A modular cis-regulatory system controls isoform-specific pitx expression in ascidian stomodæum

Lionel Christiaen, Franck Bourrat, Jean Stéphane Joly

Research output: Contribution to journalArticle

Abstract

Pituitary homeobox (pitx) genes have been identified in vertebrates as critical molecular determinants of various craniofacial ontogenetic processes including pituitary organogenesis. Accordingly, a prominent conserved feature of pitx genes in chordates is their early expression in the anterior neural boundary (ANB) and oral ectoderm, also known as the stomodæum. Here we used the ascidian model species Ciona intestinalis to investigate pitx gene organization and cis-regulatory logic during early stages of oral development. Two distinct Ci-pitx mRNA variants were found to be expressed in mutually exclusive embryonic domains. Ci-pitx and vertebrate pitx2 genes display remarkably similar exon usage and organization, suggesting ancestry of the pitx transcriptional unit and regulation in chordates. We next combined phylogenetic footprinting, transient transgenesis, and confocal imaging methods to study the Ci-pitx cis-regulatory system, with special emphasis on the regulation of isoform-specific ANB/stomodæal expression. Among 10 conserved noncoding sequences (CNSs) interspersed in C. intestinalis and Ciona savignyi pitx loci, we identified two separate cis-regulatory modules (CRMs) that drive ANB/stomodæal expression in complementary spatiotemporal patterns. We discuss the developmental relevance of these data that provide an entry point to investigate the gene regulatory networks (GRNs) that position and shape oral structures in chordates.

Original languageEnglish (US)
Pages (from-to)557-566
Number of pages10
JournalDevelopmental Biology
Volume277
Issue number2
DOIs
StatePublished - Jan 15 2005

Fingerprint

Urochordata
Homeobox Genes
Protein Isoforms
Chordata
Ciona intestinalis
Vertebrates
Oral Stage
Gene Transfer Techniques
Ectoderm
Organogenesis
Conserved Sequence
Gene Regulatory Networks
Exons
Messenger RNA

Keywords

  • Ascidian
  • Differential isoform expression
  • Evolution
  • Gene regulation
  • Oral development
  • Pituitary homeobox

ASJC Scopus subject areas

  • Developmental Biology

Cite this

A modular cis-regulatory system controls isoform-specific pitx expression in ascidian stomodæum. / Christiaen, Lionel; Bourrat, Franck; Joly, Jean Stéphane.

In: Developmental Biology, Vol. 277, No. 2, 15.01.2005, p. 557-566.

Research output: Contribution to journalArticle

@article{184ab5592f464989823045ec59f2446b,
title = "A modular cis-regulatory system controls isoform-specific pitx expression in ascidian stomod{\ae}um",
abstract = "Pituitary homeobox (pitx) genes have been identified in vertebrates as critical molecular determinants of various craniofacial ontogenetic processes including pituitary organogenesis. Accordingly, a prominent conserved feature of pitx genes in chordates is their early expression in the anterior neural boundary (ANB) and oral ectoderm, also known as the stomod{\ae}um. Here we used the ascidian model species Ciona intestinalis to investigate pitx gene organization and cis-regulatory logic during early stages of oral development. Two distinct Ci-pitx mRNA variants were found to be expressed in mutually exclusive embryonic domains. Ci-pitx and vertebrate pitx2 genes display remarkably similar exon usage and organization, suggesting ancestry of the pitx transcriptional unit and regulation in chordates. We next combined phylogenetic footprinting, transient transgenesis, and confocal imaging methods to study the Ci-pitx cis-regulatory system, with special emphasis on the regulation of isoform-specific ANB/stomod{\ae}al expression. Among 10 conserved noncoding sequences (CNSs) interspersed in C. intestinalis and Ciona savignyi pitx loci, we identified two separate cis-regulatory modules (CRMs) that drive ANB/stomod{\ae}al expression in complementary spatiotemporal patterns. We discuss the developmental relevance of these data that provide an entry point to investigate the gene regulatory networks (GRNs) that position and shape oral structures in chordates.",
keywords = "Ascidian, Differential isoform expression, Evolution, Gene regulation, Oral development, Pituitary homeobox",
author = "Lionel Christiaen and Franck Bourrat and Joly, {Jean St{\'e}phane}",
year = "2005",
month = "1",
day = "15",
doi = "10.1016/j.ydbio.2004.10.008",
language = "English (US)",
volume = "277",
pages = "557--566",
journal = "Developmental Biology",
issn = "0012-1606",
publisher = "Academic Press Inc.",
number = "2",

