Personal Perspectives on Plant Ribosomal RNA Genes Research: From Precursor-rRNA to Molecular Evolution

. 2021 ; 12 () : 797348. [epub] 20211221

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid34992624

The history of rDNA research started almost 90 years ago when the geneticist, Barbara McClintock observed that in interphase nuclei of maize the nucleolus was formed in association with a specific region normally located near the end of a chromosome, which she called the nucleolar organizer region (NOR). Cytologists in the twentieth century recognized the nucleolus as a common structure in all eukaryotic cells, using both light and electron microscopy and biochemical and genetic studies identified ribosomes as the subcellular sites of protein synthesis. In the mid- to late 1960s, the synthesis of nuclear-encoded rRNA was the only system in multicellular organisms where transcripts of known function could be isolated, and their synthesis and processing could be studied. Cytogenetic observations of NOR regions with altered structure in plant interspecific hybrids and detailed knowledge of structure and function of rDNA were prerequisites for studies of nucleolar dominance, epistatic interactions of rDNA loci, and epigenetic silencing. In this article, we focus on the early rDNA research in plants, performed mainly at the dawn of molecular biology in the 60 to 80-ties of the last century which presented a prequel to the modern genomic era. We discuss - from a personal view - the topics such as synthesis of rRNA precursor (35S pre-rRNA in plants), processing, and the organization of 35S and 5S rDNA. Cloning and sequencing led to the observation that the transcribed and processed regions of the rRNA genes vary enormously, even between populations and species, in comparison with the more conserved regions coding for the mature rRNAs. Epigenetic phenomena and the impact of hybridization and allopolyploidy on rDNA expression and homogenization are discussed. This historical view of scientific progress and achievements sets the scene for the other articles highlighting the immense progress in rDNA research published in this special issue of Frontiers in Plant Science on "Molecular organization, evolution, and function of ribosomal DNA."

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Adesnik M., Levinthal C. (1969). Synthesis and maturation of ribosomal RNA in Escherichia coli. J. Mol. Biol. 46, 281–303. doi: 10.1016/0022-2836(69)90422-7, PMID: PubMed DOI

Appels R., Moran L. B., Gustafson J. P. (1986). Rye heterochromatin. 1. Studies on clusters of the major repeating sequence and the identification of a new dispersed repetitive sequence element. Can. J. Genet. Cytol. 28, 645–657. doi: 10.1139/g86-094 DOI

Appels R., Wang P., Islam S. (2021). Integrating wheat nucleolus structure and function: variation in the wheat ribosomal RNA and protein genes. Front. Plant Sci. PubMed PMC

Bendich A. J., Anderson R. S. (1974). Novel properties of satellite DNA from muskmelon. Proc. Natl. Acad. Sci. U. S. A. 71, 1511–1515. doi: 10.1073/pnas.71.4.1511, PMID: PubMed DOI PMC

Bersaglieri C., Santoro R. (2019). Genome organization in and around the nucleolus. Cell 8:579. doi: 10.3390/cells8060579, PMID: PubMed DOI PMC

Birnstiel M., Speirs J., Purdom I., Jones K., Loening U. E. (1968). Properties and composition of isolated ribosomal DNA satellite of Xenopus laevis. Nature 219, 454–463. doi: 10.1038/219454a0, PMID: PubMed DOI

Birnstiel M. L., Wallace H., Stirlin L., Fischberger M. (1966). Localization of the ribosomal DNA complements in the nucleolar organizer regions in Xenopus laevis. Natl. Cancer Inst. Monogr. 23, 431–447. PMID: PubMed

Borisjuk N., Borisjuk L., Komarnytsky S., Timeva S., Hemleben V., Gleba Y., et al. . (2000). Tobacco ribosomal DNA spacer element stimulates amplification and expression of heterologous genes. Nat. Biotechnol. 18, 1303–1306. doi: 10.1038/82430, PMID: PubMed DOI

Borisjuk N., Borisjuk L., Petjuch G., Hemleben V. (1994). Comparison of nuclear ribosomal RNA genes among Solanum species and other Solanaceae. Genome 37, 271–279. doi: 10.1139/g94-038, PMID: PubMed DOI

Borisjuk N. V., Davidjuk Y. M., Kostishin S. S., Miroshnichenco G. P., Velasco R., Hemleben V., et al. . (1997). Structural analysis of rDNA in the genus Nicotiana. Plant Mol. Biol. 35, 655–660. doi: 10.1023/A:1005856618898, PMID: PubMed DOI

Borisjuk N., Hemleben V. (1993). Nucleotide sequence of the potato rDNA intergenic spacer. Plant Mol. Biol. 21, 381–384. doi: 10.1007/Bf00019953, PMID: PubMed DOI

Borisjuk N. V., Kostyshin S. S., Volkov R. A., Miroshnichenko G. P. (1989). Ribosomal RNA gene organization in higher plants from Nicotiana genus. Mol. Biol. 23, 1067–1074.

Borisjuk N. V., Miroshnichenko G. P. (1989). Organization of ribosomal RNA genes in Brassica oleracea, B. campestris and their natural allotetraploid hybrid B. napus. Genetika 25, 417–424.

Borisjuk N. V., Momot V. P., Gleba Y. (1988). Novel class of rDNA repeat units in somatic hybrids between Nicotiana and Atropa. Theor. Appl. Genet. 76, 108–112. doi: 10.1007/Bf00288839, PMID: PubMed DOI

Brown D. D., Gurdon J. B. (1964). Absence of ribosomal RNA synthesis in anucleolate mutant of Xenopus laevis. Proc. Natl. Acad. Sci. U. S. A. 51, 139–146. doi: 10.1073/pnas.51.1.139, PMID: PubMed DOI PMC

Brown J. W. S., Shaw P. J. (1998). Small nucleolar RNAs and pre-rRNA processing in plants. Plant Cell 10, 649–657. doi: 10.1105/tpc.10.5.649, PMID: PubMed DOI PMC

Brown D. D., Wensink P. C., Jordan E. (1972). A comparison of ribosomal DNAs of Xenopus laevis and Xenopus mulleri: evolution of tandem genes. J. Mol. Biol. 63, 57–73. doi: 10.1016/0022-2836(72)90521-9, PMID: PubMed DOI

Cantara W. A., Crain P. F., Rozenski J., McCloskey J. A., Harris K. A., Zhang X. N., et al. . (2011). The RNA modification database, RNAMDB: 2011 update. Nucl. Acids Res. 39, D195–D201. doi: 10.1093/nar/gkq1028, PMID: PubMed DOI PMC

