The peculiar genetics of the ribosomal DNA blurs the boundaries of transgenerational epigenetic inheritance

Bughio, Farah; Maggert, Keith A.

doi:10.1007/s10577-018-9591-2

Cited by 17 publications

(16 citation statements)

References 128 publications

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“…Similar to 35S loci, 5S rDNA loci undergo concerted evolution, a process maintaining high homogeneity within and often between arrays (Dover, 1982;Elder and Turner, 1995;Parks et al, 2019). Such a process may rapidly homogenize rDNA sequences and induce copy number variation (Bughio and Maggert, 2019) blurring their hybridogenic signatures in allopolyploids (Wendel et al, 1995a;Volkov et al, 1999;Muir et al, 2001;Matyasek et al, 2003). In contrast to 35S rDNA, the 5S rDNA loci appear to be less sensitive to homogenization in some allopolyploids (Fulnecek et al, 2002;Pedrosa-Harand et al, 2006;Weiss-Schneeweiss et al, 2008;Garcia et al, 2017), retaining diagnostic capacity with respect to their parental origin.…”

Section: Discussionmentioning

confidence: 99%

The Utility of Graph Clustering of 5S Ribosomal DNA Homoeologs in Plant Allopolyploids, Homoploid Hybrids, and Cryptic Introgressants

et al. 2020

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Introduction: Ribosomal DNA (rDNA) loci have been widely used for identification of allopolyploids and hybrids, although few of these studies employed high-throughput sequencing data. Here we use graph clustering implemented in the RepeatExplorer (RE) pipeline to analyze homoeologous 5S rDNA arrays at the genomic level searching for hybridogenic origin of species. Data were obtained from more than 80 plant species, including several well-defined allopolyploids and homoploid hybrids of different evolutionary ages and from widely dispersed taxonomic groups.Results: (i) Diploids show simple circular-shaped graphs of their 5S rDNA clusters. In contrast, most allopolyploids and other interspecific hybrids exhibit more complex graphs composed of two or more interconnected loops representing intergenic spacers (IGS). (ii) There was a relationship between graph complexity and locus numbers. (iii) The sequences and lengths of the 5S rDNA units reconstituted in silico from k-mers were congruent with those experimentally determined. (iv) Three-genomic comparative cluster analysis of reads from allopolyploids and progenitor diploids allowed identification of homoeologous 5S rRNA gene families even in relatively ancient (c. 1 Myr) Gossypium and Brachypodium allopolyploids which already exhibit uniparental partial loss of rDNA repeats. (v) Finally, species harboring introgressed genomes exhibit exceptionally complex graph structures. Conclusion:We found that the cluster graph shapes and graph parameters (k-mer coverage scores and connected component index) well-reflect the organization and intragenomic homogeneity of 5S rDNA repeats. We propose that the analysis of 5S rDNA cluster graphs computed by the RE pipeline together with the cytogenetic analysis might be a reliable approach for the determination of the hybrid or allopolyploid plant species parentage and may also be useful for detecting historical introgression events.

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Section: Discussionmentioning

confidence: 99%

The Utility of Graph Clustering of 5S Ribosomal DNA Homoeologs in Plant Allopolyploids, Homoploid Hybrids, and Cryptic Introgressants

et al. 2020

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“…For these reasons, a heavy body of literature on molecular cytogenetics of rDNA has accumulated (for plants [17], for animals [5]). Since rDNA was omitted from many genome sequencing projects due to issues with its assembling [50,67], any precise quantification of rDNA copies is mostly still impossible. On the other hand, the still increasing availability of long-read sequencing can overcome assembling issues and provides opportunity to link the numerous results from molecular cytogenetics with genomics as was successfully demonstrated in fish cytogenomics [54,56].…”

Section: Copy Number Really Mattersmentioning

confidence: 99%

“…A very special chapter of the rDNAomics book deals with rDNA of eukaryotic microorganisms [67]. In their 2010 review, Torres-Machorro et al present available information on both rDNA fractions from about hundred microbial eukaryotes and show an unexpected diversity in their genomic organization [68].…”

Section: Copy Number Really Mattersmentioning

confidence: 99%

Integrative rDNAomics—Importance of the Oldest Repetitive Fraction of the Eukaryote Genome

