Genetica

, Volume 135, Issue 1, pp 87–93

Molecular cytogenetic characterization of Rumex papillaris, a dioecious plant with an XX/XY1Y2 sex chromosome system

  • Rafael Navajas-Pérez
  • Trude Schwarzacher
  • Manuel Ruiz Rejón
  • Manuel A. Garrido-Ramos
Article

Abstract

Rumex papillaris Boiss, & Reut., an Iberian endemic, belongs to the section Acetosa of the genus Rumex whose main representative is R. acetosa L., a species intensively studied in relation to sex-chromosome evolution. Here, we characterize cytogenetically the chromosomal complement of R. papillaris in an effort to enhance future comparative genomic approaches and to better our understanding of sex chromosome structure in plants. Rumex papillaris, as is common in this group, is a dioecious species characterized by the presence of a multiple sex chromosome system (with females 2n = 12 + XX and males 2n = 12 + XY1Y2). Except for the X chromosome both Y chromosomes are the longest in the karyotype and appear heterochromatic due to the accumulation of at least two satellite DNA families, RAE180 and RAYSI. Each chromosome of pair VI has an additional major heterochromatin block at the distal region of the short arm. These supernumerary heterochromatic blocks are occupied by RAE730 satellite DNA family. The Y-related RAE180 family is also present in an additional minor autosomal locus. Our comparative study of the chromosomal organization of the different satellite-DNA sequences in XX/XY and XX/XY1Y2Rumex species demonstrates that of active mechanisms of heterochromatin amplification occurred and were accompanied by chromosomal rearrangements giving rise to the multiple XX/XY1Y2 chromosome systems observed in Rumex. Additionally, Y1 and Y2 chromosomes have undergone further rearrangements leading to differential patterns of Y-heterochromatin distribution between Rumex species with multiple sex chromosome systems.

Keywords

Heterochromatin In situ hybridization Satellite DNA Sex chromosomes Rumex papillaris 

Abbreviations

A

Adenosine

bp

Base pair(s)

DAPI

4′,6-diamidino-2-phenylindole

dNTP

Deoxyribonucleoside triphosphate

EDTA

Ethylenediaminetetraacetic acid

h

Hour(s)

ng

Nanogram(s)

ml

Milliliter(s)

