Variation and inheritance of nuclear ribosomal DNA clusters in Streptocarpus (Gesneriaceae) and their biological and phylogenetic implications

International Journal of Plant Sciences

Volumn 168, Issue 4, 2007, Pages 455-467

  Denduangboripant, Jessada ^a   Cronk, Quentin C B ^b,d   Kokubugata, Goro ^c   Möller, Michael ^d  

^a CHULALONGKORN UNIVERSITY   (Thailand)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c DEPARTMENT OF BOTANY   (Japan)

^d ROYAL BOTANIC GARDEN EDINBURGH   (United Kingdom)

Author keywords

Fluorescent in situ hybridization (FISH); Hybrids; Inheritance; Internal transcribed spacers (ITS); Nuclear ribosomal DNA (nrDNA); Streptocarpus

Indexed keywords

ARRAY; CHROMOSOME; DNA; HERB; HERITABILITY; HYBRIDIZATION; PHYLOGENETICS; POLYMERASE CHAIN REACTION;

GESNERIACEAE; STREPTOCARPUS; STREPTOCARPUS DUNNII; STREPTOCARPUS REXII;

EID: 34247606354     PISSN: 10585893     EISSN: None     Source Type: Journal    
DOI: 10.1086/512103     Document Type: Article

References (71)

1. Adams SP, IJ Leitch, MD Bennett, CW Chase, AR Leitch 2000 Ribosomal DNA evolution and phylogeny in Aloe (Asphodelaceae). Am J Bot 87:1578-1583.
2. Albini SM 1994 A karyotype of the Arabidopsis thaliana genome derived from synaptonemal complex analysis at prophase I of meiosis. Plant J 5:665-672.
3. Alvarez I, JF Wendel 2003 Ribosomal ITS sequences and plant phylogenetic inference. Mol Phylogenet Evol 29:417-434.
4. Appels R, RL Honeycutt 1986 rDNA evolution over a billion years. Pages 81-135 in SK Dutta, ed. DNA systematics. CRC, Boca Raton, FL.
5. Bailey CD, TG Carr, SA Harris, CE Hughes 2003 Characterization of angiosperm nrDNA polymorphism, paralogy, and pseudogenes. Mol Phylogenet Evol 29:417-434.
6. Borgen L, IJ Leitch, A Santos-Guerra 2003 Genome organisation in diploid hybrid species of Argyranthemum (Asteraceae) in the Canary Islands. Bot J Lin Soc 141:491-501.
7. Butterfass T 1979 Patterns of chloroplast reproduction: a developmental approach to protoplasmic plant anatomy. Springer, New York. 205 pp.
8. Chase MW, S Knapp, AV Cox, JJ Clarkson, Y Butsko, J Joseph, V Savolainen, AS Parokonny 2003 Molecular systematics, GISH and the origin of hybrid taxa in Nicotiana (Solanaceae). Ann Bot 92:107-127.
9. Copenhaver GP, CS Pikaard 1996 Two-dimensional RFLP analyses reveal megabase-sized clusters of rRNA gene variants in Arabidopsis thaliana, suggesting local spreading of variants as the mode for gene homogenization during concerted evolution. Plant J 9:273-282.
10. Coyer JA, AF Peters, G Hoarau, WT Stam, JL Olsen 2002 Inheritance patterns of ITS1, chloroplasts and mitochondria in artificial hybrids of the seaweed Fucus serratus and F. evanescens (Phaeophyceae). Eur J Phycol 37:173-178.
11. Denduangboripant J, QCB Cronk 2000 High intra-individual variation in ITS sequences in Aeschynanthus (Gesneriaceae): implications for phylogenetics. Proc R Soc B 267:1407-1415.
12. _ 2001 Evolution and alignment of the hypervariable arm 1 of Aeschynanthus (Gesneriaceae) ITS2 nuclear ribosomal DNA. Mol Phylogenet Evol 20:163-172.
13. Denduangboripant J, M Mendum, QCB Cronk 2001 Evolution in Aeschynanthus (Gesneriaceae) inferred from ITS sequences. Plant Syst Evol 228:181-197.
14. Dover GA 1994 Concerted evolution, molecular drive and natural selection. Curr Biol 4:1165-1166.
