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Curr Genomics
2015 Oct 01;175:444-449. doi: 10.2174/1389202917666160616082436.
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Hox Gene Collinearity: From A-P Patterning to Radially Symmetric Animals.
Papageorgiou S
.
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Hox gene collinearity relates the gene order of the Hox cluster in the chromosome (telomeric to centromeric end) with the serial activation of these genes in the ontogenetic units along the Anterior-Posterior embryonic axis. Although this collinearity property is well respected in bilaterians (e.g. vertebrates), it is violated in other animals. The A-P axis is established in the early embryo of the sea urchin. Subsequently, rotational symmetry is superimposed when the vestibula larva is formed. In analogy to the linear A-P case, it is here hypothesized that the circular topology of the ontogenetic modules is associated to the architectural restructuring of the Hox loci where the two discrete ends of the Hox cluster approach each other so that an almost circular DNA contour is created. In the evolutionary process the circular mode undergoes double strand breaks and the generated cluster ends are attached to the open ends of the flanking chromosome. This event may lead to a novel gene ordering associated with an evolutionary innovation. For example, the loss of Hox4 is followed by the formation of a shorter gene circular arrangement. The opening of this contour at the missing Hox4 location and its connection to the chromosomal flanking ends leads to a new diversification namely the creation of the unusual gene order of the sea urchin Hox cluster.
Fig. (1).
Developmental stages of echinoderms. a) Strongylocentrotus purpuratus embryo where m and s stand for the mouth and stomach along the A-P axis respectively [17]. b) Holopneustes purpurescens vestibula larva with A, B, C, D and E podia locations [21]. c) Juvenile sea urchin [17].
Fig. (2).
Gene ordering in Hox gene clusters. a) Theoretical Hox gene order of the common ancestor. Mox and Evx genes are located in the side of the anterior and posterior ends of the Hox cluster respectively [20]. b) The HoxA cluster of the mouse (vertebrate) [20]. c) The Hox cluster of A. planci. Hox6 is missing [28]. d) The Hox cluster of the sea urchin S. purpuratus. Hox4 is missing [29].
Fig. (3).
DNA contours. a) The linear DNA fiber is restructured and twisted so that the two ends of the linear Hox cluster come close together. b) In the encircled domain the ends of the circularized cluster (Hox1 and Hox13) are connected to the 3’ and 5’ ends of the flanking chromosome. If Hox1 is attached to the 3’ end and Hox13 to the 5’ end the linear arrangement produces the A. planci gene order (Fig. 2c). c) If Hox5 is connected to the 3’ end and Hox13 to Hox3 on the flanking chromosome, the linear arrangement represents the sea urchin Hox cluster (Fig. 2d).
Fig. (4).
Simplified phylogenic diagram for Vertebrates, Asteroids and Echinoids. Diversifications from the Common Ancestor (left) of the gene order in the Hox cluster. The vertebrates (top) retain the usual gene order of the common ancestor. The gene order of the asteroid Hox cluster (middle) is similar to the usual ordering and with a subsequent rearrangement of the gene order, the sea urchin Hox cluster is created (bottom).
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