A stem-deuterostome origin of the vertebrate pharyngeal transcriptional network

Gillis, J. Andrew; Fritzenwanker, Jens H.; Lowe, Christopher J.

doi:10.1098/rspb.2011.0599

Cited by 90 publications

(86 citation statements)

References 59 publications

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“…Second, when chordate features such as a notochord, a dorsal neural tube, myotomes, a postanal tail, pharyngeal slits and an endostyle are rethought in relation to their function, it appears that the first four are primarily associated with locomotion, while the last two pertain to the digestive system. Recent studies reveal the presence of genes relevant to formation of pharyngeal slits not only in chordates but also hemichordates [69,70]. The stomochord is an anterior outgrowth of the pharynx into the proboscis of acorn worms.…”

Section: (D) the Aboral-dorsalization Hypothesismentioning

confidence: 99%

Chordate evolution and the three-phylum system

2014

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Traditional metazoan phylogeny classifies the Vertebrata as a subphylum of the phylum Chordata, together with two other subphyla, the Urochordata (Tunicata) and the Cephalochordata. The Chordata, together with the phyla Echinodermata and Hemichordata, comprise a major group, the Deuterostomia. Chordates invariably possess a notochord and a dorsal neural tube. Although the origin and evolution of chordates has been studied for more than a century, few authors have intimately discussed taxonomic ranking of the three chordate groups themselves. Accumulating evidence shows that echinoderms and hemichordates form a clade (the Ambulacraria), and that within the Chordata, cephalochordates diverged first, with tunicates and vertebrates forming a sister group. Chordates share tadpole-type larvae containing a notochord and hollow nerve cord, whereas ambulacrarians have dipleurula-type larvae containing a hydrocoel. We propose that an evolutionary occurrence of tadpole-type larvae is fundamental to understanding mechanisms of chordate origin. Protostomes have now been reclassified into two major taxa, the Ecdysozoa and Lophotrochozoa, whose developmental pathways are characterized by ecdysis and trochophore larvae, respectively. Consistent with this classification, the profound dipleurula versus tadpole larval differences merit a category higher than the phylum. Thus, it is recommended that the Ecdysozoa, Lophotrochozoa, Ambulacraria and Chordata be classified at the superphylum level, with the Chordata further subdivided into three phyla, on the basis of their distinctive characteristics.

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Section: (D) the Aboral-dorsalization Hypothesismentioning

confidence: 99%

Chordate evolution and the three-phylum system

2014

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“…The present study shows that the genetic regulation of pax1 and tbx1 and the function of pax1 in gill slit segmentation are conserved among aquatic chordates. Furthermore, our model provides a reasonable explanation for gill slit development in hemichordates, which lack tbx1/10 expression in the pharynx (Gillis et al, 2012). Regarding the origin of the deuterostome gill slit, pax1/9 might have acquired a reiterative expression pattern in the pharyngeal endoderm, which may then have facilitated the segmental development of endodermal outpocketings.…”

Section: Impact Of Pax1 On Pharyngeal Segmentation and Derivativesmentioning

confidence: 64%

“…Previous studies demonstrated the remarkable conservation of the expression patterns of genes governing the development of vertebrate pharyngeal pouches and the gill slits of non-vertebrate deuterostomes, clearly illustrating the homology between these structures (Holland et al, 1995;Müller et al, 1996;Wallin et al, 1996;Ogasawara et al, 1999Ogasawara et al, , 2000Lowe et al, 2003;Gillis et al, 2012). Therefore, revealing the mechanism of segmented pharyngeal pouch formation is indispensable for shedding light on not only vertebrate developmental principles but also the evolutionary origins of the vertebrate body plan (Graham et al, 2014).…”

Section: Introductionmentioning

confidence: 88%

“…The original function of pax1/9 might be related to gill slit segmentation itself, as evidenced by the highly conserved expression patterns of the cognates in deuterostome pharyngeal endoderm (Holland et al, 1995;Müller et al, 1996;Wallin et al, 1996;Ogasawara et al, 1999Ogasawara et al, , 2000Lowe et al, 2003;Gillis et al, 2012). Recent pax1/9 knockdown experiments in amphioxus revealed a role in gill slit segmentation and that pax1/9 deficiency leads to a reduction in tbx1/10 expression (Liu et al, 2015).…”