}

TY - JOUR

T1 - A modular cis-regulatory system controls isoform-specific pitx expression in ascidian stomodæum

AU - Christiaen, Lionel

AU - Bourrat, Franck

AU - Joly, Jean Stéphane

PY - 2005/1/15

Y1 - 2005/1/15

N2 - Pituitary homeobox (pitx) genes have been identified in vertebrates as critical molecular determinants of various craniofacial ontogenetic processes including pituitary organogenesis. Accordingly, a prominent conserved feature of pitx genes in chordates is their early expression in the anterior neural boundary (ANB) and oral ectoderm, also known as the stomodæum. Here we used the ascidian model species Ciona intestinalis to investigate pitx gene organization and cis-regulatory logic during early stages of oral development. Two distinct Ci-pitx mRNA variants were found to be expressed in mutually exclusive embryonic domains. Ci-pitx and vertebrate pitx2 genes display remarkably similar exon usage and organization, suggesting ancestry of the pitx transcriptional unit and regulation in chordates. We next combined phylogenetic footprinting, transient transgenesis, and confocal imaging methods to study the Ci-pitx cis-regulatory system, with special emphasis on the regulation of isoform-specific ANB/stomodæal expression. Among 10 conserved noncoding sequences (CNSs) interspersed in C. intestinalis and Ciona savignyi pitx loci, we identified two separate cis-regulatory modules (CRMs) that drive ANB/stomodæal expression in complementary spatiotemporal patterns. We discuss the developmental relevance of these data that provide an entry point to investigate the gene regulatory networks (GRNs) that position and shape oral structures in chordates.

AB - Pituitary homeobox (pitx) genes have been identified in vertebrates as critical molecular determinants of various craniofacial ontogenetic processes including pituitary organogenesis. Accordingly, a prominent conserved feature of pitx genes in chordates is their early expression in the anterior neural boundary (ANB) and oral ectoderm, also known as the stomodæum. Here we used the ascidian model species Ciona intestinalis to investigate pitx gene organization and cis-regulatory logic during early stages of oral development. Two distinct Ci-pitx mRNA variants were found to be expressed in mutually exclusive embryonic domains. Ci-pitx and vertebrate pitx2 genes display remarkably similar exon usage and organization, suggesting ancestry of the pitx transcriptional unit and regulation in chordates. We next combined phylogenetic footprinting, transient transgenesis, and confocal imaging methods to study the Ci-pitx cis-regulatory system, with special emphasis on the regulation of isoform-specific ANB/stomodæal expression. Among 10 conserved noncoding sequences (CNSs) interspersed in C. intestinalis and Ciona savignyi pitx loci, we identified two separate cis-regulatory modules (CRMs) that drive ANB/stomodæal expression in complementary spatiotemporal patterns. We discuss the developmental relevance of these data that provide an entry point to investigate the gene regulatory networks (GRNs) that position and shape oral structures in chordates.

KW - Ascidian

KW - Differential isoform expression

KW - Evolution

KW - Gene regulation

KW - Oral development

KW - Pituitary homeobox

UR - http://www.scopus.com/inward/record.url?scp=11144335316&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=11144335316&partnerID=8YFLogxK

U2 - 10.1016/j.ydbio.2004.10.008

DO - 10.1016/j.ydbio.2004.10.008

M3 - Article

C2 - 15617693

AN - SCOPUS:11144335316

VL - 277

SP - 557

EP - 566

JO - Developmental Biology

JF - Developmental Biology

SN - 0012-1606

IS - 2

ER -