David B and Mooi R (2014), How Hox genes can shed light on the place of ec...

ECB-ART-48250

Evodevo 2014 Jun 17;5:22. doi: 10.1186/2041-9139-5-22.

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

David B , Mooi R .

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BACKGROUND: The Hox gene cluster ranks among the greatest of biological discoveries of the past 30 years. Morphogenetic patterning genes are remarkable for the systems they regulate during major ontogenetic events, and for their expressions of molecular, temporal, and spatial colinearity. Recent descriptions of exceptions to these colinearities are suggesting deep phylogenetic signal that can be used to explore origins of entire deuterostome phyla. Among the most enigmatic of these deuterostomes in terms of unique body patterning are the echinoderms. However, there remains no overall synthesis of the correlation between this signal and the variations observable in the presence/absence and expression patterns of Hox genes. RESULTS: Recent data from Hox cluster analyses shed light on how the bizarre shift from bilateral larvae to radial adults during echinoderm ontogeny can be accomplished by equally radical modifications within the Hox cluster. In order to explore this more fully, a compilation of observations on the genetic patterns among deuterostomes is integrated with the body patterning trajectories seen across the deuterostome clade. CONCLUSIONS: Synthesis of available data helps to explain morphogenesis along the anterior/posterior axis of echinoderms, delineating the origins and fate of that axis during ontogeny. From this, it is easy to distinguish between ''seriality'' along echinoderm rays and true A/P axis phenomena such as colinearity within the somatocoels, and the ontogenetic outcomes of the unique translocation and inversion of the anterior Hox class found within the Echinodermata. An up-to-date summary and integration of the disparate lines of research so far produced on the relationship between Hox genes and pattern formation for all deuterostomes allows for development of a phylogeny and scenario for the evolution of deuterostomes in general, and the Echinodermata in particular.

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Species referenced: Echinodermata
Genes referenced: evxl Hoxa2l hoxa3l hoxa7l hoxa9 hoxal hoxb1l hoxb8 LOC100887844 LOC100893907 LOC105439231 LOC575073 meox1 otx2 pax2 pax2l