Capesius I. (1997). Analysis of the ribosomal RNA gene repeat from the moss Funaria hygrometrica. Plant Mol. Biol. 33, 559–564. doi: 10.1023/a:1005740031313, PMID: PubMed DOI

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, 31577–31584. doi: 10.1074/jbc.M202737200, PMID: PubMed DOI

Chandrasekhara C., Mohannath G., Blevins T., Pontvianne F., Pikaard C. S. (2016). Chromosome-specific NOR inactivation explains selective rRNA gene silencing and dosage control in Arabidopsis. Genes Dev. 30, 177–190. doi: 10.1101/gad.273755.115, PMID: PubMed DOI PMC

Chandrashekaran M. (2006). Erwin Bünning (1906–1990): a centennial homage. J. Biosci. 31, 5–12. doi: 10.1007/BF02705230, PMID: PubMed DOI

Chen Z. J., Comai L., Pikaard C. S. (1988). 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. doi: 10.1073/pnas.95.25.14891 PubMed DOI PMC

Chen Z. J., Pikaard C. S. (1997a). Epigenetic silencing of RNA polymerase I transcription: a role for DNA methylation and histone modification in nucleolar dominance. Genes Dev. 11, 2124–2136. doi: 10.1101/gad.11.16.2124, PMID: PubMed DOI PMC

Chen Z. J., Pikaard C. S. (1997b). Transcriptional analysis of nucleolar dominance in polyploid plants: biased expression/silencing of progenitor rRNA genes is developmentally regulated in Brassica. Proc. Natl. Acad. Sci. U. S. A. 94, 3442–3447. doi: 10.1073/pnas.94.7.3442, PMID: PubMed DOI PMC

Chen G., Stepanenko A., Borisjuk N. (2021). Mosaic arrangement of the 5S rDNA in the aquatic plant Landoltia punctata (Lemnaceae). Front. Plant Sci. 12:678689. doi: 10.3389/fpls.2021.678689, PMID: PubMed DOI PMC

Cox B. J., Turnock G. (1973). Synthesis and processing of ribosomal RNA in cultured plant cells. Eur. J. Biochem. 37, 367–376. doi: 10.1111/j.1432-1033.1973, PMID: PubMed DOI

Dadejova M., Lim K. Y., Souckova-Skalicka K., Matyasek R., Grandbastien M. A., Leitch A., et al. . (2007). Transcription activity of rRNA genes correlates with a tendency towards intergenomic homogenization in Nicotiana allotetraploids. New Phytol. 174, 658–668. doi: 10.1111/j.1469-8137.2007.02034.x, PMID: PubMed DOI

Dahlberg A. E., Peacock A. C. (1971). Studies of 16 and 23 S ribosomal RNA of Escherichia coli using composite gel electrophoresis. J. Mol. Biol. 55, 61–74. doi: 10.1016/0022-2836(71)90281-6, PMID: PubMed DOI

Delcasso-Tremousaygue D., Grellet F., Panabieres F., Ananiev E. D., Delseny M. (1988). Structural and transcriptional characterization of the external spacer of a ribosomal RNA nuclear gene from a higher plant. Eur. J. Biochem. 172, 767–776. doi: 10.1111/j.1432-1033.1988.tb13956.x, PMID: PubMed DOI

Denk T., Grimm G. (2010). The oaks of western Eurasia: traditional classifications and evidence from two nuclear markers. Taxon 59, 351–366. doi: 10.1002/tax.592002 DOI

Denk T., Grimm G. W., Hemleben V. (2005). Patterns of molecular and morphological differentiation in Fagus (Fagaceae): phylogenetic implications. Am. J. Bot. 92, 1006–1016. doi: 10.3732/ajb.92.6.1006, PMID: PubMed DOI

Dodsworth S., Kovarik A., Grandbastien M.-A., Leitch I. J., Leitch A. R. (2020). “Repetitive DNA dynamics and polyploidization in the genus Nicotiana (Solanaceae),” in The Tobacco Plant Genome. Compendium of Plant Genomes. eds. Ivanov N., Sierro N., Peitsch M. (Cham: Springer; ).

Dover G. A. (1982). Molecular drive: a cohesive mode of species evolution. Nature 299, 111–117. doi: 10.1038/299111a0, PMID: PubMed DOI

Earley K., Lawrence R. J., Pontes O., Reuther R., Enciso A. J., Silva M., et al. . (2006). Erasure of histone acetylation by Arabidopsis HDA6 mediates large-scale gene silencing in nucleolar dominance. Genes Dev. 20, 1283–1293. doi: 10.1101/gad.1417706, PMID: PubMed DOI PMC

Eickbush T. H., Eickbush D. G. (2007). Finely orchestrated movements: evolution of the ribosomal RNA genes. Genetics 175, 477–485. doi: 10.1534/genetics.107.071399, PMID: PubMed DOI PMC

Ellis T. H., Lee D., Thomas C. M., Simpson P. R., Cleary W. G., Newman M. A., et al. . (1988). 5S rRNA genes in Pisum: sequence, long range and chromosomal organization. Mol. Gen. Genet. 214, 333–342. doi: 10.1007/BF00337732, PMID: PubMed DOI

Flavell R. B., O'Dell M., Thompson W. F. (1988). Regulation of cytosine methylation in ribosomal DNA and nucleolus organizer expression in wheat. J. Mol. Biol. 204, 523–534. doi: 10.1016/0022-2836(88)90352-X, PMID: PubMed DOI

Fraser R., Loening U. (1974). RNA synthesis during synchronous cell division in cultured explants of Jerusalem artichoke tuber. J. Exp. Bot. 25, 847–859. doi: 10.1093/jxb/25.5.847, PMID: PubMed DOI

Friedrich H., Hemleben V., Meagher R. B., Key J. L. (1979). Purification and restriction endonuclease mapping of soybean 18 S and 25 S ribosomal RNA genes. Planta 146, 467–473. doi: 10.1007/Bf00380862, PMID: PubMed DOI

Fulnecek J., Lim K. Y., Leitch A. R., Kovarik A., Matyasek R. (2002). Evolution and structure of 5S rDNA loci in allotetraploid Nicotiana tabacum and its putative parental species. Heredity 88, 19–25. doi: 10.1038/sj.hdy.6800001, PMID: PubMed DOI

Fulnecek J., Matyasek R., Kovarik A., Bezdek M. (1998). Mapping of 5-methylcytosine residues in Nicotiana tabacum 5S rRNA genes by genomic sequencing. Mol. Gen. Genet. 259, 133–141. doi: 10.1007/s004380050798, PMID: PubMed DOI

