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Divergent mechanisms regulate conserved cardiopharyngeal development and gene expression in distantly related ascidians.

Stolfi A, Lowe EK, Racioppi C, Ristoratore F, Brown CT, Swalla BJ, Christiaen L - Elife (2014)

Bottom Line: Ascidians present a striking dichotomy between conserved phenotypes and divergent genomes: embryonic cell lineages and gene expression patterns are conserved between distantly related species.Much research has focused on Ciona or Halocynthia spp. but development in other ascidians remains poorly characterized.In this study, we surveyed the multipotent myogenic B7.5 lineage in Molgula spp.

View Article: PubMed Central - PubMed

Affiliation: Center for Developmental Genetics, Department of Biology, New York University, New York, United States.

ABSTRACT
Ascidians present a striking dichotomy between conserved phenotypes and divergent genomes: embryonic cell lineages and gene expression patterns are conserved between distantly related species. Much research has focused on Ciona or Halocynthia spp. but development in other ascidians remains poorly characterized. In this study, we surveyed the multipotent myogenic B7.5 lineage in Molgula spp. Comparisons to the homologous lineage in Ciona revealed identical cell division and fate specification events that result in segregation of larval, cardiac, and pharyngeal muscle progenitors. Moreover, the expression patterns of key regulators are conserved, but cross-species transgenic assays uncovered incompatibility, or 'unintelligibility', of orthologous cis-regulatory sequences between Molgula and Ciona. These sequences drive identical expression patterns that are not recapitulated in cross-species assays. We show that this unintelligibility is likely due to changes in both cis- and trans-acting elements, hinting at widespread and frequent turnover of regulatory mechanisms underlying otherwise conserved aspects of ascidian embryogenesis.

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Configuration of Lhx3/4 protein domains and Tbx6-r locus in M. occidentalis.(A) Schematic of Moocci.Lhx3/4.b and Moocci.Lhx3/4.a proteins. LIM domains (LD1 and LD2) are in yellow, and the homeodomain (HD) is in green. Moocci.Lhx3/4.a retains a more extensive C-terminus including a highly conserved motif (highlighted in red) of unknown function. Alignment to Lhx3/4 orthologs from C. intestinalis (Ciinte) and humans (H.sapi.) is shown in inset. (B) Schematic representing the Tbx6-related locus in M. occidentalis, showing head-to-head configuration of Tbx6-r.a and Tbx6-r.b. Exons are represented by thick blocks. Tbx6-r.a is encoded by 6 exons, while Tbx6-r.b is encoded by only 2 exons. The region corresponding to the Moocci.Tbx6-r.b driver used in this study is shown in periwinkle.DOI:http://dx.doi.org/10.7554/eLife.03728.019
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fig4s2: Configuration of Lhx3/4 protein domains and Tbx6-r locus in M. occidentalis.(A) Schematic of Moocci.Lhx3/4.b and Moocci.Lhx3/4.a proteins. LIM domains (LD1 and LD2) are in yellow, and the homeodomain (HD) is in green. Moocci.Lhx3/4.a retains a more extensive C-terminus including a highly conserved motif (highlighted in red) of unknown function. Alignment to Lhx3/4 orthologs from C. intestinalis (Ciinte) and humans (H.sapi.) is shown in inset. (B) Schematic representing the Tbx6-related locus in M. occidentalis, showing head-to-head configuration of Tbx6-r.a and Tbx6-r.b. Exons are represented by thick blocks. Tbx6-r.a is encoded by 6 exons, while Tbx6-r.b is encoded by only 2 exons. The region corresponding to the Moocci.Tbx6-r.b driver used in this study is shown in periwinkle.DOI:http://dx.doi.org/10.7554/eLife.03728.019

Mentions: In each of the three Molgula genome assemblies, we identified two Tbx6-r genes of uncertain orthology relationships to the four Tbx6-r genes in the C. intestinalis genome (Stolfi et al., 2014). In all three Molgula genomes, the two Tbx6-r genes are arranged in head-to-head configuration with ∼2 kb separating the transcript start sites (Figure 4—figure supplement 2B). Despite the uncertain phylogeny of tunicate Tbx6-r genes, we named these genes Tbx6-r.a and Tbx6-r.b in Molgula. In M. occidentalis, both Tbx6-r.a and Tbx6-r.b are expressed in a broad posterior swath of the pre-gastrula embryo in a manner similar to the expression pattern of Tbx6-r genes in C. intestinalis (Figure 4C,D; Yagi et al., 2004).


