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Landscape of histone modifications in a sponge reveals the origin of animal cis-regulatory complexity.

eLife | 2017

Combinatorial patterns of histone modifications regulate developmental and cell type-specific gene expression and underpin animal complexity, but it is unclear when this regulatory system evolved. By analysing histone modifications in a morphologically-simple, early branching animal, the sponge Amphimedonqueenslandica, we show that the regulatory landscape used by complex bilaterians was already in place at the dawn of animal multicellularity. This includes distal enhancers, repressive chromatin and transcriptional units marked by H3K4me3 that vary with levels of developmental regulation. Strikingly, Amphimedon enhancers are enriched in metazoan-specific microsyntenic units, suggesting that their genomic location is extremely ancient and likely to place constraints on the evolution of surrounding genes. These results suggest that the regulatory foundation for spatiotemporal gene expression evolved prior to the divergence of sponges and eumetazoans, and was necessary for the evolution of animal multicellularity.

Pubmed ID: 28395144 RIS Download

Associated grants

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This is a list of tools and resources that we have found mentioned in this publication.


Bioconductor (tool)

RRID:SCR_006442

Software repository for R packages related to analysis and comprehension of high throughput genomic data. Uses separate set of commands for installation of packages. Software project based on R programming language that provides tools for analysis and comprehension of high throughput genomic data.

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KEGG (tool)

RRID:SCR_012773

Integrated database resource consisting of 16 main databases, broadly categorized into systems information, genomic information, and chemical information. In particular, gene catalogs in completely sequenced genomes are linked to higher-level systemic functions of cell, organism, and ecosystem. Analysis tools are also available. KEGG may be used as reference knowledge base for biological interpretation of large-scale datasets generated by sequencing and other high-throughput experimental technologies.

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FastQC (tool)

RRID:SCR_014583

Quality control software that perform checks on raw sequence data coming from high throughput sequencing pipelines. This software also provides a modular set of analyses which can give a quick impression of the quality of the data prior to further analysis.

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ChIP-seq (tool)

RRID:SCR_001237

Set of software modules for performing common ChIP-seq data analysis tasks across the whole genome, including positional correlation analysis, peak detection, and genome partitioning into signal-rich and signal-poor regions. The tools are designed to be simple, fast and highly modular. Each program carries out a well defined data processing procedure that can potentially fit into a pipeline framework. ChIP-Seq is also freely available on a Web interface.

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Cytoscape (tool)

RRID:SCR_003032

Software platform for complex network analysis and visualization. Used for visualization of molecular interaction networks and biological pathways and integrating these networks with annotations, gene expression profiles and other state data.

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UniPROBE (tool)

RRID:SCR_005803

Database that hosts experimental data from universal protein binding microarray (PBM) experiments (Berger et al., 2006) and their accompanying statistical analyses from prokaryotic and eukaryotic organisms, malarial parasites, yeast, worms, mouse, and human. It provides a centralized resource for accessing comprehensive data on the preferences of proteins for all possible sequence variants ("words") of length k ("k-mers"), as well as position weight matrix (PWM) and graphical sequence logo representations of the k-mer data. The database's web tools include a text-based search, a function for assessing motif similarity between user-entered data and database PWMs, and a function for locating putative binding sites along user-entered nucleotide sequences.

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InterProScan (tool)

RRID:SCR_005829

Software package for functional analysis of sequences by classifying them into families and predicting presence of domains and sites. Scans sequences against InterPro's signatures. Characterizes nucleotide or protein function by matching it with models from several different databases. Used in large scale analysis of whole proteomes, genomes and metagenomes. Available as Web based version and standalone Perl version and SOAP Web Service.

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DESeq2 (tool)

RRID:SCR_015687

Software package for differential gene expression analysis based on the negative binomial distribution. Used for analyzing RNA-seq data for differential analysis of count data, using shrinkage estimation for dispersions and fold changes to improve stability and interpretability of estimates.

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Deeptools (tool)

RRID:SCR_016366

Python based tools to process, visualize and analyse high-throughput sequencing data, such as ChIP-seq, RNA-seq or MNase-seq. Implemented within Galaxy framework. Used to perform complete bioinformatic workflows ranging from quality controls and normalizations of aligned reads to integrative analyses, including clustering and visualization approaches.

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GeneOverlap (tool)

RRID:SCR_018419

Software package to test and visualize gene overlaps. Given two gene lists, tests significance of their overlap in comparison with genomic background.

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ChIPAb+ Trimethyl-Histone H3 (Lys36) (antibody)

RRID:AB_10615601

This monoclonal targets ChIPAb+ Trimethyl-Histone H3 (Lys36)

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Mouse Anti-ChIPAb+ Monomethyl-Histone H3 (Lys4) ChIPAb+? Monoclonal Antibody, Unconjugated (antibody)

RRID:AB_10806625

This monoclonal targets Mouse ChIPAb+ Monomethyl-Histone H3 (Lys4) ChIPAb+?

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Bowtie (software resource)

RRID:SCR_005476

Software ultrafast memory efficient tool for aligning sequencing reads. Bowtie is short read aligner.

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MACS (software resource)

RRID:SCR_013291

Software Python package for identifying transcript factor binding sites. Used to evaluate significance of enriched ChIP regions. Improves spatial resolution of binding sites through combining information of both sequencing tag position and orientation. Can be used for ChIP-Seq data alone, or with control sample with increase of specificity.

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Trimmomatic (data processing software)

RRID:SCR_011848

Software Java pipeline for trimming tasks for Illumina paired end and single ended data. Flexible Trimmer for Illumina Sequence Data. Pair aware preprocessing tool optimized for Illumina next generation sequencing data. Includes several processing steps for read trimming and filtering. Operating systems Unix/Linux, Mac OS, Windows.

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BLASTP (service resource)

RRID:SCR_001010

Data analysis service whose programs search protein databases using a protein query. The algorithms used include blastp, psi-blast, phi-blast, and delta-blast.

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NCBI Sequence Read Archive (SRA) (data repository)

RRID:SCR_004891

Repository of raw sequencing data from next generation of sequencing platforms including including Roche 454 GS System, Illumina Genome Analyzer, Applied Biosystems SOLiD System, Helicos Heliscope, Complete Genomics, and Pacific Biosciences SMRT. In addition to raw sequence data, SRA now stores alignment information in form of read placements on reference sequence. Data submissions are welcome. Archive of high throughput sequencing data,part of international partnership of archives (INSDC) at NCBI, European Bioinformatics Institute and DNA Database of Japan. Data submitted to any of this three organizations are shared among them.

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Gene Expression Omnibus (GEO) (data repository)

RRID:SCR_007303

Functional genomics data repository supporting MIAME-compliant data submissions. Includes microarray-based experiments measuring the abundance of mRNA, genomic DNA, and protein molecules, as well as non-array-based technologies such as serial analysis of gene expression (SAGE) and mass spectrometry proteomic technology. Array- and sequence-based data are accepted. Collection of curated gene expression DataSets, as well as original Series and Platform records. The database can be searched using keywords, organism, DataSet type and authors. DataSet records contain additional resources including cluster tools and differential expression queries.

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MAFFT (software resource)

RRID:SCR_011811

Software package as multiple alignment program for amino acid or nucleotide sequences. Can align up to 500 sequences or maximum file size of 1 MB. First version of MAFFT used algorithm based on progressive alignment, in which sequences were clustered with help of Fast Fourier Transform. Subsequent versions have added other algorithms and modes of operation, including options for faster alignment of large numbers of sequences, higher accuracy alignments, alignment of non-coding RNA sequences, and addition of new sequences to existing alignments.

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DESeq (software resource)

RRID:SCR_000154

THIS RESOURCE IS NO LONGER IN SERVICE. Documented on August 30,2023. Software for differential gene expression analysis based on the negative binomial distribution. It estimates variance-mean dependence in count data from high-throughput sequencing assays and tests for differential expression.

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UCSC Genome Browser (data or information resource)

RRID:SCR_005780

Portal to interactively visualize genomic data. Provides reference sequences and working draft assemblies for collection of genomes and access to ENCODE and Neanderthal projects. Includes collection of vertebrate and model organism assemblies and annotations, along with suite of tools for viewing, analyzing and downloading data.

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ngs.plot (software resource)

RRID:SCR_011795

A software program that allows you to easily visualize your next-generation sequencing (NGS) samples at functional genomic regions.

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BiNGO: A Biological Networks Gene Ontology tool (software resource)

RRID:SCR_005736

The Biological Networks Gene Ontology tool (BiNGO) is an open-source Java tool to determine which Gene Ontology (GO) terms are significantly overrepresented in a set of genes. BiNGO can be used either on a list of genes, pasted as text, or interactively on subgraphs of biological networks visualized in Cytoscape. BiNGO maps the predominant functional themes of the tested gene set on the GO hierarchy, and takes advantage of Cytoscape''''s versatile visualization environment to produce an intuitive and customizable visual representation of the results. Platform: Windows compatible, Mac OS X compatible, Linux compatible, Unix compatible

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MEME Suite - Motif-based sequence analysis tools (software resource)

RRID:SCR_001783

Suite of motif-based sequence analysis tools to discover motifs using MEME, DREME (DNA only) or GLAM2 on groups of related DNA or protein sequences; search sequence databases with motifs using MAST, FIMO, MCAST or GLAM2SCAN; compare a motif to all motifs in a database of motifs; associate motifs with Gene Ontology terms via their putative target genes, and analyze motif enrichment using SpaMo or CentriMo. Source code, binaries and a web server are freely available for noncommercial use.

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BEDTools (software resource)

RRID:SCR_006646

A powerful toolset for genome arithmetic allowing one to address common genomics tasks such as finding feature overlaps and computing coverage. Bedtools allows one to intersect, merge, count, complement, and shuffle genomic intervals from multiple files in widely-used genomic file formats such as BAM, BED, GFF/GTF, VCF. While each individual tool is designed to do a relatively simple task (e.g., intersect two interval files), quite sophisticated analyses can be conducted by combining multiple bedtools operations on the UNIX command line.

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cutadapt (software resource)

RRID:SCR_011841

Software tool that removes adapter sequences from DNA sequencing reads.

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Peakzilla (software resource)

RRID:SCR_007471

An algorithm to identify transcription factor binding sites from ChIP-seq data.

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SPP (software resource)

RRID:SCR_001790

R analysis and processing package for Illumina platform Chip-Seq data.

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SAMTOOLS (software resource)

RRID:SCR_002105

Original SAMTOOLS package has been split into three separate repositories including Samtools, BCFtools and HTSlib. Samtools for manipulating next generation sequencing data used for reading, writing, editing, indexing,viewing nucleotide alignments in SAM,BAM,CRAM format. BCFtools used for reading, writing BCF2,VCF, gVCF files and calling, filtering, summarising SNP and short indel sequence variants. HTSlib used for reading, writing high throughput sequencing data.

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Clustal Omega (software resource)

RRID:SCR_001591

Software package as multiple sequence alignment tool that uses seeded guide trees and HMM profile-profile techniques to generate alignments between three or more sequences. Accepts nucleic acid or protein sequences in multiple sequence formats NBRF/PIR, EMBL/UniProt, Pearson (FASTA), GDE, ALN/Clustal, GCG/MSF, RSF.

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Bowtie (software resource)

RRID:SCR_005476

Software ultrafast memory efficient tool for aligning sequencing reads. Bowtie is short read aligner.

View all literature mentions

Trimmomatic (data processing software)

RRID:SCR_011848

Software Java pipeline for trimming tasks for Illumina paired end and single ended data. Flexible Trimmer for Illumina Sequence Data. Pair aware preprocessing tool optimized for Illumina next generation sequencing data. Includes several processing steps for read trimming and filtering. Operating systems Unix/Linux, Mac OS, Windows.

View all literature mentions

MACS (software resource)

RRID:SCR_013291

Software Python package for identifying transcript factor binding sites. Used to evaluate significance of enriched ChIP regions. Improves spatial resolution of binding sites through combining information of both sequencing tag position and orientation. Can be used for ChIP-Seq data alone, or with control sample with increase of specificity.

View all literature mentions

BLASTP (service resource)

RRID:SCR_001010

Data analysis service whose programs search protein databases using a protein query. The algorithms used include blastp, psi-blast, phi-blast, and delta-blast.

View all literature mentions