Galian J. A., Rosato M., Rossello J. A. (2012). Early evolutionary colocalization of the nuclear ribosomal 5S and 45S gene families in seed plants: evidence from the living fossil gymnosperm Ginkgo biloba. Heredity 108, 640–646. doi: 10.1038/hdy.2012.2, PMID: PubMed DOI PMC

Gall J. G. (1981). Chromosome structure and the C-value paradox. J. Cell Biol. 91, 3s–14s. doi: 10.1083/jcb.91.3.3s, PMID: PubMed DOI PMC

Ganal M., Hemleben V. (1986). Comparison of the ribosomal-RNA genes in 4 closely related Cucurbitaceae. Plant Syst. Evol. 154, 63–77. doi: 10.1007/Bf00984868 DOI

Ganal M., Torres R., Hemleben V. (1988). Complex structure of the DNA ribosomal spacer of Cucumis sativus (cucumber). Mol. Gen. Genet. 212, 548–554. doi: 10.1007/BF00330863, PMID: PubMed DOI

Garcia S., Borowska-Zuchowska N., Wendel J. F., Ainouche M., Kuderova A., Kovarik A. (2020). The utility of graph clustering of 5S ribosomal DNA homoeologs in plant allopolyploids, homoploid hybrids and cryptic introgressants. Front. Plant Sci. 11:41. doi: 10.3389/fpls.2020.00041, PMID: PubMed DOI PMC

Garcia S., Garnatje T., Kovarik A. (2012). Plant rDNA database: ribosomal DNA loci information goes online. Chromosoma 121, 389–394. doi: 10.1007/s00412-012-0368-7, PMID: PubMed DOI

Garcia S., Kovarik A. (2013). Dancing together and separate again: gymnosperms exhibit frequent changes of fundamental 5S and 35S rRNA gene (rDNA) organisation. Heredity 111, 23–33. doi: 10.1038/hdy.2013.11, PMID: PubMed DOI PMC

Garcia S., Kovarik A., Leitch A. R., Garnatje T. (2016). Cytogenetic features of rRNA genes across land plants: analysis of the plant rDNA database. Plant J. 89, 1020–1030. doi: 10.1111/tpj.13442, PMID: PubMed DOI

Garcia S., Lim K. Y., Chester M., Garnatje T., Pellicer J., Valles J., et al. . (2009). Linkage of 35S and 5S rRNA genes in Artemisia (family Asteraceae): first evidence from angiosperms. Chromosoma 118, 85–97. doi: 10.1007/s00412-008-0179-z, PMID: PubMed DOI

Garcia S., Panero J. L., Siroky J., Kovarik A. (2010). Repeated reunions and splits feature the highly dynamic evolution of 5S and 35S ribosomal RNA genes (rDNA) in the Asteraceae family. BMC Plant Biol. 10:176. doi: 10.1186/1471-2229-10-176, PMID: PubMed DOI PMC

Gerstner J., Schiebel K., von Waldburg G., Hemleben V. (1988). Complex organization of the length heterogeneous 5' external spacer of mung bean (Vigna radiata) ribosomal DNA. Genome 30, 723–733. doi: 10.1139/g88-120, PMID: PubMed DOI

Gleba Y. Y., Hinnisdaels S., Sidorov V. A., Kaleda V. A., Parokonny A. S., Boryshuk N. V., et al. . (1988). Intergeneric asymmetric hybrids between Nicotiana plumbaginifolia and Atropa belladonna obtained by "gamma-fusion". Theor. Appl. Genet. 76, 760–766. doi: 10.1007/BF00303523, PMID: PubMed DOI

Goldberg R. B., Bemis W. P., Siegel A. (1972). Nucleic acid hybridization studies within the genus Cucurbitaceae. Genetics 72, 253–266. doi: 10.1093/genetics/72.2.253, PMID: PubMed DOI PMC

Goodspeed T. H. (1954). The Genus Nicotiana. Massachusetts, USA: Waltham

Gray M. W. (2017). Lynn Margulis and the endosymbiont hypothesis: 50 years later. Mol. Biol. Cell 28, 1285–1287. doi: 10.1091/mbc.E16-07-0509, PMID: PubMed DOI PMC

Grebenstein B., Röser M., Sauer W., Hemleben V. (1998). Molecular phylogenetic relationships in Aveneae (Poaceae) species and other grasses as inferred from ITS1 and ITS2 rDNA sequences. Plant Syst. Evol. 213, 233–250. doi: 10.1007/Bf00985203 DOI

Grierson D. (1972). The Synthesis of rRNA in Developing Primary Leaves of Phaseolus aureus. PhD, Edinburgh, UK.

Grierson D. (1984). “Structure and expression of nuclear genes,” in Plant Molecular Biology. eds. Grierson D., Covey S. N. (Glasgow: Blackie; ).

Grierson D., Hemleben V. (1977). Ribonucleic acid from higher plant Matthiola incana. Molecular weight measurements and DNA RNA hybridization studies. Biochim. Biophys. Acta 475, 424–436. doi: 10.1016/0005-2787(77)90058-2, PMID: PubMed DOI

Grierson D., Loening U. E. (1972). Distinct transcription products of ribosomal genes in 2 different tissues. Nature New Biol. 235, 80–82. doi: 10.1038/newbio235080a0, PMID: PubMed DOI

Grierson D., Loening U. (1974). Ribosomal RNA precursors and synthesis of chloroplast and cytoplasmic ribosomal acid in leaves of Phaseolus aureus. Eur. J. Biochem. 44, 501–507. doi: 10.1111/j.1432-1033.1974.tb03508.x, PMID: PubMed DOI

Grierson D., Rogers M. E., Sartiran M., Loening U. E. (1970). The synthesis of ribosomal RNA in different organisms: structure and evolution of rRNA precursor. Cold Spring Harb. Symp. Quant. Biol. 35, 589–598. doi: 10.1101/Sqb.1970.035.01.074 DOI

Grierson D., Smith H. (1973). The synthesis and stability of ribosomal RNA in blue-green algae. Eur. J. Biochem. 36, 280–285. doi: 10.1111/j.1432-1033.1973.tb02911.x, PMID: PubMed DOI

Grimm G. W., Schlee M., Komarova N. Y., Volkov R. A., Hemleben V. (2005). “Low-level taxonomy and intrageneric evolutionary trends in higher plants,” in From Plant Taxonomy to Evolutionary Biology. Nova Acta Leopoldina NF, Vol. 92, No. 342. eds. Endress P. K., Lüttge U., Parthier B. (Stuttgart: Wissenschaftl. Verlagsges. mbH; ), 129–145.

