Arabidopsis ATRX Modulates H3.3 Occupancy and Fine-Tunes Gene Expression

Handle URI:
http://hdl.handle.net/10754/625666
Title:
Arabidopsis ATRX Modulates H3.3 Occupancy and Fine-Tunes Gene Expression
Authors:
Duc, Céline ( 0000-0001-7426-4541 ) ; Benoit, Matthias ( 0000-0002-3958-3173 ) ; Détourné, Gwénaëlle ( 0000-0001-8328-7059 ) ; Simon, Lauriane ( 0000-0001-7285-9437 ) ; Poulet, Axel ( 0000-0002-3415-8960 ) ; Jung, Matthieu ( 0000-0002-3272-7322 ) ; Veluchamy, Alaguraj ( 0000-0002-5349-5794 ) ; Latrasse, David ( 0000-0003-2149-0128 ) ; Le Goff, Samuel ( 0000-0002-9991-6435 ) ; Cotterell, Sylviane ( 0000-0001-9665-5009 ) ; Tatout, Christophe ( 0000-0001-5215-2338 ) ; Benhamed, Moussa ( 0000-0002-4181-1702 ) ; Probst, Aline V. ( 0000-0001-9534-8058 )
Abstract:
Histones are essential components of the nucleosome, the major chromatin subunit that structures linear DNA molecules and regulates access of other proteins to DNA. Specific histone chaperone complexes control the correct deposition of canonical histones and their variants to modulate nucleosome structure and stability. In this study, we characterize the Arabidopsis Alpha Thalassemia-mental Retardation X-linked (ATRX) ortholog and show that ATRX is involved in histone H3 deposition. Arabidopsis ATRX mutant alleles are viable, but show developmental defects and reduced fertility. Their combination with mutants of the histone H3.3 chaperone HIRA (Histone Regulator A) results in impaired plant survival, suggesting that HIRA and ATRX function in complementary histone deposition pathways. Indeed, ATRX loss of function alters cellular histone H3.3 pools and in consequence modulates the H3.1/H3.3 balance in the cell. H3.3 levels are affected especially at genes characterized by elevated H3.3 occupancy, including the 45S ribosomal DNA (45S rDNA) loci, where loss of ATRX results in altered expression of specific 45S rDNA sequence variants. At the genome-wide scale, our data indicate that ATRX modifies gene expression concomitantly to H3.3 deposition at a set of genes characterized both by elevated H3.3 occupancy and high expression. Altogether, our results show that ATRX is involved in H3.3 deposition and emphasize the role of histone chaperones in adjusting genome expression.
KAUST Department:
Division of Biological and Environmental Sciences and Engineering
Citation:
Duc C, Benoit M, Détourné G, Simon L, Poulet A, et al. (2017) Arabidopsis ATRX Modulates H3.3 Occupancy and Fine-Tunes Gene Expression. The Plant Cell 29: 1773–1793. Available: http://dx.doi.org/10.1105/tpc.16.00877.
Publisher:
American Society of Plant Biologists (ASPB)
Journal:
The Plant Cell
Issue Date:
7-Jul-2017
DOI:
10.1105/tpc.16.00877
Type:
Article
ISSN:
1040-4651; 1532-298X
Sponsors:
We thank S. Amiard for seeds and help with the EdU detection, HU and gamma irradiation experiments, P. Pouchin and N. Goué for help with bioinformatics analyses, A. Lhomme for technical assistance, E. Vanrobays for the NLS-GFP construct, O. Mittelsten Scheid for critical reading of the manuscript and F. Pontvianne for valuable advice with 45S rDNA variant analysis and for critical reading of the manuscript. The RNA Sequencing was performed by the IGBMC Microarray and Sequencing platform, a member of the ‘France Génomique’ consortium (ANR-10-INBS-0009). This work was supported by doctoral stipends from the Region Auvergne, ANR grant ‘Dynam’Het’ ANR-11 JSV2 009 01 and ‘SINODYN’ ANR-12 ISV6 0001. This work was further supported by the Centre National de la Recherche Scientifique, the Institut National de la Santé et de la Recherche Médicale and Université Clermont Auvergne.
