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Satb2 acts as a gatekeeper for major developmental transitions during early vertebrate embryogenesis

View ORCID ProfileSaurabh J. Pradhan, View ORCID ProfilePuli Chandramouli Reddy, View ORCID ProfileMichael Smutny, View ORCID ProfileAnkita Sharma, Keisuke Sako, View ORCID ProfileMeghana S. Oak, View ORCID ProfileRini Shah, View ORCID ProfileMrinmoy Pal, Ojas Deshpande, Yin Tang, View ORCID ProfileRakesh Mishra, View ORCID ProfileGirish Deshpande, View ORCID ProfileAntonio J. Giraldez, Mahendra Sonawane, View ORCID ProfileCarl-Philipp Heisenberg, View ORCID ProfileSanjeev Galande
doi: https://doi.org/10.1101/2020.11.23.394171
Saurabh J. Pradhan
1Centre of Excellence in Epigenetics, Department of Biology, Indian Institute of Science Education and Research, Pune, 411008 India
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Puli Chandramouli Reddy
1Centre of Excellence in Epigenetics, Department of Biology, Indian Institute of Science Education and Research, Pune, 411008 India
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Michael Smutny
2Institute of Science and Technology Austria, Klosterneuburg, Austria
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Ankita Sharma
1Centre of Excellence in Epigenetics, Department of Biology, Indian Institute of Science Education and Research, Pune, 411008 India
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Keisuke Sako
2Institute of Science and Technology Austria, Klosterneuburg, Austria
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Meghana S. Oak
3Indian Institute of Science Education and Research, Kolkata, 741246 India
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Rini Shah
1Centre of Excellence in Epigenetics, Department of Biology, Indian Institute of Science Education and Research, Pune, 411008 India
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Mrinmoy Pal
1Centre of Excellence in Epigenetics, Department of Biology, Indian Institute of Science Education and Research, Pune, 411008 India
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Ojas Deshpande
1Centre of Excellence in Epigenetics, Department of Biology, Indian Institute of Science Education and Research, Pune, 411008 India
4Department of Biological Sciences, Tata Institute of Fundamental Research, Homi Bhabha Road, Mumbai 400 005, India
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Yin Tang
5Department of Genetics, Yale University School of Medicine, New Haven, CT, USA
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Rakesh Mishra
6Centre for Cellular and Molecular Biology, Uppal Road, Hyderabad, India
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Girish Deshpande
7Department of Molecular Biology, Princeton University, Princeton, NJ 08540, USA
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Antonio J. Giraldez
5Department of Genetics, Yale University School of Medicine, New Haven, CT, USA
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Mahendra Sonawane
4Department of Biological Sciences, Tata Institute of Fundamental Research, Homi Bhabha Road, Mumbai 400 005, India
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Carl-Philipp Heisenberg
2Institute of Science and Technology Austria, Klosterneuburg, Austria
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  • For correspondence: heisenberg@ist.ac.at sanjeev@iiserpune.ac.in
Sanjeev Galande
1Centre of Excellence in Epigenetics, Department of Biology, Indian Institute of Science Education and Research, Pune, 411008 India
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  • For correspondence: heisenberg@ist.ac.at sanjeev@iiserpune.ac.in
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Abstract

Zygotic genome activation (ZGA) initiates regionalized transcription responsible for the acquisition of distinct cellular identities. ZGA is dependent upon dynamic chromatin architecture sculpted by conserved DNA-binding proteins. However, whether the tissue-specific transcription is mechanistically linked with the onset of ZGA is unknown. Here, we have addressed the involvement of chromatin organizer SATB2 in orchestrating these processes during vertebrate embryogenesis. Integrative analysis of transcriptome, genome-wide occupancy and chromatin accessibility revealed contrasting molecular functions of maternal and zygotic pools of Satb2. Maternal Satb2 represses zygotic genes by influencing the interplay between the pluripotency factors. By contrast, zygotic Satb2 activates transcription of the same group of genes during neural crest development and organogenesis. Comparative analysis of maternal versus zygotic function of Satb2 underscores how these antithetical activities are temporally coordinated and functionally implemented. We discuss the evolutionary implications of the biphasic and bimodal regulation of landmark developmental transitions by a single determinant.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵8 Lead contact.

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Posted November 23, 2020.
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Satb2 acts as a gatekeeper for major developmental transitions during early vertebrate embryogenesis
Saurabh J. Pradhan, Puli Chandramouli Reddy, Michael Smutny, Ankita Sharma, Keisuke Sako, Meghana S. Oak, Rini Shah, Mrinmoy Pal, Ojas Deshpande, Yin Tang, Rakesh Mishra, Girish Deshpande, Antonio J. Giraldez, Mahendra Sonawane, Carl-Philipp Heisenberg, Sanjeev Galande
bioRxiv 2020.11.23.394171; doi: https://doi.org/10.1101/2020.11.23.394171
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Satb2 acts as a gatekeeper for major developmental transitions during early vertebrate embryogenesis
Saurabh J. Pradhan, Puli Chandramouli Reddy, Michael Smutny, Ankita Sharma, Keisuke Sako, Meghana S. Oak, Rini Shah, Mrinmoy Pal, Ojas Deshpande, Yin Tang, Rakesh Mishra, Girish Deshpande, Antonio J. Giraldez, Mahendra Sonawane, Carl-Philipp Heisenberg, Sanjeev Galande
bioRxiv 2020.11.23.394171; doi: https://doi.org/10.1101/2020.11.23.394171

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