Symonová

2019

Genes

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Nuclear ribosomal RNA (rRNA) genes represent the oldest repetitive fraction universal to all eukaryotic genomes. Their deeply anchored universality and omnipresence during eukaryotic evolution reflects in multiple roles and functions reaching far beyond ribosomal synthesis. Merely the copy number of non-transcribed rRNA genes is involved in mechanisms governing e.g., maintenance of genome integrity and control of cellular aging. Their copy number can vary in response to environmental cues, in cellular stress sensing, in development of cancer and other diseases. While reaching hundreds of copies in humans, there are records of up to 20,000 copies in fish and frogs and even 400,000 copies in ciliates forming thus a literal subgenome or an rDNAome within the genome. From the compositional and evolutionary dynamics viewpoint, the precursor 45S rDNA represents universally GC-enriched, highly recombining and homogenized regions. Hence, it is not accidental that both rDNA sequence and the corresponding rRNA secondary structure belong to established phylogenetic markers broadly used to infer phylogeny on multiple taxonomical levels including species delimitation. However, these multiple roles of rDNAs have been treated and discussed as being separate and independent from each other. Here, I aim to address nuclear rDNAs in an integrative approach to better assess the complexity of rDNA importance in the evolutionary context.

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“…We and others have observed that the 18S/5.8S/28S ribosomal RNA gene cluster (henceforth referred to as the "45S rDNA," from the human nomenclature) is a sensitive locus of copy number changes in Drosophila induced by mutation or by ecological conditions (Aldrich and Maggert 2014;Aldrich and Maggert 2015;Gibbons et al 2015). This is expected to be broadly pleiotropic to a cell since the rDNA not only controls rRNA production and translational capacity, but the rDNA also mediates other processes regulated by the nucleolus (Kobayashi 2008;Xu et al 2017;Bughio and Maggert 2019;Salim and Gerton 2019).…”

Section: Introductionmentioning

confidence: 99%

Human rDNA copy number is unstable in metastatic breast cancers

et al. 2019

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Chromatin-mediated silencing, including the formation of heterochromatin, silent chromosome territories, and repressed gene promoters, acts to stabilize patterns of gene regulation and the physical structure of the genome. Reduction of chromatin-mediated silencing can result in genome rearrangements, particularly at intrinsically unstable regions of the genome such as transposons, satellite repeats, and repetitive gene clusters including the rRNA gene clusters (rDNA). It is thus expected that mutational or environmental conditions that compromise heterochromatin function might cause genome instability, and diseases associated with decreased epigenetic stability might exhibit genome changes as part of their etiology. We find support of this hypothesis in invasive ductal breast carcinoma, in which reduced epigenetic silencing has been previously described, by using a facile method to quantify rDNA copy number in biopsied breast tumors and pair-matched healthy tissue. We found that rDNA and satellite DNA sequences had significant copy number variation-both losses and gains of copies-compared to healthy tissue, arguing that these genome rearrangements are common in developing breast cancer. Thus, any proposed etiology onset or progression of breast cancer should consider alterations to the epigenome, but must also accommodate concomitant changes to genome sequence at heterochromatic loci. Authors' Statement One of the common hallmarks of cancer is genome instability, including hypermutation and changes to chromosome structure. Using tumor tissues obtained from women with invasive ductal carcinoma, we find that a sensitive area of the genome-the ribosomal DNA gene repeat cluster-shows hypervariability in copy number. The patterns we observe as not consistent with an adaptive loss leading to increased tumor growth, but rather we conclude that copy number variation at repeat DNA is a general consequence of reduced heterochromatin function in cancer progression.

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The peculiar genetics of the ribosomal DNA blurs the boundaries of transgenerational epigenetic inheritance

Cited by 17 publications

References 128 publications

The Utility of Graph Clustering of 5S Ribosomal DNA Homoeologs in Plant Allopolyploids, Homoploid Hybrids, and Cryptic Introgressants

The Utility of Graph Clustering of 5S Ribosomal DNA Homoeologs in Plant Allopolyploids, Homoploid Hybrids, and Cryptic Introgressants

Integrative rDNAomics—Importance of the Oldest Repetitive Fraction of the Eukaryote Genome

Human rDNA copy number is unstable in metastatic breast cancers

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