Divergent mechanisms regulate conserved cardiopharyngeal development and gene expression in distantly related ascidians.

Stolfi A, Lowe EK, Racioppi C, Ristoratore F, Brown CT, Swalla BJ, Christiaen L - Elife (2014)

Configuration of Lhx3/4 protein domains and Tbx6-r locus in M. occidentalis.(A) Schematic of Moocci.Lhx3/4.b and Moocci.Lhx3/4.a proteins. LIM domains (LD1 and LD2) are in yellow, and the homeodomain (HD) is in green. Moocci.Lhx3/4.a retains a more extensive C-terminus including a highly conserved motif (highlighted in red) of unknown function. Alignment to Lhx3/4 orthologs from C. intestinalis (Ciinte) and humans (H.sapi.) is shown in inset. (B) Schematic representing the Tbx6-related locus in M. occidentalis, showing head-to-head configuration of Tbx6-r.a and Tbx6-r.b. Exons are represented by thick blocks. Tbx6-r.a is encoded by 6 exons, while Tbx6-r.b is encoded by only 2 exons. The region corresponding to the Moocci.Tbx6-r.b driver used in this study is shown in periwinkle.DOI:http://dx.doi.org/10.7554/eLife.03728.019
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4356046&req=5

fig4s2: Configuration of Lhx3/4 protein domains and Tbx6-r locus in M. occidentalis.(A) Schematic of Moocci.Lhx3/4.b and Moocci.Lhx3/4.a proteins. LIM domains (LD1 and LD2) are in yellow, and the homeodomain (HD) is in green. Moocci.Lhx3/4.a retains a more extensive C-terminus including a highly conserved motif (highlighted in red) of unknown function. Alignment to Lhx3/4 orthologs from C. intestinalis (Ciinte) and humans (H.sapi.) is shown in inset. (B) Schematic representing the Tbx6-related locus in M. occidentalis, showing head-to-head configuration of Tbx6-r.a and Tbx6-r.b. Exons are represented by thick blocks. Tbx6-r.a is encoded by 6 exons, while Tbx6-r.b is encoded by only 2 exons. The region corresponding to the Moocci.Tbx6-r.b driver used in this study is shown in periwinkle.DOI:http://dx.doi.org/10.7554/eLife.03728.019
Mentions: In each of the three Molgula genome assemblies, we identified two Tbx6-r genes of uncertain orthology relationships to the four Tbx6-r genes in the C. intestinalis genome (Stolfi et al., 2014). In all three Molgula genomes, the two Tbx6-r genes are arranged in head-to-head configuration with ∼2 kb separating the transcript start sites (Figure 4—figure supplement 2B). Despite the uncertain phylogeny of tunicate Tbx6-r genes, we named these genes Tbx6-r.a and Tbx6-r.b in Molgula. In M. occidentalis, both Tbx6-r.a and Tbx6-r.b are expressed in a broad posterior swath of the pre-gastrula embryo in a manner similar to the expression pattern of Tbx6-r genes in C. intestinalis (Figure 4C,D; Yagi et al., 2004).

Bottom Line: Ascidians present a striking dichotomy between conserved phenotypes and divergent genomes: embryonic cell lineages and gene expression patterns are conserved between distantly related species.Much research has focused on Ciona or Halocynthia spp. but development in other ascidians remains poorly characterized.In this study, we surveyed the multipotent myogenic B7.5 lineage in Molgula spp.

View Article: PubMed Central - PubMed

Affiliation: Center for Developmental Genetics, Department of Biology, New York University, New York, United States.

ABSTRACT
Ascidians present a striking dichotomy between conserved phenotypes and divergent genomes: embryonic cell lineages and gene expression patterns are conserved between distantly related species. Much research has focused on Ciona or Halocynthia spp. but development in other ascidians remains poorly characterized. In this study, we surveyed the multipotent myogenic B7.5 lineage in Molgula spp. Comparisons to the homologous lineage in Ciona revealed identical cell division and fate specification events that result in segregation of larval, cardiac, and pharyngeal muscle progenitors. Moreover, the expression patterns of key regulators are conserved, but cross-species transgenic assays uncovered incompatibility, or 'unintelligibility', of orthologous cis-regulatory sequences between Molgula and Ciona. These sequences drive identical expression patterns that are not recapitulated in cross-species assays. We show that this unintelligibility is likely due to changes in both cis- and trans-acting elements, hinting at widespread and frequent turnover of regulatory mechanisms underlying otherwise conserved aspects of ascidian embryogenesis.

Show MeSH
Related in: MedlinePlus