Evolutionary dynamics and preferential expression of homeologous 18S-5.8S-26S nuclear ribosomal genes in natural and artificial glycine allopolyploids

Molecular Biology and Evolution

Volumn 21, Issue 7, 2004, Pages 1409-1421

  Joly, Simon ^a,c   Rauscher, Jason T ^a,d   Sherman Broyles, Susan L ^a   Brown, A H D ^b   Doyle, Jeff J ^a  

^a Cornell University ^*  (United States)

^b CSIRO   (Australia)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d UNIVERSIDAD DE LOS ANDES   (Colombia)

Author keywords

Gene expression; Glycine; Internal transcribed spacers; Nucleolar dominance; Polyploidy; Ribosomal gene family

Indexed keywords

GLYCINE; INTERNAL TRANSCRIBED SPACER; RIBOSOME RNA; RNA 18S; RNA 26S; UNCLASSIFIED DRUG;

ALLOPOLYPLOIDY; ARTICLE; DIPLOIDY; EVOLUTION; GENE EXPRESSION; GENE LOCUS; GENE SEGREGATION; GENETIC TRANSCRIPTION; GENOME; GENOTYPE; HYBRIDIZATION; MULTIGENE FAMILY; NONHUMAN; NUCLEAR RIBOSOMAL GENE; NUCLEOLUS; NUCLEOTIDE REPEAT; PLANT; POLYMERASE CHAIN REACTION; STOCHASTIC MODEL; TETRAPLOIDY; TISSUE SPECIFICITY;

DNA, RIBOSOMAL; EVOLUTION, MOLECULAR; GENE EXPRESSION; GENES, PLANT; GENES, RRNA; POLYPLOIDY; RNA, RIBOSOMAL; RNA, RIBOSOMAL, 18S; RNA, RIBOSOMAL, 5.8S; SOYBEANS; VARIATION (GENETICS);

GLYCINE MAX; NEONOTONIA WIGHTII;

EID: 3042588947     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msh140     Document Type: Article

References (79)