Grossmann K., Friedrich H., Seitz U. (1980). Purification and characterization of chromatin-bound DNA-dependent RNA polymerase-I from parsley (Petroselinum crispum) - influence of nucleoside triphosphates. Biochem. J. 191, 165–171. doi: 10.1042/bj1910165, PMID: PubMed DOI PMC

Grossmann K., Seitz U., Seitz H. U. (1979). Transcription and release of RNA in isolated nuclei from parsley cells. Z. Naturforsch. C. J. Biosci. 34, 431–435. doi: 10.1515/znc-1979-5-619 DOI

Gruendler P., Unfried I., Pointner R., Schweizer D. (1989). Nucleotide sequence of the 25S-18S ribosomal gene spacer from Arabidopsis thaliana. Nucl. Acids Res. 17, 6395–6396. doi: 10.1093/nar/17.15.6395, PMID: PubMed DOI PMC

Grummt I., Sorbaz H., Hofmann A., Roth E. (1985). Spacer sequences downstream of the 28S RNA coding region are part of the mouse rDNA transcription unit. Nucl. Acids Res. 13, 2293–2304. doi: 10.1093/nar/13.7.2293, PMID: PubMed DOI PMC

Handa H., Kanamori H., Tanaka T., Murata K., Kobayashi F., Robinson S. J., et al. . (2018). Structural features of two major nucleolar organizer regions (NORs), nor-B1 and nor-B2, and chromosome-specific rRNA gene expression in wheat. Plant J. 96, 1148–1159. doi: 10.1111/tpj.14094, PMID: PubMed DOI

Hartley M. R., Ellis R. J. (1973). Ribonucleic acid synthesis in chloroplasts. Biochem. J. 134, 249–262. doi: 10.1042/bj1340249, PMID: PubMed DOI PMC

Hemleben V. (1972). Untersuchungen zur Biosynthese und Funktion von Nucleinsäuren in höheren Pflanzen. Habilitation, University of Tübingen.

Hemleben V., Ermisch N., Kimmich D., Leber B., Peter G. (1975). Studies on fate of homologous DNA applied to seedlings of Matthiola incana. Eur. J. Biochem. 56, 403–411. doi: 10.1111/j.1432-1033.1975.tb02246.x PubMed DOI

Hemleben V., Grierson D. (1978). Evidence that in higher plants the 25S and 18S rRNA genes are not interspersed with genes for 5S rRNA. Chromosoma 65, 353–358. doi: 10.1007/Bf00286414 DOI

Hemleben V., Grierson D., Dertmann H. (1977). Use of equilibrium centrifugation in actinomycin cesium chloride for purification of ribosomal DNA. Plant Sci. Lett. 9, 129–135. doi: 10.1016/0304-4211(77)90090-6 DOI

Hemleben V., Kovarik A., Torres R. A., Volkov R. A., Beridze T. (2007). Plant highly repeated satellite DNA: molecular evolution, distribution and use for identification of hybrids. Syst. Biodivers. 5, 277–289. doi: 10.1017/S147720000700240X DOI

Hemleben V., Werts D. (1988). Sequence organization and putative regulatory elements in the 5S rRNA genes of 2 higher plants (Vigna radiata and Matthiola incana). Gene 62, 165–169. doi: 10.1016/0378-1119(88)90591-4, PMID: PubMed DOI

Hemleben V., Zentgraf U. (1994). “Structural organisation and regulation of transcription by RNA polymerase I of plant nuclear ribosomal genes,” in Plant Promoters and Transcription Factors. ed. Nover L. (Berlin/Heidelberg: Springer-Verlag; ), 3–24. PubMed

Hemleben-Vielhaben V. (1966). Characterization of rapidly labelled nucleic acids in tissues of plant seedlings. Z. Naturforsch. Pt. B. 21, 983–992. doi: 10.1515/znb-1966-1016 DOI

Hoang P. T. N., Fiebig A., Novák P., Macas J., Cao H. X., Stepanenko A., et al. . (2020). Chromosome-scale genome assembly for the duckweed Spirodela intermedia, integrating cytogenetic maps, PacBio and Oxford Nanopore libraries. Sci. Rep. 10:19230. doi: 10.1038/s41598-020-75728-9, PMID: PubMed DOI PMC

Ingle J., Timmis J. N., Sinclair J. (1975). The relationship between satellite deoxyribonucleic acid, ribosomal ribonucleic acid gene redundancy, and genome size in plants. Plant Physiol. 55, 496–501. doi: 10.1104/pp.55.3.496, PMID: PubMed DOI PMC

Ishchenko O. O., Bednarska O. I., Panchuk I. I. (2021). Application of 5S ribosomal DNA for molecular taxonomy of subtribe Loliinae (Poaceae). Cytol. Genet. 55, 10–18. doi: 10.3103/S0095452721010096 DOI

Ishchenko O. O., Mel’nyk V. М., Parnikoza І. Y., Budzhak V. V., Panchuk І. І., Kunakh V. А., et al. . (2020). Molecular organization of 5S ribosomal DNA and taxonomic status of Avenella flexuosa (L.) Drejer (Poaceae). Cytol. Genet. 54, 505–513. doi: 10.3103/S0095452720060055 DOI

Ishchenko O. O., Panchuk І. І., Andreev І. O., Kunakh V. A., Volkov R. A. (2018). Molecular organization of 5S ribosomal DNА of Deschampsia antarctica. Cytol. Genet. 52, 416–421. doi: 10.3103/S0095452718060105 DOI

Jo S. H., Koo D. H., Kim J. F., Hu C.-G., Lee S., Yang T. J., et al. . (2009). Evolution of ribosomal DNA-derived satellite repeat in tomato genome. BMC Plant Biol. 9:42. doi: 10.1186/1471-2229-9-42, PMID: PubMed DOI PMC

Jobst J., King K., Hemleben V. (1998). Molecular evolution of the internal transcribed spacers (ITS1 and ITS2) and phylogenetic relationships among species of the family Cucurbitaceae. Mol. Phylogenetics Evol. 9, 204–219. doi: 10.1006/mpev.1997.0465, PMID: PubMed DOI

Jung H., Winefield C., Bombarelym A., Prentis P., Waterhouse P. (2019). Tools and strategies for long-read sequencing and de novo assembly of plant genomes. Trends Plant Sci. 24, 700–724. doi: 10.1016/j.tplants.2019.05.003, PMID: PubMed DOI

Kalendar R., Tanskanen J., Chang W., Antonius K., Sela H., Peleg O., et al. . (2008). Cassandra retrotransposons carry independently transcribed 5S RNA. Proc. Natl. Acad. Sci. U. S. A. 105, 5833–5838. doi: 10.1073/pnas.0709698105, PMID: PubMed DOI PMC

