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The canonical E2Fs together with RETINOBLASTOMA-RELATED are required to establish quiescence during plant development

Magdolna Gombos, Cécile Raynaud, Yuji Nomoto, Eszter Molnár, Rim Brik-Chaouche, Hirotomo Takatsuka, Ahmad Zaki, Dóri Bernula, David Latrasse, Keito Mineta, Fruzsina Nagy, Xiaoning He, Hidekazu Iwakawa, Erika Őszi, Jing An, Takamasa Suzuki, Csaba Papdi, Clara Bergis, View ORCID ProfileMoussa Benhamed, View ORCID ProfileLászló Bögre, View ORCID ProfileMasaki Ito, Zoltán Magyar
doi: https://doi.org/10.1101/2022.12.05.519120
Magdolna Gombos
1Institute of Plant Biology, Biological Research Centre, H-6726 Szeged, Hungary
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Cécile Raynaud
2Université Paris-Saclay, CNRS, INRAE, Université Evry, Institute of Plant Sciences Paris-Saclay (IPS2), 91190, Gif sur Yvette, France
3Université de Paris Cité, CNRS, INRAE, Institute of Plant Sciences Paris-Saclay (IPS2), 91190, Gif sur Yvette, France
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Yuji Nomoto
4School of Biological Science and Technology, College of Science and Engineering, Kanazawa University, Kakuma-machi, Kanazawa, 920-1192 Japan
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Eszter Molnár
1Institute of Plant Biology, Biological Research Centre, H-6726 Szeged, Hungary
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Rim Brik-Chaouche
2Université Paris-Saclay, CNRS, INRAE, Université Evry, Institute of Plant Sciences Paris-Saclay (IPS2), 91190, Gif sur Yvette, France
3Université de Paris Cité, CNRS, INRAE, Institute of Plant Sciences Paris-Saclay (IPS2), 91190, Gif sur Yvette, France
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Hirotomo Takatsuka
4School of Biological Science and Technology, College of Science and Engineering, Kanazawa University, Kakuma-machi, Kanazawa, 920-1192 Japan
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Ahmad Zaki
5Royal Holloway, University of London, Department of Biological Sciences, Egham, Surrey TW20 0EX, UK
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Dóri Bernula
1Institute of Plant Biology, Biological Research Centre, H-6726 Szeged, Hungary
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David Latrasse
2Université Paris-Saclay, CNRS, INRAE, Université Evry, Institute of Plant Sciences Paris-Saclay (IPS2), 91190, Gif sur Yvette, France
3Université de Paris Cité, CNRS, INRAE, Institute of Plant Sciences Paris-Saclay (IPS2), 91190, Gif sur Yvette, France
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Keito Mineta
4School of Biological Science and Technology, College of Science and Engineering, Kanazawa University, Kakuma-machi, Kanazawa, 920-1192 Japan
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Fruzsina Nagy
1Institute of Plant Biology, Biological Research Centre, H-6726 Szeged, Hungary
6Doctoral School in Biology, Faculty of Science and Informatics, University of Szeged, H-6726 Szeged, Hungary
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Xiaoning He
2Université Paris-Saclay, CNRS, INRAE, Université Evry, Institute of Plant Sciences Paris-Saclay (IPS2), 91190, Gif sur Yvette, France
3Université de Paris Cité, CNRS, INRAE, Institute of Plant Sciences Paris-Saclay (IPS2), 91190, Gif sur Yvette, France
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Hidekazu Iwakawa
4School of Biological Science and Technology, College of Science and Engineering, Kanazawa University, Kakuma-machi, Kanazawa, 920-1192 Japan
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Erika Őszi
1Institute of Plant Biology, Biological Research Centre, H-6726 Szeged, Hungary
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Jing An
2Université Paris-Saclay, CNRS, INRAE, Université Evry, Institute of Plant Sciences Paris-Saclay (IPS2), 91190, Gif sur Yvette, France
3Université de Paris Cité, CNRS, INRAE, Institute of Plant Sciences Paris-Saclay (IPS2), 91190, Gif sur Yvette, France
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Takamasa Suzuki
7College of Bioscience and Biotechnology, Chubu University, Kasugai, Aichi 487-8501, Japan
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Csaba Papdi
5Royal Holloway, University of London, Department of Biological Sciences, Egham, Surrey TW20 0EX, UK
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Clara Bergis
2Université Paris-Saclay, CNRS, INRAE, Université Evry, Institute of Plant Sciences Paris-Saclay (IPS2), 91190, Gif sur Yvette, France
3Université de Paris Cité, CNRS, INRAE, Institute of Plant Sciences Paris-Saclay (IPS2), 91190, Gif sur Yvette, France
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Moussa Benhamed
2Université Paris-Saclay, CNRS, INRAE, Université Evry, Institute of Plant Sciences Paris-Saclay (IPS2), 91190, Gif sur Yvette, France
3Université de Paris Cité, CNRS, INRAE, Institute of Plant Sciences Paris-Saclay (IPS2), 91190, Gif sur Yvette, France
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  • ORCID record for Moussa Benhamed
László Bögre
5Royal Holloway, University of London, Department of Biological Sciences, Egham, Surrey TW20 0EX, UK
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Masaki Ito
4School of Biological Science and Technology, College of Science and Engineering, Kanazawa University, Kakuma-machi, Kanazawa, 920-1192 Japan
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Zoltán Magyar
1Institute of Plant Biology, Biological Research Centre, H-6726 Szeged, Hungary
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  • For correspondence: magyarz@brc.hu
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Abstract

