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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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Asymmetric intelligibility between Molgula and Ciona Hand-r TVC enhancers.(A) β-galactosidase immunodetection on M. occidentalis late tailbud embryo electroporated with Ciinte.Hand-r>nls::lacZ., showing reporter gene expression in TVC descendents (heart precursors and atrial siphon muscle founder cells) on one side of the embryo. (B) M. occidentalis embryo electroporated with Moocul.Hand-r>H2B::GFP, showing recapitulation of endogenous Moocci.Hand-r expression in endoderm, A7.6 lineage, and TVCs. (C) C. intestinalis embryo electroporated with Moocul.Hand-r>H2B::GFP showing slight expression in A7.6 lineage and B-line mesenchyme cells, but no expression in TVCs (hollow arrowheads).DOI:http://dx.doi.org/10.7554/eLife.03728.024
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fig7s1: Asymmetric intelligibility between Molgula and Ciona Hand-r TVC enhancers.(A) β-galactosidase immunodetection on M. occidentalis late tailbud embryo electroporated with Ciinte.Hand-r>nls::lacZ., showing reporter gene expression in TVC descendents (heart precursors and atrial siphon muscle founder cells) on one side of the embryo. (B) M. occidentalis embryo electroporated with Moocul.Hand-r>H2B::GFP, showing recapitulation of endogenous Moocci.Hand-r expression in endoderm, A7.6 lineage, and TVCs. (C) C. intestinalis embryo electroporated with Moocul.Hand-r>H2B::GFP showing slight expression in A7.6 lineage and B-line mesenchyme cells, but no expression in TVCs (hollow arrowheads).DOI:http://dx.doi.org/10.7554/eLife.03728.024

Mentions: Curiously, we found that the Ciinte.Hand-r reporter can drive reporter gene expression in M. occidentalis TVCs (Figure 7—figure supplement 1). Thus, unlike the case of Foxf, there is an asymmetric intelligibility of Hand-r TVC enhancers between M. occidentalis and C. intestinalis. Moreover, a M. oculata Hand-r TVC enhancer is functional in M. occidentalis but not in C. intestinalis (Figure 7—figure supplement 1). Taken together, these data suggest that differences in enhancer logic may have accumulated over the course of the deep evolutionary history between Molgula and Ciona but not between M. occidentalis and M. oculata, and that some enhancers may have evolved asymmetrically in the two branches, retaining greater pan-ascidian ‘intelligibility’ in one or the other.


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)

Asymmetric intelligibility between Molgula and Ciona Hand-r TVC enhancers.(A) β-galactosidase immunodetection on M. occidentalis late tailbud embryo electroporated with Ciinte.Hand-r>nls::lacZ., showing reporter gene expression in TVC descendents (heart precursors and atrial siphon muscle founder cells) on one side of the embryo. (B) M. occidentalis embryo electroporated with Moocul.Hand-r>H2B::GFP, showing recapitulation of endogenous Moocci.Hand-r expression in endoderm, A7.6 lineage, and TVCs. (C) C. intestinalis embryo electroporated with Moocul.Hand-r>H2B::GFP showing slight expression in A7.6 lineage and B-line mesenchyme cells, but no expression in TVCs (hollow arrowheads).DOI:http://dx.doi.org/10.7554/eLife.03728.024
© Copyright Policy
Related In: Results  -  Collection

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

fig7s1: Asymmetric intelligibility between Molgula and Ciona Hand-r TVC enhancers.(A) β-galactosidase immunodetection on M. occidentalis late tailbud embryo electroporated with Ciinte.Hand-r>nls::lacZ., showing reporter gene expression in TVC descendents (heart precursors and atrial siphon muscle founder cells) on one side of the embryo. (B) M. occidentalis embryo electroporated with Moocul.Hand-r>H2B::GFP, showing recapitulation of endogenous Moocci.Hand-r expression in endoderm, A7.6 lineage, and TVCs. (C) C. intestinalis embryo electroporated with Moocul.Hand-r>H2B::GFP showing slight expression in A7.6 lineage and B-line mesenchyme cells, but no expression in TVCs (hollow arrowheads).DOI:http://dx.doi.org/10.7554/eLife.03728.024
Mentions: Curiously, we found that the Ciinte.Hand-r reporter can drive reporter gene expression in M. occidentalis TVCs (Figure 7—figure supplement 1). Thus, unlike the case of Foxf, there is an asymmetric intelligibility of Hand-r TVC enhancers between M. occidentalis and C. intestinalis. Moreover, a M. oculata Hand-r TVC enhancer is functional in M. occidentalis but not in C. intestinalis (Figure 7—figure supplement 1). Taken together, these data suggest that differences in enhancer logic may have accumulated over the course of the deep evolutionary history between Molgula and Ciona but not between M. occidentalis and M. oculata, and that some enhancers may have evolved asymmetrically in the two branches, retaining greater pan-ascidian ‘intelligibility’ in one or the other.

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