral-de-Mello
    • 1
  1. 1.Departamento de BiologiaUNESP—Univ Estadual Paulista, Instituto de Biociências/IBRio ClaroBrazil
  2. 2.Laboratorio de Genética Evolutiva, IBS, Facultad de Ciencias Exactas, Químicas y NaturalesUniversidad Nacional de Misiones, CONICETPosadasArgentina

Personalised recommendations