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Syntax compensates for poor binding sites to encode tissue specificity of developmental enhancers

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What this work says

Outgoing claims: the papers this work cites, builds on, or argues with.

inferredcites →https://doi.org/10.1016/0092-8674(93)90402-copenalex-snapshot

Binding affinities and cooperative interactions with bHLH activators delimit threshold responses to the dorsal gradient morphogen

inferredcites →https://doi.org/10.1016/j.cell.2014.11.041openalex-snapshot

Low Affinity Binding Site Clusters Confer Hox Specificity and Regulatory Robustness

inferredcites →https://doi.org/10.1016/j.cub.2010.03.063openalex-snapshot

A cis-Regulatory Signature in Ascidians and Flies, Independent of Transcription Factor Binding Sites

inferredcites →https://doi.org/10.1016/j.cub.2010.07.043openalex-snapshot

Shadow Enhancers Foster Robustness of Drosophila Gastrulation

inferredcites →https://doi.org/10.1016/j.cub.2011.05.056openalex-snapshot

Rapid Evolutionary Rewiring of a Structurally Constrained Eye Enhancer

inferredcites →https://doi.org/10.1016/j.ydbio.2006.08.075openalex-snapshot

FGF8/17/18 functions together with FGF9/16/20 during formation of the notochord in Ciona embryos

inferredcites →https://doi.org/10.1016/j.ydbio.2007.03.034openalex-snapshot

Direct activation by Ets and Zic is required for initial expression of the Brachyury gene in the ascidian notochord

inferredcites →https://doi.org/10.1016/j.ydbio.2013.09.016openalex-snapshot

Shadow enhancers flanking the HoxB cluster direct dynamic Hox expression in early heart and endoderm development

inferredcites →https://doi.org/10.1016/s0092-8674(03)00928-0openalex-snapshot

Neural Tissue in Ascidian Embryos Is Induced by FGF9/16/20, Acting via a Combination of Maternal GATA and Ets Transcription Factors

inferredcites →https://doi.org/10.1016/s0925-4773(00)00528-1openalex-snapshot

Induction of anterior neural fates in the ascidian Ciona intestinalis

inferredcites →https://doi.org/10.1038/emboj.2010.106openalex-snapshot

Genome‐wide analysis of ETS‐family DNA‐binding in vitro and in vivo

inferredcites →https://doi.org/10.1073/pnas.1220010110openalex-snapshot

SoxB1-driven transcriptional network underlies neural-specific interpretation of morphogen signals

inferredcites →https://doi.org/10.1093/nar/gku1045openalex-snapshot

UniPROBE, update 2015: new tools and content for the online database of protein-binding microarray data on protein–DNA interactions

inferredcites →https://doi.org/10.1098/rstb.2013.0018openalex-snapshot

Low-affinity transcription factor binding sites shape morphogen responses and enhancer evolution

inferredcites →https://doi.org/10.1101/gad.5.5.827openalex-snapshot

Transcriptional regulation of a pair-rule stripe in Drosophila.

inferredcites →https://doi.org/10.1101/gad.861201openalex-snapshot

Brinker is a sequence-specific transcriptional repressor in theDrosophilaembryo

inferredcites →https://doi.org/10.1101/gad.976502openalex-snapshot

Three habits of highly effective signaling pathways: principles of transcriptional control by developmental cell signaling

inferredcites →https://doi.org/10.1101/pdb.prot5345openalex-snapshot

Electroporation of Transgenic DNAs in the Sea Squirt Ciona

inferredcites →https://doi.org/10.1126/science.1123404openalex-snapshot

Regulatory Blueprint for a Chordate Embryo

inferredcites →https://doi.org/10.1126/science.1160631openalex-snapshot

Shadow Enhancers as a Source of Evolutionary Novelty

inferredcites →https://doi.org/10.1126/science.aac6948openalex-snapshot

Suboptimization of developmental enhancers

inferredcites →https://doi.org/10.1128/mcb.19.8.5732openalex-snapshot

Dual Requirement for the EcR/USP Nuclear Receptor and the dGATAb Factor in an Ecdysone Response in Drosophila melanogaster