Additional Links:
http://www.plantcell.org/content/early/2017/07/06/tpc.16.00877
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Full metadata record

DC FieldValue Language
dc.contributor.authorDuc, Célineen
dc.contributor.authorBenoit, Matthiasen
dc.contributor.authorDétourné, Gwénaëlleen
dc.contributor.authorSimon, Laurianeen
dc.contributor.authorPoulet, Axelen
dc.contributor.authorJung, Matthieuen
dc.contributor.authorVeluchamy, Alagurajen
dc.contributor.authorLatrasse, Daviden
dc.contributor.authorLe Goff, Samuelen
dc.contributor.authorCotterell, Sylvianeen
dc.contributor.authorTatout, Christopheen
dc.contributor.authorBenhamed, Moussaen
dc.contributor.authorProbst, Aline V.en
dc.date.accessioned2017-10-03T12:49:32Z-
dc.date.available2017-10-03T12:49:32Z-
dc.date.issued2017-07-07en
dc.identifier.citationDuc C, Benoit M, Détourné G, Simon L, Poulet A, et al. (2017) Arabidopsis ATRX Modulates H3.3 Occupancy and Fine-Tunes Gene Expression. The Plant Cell 29: 1773–1793. Available: http://dx.doi.org/10.1105/tpc.16.00877.en
dc.identifier.issn1040-4651en
dc.identifier.issn1532-298Xen
dc.identifier.doi10.1105/tpc.16.00877en
dc.identifier.urihttp://hdl.handle.net/10754/625666-
dc.description.abstractHistones are essential components of the nucleosome, the major chromatin subunit that structures linear DNA molecules and regulates access of other proteins to DNA. Specific histone chaperone complexes control the correct deposition of canonical histones and their variants to modulate nucleosome structure and stability. In this study, we characterize the Arabidopsis Alpha Thalassemia-mental Retardation X-linked (ATRX) ortholog and show that ATRX is involved in histone H3 deposition. Arabidopsis ATRX mutant alleles are viable, but show developmental defects and reduced fertility. Their combination with mutants of the histone H3.3 chaperone HIRA (Histone Regulator A) results in impaired plant survival, suggesting that HIRA and ATRX function in complementary histone deposition pathways. Indeed, ATRX loss of function alters cellular histone H3.3 pools and in consequence modulates the H3.1/H3.3 balance in the cell. H3.3 levels are affected especially at genes characterized by elevated H3.3 occupancy, including the 45S ribosomal DNA (45S rDNA) loci, where loss of ATRX results in altered expression of specific 45S rDNA sequence variants. At the genome-wide scale, our data indicate that ATRX modifies gene expression concomitantly to H3.3 deposition at a set of genes characterized both by elevated H3.3 occupancy and high expression. Altogether, our results show that ATRX is involved in H3.3 deposition and emphasize the role of histone chaperones in adjusting genome expression.en
dc.description.sponsorshipWe thank S. Amiard for seeds and help with the EdU detection, HU and gamma irradiation experiments, P. Pouchin and N. Goué for help with bioinformatics analyses, A. Lhomme for technical assistance, E. Vanrobays for the NLS-GFP construct, O. Mittelsten Scheid for critical reading of the manuscript and F. Pontvianne for valuable advice with 45S rDNA variant analysis and for critical reading of the manuscript. The RNA Sequencing was performed by the IGBMC Microarray and Sequencing platform, a member of the ‘France Génomique’ consortium (ANR-10-INBS-0009). This work was supported by doctoral stipends from the Region Auvergne, ANR grant ‘Dynam’Het’ ANR-11 JSV2 009 01 and ‘SINODYN’ ANR-12 ISV6 0001. This work was further supported by the Centre National de la Recherche Scientifique, the Institut National de la Santé et de la Recherche Médicale and Université Clermont Auvergne.en
dc.publisherAmerican Society of Plant Biologists (ASPB)en
dc.relation.urlhttp://www.plantcell.org/content/early/2017/07/06/tpc.16.00877en
dc.titleArabidopsis ATRX Modulates H3.3 Occupancy and Fine-Tunes Gene Expressionen
dc.typeArticleen
dc.contributor.departmentDivision of Biological and Environmental Sciences and Engineeringen
dc.identifier.journalThe Plant Cellen
dc.contributor.institutionCNRS 24 avenue des Landais CITY: Aubiere POSTAL_CODE: 63171 Cedex France [FR].en
dc.contributor.institutionSainsbury Laboratory - University of Cambridge CITY: Cambridge United Kingdom [GB].en
dc.contributor.institutionCNRS CITY: Aubiere France [FR].en
dc.contributor.institutionGReD - CNRS UMR6293 - INSERM U1103 - Clermont University CITY: clermont ferrand France [FR].en
dc.contributor.institutionGReD - CNRS UMR6293 - INSERM U1103 - Clermont University CITY: Aubière France [FR].en
dc.contributor.institutionDepartment of Functional Genomics and Cancer, Institut de Gé nétique et de Biologie Moléculaire et Cellulaire, CNRS/INSERM/ULP CITY: Illkirch France [FR].en
dc.contributor.institutionUniversité Paris Sud CITY: Orsay France [FR].en
dc.contributor.institutionUniversité Paris Sud CITY: ORSAY POSTAL_CODE: 91405 France [FR].en
dc.contributor.institutionGReD, Université Clermont Auvergne, CNRS, INSERM CITY: Clermont-Ferrand POSTAL_CODE: 63001 France [FR].en
kaust.authorVeluchamy, Alagurajen
kaust.authorBenhamed, Moussaen
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