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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 5′ flanking sequences from Mesp orthologs.Top: diagram of mVISTA (Frazer et al., 2004; genome.lbl.gov/vista/) alignment of M. occidentalis Mesp (Moocci.Mesp) locus to orthologs in (from top to bottom) M. oculata, M. occulta, and C. intestinalis. Bottom: diagram of mVISTA alignment of C. intestinalis Mesp (Moocci.Mesp) locus to orthologs in (from top to bottom) M. oculata, M. occulta, and M. occidentalis. Blue-shaded peaks indicate protein-coding sequence conservation above 70% in 100-bp windows. Arrows indicate direction of transcription of protein-coding genes Slc5a-related and Mesp.DOI:http://dx.doi.org/10.7554/eLife.03728.004
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fig1s1: Alignment of 5′ flanking sequences from Mesp orthologs.Top: diagram of mVISTA (Frazer et al., 2004; genome.lbl.gov/vista/) alignment of M. occidentalis Mesp (Moocci.Mesp) locus to orthologs in (from top to bottom) M. oculata, M. occulta, and C. intestinalis. Bottom: diagram of mVISTA alignment of C. intestinalis Mesp (Moocci.Mesp) locus to orthologs in (from top to bottom) M. oculata, M. occulta, and M. occidentalis. Blue-shaded peaks indicate protein-coding sequence conservation above 70% in 100-bp windows. Arrows indicate direction of transcription of protein-coding genes Slc5a-related and Mesp.DOI:http://dx.doi.org/10.7554/eLife.03728.004

Mentions: Our sequencing efforts revealed extreme genetic divergence not only between Ciona and Molgula, as expected, but even within the Molgulids. For example, we used BLAST to identify the Molgula orthologs of C. intestinalis Mesp (Ciinte.Mesp, as per the proposed tunicate gene nomenclature rules, see Stolfi et al., 2014). Ciinte.Mesp is the sole ortholog of vertebrate genes coding for MesP and Mesogenin bHLH transcription factor family members (Satou et al., 2004). VISTA alignment shows high sequence similarity between sequences 5′ upstream of the Mesp genes from the closely related M. oculata and M. occulta (Figure 1B). However, there is no conservation of Mesp DNA sequences, coding or non-coding, between M. oculata/occulta and M. occidentalis, nor between C. intestinalis and any of the three Molgula species (Figure 1—figure supplement 1). In previous phylogenetic surveys, M. occidentalis has been placed as an early-branching Molgula species, often grouped together in a subfamily with species ascribed to the genera Eugyra and Bostrichobranchus instead (Hadfield et al., 1995; Huber et al., 2000; Tsagkogeorga et al., 2009). Our sequencing results support the view that M. occidentalis is highly diverged from other Molgula spp.


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 5′ flanking sequences from Mesp orthologs.Top: diagram of mVISTA (Frazer et al., 2004; genome.lbl.gov/vista/) alignment of M. occidentalis Mesp (Moocci.Mesp) locus to orthologs in (from top to bottom) M. oculata, M. occulta, and C. intestinalis. Bottom: diagram of mVISTA alignment of C. intestinalis Mesp (Moocci.Mesp) locus to orthologs in (from top to bottom) M. oculata, M. occulta, and M. occidentalis. Blue-shaded peaks indicate protein-coding sequence conservation above 70% in 100-bp windows. Arrows indicate direction of transcription of protein-coding genes Slc5a-related and Mesp.DOI:http://dx.doi.org/10.7554/eLife.03728.004
© Copyright Policy
Related In: Results  -  Collection

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

fig1s1: Alignment of 5′ flanking sequences from Mesp orthologs.Top: diagram of mVISTA (Frazer et al., 2004; genome.lbl.gov/vista/) alignment of M. occidentalis Mesp (Moocci.Mesp) locus to orthologs in (from top to bottom) M. oculata, M. occulta, and C. intestinalis. Bottom: diagram of mVISTA alignment of C. intestinalis Mesp (Moocci.Mesp) locus to orthologs in (from top to bottom) M. oculata, M. occulta, and M. occidentalis. Blue-shaded peaks indicate protein-coding sequence conservation above 70% in 100-bp windows. Arrows indicate direction of transcription of protein-coding genes Slc5a-related and Mesp.DOI:http://dx.doi.org/10.7554/eLife.03728.004
Mentions: Our sequencing efforts revealed extreme genetic divergence not only between Ciona and Molgula, as expected, but even within the Molgulids. For example, we used BLAST to identify the Molgula orthologs of C. intestinalis Mesp (Ciinte.Mesp, as per the proposed tunicate gene nomenclature rules, see Stolfi et al., 2014). Ciinte.Mesp is the sole ortholog of vertebrate genes coding for MesP and Mesogenin bHLH transcription factor family members (Satou et al., 2004). VISTA alignment shows high sequence similarity between sequences 5′ upstream of the Mesp genes from the closely related M. oculata and M. occulta (Figure 1B). However, there is no conservation of Mesp DNA sequences, coding or non-coding, between M. oculata/occulta and M. occidentalis, nor between C. intestinalis and any of the three Molgula species (Figure 1—figure supplement 1). In previous phylogenetic surveys, M. occidentalis has been placed as an early-branching Molgula species, often grouped together in a subfamily with species ascribed to the genera Eugyra and Bostrichobranchus instead (Hadfield et al., 1995; Huber et al., 2000; Tsagkogeorga et al., 2009). Our sequencing results support the view that M. occidentalis is highly diverged from other Molgula spp.

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