Eur. J. Entomol. 115: 632-640, 2018 | DOI: 10.14411/eje.2018.061

Detection of telomeric sequences and ribosomal RNA genes in holokinetic chromosomes of five jumping plant-lice species: First data on the superfamily Psylloidea (Hemiptera: Sternorrhyncha)Original article

Anna MARYAŃSKA-NADACHOWSKA1, Valentina G. KUZNETSOVA2, Natalia V. GOLUB2, Boris A. ANOKHIN2
1 Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Sławkowska 17, 31-016 Kraków, Poland; e-mail: maryanska@isez.pan.krakow.pl
2 Department of Karyosystematics, Zoological Institute, Russian Academy of Sciences, Universitetskaya nab. 1, 199034 St. Petersburg, Russia; e-mails: valentina_kuznetsova@yahoo.com, psocid@zin.ru, cnidaria@zin.ru

Fluorescence in situ hybridization (FISH) is a technique used to determine the chromosomal position of DNA and RNA probes. The present study contributes to knowledge on jumping plant-lice genomes by using FISH with 18S rDNA and telomeric (TTAGG)n probes on meiotic chromosomes of Psylla alni (2n = 24 + X), Cacopsylla mali (2n = 22 + neo-XY and 20 + neo-X1X2Y), C. sorbi (2n = 20 + neo-XY), Baeopelma foersteri (2n = 14 + X), and Rhinocola aceris (2n = 10 + X). This is the first study that has used FISH on the hemipteran superfamily Psylloidea. We found that the chromosomes of all studied species contain the insect-type telomere motif, (TTAGG)n. In C. mali and C. sorbi, the neo-sex chromosomes originating from autosome-sex chromosome fusions showed no interstitially located clusters of TTAGG repeats, suggesting their loss or inactivation. Similarly, no interstitial (TTAGG)n clusters were detected in an extremely large autosome pair of B. foersteri that most likely originated from a fusion of at least five ancestral chromosome pairs. Clusters of 18S rDNA were detected on the fused and second largest autosome pairs of B. foersteri and on one of the large autosome pairs of the remaining species. In C. mali and B. foersteri, the rDNA clusters were shown to coincide with the NORs as detected by the AgNOR method. Finally, we speculate, based on the obtained FISH markers, on the mechanisms of karyotype evolution of psylloid species differing in chromosome numbers and sex chromosome systems.

Keywords: Hemiptera, Sternorrhyncha, Psylloidea, Psyllidae, Aphalaridae, telomeric repeats, 18S rDNA, FISH, NOR

Received: July 12, 2018; Revised: October 19, 2018; Accepted: October 19, 2018; Published online: November 5, 2018  Show citation

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MARYAŃSKA-NADACHOWSKA, A., KUZNETSOVA, V.G., GOLUB, N.V., & ANOKHIN, B.A. (2018). Detection of telomeric sequences and ribosomal RNA genes in holokinetic chromosomes of five jumping plant-lice species: First data on the superfamily Psylloidea (Hemiptera: Sternorrhyncha). EJE115, Article 632-640. https://doi.org/10.14411/eje.2018.061
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References

