High nrDNA ITS polymorphism in the ancient extant seed plant Cycas: Incomplete concerted evolution and the origin of pseudogenes

Molecular Phylogenetics and Evolution

Volumn 55, Issue 1, 2010, Pages 168-177

  Xiao, Long Qian ^a,b   Möller, Michael ^c   Zhu, Hua ^a  

^a CHINESE ACADEMY OF SCIENCES   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c ROYAL BOTANIC GARDEN EDINBURGH   (United Kingdom)

Author keywords

Concerted evolution; Cycas; Internal transcribed spacer (ITS); Phylogeny; Pseudogenes

Indexed keywords

PLANT DNA; RIBOSOMAL SPACER DNA; RNA 5.8S;

ARTICLE; BIOLOGICAL MODEL; CYCAS; DNA BASE COMPOSITION; DNA SEQUENCE; GENETIC POLYMORPHISM; GENETICS; MOLECULAR EVOLUTION; PHYLOGENY; PLANT GENE; PSEUDOGENE;

BASE COMPOSITION; CYCAS; DNA, PLANT; DNA, RIBOSOMAL SPACER; EVOLUTION, MOLECULAR; GENES, PLANT; MODELS, GENETIC; PHYLOGENY; POLYMORPHISM, GENETIC; PSEUDOGENES; RNA, RIBOSOMAL, 5.8S; SEQUENCE ANALYSIS, DNA;

CYCAS; CYCAS CIRCINALIS; CYCAS RUMPHII; SPERMATOPHYTA;

EID: 76849085808     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2009.11.020     Document Type: Article

References (72)