inferredcites →https://doi.org/10.1242/dev.01011openalex-snapshot

A zinc finger transcription factor, ZicL, is a direct activator ofBrachyuryin the notochord specification ofCiona intestinalis

inferredcites →https://doi.org/10.1242/dev.010850openalex-snapshot

A combinatorial code of maternal GATA, Ets and β-catenin-TCF transcription factors specifies and patterns the early ascidian ectoderm

inferredcites →https://doi.org/10.1242/dev.011940openalex-snapshot

Ephrin signaling establishes asymmetric cell fates in an endomesoderm lineage of theCionaembryo

inferredcites →https://doi.org/10.1242/dev.072108openalex-snapshot

Neural tube patterning by Ephrin, FGF and Notch signaling relays

inferredcites →https://doi.org/10.1242/dev.078485openalex-snapshot

FGF signaling establishes the anterior border of the Ciona neural tube

inferredcites →https://doi.org/10.1242/dev.129.11.2723openalex-snapshot

Multiple functions of a Zic-like gene in the differentiation of notochord, central nervous system and muscle inCiona savignyiembryos

inferredcites →https://doi.org/10.7554/elife.04837openalex-snapshot

Conservation of transcription factor binding specificities across 600 million years of bilateria evolution

inferredcites →https://doi.org/10.7554/elife.04837.037openalex-snapshot

Author response: Conservation of transcription factor binding specificities across 600 million years of bilateria evolution

What points at this work

Incoming claims: where this work appears in other papers’ reference lists and arguments.

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Gene regulation in regeneration after acute kidney injury

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PAX8 controls proximal tubule epithelial identity and stress response through epigenetic modification of distal regulatory elements

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Multi-layered transcriptional control of cranial neural crest development

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Homeodomain complex formation and biomolecular condensates in Hox gene regulation

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Motif orientation matters: Structural characterization of TEAD1 recognition of genomic DNA

inferred← citeshttps://doi.org/10.1016/j.tcb.2018.04.003openalex-snapshot

Enhancer Logic and Mechanics in Development and Disease

inferred← citeshttps://doi.org/10.1016/j.xgen.2022.100191openalex-snapshot

A cis-regulatory lexicon of DNA motif combinations mediating cell-type-specific gene regulation

inferred← citeshttps://doi.org/10.1016/j.xgen.2025.100821openalex-snapshot

Interpreting regulatory mechanisms of Hippo signaling through a deep learning sequence model

inferred← citeshttps://doi.org/10.1016/j.xpro.2024.103107openalex-snapshot

Protocol to electroporate DNA plasmids into Ciona robusta embryos at the 1-cell stage

inferred← citeshttps://doi.org/10.1016/j.ydbio.2018.09.021openalex-snapshot

Multiple inputs into a posterior-specific regulatory network in the Ciona notochord

inferred← citeshttps://doi.org/10.1016/j.ydbio.2019.01.003openalex-snapshot

Evolution of embryonic cis-regulatory landscapes between divergent Phallusia and Ciona ascidians

inferred← citeshttps://doi.org/10.1016/j.ydbio.2025.03.007openalex-snapshot

A gene regulatory network for specification and morphogenesis of a Mauthner Cell homolog in non-vertebrate chordates

inferred← citeshttps://doi.org/10.1021/acssynbio.8b00236openalex-snapshot

Design of Large-Scale Reporter Construct Arrays for Dynamic, Live Cell Systems Biology

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Putting enhancers into context

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Conserved regulatory logic at accessible and inaccessible chromatin during the acute inflammatory response in mammals

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Specificity of the Hox member Deformed is determined by transcription factor levels and binding site affinities

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Conserved enhancers control notochord expression of vertebrate Brachyury

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Cis-regulatory interfaces reveal the molecular mechanisms underlying the notochord gene regulatory network of Ciona

