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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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Alignment of Foxf coding and non-coding sequences.Diagram of mVISTA alignment of M. oculata Foxf (Moocul.Foxf) locus aligned to orthologs in (from top to bottom) M. occulta, M. occidentalis, and C. intestinalis. Blue-shaded peaks indicate protein-coding sequence conservation above 70% in 100-bp windows. Red-shaded peaks indicate non-coding sequence conservation above 70% in 100-bp windows. Sequence conservation between the Roscovite Molgulids (M. oculata and M. occulta) and M. occidentalis is limited to protein-coding portions, and conservation between Molgula and Ciona is limited to a narrow portion of the sequence coding for the Foxf DNA-binding domain. Only the first exon of Foxf is shown.DOI:http://dx.doi.org/10.7554/eLife.03728.026
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fig6s1: Alignment of Foxf coding and non-coding sequences.Diagram of mVISTA alignment of M. oculata Foxf (Moocul.Foxf) locus aligned to orthologs in (from top to bottom) M. occulta, M. occidentalis, and C. intestinalis. Blue-shaded peaks indicate protein-coding sequence conservation above 70% in 100-bp windows. Red-shaded peaks indicate non-coding sequence conservation above 70% in 100-bp windows. Sequence conservation between the Roscovite Molgulids (M. oculata and M. occulta) and M. occidentalis is limited to protein-coding portions, and conservation between Molgula and Ciona is limited to a narrow portion of the sequence coding for the Foxf DNA-binding domain. Only the first exon of Foxf is shown.DOI:http://dx.doi.org/10.7554/eLife.03728.026

Mentions: Given the conservation of the MAPK/Ets pathway in ascidian TVC specification, we reasoned that Foxf cis-regulatory sequences should be compatible in cross-species assays. We identified a sequence upstream of the Moocci.Foxf gene that is sufficient to drive TVC-specific expression in M. occidentalis (Figure 6G, Figure 6—figure supplement 1). However, this sequence is completely non-functional when tested in C. intestinalis (Figure 6H). Likewise, a previously identified Ciinte.Foxf TVC enhancer (Figure 6J; Beh et al., 2007) is incapable of driving TVC-specific expression in M. occidentalis embryos (Figure 6I).


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)

Alignment of Foxf coding and non-coding sequences.Diagram of mVISTA alignment of M. oculata Foxf (Moocul.Foxf) locus aligned to orthologs in (from top to bottom) M. occulta, M. occidentalis, and C. intestinalis. Blue-shaded peaks indicate protein-coding sequence conservation above 70% in 100-bp windows. Red-shaded peaks indicate non-coding sequence conservation above 70% in 100-bp windows. Sequence conservation between the Roscovite Molgulids (M. oculata and M. occulta) and M. occidentalis is limited to protein-coding portions, and conservation between Molgula and Ciona is limited to a narrow portion of the sequence coding for the Foxf DNA-binding domain. Only the first exon of Foxf is shown.DOI:http://dx.doi.org/10.7554/eLife.03728.026
© Copyright Policy
Related In: Results  -  Collection

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

fig6s1: Alignment of Foxf coding and non-coding sequences.Diagram of mVISTA alignment of M. oculata Foxf (Moocul.Foxf) locus aligned to orthologs in (from top to bottom) M. occulta, M. occidentalis, and C. intestinalis. Blue-shaded peaks indicate protein-coding sequence conservation above 70% in 100-bp windows. Red-shaded peaks indicate non-coding sequence conservation above 70% in 100-bp windows. Sequence conservation between the Roscovite Molgulids (M. oculata and M. occulta) and M. occidentalis is limited to protein-coding portions, and conservation between Molgula and Ciona is limited to a narrow portion of the sequence coding for the Foxf DNA-binding domain. Only the first exon of Foxf is shown.DOI:http://dx.doi.org/10.7554/eLife.03728.026
Mentions: Given the conservation of the MAPK/Ets pathway in ascidian TVC specification, we reasoned that Foxf cis-regulatory sequences should be compatible in cross-species assays. We identified a sequence upstream of the Moocci.Foxf gene that is sufficient to drive TVC-specific expression in M. occidentalis (Figure 6G, Figure 6—figure supplement 1). However, this sequence is completely non-functional when tested in C. intestinalis (Figure 6H). Likewise, a previously identified Ciinte.Foxf TVC enhancer (Figure 6J; Beh et al., 2007) is incapable of driving TVC-specific expression in M. occidentalis embryos (Figure 6I).

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