Advertisement

Molecular Genetics and Genomics

, Volume 291, Issue 5, pp 1919–1925 | Cite as

Chromosomal evolutionary dynamics of four multigene families in Coreidae and Pentatomidae (Heteroptera) true bugs

  • Vanessa Bellini Bardella
  • José Antônio Marin Fernandes
  • Diogo Cavalcanti Cabral-de-Mello
Original Article

Abstract

Previous chromosome mapping of multigene families in Pentatomomorpha (Heteroptera) insects, which was restricted to the major rDNA, revealed remarkable conservation of number of clusters and chromosomal positions. Aiming to understand the chromosomal organization and evolutionary patterns of multigene families in karyotypes of Heteroptera, we performed a chromosomal mapping using four distinct multigene families in representatives of Coreidae (ten species) and Pentatomidae (five species). A single pair of the major rDNA cluster (18S rDNA probe) and a single pair of the minor rDNA cluster (5S rDNA probe), both terminally located were primarily observed, being, in most species, located in distinct chromosomes. However, some alternative patterns were also observed. In species in which the U2 snDNA and H4 gene clusters were mapped, they were mainly located in one autosomal pair each, wherein the H4 gene cluster was located in different positions. Our data suggest that the karyotype diversity reported in Coreidae is not reflected in the distribution diversity of multigene families. This contrasts with the data for Pentatomidae, with a conserved gross karyotype but a discrete diversity in the location of the clusters of multigene families, indicating genome dynamics for these markers. The findings are discussed to shed light on the possible causes for the conservation or variation observed and to assist in understanding the chromosomal evolutionary trends in the group.

Keywords

Fluorescence in situ hybridization H4 histone rDNA U2 snDNA 

Notes

Acknowledgments

This study was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (Process Number 2014/11763-8), Coordenadoria de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). We are also grateful to the anonymous reviewers for valuable comments. DCCM and JAMF were the recipients of a research productivity fellowship from the Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq (Process Numbers 304758/2014-0, 311403/2012-3, respectively) and VBB was a recipient of PNPD scholarship.

Compliance with ethical standards

Funding

This study was founded by Fundação de Amparo a Pesquisa do Estado de São Paulo-FAPESP (Process Number 2014/11763-8) and Coordenadoria de Aperfeiçoamento de Pessoal de Nível Superior-CAPES.

Conflict of interest

Vanessa Bellini Bardella declares that she has no conflict of interest. José Antônio Marin Fernandes declares that he has no conflict of interest. Diogo Cavalcanti Cabral-de-Mello declares that he has no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