Maintaining stable and transient quiescence in differentiated and stem cells, respectively, requires repression of the cell cycle. The plant RETINOBLASTOMA-RELATED (RBR) has been implicated in stem cell maintenance, presumably by forming repressor complexes with E2F transcription factors. Surprisingly we find that mutations in all three canonical E2Fs do not compromise the cell cycle, but similarly to RBR silencing, result in overproliferation. Contrary to the growth arrest upon RBR silencing, when exit from proliferation to differentiation is inhibited, the e2fabc mutant develops enlarged organs with supernumerary stem and differentiated cells as the quiescence is compromised. While E2F, RBR and the M-phase regulatory MYB3Rs are part of the DREAM repressor complexes, and recruited to overlapping groups of targets, they regulate distinct sets of genes. Only the loss of E2Fs but not the MYB3Rs interferes with quiescence, which might be due to the ability of E2Fs to control both G1-S and some key G2-M targets. We conclude that collectively the three canonical E2Fs in complex with RBR have central roles in establishing cellular quiescence during organ development, leading to enhanced plant growth.

Competing Interest Statement

The authors have declared no competing interest.

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 December 06, 2022.
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The canonical E2Fs together with RETINOBLASTOMA-RELATED are required to establish quiescence during plant development
Magdolna Gombos, Cécile Raynaud, Yuji Nomoto, Eszter Molnár, Rim Brik-Chaouche, Hirotomo Takatsuka, Ahmad Zaki, Dóri Bernula, David Latrasse, Keito Mineta, Fruzsina Nagy, Xiaoning He, Hidekazu Iwakawa, Erika Őszi, Jing An, Takamasa Suzuki, Csaba Papdi, Clara Bergis, Moussa Benhamed, László Bögre, Masaki Ito, Zoltán Magyar
bioRxiv 2022.12.05.519120; doi: https://doi.org/10.1101/2022.12.05.519120
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The canonical E2Fs together with RETINOBLASTOMA-RELATED are required to establish quiescence during plant development
Magdolna Gombos, Cécile Raynaud, Yuji Nomoto, Eszter Molnár, Rim Brik-Chaouche, Hirotomo Takatsuka, Ahmad Zaki, Dóri Bernula, David Latrasse, Keito Mineta, Fruzsina Nagy, Xiaoning He, Hidekazu Iwakawa, Erika Őszi, Jing An, Takamasa Suzuki, Csaba Papdi, Clara Bergis, Moussa Benhamed, László Bögre, Masaki Ito, Zoltán Magyar
bioRxiv 2022.12.05.519120; doi: https://doi.org/10.1101/2022.12.05.519120

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