1. Alhiyafi J., Sebesan C., Shiyong L., Harriott M., Jurczyszyn D., Ritchie R.P., Gonzales F.S., and Ram J.L. Computational methods for analysis of cryptic recombination in the performance of genomic recombination detection software. AINA Workshops 1 (2007) 707-712
2. Álvarez I., and Wendel J.F. Ribosomal ITS sequences and plant phylogenetic inference. Mol. Phylogenet. Evol. 29 (2003) 417-434
3. Anderson F.E., and Swofford D.L. Should we be worried about long-branch attraction in real data sets? Investigations using metazoan 18S rDNA. Mol. Phylogenet. Evol. 33 (2004) 440-451
4. Bailey J.A., Liu G., and Eichler E.E. An Alu transposition model for the origin and expansion of human segmental duplications. Am. J. Hum. Genet. 73 (2003) 823-834
5. Benson G. Tandem repeats finder: a program to analyze DNA sequence. Nucleic Acids Res. 27 (1999) 573-580
6. Bradley R.D., and Hillis D.M. Recombinant DNA sequences generated by PCR amplification. Mol. Biol. Evol. 14 (1997) 592-593
7. Buckler E.S., and Holtsford T.P. Zea ribosomal repeat evolution and mutation patterns. Mol. Biol. Evol. 13 (1996) 623-632
8. Buckler E.S., and Holtsford T.P. Zea systematics: ribosomal ITS evidence. Mol. Biol. Evol. 13 (1996) 612-622
9. Buckler E.S., Ippolito A., and Holtsford T.P. The evolution of ribosomal DNA: divergent paralogues and phylogenetic implications. Genetics 145 (1997) 821-832
10. Buckley, R., 1999. A brief review of the fossil cycads. Available from: .
11. Campbell C.S., Wright W.A., Cox M., Vining T.F., Major C.S., and Arsenault M.P. Nuclear ribosomal DNA internal transcribed spacer 1 (ITS1) in Picea (Pinaceae), sequence divergence and structure. Mol. Phylogenet. Evol. 35 (2005) 165-185
12. Chaw S.M., Parkinson C.L., Cheng Y., Vincent T.M., and Palmer J.D. Seed plant phylogeny inferred from all three plant genomes: Monophyly of extant gymnosperms and origin of Gnetales from conifers. Proc. Natl. Acad. Sci. USA 97 (2000) 4086-4091
13. Chaw S.M., Walters T.W., Chang C.C., Hu S.H., and Chen S.H. A phylogeny of cycads (Cycadales) inferred from chloroplast matK gene, trnK intron, and nuclear rDNA ITS region. Mol. Phylogenet. Evol. 37 (2005) 214-234
14. Childs G., Maxson R., Cohn R.H., and Kedes L. Orphans, dispersed genetic elements derived from tandem repetitive genes of eucaryotes. Cell 23 (1981) 651-663
15. Datson P.M., and Murray B.G. Ribosomal DNA locus evolution in Nemesia: transposition rather than structural rearrangement as the key mechanism?. Chromosome Res. 14 (2006) 845-857
16. Denduangboripant J., and Cronk Q.C.B. High intraindividual variation in internal transcribed spacer sequences in Aeschynanthus (Gesneriaceae): implication for phylogenetics. Proc. R. Soc. Lond. 267 (2000) 1407-1415
17. Doyle J. DNA protocols for plants - CTAB total DNA isolation. In: Hewitt G.M., and Johnston A. (Eds). Molecular Techniques in Taxonomy (1991), Berlin, Springer 283-293
18. Grimm G.W., and Denk T. ITS evolution in Platanus (Platanaceae): homoeologues, pseudogenes and ancient hybridization. Ann. Bot. 101 (2007) 403-419
19. Gernandt D.S., Liston A., and Pinero D. Variation in the nrDNA ITS of Pinus subsection Cembroides: implications for molecular systematic studies of pine species complexes. Mol. Phylogenet. Evol. 21 (2001) 449-467
20. Hall T.A. BioEdit, a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids. Symp. Ser. 41 (1999) 95-98
21. Harpke D., and Peterson A. Non-concerted ITS evolution in Mammillaria (Cactaceae). Mol. Phylogenet. Evol. 41 (2006) 579-593
22. Hershkovitz M.A., Zimmer E.A., and Hahn W.J. Ribosomal DNA sequences and angiosperm systematics. In: Hollingsworth P.M., Bateman R.M., and Gornall R.J. (Eds). Molecular Systematics and Plant Evolution (1999), Taylor and Francis, London 268-326
23. Hill K.D. The Cycas rumphii complex (Cycadaceae) in New Guinea and the Western Pacific. Aust. Syst. Bot. 7 (1994) 543-567
24. Hill K.D. Cycas - an evolutionary perspective. In: Chen C.J. (Ed). Biology and Conservation of Cycads - Proceedings of the Fourth International Conference on Cycad Biology (1999), International Academic Publishers, Beijing
