Genetic–epigenetic interplay in the determination of plant 3D genome organization

Author:

He Xiaoning1ORCID,Dias Lopes Chloé1ORCID,Pereyra-Bistrain Leonardo I12ORCID,Huang Ying1ORCID,An Jing1ORCID,Chaouche Rim Brik1,Zalzalé Hugo12,Wang Qingyi1,Ma Xing1,Antunez-Sanchez Javier3ORCID,Bergounioux Catherine1,Piquerez Sophie1,Fragkostefanakis Sotirios4ORCID,Zhang Yijing5,Zheng Shaojian6,Crespi Martin1ORCID,Mahfouz Magdy M7ORCID,Mathieu Olivier8ORCID,Ariel Federico9ORCID,Gutierrez-Marcos Jose3ORCID,Li Xingwang10ORCID,Bouché Nicolas11ORCID,Raynaud Cécile1ORCID,Latrasse David1ORCID,Benhamed Moussa1212ORCID

Affiliation:

1. Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2) , Orsay  91405 , France

2. Université de Paris Cité, Institute of Plant Sciences Paris-Saclay (IPS2) , 91190  Gif-sur-Yvette , France

3. School of Life Science, University of Warwick , Coventry CV4 7AL, UK

4. Department of Biosciences, Molecular Cell Biology of Plants, Goethe University Frankfurt am Main , Max-von-Laue Str. 9 , 60438  Frankfurt am Main, Germany

5. State Key Laboratory of Genetic Engineering, Collaborative Innovation Center of Genetics and Development, Department of Biochemistry, Institute of Plant Biology, School of Life Sciences, Fudan University , Shanghai  200438 , China

6. State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zheijang University , Hangzhou  310058 , China

7. Division of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology , Thuwal 23955 -6900, Kingdom of Saudi Arabia

8. Institute of Genetics Reproduction and Development (iGReD), Université Clermont Auvergne , CNRS, Inserm, Clermont -Ferrand, F- 63000 , France

9. Universidad de Buenos Aires (UBA), Facultad de Ciencias Exactas y Naturales, and Instituto de Fisiología, Biología Molecular y Neurociencias (IFIBYNE) , CONICET-UBA, Buenos Aires, Argentina

10. National Key Laboratory of Crop Genetic Improvment, Hubei Hongshan Laboratory, Huazhong Agricultural University , Wuhan 430070  Hubei , China

11. Université Paris-Saclay, INRAE, AgroParisTech, Institute Jean-Pierre Bourgin for Plant Sciences (IJPB) , 78000  Versailles , France

12. Institut Universitaire de France (IUF) , Orsay , France

Abstract

Abstract The 3D chromatin organization plays a major role in the control of gene expression. However, our comprehension of the governing principles behind nuclear organization remains incomplete. Particularly, the spatial segregation of loci with similar repressive transcriptional states in plants poses a significant yet poorly understood puzzle. In this study, employing a combination of genetics and advanced 3D genomics approaches, we demonstrated that a redistribution of facultative heterochromatin marks in regions usually occupied by constitutive heterochromatin marks disrupts the 3D genome compartmentalisation. This disturbance, in turn, triggers novel chromatin interactions between genic and transposable element (TE) regions. Interestingly, our results imply that epigenetic features, constrained by genetic factors, intricately mold the landscape of 3D genome organisation. This study sheds light on the profound genetic-epigenetic interplay that underlies the regulation of gene expression within the intricate framework of the 3D genome. Our findings highlight the complexity of the relationships between genetic determinants and epigenetic features in shaping the dynamic configuration of the 3D genome.

Funder

European Research Council

Agence Nationale de la Recherche

Institut Universitaire de France

Saclay Plant Sciences-SPS

China Scholar Council

Publisher

Oxford University Press (OUP)

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