15. Dover GA, E Coen 1981 Springcleaning ribosomal DNA: a model for multigene evolution? Nature 290:731-732.
16. Doyle JJ, JL Doyle 1987 A rapid DNA isolation procedure for small quantities of fresh tissue. Phytochem Bull 19:11-15.
17. Drouin G, M Moniz de Sá 1995 The concerted evolution of 5S ribosomal genes linked to the repeat units of other multigene families. Mol Biol Evol 12:481-493.
18. Elder JF Jr, BJ Turner 1995 Concerted evolution of repetitive DNA sequences in eukaryotes. Q Rev Biol 70:297-320.
19. Flavell RB, M O'Dell, P Sharp, E Nevo, A Beiles 1986 Variation in the intergenic spacer of ribosomal DNA of wild wheat, Triticum dicoccoides, in Israel. Mol Biol Evol 3:547-558.
20. Franzke A, K Mummenhoff 1999 Recent hybrid speciation in Cardamine (Brassicaceae): conversion of nuclear ribosomal ITS sequences in statu nascendi. Theor Appl Genet 98:831-834.
21. Hayasaki M, T Morikawa, JM Leggett 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.
22. Hilliard OM, BL Burtt 1971 Streptocarpus: an African plant study. University of Natal Press, Pietermaritzburg.
23. Hillis DM, SK Davis 1988 Ribosomal DNA: intraspecific polymorphism, concerted evolution, and phylogeny reconstruction. Syst Zool 37:63-66.
24. Hillis DM, MT Dixon 1991 Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 66:411-453.
25. Hughes M, M Möller, DU Bellstedt, TJ Edwards 2005 Refugia, dispersal and divergence in a forest archipelago: a study of Streptocarpus in eastern South Africa. Mol Ecol 14:4415-4426.
26. Jorgensen RA, RE Cuellar, WF Thompson 1987 Structure and variation in ribosomal RNA genes of pea: characterization of a cloned rDNA repeat and chromosomal rDNA variants. Plant Mol Biol 8:3-12.
27. Kim KJ, RK Jansen 1994 Comparison of phylogenetic hypotheses among different data sets in dwarf dandelions (Krigia): additional information from internal transcribed space sequences of nuclear ribosomal DNA. Plant Syst Evol 190:157-185.
28. Kokubugata G, CI Peng 2002 Taxonomic study of Conandron ramondioides from Japan and Taiwan. Gesneriaceae Workshop, Royal Botanic Garden Edinburgh, Program and Abstracts, p 29.
29. Kovarik A, JC Pires, AR Leitch, KY Lim, AM Sherwood, R Matyášek, J Rocca, DE Soltis, PS Soltis 2005 Rapid concerted evolution of nuclear ribosomal DNA in two Tragopogon allopolyploids of recent and recurrent origin. Genetics 169:931-944.
30. Lim KY, A Kovarik, R Matyášek, M Bezdek, CP Lichtenstein, AR Leitch 2000a Gene conversion of ribosomal DNA in Nicotiana tabacum is associated with undermethylated, decondensed and probably active gene units. Chromosoma 109:161-172.
31. Lim KY, R Matyášek, CP Lichtenstein, AR Leitch 2000b Molecular cytogenetic analysis and phylogenetic studies in the Nicotiana section Tomentosae. Chromosoma 109:245-258.
32. Maluszynska J, JS Heslop-Harrison 1993 Physical mapping of rDNA loci in Brassica species. Genome 36:774-781.
33. Manen JF 2004 Are both sympatric species Ilex perado and Ilex canariensis secretly hybridizing? indication from nuclear markers collected in Tenerife. BMC Evol Biol 4:46.
34. Möller M 2000 How universal are universal rDNA primers? a cautionary note for plant systematists and phylogeneticists. Edinb J Bot 57:151-156.