King K., Torres R. A., Zentgraf U., Hemleben V. (1993). Molecular evolution of the intergenic spacer in the nuclear ribosoma RNA genes of Cucurbitaceae. J. Mol. Evol. 36, 144–152. doi: 10.1007/Bf00166250, PMID: PubMed DOI

Kirov I., Gilyok M., Knyazev A., Fesenko I. (2018). Pilot satellitome analysis of the model plant, Physcomitrella patens, revealed a transcribed and high-copy IGS related tandem repeat. Comp. Cytogenet. 12, 493–513. doi: 10.3897/CompCytogen.v12i4.31015, PMID: PubMed DOI PMC

Komarova N. Y., Grabe T., Huigen D. J., Hemleben V., Volkov R. A. (2004). Organization, differential expression and methylation of rDNA in artificial Solanum allopolyploids. Plant Mol. Biol. 56, 439–463. doi: 10.1007/s11103-004-4678-x, PMID: PubMed DOI

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. doi: 10.1007/s00606-008-0091-2 DOI

Koukalova B., Fojtova M., Lim K. Y., Fulnecek J., Leitch A. R., Kovarik A. (2005). Dedifferentiation of tobacco cells is associated with ribosomal RNA gene hypomethylation, increased transcription, and chromatin alterations. Plant Physiol. 139, 275–286. doi: 10.1104/pp.105.061788, PMID: PubMed DOI PMC

Kovarik A., Dadejova M., Lim Y. K., Chase M. W., Clarkson J. J., Knapp S., et al. . (2008). Evolution of rDNA in Nicotiana allopolyploids: a potential link between rDNA homogenization and epigenetics. Ann. Bot. 101, 815–823. doi: 10.1093/aob/mcn019, PMID: PubMed DOI PMC

Kovarik A., Fajkus J., Koukalova B., Bezdek M. (1996). Species-specific evolution of telomeric and rDNA repeats in the tobacco composite genome. Theor. Appl. Genet. 92, 1108–1111. doi: 10.1007/BF00224057, PMID: PubMed DOI

Kovarik A., Matyasek R., Lim K. Y., Skalicka K., Koukalova B., Knapp S., et al. . (2004). Concerted evolution of 18-5.8-26S rDNA repeats in Nicotiana allotetraploids. Biol. J. Linn. Soc. 82, 615–625. doi: 10.1111/j.1095-8312.2004.00345.x DOI

Layat E., Sáez-Vásquez J., Tourmente S. (2012). Regulation of pol I-transcribed 45S rDNA and pol III-transcribed 5S rDNA in Arabidopsis. Plant Cell Physiol. 53, 267–276. doi: 10.1093/pcp/pcr177, PMID: PubMed DOI

Leaver C. J., Key J. L. (1970). Ribosomal RNA synthesis in plants. J. Mol. Biol. 49, 671–680. doi: 10.1016/0022-2836(70)90290-1, PMID: PubMed DOI

Leber B., Hemleben V. (1979). Structure of plant nuclear and ribosomal DNA containing chromatin. Nucl. Acids Res. 7, 1263–1282. doi: 10.1093/nar/7.5.1263, PMID: PubMed DOI PMC

Leweke B., Hemleben V. (1982). Organization of rDNA in chromatin: plants. Cell Nucleus 11, 225–253.

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, 161–172. doi: 10.1007/s004120050424, PMID: PubMed DOI

Lim K. Y., Kovarik A., Matyasek R., Chase M. W., Clarkson J. J., Grandbastien M. A., et al. . (2007). Sequence of events leading to near complete genome turnover in allopolyploid Nicotiana within five million years. New Phytol. 175, 756–763. doi: 10.1111/j.1469-8137.2007.02121.x, PMID: PubMed DOI

Lim K. Y., Matyasek R., Kovarik A., Leitch A. (2004a). Genome evolution in allotetraploid Nicotiana. Biol. J. Linn. Soc. 82, 599–606. doi: 10.1111/j.1095-8312.2004.00344.x DOI

Lim K. Y., Skalicka K., Koukalova B., Volkov R. A., Matyasek R., Hemleben V., et al. . (2004b). Dynamic changes in the distribution of a satellite homologous to intergenic 26-18S rDNA spacer in the evolution of Nicotiana. Genetics 166, 1935–1946. doi: 10.1534/genetics.166.4.1935, PMID: PubMed DOI PMC

Lin C. Y., Chen Y. M., Guilfoyle T. J., Key J. L. (1976). Selective modulation of RNA polymerase I activity during growth transitions in the soybean seedling. Plant Physiol. 58, 614–617. doi: 10.1104/pp.58.5.614 PubMed DOI PMC

Loening U. E. (1969). The determination of molecular weight of ribonucleic acid by polyacrylamide-gel electrophoresis - effects of changes in conformation. Biochem. J. 113, 131–138. doi: 10.1042/bj1130131, PMID: PubMed DOI PMC

Lunerova J., Renny-Byfield S., Matyasek R., Leitch A., Kovarik A. (2017). Concerted evolution rapidly eliminates sequence variation in rDNA coding regions but not in intergenic spacers in Nicotiana tabacum allotetraploid. Plant Syst. Evol. 303, 1043–1060. doi: 10.1007/s00606-017-1442-7 DOI

Macas J., Navratilova A., Meszaros T. (2003). Sequence subfamilies of satellite repeats related to rDNA intergenic spacer are differentially amplified on Vicia sativa chromosomes. Chromosoma 112, 152–158. doi: 10.1007/s00412-003-0255-3, PMID: PubMed DOI

Manoharlal R., Saiprasad G. V. S., Kovarik A. (2019). “Smoking and tobacco use,” in New Research on Tobacco. ed. Dreher U. (New York: Nova Science Publishers Inc; ), 23–82.

