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. 2002 Nov;162(3):1435–1444. doi: 10.1093/genetics/162.3.1435

Highly condensed potato pericentromeric heterochromatin contains rDNA-related tandem repeats.

Robert M Stupar 1, Junqi Song 1, Ahmet L Tek 1, Zhukuan Cheng 1, Fenggao Dong 1, Jiming Jiang 1
PMCID: PMC1462313  PMID: 12454086

Abstract

The heterochromatin in eukaryotic genomes represents gene-poor regions and contains highly repetitive DNA sequences. The origin and evolution of DNA sequences in the heterochromatic regions are poorly understood. Here we report a unique class of pericentromeric heterochromatin consisting of DNA sequences highly homologous to the intergenic spacer (IGS) of the 18S.25S ribosomal RNA genes in potato. A 5.9-kb tandem repeat, named 2D8, was isolated from a diploid potato species Solanum bulbocastanum. Sequence analysis indicates that the 2D8 repeat is related to the IGS of potato rDNA. This repeat is associated with highly condensed pericentromeric heterochromatin at several hemizygous loci. The 2D8 repeat is highly variable in structure and copy number throughout the Solanum genus, suggesting that it is evolutionarily dynamic. Additional IGS-related repetitive DNA elements were also identified in the potato genome. The possible mechanism of the origin and evolution of the IGS-related repeats is discussed. We demonstrate that potato serves as an interesting model for studying repetitive DNA families because it is propagated vegetatively, thus minimizing the meiotic mechanisms that can remove novel DNA repeats.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams M. D., Celniker S. E., Holt R. A., Evans C. A., Gocayne J. D., Amanatides P. G., Scherer S. E., Li P. W., Hoskins R. A., Galle R. F. The genome sequence of Drosophila melanogaster. Science. 2000 Mar 24;287(5461):2185–2195. doi: 10.1126/science.287.5461.2185. [DOI] [PubMed] [Google Scholar]
  2. Arabidopsis Genome Initiative Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 2000 Dec 14;408(6814):796–815. doi: 10.1038/35048692. [DOI] [PubMed] [Google Scholar]
  3. Arnheim N., Seperack P., Banerji J., Lang R. B., Miesfeld R., Marcu K. B. Mouse rDNA nontranscribed spacer sequences are found flanking immunoglobulin CH genes and elsewhere throughout the genome. Cell. 1980 Nov;22(1 Pt 1):179–185. doi: 10.1016/0092-8674(80)90166-x. [DOI] [PubMed] [Google Scholar]
  4. Bennetzen J. L., Schrick K., Springer P. S., Brown W. E., SanMiguel P. Active maize genes are unmodified and flanked by diverse classes of modified, highly repetitive DNA. Genome. 1994 Aug;37(4):565–576. doi: 10.1139/g94-081. [DOI] [PubMed] [Google Scholar]
  5. Borisjuk N., Borisjuk L., Komarnytsky S., Timeva S., Hemleben V., Gleba Y., Raskin I. Tobacco ribosomal DNA spacer element stimulates amplification and expression of heterologous genes. Nat Biotechnol. 2000 Dec;18(12):1303–1306. doi: 10.1038/82430. [DOI] [PubMed] [Google Scholar]
  6. Borisjuk N., Hemleben V. Nucleotide sequence of the potato rDNA intergenic spacer. Plant Mol Biol. 1993 Jan;21(2):381–384. doi: 10.1007/BF00019953. [DOI] [PubMed] [Google Scholar]
  7. Boulikas T. Chromatin domains and prediction of MAR sequences. Int Rev Cytol. 1995;162A:279–388. doi: 10.1016/s0074-7696(08)61234-6. [DOI] [PubMed] [Google Scholar]
  8. Cheng Z., Stupar R. M., Gu M., Jiang J. A tandemly repeated DNA sequence is associated with both knob-like heterochromatin and a highly decondensed structure in the meiotic pachytene chromosomes of rice. Chromosoma. 2001 Apr;110(1):24–31. doi: 10.1007/s004120000126. [DOI] [PubMed] [Google Scholar]
  9. Childs G., Maxson R., Cohn R. H., Kedes L. Orphons: dispersed genetic elements derived from tandem repetitive genes of eucaryotes. Cell. 1981 Mar;23(3):651–663. doi: 10.1016/0092-8674(81)90428-1. [DOI] [PubMed] [Google Scholar]
  10. Copenhaver G. P., Pikaard C. S. 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. 1996 Feb;9(2):273–282. doi: 10.1046/j.1365-313x.1996.09020273.x. [DOI] [PubMed] [Google Scholar]
  11. Csink A. K., Henikoff S. Something from nothing: the evolution and utility of satellite repeats. Trends Genet. 1998 May;14(5):200–204. doi: 10.1016/s0168-9525(98)01444-9. [DOI] [PubMed] [Google Scholar]
  12. De Lucchini S., Andronico F., Andreazzoli M., Giuliani M., Savino R., Nardi I. Extra-ribosomal spacer sequences in Triturus. J Mol Biol. 1988 Dec 20;204(4):805–813. doi: 10.1016/0022-2836(88)90043-5. [DOI] [PubMed] [Google Scholar]
  13. Dover G. A., Flavell R. B. Molecular coevolution: DNA divergence and the maintenance of function. Cell. 1984 Oct;38(3):622–623. doi: 10.1016/0092-8674(84)90255-1. [DOI] [PubMed] [Google Scholar]
  14. Dover G. Molecular drive: a cohesive mode of species evolution. Nature. 1982 Sep 9;299(5879):111–117. doi: 10.1038/299111a0. [DOI] [PubMed] [Google Scholar]
  15. Dvorák J., Jue D., Lassner M. Homogenization of tandemly repeated nucleotide sequences by distance-dependent nucleotide sequence conversion. Genetics. 1987 Jul;116(3):487–498. doi: 10.1093/genetics/116.3.487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Flavell R. B. Repetitive DNA and chromosome evolution in plants. Philos Trans R Soc Lond B Biol Sci. 1986 Jan 29;312(1154):227–242. doi: 10.1098/rstb.1986.0004. [DOI] [PubMed] [Google Scholar]
  17. Gerlach W. L., Bedbrook J. R. Cloning and characterization of ribosomal RNA genes from wheat and barley. Nucleic Acids Res. 1979 Dec 11;7(7):1869–1885. doi: 10.1093/nar/7.7.1869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Guimond A., Moss T. A ribosomal orphon sequence from Xenopus laevis flanked by novel low copy number repetitive elements. Biol Chem. 1999 Feb;380(2):167–174. doi: 10.1515/BC.1999.025. [DOI] [PubMed] [Google Scholar]
  19. Hancock J. M. Simple sequences and the expanding genome. Bioessays. 1996 May;18(5):421–425. doi: 10.1002/bies.950180512. [DOI] [PubMed] [Google Scholar]
  20. Horvath J. E., Bailey J. A., Locke D. P., Eichler E. E. Lessons from the human genome: transitions between euchromatin and heterochromatin. Hum Mol Genet. 2001 Oct 1;10(20):2215–2223. doi: 10.1093/hmg/10.20.2215. [DOI] [PubMed] [Google Scholar]
  21. Kominami R., Muramatsu M. Amplified ribosomal spacer sequence: structure and evolutionary origin. J Mol Biol. 1987 Jan 5;193(1):217–222. doi: 10.1016/0022-2836(87)90639-5. [DOI] [PubMed] [Google Scholar]
  22. Koo H. S., Wu H. M., Crothers D. M. DNA bending at adenine . thymine tracts. Nature. 1986 Apr 10;320(6062):501–506. doi: 10.1038/320501a0. [DOI] [PubMed] [Google Scholar]
