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Odd-paired is a pioneer-like factor that coordinates with Zelda to control gene expression in embryos

Koromila, Theodora and Gao, Fan and Iwasaki, Yasuno and He, Peng and Pachter, Lior and Gergen, J. Peter and Stathopoulos, Angelike (2020) Odd-paired is a pioneer-like factor that coordinates with Zelda to control gene expression in embryos. eLife, 9 . Art. No. e59610. ISSN 2050-084X. https://resolver.caltech.edu/CaltechAUTHORS:20191125-141648000

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Abstract

Pioneer factors such as Zelda (Zld) help initiate zygotic transcription in Drosophila early embryos, but whether other factors support this dynamic process is unclear. Odd-paired (Opa), a zinc-finger transcription factor expressed at cellularization, controls the transition of genes from pair-rule to segmental patterns along the anterior-posterior axis. Finding that Opa also regulates expression through enhancer sog_Distal along the dorso-ventral axis, we hypothesized Opa’s role is more general. Chromatin-immunoprecipitation (ChIP-seq) confirmed its in vivo binding to sog_Distal but also identified widespread binding throughout the genome, comparable to Zld. Furthermore, chromatin assays (ATAC-seq) demonstrate that Opa, like Zld, influences chromatin accessibility genome-wide at cellularization, suggesting both are pioneer factors with common as well as distinct targets. Lastly, embryos lacking opa exhibit widespread, late patterning defects spanning both axes. Collectively, these data suggest Opa is a general timing factor and likely late-acting pioneer factor that drives a secondary wave of zygotic gene expression.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.7554/eLife.59610DOIArticle
https://doi.org/10.1101/853028DOIDiscussion Paper
https://github.com/gaofan83/Stathopoulos_LabRelated ItemCode
https://github.com/caltech-bioinformatics-resource-center/Stathopoulos_LabRelated ItemCode
ORCID:
AuthorORCID
Koromila, Theodora0000-0001-5504-1369
Pachter, Lior0000-0002-9164-6231
Stathopoulos, Angelike0000-0001-6597-2036
Alternate Title:Late-acting pioneer factor Opa, Odd-paired is a late-acting pioneer factor coordinating with Zelda to broadly regulate gene expression in early embryos
Additional Information:© 2020 Koromila et al. This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited. Received: 26 November 2019; Accepted: 22 July 2020; Published: 23 July 2020. We thank Chris Rushlow and Deborah Hursh for sharing fly stocks, Igor Antoshechkin and Henry Amrhein at the Millard and Muriel Jacobs Genetics and Genomics Laboratory at the California Institute of Technology for sequencing support, the lab of Josh Dubnau for assistance with Bioanalyzer samples, David Carlson and the Institute for Advanced Computational Science at the Stony Brook University, and Susie Newcomb, Leslie Dunipace and Frank Macabenta for assistance with experiments and comments on the manuscript. This study was supported by funding from NIH R35GM118146 and R03HD097535 to AS, the Bioinformatics Resource Center at the Beckman Institute of Caltech to FG and LP, and the Stony Brook University College of Arts and Sciences to JPG. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. Author contributions: Theodora Koromila, Conceived the project and planned the experimental approach, performed wet experiments except ChIP-seq, oversaw computational approach, carried out quantitative analysis of imaging data, analyzed data, wrote manuscript with input and editing help from FG, YI, PH, LP and JPG.; Fan Gao, Oversaw computational approach, performed all computational analysis except normalization of ATAC-seq data for visualization of individual loci, ATAC-seq peak calling, and nucleosome signature, analyzed data, gave input and editing help for writing the manuscript.; Yasuno Iwasaki, Performed ChIP-seq experiments with support of the Caltech genomics core, conducted an initial, independent analysis of the Opa-ChIP-seq data that first identified the new 7 bp consensus binding motif for Opa, gave input and editing help for writing the manuscript.; Peng He, Oversaw computational approach, conducted normalization of ATAC-seq data for visualization of individual loci, ATAC-seq peak calling, and nucleosome signature, analyzed data, gave input and editing help for writing the manuscript.; Lior Pachter, J Peter Gergen, Gave input and editing help for writing the manuscript.; Angelike Stathopoulos, Conceived the project and planned the experimental approach, directed the project, analyzed data, wrote manuscript with input and editing help from FG, YI, PH, LP and JPG. Data availability: GEO accession number SuperSeries GSE153329. SubSeries: ChIP-seq and singled-end ATAC-seq (GSE140722), and RNA-seq and paired-end ATAC-seq data access (GSE153328). The codes for RNA-seq, Opa ChIP-seq and ATAC-seq processing (alignment and peak calling) were uploaded to github: https://github.com/caltech-bioinformatics-resource-center/Stathopoulos_Lab (copy archived at https://github.com/elifesciences-publications/Stathopoulos_Lab).
Group:Millard and Muriel Jacobs Genetics and Genomics Laboratory
Funders:
Funding AgencyGrant Number
NIHR35GM118146
NIHR03HD097535
Caltech Beckman InstituteUNSPECIFIED
Stony Brook UniversityUNSPECIFIED
Subject Keywords:Drosophila melanogaster, Odd-paired (Opa), Zelda, maternal-to-zygotic transition (MZT), midblastula transition (MBT), short gastrulation (sog), ChIP-seq, RNA-seq, ATAC-seq, Histone mark
Record Number:CaltechAUTHORS:20191125-141648000
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20191125-141648000
Official Citation:Odd-paired is a pioneer-like factor that coordinates with Zelda to control gene expression in embryos. eLife 2020; 9:e59610 DOI: 10.7554/eLife.59610
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:100041
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:25 Nov 2019 23:22
Last Modified:12 Aug 2020 15:18

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