skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: The fate of 35S rRNA genes in the allotetraploid grass Brachypodium hybridum

Abstract

Nucleolar dominance (ND) consists of the reversible silencing of 35S/45S rDNA loci inherited from one of the ancestors of an allopolyploid. The molecular mechanisms by which one ancestral rDNA set is selected for silencing remain unclear. We applied a combination of molecular (Southern blot hybridization and reverse-transcription cleaved amplified polymorphic sequence analysis), genomic (analysis of variants) and cytogenetic (fluorescence in situ hybridization) approaches to study the structure, expression and epigenetic landscape of 35S rDNA in an allotetraploid grass that exhibits ND, Brachypodium hybridum (genome composition DDSS), and its putative progenitors, Brachypodium distachyon (DD) and Brachypodium stacei (SS). In progenitor genomes, B. stacei showed a higher intragenomic heterogeneity of rDNA compared with B. distachyon. In all studied accessions of B. hybridum, there was a reduction in the copy number of S homoeologues, which was accompanied by their inactive transcriptional status. The involvement of DNA methylation in CG and CHG contexts in the silencing of the S-genome rDNA loci was revealed. In the B. hybridum allotetraploid, ND is stabilized towards the D-genome units, irrespective of the polyphyletic origin of the species, and does not seem to be influenced by homoeologous 35S rDNA ratios and developmental stage.

Authors:
 [1];  [2];  [1];  [3];  [4];  [5];  [6];  [1]
  1. Univ. of Silesia in Katowice (Poland)
  2. Academy of Sciences of the Czech Republic, Brno (Czech Republic)
  3. Tekirdag Namik Kemal Univ., Tekirdag (Turkey)
  4. Tekirdag Anatolian High School, Tekirdag (Turkey)
  5. USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
  6. USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); Polish National Science Centre (NCN); Czech Science Foundation
OSTI Identifier:
1713233
Grant/Contract Number:  
AC02-05CH11231; 2018/31/B/NZ3/01761; 2018/02/X/NZ3/03518; 20-14133J
Resource Type:
Accepted Manuscript
Journal Name:
The Plant Journal
Additional Journal Information:
Journal Volume: 103; Journal Issue: 5; Journal ID: ISSN 0960-7412
Publisher:
Society for Experimental Biology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 35S rDNA evolution; 35S rRNA gene expression; allopolyploidy; Bracypodium hybridum; nucleolar dominance

Citation Formats

Borowska-Zuchowska, Natalia, Kovarik, Ales, Robaszkiewicz, Ewa, Tuna, Metin, Tuna, Gulsemin Savas, Gordon, Sean, Vogel, John P, and Hasterok, Robert. The fate of 35S rRNA genes in the allotetraploid grass Brachypodium hybridum. United States: N. p., 2020. Web. doi:10.1111/tpj.14869.
Borowska-Zuchowska, Natalia, Kovarik, Ales, Robaszkiewicz, Ewa, Tuna, Metin, Tuna, Gulsemin Savas, Gordon, Sean, Vogel, John P, & Hasterok, Robert. The fate of 35S rRNA genes in the allotetraploid grass Brachypodium hybridum. United States. doi:10.1111/tpj.14869.
Borowska-Zuchowska, Natalia, Kovarik, Ales, Robaszkiewicz, Ewa, Tuna, Metin, Tuna, Gulsemin Savas, Gordon, Sean, Vogel, John P, and Hasterok, Robert. Fri . "The fate of 35S rRNA genes in the allotetraploid grass Brachypodium hybridum". United States. doi:10.1111/tpj.14869. https://www.osti.gov/servlets/purl/1713233.
@article{osti_1713233,
title = {The fate of 35S rRNA genes in the allotetraploid grass Brachypodium hybridum},
author = {Borowska-Zuchowska, Natalia and Kovarik, Ales and Robaszkiewicz, Ewa and Tuna, Metin and Tuna, Gulsemin Savas and Gordon, Sean and Vogel, John P and Hasterok, Robert},
abstractNote = {Nucleolar dominance (ND) consists of the reversible silencing of 35S/45S rDNA loci inherited from one of the ancestors of an allopolyploid. The molecular mechanisms by which one ancestral rDNA set is selected for silencing remain unclear. We applied a combination of molecular (Southern blot hybridization and reverse-transcription cleaved amplified polymorphic sequence analysis), genomic (analysis of variants) and cytogenetic (fluorescence in situ hybridization) approaches to study the structure, expression and epigenetic landscape of 35S rDNA in an allotetraploid grass that exhibits ND, Brachypodium hybridum (genome composition DDSS), and its putative progenitors, Brachypodium distachyon (DD) and Brachypodium stacei (SS). In progenitor genomes, B. stacei showed a higher intragenomic heterogeneity of rDNA compared with B. distachyon. In all studied accessions of B. hybridum, there was a reduction in the copy number of S homoeologues, which was accompanied by their inactive transcriptional status. The involvement of DNA methylation in CG and CHG contexts in the silencing of the S-genome rDNA loci was revealed. In the B. hybridum allotetraploid, ND is stabilized towards the D-genome units, irrespective of the polyphyletic origin of the species, and does not seem to be influenced by homoeologous 35S rDNA ratios and developmental stage.},
doi = {10.1111/tpj.14869},
journal = {The Plant Journal},
number = 5,
volume = 103,
place = {United States},
year = {2020},
month = {7}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Save / Share:

Works referenced in this record:

Rapid Concerted Evolution of Nuclear Ribosomal DNA in Two Tragopogon Allopolyploids of Recent and Recurrent Origin
journal, January 2005


The developmental stage of inactivation of rye origin rRNA genes in the embryo and endosperm of wheat � rye F1 hybrids
journal, May 1995

  • Castilho, A.; Queiroz, A.; Neves, N.
  • Chromosome Research, Vol. 3, Issue 3
  • DOI: 10.1007/BF00710710

‘Nucleolar dominance’ as observed in barley translocation lines with specifically reconstructed SAT chromosomes
journal, November 1979

  • Nicoloff, H.; Anastassova-Kristeva, M.; Rieger, R.
  • Theoretical and Applied Genetics, Vol. 55, Issue 6
  • DOI: 10.1007/BF00265358

Extra views on RNA-dependent DNA methylation and MBD6-dependent heterochromatin formation in nucleolar dominance
journal, May 2010

  • Costa-Nunes, Pedro; Pontes, Olga; Preuss, Sasha B.
  • Nucleus, Vol. 1, Issue 3
  • DOI: 10.4161/nucl.11741

BAC 'landing' on chromosomes of Brachypodium distachyon for comparative genome alignment
journal, January 2007


Ribosomal DNA in plant hybrids: Inheritance, rearrangement, expression
journal, August 2007

  • Volkov, Roman A.; Komarova, Nataliya Y.; Hemleben, Vera
  • Systematics and Biodiversity, Vol. 5, Issue 3
  • DOI: 10.1017/S1477200007002447

Evolution of rDNA in Nicotiana Allopolyploids: A Potential Link between rDNA Homogenization and Epigenetics
journal, March 2008

  • Kovarik, A.; Dadejova, M.; Lim, Y. K.
  • Annals of Botany, Vol. 101, Issue 6
  • DOI: 10.1093/aob/mcn019

rRNA gene activity and control of expression mediated by methylation and imprinting during embryo development in wheat x rye hybrids
journal, August 1995

  • Neves, N.; Heslop-Harrison, J. S.; Viegas, W.
  • Theoretical and Applied Genetics, Vol. 91, Issue 3
  • DOI: 10.1007/BF00222984

Postembryonic Establishment of Megabase-Scale Gene Silencing in Nucleolar Dominance
journal, November 2007


Epigenetic phenomena and the evolution of plant allopolyploids
journal, December 2003


Ribosomal RNA Genes Contribute to the Formation of Pseudogenes and Junk DNA in the Human Genome
journal, February 2017

  • Robicheau, Brent M.; Susko, Edward; Harrigan, Amye M.
  • Genome Biology and Evolution, Vol. 9, Issue 2
  • DOI: 10.1093/gbe/evw307

Genomic Plasticity and the Diversity of Polyploid Plants
journal, April 2008


Gene conversion events and variable degree of homogenization of rDNA loci in cultivars of Brassica napus
journal, October 2016

  • Sochorová, Jana; Coriton, Olivier; Kuderová, Alena
  • Annals of Botany, Vol. 119, Issue 1
  • DOI: 10.1093/aob/mcw187

The cytological and molecular role of DOMAINS REARRANGED METHYLTRANSFERASE3 in RNA-dependent DNA methylation of Arabidopsis thaliana
journal, January 2014


DnaSP 6: DNA Sequence Polymorphism Analysis of Large Data Sets
journal, September 2017

  • Rozas, Julio; Ferrer-Mata, Albert; Sánchez-DelBarrio, Juan Carlos
  • Molecular Biology and Evolution, Vol. 34, Issue 12
  • DOI: 10.1093/molbev/msx248

The complete nucleotide sequence of a rice 25S β rRNA gene
journal, January 1985


Ribosomal DNA heterochromatin in plants
journal, January 2005

  • Neves, N.; Delgado, M.; Silva, M.
  • Cytogenetic and Genome Research, Vol. 109, Issue 1-3
  • DOI: 10.1159/000082388

Evolution and taxonomic split of the model grass Brachypodium distachyon
journal, January 2012