References

  1. Anjos A, Ruiz-Ruano FJ, Camacho JPM, Loreto V, Cabrero J, Souza MJ, Cabral-de-Mello DC (2015) U1 snDNA clusters in grasshoppers: chromosomal dynamics and genomic organization. Heredity 114:207–219CrossRefPubMedGoogle Scholar
  2. Bardella VB, Fernandes T, Vanzela ALL (2013) The conservation of number and location of 18S sites indicates the relative stability of rDNA in species of Pentatomomorpha (Heteroptera). Genome 56:425–429CrossRefPubMedGoogle Scholar
  3. Bardella VB, Grazia J, Fernandes JAM, Vanzela ALL (2014) High diversity in CMA3/DAPI-banding patterns in heteropterans. Cytogenet Genome Res 142(1):46–53CrossRefPubMedGoogle Scholar
  4. Bowen RH (1922) Notes on the occurrence of abnormal mitosis in spermatogenesis. Biol Bull 43:184–203CrossRefGoogle Scholar
  5. Bressa MJ, Larramendy M, Papeschi AG (2005) Heterochromatin characterization in five species of Heteroptera. Genetica 124:307–317CrossRefPubMedGoogle Scholar
  6. Bueno D, Palacio-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:e66532CrossRefPubMedPubMedCentralGoogle Scholar
  7. 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
  8. Cabral-de-Mello DC, Moura RC, Martins C (2011a) Cytogenetic mapping of rRNAs and histone H3 genes in 14 species of Dichotomius (Coleoptera, Scarabaeidae, Scarabaeinae) beetles. Cytogenet Genome Res 134:127–135CrossRefPubMedGoogle Scholar
  9. Cabral-de-Mello DC, Cabrero J, López-León MD, Camacho JPM (2011b) Evolutionary dynamics of 5S rDNA location in acridid grasshoppers and its relationship with H3 histone gene and 45S rDNA location. Genetica 139:921–931CrossRefPubMedGoogle Scholar
  10. Cabrero J, Camacho JP (2008) Location and expression of ribosomal RNA genes in grasshoppers abundance of silent and cryptic loci. Chromosome Res 16:595–607CrossRefPubMedGoogle Scholar
  11. Cabrero J, López-León MD, Teruel M, Camacho JPM (2009) Chromosome mapping of H3 and H4 histone gene clusters in 35 species of acridid grasshoppers. Chromosome Res 17:397–404CrossRefPubMedGoogle Scholar
  12. Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215–220CrossRefPubMedGoogle Scholar
  13. Chirino MG, Papeschi AG, Bressa MJ (2013) The significance of cytogenetics for the study of karyotypes evolution and taxonomy of water bugs (Heteroptera, Belostomatidae) native to Argentina. Comp Cytogenet 7:111–129CrossRefGoogle Scholar
  14. Colombo PC, Bidau CJ (1985) Estudios cromosómicos en heterópteros argentinos. I. Los cromosomas meióticos de cinco espécies de Coreidae. Physis 43:29–40Google Scholar
  15. Da Silva M, Matoso DA, Vicari MR, De Almeida MC, Margarido VP, Artoni RF (2011) Physical mapping of 5S rDNA in two species of knifefishes: Gymnotus pantanal and Gymnotus paraguensis (Gymnotiformes). Cytogenet Genome Res 134(4):303–307CrossRefPubMedGoogle Scholar
  16. De Castro YGP (1947) Comportamento dos cromossômios no gênero Hypselonotus (Hemiptera-Coreidae). An Esc Super Agric Luiz de Queiroz 4:313–325CrossRefGoogle Scholar
  17. Drouin G, Tsang C (2012) 5S rRNA gene arrangements in protists: a case of nonadaptive evolution. J Mol Evol 74(5–6):342–351CrossRefPubMedGoogle Scholar
  18. Franco MJ, Bressa MJ, Papeschi AG (2006) Karyotype and male meiosis in Spartocera batatas and meiotic behavior of multiple sex chromosome in Coreidae (Heteroptera). Eur J Entomol 103(1):9–16CrossRefGoogle Scholar
  19. Golub NV, Golub VB, Kuznetsova VG (2015) Variability of 18S rDNA loci in four lace bug species (Hemiptera, Tingidae) with the same chromosome number. Comp Cytogenet 9(4):513–522CrossRefPubMedPubMedCentralGoogle Scholar
  20. González-García JM, Antonio C, Suja JA, Rufas JS (1996) Meiosis in holocentric chromosomes: chromatid ends of sex univalents in Graphosoma italicum (Heteroptera). Chromosome Res 4(2):124–132CrossRefPubMedGoogle Scholar
  21. Grozeva S, Kuznetsova VG, Anokhin BA (2011) Karyotypes, male meiosis and comparative FISH mapping of 18S ribosomal DNA and telomeric (TTAGG)n repeat in eight species of true bugs (Hemiptera, Heteroptera). Comp Cytogenet 5(4):355–374CrossRefPubMedPubMedCentralGoogle Scholar
  22. Gunderina L, Golygina V, Broshkov A (2015) Chromosomal organization of the ribosomal RNA genes in the genus Chironomus (Diptera, Chironomidae). Comp Cytogenet 9(2):201–220CrossRefPubMedPubMedCentralGoogle Scholar
  23. López-Flores I, Garrido-Ramos MM (2012) The repetitive DNA content of eukaryotic genomes. Cytogenet Genome Res 7:1–28Google Scholar
  24. Mandrioli M, Manicardi GC (2013) Chromosomal reveals a dynamic organization of the histone genes in aphids (Hemiptera: Aphididae). Entomologia 1(1):e2CrossRefGoogle Scholar
  25. Nguyen P, Sahara K, Yoshido A, Marec F (2010) Evolutionary dynamics of rDNA clusters on chromosomes of moths and butterflies (Lepidoptera). Genetica 138(3):343–354CrossRefPubMedGoogle Scholar
  26. Novotná J, Havelka J, Starý P, Koutecký P, Vítková M (2011) Karyotype analysis of the Russian wheat aphid, Diuraphis noxia (Kurdjumov) (Hemiptera: Aphididae) reveals a large X chromosome with rRNA and histone gene families. Genetica 139(3):281–289CrossRefPubMedGoogle Scholar
