To Be or Not to Be Expressed: The First Evidence of a Nucleolar Dominance Tissue-Specificity in Brachypodium hybridum

. 2021 ; 12 () : 768347. [epub] 20211206

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

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid34938308

Nucleolar dominance (ND) is an epigenetic, developmentally regulated phenomenon that describes the selective inactivation of 35S rDNA loci derived from one progenitor of a hybrid or allopolyploid. The presence of ND was documented in an allotetraploid grass, Brachypodium hybridum (genome composition DDSS), which is a polyphyletic species that arose from crosses between two putative ancestors that resembled the modern B. distachyon (DD) and B. stacei (SS). In this work, we investigated the developmental stability of ND in B. hybridum genotype 3-7-2 and compared it with the reference genotype ABR113. We addressed the question of whether the ND is established in generative tissues such as pollen mother cells (PMC). We examined condensation of rDNA chromatin by fluorescence in situ hybridization employing state-of-art confocal microscopy. The transcription of rDNA homeologs was determined by reverse-transcription cleaved amplified polymorphic sequence analysis. In ABR113, the ND was stable in all tissues analyzed (primary and adventitious root, leaf, and spikes). In contrast, the 3-7-2 individuals showed a strong upregulation of the S-genome units in adventitious roots but not in other tissues. Microscopic analysis of the 3-7-2 PMCs revealed extensive decondensation of the D-genome loci and their association with the nucleolus in meiosis. As opposed, the S-genome loci were always highly condensed and localized outside the nucleolus. These results indicate that genotype-specific loss of ND in B. hybridum occurs probably after fertilization during developmental processes. This finding supports our view that B. hybridum is an attractive model to study ND in grasses.

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Amado L., Abranches R., Neves N., Viegas W. (1997). Development-dependent inheritance of 5-azacytidine-induced epimutations in triticale: analysis of rDNA expression patterns. PubMed DOI

Bass H. W., Marshall W. F., Sedat J. W., Agard D. A., Cande W. Z. (1997). Telomeres cluster de novo before the initiation of synapsis: a three-dimensional spatial analysis of telomere positions before and during meiotic prophase. PubMed DOI PMC

Bellini C., Pacurar D. I., Perrone I. (2014). Adventitious roots and lateral roots: similarities and differences. PubMed DOI

Borowska-Zuchowska N., Hasterok R. (2017). Epigenetics of the preferential silencing of PubMed DOI PMC

Borowska-Zuchowska N., Kovarik A., Robaszkiewicz E., Tuna M., Tuna G. S., Gordon S., et al. (2020). The fate of 35S rRNA genes in the allotetraploid grass PubMed DOI PMC

Borowska-Zuchowska N., Kwasniewski M., Hasterok R. (2016). Cytomolecular analysis of ribosomal DNA evolution in a natural allotetraploid PubMed DOI PMC

Borowska-Zuchowska N., Robaszkiewicz E., Wolny E., Betekhtin A., Hasterok R. (2019). Ribosomal DNA loci derived from PubMed DOI PMC

Castilho A., Queiroz A., Neves N., Barao A., Silva M., Viegas W. (1995). The developmental stage of inactivation of rye origin rRNA genes in the embryo and endosperm of wheat x rye F1 hybrids. PubMed DOI

Catalan P., Muller J., Hasterok R., Jenkins G., Mur L. A., Langdon T., et al. (2012). Evolution and taxonomic split of the model grass Brachypodium distachyon. PubMed DOI PMC

Cermeno M. C., Orellana J., Santos J. L., Lacadena J. R. (1984). Nucleolar organizer activity in wheat, rye and derivatives analyzed by a silver-staining procedure. 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. 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. PubMed 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 PubMed PMC

Chester M., Gallagher J. P., Symonds V. V., da Silva A. V. C., Mavrodiev E. V., Leitch A. R., et al. (2012). Extensive chromosomal variation in a recently formed natural allopolyploid species, PubMed DOI PMC