25. Hill K.D. Character evolution, species recognition and classification concepts in the Cycadaceae. In: Walters T., and Osborne R. (Eds). Cycad Classification Concepts and Recommendations (2004), CABI Publishing, Wallingford 23-44
26. Hizume M., Ishida F., and Kondo K. Differential staining and in situ hybridization of nucleolar organizers and centromeres in Cycas revoluta chromosomes. Jpn. J. Genet. 67 (1992) 381-387
27. Jobes D.V., and Thien L.B. A conserved motif in the 5.8S ribosomal RNA (rRNA) gene is a useful diagnostic marker for plant internal transcribed spacer (ITS) sequences. Plant Mol. Biol. Rep. 15 (1997) 326-334
28. Johnson L.A.S., and Wilson K.L. General traits of the Cycadales. In: Kramer K.U., and Green P.S. (Eds). The Families and Genera of Vascular Plants (1990), Springer-Verlag, Berlin 363-368
29. Kan X.Z., Wang S.S., Ding X., and Wang X.Q. Structural evolution of nrDNA ITS in Pinaceae and its phylogenetic implications. Mol. Phylogenet. Evol. 44 (2007) 765-777
30. Karvonen P., and Savolainen O. Variation and inheritance of ribosomal DNA in Pinus sylvestris L. (Scots Pine). Heredity 71 (1993) 614-622
31. Kimura M. A simple model for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16 (1980) 111-120
32. Kita Y., and Ito M. Nuclear ribosomal ITS sequences and phylogeny in East Asian Aconitum subgenus Aconitum (Ranunculaceae), with special reference to extensive polymorphism in individual plants. Plant Syst. Evol. 225 (2000) 1-13
33. Komarova N.Y., Grabe T., Huigen D.J., Hemleben V., and Volkov R.A. Organization, differential expression and methylation of rDNA in artificial Solanum allopolyploids. Plant Mol. Biol. 56 (2004) 439-463
34. Kumar S., Tamura K., and Nei M. MEGA, Molecular Evolutionary Genetics Analysis software for microcomputers. Bioinformatics 10 (1994) 189-191
35. Liston A., Robinson W.A., Oliphant J.M., and Alvarez-Buylla E.R. Length variation in the nuclear ribosomal DNA internal transcribed spacer region of non-flowering seed plants. Syst. Bot. 21 (1996) 109-120
36. Long E.O., and Dawid I.B. Repeated genes in eukaryotes. Annu. Rev. Biochem. 49 (1980) 727-764
37. Lubaretz O., Fuchs J., Ahne R., and Meister A. Karyotyping of three Pinaceae species via fluorescent in situ hybridization and computer-aided chromosome analysis. Theor. Appl. Genet. 92 (1996) 411-416
38. Mai J.C., and Coleman A.W. The internal transcribed spacer 2 exhibits a common secondary structure in green algae and flowering plants. J. Mol. Evol. 44 (1997) 258-271
39. Mayol M., and Rosselló J.A. Why nuclear ribosomal DNA spacers (ITS) tell different stories in Quercus. Mol. Phylogenet. Evol. 19 (2001) 167-176
40. McDade L.A. Hybrids and phylogenetic systematics II. The impact of hybrids on cladistic analysis. Evolution 46 (1992) 1329-1346
41. Möller M., Kokubugata G., and Jong K. Aspects of genome evolution in Gesneriaceae: patterns of 45S-nrDNA site evolution based on evidence from fluorescent in situ hybridization (FISH). Int. J. Plant Sci. 169 5 (2008) 667-676
42. Muir G., Fleming C.C., and Schlötterer C. Three divergent rDNA clusters predate the species divergence in Quercus petraea (Matt.) Liebl. and Quercus robur L. Mol. Biol. Evol. 18 (2001) 112-119
43. Nagylaki T. The evolution of multigene families under intrachromosomal gene conversion. Genetics 106 (1984) 529-548
44. Nei M. Molecular Evolutionary Genetics (1987), Columbia University Press, New York
45. Nickrent D.L., Schuette K.P., and Starr E.M. A molecular phylogeny of Arceuthobium (Viscaceae) based on nuclear ribosomal DNA internal transcribed spacer sequences. Am. J. Bot. 81 (1994) 1149-1160
46. Ochieng J.W., Henry R.J., Baverstock P.R., Steane D.A., and Shepherd M. Nuclear ribosomal pseudogenes resolve a corroborated monophyly of the eucalypt genus Corymbia despite misleading hypotheses at functional ITS paralogs. Mol. Phylogenet. Evol. 44 (2007) 752-764
47. Padidam M., Sawyer S., and Fauquet C.M. Possible emergence of new geminiviruses by frequent recombination. Virology 265 (1999) 218-225
