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GC content but not nucleosome positioning directly contributes to intron-splicing efficiency in Paramecium

View ORCID ProfileStefano Gnan, Mélody Matelot, Marion Weiman, View ORCID ProfileOlivier Arnaiz, View ORCID ProfileFrédéric Guérin, View ORCID ProfileLinda Sperling, View ORCID ProfileMireille Bétermier, View ORCID ProfileClaude Thermes, View ORCID ProfileChun-Long Chen, View ORCID ProfileSandra Duharcourt
doi: https://doi.org/10.1101/2021.08.05.455221
Stefano Gnan
1Institut Curie, Université PSL, Sorbonne Université, CNRS UMR3244, Dynamics of Genetic Information, Paris, 75005, France
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Mélody Matelot
2Université de Paris, CNRS, Institut Jacques Monod, F-75006, Paris, France
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Marion Weiman
3Université Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), 91198, Gif-sur-Yvette, France
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Olivier Arnaiz
3Université Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), 91198, Gif-sur-Yvette, France
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Frédéric Guérin
2Université de Paris, CNRS, Institut Jacques Monod, F-75006, Paris, France
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Linda Sperling
3Université Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), 91198, Gif-sur-Yvette, France
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Mireille Bétermier
3Université Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), 91198, Gif-sur-Yvette, France
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Claude Thermes
3Université Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), 91198, Gif-sur-Yvette, France
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Chun-Long Chen
1Institut Curie, Université PSL, Sorbonne Université, CNRS UMR3244, Dynamics of Genetic Information, Paris, 75005, France
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  • For correspondence: sandra.duharcourt@ijm.fr chunlong.chen@curie.fr
Sandra Duharcourt
2Université de Paris, CNRS, Institut Jacques Monod, F-75006, Paris, France
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  • For correspondence: sandra.duharcourt@ijm.fr chunlong.chen@curie.fr
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ABSTRACT

Eukaryotic genes are interrupted by introns that must be accurately spliced from mRNA precursors. With an average length of 25 nt, the >90,000 introns of Paramecium tetraurelia stand among the shortest introns reported in eukaryotes. The mechanisms specifying the correct recognition of these tiny introns remain poorly understood. Splicing can occur co-transcriptionally and it has been proposed that chromatin structure might influence splice site recognition. To investigate the roles of nucleosome positioning in intron recognition, we determined the nucleosome occupancy along the P. tetraurelia genome. We showed that P. tetraurelia displays a regular nucleosome array with a nucleosome repeat length of ∼151 bp, amongst the smallest periodicities reported. Our analysis revealed that introns are frequently associated with inter-nucleosomal DNA, pointing to an evolutionary constraint to locate introns at the AT-rich nucleosome edge sequences. Using accurate splicing efficiency data from cells depleted for the nonsense-mediated decay effectors, we showed that introns located at the edge of nucleosomes display higher splicing efficiency than those at the centre. However, multiple regression analysis indicated that the GC content, rather than nucleosome positioning, directly contributes to intron splicing efficiency. Our data reveal a complex link between GC content, nucleosome positioning and intron evolution in Paramecium.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵4 The authors wish it to be known that, in their opinion, the first 2 authors should be regarded as joint First Authors.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted August 06, 2021.
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GC content but not nucleosome positioning directly contributes to intron-splicing efficiency in Paramecium
Stefano Gnan, Mélody Matelot, Marion Weiman, Olivier Arnaiz, Frédéric Guérin, Linda Sperling, Mireille Bétermier, Claude Thermes, Chun-Long Chen, Sandra Duharcourt
bioRxiv 2021.08.05.455221; doi: https://doi.org/10.1101/2021.08.05.455221
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GC content but not nucleosome positioning directly contributes to intron-splicing efficiency in Paramecium
Stefano Gnan, Mélody Matelot, Marion Weiman, Olivier Arnaiz, Frédéric Guérin, Linda Sperling, Mireille Bétermier, Claude Thermes, Chun-Long Chen, Sandra Duharcourt
bioRxiv 2021.08.05.455221; doi: https://doi.org/10.1101/2021.08.05.455221

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