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Heterochromatin characterization and ribosomal gene location in two monotypic genera of bloodsucker bugs (Cimicidae, Heteroptera) with holokinetic chromosomes and achiasmatic male meiosis

Published online by Cambridge University Press:  11 September 2014

M.G. Poggio ,
O. Di Iorio ,
P. Turienzo ,
A. G. Papeschi  and
M.J. Bressa
M.G. Poggio*
Affiliation:
Instituto de Ecología, Genética y Evolución de Buenos Aires (IEGEBA), Departamento de Ecología, Genética y Evolución (EGE), Facultad de Ciencias Exactas y Naturales (FCEyN), Universidad de Buenos Aires (UBA), Ciudad Autónoma de Buenos Aires, Argentina
O. Di Iorio
Affiliation:
Entomología. Departamento de Biodiversidad y Biología Experimental (DBBE), FCEyN, UBA, Ciudad Autónoma de Buenos Aires, Argentina
P. Turienzo
Affiliation:
Entomología. Departamento de Biodiversidad y Biología Experimental (DBBE), FCEyN, UBA, Ciudad Autónoma de Buenos Aires, Argentina
A. G. Papeschi
Affiliation:
Instituto de Ecología, Genética y Evolución de Buenos Aires (IEGEBA), Departamento de Ecología, Genética y Evolución (EGE), Facultad de Ciencias Exactas y Naturales (FCEyN), Universidad de Buenos Aires (UBA), Ciudad Autónoma de Buenos Aires, Argentina
M.J. Bressa
Affiliation:
Instituto de Ecología, Genética y Evolución de Buenos Aires (IEGEBA), Departamento de Ecología, Genética y Evolución (EGE), Facultad de Ciencias Exactas y Naturales (FCEyN), Universidad de Buenos Aires (UBA), Ciudad Autónoma de Buenos Aires, Argentina
*
*Author for correspondence Phone: +54-11 4576-3300 Fax: +54-11 4576-3354 E-mail: [email protected]
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Abstract

Members of the family Cimicidae (Heteroptera: Cimicomorpha) are temporary bloodsuckers on birds and bats as primary hosts and humans as secondary hosts. Acanthocrios furnarii (2n=12=10+XY, male) and Psitticimex uritui (2n=31=28+X1X2Y, male) are two monotypic genera of the subfamily Haematosiphoninae, which have achiasmatic male meiosis of collochore type. Here, we examined chromatin organization and constitution of cimicid holokinetic chromosomes by determining the amount, composition and distribution of constitutive heterochromatin, and number and location of nucleolus organizer regions (NORs) in both species. Results showed that these two bloodsucker bugs possess high heterochromatin content and have an achiasmatic male meiosis, in which three regions can be differentiated in each autosomal bivalent: (i) terminal heterochromatic regions in repulsion; (ii) a central region, where the homologous chromosomes are located parallel but without contact between them; and (iii) small areas within the central region, where collochores are detected. Acanthocrios furnarii presented a single NOR on an autosomal pair, whereas P. uritui presented two NORs, one on an autosomal pair and the other on a sex chromosome. All NORs were found to be associated with CMA3 bright bands, indicating that the whole rDNA repeating unit is rich in G+C base pairs. Based on the variations in the diploid autosomal number, the presence of simple and multiple sex chromosome systems, and the number and location of 18S rDNA loci in the two Cimicidae species studied, we might infer that rDNA clusters and genome are highly dynamic among the representatives of this family.

Keywords

achiasmatic male meiosisconstitutive heterochromatinholokinetic chromosomeskaryotype evolutionribosomal DNA
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 104 , Issue 6 , December 2014 , pp. 788 - 793
Copyright
Copyright © Cambridge University Press 2014 