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Synergistic activation by Glass and Pointed promotes neuronal identity in the Drosophila eye disc

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Multimeric transcription factor BCL11A utilizes two zinc-finger tandem arrays to bind clustered short sequence motifs

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Optimization of the Irf8 +32-kb enhancer disrupts dendritic cell lineage segregation

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How to tune an enhancer

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Two distinct evolutionary conserved neural degeneration pathways characterized in a colonial chordate

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A statistical framework for predicting critical regions of p53-dependent enhancers

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Crosstalk between paralogs and isoforms influences p63-dependent regulatory element activity

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MEPP: more transparent motif enrichment by profiling positional correlations

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Sequence-based modeling of low-affinity transcription factor–DNA binding through deep learning

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Plant enhancers exhibit both cooperative and additive interactions among their functional elements

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The Nucleosome Remodelling and Deacetylation complex restricts Mediator access to enhancers to control transcription

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A flexible repertoire of transcription factor binding sites and diversity threshold determines enhancer activity in embryonic stem cells

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Brachyury controls Ciona notochord fate as part of a feedforward network and not as a unitary master regulator

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Wnt target enhancer regulation by a CDX/TCF transcription factor collective and a novel DNA motif

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Affinity-optimizing variants within cardiac enhancers disrupt heart development and contribute to cardiac traits

inferred← citeshttps://doi.org/10.1101/2022.05.27.493789openalex-snapshot

Affinity-optimizing variants within the ZRS enhancer disrupt limb development

inferred← citeshttps://doi.org/10.1101/2022.11.25.517987openalex-snapshot

Unique functions of two overlapping PAX6 retinal enhancers

inferred← citeshttps://doi.org/10.1101/2023.04.20.536761openalex-snapshot

Conserved enhancer logic controls the notochord expression of vertebrate Brachyury

inferred← citeshttps://doi.org/10.1101/2023.05.11.540401openalex-snapshot

De novo distillation of thermodynamic affinity from deep learning regulatory sequence models of in vivo protein-DNA binding

inferred← citeshttps://doi.org/10.1101/2023.08.08.552077openalex-snapshot

Machine-guided design of synthetic cell type-specific cis -regulatory elements

inferred← citeshttps://doi.org/10.1101/2024.05.09.593326openalex-snapshot

Context dependent activity of p63-bound gene regulatory elements

inferred← citeshttps://doi.org/10.1101/2024.12.12.628285openalex-snapshot

Deep homology of a brachyury regulatory syntax and origin of the notochord

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Quantifying the impact of genetic mutations on enhancer dynamics

inferred← citeshttps://doi.org/10.1101/205724openalex-snapshot

Cooperative recruitment of Yan to paired high affinity ETS sites organizes repression to confer specificity and robustness to cardiac cell fate specification

inferred← citeshttps://doi.org/10.1101/gad.310367.117openalex-snapshot

Assessing sufficiency and necessity of enhancer activities for gene expression and the mechanisms of transcription activation

inferred← citeshttps://doi.org/10.1101/gad.311985.118openalex-snapshot

A feed-forward relay integrates the regulatory activities of Bicoid and Orthodenticle via sequential binding to suboptimal sites

inferred← citeshttps://doi.org/10.1101/gr.272468.120openalex-snapshot

A flexible repertoire of transcription factor binding sites and a diversity threshold determines enhancer activity in embryonic stem cells

inferred← citeshttps://doi.org/10.1101/gr.277246.122openalex-snapshot

Enhancers display constrained sequence flexibility and context-specific modulation of motif function

inferred← citeshttps://doi.org/10.1101/gr.279652.124openalex-snapshot

Integrating genetic variation with deep learning provides context for variants impacting transcription factor binding during embryogenesis

inferred← citeshttps://doi.org/10.1101/sqb.2015.80.027227openalex-snapshot

Regulatory Principles Governing Tissue Specificity of Developmental Enhancers

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Exploring the roles of conserved context‐dependent cis‐regulatory elements ( cdCREs ) in multicellularity, human health and disease

