How Hox genes can shed light on the place of echinoderms among the deuterostomes

David, Bruno; Mooi, Rich

doi:10.1186/2041-9139-5-22

Cited by 43 publications

(62 citation statements)

References 106 publications

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“…Apomorphies of the Ambulacraria: planktotrophic tornaria larvae with ciliary bands of monociliate cells showing ciliary reversal (Strathmann, 2007); excretory axial complex (Nielsen, 2012a); Hox genes 9/11, 11/13abc (David & Mooi, 2014).…”

Section: The Origin Of the Chordatamentioning

confidence: 99%

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Evolution of deuterostomy - and origin of the chordates

Nielsen

2015

Biol Rev

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The chordates are usually characterized as bilaterians showing deuterostomy, i.e. the mouth developing as a new opening between the archenteron and the ectoderm, serial gill pores/slits, and the complex of chorda and neural tube. Both numerous molecular studies and studies of morphology and embryology demonstrate that the neural tube must be considered homologous to the ventral nerve cord(s) of the protostomes, but the origin of the 'new' mouth of the deuterostomes has remained enigmatic. However, deuterostomy is known to occur in several protostomian groups, such as the chaetognaths and representatives of annelids, molluscs, arthropods and priapulans. This raises the question whether the deuterostomian mouth is in fact homologous with that of the protostomes, viz. the anterior opening of the ancestral blastopore divided through lateral blastopore fusion, i.e. amphistomy. A few studies of gene expression show identical expression patterns around mouth and anus in protostomes and deuterostomes. Closer studies of the embryology of ascidians and vertebrates show that the mouth/stomodaeum differentiates from the anterior edge of the neural plate. Together this indicates that the chordate mouth has moved to the anterior edge of the blastopore, so that the anterior loop of the ancestral circumblastoporal nerve cord, which is narrow in the protostomes, has become indistinguishable. In the vertebrates, the mouth has moved further around the anterior pole to the 'ventral' side. The conclusion must be that the chordate mouth (and that of the deuterostomes in general) is homologous to the protostomian mouth and that the latest common ancestor of protostomes and deuterostomes developed through amphistomy, as suggested by the trochaea theory.

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Section: The Origin Of the Chordatamentioning

confidence: 99%

“…Apomorphies of the Chordata: direct development; chorda + neural tube complex; segmented body musculature; Hox genes 9-13 (David & Mooi, 2014).…”

Section: The Origin Of the Chordatamentioning

confidence: 99%

Evolution of deuterostomy - and origin of the chordates

Nielsen

2015

Biol Rev

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“…The gene locations in these two characteristic clusters are depicted in Fig.1. In the unusual sea urchin cluster, Hox1 to Hox3 have been translocated to the 5’ end while the other genes are inverted and translocated to the 3’ end as shown in Fig.1b [13].…”

Section: Ontogeny Of Echinodermsmentioning

confidence: 99%

“…In Echinoderms, bilateral symmetry and anterior-posterior patterning clearly appear at the very early stages of their ontogeny [13,14]. Subsequently and for the sea urchin larva stages, rotational and radial symmetries emerge [14].…”

Section: Ontogeny Of Echinodermsmentioning

confidence: 99%

The unusual gene order in the Echinoderm Hox cluster is related to the embryo and larva symmetries

Papageorgiou

2015

Preprint

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Background Hox gene collinearity relates the sequential location of Hox genes in the 3’ to 5’ direction on the chromosome with the linear arrangement of the body elements along the anterior-posterior (A/P) axis of bilaterian embryos. This spatial Hox gene collinearity has been almost universally respected in diverse organisms like worms, insects or vertebrates. It is therefore surprising that the above well established collinearity rule is violated in the case of Echinoderms. No explanation of this violation is apparent. Here a hypothesis is put forward which provides a cue to understand the abnormal serial gene location in the sea urchin disorganized Hox cluster. Results Bilateral symmetry along the A/P embryo axis is established at the very early stages of ontogeny of the sea urchin. For the subsequent developmental stages, rotational symmetry emerges in the vestibula larva. In analogy to the linear A/P case, the circular topology of modules might be a reflection of the architectural restructuring of the Hox loci where the 3’ and 5’ ends of the Hox cluster approach each other so that a closed contour of the chromatin fiber is formed. At a later stage, the break and opening of the cluster contour at the level of Hox4 combined with the rotational symmetry leads to the observed Hox gene sequence that violates the standard 3’ to 5’ collinearity. Conclusion The unusual gene series manifests the congruence of Hox gene sequence in the cluster with the circular arrangement of the sea urchin primary podia. Accordingly, the Hox sequence after the break at Hox4 is not a violation but an extension of Hox gene collinearity to animals with rotational symmetry.

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“…Select species have been a focus of investigation for over a century, and recent work on developmental gene regulatory networks has revolutionized our understanding of cell specification mechanisms [2]. Most scenarios for the evolution of development in echinoderms are thus founded chiefly on extant taxa [3]. However, living echinoderms have diverged greatly from the latest common ancestor they share with all deuterostomes and, hence, might not closely reflect developmental processes in the earliest forms.…”

Section: Introductionmentioning

confidence: 99%

Early post-metamorphic, Carboniferous blastoid reveals the evolution and development of the digestive system in echinoderms

et al. 2015

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Inferring the development of the earliest echinoderms is critical to uncovering the evolutionary assembly of the phylum-level body plan but has long proven problematic because early ontogenetic stages are rarely preserved as fossils. Here, we use synchrotron tomography to describe a new early postmetamorphic blastoid echinoderm from the Carboniferous (approx. 323 Ma) of China. The resulting three-dimensional reconstruction reveals a U-shaped tubular structure in the fossil interior, which is interpreted as the digestive tract. Comparisons with the developing gut of modern crinoids demonstrate that crinoids are an imperfect analogue for many extinct groups. Furthermore, consideration of our findings in a phylogenetic context allows us to reconstruct the evolution and development of the digestive system in echinoderms more broadly; there was a transition from a straight to a simple curved gut early in the phylum's evolution, but additional loops and coils of the digestive tract (as seen in crinoids) were not acquired until much later.

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How Hox genes can shed light on the place of echinoderms among the deuterostomes

Cited by 43 publications

References 106 publications

Evolution of deuterostomy - and origin of the chordates

Evolution of deuterostomy - and origin of the chordates

The unusual gene order in the Echinoderm Hox cluster is related to the embryo and larva symmetries

Early post-metamorphic, Carboniferous blastoid reveals the evolution and development of the digestive system in echinoderms

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