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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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Divergent Molgula Lhx3/4.b homeodomains are not predicted to have altered DNA binding specificities.(A) Alignment of homeodomains (HDs) from a set of Molgula Lhx3/4 family proteins, with HD recognition positions highlighted in yellow. HD recognition positions are invariant while intervening sequence is highly diverged between Lhx3/4.a and Lhx3/4.b. (B) Logos and matrices for predicted homeodmain specificities for Moocci.Lhx3/4.a (top) and Moocci.Lhx3/4.b (bottom), generated by the Homeodomain Specificity Prediction web page (http://stormo.wustl.edu/cgi-bin/flyhd/hd_pred.cgi; Noyes et al., 2008). The two predicted binding specificities are identical to one another, due to perfect conservation of the HD recognition positions.DOI:http://dx.doi.org/10.7554/eLife.03728.020
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fig4s3: Divergent Molgula Lhx3/4.b homeodomains are not predicted to have altered DNA binding specificities.(A) Alignment of homeodomains (HDs) from a set of Molgula Lhx3/4 family proteins, with HD recognition positions highlighted in yellow. HD recognition positions are invariant while intervening sequence is highly diverged between Lhx3/4.a and Lhx3/4.b. (B) Logos and matrices for predicted homeodmain specificities for Moocci.Lhx3/4.a (top) and Moocci.Lhx3/4.b (bottom), generated by the Homeodomain Specificity Prediction web page (http://stormo.wustl.edu/cgi-bin/flyhd/hd_pred.cgi; Noyes et al., 2008). The two predicted binding specificities are identical to one another, due to perfect conservation of the HD recognition positions.DOI:http://dx.doi.org/10.7554/eLife.03728.020

Mentions: We also identified two Lhx3/4 genes in each Molgula genome. This was unexpected because no Lhx3/4 duplications have been identified in any ascidian species (Christiaen et al., 2009a; Kobayashi et al., 2010). We named these genes Lhx3/4.a and Lhx3/4.b. In all three Molgula species, Lhx3/4.a is the more conserved paralog, while Lhx3/4.b is more divergent, lacking a well-conserved C-terminal motif (Figure 4—figure supplement 2A). However, the amino acid sequence changes are not predicted to change the DNA-binding preference of the homeodomain (Figure 4—figure supplement 3; Noyes et al., 2008). In each of the three Molgula species’ genome assemblies, the two Lhx3/4 genes were found to be located on separate contigs.


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)

Divergent Molgula Lhx3/4.b homeodomains are not predicted to have altered DNA binding specificities.(A) Alignment of homeodomains (HDs) from a set of Molgula Lhx3/4 family proteins, with HD recognition positions highlighted in yellow. HD recognition positions are invariant while intervening sequence is highly diverged between Lhx3/4.a and Lhx3/4.b. (B) Logos and matrices for predicted homeodmain specificities for Moocci.Lhx3/4.a (top) and Moocci.Lhx3/4.b (bottom), generated by the Homeodomain Specificity Prediction web page (http://stormo.wustl.edu/cgi-bin/flyhd/hd_pred.cgi; Noyes et al., 2008). The two predicted binding specificities are identical to one another, due to perfect conservation of the HD recognition positions.DOI:http://dx.doi.org/10.7554/eLife.03728.020
© Copyright Policy
Related In: Results  -  Collection

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

fig4s3: Divergent Molgula Lhx3/4.b homeodomains are not predicted to have altered DNA binding specificities.(A) Alignment of homeodomains (HDs) from a set of Molgula Lhx3/4 family proteins, with HD recognition positions highlighted in yellow. HD recognition positions are invariant while intervening sequence is highly diverged between Lhx3/4.a and Lhx3/4.b. (B) Logos and matrices for predicted homeodmain specificities for Moocci.Lhx3/4.a (top) and Moocci.Lhx3/4.b (bottom), generated by the Homeodomain Specificity Prediction web page (http://stormo.wustl.edu/cgi-bin/flyhd/hd_pred.cgi; Noyes et al., 2008). The two predicted binding specificities are identical to one another, due to perfect conservation of the HD recognition positions.DOI:http://dx.doi.org/10.7554/eLife.03728.020
Mentions: We also identified two Lhx3/4 genes in each Molgula genome. This was unexpected because no Lhx3/4 duplications have been identified in any ascidian species (Christiaen et al., 2009a; Kobayashi et al., 2010). We named these genes Lhx3/4.a and Lhx3/4.b. In all three Molgula species, Lhx3/4.a is the more conserved paralog, while Lhx3/4.b is more divergent, lacking a well-conserved C-terminal motif (Figure 4—figure supplement 2A). However, the amino acid sequence changes are not predicted to change the DNA-binding preference of the homeodomain (Figure 4—figure supplement 3; Noyes et al., 2008). In each of the three Molgula species’ genome assemblies, the two Lhx3/4 genes were found to be located on separate contigs.

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