Marazia T., Barsanti P., Maggini F. (1980). Individual quantitative rDNA variation in 3 species of the Cucurbitaceae family. Biochem. Genet. 18, 509–517. doi: 10.1007/Bf00484398, PMID: PubMed DOI

Matsuda K., Siegel A. (1967). Hybridization of plant ribosomal RNA to DNA - isolation of a DNA component rich in ribosomal RNA cistrons. Proc. Natl. Acad. Sci. U. S. A. 58, 673–680. doi: 10.1073/pnas.58.2.673, PMID: PubMed DOI PMC

Matyasek R., Dobesova E., Huska D., Jezkova I., Soltis P. S., Soltis D. E., et al. . (2016). Interpopulation hybridization generates meiotically stable rDNA epigenetic variants in allotetraploid Tragopogon mirus. Plant J. 85, 362–377. doi: 10.1111/tpj.13110, PMID: PubMed DOI

Matyasek R., Lim K. Y., Kovarik A., Leitch A. R. (2003). Ribosomal DNA evolution and gene conversion in Nicotiana rustica. Heredity 91, 268–275. doi: 10.1038/sj.hdy.6800333, PMID: PubMed DOI

McClintock B. (1934). The relationship of a particular crhomosomal element to the development of the nucleoli in Zea mays. Z. Zellforsch Microsk. 21, 294–398. doi: 10.1007/BF00374060 DOI

Michael T., Bryant D., Gutierrez R., Borisjuk N., Chu P., Zhang H., et al. . (2017). Comprehensive definitions of genome features in Spirodela polyrhiza by high-depth physical mapping and short-read DNA sequencing strategies. Plant J. 89, 617–635. doi: 10.1111/tpj.13400, PMID: PubMed DOI

Michael T. P., Van Buren R. (2020). Building near-complete plant genomes. Curr. Opin. Plant Biol. 54, 26–33. doi: 10.1016/j.pbi.2019.12.009, PMID: PubMed DOI

Miroshnichenko G. P., Borisjuk N. V., Volkov R. A. (1989). Organization of rDNA repeat units in the Solanaceae sexual and parasexual hybrids. Biochemistry 54, 669–675.

Mohannath G., Pontvianne F., Pikaard C. S. (2016). Chromosome-specific selective nucleolus organizer inactivation in Arabisopsis is a chromosome position-effect phenomenon. Proc. Natl. Acad. Sci. U. S. A. 113, 13426–13431. doi: 10.1073/pnas.1608140113, PMID: PubMed DOI PMC

Moss T. (2004). At the crossroads of growth control: making ribosomal RNA. Curr. Opin. Genet. Dev. 14, 210–217. doi: 10.1016/j.gde.2004.02.005, PMID: PubMed DOI

Nagl W., Ehrendorfer F., Hemleben V. (1979). “Genome and Chromatin: Organization, Evolution and Function,” in Plant Systematics and Evolution. 2nd Edn. eds. Nagl W., Ehrendorfer F., Hemleben V. (Wien: Springer Verlag; ).

Navashin M. (1934). Chromosomal alterations caused by hybridisation and their bearing upon certain genetic problems. Cytologia 5, 169–203.

Nieto Feliner G., Rossello J. A. (2012). “Concerted evolution of multigene families and homeologous recombination,” in Plant Genome Diversity. ed. Wendel J. F. (Wien: Springer-Verlag; ), 171–194.

Noller H. F., Kop J., Wheaton V., Brosius J., Gutell R. R., Kopylov A. M., et al. . (1981). Secondary structure model for 23S ribosomal RNA. Nucl. Acids Res. 9, 6167–6189. doi: 10.1093/nar/9.22.6167, PMID: PubMed DOI PMC

Pikaard C. S., Reeder R. H. (1988). Sequence elements essential for function of the Xenopus laevis ribosomal DNA enhancers. Mol. Cell. Biol. 8, 4282–4288. doi: 10.1128/Mcb.8.10.4282, PMID: PubMed DOI PMC

Poczai P., Hyvonen J. (2010). Nuclear ribosomal spacer regions in plant phylogenetics: problems and prospects. Mol. Biol. Rep. 37, 1897–1912. doi: 10.1007/s11033-009-9630-3, PMID: PubMed DOI

Pontvianne F., Abou-Ellail M., Douet J., Comella P., Matia I., Chandrasekhara C., et al. . (2010). Nucleolin is required for DNA methylation state and the expression of rRNA gene variants in Arabidopsis thaliana. PLoS Genet. 6:e1001225. doi: 10.1371/journal.pgen.1001225, PMID: PubMed DOI PMC

Quast C., Pruesse E., Yilmaz P., Gerken J., Schweer T., Yarza P., et al. . (2012). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucl. Acids Res. 41, D590–D596. doi: 10.1093/nar/gks1219, PMID: PubMed DOI PMC

Rabanal F. A., Mandáková T., Soto-Jiménez L. M., Greenhalgh R., Parrott D. L., Lutzmayer S., et al. . (2017). Epistatic and allelic interactions control expression of ribosomal RNA gene clusters in Arabidopsis thaliana. Genome Biol. 18:75. doi: 10.1186/s13059-017-1209-z, PMID: PubMed DOI PMC

Rathgeber J., Capesius I. (1990). Nucleotide sequence of the intergenic spacer and the 18S ribosomal-RNA gene from mustard (Sinapis alba). Nucl. Acids Res. 18, 1288–1288. doi: 10.1093/nar/18.5.1288, PMID: PubMed DOI PMC

Ribeiro T., Dos Santos K. G., Richard M. M., Sévignac M., Thareau V., Geffroy V., et al. . (2017). Evolutionary dynamics of satellite DNA repeats from Phaseolus beans. Protoplasma 254, 791–801. doi: 10.1007/s00709-016-0993-8, PMID: PubMed DOI

Robicheau B. M., Susko E., Harrigan A. M., Snyder M. (2017). Ribosomal RNA genes contribute to the formation of pseudogenes and junk DNA in the human genome. Genome Biol. Evol. 9, 380–397. doi: 10.1093/gbe/evw307, PMID: PubMed DOI PMC

Rogers S. O., Bendich A. J. (1987). Ribosomal RNA genes in plants: variability in copy number and in the intergenic spacer. Plant Mol. Biol. 9, 509–520. doi: 10.1007/BF00015882, PMID: PubMed DOI

Rogers S. O., Honda S., Bendich A. J. (1986). Variation in the ribosomal RNA genes among individuals of Vicia faba. Plant Mol. Biol. 6, 339–345. doi: 10.1007/Bf00034941, PMID: PubMed DOI

Röser M., Winterfeld G., Grebenstein B., Hemleben V. (2001). Molecular diversity and physical mapping of 5S rDNA in wild, and cultivated oat grasses (Poaceae: Aveneae). Mol. Phylogenet. Evol. 21, 198–217. doi: 10.1006/mpev.2001.1003, PMID: PubMed DOI

Sáez-Vásquez J., Delseny M. (2019). Ribosome biogenesis in plants: from functional 45S ribosomal DNA organization to ribosome assembly factors. Plant Cell 31, 1945–1967. doi: 10.1105/tpc.18.00874, PMID: PubMed DOI PMC