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	Figure 1. General organization of a complete Hox cluster with the two additional genes Mox and Evx (uppermost row). The Hox genes are grouped into three classes (Hox3 has been included in the anterior class). Also indicated are expression of the spatial (middle row) and temporal (bottom row) colinearities.
	Figure 2. Arrangement of the Hox cluster in major deuterostome clades.Evx and Mox genes, located in the vicinity of the Hox cluster, are also indicated. Tree topology is a synthesis of [17,23], and [113] for echinoderm clades. Terminals are based on data from taxa as follows: derived vertebrates on Mus (mouse); basal vertebrates on Lethenteron (lamprey); larvacean urochordates on Oikopleura; ascidian urochordates on Ciona; cephalochordates on Branchiostoma (amphioxus); hemichordates on Saccoglossus (acorn worm); crinoids on a combination of Metacrinus (sea lily) and Oxycomanthus (feather star); asteroids on a combination of Asterias and Patiriella (starfish); ophiuroids on Stegophiura (brittle star); holothuroids on Holothuria (sea cucumber); and echinoids on Strongylocentrotus (purple sea urchin). Note that for echinoderms, the alignments for the anterior class are shown in the recently discovered translocated, inverted condition. The nature of the lines through the complex on the right denotes the position of genes on a single (one continuous line), on few (several broken lines), or on many (no line) chromosomes. Putative arrangements are shown by dashed lines.
	Figure 3. Diagrammatic cross-section of a young post-metamorphic, generalized echinoderm (only the left side is portrayed). This presentation synthesizes developmental, morphological, and paleontology data [95,96]. Typically, echinoderms begin development as bilateral embryos or larvae. At metamorphosis, a new structure (the rudiment) develops on the left side of the larva. The elaboration of the rudiment involves three main coelomic cavities, which during metamorphosis turn to stack postero-anteriorly: right somatocoel (dark blue), left somatocoel (light blue), and hydrocoel (red). The hydrocoel takes on a ring shape and produces five radiating extensions (the primary lobes) that will give rise to the primary podia, which will in turn mark the extremity of the five growing radial water vessels. The adult water vascular system, derived from the hydrocoel, comprises the circumoral ring and the radial water vessels. The tube feet (secondary podia) are lateral buds branching on those radial water vessels. In the oral direction, the left somatocoel develops five extensions that proceed through the hydrocoelar ring, separate from the left somatocoel and fuse to form the hyponeural sinus (dental sacs in echinoids). From this sinus will develop the hyponeural radial canals. More anteriorly, the epidermal layer thickens and bends into five epineural folds, which will give rise to the nerves (green) and epineural sinuses (orange), following the same pattern as the hydrocoel: circumoral (epineural and nerve rings), and radial elements (epineural canals and radial nerves). In summary, there are two main regions to a developing echinoderm. One incorporates right and left somatocoels and develops from the non-rudiment region of the larva; it corresponds to the extraxial part of the body (sensu EAT [95,113]). The other incorporates the hydrocoel (water vascular system), the hyponeural elements and the epithelial derivatives (nerves and epineural strands) and is derived from a rudiment that develops laterally on the larva; it corresponds to the axial part of the body (sensu EAT).
	Figure 4. Comparison of Hox expression domains in crinoids and echinoids. Figure showing antero-posterior organization of anatomical elements at postmetamorphic stages. Hox gene assignments in square brackets represent complementary data from other taxa. Vertical purple arrows represent the somatocoelar hox vectors.
	Figure 5. Expression pattern of the Intervening Zone and of related genes among bilaterian Animalia. The IZ (separating Otx and Hox1 domains) corresponds to the midbrain-hindbrain boundary (MHB) in vertebrates, the neck region of urochordates, the anterior part of the second somite in cephalochordates, the deutocerebrum of insects, and to the anterior part of the trunk in annelids. Expression domains of Pax2/5/8 and En are shown (diamonds) only when they are located between those of Otx and Hox1. Expression domains of Pax2/5/8 are still largely unknown in Ambulacraria, hence the two alternative hypotheses shown for this character.
	Figure 6. Departure from the colinearity rules in echinoderms (crinoids and echinoids). (A) Crinoids. (B) Echinoids. The most parsimonious hypothesis regarding the spatial and temporal expression of the Hox genes in crinoids and echinoids indicates that both groups ‘violate’ the spatial colinearity rule as their body (portrayed by a conceptualized bilaterian) is subdivided according to specific Hox expression vectors. The order of Hox genes along the cluster might follow the time vector in crinoids (dashed line indicates that the gene array remains putative), whereas it does not in echinoids in which the temporal colinearity rule is likewise not entirely followed.
	Figure 7. Phylogenetic mapping of important changes in the evolution of the deuterostome Hox cluster. (A) Chordata. (B) Ambulacraria.Hox1 has been identified in all deuterostomes. Hox2 is present in all but asteroids and ophiuroids, suggesting that its absence, if confirmed, is a synapomorphy for the asterozoan clade. Hox3 has not been identified in pedunculate crinoids, nor in the larvacean Oikopleura. Hox4 is present in all the groups considered herein, except in the crownward clade grouping echinoids and holothuroids. Hox5 is missing in Oikopleura, possibly in comatulid crinoids, and putatively in the poorly known ophiuroids. Hox6 has not been detected in Oikopleura, pedunculate crinoids, and it is possibly also absent in comatulids, ophiuroids, and holothuroids. The domains of expression of Hox5 and perhaps Hox6 could have been shifted anteriorly in some echinoderms; the position of this apomorphy on the tree depends of the character state in Asterozoa. Hox7 and Hox8 are present in all deuterostomes except two groups of urochordates and perhaps holothuroids. Their absence in two urochordate clades suggests that loss of Hox7 and Hox8 is autapomorphic for this phylum. Hox9 and Hox10 have been identified in all chordates with the sole exception that Hox9 is missing in the urochordate Ciona[114]. In Ambulacraria, all groups have a Hox9/10 gene. Hox11, Hox12, and Hox13 are present in all chordates with the exception of Ciona, which is lacking Hox11[114], but Ambulacraria have Hox 11/13abc genes not ortholog with those of chordates [56]. Hox14 is convergent between cephalochordates and cyclostomes. Hox15 is exclusive to cephalochordates. Among the related genes of the extended Hox cluster, Mox could be present in all deuterostome clades, pending further explorations in echinoderms, with two paralogous copies found only in vertebrates. Evx is present in all metazoans, including clades as basal as cnidarians [13], but two copies exist in all chordate groups (presumed apomorphy), except in larvaceans (presumed reversion).

References [+] :

Acampora, Genetic and molecular roles of Otx homeodomain proteins in head development. 2000, Pubmed