  • Catalán, Pilar; Müller, Jochen; Hasterok, Robert
  • Annals of Botany, Vol. 109, Issue 2
  • DOI: 10.1093/aob/mcr294

Long-term genome diploidization in allopolyploid Nicotiana section Repandae (Solanaceae)
journal, July 2005


Chromosome identification and reconstruction of evolutionary rearrangements in Brachypodium distachyon, B. stacei and B. hybridum
journal, June 2018

  • Lusinska, Joanna; Majka, Joanna; Betekhtin, Alexander
  • Annals of Botany, Vol. 122, Issue 3
  • DOI: 10.1093/aob/mcy086

Letter to the editor
journal, January 2003


Multimegabase Silencing in Nucleolar Dominance Involves siRNA-Directed DNA Methylation and Specific Methylcytosine-Binding Proteins
journal, December 2008


Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium).
journal, January 1995

  • Wendel, J. F.; Schnabel, A.; Seelanan, T.
  • Proceedings of the National Academy of Sciences, Vol. 92, Issue 1
  • DOI: 10.1073/pnas.92.1.280

The complete nucleotide sequence of a rice 17S rRNA gene
journal, January 1984

  • Takaiwa, Furnio; Oono, Kiyoharu; Sugiura, Masahiro
  • Nucleic Acids Research, Vol. 12, Issue 13
  • DOI: 10.1093/nar/12.13.5441

Organization, differential expression and methylation of rDNA in artificial Solanum allopolyploids
journal, October 2004

  • Komarova, Nataliya Y.; Grabe, Thomas; Huigen, Dirk J.
  • Plant Molecular Biology, Vol. 56, Issue 3
  • DOI: 10.1007/s11103-004-4678-x

Astonishing 35S rDNA diversity in the gymnosperm species Cycas revoluta Thunb
journal, December 2015


Transcriptional analysis of nucleolar dominance in polyploid plants: Biased expression/silencing of progenitor rRNA genes is developmentally regulated in Brassica
journal, April 1997

  • Chen, Z. J.; Pikaard, C. S.
  • Proceedings of the National Academy of Sciences, Vol. 94, Issue 7
  • DOI: 10.1073/pnas.94.7.3442

Ribosomal cistrons and the nucleolar organizer
journal, February 1966

  • Wallace, H.; Birnstiel, M. L.
  • Biochimica et Biophysica Acta (BBA) - Nucleic Acids and Protein Synthesis, Vol. 114, Issue 2
  • DOI: 10.1016/0005-2787(66)90311-X

Concerted evolution rapidly eliminates sequence variation in rDNA coding regions but not in intergenic spacers in Nicotiana tabacum allotetraploid
journal, July 2017

  • Lunerová, J.; Renny-Byfield, S.; Matyášek, R.
  • Plant Systematics and Evolution, Vol. 303, Issue 8
  • DOI: 10.1007/s00606-017-1442-7

Cytogenetic evidence of nucleolar dominance in allotetraploid species of Brachypodium
journal, May 2008

  • Idziak, Dominika; Hasterok, Robert
  • Genome, Vol. 51, Issue 5
  • DOI: 10.1139/G08-017

Inhibition of DNA Methylation Alters Chromatin Organization, Nuclear Positioning and Activity of 45S rDNA Loci in Cycling Cells of Q. robur
journal, August 2014


1R chromosome nucleolus organizer region activation by 5-azacytidine in wheat × rye hybrids
journal, October 1990

  • Vieira, Rita; Queiroz, Álvaro; Morais, Leonor
  • Genome, Vol. 33, Issue 5
  • DOI: 10.1139/g90-106

Position-dependent NOR activity in barley
journal, September 1990


Ribosomal DNA loci derived from Brachypodium stacei are switched off for major parts of the life cycle of Brachypodium hybridum
journal, November 2018

  • Borowska-Zuchowska, Natalia; Robaszkiewicz, Ewa; Wolny, Elzbieta
  • Journal of Experimental Botany, Vol. 70, Issue 3
  • DOI: 10.1093/jxb/ery425

Transcription activity of rRNA genes correlates with a tendency towards intergenomic homogenization in Nicotiana allotetraploids
journal, May 2007


Epistatic and allelic interactions control expression of ribosomal RNA gene clusters in Arabidopsis thaliana
journal, May 2017

  • Rabanal, Fernando A.; Mandáková, Terezie; Soto-Jiménez, Luz M.
  • Genome Biology, Vol. 18, Issue 1
  • DOI: 10.1186/s13059-017-1209-z

Conserved Organisation of 45S rDNA Sites and rDNA Gene Copy Number among Major Clades of Early Land Plants
journal, September 2016


Cytosine methylation and nucleolar dominance in cereal hybrids
journal, July 1997

  • Houchins, K.; O'Dell, M.; Flavell, R. B.
  • Molecular and General Genetics MGG, Vol. 255, Issue 3
  • DOI: 10.1007/s004380050500

