Intragenomic heterogeneity of intergenic ribosomal DNA spacers in Cucurbita moschata is determined by DNA minisatellites with variable potential to form non-canonical DNA conformations

. 2019 Jun 01 ; 26 (3) : 273-286.

Jazyk angličtina Země Anglie, Velká Británie Médium print

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid31231763

The intergenic spacer (IGS) of rDNA is frequently built of long blocks of tandem repeats. To estimate the intragenomic variability of such knotty regions, we employed PacBio sequencing of the Cucurbita moschata genome, in which thousands of rDNA copies are distributed across a number of loci. The rRNA coding regions are highly conserved, indicating intensive interlocus homogenization and/or high selection pressure. However, the IGS exhibits high intragenomic structural diversity. Two repeated blocks, R1 (300-1250 bp) and R2 (290-643 bp), account for most of the IGS variation. They exhibit minisatellite-like features built of multiple periodically spaced short GC-rich sequence motifs with the potential to adopt non-canonical DNA conformations, G-quadruplex-folded and left-handed Z-DNA. The mutual arrangement of these motifs can be used to classify IGS variants into five structural families. Subtle polymorphisms exist within each family due to a variable number of repeats, suggesting the coexistence of an enormous number of IGS variants. The substantial length and structural heterogeneity of IGS minisatellites suggests that the tempo of their divergence exceeds the tempo of the homogenization of rDNA arrays. As frequently occurring among plants, we hypothesize that their instability may influence transcription regulation and/or destabilize rDNA units, possibly spreading them across the genome.

Zobrazit více v PubMed

Hemleben V., Zentgraf U.. 1994, Structural organization and regulation of transcription by RNA polymerase I of plant nuclear ribosomal RNA genes, Results Probl. Cell Differ., 20, 3–24. PubMed

Matyasek R., Dobesova E., Huska D.. 2016, Interpopulation hybridization generates meiotically stable rDNA epigenetic variants in allotetraploid Tragopogon mirus, Plant J., 85, 362–77. PubMed

Flavell R.B., Odell M., Thompson W.F., et al. 1986, The differential expression of ribosomal-RNA genes, Philos. Trans. Roy. Soc. B., 314, 385-397. doi:10.1098/rstb.1986.0060.

Martini G., O’Dell M., Flavell R.B.. 1982, Partial inactivation of wheat nucleolus organizers by the nucleolus organizer chromosomes from Aegilops-Umbellulata, Chromosoma, 84, 687–700.

Silva M., Pereira H.S., Bento M.. 2008, Interplay of ribosomal DNA loci in nucleolar dominance: dominant NORs are up-regulated by chromatin dynamics in the wheat-rye system. Plos One, 3, e3824. doi:10.1371/journal.pone.0003824. PubMed PMC

Komarova N.Y., Grabe T., Huigen D.J., et al.2004, Organization, differential expression and methylation of rDNA in artificial Solanum allopolyploids, Plant Mol. Biol., 56, 439–63. PubMed

Chen Z.J., Pikaard C.S.. 1997, 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, 3442–7. PubMed PMC

Wanzenbock E.M., Schofer C., Schweizer D., Bachmair A.. 1997, Ribosomal transcription units integrated via T-DNA transformation associate with the nucleolus and do not require upstream repeat sequences for activity in Arabidopsis thaliana, Plant J., 11, 1007–16. PubMed

Doelling J.H., Gaudino R.J., Pikaard C.S.. 1993, Functional-analysis of Arabidopsis thaliana ribosomal-RNA gene and spacer promoters in-vivo and by transient expression. Proc. Natl. Acad. Sci. USA., 90, 7528–32. PubMed PMC

Zentgraf U., Hemleben V.. 1992, Complex-formation of nuclear proteins with the RNA polymerase-I promoter and repeated elements in the external transcribed spacer of Cucumis sativus ribosomal DNA, Nucleic Acids Res., 20, 3685–91. PubMed PMC

Komarova N.Y., Grimm G.W., Hemleben V., Volkov R.A.. 2008, Molecular evolution of 35S rDNA and taxonomic status of Lycopersicon within Solanum sect. Petota, Plant Syst. Evol., 276, 59–71.