35. Möller M, KJ Brooks, M Hughes 2004 Plastid inheritance in Streptocarpus (Gesneriaceae) and an inferred hybrid origin for a population of S. aff. primulifolius from Igoda River, South Africa. Edinb J Bot 60:389-408.
36. Möller M, QCB Cronk 1997a Origin and relationships of Saintpaulia (Gesneriaceae) based on ribosomal DNA internal transcribed spacer (ITS) spacers. Am J Bot 84:950-965.
37. _ 19976 Phylogeny and disjunct, distribution: evolution of Saintpaulia (Gesneriaceae). Proc R Soc B 264:1827-1836.
38. _ 2001 Evolution of morphological novelty: a phylogenetic analysis of growth patterns in Streptocarpus (Gesneriaceae). Evolution 55:918-929.
39. Muir G, CC Fleming, C Schlotterer 2001 Three divergent rDNA clusters predate the species divergence in Quercus petraea (Matt.) Liebl. and Quercus robur L. Mol Biol Evol 18:112-119.
40. Mummenhoff K, A Franzke, M Koch 1997 Molecular phylogenetics of Thlaspi s. l. (Brassicaceae) based on chloroplast DNA, restriction-site variation and sequences of the internal transcribed spacers of nuclear ribosomal DNA. Can J Bot 75:469-482.
41. Murata M, JS Heslop-Harrison, F Motoyoshi 1997 Physical mapping of the 5S ribosomal RNA genes in Arabidopsis thaliana by multi-color fluorescence in situ hybridization with cosmid clones. Plant J 12:31-37.
42. Nagylaki T, TD Petes 1982 Intrachromosomal gene conversion and the maintenance of sequence homogeneity among repeated genes. Genetics 100:315-337.
43. Neves N, JS Heslop-Harrison, W Viegas 1995 rRNA gene activity and control of expression mediated by methyiation and imprinting during embryo development in wheat x rye hybrids. Theor Appl Genet 91:529-533.
44. O'Kane SL, BA Schaal, IA Al-Shehbaz 1996 The origins of Arabidopsis suecica as indicated by nuclear rDNA sequences. Syst Bot 21:559-566.
45. Osuji JO, J Crouch, G Harrison, JS Heslop-Harrison 1998 Molecular cytogenetics of Musa species, cultivars and hybrids: location of 18S-5.8S-25S and 5S rDNA and telomere-like sequences. Ann Bot 82:243-248.
46. Pires JC, KY Lim, A Kovarik, R Matyášek, A Boyd, AR Leitch, IJ Leitch, MD Bennett, PS Soltis, DE Soltis 2004 Molecular cytogenetic analysis of recently evolved Tragopogon (Asteraceae) allopolyploids reveals a karyotype that is additive of the diploid progenitors. Am J Bot 91:1022-1035.
47. Ratter J 1975 A survey of chromosome numbers in the Gesneriaceae of the Old World. Edinb J Bot 33:527-543.
48. Rauscher JT, JJ Doyle, AHD Brown 2004 Multiple origins and nrDNA internal transcribed spacer homeologue evolution in the Glycine tomentella (Leguminosae) allopolyploid complex. Genetics 166:987-998.
49. Rogers SO, AJ Bendich 1987 Ribosomal RNA genes in plants: variability in copy number and in the intergenic spacer. Plant Mol Biol 9:509-520.
50. Saghai-Maroof MA, KM Soliman, RA Jorgensen, RW Allard 1984 Ribosomal DNA spacer-length polymorphisms in barley: Mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci USA 81:8014-8018.
51. Sang T, DJ Crawford, TF Stuessy 1995 Documentation of reticulate evolution in peonies (Paeonia) using internal transcribed spacer sequences of nuclear ribosomal DNA: implications for biogeography and concerted evolution. Proc Natl Acad Sci USA 92:6813-6817.
52. Schlötterer C, D Tautz 1994 Chromosomal homogeneity of Drosophila ribosomal DNA arrays suggests intrachromosomal exchanges drive concerted evolution. Curr Biol 4:777-783.