  1. Angus R.B., Jeangirard C., Stoianova D., Grozeva S. & Kuznetsova V.G. 2017: A chromosomal analysis of Nepa cinerea Linnaeus, 1758 and Ranatra linearis (Linneaus, 1758) (Heteroptera, Nepidae). - Comp. Cytogenet. 11: 641-657. Go to original source...
  2. Anjos A., Rocha G.C., Paladini A., Mariguela T.C. & Cabral-de-Mello D.C. 2016: Karyotypes and repetitive DNA evolution in six species of the genus Mahanarva (Auchenorrhyncha: Cercopidae). - Cytogenet. Genome Res. 149: 321-327. Go to original source...
  3. Bizzaro D., Mandrioli M., Zanotti M., Giusti M. & Manicardi G.C. 2000: Chromosome analysis and molecular characterization of highly repeated DNAs in the aphid Acyrthosiphon pisum (Aphididae, Hemiptera). - Genetica 108: 197-202. Go to original source...
  4. Burckhardt D. 1987: Jumping plant lice (Homoptera: Psylloidea) of the temperate neotropical region. Part 2: Psyllidae (subfamilies Diaphorininae, Acizziinae, Ciriacreminae and Psyllinae). - Zool. J. Linn. Soc. 90: 145-205. Go to original source...
  5. Burckhardt D. & Ouvrard D. 2012: A revised classification of the jumping plant-lice (Hemiptera: Psylloidea). - Zootaxa 3509: 1-34. Go to original source...
  6. Burckhardt D., Ouvrard D., Percy D. & Queiroz D. 2014: Psyllid host-plants (Hemiptera: Psylloidae): resolving a semantic problem. - Fla Entomol. 97: 242-246. Go to original source...
  7. Chirino M.G., Dalíková M., Marec F. & Bressa M. 2017: Chromosomal distribution of interstitial telomeric sequences as signs of evolution through chromosome fusion in six species of the giant water bugs (Hemiptera, Belostoma). - Ecol. Evol. 7: 5227-5235. Go to original source...
  8. Frydrychová R. & Marec F. 2002: Repeated losses of TTAGG telomere repeats in evolution of beetles (Coleoptera). - Genetica 115: 179-187. Go to original source...
  9. Frydrychová R., Grossmann P., Trubač P., Vítková M. & Marec F. 2004: Phylogenetic distribution of TTAGG telomeric repeats in insects. - Genome 47: 163-178. Go to original source...
  10. Golub N.V., Kuznetsova V.G. & Rakitov R.A. 2014: First karyotype data on the family Myerslopiidae (Hemiptera, Auchenorrhyncha, Cicadomorpha). - Comp. Cytogenet. 8: 293-300. Go to original source...
  11. Goodpasture C. & Bloom S.E. 1975: Vizualization of nucleolar organizer regions in mammalian chromosomes using silver staining. - Chromosoma 53: 37-50. Go to original source...
  12. Grozeva S.M. & Maryańska-Nadachowska A. 1995: Meiosis of two species of Cacopsylla with polymorphic sex chromosomes in males (Homoptera, Psyllidae). - Folia Biol. (Kraków) 43: 93-98.
  13. Grozeva S., Kuznetsova V.G. & Anokhin B.A. 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: 355-374. Go to original source...
  14. Grozeva S., Anokhin B. & Kuznetsova V.G. 2015: Bed bugs (Hemiptera). In Sharachov I. (ed.): Protocols for Cytogenetic Mapping of Arthropod Genomes. CRC press, Taylor & Francis, Boca Raton, pp. 285-326. Go to original source...
  15. Kuznetsova V. & Aguin-Pombo D. 2015: Comparative cytogenetics of Auchenorrhyncha (Hemiptera, Homoptera): a review. - ZooKeys 538: 63-93. Go to original source...
  16. Kuznetsova V.G., Maryańska-Nadachowska A. & Nokkala S. 2003: A new approach to the Auchenorrhyncha (Hemiptera, Insecta) cytogenetics: chromosomes of the meadow spittlebug Philaenus spumarius (L.) examined using various chromosome banding techniques. - Folia Biol. (Kraków) 51: 33-40.
  17. Kuznetsova V.G., Grozeva S.M. & Anokhin B.A. 2012: The first finding of (TTAGG)n telomeric repeat in chromosomes of true bugs (Heteroptera, Belostomatidae). - Comp. Cytogenet. 6: 341-346. Go to original source...