Costa-Nunes P., Pontes O., Preuss S. B., Pikaard C. S. (2010). Extra views on RNA-dependent DNA methylation and MBD6-dependent heterochromatin formation in nucleolar dominance. PubMed DOI PMC

Diaz-Perez A., Lopez-Alvarez D., Sancho R., Catalan P. (2018). Reconstructing the origins and the biogeography of species’ genomes in the highly reticulate allopolyploid-rich model grass genus Brachypodium using minimum evolution, coalescence and maximum likelihood approaches. PubMed DOI

Dolezel J., Cizkova J., Simkova H., Bartos J. (2018). One major challenge of sequencing large plant genomes is to know how big they really are. PubMed DOI PMC

Earley K., Lawrence R. J., Pontes O., Reuther R., Enciso A. J., Silva M., et al. (2006). Erasure of histone acetylation by PubMed DOI PMC

Ge X. H., Ding L., Li Z. Y. (2013). Nucleolar dominance and different genome behaviors in hybrids and allopolyploids. PubMed DOI

Gordon S. P., Contreras-Moreira B., Levy J. J., Djamei A., Czedik-Eysenberg A., Tartaglio V. S., et al. (2020). Gradual polyploid genome evolution revealed by pan-genomic analysis of Brachypodium hybridum and its diploid progenitors. PubMed DOI PMC

Guo X., Han F. P. (2014). Asymmetric Epigenetic Modification and Elimination of rDNA Sequences by Polyploidization in Wheat. PubMed DOI PMC

Hasterok R., Draper J., Jenkins G. (2004). Laying the cytotaxonomic foundations of a new model grass, PubMed DOI

Hasterok R., Dulawa J., Jenkins G., Leggett M., Langdon T. (2006). Multi-substrate chromosome preparations for high throughput comparative FISH. PubMed DOI PMC

Hasterok R., Langdon T., Taylor S., Jenkins G. (2002). Combinatorial labelling of DNA probes enables multicolour fluorescence in situ hybridisation in plants. PubMed

Hasterok R., Maluszynska J. (2000a). Different rRNA gene expression in primary and adventitious roots of PubMed

Hasterok R., Maluszynska J. (2000b). Nucleolar dominance does not occur in root tip cells of allotetraploid PubMed

Houchins K., O’Dell M., Flavell R. B., Gustafson J. P. (1997). Cytosine methylation and nucleolar dominance in cereal hybrids. PubMed

IBI (2010). Genome sequencing and analysis of the model grass PubMed DOI

Idziak D., Betekhtin A., Wolny E., Lesniewska K., Wright J., Febrer M., et al. (2011). Painting the chromosomes of PubMed DOI PMC

Idziak D., Hasterok R. (2008). Cytogenetic evidence of nucleolar dominance in allotetraploid species of PubMed DOI

Jenkins G., Hasterok R. (2007). BAC ‘landing’ on chromosomes of PubMed DOI

Komarova N. Y., Grabe T., Huigen D. J., Hemleben V., Volkov R. A. (2004). Organization, differential expression and methylation of rDNA in artificial PubMed DOI

Kovarik A., Pires J. C., Leitch A. R., Lim K. Y., Sherwood A. M., Matyasek R., et al. (2005). Rapid concerted evolution of nuclear ribosomal DNA in two PubMed DOI PMC

Lacadena J. R., Cermeno M. C., Orellana J., Santos J. L. (1984). Evidence for wheat-rye nucleolar competition (amphiplasty) in triticale by silver-staining procedure. PubMed DOI

Lawrence R. J., Earley K., Pontes O., Silva M., Chen Z. J., Neves N., et al. (2004). A concerted DNA methylation/histone methylation switch regulates rRNA gene dosage control and nucleolar dominance. PubMed

Lusinska J., Majka J., Betekhtin A., Susek K., Wolny E., Hasterok R. (2018). Chromosome identification and reconstruction of evolutionary rearrangements in Brachypodium distachyon. B. stacei and B. hybridum. PubMed DOI PMC

Mason A. S., Wendel J. F. (2020). Homoeologous exchanges, segmental allopolyploidy, and polyploid genome evolution. 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 PubMed DOI

McKinlay A., Fultz D., Wang F., Pikaard C. S. (2021). Targeted Enrichment of rRNA Gene Tandem Arrays for Ultra-Long Sequencing by Selective Restriction Endonuclease Digestion. PubMed DOI PMC

Mohannath G., Pontvianne F., Pikaard C. S. (2016). Selective nucleolus organizer inactivation in Arabidopsis is a chromosome position-effect phenomenon. PubMed DOI PMC

Navashin M. (1934). Chromosomal alterations caused by hybridization and their bearing upon certain general genetic problems.