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References

Barros e Silva, A.E. & Guerra, M. (2010) The meaning of DAPI bands observed after C-banding and FISH procedures. Biotechnic and Histochemistry 85, 115–125.Google Scholar
Bressa, M.J., Larramendy, M. & Papeschi, A.G. (2005) Heterochromatin characterization in five species of Heteroptera. Genetica 124, 307–317.Google Scholar
Bressa, M.J., Papeschi, A.G., Vitková, M., Kubíčková, S., Fuková, I., Pigozzi, M.I. & Marec, F. (2009) Sex chromosome evolution in cotton stainers of the genus Dysdercus (Heteroptera: Pyrrhocoridae). Cytogenetic and Genome Research 125, 292–305.Google Scholar
Cabral-de-Mello, D.C., Oliveira, S.G., Moura, R.C. & Martins, C. (2011) Chromosomal organization of the 18S and 5S rRNAs and histone H3 genes in Scarabaeinae coleopterans: insights into the evolutionary dynamics of multigene families and heterochromatin. BMC Genetics 12, 88.Google Scholar
Criniti, A., Simonazzi, G., Cassanelli, S., Ferrari, M., Bizzaro, D. & Manicardi, G.C. (2009) Distribution of heterochromatin and rDNA on the holocentric chromosomes of the aphids Dysaphis plantaginea and Melanaphis pyraria (Hemiptera: Aphididae). European Journal of Entomology 106, 153–157.Google Scholar
Fuková, I., Nguyen, P. & Marec, F. (2005) Codling moth cytogenetics: karyotype, chromosomal location of rDNA, and molecular differentiation of sex chromosomes. Genome 48, 1083–1092.Google Scholar
Glaser, R.W. (1917) Ringer solutions and some notes on the physiological basis of their ionic composition. Comparative Biochemistry and Physiology 2, 241–289.Google Scholar
Grozeva, S. & Nokkala, S. (2002) Achiasmatic male meiosis in Cimex sp. (Heteroptera, Cimicidae). Caryologia 55, 189–192.CrossRefGoogle Scholar
Grozeva, S., Kuznetsova, V. & Anokhin, B. (2010) Bed bug cytogenetics: karyotype, sex chromosome system, FISH mapping of 18S rDNA, and male meiosis in Cimex lectularius Linnaeus, 1758 (Heteroptera: Cimicidae). Comparative Cytogenetics 4, 151–160.Google Scholar
Heitz, E. (1933) Die somatischen Heteropyknose bei Drosophila melanogaster und ihre genetische Bedeutung. Zeitschrift fuer Zellforschung 20, 237–287.Google Scholar
Heitz, E. (1935) Die Herkunft der Chromozentren. Planta 18, 571–635.Google Scholar
John, B. (1988) The biology of heterochromatin. pp. 1–147 in Verma, R.S. (Ed.) Heterochromatin: Molecular and Structural Aspects. Cambridge, Cambridge University Press.Google Scholar
John, B. (1990) Meiosis. Cambridge, Cambridge University Press.Google Scholar
Kuznetsova, V., Grozeva, S., Nokkala, S. & Nokkala, C. (2011) Cytogenetics of the true bug infraorder Cimicomorpha (Hemiptera, Heteroptera): a review. ZooKeys 154, 31–70.Google Scholar
Lockwood, A.P.M. (1961) “Ringer” solutions and some notes on the physiological basis of their ionic composition. Comparative Biochemical Physiology 2, 241–289.Google Scholar
Morielle-Souza, A. & Azeredo-Oliveira, M.T.V. (2007) Differential characterization of holocentric chromosomes in triatomines (Hetroptera, Traitominae) using different staining techniques and flourescent in situ hybridization. Genetics and Molecular Research 6, 713–720.Google Scholar
Panzera, F., Scvortzoff, E., Pérez, R., Panzera, Y., Hornos, S., Cestau, R., Nicolini, P., Delgado, V., Alvarez, F., Mazzella, M.C., Cossio, G., Martinez, M. & Salvatella, R. (1998) Cytogenetics of triatomines. pp. 621–664 in Carcavallo, R., Galindez Girón, I., Jurberg, J. & Lent, H. (Eds.) Atlas of Chagas' Disease Vectors in the American. Vol. II. Fiocruz, Río de Janeiro, Brasil.Google Scholar
Papeschi, A.G. (1991) DNA content and heterochromatin variation in species of Belostoma (Heteroptera, Belostomatidae). Hereditas 115, 109–114.Google Scholar
Papeschi, A.G. & Bressa, M.J. (2006) Evolutionary cytogenetics in Heteroptera. Journal of Biological Research 5, 3–21.Google Scholar
Poggio, M.G., Bressa, M.J. & Papeschi, A.G. (2007) Karyotype evolution in Reduviidae (Insecta: Heteroptera) with special reference to Stenopodainae and Harpactorinae. Comparative Cytogenetics 1, 159–168.Google Scholar
Poggio, M.G., Bressa, M.J., Papeschi, A.G., Di Iorio, O.R. & Turienzo, P.N. (2009) Insects found in birds’ nests from Argentina: cytogenetic studies in Cimicidae (Hemiptera) and its taxonomical and phylogenetic implications. Zootaxa 2315, 39–46.Google Scholar
Poggio, M.G., Bressa, M.J. & Papeschi, A.G. (2011) Male meiosis, heterochromatin characterization and chromosomal location of rDNA in Microtomus lunifer (Berg, 1900) (Hemiptera: Reduviidae: Hammacerinae). Comparative Cytogenetics 5, 1–22.Google Scholar
Raskina, O., Barber, J.C., Nevo, E. & Belyayev, A. (2008) Repetitive DNA and chromosomal rearrangements: speciation-related events in plant genomes. Cytogenetic and Genome Research 120, 351–357.Google Scholar
Ryckman, R.E. & Ueshima, N. (1964) Biosystematics of the Hesperocimex complex (Hemiptera: Cimicidae) and avian hosts (Piciformes: Picidae; Passeriformes: Hirundinidae). Annals of the Entomological Society of America 57, 624–638.Google Scholar
Sadílek, D., Št'áhlavský, F., Vilímová, J. & Zima, J. (2013) Extensive fragmentation of the X chromosome in the bed bug Cimex lectularius Linnaeus, 1758 (Heteroptera, Cimicidae): a survey across Europe. Comparative Cytogenetics 7, 253–269.Google Scholar
Schubert, I. (1984) Mobile nucleolus organizing regions (NORs) in Allium (Liliaceae S. Lat) – inferences from the specificity of silver staining. Plant Systematics and Evolution 144, 291–305.Google Scholar
Schubert, I. (2007) Chromosome evolution. Current Opinion in Plant Biology 10, 109–115.Google Scholar
Severi-Aguiar, G.D.C., Lourenço, L.B., Bicudo, H.E.M.C. & Azeredo-Oliveira, M.T.V. (2006) Meiosis aspects and nuclear activity in Triatoma vitticeps (Triatominae, Heteroptera). Genetica 126, 141–151.Google Scholar
Solari, A.J. & Agopian, S. (1987) Recombination nodules, synaptonemal complexes and heterochromatin in the hemipteran Triatoma infestans . Microscopía Electrónica y Biología Celular 11, 179–195.Google ScholarPubMed
Stack, S.M. (1984) Heterochromatin, the synaptonemal complex and crossing over. Journal of Cell Science 71, 159–176.Google Scholar
Sumner, A.T. (2003) Chromosomes: Organization and Function. Malden, Blackwell Science Ltd.Google Scholar
Toscani, M.A., Papeschi, A.G. & Pigozzi, M.I. (2011) La formación de ejes meióticos y su relación con regiones heterocromáticas en los heterópteros (Hemiptera, Insecta). Journal of Basic and Applied Genetics XXI (Supplement), 152.Google Scholar
Traut, W. (1976) Pachytene mapping in the female silkworm Bombyx mori L. (Lepidoptera). Chromosoma 58, 275–284.CrossRefGoogle ScholarPubMed
Ueshima, N. (1966) Cytology and cytogenetics. pp. 183–237 in Usinger, R.L. (Ed.) Monograph of Cimicidae. Volume VII. Thomas Say Foundation Entomology Society of America, College Park, Maryland, USA.Google Scholar
Ueshima, N. (1979) Hemiptera II: Heteroptera. pp. V+117 in John, B. (Ed.) Animal Cytogenetics. Berlin-Stuttgart, Gebrüder Borntraeger.Google Scholar
Usinger, R.L. (1966) Monograph of Cimicidae (Hemiptera – Heteroptera). Volume VII. pp. XI+586. Thomas Say Foundation Entomological Society of America, College Park, Maryland, USA.Google Scholar
Zhang, X., Eickbush, M.T. & Eickbush, T.H. (2008) Role of recombination in the longterm retention of transposable elements in rRNA gene loci. Genetics 180, 1617–1627.Google Scholar