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The Making of a cDC1 : Precision Programming of Progenitor Potential

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Regulatory encoding of quantitative variation in spatial activity of a Drosophila enhancer

inferred← citeshttps://doi.org/10.1126/sciadv.adw3307openalex-snapshot

Deep homology of a brachyury cis-regulatory syntax and the evolutionary origin of the notochord

inferred← citeshttps://doi.org/10.1146/annurev-cellbio-100617-062719openalex-snapshot

Low-Affinity Binding Sites and the Transcription Factor Specificity Paradox in Eukaryotes

inferred← citeshttps://doi.org/10.1152/ajprenal.00289.2024openalex-snapshot

Pax proteins mediate segment-specific functions in proximal tubule survival and response to ischemic injury

inferred← citeshttps://doi.org/10.1161/circgen.126.005721openalex-snapshot

Unlocking the Regulatory Genome: Interpreting the Clinical Impact of Noncoding Variants in Genetic Cardiomyopathies

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Activation of the LMO2 oncogene through a somatically acquired neomorphic promoter in T-cell acute lymphoblastic leukemia

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A k-mer grammar analysis to uncover maize regulatory architecture

inferred← citeshttps://doi.org/10.1186/s13059-023-02955-4openalex-snapshot

Decoding enhancer complexity with machine learning and high-throughput discovery

inferred← citeshttps://doi.org/10.1186/s13059-026-04186-9openalex-snapshot

Lentiviral single-cell MPRA of synthetic enhancers reveals motif affinity-based encoding of cell state specificity

inferred← citeshttps://doi.org/10.1242/bio.036897openalex-snapshot

Promoter-enhancer looping and shadow enhancers of the mouse αA-crystallin locus

inferred← citeshttps://doi.org/10.1242/dev.156174openalex-snapshot

Functional and evolutionary insights from the Ciona notochord transcriptome

inferred← citeshttps://doi.org/10.1242/dev.161430openalex-snapshot

Robust and efficient gene regulation through localized nuclear microenvironments

inferred← citeshttps://doi.org/10.1242/dev.182899openalex-snapshot

The origin of animal body plans: a view from fossil evidence and the regulatory genome

inferred← citeshttps://doi.org/10.1242/dev.195230openalex-snapshot

Brachyury controls Ciona notochord fate as part of a feed-forward network

inferred← citeshttps://doi.org/10.1242/dev.202968openalex-snapshot

A change in cis-regulatory logic underlying obligate versus facultative muscle multinucleation in chordates

inferred← citeshttps://doi.org/10.1371/journal.pcbi.1010524openalex-snapshot

On the incongruence of genotype-phenotype and fitness landscapes

inferred← citeshttps://doi.org/10.1371/journal.pgen.1007289openalex-snapshot

Degenerate Pax2 and Senseless binding motifs improve detection of low-affinity sites required for enhancer specificity

inferred← citeshttps://doi.org/10.1371/journal.pgen.1009305openalex-snapshot

Ciona Brachyury proximal and distal enhancers have different FGF dose-response relationships

inferred← citeshttps://doi.org/10.1387/ijdb.180294ilopenalex-snapshot

Hox transcription factors: an overview of multi-step regulators of gene expression

inferred← citeshttps://doi.org/10.26508/lsa.202302126openalex-snapshot

Unique activities of two overlapping PAX6 retinal enhancers

inferred← citeshttps://doi.org/10.3389/fcell.2021.804032openalex-snapshot

Quantitative Dissection of the Proximal Ciona brachyury Enhancer

inferred← citeshttps://doi.org/10.3389/fgene.2021.642975openalex-snapshot

Heart Enhancers: Development and Disease Control at a Distance

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The Causes and Consequences of Spatial Organization of the Genome in Regulation of Gene Expression