Section: Impact Of Pax1 On Pharyngeal Segmentation and Derivativesmentioning

confidence: 99%

“…Conserved expression of pax1/9 homologs in pharyngeal gill slits provides key evidence of the homology between deuterostome gill slits and pharyngeal pouches (Holland et al, 1995;Müller et al, 1996;Wallin et al, 1996;Ogasawara et al, 1999Ogasawara et al, , 2000Lowe et al, 2003;Gillis et al, 2012). Previous reports clearly demonstrated the developmental functions of Pax1 in organogenesis of the thymus and parathyroid glands, sclerotome delineation, chondrogenesis and vertebral column formation (Wallin et al, 1996;Peters et al, 1999;Su et al, 2001;Mise et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

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Reiterative expression of pax1 directs pharyngeal pouch segmentation in medaka (Oryzias latipes)

et al. 2016

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A striking characteristic of vertebrate development is the pharyngeal arches, which are a series of bulges on the lateral surface of the head of vertebrate embryos. Although each pharyngeal arch is segmented by the reiterative formation of endodermal outpocketings called pharyngeal pouches, the molecular network underlying the reiterative pattern remains unclear. Here, we show that pax1 plays crucial roles in pouch segmentation in medaka (Oryzias latipes) embryos. Importantly, pax1 expression in the endoderm prefigures the location of the next pouch before the cells bud from the epithelium. TALEN-generated pax1 mutants did not form pharyngeal pouches posterior to the second arch. Segmental expression of tbx1 and fgf3, which play essential roles in pouch development, was almost nonexistent in the pharyngeal endoderm of pax1 mutants, with disturbance of the reiterative pattern of pax1 expression. These results suggest that pax1 plays a key role in generating the primary pattern for segmentation in the pharyngeal endoderm by regulating tbx1 and fgf3 expression. Our findings illustrate the crucial roles of pax1 in vertebrate pharyngeal segmentation and provide insights into the evolutionary origin of the deuterostome gill slit.

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Hemichordates: Development

Miyamoto

Wada

2015

Encyclopedia of Life Sciences

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Hemichordates are marine invertebrates consisting of two distinct groups: the solitary enteropneusts, or acorn worms (comprising a few hundred species), and the colonial and tube‐dwelling pterobranchs (comprising 20 or so species). Phylogenetically, hemichordates are the sister group to echinoderms, together composing the Ambulacraria, and share some features with chordates. Hemichordates are thus considered key organisms for addressing the origins of deuterostome and chordate body plans. Unlike the other deuterostome models including echinoderms and chordates, however, information about the developmental biology of this group is limited. Recent improvements in the accessibility of embryos, functional tool development and genomic resources from several model organisms have yielded important information on the cellular and genetic mechanisms of embryogenesis and organogenesis in hemichordates. Comparisons of hemichordates and other deuterostomes permit identification of the common ancestor of deuterostomes and help elucidate the origin of the chordate body plan. Key Concepts Hemichordate developmental biology is key to elucidating the origin of chordates and the early evolution of deuterostomes. Descriptive and comparative studies using novel model species provide new insights into hemichordate evolution and diversity. Establishment of genetic resources and experimental methods drive the molecular developmental biology of hemichordates. Hemichordates and chordates show a conserved anteroposterior patterning mechanism. Hemichordate research indicates that inversion of the dorsoventral axis occurred in the chordate lineage. Gill slits of hemichordates and chordates are almost certainly homologous. The stomochord of hemichordates and the notochord of chordates share some genetic features, but are unlikely to be homologous. The origin of the tubular nervous system predates the diversification of hemichordates and chordates, but the homology of the collar nerve cord and neural tube still requires resolution.

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A stem-deuterostome origin of the vertebrate pharyngeal transcriptional network

Cited by 90 publications

References 59 publications

Chordate evolution and the three-phylum system

Chordate evolution and the three-phylum system

Reiterative expression of pax1 directs pharyngeal pouch segmentation in medaka (Oryzias latipes)

Hemichordates: Development

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