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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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Delayed atrial siphon primordium specification in M. occidentalis.(A) Dorsal view of hatched larva (13 hpf) stained with Alexa Fluor 546 phalloidin, showing oral siphon primordium (OSP) as a distinct structure, while the atrial siphon primordium (ASP) has not formed yet. (B) Dorsal view of metamorphosing juvenile (>72 hpf) stained with Alexa Fluor 546 phalloidin showing fully formed ASP as a rosette of apically constricted cells. OSP is out of the plane of view. (C) Dorsal view of M. oculata hatched larva stained with Alexa Fluor 633 phalloidin, showing formation of both OSP and ASP at this stage.DOI:http://dx.doi.org/10.7554/eLife.03728.015
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fig3s2: Delayed atrial siphon primordium specification in M. occidentalis.(A) Dorsal view of hatched larva (13 hpf) stained with Alexa Fluor 546 phalloidin, showing oral siphon primordium (OSP) as a distinct structure, while the atrial siphon primordium (ASP) has not formed yet. (B) Dorsal view of metamorphosing juvenile (>72 hpf) stained with Alexa Fluor 546 phalloidin showing fully formed ASP as a rosette of apically constricted cells. OSP is out of the plane of view. (C) Dorsal view of M. oculata hatched larva stained with Alexa Fluor 633 phalloidin, showing formation of both OSP and ASP at this stage.DOI:http://dx.doi.org/10.7554/eLife.03728.015

Mentions: We also noticed a difference in ASM precursor behavior. In C. intestinalis, migrating ASMPs from either side of the embryo migrate dorsally, forming rings around a bilateral pair of atrial siphon primordia (ASPs) on the corresponding side (Stolfi et al., 2010). The ASPs are placode-like rosettes of molecularly and morphologically distinct ectodermal cells that arise through a retinoic acid/Hox1- and FGF/MAPK-dependent program and are proposed to be homologous to vertebrate otic placodes (Wada et al., 1998; Mazet et al., 2005; Kourakis and Smith, 2007; Sasakura et al., 2012). In juveniles of C. intestinalis and other phlebobranch ascidians, there are initially two atrial siphons, one on either side of the animal, that eventually fuse into a single one at the end of the ‘1st Ascidian’ stage (Chiba et al., 2004; Kourakis et al., 2010). In contrast, all stolidobranch ascidians initially specify a single ASP, bypassing the two-siphon fusion process (Manni et al., 2004; Grave, 1926; Figure 3—figure supplement 2A–C). Indeed, we observed the formation of a single ASP in M. occidentalis late in metamorphosis and in the larvae of M. oculata (Figure 3—figure supplement 2A,B). This flexibility in atrial siphon development in ascidians is an example of DSD at the morphogenetic level. It is believed that the dual primordium condition is ancestral and that the specification of a single primordium is a derived, Stolidobranchia-specific trait (Kourakis et al., 2010).


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)

Delayed atrial siphon primordium specification in M. occidentalis.(A) Dorsal view of hatched larva (13 hpf) stained with Alexa Fluor 546 phalloidin, showing oral siphon primordium (OSP) as a distinct structure, while the atrial siphon primordium (ASP) has not formed yet. (B) Dorsal view of metamorphosing juvenile (>72 hpf) stained with Alexa Fluor 546 phalloidin showing fully formed ASP as a rosette of apically constricted cells. OSP is out of the plane of view. (C) Dorsal view of M. oculata hatched larva stained with Alexa Fluor 633 phalloidin, showing formation of both OSP and ASP at this stage.DOI:http://dx.doi.org/10.7554/eLife.03728.015
© Copyright Policy
Related In: Results  -  Collection

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

fig3s2: Delayed atrial siphon primordium specification in M. occidentalis.(A) Dorsal view of hatched larva (13 hpf) stained with Alexa Fluor 546 phalloidin, showing oral siphon primordium (OSP) as a distinct structure, while the atrial siphon primordium (ASP) has not formed yet. (B) Dorsal view of metamorphosing juvenile (>72 hpf) stained with Alexa Fluor 546 phalloidin showing fully formed ASP as a rosette of apically constricted cells. OSP is out of the plane of view. (C) Dorsal view of M. oculata hatched larva stained with Alexa Fluor 633 phalloidin, showing formation of both OSP and ASP at this stage.DOI:http://dx.doi.org/10.7554/eLife.03728.015
Mentions: We also noticed a difference in ASM precursor behavior. In C. intestinalis, migrating ASMPs from either side of the embryo migrate dorsally, forming rings around a bilateral pair of atrial siphon primordia (ASPs) on the corresponding side (Stolfi et al., 2010). The ASPs are placode-like rosettes of molecularly and morphologically distinct ectodermal cells that arise through a retinoic acid/Hox1- and FGF/MAPK-dependent program and are proposed to be homologous to vertebrate otic placodes (Wada et al., 1998; Mazet et al., 2005; Kourakis and Smith, 2007; Sasakura et al., 2012). In juveniles of C. intestinalis and other phlebobranch ascidians, there are initially two atrial siphons, one on either side of the animal, that eventually fuse into a single one at the end of the ‘1st Ascidian’ stage (Chiba et al., 2004; Kourakis et al., 2010). In contrast, all stolidobranch ascidians initially specify a single ASP, bypassing the two-siphon fusion process (Manni et al., 2004; Grave, 1926; Figure 3—figure supplement 2A–C). Indeed, we observed the formation of a single ASP in M. occidentalis late in metamorphosis and in the larvae of M. oculata (Figure 3—figure supplement 2A,B). This flexibility in atrial siphon development in ascidians is an example of DSD at the morphogenetic level. It is believed that the dual primordium condition is ancestral and that the specification of a single primordium is a derived, Stolidobranchia-specific trait (Kourakis et al., 2010).

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