1. Adams K. L., R. Cronn, R. Percifield, and J. F. Wendel. 2003. Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proc. Natl. Acad. Sci. USA 100:4649-4654.
2. Baldwin, B. G., M. J. Sanderson, J. M. Porter, M. F. Wojciechowski, C. S. Campbell, and M. J. Donoghue. 1995. The ITS region of nuclear ribosomal DNA: a valuable source of evidence on angiosperm phylogeny. Ann. MO Bot. Gard. 82:247-277.
3. Brown, A. H. D., J. J. Doyle, J. P. Grace, and J. L. Doyle. 2002. Molecular phylogenetic relationships within and among diploid races of Glycine tomentella (Leguminosae). Aust. Syst. Bot. 15:37-47.
4. Caudy, A. A., and C. S. Pikaard. 2002. Xenopus ribosomal RNA gene intergenic spacer elements conferring transcriptional enhancement and nucleolar dominance-like competition in oocytes. J. Biol. Chem. 277:31577-31584.
5. Chen, Z. J., L. Comai, and C. S. Pikaard. 1998. Gene dosage and stochastic effects determine the severity and direction of uniparental ribosomal RNA gene silencing (nucleolar dominance) in Arabidopsis allopolyploids. Proc. Natl. Acad. Sci. USA 95:14891-14896.
6. Chen, Z. J., and C. S. Pikaard. 1997a. Transcriptional analysis of nucleolar dominance in polyploid plants: biased expression/silencing of progenitor rRNA genes is developmentally regulated in Brassica. Proc. Natl. Acad. Sci. USA 94:3442-3447.
7. -. 1997b. Epigenetic silencing of RNA polymerase I transcription: a role for DNA methylation and histone modification in nucleolar dominance. Genes Dev. 11:2124-2136.
8. Comai, L. 2000. Genetic and epigenetic interactions in allopolyploid plants. Plant Mol. Biol. 43:387-399.
9. Comai, L., A. P. Tyagi, K. Winter, R. Holmes-Davis, S. H. Reynolds, Y. Stevens, and B. Byers. 2000. Phenotypic instability and rapid gene silencing in newly formed Arabidopsis allotetraploids. Plant Cell 12:1551-1567.
10. Crosby, M. R. 1980. Polyploidy in bryophytes with special emphasis on mosses. Pp. 193-198 in W. H. Lewis, ed. Polyploidy: biological relevance. Plenum Press, New York.
11. Doyle, J. J., and J. L. Doyle. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19:11-15.
12. Doyle, J. J., J. L. Doyle, and A. H. D. Brown. 1999. Origins, colonization, and lineage recombination in a widespread perennial soybean polyploid complex. Proc. Natl. Acad. Sci. USA 96:10741-10745.
13. Doyle, J. J., J. L. Doyle, A. H. D. Brown, and R. G. Palmer. 2002. Genomes, multiple origins, and lineage recombination in the Glycine tomentella (Leguminosae) polyploid complex: histone H3-D gene sequences. Evolution 56:1388-1402.
14. Doyle, J. J., J. L. Doyle, A. H. D. Brown, and J. P. Grace. 1990a. Multiple origins of polyploids in the Glycine tabacina complex inferred from chloropast DNA polymorphism. Proc. Natl. Acad. Sci. USA 87:714-717.
15. Doyle, J. J., J. L. Doyle, J. P. Grace, and A. H. D. Brown. 1990b. Reproductively isolated polyploid races of Glycine tabacina (Leguminosae) had different chloroplast genome donors. Syst. Bot. 15:173-181.
16. Doyle, J. J., J. L. Doyle, J. T. Rauscher, and A. H. D. Brown. 2004. Evolution of the perennial soybean polyploid complex (Glycine subgenus Glycine): a study of contrasts. Biol. J. Linn. Soc.(in press).
17. Doyle, M. J., J. E. Grant, and A. H. D. Brown. 1986. Reproductive isolation between isozyme groups of Glycine tomentella (Leguminosae) and spontaneous doubling in their hybrids. Austral. J. Bot. 34:523-535.
18. Durica, D. S., and H. M. Krider. 1977. Studies on the ribosomal RNA cistrons in interspecific Drosophila hybrids. I. Nucleolar dominance. Dev. Biol. 59:62-74.
19. -. 1978. Studies on the ribosomal RNA cistron in interspecific Drosophila hybrids. II. Heterochromatic regions mediating nucleolar dominance. Genetics 89:37-64.
20. Ehrendorfer, F. 1980. Polyploidy and distribution. Pp. 45-60 in W. H. Lewis, ed. Polyploidy: biological relevance. Plenum Press, New York.
21. Favarger, C. 1967. Cytologie et distribution des plantes. Biol. Rev. 42:163-206.
22. Ferguson, D., and T. Sang. 2001. Speciation through homoploid hybridization between allotetraploids in peonies (Paeonia). Proc. Natl. Acad. Sci. USA 98:3915-3919.
23. Flavell, R. B. 1986. The structure and control of expression of ribosomal RNA genes. Oxf. Surv. Plant Mol. Cell Biol. 3:252-274.
24. Flavell, R. B., and M. O'Dell. 1979. The genetic comtrol of nucleolus in wheat. Chromosoma 71:135-152.
