Abstract
Ribosomal RNA (5S and 45S) genes were investigated by FISH in two related legumes: soybean [Glycine max (L.) Merr.] and common bean (Phaseolis vulgaris L.). These species are both members of the same tribe (Phaseoleae), but common bean is diploid while soybean is a tetraploid which has undergone diploidization. In contrast to ploidy expectations, soybean had only one 5S and one 45S rDNA locus whereas common bean had more than two 5S rDNA loci and two 45S rDNA loci. Double hybridization experiments with differentially labelled probes indicated that the soybean 45S and 5S rDNA loci are located on different chromosomes and in their distal regions. Likewise, the common bean 45S and 5S rDNA loci were on unique chromosomes, though two of the 5S rDNA loci were on the same chromosome. FISH analysis of interphase nuclei revealed the spatial arrangement of rDNA loci and suggested expression patterns. In both species, we observed one or more 5S rDNA hybridization sites and two 45S rDNA hybridization sites associated with the nucleolar periphery. The 45S rDNA hybridization patterns frequently exhibited gene puffs as de-condensed chromatin strings within the nucleoli. The other condensed rDNA sites (both 5S and 45S) were spatially distant from the nucleolus in nucleoplasmic regions containing heterochromatin. The distribution of rDNA between the nucleoplasm and the nucleoli is consistent with differential gene expression between homologous alleles and among homoeologous loci.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bauwens S, Van Ostveldt P, Engler G, Van Montagu M (1991) Distribution of the rDNA and three classes of highly repetitive DNA in the chromatin of interphase nuclei of Arabidopsis thaliana. Chromosoma 101:41–48
Becker TA, Nagl W (1994) Disproportional numbers of rDNA loci in diploid and polyploid testis nuclei of Gerris najas detected by fluorescence in situ hybridization. Cell Biol Int 18:245–255
Crane CF, Price HJ, Stelly DM, Czeschin DG Jr, McKnight TD (1993) Identification of a homoeologous chromosome pair by in situ DNA hybridization to ribosomal RNA loci in meiotic chromosomes of cotton (Gossypium hirsutum). Genome 36:1015–1022
Danna, KJ, Workman R, Coryell V, Keim P (1996) 5S rRNA genes in tribe Phaseoleae: array size, number, and dynamics. Genome 39:445–455
Delseny M, McGarth JM, This P, Chevre AM, Quiros CF (1990) Ribosomal RNA genes in diploid and amphiploid Brassica and related species: organization, polymorphism, and evolution. Genome 33:733–744
Ellis THN, Thomas CM, Simpson PR, Cleary WG, Newman M-A, Burcham KWG (1988) 5S rRNA genes in Pisum: sequence, long range and chromosomal organization. Mol Gen Genet 214:333–342
Ellis THN, Delseny M, Lee D, Burcham WG (1989) Methylated and undermethylated rDNA repeats are interspersed at random in two higher plant species. Plant Mol Biol 14:73–80
Errico A, Conicella C, Venora G (1991) Karyotype studies on Pisum fulvum and Pisum sativum, using a chromosome image-analysis system. Genome 34:105–108
Flavell RB, O'Dell M, Sardana R, Jackson S (1993) Regulatory DNA of ribosomal RNA genes and control of nucleolus organizer activity in wheat. Crop Sci 85:889–894
Fukui K, Ohmido N, Klush, GS (1994) Variability in rDNA loci in the genus Oryza detected through fluorescence in situ hybridization. Theor Appl Genet 87:893–899
Griffor MC, Vodkin LO, Singh RJ, Hymowitz T (1991) Fluorescent situ hybridization to soybean metaphase chromosomes. Plant Mol Biol 17:101–109
Highett ML, Rawlins DJ, Shaw PJ (1993) Different patterns of rDNA distribution in Pisum sativum nucleoli correlate with different levels of nucleolar activity. J Cell Sci 104:843–852
Hymowitz T, Singh RJ (1987) Taxonomy and speciation. In: Wilcox JR (ed) Soybeans: improvement, production, and uses. 2nd edn. Agron Ser 16 ASA, CSSA, SSSA. Madison, Wisconsin
Jackson PJ, Lark KG (1982) Ribosomal RNA synthesis in soybean suspension cultures growing in different media. Plant Physiol 69:234–239
