Nodal and Hedgehog synergize in gill slit formation during development of the cephalochordate <i>Branchiostoma floridae</i>

Ono, Hiroki; Koop, Demian; Holland, Linda Z.

doi:10.1242/dev.162586

Cited by 10 publications

(7 citation statements)

References 72 publications

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“…A single amphioxus hedgehog gene, hh, is expressed in the notochord and ventral neural tube, embryonic tissues that express Sonic-type genes in vertebrates (Shimeld, 1999;Ono et al, 2018;Zhu et al, 2020). Our scRNA-seq analysis detected cells with hh expression in cluster 9 at late gastrula and later stages (Figure 4B and Supplementary Figure 5B), indicating that cluster 9 comprises cells that form the notochord.…”

Section: Characterization Of Notochord Cluster 9 With Other Transcription Factor Genesmentioning

confidence: 79%

A Preliminary Single-Cell RNA-Seq Analysis of Embryonic Cells That Express Brachyury in the Amphioxus, Branchiostoma japonicum

Satoh

Tominaga

Kiyomoto

et al. 2021

Front. Cell Dev. Biol.

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Among chordate taxa, the cephalochordates diverged earlier than urochordates and vertebrates; thus, they retain unique, primitive developmental features. In particular, the amphioxus notochord has muscle-like properties, a feature not seen in urochordates or vertebrates. Amphioxus contains two Brachyury genes, Bra1 and Bra2. Bra2 is reportedly expressed in the blastopore, notochord, somites, and tail bud, in contrast to a low level of Bra1 expression only in notochord. To distinguish the expression profiles of the two Brachyury genes at the single-cell level, we carried out single-cell RNA-seq (scRNA-seq) analysis using the amphioxus, Branchiostoma japonicum. This scRNA-seq analysis classified B. japonicum embryonic cells into 15 clusters at developmental stages from midgastrula to early swimming larva. Brachyury was expressed in cells of clusters 4, 5, 8, and 9. We first confirmed that cluster 8 comprises cells that form somites since this cluster specifically expresses four myogenic factor genes. Cluster 9 contains a larger number of cells with high levels of Bra2 expression and a smaller number of cells with Bra1 expression. Simultaneous expression in cluster 9 of tool-kit genes, including FoxA, Goosecoid, and hedgehog, showed that this cluster comprises cells that form the notochord. Expression of Bra2, but not Bra1, in cells of clusters 4 and 5 at the gastrula stage together with expression of Wnt1 and Caudal indicates that clusters 4 and 5 comprise cells of the blastopore, which contiguously form the tail bud. In addition, Hox1, Hox3, and Hox4 were highly expressed in Bra2-expressing clusters 4, 5, 8, and 9 in a temporally coordinated manner, suggesting roles of anterior Hox genes in specification of mesodermal organs, including somites, notochord, and tail bud. This scRNA-seq analysis therefore highlights differences between the two Brachyury genes in relation to embryonic regions in which they are expressed and their levels of expression. Bra2 is the ancestral Brachyury in amphioxus, since expression in the blastopore is shared with other deuterostomes. On the other hand, Bra1 is a duplicate copy and likely evolved a supplementary function in notochord and somite formation in the Branchiostoma lineage.

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Section: Characterization Of Notochord Cluster 9 With Other Transcription Factor Genesmentioning

confidence: 79%

A Preliminary Single-Cell RNA-Seq Analysis of Embryonic Cells That Express Brachyury in the Amphioxus, Branchiostoma japonicum

Satoh

Tominaga

Kiyomoto

et al. 2021

Front. Cell Dev. Biol.

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“…Animals were maintained in the laboratory as previously described ( Zhang et al, 2007 ; Yong et al, 2019 ). Gametes were obtained either by electric stimulation, heat shock, or spontaneous spawning ( Holland and Yu, 2004 ; Ono et al, 2018 ). Embryos and larvae were cultured at constant temperatures (25°C or 30°C) until the desired stages, and larvae were fed daily with Isochrysis sp.…”

Section: Methodsmentioning

confidence: 99%

An Updated Staging System for Cephalochordate Development: One Table Suits Them All

Carvalho

Lahaye

Yong

et al. 2021

Front. Cell Dev. Biol.

