Natural variation in nucleolar dominance reveals the relationship between nucleolus organizer chromatin topology and rRNA gene transcription in
            <i>Arabidopsis</i>

Pontes, Olga; Lawrence, Richard J.; Neves, Nuno; Silva, Maria Manuela; Lee, Jae‐Hyeok; Chen, Z. Jeffrey; Viegas, Wanda; Pikaard, Craig S.

doi:10.1073/pnas.1932522100

Cited by 84 publications

(74 citation statements)

References 39 publications

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“…In A. thaliana cells, four rDNA loci located at the tips of chromosomes 2 and 4 are found in diploid nucleus. As shown in Figure 8, we detected two to four NOR fluorescence signals in WT interphase nuclei, in agreement with Pontes et al (2003), due to association of homologous NORs. FISH analysis of the WT nuclei revealed a high condensation of NOR sequences and shows a tight colocalization with heterochromatin structure counterstained with DAPI (Figure 8, a-c).…”

Section: Atnuc-l1 Gene Disruption Induces Rdna Heterochromatin Decondsupporting

confidence: 83%

Characterization of AtNUC-L1 Reveals a Central Role of Nucleolin in Nucleolus Organization and Silencing of AtNUC-L2 Gene in Arabidopsis

Pontvianne

Matı́a

Douet

et al. 2007

MBoC

125

207

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Nucleolin is one of the most abundant protein in the nucleolus and is a multifunctional protein involved in different steps of ribosome biogenesis. In contrast to animals and yeast, the genome of the model plant Arabidopsis thaliana encodes two nucleolin-like proteins, AtNUC-L1 and AtNUC-L2. However, only the AtNUC-L1 gene is ubiquitously expressed in normal growth conditions. Disruption of this AtNUC-L1 gene leads to severe plant growth and development defects. AtNUC-L1 is localized in the nucleolus, mainly in the dense fibrillar component. Absence of this protein in Atnuc-L1 plants induces nucleolar disorganization, nucleolus organizer region decondensation, and affects the accumulation levels of pre-rRNA precursors. Remarkably, in Atnuc-L1 plants the AtNUC-L2 gene is activated, suggesting that AtNUC-L2 might rescue, at least partially, the loss of AtNUC-L1. This work is the first description of a higher eukaryotic organism with a disrupted nucleolin-like gene and defines a new role for nucleolin in nucleolus structure and rDNA chromatin organization.

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Section: Atnuc-l1 Gene Disruption Induces Rdna Heterochromatin Decondsupporting

confidence: 83%

Characterization of AtNUC-L1 Reveals a Central Role of Nucleolin in Nucleolus Organization and Silencing of AtNUC-L2 Gene in Arabidopsis

Pontvianne

Matı́a

Douet

et al. 2007

MBoC

125

207

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“…The ability of a single master locus to dominate supernumerary loci has been noted before, e.g., a single NORbearing chromosome from Aegilops umbellutata can suppress all remaining NORs in hexaploid wheat (Martini et al 1982), and in Solanum somatic hybrids, a single tomato locus can dominate NORs from potato (Komarova et al 2004). But in Arabidopsis suecica, six A. arenosa-origin NORs dominated expression over two NORs inherited from the A. thaliana parent (Pontes et al 2003).…”

Section: Discussionmentioning

confidence: 70%

“…In synthetic A. suecica, the direction of silencing was concordant with natural A. suecica, suggesting that there might be a predisposition toward silencing of parental genomes. Nevertheless, one strain of A. suecica showed codominance (Pontes et al 2003), and only certain inter-ecotype diploid Arabidopsis hybrids exhibited NOR silencing . These data indicate that ND may depend on the particular genotype or combination of alleles.…”

Section: Discussionmentioning

confidence: 99%

Concerted Evolution of rDNA in Recently Formed Tragopogon Allotetraploids Is Typically Associated With an Inverse Correlation Between Gene Copy Number and Expression

et al. 2007

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We analyzed nuclear ribosomal DNA (rDNA) transcription and chromatin condensation in individuals from several populations of Tragopogon mirus and T. miscellus, allotetraploids that have formed repeatedly within only the last 80 years from T. dubius and T. porrifolius and T. dubius and T. pratensis, respectively. We identified populations with no (2), partial (2), and complete (4) nucleolar dominance. It is probable that epigenetic regulation following allopolyploidization varies between populations, with a tendency toward nucleolar dominance by one parental homeologue. Dominant rDNA loci are largely decondensed at interphase while silent loci formed condensed heterochromatic regions excluded from nucleoli. Those populations where nucleolar dominance is fixed are epigenetically more stable than those with partial or incomplete dominance. Previous studies indicated that concerted evolution has partially homogenized thousands of parental rDNA units typically reducing the copy numbers of those derived from the T. dubius diploid parent. Paradoxically, despite their low copy number, repeats of T. dubius origin dominate rDNA transcription in most populations studied, i.e., rDNA units that are genetic losers (copy numbers) are epigenetic winners (high expression). E PIGENETIC silencing of parental genes is an important feature of newly established allopolyploids and is believed to reconcile regulatory incompatibilities between parental subgenomes (Adams and Wendel 2005;Birchler et al., 2005). Nucleolus organizer regions (NORs) contain tandemly arranged highly reiterated ribosomal rRNA genes coding for 18S-5.8S-26S rRNA whose expression is under epigenetic control (Pikaard 2000; for review see Neves et al. 2005). Indeed nucleolar dominance (ND) was one of the first examples of differential gene expression discovered in plant hybrids nearly a century ago (Navashin 1934). Numerous studies in both plants and animals support the view that ND/rRNA gene silencing may be stable or unstable, partial, or reversible (Volkov et al. 2007). In Arabidopsis and Brassica biochemical (Chen and Pikaard 1997a) and genetic (Lawrence et al. 2004;Probst et al. 2004) studies provided evidence that rRNA silencing depends on epigenetic factors, including DNA methylation and histone acetylation (for review see Preuss and Pikaard 2007). Other factors may also play a role in ND, e.g., the position of rRNA genes in the nucleus (Shaw and Jordan 1995), the relative amount of heterochromatin (Viegas et al. 2002), and the activity of unlinked genes . Despite considerable progress in our understanding of ND, little is known about the relationship between ND and sequence homogenization, particularly in young populations of newly formed polyploidy species. The goal of this article is to study this relationship and the inheritance patterns of ND and sequence homogenization at individual and population levels in recently formed allotetraploid species.Besides epigenetic silencing homogenization of repeats seems to be another interesting aspect of rDNA...

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“…An additional wild accession of A. suecica was obtained from the Helsinki Botanical Garden (seed exchange). A. suecica laboratory strains LC1 and 9502 were provided by C. Pikaard (Pontes et al 2003). A. suecica LC1 is derived from Sue-1 (Comai et al 2000).…”

Section: Methodsmentioning

confidence: 99%

Natural Variation in a Subtelomeric Region of Arabidopsis: Implications for the Genomic Dynamics of a Chromosome End

2006

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We investigated genome dynamics at a chromosome end in the model plant Arabidopsis thaliana through a study of natural variation in 35 wild accessions. We focused on the single-copy subtelomeric region of chromosome 1 north (3.5 kb), which represents the relatively simple organization of subtelomeric regions in this species. PCR fragment-length variation across the subtelomeric region indicated that the 1.4-kb distal region showed elevated structural variation relative to the centromere-proximal region. Examination of nucleotide sequences from this 1.4-kb region revealed diverse DNA rearrangements, including an inversion, several deletions, and an insertion of a retrotransposon LTR. The structures at the deletion and inversion breakpoints are characteristic of simple deletion-associated nonhomologous endjoining (NHEJ) events. There was strong linkage disequilibrium between the distal subtelomeric region and the proximal telomere, which contains degenerate and variant telomeric repeats. Variation in the proximal telomere was characterized by the expansion and deletion of blocks of repeats. Our sample of accessions documented two independent chromosome-healing events associated with terminal deletions of the subtelomeric region as well as the capture of a scrambled mitochondrial DNA segment in the proximal telomeric array. This natural variation study highlights the variety of genomic events that drive the fluidity of chromosome termini.

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Natural variation in nucleolar dominance reveals the relationship between nucleolus organizer chromatin topology and rRNA gene transcription in Arabidopsis

Cited by 84 publications

References 39 publications

Characterization of AtNUC-L1 Reveals a Central Role of Nucleolin in Nucleolus Organization and Silencing of AtNUC-L2 Gene in Arabidopsis

Characterization of AtNUC-L1 Reveals a Central Role of Nucleolin in Nucleolus Organization and Silencing of AtNUC-L2 Gene in Arabidopsis

Concerted Evolution of rDNA in Recently Formed Tragopogon Allotetraploids Is Typically Associated With an Inverse Correlation Between Gene Copy Number and Expression

Natural Variation in a Subtelomeric Region of Arabidopsis: Implications for the Genomic Dynamics of a Chromosome End

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