Genomic and Evolutionary Insights into Chordate Origins

Luttrell, Shawn M.; Swalla, Billie J.

doi:10.1016/b978-0-12-405945-0.00007-7

Cited by 3 publications

(4 citation statements)

References 98 publications

(181 reference statements)

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“…Many of the genes involved in placode development are highly conserved from invertebrates to vertebrates, indicating that the underlying transcriptional pathways are evolutionarily very old (Bassham and Postlthwait, 2005; Schlosser, 2005; Schlosser, 2007; Gasparini et al, 2013; Graham and Shimeld, 2013; Luttrell and Swalla, 2014). Mutation of genes involved in placode development lead to a variety of congenital syndromes in humans that share craniofacial dysmorphologies and hearing loss.…”

Section: Discussionmentioning

confidence: 99%

Transcriptional Regulation of Cranial Sensory Placode Development

Moody

LaMantia

2015

Current Topics in Developmental Biology

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Cranial sensory placodes derive from discrete patches of the head ectoderm, and give rise to numerous sensory structures. During gastrulation, a specialized “neural border zone” forms around the neural plate in response to interactions between the neural and non-neural ectoderm and signals from adjacent mesodermal and/or endodermal tissues. This zone subsequently gives rise to two distinct precursor populations of the peripheral nervous system: the neural crest and the pre-placodal ectoderm (PPE). The PPE is a common field from which all cranial sensory placodes arise (adenohypophyseal, olfactory, lens, trigeminal, epibranchial, otic). Members of the Six family of transcription factors are major regulators of PPE specification, in partnership with co-factor proteins such as Eya. Six gene activity also maintains tissue boundaries between the PPE, neural crest and epidermis by repressing genes that specify the fates of those adjacent ectodermally-derived domains. As the embryo acquires anterior-posterior identity, the PPE becomes transcriptionally regionalized, and it subsequently subdivides into specific placodes with distinct developmental fates in response to signaling from adjacent tissues. Each placode is characterized by a unique transcriptional program that leads to the differentiation of highly specialized cells, such as neurosecretory cells, somatic sensory receptor cells, chemosensory neurons, peripheral glia and supporting cells. In this review, we summarize the transcriptional and signaling factors that regulate key steps of placode development, influence subsequent sensory neuron specification, and discuss what is known about mutations in some of the essential PPE genes that underlie human congenital syndromes.

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Section: Discussionmentioning

confidence: 99%

Transcriptional Regulation of Cranial Sensory Placode Development

Moody

LaMantia

2015

Current Topics in Developmental Biology

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“…In addition to nerve cords, P. flava also develops a hollow, neural tube that is positioned dorsally in the collar region. Our lab has shown this structure forms from ectoderm that invaginates and rolls up forming a hollow tube, similar to chordate neurulation (Morgan, 1894;Luttrell et al, 2012;Miyamoto and Wada, 2013;Luttrell and Swalla, 2014).…”

Section: Introductionmentioning

confidence: 91%

“…Upon metamorphosis, the larva develops into a juvenile worm that settles to the ocean floor to begin a benthic lifestyle. Solitary hemichordates are exclusively marine and adult animals have a tripartite body plan with an anterior proboscis that is used for digging and burrowing in the sand and mud, a middle collar region with a hollow, dorsal neural tube in ptychoderid hemichordates, a ventral mouth between the proboscis and collar, and a long posterior trunk with pharyngeal gill slits and gonads in the anterior trunk, a hepatic region in the mid-trunk and a terminal anus (Balser and Ruppert, 1990;Brown et el., 2008;Luttrell and Swalla, 2014). The hemichordate nervous system is quite interesting.…”