  18. Kuznetsova V.G., Maryańska-Nadachowska A. & Karamysheva T. 2015a: Spittlebugs (Hemiptera). In Sharakhov I. (ed.): Protocols for Cytogenetic Mapping of Arthropod Genomes. CRC Press, Taylor & Francis Group, Boca Raton, pp. 351-380. Go to original source...
  19. Kuznetsova V.G., Grozeva S.M., Hartung V. & Anokhin B.V. 2015b: First evidence for (TTAGG)n telomeric sequence and sex chromosome postreduction in Coleorrhyncha (Insecta, Hemiptera). - Comp. Cytogenet. 9: 523-532. Go to original source...
  20. Kuznetsova V.G., Maryańska-Nadachowska A., Anokhin B.V. & Aguin-Pombo D. 2015c: Evidence for TTAGG telomere repeats and rRNA gene clusters in leafhoppers of the genus Alebra (Hemiptera: Auchenorrhyncha: Cicadellidae). - Eur. J. Entomol. 112: 207-214. Go to original source...
  21. Labina E.S., Maryańska-Nadachowska A. & Kuznetsova V.G. 2007: Meiotic karyotypes in males of nineteen species of Psylloidea (Hemiptera) in the families Psyllidae and Triozidae. -Folia Biol. (Kraków) 55: 27-34. Go to original source...
  22. Lin K.W. & Yan J. 2008: Ending in the middle: Current knowledge of interstitial telomeric sequences. - Mutat. Res. 658: 95-110. Go to original source...
  23. Luan J., Sun X., Fei Z. & Douglas A.E. 2018: Maternal inheritance of a single somatic animal cell displayed by the bacteriocyte in the whitefly Bemisia tabaci. - Curr. Biol. 28: 459-465. Go to original source...
  24. Manicardi G.C., Mandrioli M. & Blackman R.L. 2015: The cytogenetic architecture of the aphid genome. - Biol. Rev. 90: 112-125. Go to original source...
  25. Maryańska-Nadachowska A. 1999: B-chromosome polymorphism in Rhinocola aceris (Psylloidea, Homoptera). - Folia Biol. (Kraków) 47: 115-121.
  26. Maryańska-Nadachowska A. 2002: Review of karyotype variation in jumping plant-lice (Psylloidea, Sternorrhyncha, Hemiptera) and checklist of chromosome numbers. - Folia Biol. (Kraków) 50: 135-152.
  27. Maryańska-Nadachowska A. & Głowacka E. 2005: Meiotic karyotypes and structure of testes of nineteetn species of jumping-lice (Hemiptera, Psylloidea) from South Africa. - Folia Biol. (Kraków) 53: 143-148. Go to original source...
  28. Maryańska-Nadachowska A. & Grozeva S. 2001: Patterns of C- and AgNO3 bands in Cacopsylla mali (Schmidberger) and C. sorbi (Linnaeus) (Homoptera, Psyllidae) - species with polymorphic sex chromosome system. - Folia Biol. (Kraków) 49: 157-161.
  29. Maryańska-Nadachowska A., Kuznetsova V.G. & Warchałowska-Śliwa E. 1992a: Karyotypes of Psyllina (Homoptera). I. New data and check-list. - Folia Biol. (Kraków) 40: 15-25.
  30. Maryańska-Nadachowska A., Warchalowska-Śliwa E. & Kuznetsova V.G. 1992b: The NOR and nucleolus in the spermatogenesis of Psyla alni (L.) (Homoptera) analysed by silver staining. - Folia Biol. (Kraków) 40: 41-45. Go to original source...
  31. Maryańska-Nadachowska A., Kuznetsova V.G., Yang C.T. & Woudstra I.H. 1996: New data on karyotypes and the number of testicular follicles in the psyllid families Aphalaridae, Psyllidae, Carsidaridae, and Triozidae (Homoptera, Psylloidea). - Caryologia 49: 279-285. Go to original source...
  32. Maryańska-Nadachowska A., Kuznetsova V.G. & Karamysheva T.V. 2013: Chromosomal location of rDNA clusters and TTAGG telomeric repeats in eight species of the spittlebug genus Philaenus (Hemiptera: Auchenorrhyncha: Aphrophoridae). - Eur. J. Entomol. 110: 411-418. Go to original source...
  33. Maryańska-Nadachowska A., Anokhin B.A., Gnezdilov V.M. & Kuznetsova V.G. 2016: Karyotype staility in the family Issidae (Hemiptera, Auchenorrhyncha) revealed by chromosome techniques and FISH with telomeric (TTAGG)n and 18S rDNA probes. - Comp. Cytogenet. 10: 347-369. Go to original source...
