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Diverse logics and grammar encode notochord enhancers.

Benjamin P Song1, Michelle F Ragsac2, Krissie Tellez3

  • 1Department of Medicine, Health Sciences, University of California San Diego, La Jolla, CA 92093, USA; Department of Molecular Biology, Biological Sciences, University of California San Diego, La Jolla, CA 92093, USA; Biological Sciences Graduate Program, University of California San Diego, La Jolla, CA 92093, USA.

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|February 2, 2023
PubMed
Summary

This study reveals that the specific arrangement, or grammar, of transcription factor binding sites is crucial for notochord development in chordates. This conserved enhancer logic is essential for gene regulation across species.

Keywords:
Brachyury:TCP: Developmental biologyCP: Molecular biologyCionaETSFoxAMPRAZicenhancerenhancer grammarenhancer logicenhancer randomizationlamininlow-affinitynotochord

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Area of Science:

  • Developmental Biology
  • Genetics
  • Evolutionary Biology

Background:

  • The notochord, a key structure in chordates, requires precise gene regulation for its development.
  • Transcription factors like Zic and ETS are known to control gene activity in the notochord.
  • Understanding how these factors regulate enhancers is vital for deciphering developmental processes.

Purpose of the Study:

  • To investigate how Zic and ETS binding sites within genomic elements dictate notochord activity.
  • To identify and characterize enhancers controlling notochord development using high-throughput screening.
  • To explore the conservation of notochord enhancer logic and grammar across chordate species.

Main Methods:

  • High-throughput screening of genomic elements in developing Ciona (sea squirt) embryos.
  • Functional analysis of enhancer activity by manipulating transcription factor binding site orientation.
  • Comparative analysis of conserved binding site arrangements in vertebrate Lama1 and Brachyury enhancers.

Main Results:

  • Discovery of a novel enhancer near the Lama gene, critical for notochord development.
  • Demonstration that the orientation of ETS binding sites within enhancers is essential for notochord expression.
  • Identification of conserved clusters of Zic and ETS binding sites in Lama1 introns across species.
  • Characterization of a Brachyury (Bra) enhancer requiring FoxA, Bra, Zic, and ETS sites for notochord expression.
  • Evidence of conserved binding site logic within Brachyury enhancers in both Ciona and vertebrates.

Conclusions:

  • The study highlights the critical role of 'enhancer grammar'—the specific arrangement of transcription factor binding sites—in regulating notochord development.
  • Identified conserved signatures of enhancer logic and grammar across diverse chordate species, suggesting deep evolutionary conservation.
  • Provides fundamental insights into the regulatory mechanisms underlying notochord formation and its evolutionary persistence.