Section: Introductionmentioning

confidence: 99%

Head regeneration in hemichordates is not a strict recapitulation of development

Luttrell

Gotting

Ross

et al. 2016

Developmental Dynamics

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Background: Head or anterior body part regeneration is commonly associated with protostome, but not deuterostome invertebrates. However, it has been shown that the solitary hemichordate Ptychodera flava possesses the remarkable capacity to regenerate their entire nervous system, including their dorsal neural tube and their anterior head‐like structure, or proboscis. Hemichordates, also known as acorn worms, are marine invertebrate deuterostomes that have retained chordate traits that were likely present in the deuterostome ancestor, placing these animals in a vital position to study regeneration and chordate evolution. All acorn worms have a tripartite body plan, with an anterior proboscis, middle collar region, and a posterior trunk. The collar houses a hollow, dorsal neural tube in ptychoderid hemichordates and numerous chordate genes involved in brain and spinal cord development are expressed in a similar anterior–posterior spatial arrangement along the body axis. Results: We have examined anterior regeneration in the hemichordate Ptychodera flava and report the spatial and temporal morphological changes that occur. Additionally, we have sequenced, assembled, and analyzed the transcriptome for eight stages of regenerating P. flava, revealing significant differential gene expression between regenerating and control animals. Conclusions: Importantly, we have uncovered developmental steps that are regeneration‐specific and do not strictly follow the embryonic program. Developmental Dynamics 245:1159–1175, 2016. © 2016 The Authors. Developmental Dynamics published by Wiley Periodicals, Inc. on behalf of American Association of Anatomists

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“…This poses the question of whether indirect development was a trait present in the common ancestor of both animal lineages. On the other hand, in contrast to pentaradial symmetry in adult echinoderms, hemichordates share bilateral symmetry with chordates, with a distinctive tripartite body plan of proboscis, collar and trunk (Urata and Yamaguchi 2004;Billie J. Swalla 2007). They show conserved structures such as pharyngeal gill slits, supporting their position within deuterostomes (Simakov et al 2015;Lowe et al 2015).…”

Section: Introductionmentioning

confidence: 99%

Insights into deuterostome evolution from the biphasic transcriptional programme of hemichordates

Pérez-Posada

Lin

et al. 2022

Preprint

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Evolutionary history of deuterostomes has remained unsolved and is intimately related to how chordates originated. Within the clade of deuterostomes, hemichordates and echinoderms (together called Ambulacraria) are sister groups of chordates; comparative studies among the three are insightful for understanding deuterostome evolution. Indirect-developing hemichordates, such as Ptychodera flava, develop into planktonic larvae, which are morphologically similar to echinoderm larvae, before metamorphosing into the adult body plan that retains an anteroposterior polarity homologous to that of chordates. Therefore, deciphering developmental programmes of indirect-developing hemichordates may provide a key for understanding the evolution of deuterostomes and chordate origins. Here, we characterise transcriptomes and chromatin accessibility across multiple developmental stages of P. flava and uncover biphasic developmental programmes controlled by different sets of transcription factors and their corresponding cis-regulatory elements. Transcriptome age and network analyses reveal that the gastrula transcriptome is relatively ancient and highly connected. By comparing developmental transcriptomes of hemichordate, sea urchin and amphioxus, a high conservation of gene expression during gastrulation is identified and extended to neurula stages of amphioxus, in addition to the highly similar larval transcriptomes among the three species. Moreover, P. flava possesses conserved interactions of transcription factors required for the development of echinoderm endomesoderm and chordate axial mesoderm. These results suggest a deuterostome phylotypic stage during gastrulation (corresponding to amphioxus gastrulation and neurulation) controlled by gene regulatory networks with conserved cis-regulatory interactions, and support the hypothesis that the deuterostome ancestor is an indirect-developer.

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Genomic and Evolutionary Insights into Chordate Origins

Cited by 3 publications

References 98 publications

Transcriptional Regulation of Cranial Sensory Placode Development

Transcriptional Regulation of Cranial Sensory Placode Development

Head regeneration in hemichordates is not a strict recapitulation of development

Insights into deuterostome evolution from the biphasic transcriptional programme of hemichordates

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