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

Pradhan, Saurabh J.; Reddy, Puli Chandramouli; Smutny, Michael; Sharma, Ankita; Sako, Keisuke; Oak, Meghana S.; Shah, Rini; Pal, Mrinmoy; Deshpande, Ojas; Dsilva, Greg; Tang, Yin; Mishra, Rakesh; Deshpande, Girish; Giraldez, Antonio J.; Sonawane, Mahendra; Heisenberg, Carl-Philipp J; Galande, Sanjeev

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

Pradhan SJ, Reddy PC, Smutny M, Sharma A, Sako K, Oak MS, Shah R, Pal M, Deshpande O, Dsilva G, Tang Y, Mishra R, Deshpande G, Giraldez AJ, Sonawane M, Heisenberg C-PJ, Galande S. 2021. Satb2 acts as a gatekeeper for major developmental transitions during early vertebrate embryogenesis. Nature Communications. 12(1), 6094.

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DOI

10.1038/s41467-021-26234-7

Journal Article | Published | English

Scopus indexed

Author

Pradhan, Saurabh J.; Reddy, Puli Chandramouli; Smutny, Michael^ISTA ; Sharma, Ankita; Sako, Keisuke^ISTA ; Oak, Meghana S.; Shah, Rini; Pal, Mrinmoy; Deshpande, Ojas; Dsilva, Greg; Tang, Yin; Mishra, Rakesh
All

Corresponding author has ISTA affiliation

Department

Heisenberg Group

Abstract

Zygotic genome activation (ZGA) initiates regionalized transcription underlying distinct cellular identities. ZGA is dependent upon dynamic chromatin architecture sculpted by conserved DNA-binding proteins. However, the direct mechanistic link between the onset of ZGA and the tissue-specific transcription remains unclear. Here, we have addressed the involvement of chromatin organizer Satb2 in orchestrating both processes during zebrafish embryogenesis. Integrative analysis of transcriptome, genome-wide occupancy and chromatin accessibility reveals contrasting molecular activities of maternally deposited and zygotically synthesized Satb2. Maternal Satb2 prevents premature transcription of 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. Thus, our comparative analysis of maternal versus zygotic function of Satb2 underscores how these antithetical activities are temporally coordinated and functionally implemented highlighting the evolutionary implications of the biphasic and bimodal regulation of landmark developmental transitions by a single determinant.

Publishing Year

2021

Date Published

2021-10-19

Journal Title

Nature Communications

Publisher

Springer Nature

Acknowledgement

We are grateful to the members of C.-P.H. and SG lab for discussions. Authors thank Shubha Tole for providing embryonic mouse tissues. Authors are grateful to Alessandro Mongera and Chetana Sachidanandan for generous help with Tg: Sox10: GFP line. Authors would like to thank Satyajeet Khare, Vanessa Barone, Jyothish S., Shalini Mishra, Yoshita Bhide, and Keshav Jha for assistance in experiments. We would also like to thank Chaitanya Dingare for valuable suggestions. We thank Diana Pinhiero and Alexandra Schauer for critical reading of early versions of the manuscript. This work was supported by the Centre of Excellence in Epigenetics program of the Department of Biotechnology, Government of India Phase I (BT/01/COE/09/07) to S.G. and R.K.M., and Phase II (BT/COE/34/SP17426/2016) to S.G. and JC Bose Fellowship (JCB/2019/000013) from Science and Engineering Research Board, Government of India to S.G., DST-BMWF Indo-Austrian bilateral program grant to S.G. and C.-P.H. The work using animal models was partly supported by the infrastructure support grants from the Department of Biotechnology (National Facility for Laboratory Model Organisms: BT/INF/22/SP17358/2016 and Establishment of a Pune Biotech Cluster, Model Organism to Human Disease: B-2 Whole Animal Imaging & Tissue Processing FacilityBT/Pune-Biocluster/01/2015). S.J.P. was supported by Fellowship from the Council of Scientific and Industrial Research, India and travel fellowship from the Company of Biologists, UK. P.C.R. was supported by the Early Career Fellowship of the Wellcome Trust-DBT India Alliance (IA/E/16/1/503057). A.S. was supported by UGC and R.S. was supported by CSIR India. M.S. was supported by core funding from the Tata Institute of Fundamental Research (TIFR 12P-121).

Volume

Issue

Article Number

6094

eISSN

20411723

IST-REx-ID

10202

Cite this

Pradhan SJ, Reddy PC, Smutny M, et al. Satb2 acts as a gatekeeper for major developmental transitions during early vertebrate embryogenesis. Nature Communications. 2021;12(1). doi:10.1038/s41467-021-26234-7

Pradhan, S. J., Reddy, P. C., Smutny, M., Sharma, A., Sako, K., Oak, M. S., … Galande, S. (2021). Satb2 acts as a gatekeeper for major developmental transitions during early vertebrate embryogenesis. Nature Communications. Springer Nature. https://doi.org/10.1038/s41467-021-26234-7

Pradhan, Saurabh J., Puli Chandramouli Reddy, Michael Smutny, Ankita Sharma, Keisuke Sako, Meghana S. Oak, Rini Shah, et al. “Satb2 Acts as a Gatekeeper for Major Developmental Transitions during Early Vertebrate Embryogenesis.” Nature Communications. Springer Nature, 2021. https://doi.org/10.1038/s41467-021-26234-7.

S. J. Pradhan et al., “Satb2 acts as a gatekeeper for major developmental transitions during early vertebrate embryogenesis,” Nature Communications, vol. 12, no. 1. Springer Nature, 2021.

Pradhan, Saurabh J., et al. “Satb2 Acts as a Gatekeeper for Major Developmental Transitions during Early Vertebrate Embryogenesis.” Nature Communications, vol. 12, no. 1, 6094, Springer Nature, 2021, doi:10.1038/s41467-021-26234-7.

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