Nucleolar dominance is an epigenetic phenomenon that occurs in both the plant and animal kingdoms and describes the transcription of ribosomal RNA genes inherited from one progenitor, but not the other, in an interspecies hybrid or allopolyploid. It has long been thought that dominant genes are selectively activated. However, recent evidence suggests that under-dominant genes are selectively silenced. Cytosine methylation and histone deacetylation are partners in the repression pathway but it is not known if they act in parallel or in series. It is also not clear if chromatin modifications act on the individual rRNA genes, the multi-megabase chromosomal regions where rRNA genes are clustered (NORs), or other regulatory loci. These questions will be addressed using, as our model system, Arabidopsis suecica, an allotetraploid that combines the genomes of A. thaliana and C. arenosa (also known as A. arenosa) In A. suecica, rRNA genes derived from C. arenosa are transcriptionally active and A. thaliana rRNA genes are silenced. To test the hypothesis that cytosine methylation patterns in the progenitor genomes is needed to establish nucleolar dominance, the A. thaliana cytosine hypomethylation mutant ddm1 will be used as one parent to recreate A. suecica lines. The possibility that histone deacetylation causes cytosine demethylation or that cytosine demethylation causes histone hyperacetylation will be examined to test the hypothesis that these chromatin modifications act in series in the control of nucleolar dominance. The hypothesis that rRNA genes are regulated independent of chromosomal location will be tested by determining if rRNA transgenes at ectopic locations are silenced in newly formed A. suecica lines. In a related aim, we will determine if silencing is restricted to the NORs or if it spreads to neighboring genes adjacent to the NORs. These experiments are part of our long-term effort to understand the positive and negative regulatory mechanisms that control rRNA gene transcription. Understanding nucleolar dominance may also shed light on other epigenetic phenomena such as X-chromosome, provirus, and transposable element inactivation or gametic imprinting. Practical benefits may come from such understanding. For instance, derepression of developmentally silenced genes could have potential for rescuing disease phenotypes due to defects in adult-specific paralogs. Our work on nucleolar dominance is expected to contribute new information to our understanding of chromosomal controls of gene expression.

Agency
National Institute of Health (NIH)
Institute
National Institute of General Medical Sciences (NIGMS)
Type
Research Project (R01)
Project #
5R01GM060380-04
Application #
6636369
Study Section
Genetics Study Section (GEN)
Program Officer
Carter, Anthony D
Project Start
2000-04-01
Project End
2005-07-31
Budget Start
2003-04-01
Budget End
2005-07-31
Support Year
4
Fiscal Year
2003
Total Cost
$236,112
Indirect Cost
Name
Washington University
Department
Biology
Type
Schools of Arts and Sciences
DUNS #
068552207
City
Saint Louis
State
MO
Country
United States
Zip Code
63130
Pontvianne, Frédéric; Carpentier, Marie-Christine; Durut, Nathalie et al. (2016) Identification of Nucleolus-Associated Chromatin Domains Reveals a Role for the Nucleolus in 3D Organization of the A. thaliana Genome. Cell Rep 16:1574-1587
Mohannath, Gireesha; Pikaard, Craig S (2016) Analysis of rRNA Gene Methylation in Arabidopsis thaliana by CHEF-Conventional 2D Gel Electrophoresis. Methods Mol Biol 1455:183-202
Mohannath, Gireesha; Pontvianne, Frederic; Pikaard, Craig S (2016) Selective nucleolus organizer inactivation in Arabidopsis is a chromosome position-effect phenomenon. Proc Natl Acad Sci U S A 113:13426-13431
Chandrasekhara, Chinmayi; Mohannath, Gireesha; Blevins, Todd et al. (2016) Chromosome-specific NOR inactivation explains selective rRNA gene silencing and dosage control in Arabidopsis. Genes Dev 30:177-90
Pikaard, Craig S; Mittelsten Scheid, Ortrun (2014) Epigenetic regulation in plants. Cold Spring Harb Perspect Biol 6:a019315
Pontvianne, Frederic; Blevins, Todd; Chandrasekhara, Chinmayi et al. (2013) Subnuclear partitioning of rRNA genes between the nucleolus and nucleoplasm reflects alternative epiallelic states. Genes Dev 27:1545-50
Pikaard, Craig S (2013) Methylating the DNA of the most repressed: special access required. Mol Cell 49:1021-2
Pontvianne, Frédéric; Blevins, Todd; Chandrasekhara, Chinmayi et al. (2012) Histone methyltransferases regulating rRNA gene dose and dosage control in Arabidopsis. Genes Dev 26:945-57
Earley, Keith W; Pontvianne, Frédéric; Wierzbicki, Andrzej T et al. (2010) Mechanisms of HDA6-mediated rRNA gene silencing: suppression of intergenic Pol II transcription and differential effects on maintenance versus siRNA-directed cytosine methylation. Genes Dev 24:1119-32
Pontvianne, Frédéric; Blevins, Todd; Pikaard, Craig S (2010) Arabidopsis Histone Lysine Methyltransferases. Adv Bot Res 53:1-22

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