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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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Ets.b expression in B7.5 of M. occidentalis.In situ hybridization (ISH) for Moocci.Ets.b in 110-cell st/early gastrula embryo, showing expression (green) in the B7.5 blastomeres. Nuclei are counterstained with DAPI (blue). Embryo was imaged from a vegetal view, with anterior to the top.DOI:http://dx.doi.org/10.7554/eLife.03728.009
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fig2s1: Ets.b expression in B7.5 of M. occidentalis.In situ hybridization (ISH) for Moocci.Ets.b in 110-cell st/early gastrula embryo, showing expression (green) in the B7.5 blastomeres. Nuclei are counterstained with DAPI (blue). Embryo was imaged from a vegetal view, with anterior to the top.DOI:http://dx.doi.org/10.7554/eLife.03728.009

Mentions: In M. occidentalis, Ets.b expression is initiated in B7.5 blastomeres (Figure 2—figure supplement 1), is maintained in their daughter cells the cardiopharyngeal founders and in the TVCs during their migration (Figure 2A). This profile is similar to the expression of C. intestinalis Ets.b (Ciinte.Ets.b), previously named Ets/pointed2 or Ets1/2 (see Supplementary file 2 for list of old and new gene name correspondences). In C. intestinalis, Ets.b mediates the FGF/MAPK-dependent induction of TVCs in part by the activation of key regulators such as Foxf, Hand-related (Hand-r, also known as Hand-like or NoTrlc), and Gata4/5/6 (also known as GATA-a) prior to the onset of TVC migration (Davidson et al., 2006; Beh et al., 2007). In M. occidentalis, orthologs of Foxf and Hand-r are also activated in the TVCs shortly before and throughout their migration away from the ATMs (Figure 2B,C). Moocci.Gata4/5/6 expression was detected in migrating TVCs but not before migration (Figure 2D). This is slightly different from Ciinte.Gata4/5/6, which is expressed in C. intestinalis TVCs prior to migration (Christiaen et al., 2010; Ragkousi et al., 2011). Expression of Moocci.Foxf and Moocci.Gata4/5/6 in surrounding epidermis and endoderm, respectively, is identical to the expression domains of their orthologs in C. intestinalis and sometimes obscured TVC expression. However, double ISH/immunohistochemical detection (ISH/IHC) of Moocci.Mesp promoter-driven reporter gene clearly shows transcripts in the migrating B7.5-derived TVCs (Figure 2—figure supplement 2A–C).


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)

Ets.b expression in B7.5 of M. occidentalis.In situ hybridization (ISH) for Moocci.Ets.b in 110-cell st/early gastrula embryo, showing expression (green) in the B7.5 blastomeres. Nuclei are counterstained with DAPI (blue). Embryo was imaged from a vegetal view, with anterior to the top.DOI:http://dx.doi.org/10.7554/eLife.03728.009
© Copyright Policy
Related In: Results  -  Collection

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

fig2s1: Ets.b expression in B7.5 of M. occidentalis.In situ hybridization (ISH) for Moocci.Ets.b in 110-cell st/early gastrula embryo, showing expression (green) in the B7.5 blastomeres. Nuclei are counterstained with DAPI (blue). Embryo was imaged from a vegetal view, with anterior to the top.DOI:http://dx.doi.org/10.7554/eLife.03728.009
Mentions: In M. occidentalis, Ets.b expression is initiated in B7.5 blastomeres (Figure 2—figure supplement 1), is maintained in their daughter cells the cardiopharyngeal founders and in the TVCs during their migration (Figure 2A). This profile is similar to the expression of C. intestinalis Ets.b (Ciinte.Ets.b), previously named Ets/pointed2 or Ets1/2 (see Supplementary file 2 for list of old and new gene name correspondences). In C. intestinalis, Ets.b mediates the FGF/MAPK-dependent induction of TVCs in part by the activation of key regulators such as Foxf, Hand-related (Hand-r, also known as Hand-like or NoTrlc), and Gata4/5/6 (also known as GATA-a) prior to the onset of TVC migration (Davidson et al., 2006; Beh et al., 2007). In M. occidentalis, orthologs of Foxf and Hand-r are also activated in the TVCs shortly before and throughout their migration away from the ATMs (Figure 2B,C). Moocci.Gata4/5/6 expression was detected in migrating TVCs but not before migration (Figure 2D). This is slightly different from Ciinte.Gata4/5/6, which is expressed in C. intestinalis TVCs prior to migration (Christiaen et al., 2010; Ragkousi et al., 2011). Expression of Moocci.Foxf and Moocci.Gata4/5/6 in surrounding epidermis and endoderm, respectively, is identical to the expression domains of their orthologs in C. intestinalis and sometimes obscured TVC expression. However, double ISH/immunohistochemical detection (ISH/IHC) of Moocci.Mesp promoter-driven reporter gene clearly shows transcripts in the migrating B7.5-derived TVCs (Figure 2—figure supplement 2A–C).

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