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

Céline Duc; Matthias Benoit; Gwénaëlle Détourné; Lauriane Simon; Axel Poulet; Matthieu Jung; Alaguraj Veluchamy; David Latrasse; Samuel Le Goff; Sylviane Cotterell; Christophe Tatout; Moussa Benhamed; Aline V. Probst

doi:10.1105/tpc.16.00877

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

Céline Duc, Matthias Benoit, Gwénaëlle Détourné, Lauriane Simon, Axel Poulet, Matthieu Jung, Alaguraj Veluchamy, David Latrasse, Samuel Le Goff, Sylviane Cotterell, Christophe Tatout, Moussa Benhamed, Aline V. Probst

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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.

Original language	English (US)
Pages (from-to)	1773-1793
Number of pages	21
Journal	The Plant Cell
Volume	29
Issue number	7
DOIs	https://doi.org/10.1105/tpc.16.00877
State	Published - Jul 6 2017

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: 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.

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@article{18365c8d755e4f219f12f9472cbcbc79,

title = "Arabidopsis ATRX Modulates H3.3 Occupancy and Fine-Tunes Gene Expression",

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.",

author = "C{\'e}line Duc and Matthias Benoit and Gw{\'e}na{\"e}lle D{\'e}tourn{\'e} and Lauriane Simon and Axel Poulet and Matthieu Jung and Alaguraj Veluchamy and David Latrasse and {Le Goff}, Samuel and Sylviane Cotterell and Christophe Tatout and Moussa Benhamed and Probst, {Aline V.}",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We thank S. Amiard for seeds and help with the EdU detection, HU and gamma irradiation experiments, P. Pouchin and N. Gou{\'e} 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 {\textquoteleft}France G{\'e}nomique{\textquoteright} consortium (ANR-10-INBS-0009). This work was supported by doctoral stipends from the Region Auvergne, ANR grant {\textquoteleft}Dynam{\textquoteright}Het{\textquoteright} ANR-11 JSV2 009 01 and {\textquoteleft}SINODYN{\textquoteright} ANR-12 ISV6 0001. This work was further supported by the Centre National de la Recherche Scientifique, the Institut National de la Sant{\'e} et de la Recherche M{\'e}dicale and Universit{\'e} Clermont Auvergne.",

year = "2017",

month = jul,

day = "6",

doi = "10.1105/tpc.16.00877",

language = "English (US)",

volume = "29",

pages = "1773--1793",

journal = "The Plant Cell",

issn = "1040-4651",

publisher = "American Society of Plant Biologists",

number = "7",

}

TY - JOUR

T1 - Arabidopsis ATRX Modulates H3.3 Occupancy and Fine-Tunes Gene Expression

AU - Duc, Céline

AU - Benoit, Matthias

AU - Détourné, Gwénaëlle

AU - Simon, Lauriane

AU - Poulet, Axel

AU - Jung, Matthieu

AU - Veluchamy, Alaguraj

AU - Latrasse, David

AU - Le Goff, Samuel

AU - Cotterell, Sylviane

AU - Tatout, Christophe

AU - Benhamed, Moussa

AU - Probst, Aline V.

N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: 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.

PY - 2017/7/6

Y1 - 2017/7/6

N2 - 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.

AB - 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.

UR - http://hdl.handle.net/10754/625666

UR - http://www.plantcell.org/content/early/2017/07/06/tpc.16.00877

UR - http://www.scopus.com/inward/record.url?scp=85027411373&partnerID=8YFLogxK

U2 - 10.1105/tpc.16.00877

DO - 10.1105/tpc.16.00877

M3 - Article

C2 - 28684426

SN - 1040-4651

VL - 29

SP - 1773

EP - 1793

JO - The Plant Cell

JF - The Plant Cell

IS - 7

ER -

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

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