Extensive ribosomal DNA amplification during Andean common bean (Phaseolus vulgaris L.) evolution

Abstract

The extent of 5S and 45S ribosomal DNA (rDNA) variation was investigated in wild and domesticated common beans (Phaseolus vulgaris) chosen to represent the known genetic diversity of the species. 5S and 45S rDNA probes were localized on mitotic chromosomes of 37 accessions by fluorescent in situ hybridization (FISH). The two 5S rDNA loci were largely conserved within the species, whereas a high variation in the number of 45S rDNA loci and changes in position of loci and number of repeats per locus were observed. Domesticated accessions from the Mesoamerican gene pool frequently had three 45S rDNA loci per haploid genome, and rarely four. Domesticated accessions from Andean gene pool, particularly from the race Peru, showed six, seven, eight or nine loci, but seven loci were found in all three races of this gene pool. Between three and eight loci were observed in accessions resulting from crosses between Andean and Mesoamerican genotypes. The presence of two to eight 45S rDNA loci in wild common beans from different geographic locations indicates that the 45S rDNA amplification observed in the Andean lineage took place before domestication. Our data suggest that ectopic recombination between terminal chromosomal regions might be the mechanism responsible for this variation.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Adams SP, Leitch IJ, Bennett MD, Chase MW, Leitch AR (2000) Ribosomal DNA evolution and phylogeny in Aloe (Asphodelaceae). Am J Bot 87:1578–1583

    PubMed  Article  CAS  Google Scholar 

  2. Amirul Islam FM, Beebe S, Munoz M, Tohme J, Redden RJ, Basford KE (2004) Using molecular markers to assess the effect of introgression on quantitative attributes of common bean in the Andean gene pool. Theor Appl Genet 108:243–252

    Article  PubMed  CAS  Google Scholar 

  3. Arnheim N, Krystal M, Schmickel R, Wilson G, Ryder O, Zimmer E (1980) Molecular evidence for genetic exchanges among ribosomal genes on non-homologous chromosomes in man and apes. Proc Natl Acad Sci USA 77:7323–7327

    PubMed  Article  CAS  Google Scholar 

  4. Becerra Velasquez VL, Gepts P (1994) RFLP diversity of common bean (Phaseolus vulgaris) in its centres of origin. Genome 37:256–263

    Article  Google Scholar 

  5. Beebe S, Skroch PW, Tohme J, Duque MC, Pedraza F, Nienhuis J (2000) Structure of genetic diversity among common bean landraces of Middle American origin based on correspondence analysis of RAPD. Crop Sci 40:264–273

    Article  Google Scholar 

  6. Beebe S, Rengifo J, Gaitán E, Duque MC, Tohme J (2001) Diversity and origin of Andean landraces of common bean. Crop Sci 41:854–862

    Article  Google Scholar 

  7. Blair MW, Pedraza F, Buendia HF, Gaitán-Solís E, Beebe SE, Gepts P, Tohme J (2003) Development of a genome-wide anchored microsatellite map for common bean (Phaseolus vulgaris L.). Theor Appl Genet 107:1362–1374

    Article  PubMed  CAS  Google Scholar 

  8. Chácon MI, Pickersgill SB, Debouck DG (2005) Domestication patterns in common bean (Phaseolus vulgaris L.) and the origin of the Mesoamerican and Andean cultivated races. Theor Appl Genet 110:432–444

    Article  PubMed  CAS  Google Scholar 

  9. Delgado-Salinas A, Turley T, Richman A, Lavin M (1999) Phylogenetic analysis of the cultivated and wild species of Phaseolus (Fabaceae). Syst Bot 24:438–460

    Article  Google Scholar 

  10. Dubcovsky J, Dvorak J (1995) Ribosomal RNA multigene loci: nomads of the Triticeae genomes. Genetics 140:1367–1377

    PubMed  CAS  Google Scholar 

  11. Frello S, Heslop-Harrison JS (2000) Chromosomal variation in Crocus vernus Hill (Iridaceae) investigated by in situ hybridization of rDNA and tandemly repeated sequence. Ann Bot 86:317–322

    Article  CAS  Google Scholar 

  12. Freyre R, Skroch PW, Geffroy V, Adam-Blondon A-F, Shirmohamadali A, Johnson WC, Llaca V, Nodari RO, Pereira PA, Tsai S-M, Tohme J, Dron M, Nienhuis J, Vallejos CE, Gepts P (1998) Towards an integrated linkage map of common bean. 4. Development of a core linkage map and alignment of RFLP maps. Theor Appl Genet 97:847–856

    Article  CAS  Google Scholar 

  13. Gepts P (1998) Origin and evolution of common bean: past events and recent trends. HortScience 33:1124–1130

    Google Scholar 

  14. Guerra M, Kenton A (1996) Distribution of telomere DNA in mitotic and polytene nuclei of the anther tapetum of a tetraploid hybrid bean Phaseolus vulgaris × P. acutifolius. Brazil J Genet 19:313–318

    CAS  Google Scholar 

  15. Guerra M, Kenton A, Bennett M (1996) rDNA sites in mitotic and polytene chromosomes of Vigna unguiculata (L.) Walp. and Phaseolus coccineus L. revealed by in situ hybridization. Ann Bot 78:157–161

    Article  CAS  Google Scholar 

  16. Hanson RE, Islam-Faridi MN, Percival EA, Crane CF, Ji Y, McKnight TD, Stelly DM, Price HJ (1996) Distribution of 5S and 18S-28S rDNA loci in a tetraploid cotton (Gossypium hirsutum L.) and its putative diploid ancestors. Chromosoma 105:55–61

    Article  PubMed  CAS  Google Scholar 

  17. Hayasaki M, Morikawa T, Legget JM (2001) Intraspecific variation of 18S-5.8S-26S rDNA sites revealed by FISH and RFLP in wild oat, Avena agadiriana. Genes Genet Syst 76:9–14

    Article  PubMed  CAS  Google Scholar 

  18. Hayashi M, Miyahara A, Sato S, Kato T, Yoshikawa M, Taketa M, Hayashi M, Pedrosa A, Onda R, Imaizumi-Anraku H, Bachmair A, Sandal N, Stougaard J, Murooka Y, Tabata S, Kawasaki S, Kawaguchi M, Harada K (2001) Construction of a genetic linkage map of the model legume Lotus japonicus using an intraspecific F2 population. DNA Res 8:301–310

    Article  PubMed  CAS  Google Scholar 

  19. Heslop-Harrison JS, Schwarzacher T, Anamthawat-Jónsson K, Leitch AR, Shi M, Leitch IJ (1991) In situ hybridization with automated chromosome denaturation. Technique 3:109–115

    Google Scholar 

  20. Kami J, Becerra Velasquez V, Debouck DG, Gepts P (1995) Identification of presumed ancestral DNA sequences of phaseolin in Phaseolus vulgaris. Proc Natl Acad Sci USA 92:1101–1104

    PubMed  Article  CAS  Google Scholar 

  21. Koenig R, Gepts P (1989) Allozyme diversity in wild Phaseolus vulgaris: further evidence for two major centers of genetic diversity. Theor Appl Genet 78:809–817

    Article  Google Scholar 

  22. Marcon AB, Barros IC, Guerra M (2005) Variation in chromosome numbers, CMA bands and 45S rDNA sites in species of Selaginella (Pteridophyta). Ann Bot 95:271–276

    PubMed  CAS  Google Scholar 

  23. Melo NF, Guerra M (2003) Variability of the 5S and 45S rDNA sites in Passiflora L. species with distinct base chromosome numbers. Ann Bot 92:309–316

    Article  PubMed  CAS  Google Scholar 

  24. Moscone EA, Klein F, Lambrou M, Fuchs J, Schweizer D (1999) Quantitative karyotyping and dual-color FISH mapping of 5S and 18S-25S rDNA probes in the cultivated Phaseolus species (Leguminosae). Genome 42:1224–1233

    Article  PubMed  CAS  Google Scholar 

  25. Navratilova A, Neumann P, Macas J (2003) Karyotype analysis of four Vicia species using in situ hybridization with repetitive sequences. Ann Bot 91:921–926

    Article  PubMed  CAS  Google Scholar 

  26. Papa R, Gepts P (2003) Asymmetry of gene flow and differential geographical structure of molecular diversity in wild and domesticated common bean (Phaseolus vulgaris L.) from Mesoamerica. Theor Appl Genet 106:239–250

    PubMed  CAS  Google Scholar 

  27. Pedrosa A, Jantsch MF, Moscone EA, Ambros PF, Schweizer D (2001) Characterisation of pericentromeric and sticky intercalary heterochromatin in Ornithogalum longibracteatum (Hyacinthaceae). Chromosoma 110:203–213

    PubMed  CAS  Google Scholar 

  28. Pedrosa A, Sandal N, Stougaard J, Schweizer D, Bachmair A (2002) Chromosomal map of the model legume Lotus japonicus. Genetics 161:1661–1672

    PubMed  CAS  Google Scholar 

  29. Pedrosa A, Vallejos CE, Bachmair A, Schweizer D (2003) Integration of common bean (Phaseolus vulgaris L.) linkage and chromosomal maps. Theor Appl Genet 106:205–212

    PubMed  CAS  Google Scholar 

  30. Pich U, Fuchs J, Schubert I (1996) How do Alliaceae stabilize their chromosome ends in the absence of TTTAGGG sequences? Chromosome Res 4:207–213

    Article  PubMed  CAS  Google Scholar 

  31. Raskina O, Belyayev A, Nevo E (2004a) Activity of the En/Spm-like transposons in meiosis as a base for chromosome repatterning in a small, isolated, peripheral population of Aegilops speltoides Tausch. Chromosome Res 12:153–161

    Article  PubMed  CAS  Google Scholar 

  32. Raskina O, Belyayev A, Nevo E (2004b) Quantum speciation in Aegilops: molecular cytogenetic evidence from rDNA cluster variability in natural populations. Proc Natl Acad Sci USA 101:14818–14823

    Article  PubMed  CAS  Google Scholar 

  33. Schubert I, Wobus U (1985) In situ hybridization confirms jumping nucleolus organizing regions in Allium. Chromosoma 92:143–148

    Article  Google Scholar 

  34. Sharma S, Raina SN (2005) Organization and evolution of highly repeated satellite DNA sequences in plant chromosomes. Cytogenet Genome Res 109:15–26

    Article  PubMed  CAS  Google Scholar 

  35. Shishido R, Sano Y, Fukui K (2000) Ribosomal DNAs: an exception to the conservation of gene order in rice genomes. Mol Gen Genet 263:586–591

    Article  PubMed  CAS  Google Scholar 

  36. Singh SP, Gepts P, Debouck DG (1991) Races of common bean (Phaseolus vulgaris, Fabaceae). Econ Bot 45:379–396

    Google Scholar 

  37. Sonnante G, Stockton T, Nodari RO, Becerra Velásquez VL, Gepts P (1994) Evolution of genetic diversity during the domestication of common-bean (Phaseolus vulgaris L.). Theor Appl Genet 89:629–635

    Article  Google Scholar 

  38. Tohme J, González DO, Beebe S, Duque MC (1996) AFLP analysis of gene pools of a wild bean core collection. Crop Sci 36:1375–1384

    CAS  Article  Google Scholar 

  39. Vaio M, Speranza P, Valls JF, Guerra M, Mazzella C (2005) Localization of the 5S and 45S rDNA sites and cpDNA sequence analysis in species of the Quadrifaria group of Paspalum (Poaceae, Paniceae). Ann Bot. DOI 10.1093/aob/mci168

  40. Vallejos CE, Sakiyama NS, Chase CD (1992) A molecular marker-based linkage map of Phaseolus vulgaris L. Genetics 131:733–740

    PubMed  CAS  Google Scholar 

  41. Wanzenböck E-M, Schöfer C, Schweizer D, Bachmair A (1997) Ribosomal transcription units integrated via T-DNA transformation associate with the nucleolus and do not require upstream repeat sequences for activity in Arabidopsis thaliana. Plant J 11:1007–1016

    Article  PubMed  Google Scholar 

  42. Wendel JF, Schnabel A, Seelanan T (1995) Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proc Natl Acad Sci USA 92:280–284

    PubMed  Article  CAS  Google Scholar 

  43. Zhang D, Sang T (1999) Physical mapping of ribosomal RNA genes in the peonies (Paeonia, Paeoniaceae) by fluorescent in situ hybridization: implications for phylogeny and concerted evolution. Am J Bot 86:735–740

    PubMed  Article  CAS  Google Scholar 

  44. Zheng J, Irifune K, Hirai K, Nakata M, Tanaka R, Morikawa H (1994) In situ hybridization to metaphase chromosomes in six species of Phaseolus and Vigna using ribosomal DNA as the probe. J Plant Res 107:365–369

    Article  CAS  Google Scholar 

Download references

Acknowledgements

A.P-H. was partially supported by a grant from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Brazil, and by the Hertha-Firnberg program from the Austrian Science Fund (FWF) on behalf of the Federal Ministry for Education, Science and Culture (BMBWK), Austria. C.C.S.A. was supported by a grant from CNPq, Brazil. The work was partially supported by a grant to D.S. from the Gregor Mendel Institute of Molecular Plant Biology (GMI), Austria.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Andrea Pedrosa-Harand.

Additional information

Communicated by J. S. Heslop-Harrison

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Pedrosa-Harand, A., de Almeida, C.C.S., Mosiolek, M. et al. Extensive ribosomal DNA amplification during Andean common bean (Phaseolus vulgaris L.) evolution. Theor Appl Genet 112, 924–933 (2006). https://doi.org/10.1007/s00122-005-0196-8

Download citation

Keywords

  • Common Bean
  • rDNA Locus
  • Wild Bean
  • Mesoamerican Gene Pool
  • Andean Gene Pool