Schiebel K., von Waldburg G., Gerstner J., Hemleben V.. 1989, Termination of transcription of ribosomal-RNA genes of mung bean occurs within a 175-bp repetitive element of the spacer region, Mol. Gen. Genet., 218, 302–7. PubMed

Eickbush T.H., Eickbush D.G.. 2007, Finely orchestrated movements: evolution of the ribosomal RNA genes, Genetics, 175, 477–85. PubMed PMC

Havlová K., Dvořáčková M., Peiro R., et al.2016, Variation of 45S rDNA intergenic spacers in Arabidopsis thaliana, Plant Mol. Biol., 92, 457–71. PubMed

Grummt I., Langst G.. 2013, Epigenetic control of RNA polymerase I transcription in mammalian cells, Biochim. Biophys. Acta, 1829, 393–404. PubMed

Durut N., Abou-Ellail M., Pontvianne F., et al.2014, A duplicated NUCLEOLIN gene with antagonistic activity is required for chromatin organization of silent 45S rDNA in Arabidopsis, Plant Cell, 26, 1330–44. PubMed PMC

Waminal N.E., Kim N.S., Kim H.H.. 2011, Dual-color FISH karyotype analyses using rDNAs in three Cucurbitaceae species, Genes Genom., 33, 521–8.

King K., Torres R.A., Zentgraf U., Hemleben V.. 1993, Molecular evolution of the intergenic spacer in the nuclear ribosomal-RNA genes of Cucurbitaceae, J. Mol. Evol., 36, 144–52. PubMed

Siegel A., Kolacz K.. 1983, Heterogeneity of pumpkin ribosomal DNA, Plant Physiol., 72, 166–71. PubMed PMC

Matyasek R., Fulnecek J., Leitch A.R., Kovarik A.. 2011, Analysis of two abundant, highly related satellites in the allotetraploid Nicotiana arentsii using double-strand conformation polymorphism analysis and sequencing, New Phytol., 192, 747–59. PubMed

Lim K.Y., Kovarik A., Matyasek R., Bezdek M., Lichtenstein C.P., Leitch A.R.. 2000, Gene conversion of ribosomal DNA in Nicotiana tabacum is associated with undermethylated, decondensed and probably active gene units, Chromosoma, 109, 161–72. PubMed

Benson G. 1999, Tandem repeats finder: a program to analyze DNA sequences, Nucleic Acids Res., 27, 573–80. PubMed PMC

Kikin O., D’Antonio L., Bagga P.S.. 2006, QGRS Mapper: a web-based server for predicting G-quadruplexes in nucleotide sequences, Nucleic Acids Res., 34, W676–82. PubMed PMC

Shin S.I., Ham S., Park J.. 2016, Z-DNA-forming sites identified by ChIP-Seq are associated with actively transcribed regions in the human genome, DNA Res., 23, 477–86. PubMed PMC

Tamura K., Nei M.. 1993, Estimation of the number of nucleotide substitutions in the control region of mitochondrial-DNA in humans and chimpanzees, Mol. Biol. Evol., 10, 512–26. PubMed

Jenkins G., Hasterok R.. 2007, BAC ‘landing’ on chromosomes of Brachypodium distachyon for comparative genome alignment, Nat. Protoc., 2, 88–98. PubMed

Lim K.Y., Skalicka K., Koukalova B., et al.2004, Dynamic changes in the distribution of a satellite homologous to intergenic 26-18S rDNA spacer in the evolution of Nicotiana, Genetics, 166, 1935–46. PubMed PMC

Richard G.F., Paques F.. 2000, Mini- and microsatellite expansions: the recombination connection, EMBO Rep., 1, 122–6. PubMed PMC

Gemayel R., Vinces M.D., Legendre M., Verstrepen K.J.. 2010, Variable tandem repeats accelerate evolution of coding and regulatory sequences, Annu. Rev. Genet., 44, 445–77. PubMed

Espley R.V., Brendolise C., Chagne D., et al.2009, Multiple repeats of a promoter segment causes transcription factor autoregulation in red apples, Plant Cell, 21, 168–83. PubMed PMC

Schmitz M.L., Maier U.G., Brown J.W.S., Feix G.. 1989, Specific binding of nuclear proteins to the promoter region of a maize nuclear ribosomal-RNA gene unit, J. Biol. Chem., 264, 1467–72. PubMed