mya

Million years ago

PCR

Polymerase chain reaction

SDS

Sodium dodecyl sulfate

SSC

Saline–sodium citrate

T

Thymidine

References

  1. Ainsworth CC, Lu J, Winfield M et al (1999) Sex determination by X: autosome dosage: Rumex acetosa (sorrel). In: Ainsworth CC (ed) Sex determination in plants. BIOS Scientific Publishers Limited, pp 124–136Google Scholar
  2. Charlesworth B (1996) The evolution of chromosomal sex determination and dosage compensation. Curr Biol 6:149–162PubMedCrossRefGoogle Scholar
  3. Cuñado N, Navajas-Pérez R, de la Herrán R et al (2007) The evolution of sex chromosomes in the genus Rumex (Polygonaceae): identification of a new species with heteromorphic sex chromosomes. Chromosome Res 15:825–833PubMedCrossRefGoogle Scholar
  4. Degraeve N (1976) Contribution à l’étude cytotaxonomique des Rumex. IV Le genre Acetosa Mill. Cellule 71:231–240Google Scholar
  5. Kihara H, Ono T (1923) Cytological studies on Rumex L. I. Chromosomes of Rumex acetosa L. Bot Mag Tokyo 37:84–90Google Scholar
  6. Koch M, Haubold AB, Mitchell-Olds T (2000) Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol Biol Evol 17:1483–1498PubMedGoogle Scholar
  7. Kuroki Y (1987) Karyotype variation and heterochromatin in Rumex acetosa. Plant Chromosome Res 1987. Nishiki Print Co, Ltd, Hiroshima, Japan, pp 227–230Google Scholar
  8. Kuroki Y, Yokohama A, Iwatsubo Y (1994) Fluorescent chromosome banding in Rumex montanus (Polygonaceae). Kromosomo 74:2591–2597Google Scholar
  9. Lengerova M, Vyskot B (2001) Sex chromatin and nucleolar analyses in Rumex acetosa L. Protoplasma 217:147–153PubMedCrossRefGoogle Scholar
  10. López González G (1990) Género Rumex L. In: Castroviejo S, Laínz M, López González G, Montserrat P, Muñoz Garmendia F, Paiva J, Villar L (eds) Flora Iberica, vol 2. CSIC, Real Jardín Botánico de Madrid, Madrid, Spain, pp 595–634Google Scholar
  11. Löve Á (1944) Cytogenetic studies on Rumex subgenus acetosella. Hereditas 30:1–136CrossRefGoogle Scholar
  12. Löve Á, Kapoor B (1967) A chromosome atlas of the collective genus Rumex. Cytologia 32:320–342Google Scholar
  13. Mariotti B, Navajas-Pérez R, Lozano R et al (2006) Cloning and characterisation of dispersed repetitive DNA derived from microdissected sex chromosomes of Rumex acetosa. Genome 49:114–121PubMedGoogle Scholar
  14. Mosiolek M, Pasierbek P, Malarz J et al (2005) Rumex acetosa Y chromosomes: constitutive or facultative heterochromatin? Folia Histochem Cytobiol 43:161–167PubMedGoogle Scholar
  15. Navajas-Pérez R, de la Herrán R, López González G et al (2005a) The evolution of reproductive systems and sex-determining mechanisms within Rumex (Polygonaceae) inferred from nuclear and chloroplastidial sequence data. Mol Biol Evol 22:1929–1939PubMedCrossRefGoogle Scholar
  16. Navajas-Pérez R, de la Herrán R, Jamilena M et al (2005b) Reduced rates of sequence evolution of Y-linked satellite DNA in Rumex (Polygonaceae). J Mol Evol 60:391–399PubMedCrossRefGoogle Scholar
  17. Navajas-Pérez R, Schwarzacher T, de la Herrán R et al (2006) The origin and evolution of the variability in a Y-specific satellite-DNA of Rumex acetosa and its relatives. Gene 368:61–71PubMedCrossRefGoogle Scholar
  18. Nicolas M, Marais G, Hykelova V et al (2005) A gradual process of recombination restriction in the evolutionary history of the sex chromosomes in dioecious plants. PLoS Biol 3:47–56CrossRefGoogle Scholar
  19. Rechinger KH Jr (1964) The genus Rumex L. In: Tutin TG, Heywood VH, Burges NA, Valentine DH, Walters SM, Webb DA (eds) Flora Europaea, vol 1. Cambridge University Press, Cambridge, UK, pp 82–89Google Scholar
  20. Renner SS, Ricklefs RE (1995) Dioecy and its correlates in the flowering plants. Am J Bot 82:596–606CrossRefGoogle Scholar
  21. Ruiz Rejón M (2004) Sex chromosomes in plants. In: Goodman RM (ed) Encyclopedia of plant and crop sciences, vol 4. Dekker Agropedia, Marcel Dekker, New York, pp 1148–1151Google Scholar
  22. Ruiz Rejón C, Jamilena M, Garrido-Ramos MA et al (1994) Cytogenetic and molecular analysis of the multiple sex chromosome system of Rumex acetosa. Heredity 72:209–215CrossRefGoogle Scholar
  23. Schwarzacher T (2003) DNA, chromosomes and in situ hybridization. Genome 46:953–962PubMedCrossRefGoogle Scholar
  24. Schwarzacher T, Heslop-Harrison JS (2000) Practical in situ hybridization. BIOS Scientific Publishers Limited, Oxford, UKGoogle Scholar
  25. Shibata F, Hizume M, Kuroki Y (1999) Chromosome painting of Y chromosomes and isolation of a Y chromosome-specific repetitive sequence in the dioecious plant Rumex acetosa. Chromosoma 108:266–270PubMedCrossRefGoogle Scholar
  26. Shibata F, Hizume M, Kuroki Y (2000a) Differentiation and the polymorphic nature of the Y chromosomes revealed by repetitive sequences in the dioecious plant, Rumex acetosa. Chromosome Res 8:229–236PubMedCrossRefGoogle Scholar
  27. Shibata F, Hizume M, Kuroki Y (2000b) Molecular cytogenetic analysis of supernumerary heterochromatic segments in Rumex acetosa. Genome 43:391–397PubMedCrossRefGoogle Scholar
  28. Smith BW (1964) The evolving karyotype of Rumex hastatulus. Evolution 18:93–104CrossRefGoogle Scholar
  29. Smith BW (1968) Cytogeography and cytotaxonomic relationships of Rumex paucifolius. Am J Bot 55:673–683CrossRefGoogle Scholar
  30. 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 423:825–837PubMedCrossRefGoogle Scholar
  31. Steinemann M, Steinemann S (1997) The enigma of the Y chromosome degeneration: TRAM, a novel retrotransposon is preferentially located on the neo-Y chromosome of Drosophila miranda. Genetics 145:261–266PubMedGoogle Scholar
  32. Wilby AS, Parker JS (1988a) The supernumerary segment systems of Rumex acetosa. Heredity 60:109–117CrossRefGoogle Scholar
  33. Wilby AS, Parker JS (1988b) Recurrent patterns of chromosome variation in a species group. Heredity 61:55–62CrossRefGoogle Scholar
  34. Yu Q, Hou S, Feltus FA et al (2008a) Low X/Y divergence in four pairs of papaya sex-linked genes. Plant J 53:124–132 PubMedCrossRefGoogle Scholar
  35. Yu Q, Navajas-Pérez R, Tong E et al (2008b) Recent origin of dioecious and gynodioecious Y chromosomes in papaya. Trop Plant Biol. doi: 10.1007/s12042-007-9005-7

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Rafael Navajas-Pérez
    • 1
  • Trude Schwarzacher
    • 2
  • Manuel Ruiz Rejón
    • 3
  • Manuel A. Garrido-Ramos
    • 3
  1. 1.Plant Genome Mapping LaboratoryUniversity of GeorgiaAthensUSA
  2. 2.Department of BiologyUniversity of LeicesterLeicesterUK
  3. 3.Departamento de Genética, Facultad de CienciasUniversidad de GranadaGranadaSpain

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