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Association of Two Polymorphisms in CCL2 With Parkinson's Disease: A Case-Control Study

inferred← citeshttps://doi.org/10.3390/ani13182935openalex-snapshot

PorcineAI-Enhancer: Prediction of Pig Enhancer Sequences Using Convolutional Neural Networks

inferred← citeshttps://doi.org/10.3390/cancers14184375openalex-snapshot

Typical Enhancers, Super-Enhancers, and Cancers

inferred← citeshttps://doi.org/10.3390/ijms21217856openalex-snapshot

Perspective: Quality Versus Quantity; Is It Important to Assess the Role of Enhancers in Complex Disease from an In Vivo Perspective?

inferred← citeshttps://doi.org/10.3390/ijms21228556openalex-snapshot

Role of Non-Coding Variants in Brugada Syndrome

inferred← citeshttps://doi.org/10.3390/ijms252413631openalex-snapshot

Fine-Tuned Expression of Evolutionarily Conserved Signaling Molecules in the Ciona Notochord

inferred← citeshttps://doi.org/10.4049/jimmunol.2100777openalex-snapshot

A Bcl6 Intronic Element Regulates T Follicular Helper Cell Differentiation

inferred← citeshttps://doi.org/10.53846/goediss-8835openalex-snapshot

Statistical methods for biological sequence analysis for DNA binding motifs and protein contacts

inferred← citeshttps://doi.org/10.64898/2026.02.27.708495openalex-snapshot

Lentiviral single-cell MPRA of synthetic enhancers reveals motif affinity-based encoding of cell type specificity

inferred← citeshttps://doi.org/10.64898/2026.05.01.721897openalex-snapshot

Bipartite DNA binding domain of transcription factor BCL11B binds clustered short DNA sequence motifs

inferred← citeshttps://doi.org/10.64898/2026.09.20.752987openalex-snapshot

Mapping and rewiring the MYBPC3 promoter for rescue of haploinsufficiency driven hypertrophic cardiomyopathy

inferred← citeshttps://doi.org/10.70675/50757190zb2d8z4fc2zbc96zfea34ff0071copenalex-snapshot

Dose et cofacteurs des protéines Hox lors du développement des organes de vol chez les insectes

inferred← citeshttps://doi.org/10.70675/6da04ca8z76d8z4fd4z9f55zde97179c8e99openalex-snapshot

Evolution of regulation of ascidian species

inferred← citeshttps://doi.org/10.70675/b29d142fzed1az4785zbb11z225e807d15e5openalex-snapshot

Analyse d'interactions Hox/Cofacteur à l'échelle super-résolutive et contrôle transcriptionnel de l'autophagie chez la drosophile

inferred← citeshttps://doi.org/10.7554/elife.28620openalex-snapshot

Cooperative interactions enable singular olfactory receptor expression in mouse olfactory neurons

inferred← citeshttps://doi.org/10.7554/elife.28975openalex-snapshot

Nuclear microenvironments modulate transcription from low-affinity enhancers

inferred← citeshttps://doi.org/10.7554/elife.29656openalex-snapshot

An FGF-driven feed-forward circuit patterns the cardiopharyngeal mesoderm in space and time

inferred← citeshttps://doi.org/10.7554/elife.36187openalex-snapshot

Transcriptional and epigenomic landscapes of CNS and non-CNS vascular endothelial cells

inferred← citeshttps://doi.org/10.7554/elife.45325openalex-snapshot

Multi-enhancer transcriptional hubs confer phenotypic robustness

inferred← citeshttps://doi.org/10.7554/elife.59650openalex-snapshot

A low affinity cis-regulatory BMP response element restricts target gene activation to subsets of Drosophila neurons

inferred← citeshttps://doi.org/10.7554/elife.67403openalex-snapshot

Information content differentiates enhancers from silencers in mouse photoreceptors

inferred← citeshttps://doi.org/10.7554/elife.74509openalex-snapshot

Synthetic reconstruction of the hunchback promoter specifies the role of Bicoid, Zelda and Hunchback in the dynamics of its transcription

inferred← citeshttps://doi.org/10.7554/elife.76500openalex-snapshot

Characterization of sequence determinants of enhancer function using natural genetic variation

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