Caudy A.A., Pikaard C.S.. 2002, Xenopus ribosomal RNA gene intergenic spacer elements conferring transcriptional enhancement and nucleolar dominance-like competition in oocytes, J. Biol. Chem., 277, 31577–84. PubMed

Kuhn A., Deppert U., Grummt I.. 1990, A 140-base pair repetitive sequence element in the mouse ribosomal-RNA gene spacer enhances transcription by RNA polymerase-I in a cell-free system. Proc. Natl. Acad. Sci. USA., 87, 7527–31. PubMed PMC

Yadav V., Hemansi, Kim N., Tuteja N., Yadav P.. 2017, G quadruplex in plants: a ubiquitous regulatory element and its biological relevance, Front Plant Sci., 8,1163, 10.3389/fpls PubMed PMC

Wang G.L., Vasquez K.M.. 2007, Z-DNA, an active element in the genome, Front. Biosci., 12, 4424–38. PubMed

Mishra S.K., Tawani A., Mishra A., Kumar A.. 2016, G4IPDB: a database for G-quadruplex structure forming nucleic acid interacting proteins. Sci. Rep., 6, 38144. PubMed PMC

Chiarella S., De Cola A., Scaglione G.L., et al.2013, Nucleophosmin mutations alter its nucleolar localization by impairing G-quadruplex binding at ribosomal DNA, Nucleic Acids Res., 41, 3228–39. PubMed PMC

Nikolova E.N., Kim E., Wise A.A., O’Brien P.J., Andricioaei I., Al-Hashimi H.M.. 2011, Transient hoogsteen base pairs in canonical duplex DNA, Nature, 470, 498.U484. PubMed PMC

Sun D.K., Guo K.X., Shin Y.J.. 2011, Evidence of the formation of G-quadruplex structures in the promoter region of the human vascular endothelial growth factor gene, Nucleic Acids Res., 39, 1256–65. PubMed PMC

Moradi M., Babin V., Roland C., Sagui C.. 2013, Reaction path ensemble of the B-Z-DNA transition: a comprehensive atomistic study, Nucleic Acids Res., 41, 33–43. PubMed PMC

Temiz N.A., Donohue D.E., Bacolla A., Luke B.T., Collins J.R.. 2012, The role of methylation in the intrinsic dynamics of B- and Z-DNA, PLoS One, 7, e35558. PubMed PMC

Dobešová E., Malinská H., Matyášek R., et al.2015, Silenced rRNA genes are activated and substitute for partially eliminated active homeologs in the recently formed allotetraploid, Tragopogon mirus (Asteraceae), Heredity, 114, 356–65. PubMed PMC

Gabrielian A., Bolshoy A.. 1999, Sequence complexity and DNA curvature, Comput. Chem., 23, 263–74. PubMed

Garcia S., Garnatje T., Kovařík A.. 2012, Plant rDNA database: ribosomal DNA loci information goes online, Chromosoma, 121, 389–94. PubMed

Dadejova M., Lim K.Y., Souckova S.K.. 2007, Transcription activity of rRNA genes correlates with a tendency towards intergenomic homogenization in Nicotiana allotetraploids, New Phytol., 174, 658–68. PubMed

Sochorova J., Coriton O., Kuderova A., Lunerova J., Chevre A.M., Kovarik A.. 2017, Gene conversion events and variable degree of homogenization of rDNA loci in cultivars of Brassica napus, Ann. Bot., 119, 13–26. PubMed PMC

Bauer N., Horvat T., Birus I., Vicic V., Zoldos V.. 2009, Nucleotide sequence, structural organization and length heterogeneity of ribosomal DNA intergenic spacer in Quercus petraea (Matt.) Liebl. and Q-robur L, Mol. Genet. Genomics, 281, 207–21. PubMed

Suzuki A., Tanifuji S., Komeda Y., Kato A.. 1996, Structural and functional characterization of the intergenic spacer region of the rDNA in Daucus carota, Plant Cell Physiol., 37, 233–8. PubMed

Mestrovic N., Plohl M., Mravinac B., Ugarkovic D.. 1998, Evolution of satellite DNAs from the genus Palorus - experimental evidence for the “library” hypothesis, Mol. Biol. Evol., 15, 1062–8. PubMed

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace