Dataset Information

Intragenomic evolution of a transcriptional enhancer in the genome of Strongylocentrotus purpuratus.

ABSTRACT: General principles for how genomic regulatory elements evolve to alter patterns of gene expression remain vague. The purpose of this study was to gain insights into the evolution of genomic regulatory elements by investigating the unique features of a transcriptional enhancer that directs Spec2a gene expression in Strongylocentrotus purpuratus. The Spec2a enhancer is embedded in a repetitive sequence family interspersed throughout the genome. We surveyed the genome and identified 274 of these sequences. They displayed a continuum of sequence divergence defining high and low divergence classes. Alignment of 52 most related to the Spec2a sequence revealed a complex pattern of rearrangements, insertions and deletions, and base-pair changes. A distance tree for the 52 sequences was constructed and correlated with enhancer activity. Unexpectedly, we found a wide range of activities. Notably, repetitive sequences lacking essential cis-elements found in the Spec2a enhancer still had strong activity. We identified short, conserved motifs within the repetitive sequences that may represent novel cis-regulatory elements. Many repetitive sequences with enhancer activity were found nearby genes, suggesting that they regulate gene expression. The results show that the repetitive sequences are rapidly evolving in the S. purpuratus genome and may serve as a renewable pool of transcriptional enhancers.

SUBMITTER: Kiyama T

PROVIDER: S-EPMC3390921 | biostudies-literature | 2009 Jun

REPOSITORIES: biostudies-literature

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Intragenomic evolution of a transcriptional enhancer in the genome of Strongylocentrotus purpuratus.

Kiyama Takae T Zhang Jiexin J Liang Shoudan S Liang Shuguang S Klein William H WH

Marine genomics 20090601 2

General principles for how genomic regulatory elements evolve to alter patterns of gene expression remain vague. The purpose of this study was to gain insights into the evolution of genomic regulatory elements by investigating the unique features of a transcriptional enhancer that directs Spec2a gene expression in Strongylocentrotus purpuratus. The Spec2a enhancer is embedded in a repetitive sequence family interspersed throughout the genome. We surveyed the genome and identified 274 of these se ...[more]

PMID: 21798176

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Project description:BackgroundThe sea urchin embryo has been an important model organism in developmental biology for more than a century. This is due to its relatively simple construction, translucent appearance, and the possibility to follow the fate of individual cells as development to the pluteus larva proceeds. Because the larvae contain tiny calcitic skeletal elements, the spicules, they are also important model organisms for biomineralization research. Similar to other biominerals the spicule contains an organic matrix, which is thought to play an important role in its formation. However, only few spicule matrix proteins were identified previously.ResultsUsing mass spectrometry-based methods we have identified 231 proteins in the matrix of the S. purpuratus spicule matrix. Approximately two thirds of the identified proteins are either known or predicted to be extracellular proteins or transmembrane proteins with large ectodomains. The ectodomains may have been solubilized by partial proteolysis and subsequently integrated into the growing spicule. The most abundant protein of the spicule matrix is SM50. SM50-related proteins, SM30-related proteins, MSP130 and related proteins, matrix metalloproteases and carbonic anhydrase are among the most abundant components.ConclusionsThe spicule matrix is a relatively complex mixture of proteins not only containing matrix-specific proteins with a function in matrix assembly or mineralization, but also: 1) proteins possibly important for the formation of the continuous membrane delineating the mineralization space; 2) proteins for secretory processes delivering proteinaceous or non-proteinaceous precursors; 3) or proteins reflecting signaling events at the cell/matrix interface. Comparison of the proteomes of different skeletal matrices allows prediction of proteins of general importance for mineralization in sea urchins, such as SM50, SM30-E, SM29 or MSP130. The comparisons also help point out putative tissue-specific proteins, such as tooth phosphodontin or specific spicule matrix metalloproteases of the MMP18/19 group. Furthermore, the direct sequence analysis of peptides by MS/MS validates many predicted genes and confirms the existence of the corresponding proteins.

Project description:BackgroundThe organic matrix of biominerals plays an important role in biomineral formation and in determining biomineral properties. However, most components of biomineral matrices remain unknown at present. In sea urchin, which is an important model organism for developmental biology and biomineralization, only few matrix components have been identified and characterized at the protein level. The recent publication of the Strongylocentrotus purpuratus genome sequence rendered possible not only the identification of possible matrix proteins at the gene level, but also the direct identification of proteins contained in matrices of skeletal elements by in-depth, high-accuracy, proteomic analysis.ResultsWe identified 110 proteins as components of sea urchin test and spine organic matrix. Fourty of these proteins occurred in both compartments while others were unique to their respective compartment. More than 95% of the proteins were detected in sea urchin skeletal matrices for the first time. The most abundant protein in both matrices was the previously characterized spicule matrix protein SM50, but at least eight other members of this group, many of them only known as conceptual translation products previously, were identified by mass spectrometric sequence analysis of peptides derived from in vitro matrix degradation. The matrices also contained proteins implicated in biomineralization processes previously by inhibition studies using antibodies or specific enzyme inhibitors, such as matrix metalloproteases and members of the mesenchyme-specific MSP130 family. Other components were carbonic anhydrase, collagens, echinonectin, a alpha2-macroglobulin-like protein and several proteins containing scavenger receptor cysteine-rich domains. A few possible signal transduction pathway components, such as GTP-binding proteins, a semaphorin and a possible tyrosine kinase were also identified.ConclusionThis report presents the most comprehensive list of sea urchin skeletal matrix proteins available at present. The complex mixture of proteins identified in matrices of the sea urchin skeleton may reflect many different aspects of the mineralization process. Because LC-MS/MS-based methods directly measures peptides our results validate many predicted genes and confirm the existence of the corresponding proteins. Considering the many newly identified matrix proteins, this proteomic study may serve as a road map for the further exploration of biomineralization processes in an important model organism.

Dataset Information

Intragenomic evolution of a transcriptional enhancer in the genome of Strongylocentrotus purpuratus.

Publications

Intragenomic evolution of a transcriptional enhancer in the genome of Strongylocentrotus purpuratus.

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