Nucleolin Is Required for DNA Methylation State and the Expression of rRNA Gene Variants in Arabidopsis thaliana

Pontvianne, Frédéric; Abou-Ellail, Mohamed; Douet, Julien; Comella, Pascale; Matı́a, Isabel; Chandrasekhara, Chinmayi; Debures, Anne; Blevins, Todd; Cooke, Richard; Medina, F. Javier; Tourmente, Sylvette; Pikaard, Craig S.; Sáez‐Vasquez, Julio

doi:10.1371/journal.pgen.1001225

Cited by 125 publications

(190 citation statements)

References 61 publications

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“…All subtypes are expressed immediately following germination, but by ;10 d of seedling growth, the variant 1 subtype (Fig. 1A), accounting for ;50% of all rRNA genes, is silenced via epigenetic mechanisms that include changes in DNA methylation and histone modification (Earley et al 2006(Earley et al , 2010Pontvianne et al 2010Pontvianne et al , 2012. Chromatin modifications mediate rRNA gene dosage control in yeast, mouse, and human cells as well (Sandmeier et al 2002;McStay and Grummt 2008;Grummt and Langst 2013).…”

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confidence: 99%

Subnuclear partitioning of rRNA genes between the nucleolus and nucleoplasm reflects alternative epiallelic states

et al. 2013

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Eukaryotes can have thousands of 45S ribosomal RNA (rRNA) genes, many of which are silenced during development. Using fluorescence-activated sorting techniques, we show that active rRNA genes in Arabidopsis thaliana are present within sorted nucleoli, whereas silenced rRNA genes are excluded. DNA methyltransferase (met1), histone deacetylase (hda6), or chromatin assembly (caf1) mutants that disrupt silencing abrogate this nucleoplasmic-nucleolar partitioning. Bisulfite sequencing data indicate that active nucleolar rRNA genes are nearly completely demethylated at promoter CGs, whereas silenced genes are nearly fully methylated. Collectively, the data reveal that rRNA genes occupy distinct but changeable nuclear territories according to their epigenetic state.

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Subnuclear partitioning of rRNA genes between the nucleolus and nucleoplasm reflects alternative epiallelic states

et al. 2013

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“…In contrast, the least abundant variant (VAR4) is relatively highly expressed in WT plants. In fact, we only identified rDNA VAR4 in the genomic sequence after cloning pre-rRNA products 1 (Fig. 1B).…”

Section: Variations On a Teammentioning

confidence: 98%

“…A detailed analysis of the 3'ETS sequences revealed the presence of 3 (VAR2), 4 (VAR1 and VAR3) or 5 rDNA chromatin decondensation and affects expression of specific 45S rRNA gene variants. 1,16 Here we present additional characterization of these rDNA gene variants and discuss their possible impact on rDNA chromatin organization and gene expression.…”

Section: Variations On a Teammentioning

confidence: 99%

“…However, our studies on A. thaliana plants with a disrupted nucleolin protein gene (AtNUC-L1) clearly show that only two of the four NORs form nucleoli and are consequently transcriptionally active. 1 Whether or not rDNA VAR1 is present in transcriptionally inactive NORs or located in the knob outside the nucleolus NORs from Chr2 and/or Chr4. However, the relative amplification levels of VAR1 and VAR4 (Fig.…”

Section: Rdna Gene Variants In Arabidopsis Ecotypesmentioning

confidence: 99%

“…1,31 If binding of AtNUC-L1 maintains a transcriptionally competent methylation status of rDNA chromatin, how could the absence of this protein repress insertion of a complete chromosome after centromeric breaks and subsequent divergence of one centromere and the internal telomeric sequences. As both Arabidopsis NORs are located in subtelomeric regions and the ancestral karyotype is n = 8, 36 this could explain the presence of Chr3-VAR4 in the pericentromeric region of chr3.…”

Section: Rdna Gene Variants In Arabidopsis Ecotypesmentioning

confidence: 99%

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Variations in a team: Major and minor variants ofArabidopsisthaliana rDNA genes

Abou-Ellail¹,

Cooke²,

Sáez‐Vasquez³

2011

Nucleus

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While plant rRNA gene organization and expression have been studied for several decades, the repetitive nature and high sequence identity between the tandemly-repeated units has prevented precise studies to determine which units are active and elucidate mechanisms of spatial and temporal transcriptional control. We have detected four variants among rRNA genes of Arabidopsis thaliana by analysis of the 3' external spacer region. Surprisingly, the most abundant variant, representing ~50% of the genes, is not expressed in wild-type plants but is transcribed in lines mutated in one of the two nucleolin genes.1 Analysis of Arabidopsis ecotypes indicated considerable variability in numbers and presence/absence of variants, although more closely-related ecotypes show similar profiles. Sequence analysis showed that one of the variants is not only unexpectedly located within a 5S RNA gene cluster in the pericentromeric region of chromosome 3 but is also potentially highly expressed in wild-type plants. We present a model to explain how transcription of this this unusual variant, maintained in an active state by nucleolin binding, could be involved in control of expression of the major variant, while absence of nucleolin leads to silencing of the minor variant and consequent expression of the major variant.

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Light signals counteract alterations caused by simulated microgravity in proliferating plant cells

Manzano

Pereda-Loth

Bures

et al. 2021

American J of Botany

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Light and gravity are fundamental cues for plant development. Our understanding of the effects of light stimuli on plants in space, without gravity, is key to providing conditions for plants to acclimate to the environment. Here we tested the hypothesis that the alterations caused by the absence of gravity in root meristematic cells can be counteracted by light. Methods: Seedlings of wild-type Arabidopsis thaliana and two mutants of the essential nucleolar protein nucleolin (nuc1, nuc2) were grown in simulated microgravity, either under a white light photoperiod or under continuous darkness. Key variables of cell proliferation (cell cycle regulation), cell growth (ribosome biogenesis), and auxin transport were measured in the root meristem using in situ cellular markers and transcriptomic methods and compared with those of a 1 g control. Results: The incorporation of a photoperiod regime was sufficient to attenuate or suppress the effects caused by gravitational stress at the cellular level in the root meristem. In all cases, values for variables recorded from samples receiving light stimuli in simulated microgravity were closer to values from the controls than values from samples grown in darkness. Differential sensitivities were obtained for the two nucleolin mutants. Conclusions: Light signals may totally or partially replace gravity signals, significantly improving plant growth and development in microgravity. Despite that, molecular alterations are still compatible with the expected acclimation mechanisms, which need to be better understood. The differential sensitivity of nuc1 and nuc2 mutants to gravitational stress points to new strategies to produce more resilient plants to travel with humans in new extraterrestrial endeavors.

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Nucleolin Is Required for DNA Methylation State and the Expression of rRNA Gene Variants in Arabidopsis thaliana

Cited by 125 publications

References 61 publications

Subnuclear partitioning of rRNA genes between the nucleolus and nucleoplasm reflects alternative epiallelic states

Subnuclear partitioning of rRNA genes between the nucleolus and nucleoplasm reflects alternative epiallelic states

Variations in a team: Major and minor variants ofArabidopsisthaliana rDNA genes

Light signals counteract alterations caused by simulated microgravity in proliferating plant cells

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