Theoretical and Applied Genetics

, Volume 112, Issue 5, pp 924–933 | Cite as

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

  • Andrea Pedrosa-Harand
  • Cícero C. Souza de Almeida
  • Magdalena Mosiolek
  • Matthew W. Blair
  • Dieter Schweizer
  • Marcelo Guerra
Original Paper

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.

References

  1. Adams SP, Leitch IJ, Bennett MD, Chase MW, Leitch AR (2000) Ribosomal DNA evolution and phylogeny in Aloe (Asphodelaceae). Am J Bot 87:1578–1583PubMedCrossRefGoogle 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 108:243–252CrossRefPubMedGoogle 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 77:7323–7327PubMedCrossRefGoogle Scholar
  4. Becerra Velasquez VL, Gepts P (1994) RFLP diversity of common bean (Phaseolus vulgaris) in its centres of origin. Genome 37:256–263CrossRefGoogle 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 40:264–273CrossRefGoogle Scholar
  6. Beebe S, Rengifo J, Gaitán E, Duque MC, Tohme J (2001) Diversity and origin of Andean landraces of common bean. Crop Sci 41:854–862CrossRefGoogle 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 107:1362–1374CrossRefPubMedGoogle 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 110:432–444CrossRefPubMedGoogle 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 24:438–460CrossRefGoogle Scholar
  10. Dubcovsky J, Dvorak J (1995) Ribosomal RNA multigene loci: nomads of the Triticeae genomes. Genetics 140:1367–1377PubMedGoogle 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 86:317–322CrossRefGoogle 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 97:847–856CrossRefGoogle Scholar
  13. Gepts P (1998) Origin and evolution of common bean: past events and recent trends. HortScience 33:1124–1130Google 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 19:313–318Google 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 78:157–161CrossRefGoogle 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 105:55–61CrossRefPubMedGoogle 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 76:9–14CrossRefPubMedGoogle 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 8:301–310CrossRefPubMedGoogle 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 3:109–115Google 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 92:1101–1104PubMedCrossRefGoogle 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 78:809–817CrossRefGoogle 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 95:271–276PubMedGoogle 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 92:309–316CrossRefPubMedGoogle 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 42:1224–1233CrossRefPubMedGoogle Scholar
  25. Navratilova A, Neumann P, Macas J (2003) Karyotype analysis of four Vicia species using in situ hybridization with repetitive sequences. Ann Bot 91:921–926CrossRefPubMedGoogle 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 106:239–250PubMedGoogle 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 110:203–213PubMedGoogle Scholar
  28. Pedrosa A, Sandal N, Stougaard J, Schweizer D, Bachmair A (2002) Chromosomal map of the model legume Lotus japonicus. Genetics 161:1661–1672PubMedGoogle 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 106:205–212PubMedGoogle Scholar
  30. Pich U, Fuchs J, Schubert I (1996) How do Alliaceae stabilize their chromosome ends in the absence of TTTAGGG sequences? Chromosome Res 4:207–213CrossRefPubMedGoogle 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 12:153–161CrossRefPubMedGoogle 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 101:14818–14823CrossRefPubMedGoogle Scholar
  33. Schubert I, Wobus U (1985) In situ hybridization confirms jumping nucleolus organizing regions in Allium. Chromosoma 92:143–148CrossRefGoogle Scholar
  34. Sharma S, Raina SN (2005) Organization and evolution of highly repeated satellite DNA sequences in plant chromosomes. Cytogenet Genome Res 109:15–26CrossRefPubMedGoogle 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 263:586–591CrossRefPubMedGoogle Scholar
  36. Singh SP, Gepts P, Debouck DG (1991) Races of common bean (Phaseolus vulgaris, Fabaceae). Econ Bot 45:379–396Google 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 89:629–635CrossRefGoogle Scholar
  38. Tohme J, González DO, Beebe S, Duque MC (1996) AFLP analysis of gene pools of a wild bean core collection. Crop Sci 36:1375–1384CrossRefGoogle 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/mci168Google Scholar
  40. Vallejos CE, Sakiyama NS, Chase CD (1992) A molecular marker-based linkage map of Phaseolus vulgaris L. Genetics 131:733–740PubMedGoogle 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 11:1007–1016CrossRefPubMedGoogle Scholar
  42. Wendel JF, Schnabel A, Seelanan T (1995) Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proc Natl Acad Sci USA 92:280–284PubMedCrossRefGoogle 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 86:735–740PubMedCrossRefGoogle 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 107:365–369CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Andrea Pedrosa-Harand
    • 1
  • Cícero C. Souza de Almeida
    • 2
  • Magdalena Mosiolek
    • 3
    • 4
  • Matthew W. Blair
    • 5
  • Dieter Schweizer
    • 1
    • 4
  • Marcelo Guerra
    • 2
  1. 1.Department of Chromosome BiologyUniversity of ViennaViennaAustria
  2. 2.Laboratory of Plant Cytogenetics, Department of BotanyFederal University of PernambucoRecifeBrazil
  3. 3.Department of Plant Cytology and Embryology, Institute of BotanyJagiellonian UniversityKrakowPoland
  4. 4.GMI—Gregor Mendel Institute of Molecular Plant BiologyViennaAustria
  5. 5.CIAT—International Center for Tropical AgricultureCaliColombia

Personalised recommendations