25. Frieman, M., Z. J. Chen, J. Saez-Vasquez, A. Shen, and C. S. Pikaard. 1999. RNA polymerase I transcription in a Brassica interspecific hybrid and its progenitors: tests of transcription factor involvement in nucleolar dominance. Genetics 152:451-460.
26. Galitski, T., A. J. Saldanha, C. A. Styles, E. S. Lander, and G. R. Fink. 1999. Ploidy regulation of gene expression. Science 285:251-254.
27. Grant, J. E., J. P. Grace, A. H. D. Brown, and E. Putievsky. 1984. Interspecies hybridization in Glycine Willd. Subgenus Gylcine (Leguminosau). Aust. J. Bot. 32:655-663.
28. Grant, V. 1981. Plant speciation. 2nd edition. Columbia University Press, New York.
29. Hamby, R. K., and E. A. Zimmer. 1992. Ribosomal RNA as a phylogenetic tool in plant systematics. Pp. 50-91 in D. E. Soltis, P. S. Soltis, and J. J. Doyle, eds. Molecular systematics of plants. Chapman and Hall, New York.
30. Hasterok, R., and J. Maluszynska. 2000. Nucleolar dominance does not occur in root tip cells of allotetraploid Brassica species. Genome 43:574-579.
31. Honjo, T., and R. H. Reeder. 1973. Preferential transcription of Xenopus laevis ribosomal RNA in interspecies hybrids between Xenopus laevis and Xenopus mulleri. J. Mol. Biol. 80:217-228.
32. Houchins, K., M. O'Dell, R. B. Flavell, and J. P. Gustafson. 1997. Cytosine methylation and nucleolar dominance in cereals hybrids. Mol. Gen. Genet. 255:294-301.
33. Hymowitz, T., R. J. Singh, and K. P. Kollipara. 1998. The genomes of the Glycine. Pp. 289-317 in J. Janick, ed. Plant breeding reviews. John Wiley, New York.
34. Keep, E. 1962. Satellite and nucleolar number in hybrids between Ribes nigrum and R. grossularia and in their backcrosses. Can. J. Genet. Cytol. 4:206-218.
35. Krishnan, P., V. T. Sapra, K. M. Soliman, and A. Zipf. 2001. FISH mapping of the 5S and 18S-28S rDNA loci in different species of Glycine. J. Hered. 92:295-300.
36. Levin, D. A. 1983. Polyploidy and novelty in flowering plants. Am. Nat. 122:1-25.
37. -. 2002. The role of chromosomal change in plant evolution. Oxford University Press, Oxford, UK.
38. -. 2003. The cytoplasmic factor in plant speciation. Syst. Bot. 28:5-11.
39. Lewis, M. S., and C. S. Pikaard. 2001. Restricted chromosomal silencing in nucleolar dominance. Proc. Natl. Acad. Sci. USA 98:14536-14540.
40. Lewis, W. H. 1980. Polyploidy in species populations. Pp. 103-144 in W. H. Lewis, ed. Polyploidy: biological relevance. Plenum Press, New York.
41. Liu, B., J. M. Vega, and M. Feldman. 1998. Rapid genomic changes in newly synthesized amphiploids of Triticum and Aegilops. II. Changes in low-copy coding DNA sequences. Genome 41:535-542.
42. Liu, B., J. M. Vega, G. Segal, S. Abbo, M. Rodova, and M. Feldman. 1998. Rapid genomic changes in newly synthesized amphiploids of Triticum and Aegilops. I. Changes in low-copy noncoding DNA sequences. Genome 41:272-277.
43. Neves, N., M. Silva, J. S. Heslop-Harrison, and W. Viegas. 1997. Nucleolar dominance in triticales: control by unlinked genes. Chromosome Res. 5:125-131.
44. Nichols, H. W. 1980. Polyploidy in algae. Pp. 151-161 in W. H. Lewis, ed. Polyploidy: biological relevance. Plenum Press, New York.
45. Osborn, T. C., J. C. Pires, J. A. Birchler et al. (11 co-authors). 2003. Understanding mechanisms of novel gene expression in polyploids. Trends Genet. 19:141-147.
46. Otto, S. P., and J. Whitton. 2000. Polyploid incidence and evolution. Annu. Rev. Genet. 34:401-437.
47. Ozkan, H., A. A. Levy, and M. Feldman. 2001. Allopolyploidy-induced rapid genome evolution in the wheat (Aegilops-triticum) group. Plant Cell 13:1735-1747.
48. Petit, C., and J. D. Thompson. 1999. Species diversity and ecological range in relation to ploidy level in the flora of the Pyrenees. Evol. Ecol. 13:45-66.
49. Pikaard, C. S. 2000. Nucleolar dominance: uniparental gene silencing on a multi-megabase scale in genetic hybrids. Plant Mol. Biol. 43:163-177.
50. -. 2001. Genomic change and gene silencing in polyploids. Trends Genet. 17:675-677.
51. Pikaard, C. S., and Z. J. Chen. 1998. Nucleolar dominance. Pp. 277-294 in M. R. Paule, ed. Transcription of ribosomal RNA genes by eukaryotic RNA polymerase I. Springer-Verlag, Berlin.
52. Pikaard, C. S., and R. J. Lawrence. 2002. Uniting the path to gene silencing. Nat. Genet. 32:1-2.