  34. Mohan K.N., Rani B.S., Kulashreshta P.S. & Kadandale J.S. 2011: Characterization of TTAGG telomeric repeats, their interstitial occurrence and constitutively active telomerase in the mealybug Planococcus lilacinus (Homoptera; Coccoidea). - Chromosoma 120: 165-175. Go to original source...
  35. Mola L.M. & Papeschi A.G. 2006: Holokinetic chromosomes at a glance. - J. Basic Appl. Genet. 17: 17-33.
  36. Monti V., Manicardi G.C. & Mandrioli M. 2011: Cytogenetic and molecular analysis of the holocentric chromosomes of the potato aphid Macrosiphum euphorbiae (Thomas, 1878). - Comp. Cytogenet. 5: 163-172. Go to original source...
  37. Nokkala S. & Nokkala C. 2004: Interaction of B chromosomes with A or B chromosomes in segregation in insects. - Cytogenet. Genome Res. 106: 394-397. Go to original source...
  38. Nokkala S., Kuznetsova V. & Maryańska-Nadachowska A. 2000: Achiasmate segregation of a B chromosome from the X chromosome in two species of psyllids (Psylloidea, Homoptera). - Genetica 108: 181-189. Go to original source...
  39. Nokkala S., Kuznetsova V., Maryańska-Nadachowska A. & Nokkala C. 2004: Holocentric chromosomes in meiosis. I. Restriction of the numer of chiasmata in bivalents. - Chromosome Res. 12: 733-739. Go to original source...
  40. Nokkala S., Kuznetsova V.G., Maryańska-Nadachowska A. & Nokkala C. 2006: Holocentric chromosomes in meiosis. II. The modes of orientation and segregation of a bivalent. - Chromosome Res. 14: 559-565. Go to original source...
  41. Nokkala S. Maryańska-Nadachowska A. & Kuznetsova V.G. 2008: First evidence of polyploidy in Psylloidea (Homoptera, Sternorrhyncha): a parthenogenetic population of Cacopsylla myrtilli (W. Wagner, 1947) from northeast Finland is apomictic and triploid. - Genetica 133: 201-205. Go to original source...
  42. Nokkala C., Kuznetsova V.G. & Nokkala S. 2013: Meiosis in rare males in parthenogenetic Cacopsylla myrtilli (Wagner, 1947) (Hemiptera, Psyllidae) populations from northern Europe. - Comp. Cytogenet. 7: 241-251. Go to original source...
  43. Nokkala S., Kuznetsova V.G. & Nokkala C. 2017: Characteristics of parthenogenesis in Cacopsylla ledi (Flor, 1861) (Hemiptera, Sternorrhyncha, Psylloidea): cytological and molecular approaches. - Comp. Cytogenet. 11: 807-817. Go to original source...
  44. Papeschi A.G. & Bressa M.J. 2006: Classical and molecular cytogenetics in Heteroptera. - Res. Adv. Entomol. 1: 1-9.
  45. Percy D.M., Crampton-Platt A., Sveinsson S., Lemmon A.R., Moriarty Lemmon E., Ouvrard D. & Burckhardt D. 2018: Resolving the psyllid tree of life: phylogenetic analyses of the superfamily Psylloidea (Hemiptera). - Syst. Entomol. [in press] doi: 10.1111/syen.12302 Go to original source...
  46. Rego A. & Marec F. 2003: Telomeric and interstitial telomeric sequences in holokinetic chromosomes of Lepidoptera: Telomeric DNA mediates association between postpachytene bivalents in achiasmatic meiosis of females. - Chromosome Res. 11: 681-694. Go to original source...
  47. Sahara K., Marec F. & Traut W. 1999: TTAGG telomeric repeats in chromosomes of some insects and other arthropods. - Chromosome Res. 7: 449-460. Go to original source...
  48. Suomalainen E. & Halkka O. 1963: The mode of meiosis in the Psyllina. - Chromosoma 14: 498-510. Go to original source...
  49. Vítková M., Král J., Traut W., Zrzavý J. & Marec F. 2005: The evolutionary origin of insect telomeric repeats, (TTAGG)n. - Chromosome Res. 13: 145-156. Go to original source...
  50. Walton C.J. 1960: The life cycle of the hackberry gall-former, Pachypsylla celtidisgemma (Homoptera: Psyllidae). - Ann. Entomol. Soc. Am. 53: 265-277. Go to original source...

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