Neves N., Heslop-Harrison J. S., Viegas W. (1995). rRNA gene activity and control of expression mediated by methylation and imprinting during embryo development in wheat x rye hybrids. PubMed DOI

Nicolas S. D., Leflon M., Monod H., Eber F., Coriton O., Huteau V., et al. (2009). Genetic Regulation of Meiotic Cross-Overs between Related Genomes in Brassica napus Haploids and Hybrids. PubMed DOI PMC

Ozkan H., Levy A. A., Feldman M. (2001). Allopolyploidy-induced rapid genome evolution in the wheat ( PubMed DOI PMC

Pikaard C. S. (2000). Nucleolar dominance: uniparental gene silencing on a multi-megabase scale in genetic hybrids. PubMed

Pontes O., Lawrence R. J., Silva M., Preuss S., Costa-Nunes P., Earley K., et al. (2007). Postembryonic establishment of megabase-scale gene silencing in nucleolar dominance. PubMed DOI PMC

Preuss S. B., Costa-Nunes P., Tucker S., Pontes O., Lawrence R. J., Mosher R., et al. (2008). Multimegabase silencing in nucleolar dominance involves siRNA-directed DNA methylation and specific methylcytosine-binding proteins. PubMed DOI PMC

Reeder R. H. (1985). Mechanisms of nucleolar dominance in animals and plants. PubMed DOI PMC

Shaked H., Kashkush K., Ozkan H., Feldman M., Levy A. A. (2001). Sequence elimination and cytosine methylation are rapid and reproducible responses of the genome to wide hybridization and allopolyploidy in wheat. PubMed DOI PMC

Shaw P. (2013). The Plant Nucleolus.

Silva M., Queiroz A., Neves N., Barao A., Castilho A., Morais-Cecilio L., et al. (1995). Reprogramming of rye rDNA in triticale during microsporogenesis. PubMed DOI

Sims J., Rabanal F. A., Elgert C., von Haeseler A., Schlögelhofer P. (2021). It is just a matter of time: balancing homologous recombination and non-homologous end joining at the rDNA locus during meiosis. PubMed DOI PMC

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 PubMed DOI PMC

Soltis P. S., Marchant D. B., Van de Peer Y., Soltis D. E. (2015). Polyploidy and genome evolution in plants. PubMed DOI

Symonova R. (2019). Integrative rDNAomics-Importance of the oldest repetitive fraction of the eukaryote genome. PubMed DOI PMC

Unfried I., Gruendler P. (1990). Nucleotide sequence of the 5.8S and 25S rRNA genes and of the internal transcribed spacers from PubMed DOI PMC

Vieira R., Mellosampayo T., Viegas W. S. (1990). 1R chromosome nucleolus organizer region activation by 5-azacytidine in wheat x rye hybrids.

Volkov R. A., Komarova N. Y., Hemleben V. (2007). Ribosomal DNA in plant hybrids: Inheritance, rearrangement, expression. DOI

Volkov R. A., Medina F. R., Zentgraf U., Hemleben V. (2004). Molecular Cell Biology: Organization and molecular evolution of rDNA, nucleolar dominance, and nucleolus structure. DOI

Wendel J. F., Lisch D., Hu G., Mason A. S. (2018). The long and short of doubling down: polyploidy, epigenetics, and the temporal dynamics of genome fractionation. PubMed DOI

Yoo M. J., Liu X., Pires J. C., Soltis P. S., Soltis D. E. (2014). Nonadditive gene expression in polyploids. PubMed DOI

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