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Chordates are divided into three subphyla: Vertebrata, Tunicata, and Cephalochordata. Phylogenetically, the Cephalochordata, more commonly known as lancelets or amphioxus, constitute the sister group of Vertebrata and Tunicata. Lancelets are small, benthic, marine filter feeders, and their roughly three dozen described species are divided into three genera: Branchiostoma, Epigonichthys, and Asymmetron. Due to their phylogenetic position and their stereotypical chordate morphology and genome architecture, lancelets are key models for understanding the evolutionary history of chordates. Lancelets have thus been studied by generations of scientists, with the first descriptions of adult anatomy and developmental morphology dating back to the 19th century. Today, several different lancelet species are used as laboratory models, predominantly for developmental, molecular and genomic studies. Surprisingly, however, a universal staging system and an unambiguous nomenclature for developing lancelets have not yet been adopted by the scientific community. In this work, we characterized the development of the European lancelet (Branchiostoma lanceolatum) using confocal microscopy and compiled a streamlined developmental staging system, from fertilization through larval life, including an unambiguous stage nomenclature. By tracing growth curves of the European lancelet reared at different temperatures, we were able to show that our staging system permitted an easy conversion of any developmental time into a specific stage name. Furthermore, comparisons of embryos and larvae from the European lancelet (B. lanceolatum), the Florida lancelet (Branchiostoma floridae), two Asian lancelets (Branchiostoma belcheri and Branchiostoma japonicum), and the Bahamas lancelet (Asymmetron lucayanum) demonstrated that our staging system could readily be applied to other lancelet species. Although the detailed staging description was carried out on developing B. lanceolatum, the comparisons with other lancelet species thus strongly suggested that both staging and nomenclature are applicable to all extant lancelets. We conclude that this description of embryonic and larval development will be of great use for the scientific community and that it should be adopted as the new standard for defining and naming developing lancelets. More generally, we anticipate that this work will facilitate future studies comparing representatives from different chordate lineages.

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“…156 Hh signaling has been studied with the smoothened inhibitor cyclopamine and no changes in neural patterning gene expression were observed. 157 However, the study focus was gill slit formation, and the drug treatment time only a 20-minute window, which might explain this outcome. Through generation of Hh −/− embryos using TALEN knockout, the role of Hh signaling in regulating left-right asymmetry in amphioxus has also been studied.…”

Section: Spinal Cord Patterning In Lampreys Sea Squirts and Ammentioning

confidence: 99%

“…Bmp signaling is known to regulate the patterning of epidermal neurons, though its impact on the spinal cord is not clear . Hh signaling has been studied with the smoothened inhibitor cyclopamine and no changes in neural patterning gene expression were observed . However, the study focus was gill slit formation, and the drug treatment time only a 20‐minute window, which might explain this outcome.…”

Section: Outgroups and Evolutionary Origins: Spinal Cords Cell Typesmentioning

confidence: 99%

Evolution of vertebrate spinal cord patterning

Leung

Shimeld

2019

Developmental Dynamics

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The vertebrate spinal cord is organized across three developmental axes, anterior‐posterior (AP), dorsal‐ventral (DV), and medial‐lateral (ML). Patterning of these axes is regulated by canonical intercellular signaling pathways: the AP axis by Wnt, fibroblast growth factor, and retinoic acid (RA), the DV axis by Hedgehog, Tgfβ, and Wnt, and the ML axis where proliferation is controlled by Notch. Developmental time plays an important role in which signal does what and when. Patterning across the three axes is not independent, but linked by interactions between signaling pathway components and their transcriptional targets. Combined this builds a sophisticated organ with many different types of cell in specific AP, DV, and ML positions. Two living lineages share phylum Chordata with vertebrates, amphioxus, and tunicates, while the jawless fish such as lampreys, survive as the most basally divergent vertebrate lineage. Genes and mechanisms shared between lampreys and other vertebrates tell us what predated vertebrates, while those also shared with other chordates tell us what evolved early in chordate evolution. Between these lie vertebrate innovations: genetic and developmental changes linked to evolution of new morphology. These include gene duplications, differences in how signals are received, and new regulatory connections between signaling pathways and their target genes.

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Nodal and Hedgehog synergize in gill slit formation during development of the cephalochordate Branchiostoma floridae

Cited by 10 publications

References 72 publications

A Preliminary Single-Cell RNA-Seq Analysis of Embryonic Cells That Express Brachyury in the Amphioxus, Branchiostoma japonicum

A Preliminary Single-Cell RNA-Seq Analysis of Embryonic Cells That Express Brachyury in the Amphioxus, Branchiostoma japonicum

An Updated Staging System for Cephalochordate Development: One Table Suits Them All

Evolution of vertebrate spinal cord patterning

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