Kim N-S, Kuspira J, Armstrong K, Bhambhani R (1993) Genetic and cytogenetic analyses of the A genome of Triticum monococcum. VIII. Localization of rDNAs and characterization of 5S rRNA genes. Genome 36:77–86
Lackey JA (1980) Chromosome numbers in the Phaseoleae (Fabaceae: Favoideae) and their relation to taxonomy. Am J Bot 67:595–602
Leitch IJ, Heslop-Harrison JS (1992) Physical mapping of the 46S rRNA genes in barley by in situ hybridization. Genome 35:1013–1018
Leitch IJ, Leitch AR, Heslop-Harrison JS (1991) Physical mapping of plant DNA sequences by simultaneous in situ hybridization of two differently labelled fluorescent probes. Genome 34:329–333
Leitch AR, Mosgoller W, Shi M, Heslop-Harrison JS (1992) Different patterns of rDNA organization at interphase in nuclei of wheat and rye. J Cell Sci 101:751–757
Linde-Laursen I, Ibsen E, Von Bothmer R, Giese H (1992) Physical localization of active and inactive rRNA gene loci in Hordeum marinum sp. gussoneanum (4x) by in situ hybridization. Genome 35:1032–1036
Maluszynska J, Heslop-Harrison JS (1993a) Molecular cytogenetics of the genus Arabidopsis: in situ localization of rDNA sites, chromosome numbers and diversity in centromeric heterochromatin. Ann Bot 71:479–484
Maluszynska J, Heslop-Harrison JS (1993b) Physical mapping of rDNA loci in Brassica species. Genome 36:774–781
Mukai Y, Endo TR, Gill BS (1990) Physical mapping of the 5S rRNA multigene family in common wheat. J Hered 81:290–295
Mukai Y, Endo TR, Gill BS (1991) Physical mapping of the 18S.26S rRNA multigene family in common wheat: identification of a new locus. Chromosoma 100:71–78
Pedersen C, Linde-Laursen I (1994) Chromosomal localizations of four minor rDNA loci and a marker microsatellite sequence in barley. Chromosome Res 2:65–71
Pinkel D, Straume T, Gray JW (1986) Cytogenetic analysis using quantitative, high sensitivity, fluorescence hybridization. Proc Natl Acad Sci USA 83:2934–2938
Quemada H, Roth EJ, Lark KG (1987) Changes in methylation of tissue-cultured soybean cells detected by digestion with the restriction enzymes HpaII and MspI. Plant Cell Rep 6:63–66
Rowlins DJ, Shaw PJ (1990) Three-dimensional organization of ribosomal DNA in interphase nuclei of Pisum sativum by in situ hybridization and optical tomography. Chromosoma 99:143–151
Rogers SO, Bendich AJ (1987). Ribosomal genes in plants, variability in copy number and in the intergenic spacer. Plant Mol Biol 9:509–520
Schmidt T, Schwarzacher T, Heslop-Harrison JS (1994) Physical mapping of rRNA genes by fluorescent in situ hybridization and structural analysis of 5S rRNA genes and intergenic spacer sequences in sugar beet (Beta vulgaris). Theor Appl Genet 88:629–636
Skorupska H, Albertsen MC, Langholz KD, Palmer RG (1989) Detection of ribosomal RNA genes in soybean, Glycine max (L.) Merr., by in situ hybridization. Genome 32:1091–1095
Zheng J, Nakata M, Uchiyama H, Morikawa H, Tanaka R (1991) Giemsa C-banding pattern in several species of Phaseolus L. and Vigna Savi, Fabaceae. Cytologia 56:459–466
Zhu T, Schupp JM, Oliphont A, Keim P (1994) Hypomethylated sequences: characterization of the duplicate soybean genome. Mol Gen Genet 244:638–645
Zhu T, Shi L, Doyle JJ, Keim P (1995a) Phylogenetic analysis of DNA sequence of a single nuclear locus in soybean and relatives. Theor Appl Genet 90:990–999
Zhu T, Shi L, Keim P (1995b) Fluorescence in situ detection of single-copy DNA sequences in soybean chromosomes. Plant Mol Biol Rep 13:220–228
Author information
Authors and Affiliations
Additional information
Communicated by K. Tsunewaki
Rights and permissions
About this article
Cite this article
Shi, L., Zhu, T. & Keim, P. Ribosomal RNA genes in soybean and common bean: chromosomal organization, expression, and evolution. Theoret. Appl. Genetics 93, 136–141 (1996). https://doi.org/10.1007/BF00225738
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00225738