Unequal crossing over in the ribosomal DNA of Saccharomyces cerevisiae
journal, April 1980


Parental origin and genome evolution of several Eurasian hexaploid species of Chenopodium (Chenopodiaceae)
journal, February 2019


Uniparental loss of ribosomal DNA in the allotetraploid grass Zingeria trichopoda (2 n = 8)
journal, February 2003

  • Kotseruba, Violetta; Gernand, Dorota; Meister, Armin
  • Genome, Vol. 46, Issue 1
  • DOI: 10.1139/g02-104

Cytogenetic features of rRNA genes across land plants: analysis of the Plant rDNA database
journal, February 2017

  • Garcia, Sònia; Kovařík, Ales; Leitch, Andrew R.
  • The Plant Journal, Vol. 89, Issue 5
  • DOI: 10.1111/tpj.13442

A Concerted DNA Methylation/Histone Methylation Switch Regulates rRNA Gene Dosage Control and Nucleolar Dominance
journal, February 2004


Selective nucleolus organizer inactivation in Arabidopsis is a chromosome position-effect phenomenon
journal, November 2016

  • Mohannath, Gireesha; Pontvianne, Frederic; Pikaard, Craig S.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 47
  • DOI: 10.1073/pnas.1608140113

Asymmetric Epigenetic Modification and Elimination of rDNA Sequences by Polyploidization in Wheat
journal, November 2014


Epigenetics of the preferential silencing of Brachypodium stacei-originated 35S rDNA loci in the allotetraploid grass Brachypodium hybridum
journal, July 2017


Nucleotide sequence of the 17S–25S spacer region from tomato rDNA
journal, January 1988

  • Kiss, Tamás; Kis, Mihály; Abel, Steffen
  • Nucleic Acids Research, Vol. 16, Issue 14
  • DOI: 10.1093/nar/16.14.7179

Concerted Evolution in the Ribosomal RNA Cistron
journal, March 2013


Organellar genome, nuclear ribosomal DNA repeat unit, and microsatellites isolated from a small-scale of 454 GS FLX sequencing on two mosses
journal, March 2013

  • Liu, Yang; Forrest, Laura L.; Bainard, Jillian D.
  • Molecular Phylogenetics and Evolution, Vol. 66, Issue 3
  • DOI: 10.1016/j.ympev.2012.12.006

Evolutional dynamics of 45S and 5S ribosomal DNA in ancient allohexaploid Atropa belladonna
journal, January 2017

  • Volkov, Roman A.; Panchuk, Irina I.; Borisjuk, Nikolai V.
  • BMC Plant Biology, Vol. 17, Issue 1
  • DOI: 10.1186/s12870-017-0978-6

The long and short of doubling down: polyploidy, epigenetics, and the temporal dynamics of genome fractionation
journal, April 2018

  • Wendel, Jonathan F.; Lisch, Damon; Hu, Guanjing
  • Current Opinion in Genetics & Development, Vol. 49
  • DOI: 10.1016/j.gde.2018.01.004

Sequence organization of the repeating units in the nucleus of wheat which contain 5S rRNA genes
journal, January 1980


Evolutionary Consequences, Constraints and Potential of Polyploidy in Plants
journal, January 2013

  • Weiss-Schneeweiss, H.; Emadzade, K.; Jang, T. -S.
  • Cytogenetic and Genome Research, Vol. 140, Issue 2-4
  • DOI: 10.1159/000351727

Parental Origin and Genome Evolution in the Allopolyploid Iris versicolor
journal, June 2007

  • Lim, K. Yoong; Matyasek, Roman; Kovarik, Ales
  • Annals of Botany, Vol. 100, Issue 2
  • DOI: 10.1093/aob/mcm116

Laying the Cytotaxonomic Foundations of a New Model Grass, Brachypodium distachyon (L.) Beauv.
journal, January 2004


Painting the chromosomes of Brachypodium—current status and future prospects
journal, June 2011


Nucleotide sequence of the 5.8S and 25S rRNA genes and of the internal transcribed spacers from Arabidopsis thaliana
journal, January 1990


Nucleolar dominance does not occur in root tip cells of allotetraploid Brassica species
journal, June 2000

  • Hasterok, Robert; Maluszynska, Jolanta
  • Genome, Vol. 43, Issue 3
  • DOI: 10.1139/g00-005

Finely Orchestrated Movements: Evolution of the Ribosomal RNA Genes
journal, February 2007


The nucleolus organizer region of maize (Zea mays L.): Chromosomal site of DNA complementary to ribosomal RNA
journal, January 1971

  • Phillips, R. L.; Kleese, R. A.; Wang, S. S.
  • Chromosoma, Vol. 36, Issue 1
  • DOI: 10.1007/BF00326423