53. Pontes, O., R. J. Lawrence, N. Neves, M. Silva, J.-H. Lee, Z. J. Chen, W. Viegas, and C. S. Pikaard. 2003. Natural variation in nucleolar dominance reveals the relationship between nucleolus organizer chromatin topology and rRNA gene transcription in Arabidopsis. Proc. Natl. Acad. Sci. USA 100:11418-11423.
54. Ramsey, J., and D. W. Schemske. 2002. Neopolyploidy in flowering plants. Annu. Rev. Ecol. Syst. 33:589-639.
55. Rauscher, J. T., J. J. Doyle, and A. H. D. Brown. 2002. Internal transcribed spacer repeat-specific primers and the analysis of hybridization in the Glycine tomentella (Leguminosae) polyploid complex. Mol. Ecol. 11:2691-2702.
56. -. 2004. Multiple origins and nrDNA ITS homeoelogue evolution in the Glycine tomentella (Leguminosae) allopolyploid complex. Genetics 166.
57. Reeder, R. H. 1985. Mechanisms of nucleolar dominance in animals and plants. J. Cell Biol. 101:2013-2016.
58. Riddle, N. C., and J. A. Birchler. 2003. Effects of reunited diverged regulatory hierarchies in allopolyploids and species hybrids. Trends Ecol. Evol. 19:597-600.
59. Rieseberg, L. H. 1997. Hybrid origins of plant species. Annu. Rev. Ecol. Syst. 28:359-389.
60. Schranz, M. E., and T. C. Osborn. 2000. Novel flowering time variation in the resynthesized polyploid Brassica napus. J. Hered. 91:242-246.
61. Schubert, I., and G. Künzel. 1990. Position-dependent NOR activity in barley. Chromosoma 99:352-359.
62. Shaked, H., K. Kashkush, H. Ozkan, M. Feldman, and A. A. Levy. 2001. Sequence elimination and cytosine methylation are rapid and reproducible responses of the genome to wide hybridization and allopolyploidy in wheat. Plant Cell 13:1749-1759.
63. Simillion, C., K. Vandepoele, M. C. E. Van Montagu, M. Zabeau, and Y. Van de Peer. 2003. The hidden duplication past of Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 99:13627-13632.
64. Singh, R. J., H. H. Kim, and T. Hymowitz. 2001. Distribution of rDNA loci in the genus Glycine. Theor. Appl. Genet. 103:212-218.
65. Soltis, D. E., and P. S. Soltis. 1999. Polyploidy: recurrent formation and genome evolution. Trends Ecol. Evol. 14:348-352.
66. Soltis, P. S., and D. E. Soltis. 2000. The role of genetic and genomic attributes in the success of polyploids. Proc. Natl. Acad. Sci. USA 97:7051-7057.
67. Song, K., P. Lu, K. Tang, and T. C. Osborn. 1995. Rapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolution. Proc. Natl. Acad. Sci. USA 92:7719-7723.
68. Stebbins, G. L. 1950. Variation and evolution in plants. Columbia University Press, New York.
69. Sun, Y., D. Z. Skinner, G. H. Liang, and S. H. Hulbert. 1994. Phylogenetic analysis of Sorghum and related taxa using internal transcribed spacers of nuclear ribosomal DNA. Theor. Appl. Genet. 89:26-32.
70. Tal, M. 1980. Physiology of polyploids. Pp. 61-75 in W. H. Lewis, ed. Polyploidy: biological relevance. Plenum Press, New York.
71. Thompson, J. N., B. M. Cunningham, K. A. Segraves, D. M. Althoff, and D. Wagner. 1997. Plant polyploidy and insect/plant interactions. Am. Nat. 150:730-743.
72. Vasquez, M. L. 2001. Molecular and morphological studies on Mexican red oaks (Quercus sect. Lobatae). Ph.D. Thesis, Cornell University, Ithaca, NY.
73. Wagner, A., N. Blackstone, P. Cartwright, M. Dick, B. Misof, P. Snow, G. P. Wagner, J. Bartels, M. Murtha, and J. Pendleton. 1994. Surveys of gene families using polymerase chain reaction: PCR selection and PCR drift. Syst. Biol. 43:250-261.
74. Wagner, W. H., Jr., and F. S. Wagner. 1980. Polyploidy in pteridophytes. Pp. 199-214 in W. H. Lewis, ed. Polyploidy: biological relevance. Plenum Press, New York.
75. Wallace, H., and W. H. R. Langridge. 1971. Differential amphiplasty and the control of ribosomal RNA synthesis. Heredity. 27:1-13.
76. Wendel, J. F. 2000. Genome evolution in polyploids. Plant Mol. Biol. 42:225-249.
77. Wendel, J. F., A. Schnabel, and T. Seelanan. 1995. Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proc. Natl. Acad. Sci. USA 92:280-284.
78. White, T. J., T. Bruns, S. Lee, and J. Taylor. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenies. Pp. 315-322 in M. A. Innis, D. H. Gelfand, J. J. Sninsky and T. J. White, eds. PCR protocols. Academic Press, San Diego, Calif.
79. Ziolkowski, P. A., G. Blanc, and J. Sadowski. 2003. Structural divergence of chromosomal segments that arose from successive duplication events in the Arabidopsis genome. Nucleic Acids Res. 31:1339-1350.