Divergent mechanisms regulate conserved cardiopharyngeal development and gene expression in distantly related ascidians

Stolfi, Alberto; Lowe, Elijah K.; Racioppi, Claudia; Ristoratore, Filomena; Brown, C. Titus; Swalla, Billie J.; Christiaen, Lionel

doi:10.7554/elife.03728

Cited by 76 publications

(143 citation statements)

References 120 publications

(197 reference statements)

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“…To test whether dnSar1 expression blocked TVC specification, we used fluorescence in situ hybridization (FISH) to assay expression of the TVC and tail muscle markers Hand-r (Handrelated, renamed after Hand-like/Notrlc; Stolfi et al, 2014) and Myosin regulatory light chain 2 (Mrlc2), respectively (Davidson and Levine, 2003;Satou et al, 2004). In contrast to control embryos, where Hand-r was expressed in both TVCs, high proportions of Mesp>dnSar1-electroporated embryos failed to activate Hand-r and repress Mrlc2 in the smaller B7.5-derived cells (supplementary material Fig.…”

Section: Tissue-specific Inhibition Of the Secretory Pathwaymentioning

confidence: 99%

“…In 9 hpf embryos, only the median-ventral TVC (the presumptive leader) contacts the Gata4/ Gata5/Gata6-expressing trunk endoderm [ Fig. 4A,A′; Gata4/Gata5/ Gata6 (Gata4/5/6) is renamed after GATAa; Ragkousi et al, 2011;Stolfi et al, 2014]. By 10 hpf, the anterior and medial surfaces of the leading TVC and a region of the medial surface of the trailer contact the endoderm, appearing as though the TVCs are carving a path through the endoderm (Fig.…”

Section: Inhibiting Secretion In the Notochord Delays The Onset Of Tvmentioning

confidence: 99%

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Surrounding tissues canalize motile cardiopharyngeal progenitors towards collective polarity and directed migration

et al. 2015

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Collectively migrating cells maintain group polarity and interpret external cues to reach their destination. The cardiogenic progenitors (also known as trunk ventral cells, TVCs) of the ascidian Ciona intestinalis provide a simple chordate model with which to study collective migration. Bilateral pairs of associated TVCs undergo a stereotyped polarized migration away from the tail towards the ventral trunk, arguably constituting the simplest possible example of directed collective migration. To identify tissues contributing to TVC polarity and migration, we quantified the contact between TVCs and surrounding tissues, and blocked the secretory pathway in a tissuespecific manner. Even though TVCs normally migrate as an invariably determined leader-trailer polarized pair of adherent cells, they are capable of migrating individually, albeit a shorter distance and with altered morphology. The mesenchyme contacts newborn TVCs and contributes to robust specification of the trailer but appears to have only minor effects on directed migration. The notochord does not contact the TVCs but contributes to the onset of migration. The trunk endoderm first contacts the leader TVC, then 'encases' both migrating cells and provides the inputs maintaining leader-trailer polarity. Migrating TVCs adhere to the epidermis and need this contact for their cohesion. These phenomenological studies reveal that inherently motile cardiopharyngeal progenitors are channeled into stereotyped behaviors by interactions with surrounding tissues.

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Section: Tissue-specific Inhibition Of the Secretory Pathwaymentioning

confidence: 99%

Section: Inhibiting Secretion In the Notochord Delays The Onset Of Tvmentioning

confidence: 99%

Surrounding tissues canalize motile cardiopharyngeal progenitors towards collective polarity and directed migration

et al. 2015

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“…Therefore, reconstructed trajectories are abstract representations of possible developmental transitions, but not the actual path followed by defined successions of clonally related progenitors. Among model organisms, the nematode Caenorhabditis elegans and ascidians of the genera Ciona , Halocynthia , Phallusia and Molgula have extensively annotated genomes and develop with fixed and well-documented embryonic lineages (Brozovic et al, 2016;Hirano and Nishida, 1997;Nishida, 1987;Stolfi et al, 2014a;Sulston et al, 1983) , thus offering opportunities to reconstruct developmental trajectories using scRNA-seq datasets with unequivocal clonal relationships between individual cells. Single cell analyses comprehensively characterized very early embryonic stages (Tintori et al, 2016) , and the L2 larval stage in C. elegans (Cao, Junyue, Jonathan S. Packer, Vijay Ramani, Darren A. Cusanovich, Chau Huynh, Riza Daza, Xiaojie Qiu, et al, 2017) , but there are technical difficulties in isolated healthy single cells from embryos.…”