  23. Krystal M., D'Eustachio P., Ruddle F. H., Arnheim N. Human nucleolus organizers on nonhomologous chromosomes can share the same ribosomal gene variants. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5744–5748. doi: 10.1073/pnas.78.9.5744. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lander E. S., Linton L. M., Birren B., Nusbaum C., Zody M. C., Baldwin J., Devon K., Dewar K., Doyle M., FitzHugh W. Initial sequencing and analysis of the human genome. Nature. 2001 Feb 15;409(6822):860–921. doi: 10.1038/35057062. [DOI] [PubMed] [Google Scholar]
  25. Lohe A. R., Roberts P. A. An unusual Y chromosome of Drosophila simulans carrying amplified rDNA spacer without rRNA genes. Genetics. 1990 Jun;125(2):399–406. doi: 10.1093/genetics/125.2.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Maggini F., Cremonini R., Zolfino C., Tucci G. F., D'Ovidio R., Delre V., DePace C., Scarascia Mugnozza G. T., Cionini P. G. Structure and chromosomal localization of DNA sequences related to ribosomal subrepeats in Vicia faba. Chromosoma. 1991 May;100(4):229–234. doi: 10.1007/BF00344156. [DOI] [PubMed] [Google Scholar]
  27. Perry K. L., Palukaitis P. Transcription of tomato ribosomal DNA and the organization of the intergenic spacer. Mol Gen Genet. 1990 Mar;221(1):103–112. doi: 10.1007/BF00280374. [DOI] [PubMed] [Google Scholar]
  28. Redi C. A., Garagna S., Zacharias H., Zuccotti M., Capanna E. The other chromatin. Chromosoma. 2001 Jul;110(3):136–147. doi: 10.1007/s004120000114. [DOI] [PubMed] [Google Scholar]
  29. Schlötterer C., Tautz D. Chromosomal homogeneity of Drosophila ribosomal DNA arrays suggests intrachromosomal exchanges drive concerted evolution. Curr Biol. 1994 Sep 1;4(9):777–783. doi: 10.1016/s0960-9822(00)00175-5. [DOI] [PubMed] [Google Scholar]
  30. Schmidt E. R. Clustered and interspersed repetitive DNA sequence family of Chironomus. The nucleotide sequence of the Cla-elements and of various flanking sequences. J Mol Biol. 1984 Sep 5;178(1):1–15. doi: 10.1016/0022-2836(84)90227-4. [DOI] [PubMed] [Google Scholar]
  31. Song J., Dong F., Jiang J. Construction of a bacterial artificial chromosome (BAC) library for potato molecular cytogenetics research. Genome. 2000 Feb;43(1):199–204. [PubMed] [Google Scholar]
  32. Stark G. R., Debatisse M., Giulotto E., Wahl G. M. Recent progress in understanding mechanisms of mammalian DNA amplification. Cell. 1989 Jun 16;57(6):901–908. doi: 10.1016/0092-8674(89)90328-0. [DOI] [PubMed] [Google Scholar]
  33. Strand M., Prolla T. A., Liskay R. M., Petes T. D. Destabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair. Nature. 1993 Sep 16;365(6443):274–276. doi: 10.1038/365274a0. [DOI] [PubMed] [Google Scholar]
  34. Unfried K., Schiebel K., Hemleben V. Subrepeats of rDNA intergenic spacer present as prominent independent satellite DNA in Vigna radiata but not in Vigna angularis. Gene. 1991 Mar 1;99(1):63–68. doi: 10.1016/0378-1119(91)90034-9. [DOI] [PubMed] [Google Scholar]
  35. Wallrath L. L. Unfolding the mysteries of heterochromatin. Curr Opin Genet Dev. 1998 Apr;8(2):147–153. doi: 10.1016/s0959-437x(98)80135-4. [DOI] [PubMed] [Google Scholar]

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