Sáez-Vásquez J., Pikaard C. S. (2000). RNA polymerase I holoenzyme-promoter interactions. J. Biol. Chem. 275, 37173–37180. doi: 10.1074/jbc.M006057200 PubMed DOI

Salim D., Bradford W. D., Freeland A., Cady G., Wang J., Pruitt S. C., et al. . (2017). DNA replication stress restricts ribosomal DNA copy number. PLoS Genet. 13:e1007006. doi: 10.1371/journal.pgen.1007006, PMID: PubMed DOI PMC

Sanger F., Nicklen S., Coulson A. R. (1977). DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. U. S. A. 74, 5463–5467. doi: 10.1073/pnas.74.12.5463, PMID: PubMed DOI PMC

Sardana R., Odell M., Flavell R. (1993). Correlation between the size of the intergenic regulatory region, the status of cytosine methylation of ribosomal-RNA genes and nucleolar expression in wheat. Mol. Gen. Genet. 236, 155–162. doi: 10.1007/Bf00277107, PMID: PubMed DOI

Schiebel K., Hemleben V. (1989). Nucleotide sequence of the 18S-25S spacer region from rDNA of mung bean. Nucl. Acids Res. 17, 2852–2852. doi: 10.1093/nar/17.7.2852, PMID: PubMed DOI PMC

Schlee M., Göker M., Grimm G. W., Hemleben V. (2011). Genetic patterns in the Lathyrus pannonicus complex (Fabaceae) reflect ecological differentiation rather than biogeography and traditional subspecific division. Biol. J. Linn. Soc. 165, 402–421. doi: 10.1111/j.1095-8339.2011.01125.x DOI

Schlotterer C., Tautz D. (1994). Chromosomal homogeneity of Drosophila ribosomal DNA arrays suggests intrachromosomal exchanges drive concerted evolution. Curr. Biol. 4, 777–783. doi: 10.1016/S0960-9822(00)00175-5, PMID: PubMed DOI

Schweizer G., Borisjuk N., Borisjuk L., Stadler M., Stelzer T., Schilde L., et al. . (1993). Molecular analysis of highly repeated genome fractions in Solanum and their use as markers for the characterization of species and cultivars. Theor. Appl. Genet. 85-85, 801–808. doi: 10.1007/Bf00225022, PMID: PubMed DOI

Scoles C. J., Gill B. S. Z., Xin Y., Clarke B. C., McIntyre C. L., Chapman C., et al. . (1988). Frequent duplication and deletion events in the 5S RNA genes and the associated spacer regions of the Triticeae. Plant Syst. Evol. 160, 105–122.

Seitz U., Seitz U. (1973). Biosynthetic pathway of ribosomal-RNA in blue-green algae (Anacystis nidulans). Archiv fur Mikrobiologie. 90, 213–222. doi: 10.1007/Bf00424973 PubMed DOI

Seitz U., Seitz U. (1979). Molecular weight of rRNA precursor molecules and their processing in higher plant cells. Z. Naturforsch. C. J. Biosci. 34, 253–258. doi: 10.1515/znc-1979-3-416, PMID: PubMed DOI

Selig C., Wolf M., Müller T., Dandekar T., Schultz J. (2008). The ITS2 database II: homology modelling RNA structure for molecular systematics. Nucl. Acids Res. 36, D377–D380. doi: 10.1093/nar/gkm827, PMID: PubMed DOI PMC

Sims J., Sestini G., Elgert C., von Haeseler A., Schlögelhofer P. (2021). Sequencing of the Arabidopsis NOR2 reveals its distinct organization and tissue-specific rRNA ribosomal variants. Nat. Commun. 12, 387. doi: 10.1038/s41467-020-20728-6, PMID: PubMed DOI PMC

Soltis D. E., Soltis P. S. (2016). Mobilizing and integrating big data in studies of spatial and phylogenetic patterns of biodiversity. Plant Divers. 38, 264–270. doi: 10.1016/0022-2836(88)90353-1, PMID: PubMed DOI PMC

Souza G., Marques A., Ribeiro T., Dantas L. G., Speranza P., Guerra M., et al. . (2019). Allopolyploidy and extensive rDNA site variation underlie rapid karyotype evolution in Nothoscordum section Nothoscordum (Amaryllidaceae). Bot. J. Linn. Soc. 190, 215–228. doi: 10.1093/botlinnean/boz008 DOI

Szymanski M., Specht T., Barciszewska M. Z., Barciszewski J., Erdmann V. A. (1998). 5S rRNA Data Bank. Nucl. Acids Res. 26, 156–159. doi: 10.1093/nar/26.1.156, PMID: PubMed DOI PMC

Thompson W. F., Flavell R. B. (1988). DNAse-I sensitivity of ribosomal RNA genes in chromatin and nucleolar dominance in wheat. J. Mol. Biol. 204, 535–548. doi: 10.1016/0022-2836(88)90353-1, PMID: PubMed DOI

Tomecki R., Sikorski P. J., Zakrzewska-Placzek M. (2017). Comparison of preribosomal RNA processing pathways in yeast, plant and human cells - focus on coordinated action of endo- and exoribonucleases. FEBS Lett. 591, 1801–1850. doi: 10.1002/1873-3468.12682, PMID: PubMed DOI

Torres R. A., Zentgraf U., Hemleben V. (1989). Species and genus specificity of the intergenic spacer (IGS) in the ribosoma RNA genes of Cucurbitaceae. Z. Naturforsch. C. J. Biosci. 44, 1029–1034. doi: 10.1515/znc-1989-11-1224, PMID: PubMed DOI

Torres-Ruiz R. A., Hemleben V. (1994). Pattern and degree of methylation in ribosomal RNA genes of Cucurbita pepo L. Plant Mol. Biol. 26, 1167–1179. doi: 10.1007/Bf00040697, PMID: PubMed DOI

Tulpová Y. O., Kovařík A., Toegelová H., Navrátilová P., Kapustová V., Hřibová E., et al. . (2020). Anatomy, transcription dynamics and evolution of wheat ribosomal RNA loci deciphered by a multi-omics approach. BioRxriv [Preprint]. doi: 10.1101/2020.08.29.273623 PubMed DOI

Tynkevich Y. O., Volkov R. A. (2014). Structural organization of 5S ribosomal DNA in Rosa rugosa. Cytol. Genet. 48, 1–6. doi: 10.3103/S0095452714010095, PMID: PubMed DOI

Tynkevich Y. O., Volkov R. A. (2019). 5S ribosomal DNA of distantly related Quercus species: molecular organization and taxonomic application. Cytol. Genet. 53, 459–466. doi: 10.3103/S0095452719060100 DOI

Unfried K., Schiebel K., Hemleben V. (1991). Subrepeats of rDNA intergenic spacer present as prominent independent satellite DNA in Vigna radiata but not in Vigna angularis. Gene 99, 63–68. doi: 10.1016/0378-1119(91)90034-9, PMID: PubMed DOI

Volkov R. A., Bachmair A., Panchuk I. I., Kostyshyn S. S., Schweizer D. (1999a). 25S-18S rDNA intergenic spacer of Nicotiana sylvestris (Solanaceae): primary and secondary structure analysis. Plant Syst. Evol. 218, 89–97. doi: 10.1007/bf01087037 DOI

Volkov R. A., Borisjuk N. V., Kostishin S. S., Panchuk I. I. (1991). Variability of rRNA genes in Nicotiana correlates with the chromosome reconstruction. Mol. Biol. 25, 442–450.

