In the present study, the origin of recurrent rearrangements involving chromosome 6 in 3.2% of cells of Melolontha melolontha (Coleoptera, Scarabaeidae) was investigated. Various chromosome staining techniques, including C-banding, Giemsa and silver staining, as well as fluorescence in situ hybridization with a human 28S rDNA probe, were applied to M. melolontha chromosome spreads. In addition, related species of the genera Melolontha and Protaetia were studied. On chromosome 6 of M. melolontha, there is a fragile site-like structure which corresponds to an interstitial nucleolus organizer region (NOR). Despite this instability, the NOR remains unique and interstitial in this species, as well as in the other species studied. It is proposed that the intercalary position of the NOR both facilitates the detection of its fragile site-like instability and correlates with its relative stability during evolution. We explain this apparent paradox by strong counter-selection for imbalances of the chromosome fragment distal to the interstitial NORs, which would recurrently occur in the progeny of translocation carriers. Thus, the frequent telomeric position of the NORs in most animal and plant taxa would have no functional rationale but would be the consequence of selection against the meiotic transmission of chromosome imbalances.

Arnheim N, Krystal M, Schmickel R, Wilson G, Ryder O, Zimmer E: Molecular evidence for genetic exchanges among ribosomal genes on nonhomologous chromosomes in man and apes. Proc Natl Acad Sci USA 77:7323-7327 (1980).
Bedo DG, Webb GC: Conservation of nucleolar structure in polytene tissues of Ceratitis capitata (Diptera: Tephritidae). Chromosoma 98:443-449 (1989).
Cabrero J, Camacho JP: Location and expression of ribosomal RNA genes in grasshoppers: abundance of silent and cryptic loci. Chromosome Res 16:595-607 (2008).
Colomba MS, Vitturi R, Zunino M: Chromosome analysis and rDNA FISH in the stag beetle Dorcus parallelipipedus L. (Coleoptera: Scarabaeoidea: Lucanidae). Hereditas 133:249-253 (2000).
Colomba M, Vitturi R, Volpe N, Lannino A, Zunino M: Karyotype, banding and rDNA FISH in the scarab beetle Anoplotrupes stercorosus (Coleoptera Scarabaeoidea: Geotrupidae). Description and comparative analysis. Micron 35:717-720 (2004).
Colomba M, Vitturi R, Libertini A, Gregorini A, Zunino M: Heterochromatin of the scarab beetle, Bubas bison (Coleoptera: Scarabaeidae) II. Evidence for AT-rich compartimentalization and a high amount of rDNA copies. Micron 37:47-51 (2006).
de Arcanjo AP, Cabral-de-Mello DC, Silva AEB, de Moura RC: Cytogenetic characterization of Eurysternus caribaeus (Coleoptera: Scarabaeidae): evidence of sex-autosome fusion and diploid number reduction prior to species dispersion. J Genet 88:177-182 (2009).
Debatisse M, Le Tallec B, Letessier A, Dutrillaux B, Brison O: Common fragile sites: mechanisms of instability revisited. Trends Genet 28:22-32 (2012).
de Boer LEM: Marked chromosomes associations in catharrhine monkeys, with a note on chromosome associations in other primate groups. J Hum Evol 1:83-86 (1971).
Dimitrova DS: DNA replication initiation patterns and spatial dynamics of the human ribosomal RNA gene loci. J Cell Sci 124:2743-2752 (2011).
Durkin SG, Glover TW: Chromosome fragile sites. Ann Rev Genet 41:169-192 (2007).
Dutrillaux B: Sur la nature et l'origine des chromosomes humains. Monographie des Annales de Génétique. L'expansion Scientifique (1975).
Dutrillaux AM, Dutrillaux B: Chromosome analysis of 82 species of Scarabaeoidea (Coleoptera), with special focus on NOR localization. Cytogenet Genome Res 136:208-219 (2012).
Dutrillaux AM, Xie H, Dutrillaux B: High chromosomal polymorphism and heterozygosity in Cyclocephala tridentata from Guadeloupe: chromosome comparison with some other species of Dynastinae (Coleoptera: Scarabaeidae). Cytogenet Genome Res 119:248-254 (2007a).
Dutrillaux AM, Xie H, Dutrillaux B: Nucleolus and chromosome relationships at pachynema in four Scarabaeoidea (Coleoptera) species with various combinations of NOR and sex chromosomes. Chromosome Res 15:417-427 (2007b).
Eickbush TH, Eickbush DG: Finely orchestrated movements: evolution of the ribosomal RNA genes. Genetics 175:477-485 (2007).
Erickson JM, Rushford CL, Dorney DJ, Wilson GN, Schmickel RD: Structure and variation of human ribosomal DNA: molecular analysis of cloned fragments. Gene 16:1-9 (1981).
Giannoulis T, Dutrillaux AM, Mamuris Z, Montreuil O, Stamatis C, Dutrillaux B: Evolution of European cockchafers (Melolonthinae: Scarabaeidae: Coleoptera): a morphological, molecular and chromosomal study of intra- and inter-specific variations. Bull Entomol Res 101:345-352 (2011).
Grozeva S, Kuznetsova VG, Nokkala S: Patterns of chromosome banding in four nabid species (Heteroptera, Cimicomorpha, Nabidae) with high chromosome number karyotypes. Hereditas 140:99-104 (2004).
Grzywacz B, Maryanska-Nadachowska A, Chobanov DP, Karamysheva T, Warchalowska-Sliwa E: Comparative analysis of the location of rDNA in the Palaearctic bushcricket genus Isophya (Orthoptera: Tettigoniidae: Phaneropterinae). Eur J Entomol 108:509-517 (2011).
Guillén AK, Hirai Y, Tanoue T, Hirai H: Transcriptional repression mechanisms of nucleolus organizer regions (NORs) in humans and chimpanzees. Chromosome Res 12:225-237 (2004).
Hadjilov AA: The Nucleolus and Ribosome Biogenesis (Springer, New York 1985).
Hall KJ, Parker JS: Stable chromosome fission associated with rDNA mobility. Chromosome Res 3:417-422 (1995).
Henderson AS, Warburton D, Atwood KC: Localization of ribosomal DNA in the human chromosome complement. Proc Natl Acad Sci USA 69:3394-3398 (1972).
Henderson AS, Atwood KC, Warburton D: Chromosomal distribution of rDNA in Pan paniscus, Gorilla gorilla beringei, and Symphalangus syndactylus: comparison to related primates. Chromosoma 59:147-155 (1976).
Hennig W, Vogt P, Jacob G, Siegmund I: Nucleolus organizer regions in Drosophila species of the repleta group. Chromosoma 87:279-292 (1982).
Hirai H, Hasegawa Y, Kawamoto Y, Tokita E: Tandem duplication of nucleolus organizer region (NOR) in the Japanese macaque, Macaca fuscata fuscata. Chromosome Res 6:191-197 (1998).
Howell WM, Denton TE, Diamond JR: Differential staining of the satellite regions of human acrocentric chromosomes. Experientia 31:260-262 (1975).
ISCN 1995: An International System for Human Cytogenetic Nomenclature, Mitelman F (ed) (S Karger, Basel 1995).
Lejeune J, Dutrillaux B, Réthoré MO, Prieur M: Comparaison de la structure fine des chromatides d'Homo sapiens et de Pan troglodytes. Chromosoma 43:423-444 (1973).
Lima de Faria A: Equations defining the position of ribosomal cistrons in the eukaryotic chromosome. Nat New Biol 109:136-139 (1973).
McMurray CT: Mechanisms of trinucleotide repeat instability during human development. Nat Rev Genet 11:786-799 (2010).
Moura RC, Souza MJ, Melo NF, Lira-Neto AC: Karyotypic characterization of representatives from Melolonthinae (Coleoptera: Scarabaeidae): karyotypic analysis, banding and fluorescent in situ hybridization (FISH). Hereditas 138:200-206 (2003).
Muleris M, Richard F, Apiou F, Dutrillaux B: Hybridation in situ en cytogénétique moléculaire. Principes et techniques. Techniques et Documentation (Lavoisier, Paris 1996).
Nirchio M, Oliveira C, Alves Ferreira I, Granado A, Ron E: Extensive polymorphism and chromosomal characteristics of ribosomal DNA in the characid fish Triportheus venezuelensis (Characiformes, Characidae). Genet Mol Biol 30:25-30 (2007).
Oliveira SG, Moura RC, Silva AEB, Souza MJ: Cytogenetic analysis of two Coprophanaeus species (Scarabaeidae) revealing wide constitutive heterochromatin variability and the largest number of 45S rDNA sites among Coleoptera. Micron 41:960-965 (2010).
Page SL, Shaffer LG: Chromosome stability is maintained by short intercentromeric distance in functionally dicentric human Robertsonian translocations. Chromosome Res 6:115-122 (1998).
Phillips RB, Pleyte KA, Hatley SE: Stock-specific differences in the number and chromosome positions of the nucleolar organizer regions in arctic char (Salvelinus alpinus). Cytogenet Cell Genet 48:9-12 (1988).
Siroky J, Lysak MA, Dolezel J, Kejnovsky E, Vyskot B: Heterogeneity of rDNA distribution and genome size in Silene ssp. Chromosome Res 9:387-393 (2001).
Suja JA, Gébrane-Younès J, Géraud G, Hernandez-Verdun D: Relative distribution of rDNA and proteins of the RNA polymerase I transcription machinery at chromosomal NORs. Chromosoma 105:459-469 (1997).
Sullivan BA, Willard HF: Stable dicentric X chromosomes with two functional centromeres. Nat Genet 20:227-228 (1998).
Sutherland GR, Richards RI: Fragile sites-cytogenetic similarity with molecular diversity. Am J Hum Genet 64:354-359 (1999).
Vitturi R, Colomba MS, Barbieri R, Zunino M: Ribosomal DNA location in the scarab beetle Thorectes intermedius (Costa) (Coleoptera: Geotrupidae) using banding and fluorescent in-situ hybridization. Chromosome Res 7:255-260 (1999).
Volleth M: Differences in the location of nucleolar organizer regions in European vespertilionid bats. Cytogenet Cell Res 44:186-197 (1987).
Warburton D, Atwood KC, Henderson A: Variation in the number of genes for rRNA among human acrocentric chromosomes: correlation with frequency of satellite association. Cytogenet Cell Genet 17:221-230 (1976).
Zylber EA, Penman S: Products of RNA polymerases in HeLa cell nuclei. Proc Natl Acad Sci USA 68:2861-2865 (1971).
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.