Section: Introductionmentioning

confidence: 99%

A single cell transcriptional roadmap for cardiopharyngeal fate diversification

Wang

Niu

Jullian

et al. 2017

Preprint

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SummaryDynamic gene expression programs determine multipotent cell states and fate choices during development. Multipotent progenitors for cardiomyocytes and branchiomeric head muscles populate the pharyngeal mesoderm of vertebrate embryos, but the mechanisms underlying cardiopharyngeal multipotency and heart vs. head muscle fate choices remain elusive. The tunicate Ciona emerged as a simple chordate model to study cardiopharyngeal development with unprecedented spatio-temporal resolution. We analyzed the transcriptome of single cardiopharyngeal lineage cells isolated at successive time points encompassing the transitions from multipotent progenitors to distinct first and second heart, and pharyngeal muscle precursors. We reconstructed the three cardiopharyngeal developmental trajectories, and characterized gene expression dynamics and regulatory states underlying each fate choice.Experimental perturbations and bulk transcriptome analyses revealed that ongoing FGF/MAPK signaling maintains cardiopharyngeal multipotency and promotes the pharyngeal muscle fate, whereas signal termination permits the deployment of a full pan-cardiac program and heart fate specification. We identified the Dach1/2 homolog as a novel evolutionarily conserved second-heart-field-specific factor and demonstrate, through lineage tracing and CRISPR/Cas9 perturbations, that it operates downstream of Tbx1/10 to actively suppress the first heart lineage program. This data indicates that the regulatory state of multipotent cardiopharyngeal progenitors determines the first vs. second heart lineage choice, and that Tbx1/10 acts as a bona fide regulator of cardiopharyngeal multipotency.2 All rights reserved. No reuse allowed without permission.(which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.

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“…Alterations in gene expression are also thought to be responsible for many of the traits segregating in populations (Munafo et al 2003) and may contribute important somatic changes to the development of cancer (Ongen et al 2014). Despite this considerable interest, we currently have limited insight into which DNA sequence changes impact transcriptional regulation or how such regulatory networks evolve (Stolfi et al 2014).…”

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confidence: 99%

The frequent evolutionary birth and death of functional promoters in mouse and human

et al. 2015

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Promoters are central to the regulation of gene expression. Changes in gene regulation are thought to underlie much of the adaptive diversification between species and phenotypic variation within populations. In contrast to earlier work emphasizing the importance of enhancer evolution and subtle sequence changes at promoters, we show that dramatic changes such as the complete gain and loss (collectively, turnover) of functional promoters are common. Using quantitative measures of transcription initiation in both humans and mice across 52 matched tissues, we discriminate promoter sequence gains from losses and resolve the lineage of changes. We also identify expression divergence and functional turnover between orthologous promoters, finding only the latter is associated with local sequence changes. Promoter turnover has occurred at the majority (>56%) of protein-coding genes since humans and mice diverged. Tissue-restricted promoters are the most evolutionarily volatile where retrotransposition is an important, but not the sole, source of innovation. There is considerable heterogeneity of turnover rates between promoters in different tissues, but the consistency of these in both lineages suggests that the same biological systems are similarly inclined to transcriptional rewiring. The genes affected by promoter turnover show evidence of adaptive evolution. In mice, promoters are primarily lost through deletion of the promoter containing sequence, whereas in humans, many promoters appear to be gradually decaying with weak transcriptional output and relaxed selective constraint. Our results suggest that promoter gain and loss is an important process in the evolutionary rewiring of gene regulation and may be a significant source of phenotypic diversification.

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Divergent mechanisms regulate conserved cardiopharyngeal development and gene expression in distantly related ascidians

Cited by 76 publications

References 120 publications

Surrounding tissues canalize motile cardiopharyngeal progenitors towards collective polarity and directed migration

Surrounding tissues canalize motile cardiopharyngeal progenitors towards collective polarity and directed migration

A single cell transcriptional roadmap for cardiopharyngeal fate diversification

The frequent evolutionary birth and death of functional promoters in mouse and human

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