  27. Oliveira NL, Cabral-de-Mello DC, Rocha MF, Loreto V, Martins C, Moura RC (2011) Chromosomal mapping of rDNAs and H3 histone sequences in the grasshopper Rhammatocerus brasiliensis (Acrididae, Gomphocerinae): extensive chromosomal dispersion and co-localization of 5S rDNA/H3 histone clusters in the A complement and B chromosome. Mol Cytogenet 4:24CrossRefPubMedPubMedCentralGoogle Scholar
  28. 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 13:167CrossRefPubMedPubMedCentralGoogle Scholar
  29. Panzera Y, Pita S, Ferreiro MJ, Ferrandis I, Lages C, Pérez R et al (2012) High dynamics of rDNA cluster location in kissing bug holocentric chromosomes (Triatominae, Heteroptera). Cytogenet Genome Res 138(1):56–67CrossRefPubMedGoogle Scholar
  30. Papeschi AG, Bressa MJ (2006) Evolutionary cytogenetics in Heteroptera. J Biol Res 5:3–21Google Scholar
  31. Papeschi AG, Mola LM (1989) Meiotic studies in Acanonicus hahni (Stål) (Coreidae, Heteroptera). I. Behaviour of univalent in desynaptic individuals. Genetica 80(1):31–38CrossRefGoogle Scholar
  32. Papeschi AG, Mola LM, Bressa MJ, Greizerstein EJ, Lía V, Poggio L (2003) Behaviour of ring bivalents in holokinetic systems: alternative sites of spindle attachment in Pachylis argentines and Nezara viridula (Heteroptera). Chromosome Res 11:725–733CrossRefPubMedGoogle Scholar
  33. Pineau P, Henry M, Suspène R, Marchio A, Dettai A, Debruyne R et al (2005) A universal primer set for PCR amplification of nuclear histone H4 genes from all animal species. Mol Biol Evol 22(3):582–588CrossRefPubMedGoogle Scholar
  34. Pinkel D, Straume T, Gray JW (1986) Cytogenetic analysis using quantitative, high-sensitivity, fluorescence hybridization. Proc Natl Acad Sci 83(9):2934–2938CrossRefPubMedPubMedCentralGoogle Scholar
  35. Pita S, Panzera F, Ferrandis I, Galvão C, Gómez-Palacio A, Panzera Y (2013) Chromosomal divergence and evolutionary inferences in Rhodniini based on the chromosomal location of ribosomal genes. Mem Inst Oswaldo Cruz 108(3):376–382CrossRefPubMedCentralGoogle Scholar
  36. Rebagliati PJ, Mola LM, Papeschi AG (2001) Karyotype and meiotic behavior of the holokinetic chromosomes of six Argentine species of Pentatomidae (Heteroptera). Caryologia 54:339–347CrossRefGoogle Scholar
  37. Rebagliati PJ, Mola LM, Papeschi AG, Grazia J (2005) Cytogenetic studies in Pentatomidae (Heteroptera): a review. J Zool Sys Evol Res 43:199–213CrossRefGoogle Scholar
  38. Roa F, Guerra M (2012) Distribution of 45S rDNA sites in chromosomes of plants: structural and evolutionary implications. BMC Evol Biol 12:225CrossRefPubMedPubMedCentralGoogle Scholar
  39. Roa F, Guerra M (2015) Non-random distribution of 5S rDNA sites and its association with 45S rDNA in plant chromosomes. Cytogenet Genome Research 146(3):243–249CrossRefGoogle Scholar
  40. Sambrook J, Russell DW (2001) Molecular cloning. A laboratory manual. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  41. Šíchová J, Nguyen P, Dalíková M, Marec F (2013) Chromosomal evolution in tortricid moths: conserved karyotypes with diverged features. PLoS One 8(5):e64520CrossRefPubMedPubMedCentralGoogle Scholar
  42. Silva DMZA, Utsunomia R, Pansonato-Alves JC, Oliveira C, Foresti F (2015) Chromosomal mapping of repetitive DNA sequences in five species of Astyanax (Characiformes, Characidae) reveals independent location of U1 and U2 snRNA sites and association of U1 snRNA and 5S rDNA. Cytogenet Genome Res 146(2):144–152CrossRefPubMedGoogle Scholar
  43. Song N, Liang AP, Bu CP (2012) A molecular phylogeny of Hemiptera inferred from mitochondrial genome sequences. PLoS One 7(11):e48778CrossRefPubMedPubMedCentralGoogle Scholar
  44. Souza HV, Castanhole MMU, Bicudo HEMC, Costa LAA, Itoyama MM (2008) Morphological patterns of the heteropycnotic chromatin and nucleolar material in meiosis and spermiogenesis of some Pentatomidae (Heteroptera). Genet Mol Biol 31(3):686–691CrossRefGoogle Scholar
  45. Úbeda-Manzanaro M, Merlo MA, Palazón JL, Cross I, Sarasquete S, Rebordinos L (2010) Chromosomal mapping of the major and minor ribosomal genes (GATA)n and U2 snRNA gene by double-colour FISH in species of the Batrachoididae family. Genetica 138(7):787–794CrossRefPubMedGoogle Scholar
  46. Ueshima N (1979) Hemiptera II: Heteroptera. In: John B (ed) Animal cytogenetics. Gebrüder Bornträger, Berlin StuttgartGoogle Scholar
  47. Utsunomia R, Scacchetti PC, Pansonato-Alves JC, Oliveira C, Foresti F (2014) Comparative chromosome mapping of U2 snRNA and 5S rRNA genes in Gymnotus species (Gymnotiformes, Gymnotidae): evolutionary dynamics and sex chromosome linkage in G. pantanal. Cytogenet Genome Res 142(4):286–292CrossRefPubMedGoogle Scholar
  48. Weirauch C, Schuh R (2011) Systematics and evolution of Heteroptera: 25 years of progress. Annu Rev Entomol 56:487–510CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Vanessa Bellini Bardella
    • 1
  • José Antônio Marin Fernandes
    • 2
  • Diogo Cavalcanti Cabral-de-Mello
    • 1
  1. 1.Departamento de Biologia, Instituto de Biociências/IBUNESP-Universidade Estadual PaulistaRio ClaroBrazil
  2. 2.Instituto de Ciências BiológicasUniversidade Federal do Pará (UFPA)BelémBrazil

Personalised recommendations