48. Pant D.D. A study in contrasts, the present and past distribution and form of certain cycads. In: Chen C.J. (Ed). Biology and conservation of cycads - Proceedings of the Fourth International Conference on Cycad Biology (1999), International Academic Publishers, Beijing
49. Quijada A., Liston A., Delgado P., Vázquez-Lobo A., and Alvarez-Buylla E.R. Variation in the nuclear ribosomal DNA internal transcribed spacer (ITS) region of Pinus rzedowskii revealed by PCR-RFLP. Theor. Appl. Genet. 96 (1998) 539-544
50. Rogers S.O., and Bendich A.J. Ribosomal RNA genes in plants, variability in copy number and in the intergenic spacer. Plant Mol. Biol. 9 (1987) 509-520
51. Rose P.P., and Korber B.T. Detecting hypermutations in viral sequences with an emphasis on G A hypermutation. Bioinformatics 16 (2000) 400-401
52. Rozas J., and Rozas R. DnaSP version 3, an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15 (1999) 174-175
53. Sanderson M.J., and Doyle J.J. Reconstruction of organismal and gene phylogenies from data on multigene families: concerted evolution, homoplasy, and confidence. Syst. Biol. 41 (1992) 4-17
54. Sax K., and Beale J.M. Chromosomes of the Cycadales. J. Arnold Arbor. 15 (1934) 255-258
55. Smith G.P. Evolution of repeated DNA sequences by unequal crossover. Science 191 (1976) 528-535
56. Sone T., Fujisawa M., Takenaka M., Nakagawa S., Yamaoka S., Sakaida M., Nishiyama R., Yamato K.T., Ohmido N., Fukui K., Fukuzawa H., and Ohyama K. Bryophyte 5S rDNA was inserted into 45S rDNA repeat units after the divergence from higher land plants. Plant Mol. Biol. 41 (1999) 679-685
57. Stevenson D.W. Morphology and systematics of the Cycadales. Mem. NY Bot. Gard. 57 (1990) 8-55
58. Suh Y., Thien L.B., and Zimmer E.A. Nucleotide sequences of the internal transcribed spacers and 5.8S rRNA gene in Canella winterana (Magnoliales; Canellaceae). Nucleic Acids Res. 20 (1992) 6101-6102
59. Swofford, D.L., 2002. PAUP*: Phylogenetic Analysis Using Parsimony (* and other methods), Version 4.0. Sinauer Associates, Sunderland, MA.
60. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., and Higgins D.G. The ClustalX windows interface, flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24 (1997) 4876-4882
61. Treutlein J., and Wink M. Molecular phylogeny of cycads inferred from rbcL sequences. Naturwissenschaften 89 (2004) 221-225
62. Wang, D.Y., 2000. Studies on Morphology, Anatomy, Taxonomy and Evolution of Cycadaceae. Ph.D. Dissertation. Nanjing, Nanjing Forestry University.
63. Wei X.X., and Wang X.Q. Recolonization and radiation in Larix (Pinaceae), evidence from nuclear ribosomal DNA paralogs. Mol. Ecol. 13 (2004) 3115-3123
64. Wei X.X., Wang X.Q., and Hong D.Y. Marked intragenomic heterogeneity and geographical differentiation of nrDNA ITS in Larix potaninii (Pinaceae). J. Mol. Evol. 57 (2003) 623-635
65. Wendel J.F., Schnabel A., and Seelanan T. Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proc. Natl. Acad. Sci. USA 92 (1995) 280-284
66. Wolf M., Achtziger M., Schultz J., Dandekar T., and Müller T. Homology modeling revealed more than 20,000 rRNA internal transcribed spacer 2 (ITS2) secondary structures. RNA 11 (2005) 1616-1623
67. Won H., and Renner S.S. The internal transcribed spacer of nuclear ribosomal DNA in the gymnosperm Gnetum. Mol. Phylogenet. Evol. 36 (2005) 581-597
68. Xiang Q.P., Xiang Q.Y., Liston A., Fu L.K., and Fu D.Z. Length variation of the nuclear ribosomal DNA internal transcribed spacer in the genus Abies, with reference to its systematic utility in Pinaceae. Acta Bot. Sin. 42 (2000) 946-951
69. Yang S.L., and Meerow A.W. The Cycas pectinata (Cycadaceae) complex structure and gene flow. Int. J. Plant Sci. 157 (1996) 468-483
70. Yokota Y., Kawata T., Iida Y., Kato A., and Tanifuji S. Nucleotide sequences of the 58S rRNA gene and internal transcribed spacer regions in carrot and broad bean ribosomal DNA. J. Mol. Evol. 29 (1989) 294-301
71. Zheng X.Y., Cai D.Y., Yao L.H., and Teng Y.W. Non-concerted ITS evolution, early origin and phylogenetic utility of ITS pseudogenes in Pyrus. Mol. Phylogenet. Evol. 48 (2008) 892-903
72. Zuker M. MFold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31 (2003) 3406-3415