Volkov R. A., Borisjuk N. V., Panchuk I. I., Schweizer D., Hemleben V. (1999b). Elimination and rearrangement of parental rDNA in the allotetraploid Nicotiana tabacum. Mol. Biol. Evol. 16, 311–320. doi: 10.1093/oxfordjournals.molbev.a026112, PMID: PubMed DOI

Volkov R. A., Komarova N. Y., Hemleben V. (2007). Ribosomal DNA in plant hybrids: inheritance, rearrangement, expression. Syst. Biodivers. 5, 261–276. doi: 10.1017/S1477200007002447 DOI

Volkov R. A., Komarova N. Y., Panchuk I. I., Hemleben V. (2003). Molecular evolution of rDNA external transcribed spacer and phylogeny of sect. Petota (genus Solanum). Mol. Phylogenetics Evol. 29, 187–202. doi: 10.1016/s1055-7903(03)00092-7, PMID: PubMed DOI

Volkov R., Kostishin S., Ehrendorfer E., Schweizer D. (1996). Molecular organization and evolution of the external transcribed rDNA spacer region in two diploid relatives of Nicotiana tabacum (Solanaceae). Plant Syst. Evol. 201, 117–129. doi: 10.1007/Bf00989055 DOI

Volkov R. A., Kozeretska I. A., Kyryachenko S. S., Andreev I. O., Maidanyuk D. N., Parnikoza I. Y., et al. . (2010). Molecular evolution and variability of ITS1–ITS2 in populations of Deschampsia antarctica from two regions of the maritime Antarctic. Pol. Sci. 4, 469–478. doi: 10.1016/j.polar.2010.04.011 DOI

Volkov R. A., Medina F. J., Zentgraf U., Hemleben V. (2004). “Molecular cell biology: organization and molecular evolution of rDNA, nucleolar dominance and nucleolus structure,” in Progress in Botany. Vol. 65. eds. Esser K., Lüttge U., Beyschlag W., Murata J. (Berlin, Heidelberg, New York: Springer Verlag; ), 106–146.

Volkov R. A., Panchuk I. I., Borisjuk N. V., Maluszynska J., Hemleben V. (2017). Evolutional dynamics of 45S and 5S ribosomal DNA in ancient allohexaploid Atropa belladonna. BMC Plant Biol. 17, 21–24. doi: 10.1186/s12870-017-0978-6, PMID: PubMed DOI PMC

Volkov R. A., Zanke C., Panchuk I. I., Hemleben V. (2001). Molecular evolution of 5S rDNA of Solanum species (sect. Petota): application for molecular phylogeny and breeding. Theor. Appl. Genet. 103, 1273–1282. doi: 10.1007/s001220100670 DOI

Wang W., Wan T., Becher H., Kuderova A., Leitch I. J., Garcia S., et al. . (2019). Remarkable variation of ribosomal DNA organization and copy number in gnetophytes, a distinct lineage of gymnosperms. Ann. Bot. 123, 767–781. doi: 10.1093/aob/mcy172, PMID: PubMed DOI PMC

Weis B. L., Kovacevic J., Missbach S., Schleiff E. (2015). Plant-specific features of ribosome biogenesis. Trends Plant Sci. 20, 729–740. doi: 10.1016/j.tplants.2015.07.003, PMID: PubMed DOI

Wenzel W., Hemleben V. (1982a). A comparative study of genomes in angiosperms. Plant Syst. Evol. 139, 209–227. doi: 10.1007/Bf00989326 DOI

Wenzel W., Hemleben V. (1982b). DNA-sequence organization and RNA complexity in Matthiola incana (Brassicaceae). Plant Syst. Evol. 140, 75–86. doi: 10.1007/Bf02409898 DOI

Wicke S., Costa A., Munoz J., Quandt D. (2011). Restless 5S: the re-arrangement(s) and evolution of the nuclear ribosomal DNA in land plants. Mol. Phylogenet. Evol. 61, 321–332. doi: 10.1016/j.ympev.2011.06.023, PMID: PubMed DOI

Yan Q., Zhu C. M., Guang S. H., Feng X. Z. (2019). The functions of non-coding RNAs in rRNA regulation. Front. Genet. 10:290. doi: 10.3389/fgene.2019.00290, PMID: PubMed DOI PMC

Yokota Y., Kawata T., Iida Y., Kato A., Tanifuji S. (1989). Nucleotide sequences of the 5.8S rRNA gene and internal transcribed spacer regions in carrot and broad bean ribosomal DNA. J. Mol. Evol. 29, 294–301. doi: 10.1007/Bf02103617, PMID: PubMed DOI

Zakrzewska-Placzek M., Souret F. F., Sobczyk G. J., Green P. J., Kufel J. (2010). Arabidopsis thaliana XRN2 is required for primary cleavage in the pre-ribosomal RNA. Nucl. Acids Res. 38, 4487–4502. doi: 10.1093/nar/gkq172, PMID: PubMed DOI 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. Nucl. Acids Res. 20, 3685–3691. doi: 10.1093/nar/20.14.3685, PMID: PubMed DOI PMC

Zentgraf U., Hemleben V. (1993). Nuclear proteins interact with RNA polymerase-I promoter and repeated elements of the 5' external transcribed spacer of the rDNA of cucumber in a single-stranded stage. Plant Mol. Biol. 22, 1153–1156. doi: 10.1007/Bf00028984, PMID: PubMed DOI

Zimmer E. A., Martin S. L., Beverley S. M., Kan Y. W., Wilson A. C. (1980). Rapid duplication and loss of genes-coding for the alpha-chains of hemoglobin. Proc. Natl. Acad. Sci. U. S. A. 77, 2158–2162. doi: 10.1073/pnas.77.4.2158, PMID: PubMed DOI PMC

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