53. Schwarzacher T, JS Heslop-Harrison 2000 Practical in situ hybridization. Bios Scientific, Oxford.
54. Shan F, G Yan, JA Plummer 2003 Cyto-evolution of Boronia genomes revealed by fluorescent in situ hybridization with rDNA probes. Genome 46:507-513.
55. Smith GP 1973 Unequal crossover and the evolution of multigene families. Cold Spring Harbor Symp Quant Biol 38:507-513.
56. Soltis DE, RK Kuzoff 1995 Discordance between nuclear and chloroplast phylogenies in the Heuchera group (Saxifragaceae). Evolution 49:727-742.
57. Soltis PS, DE Soltis 1991 Multiple origins of the allotetraploid Tragopogon mirus (Compositae): rDNA evidence. Syst Bot 1:407-413.
58. Sone T, M Fujisawa, M Takenaka, S Nakagawa, S Yamaoka, M Sakaida, R Nishiyama, et al 1999 Bryophyte 5S rDNA was inserted into 45S rDNA repeat units after the divergence from higher land plants. Plant Mol Biol 41:679-685.
59. Taberlet P, L Gielly, G Pautou, J Bouvet 1991 Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1103-1109.
60. Van Houten WHJ, N Scarlet, K Bachmann 1993 Nuclear DNA markers of the Australian tetraploid Microseris scapigera and its North American diploid relatives. Theor Appl Genet 87:498-505.
61. Vanzela AL, CF Ruas, MF Oliveira, PM Ruas 2002 Characterization of diploid, tetraploid and hexaploid Helianthus species by chromosome banding and FISH with 45S rDNA probe. Genetica 114:105-111.
62. Vosa CG 2000 A revised cytotaxonomy of the genus Tulbaghia (Alliaceae). Caryologia 53:83-112.
63. Wendel JF, A Schnabel, T Seelanan 1995a Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proc Natl Acad Sci USA 92:280-284.
64. _ 1995b An unusual ribosomal DNA sequence from Gossypium gossypiodes reveals ancient cryptic intergenomic introgression. Mol Phylogenet Evol 4:298-313.
65. White TJ, T Bruns, S Lee, J Taylor 1990 Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Pages 315-322 in MA Innis, DH Gelfand, JJ Sninsky, TJ White, eds. PCR protocols. Academic Press, London.
66. Williams SC, RW DeBry, JL Feder 1988 A commentary on the use of ribosomal DNA in systematic studies. Syst Zool 37:60-62.
67. Wolfe AD, WJ Elisens 1995 Evidence of chloroplast capture and pollen-mediated gene flow in Penstemon section Peltanthera (Scrophulariaceae). Syst Bot 20:395-412.
68. Zhang D, T Sang 1999 Physical mapping of ribosomal RNA genes in peonies (Paeonia, Paeoniaceae) by fluorescent in situ hybridization: implications for phylogeny and concerted evolution. Am J Bot 86:735-740.
69. Zoldos V, D Papes, M Cerbah, O Panaud, V Besendorfer, S Siljak-Yakovlev 1999 Molecular-cytogenetic studies of ribosomal genes and heterochromatin reveal conserved genome organization among 11 Quercus species. Theor Appl Genet 99:969-977.
70. Zurita F, R Jiménez, M Burgos, RD de la Guardíã 1998 Sequential silver staining and in situ hybridization reveal a direct association between rDNA levels and the expression of homologous nucleolar organizing regions: a hypothesis for NOR structure and function. J Cell Sci 111:1433-1439.
71. Zurita F, A Sánchez, M Burgos, R Jiménez, RD de la Guardiã 1997 Interchromosomal, intercellular and interindividual variability of NORs studied with silver staining and in situ hybridization. Heredity 78:229-234.