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Open Access Research article

Identification of an intact ParaHox cluster with temporal colinearity but altered spatial colinearity in the hemichordate Ptychodera flava

Tetsuro Ikuta18, Yi-Chih Chen2, Rossella Annunziata3, Hsiu-Chi Ting2, Che-huang Tung2, Ryo Koyanagi1, Kunifumi Tagawa4, Tom Humphreys5, Asao Fujiyama6, Hidetoshi Saiga7, Nori Satoh1, Jr-Kai Yu2, Maria Ina Arnone3 and Yi-Hsien Su2*

Author Affiliations

1 Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa 904-0495, Japan

2 Institute of Cellular and Organismic Biology, Academia Sinica, Nankang, Taipei 11529, Taiwan

3 Stazione Zoologica Anton Dohrn, Napoli 80121, Italy

4 Marine Biological Laboratory, Graduate School of Science, Hiroshima University, Hiroshima 722-0073, Japan

5 Pacific Biomedical Research Center, University of Hawaii, Manoa, HI 96822, USA

6 National Institute of Genetics, Yata 1111, Mishima, Shizuoka 411-8540, Japan

7 Department of Biological Sciences, Graduate Schools of Science and Engineering, Tokyo Metropolitan University, Hachiohji, Tokyo 192-0397, Japan

8 Institute of Biogeoscience, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka 237-0061, Japan

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BMC Evolutionary Biology 2013, 13:129  doi:10.1186/1471-2148-13-129

Published: 27 June 2013

Abstract

Background

ParaHox and Hox genes are thought to have evolved from a common ancestral ProtoHox cluster or from tandem duplication prior to the divergence of cnidarians and bilaterians. Similar to Hox clusters, chordate ParaHox genes including Gsx, Xlox, and Cdx, are clustered and their expression exhibits temporal and spatial colinearity. In non-chordate animals, however, studies on the genomic organization of ParaHox genes are limited to only a few animal taxa. Hemichordates, such as the Enteropneust acorn worms, have been used to gain insights into the origins of chordate characters. In this study, we investigated the genomic organization and expression of ParaHox genes in the indirect developing hemichordate acorn worm Ptychodera flava.

Results

We found that P. flava contains an intact ParaHox cluster with a similar arrangement to that of chordates. The temporal expression order of the P. flava ParaHox genes is the same as that of the chordate ParaHox genes. During embryogenesis, the spatial expression pattern of PfCdx in the posterior endoderm represents a conserved feature similar to the expression of its orthologs in other animals. On the other hand, PfXlox and PfGsx show a novel expression pattern in the blastopore. Nevertheless, during metamorphosis, PfXlox and PfCdx are expressed in the endoderm in a spatially staggered pattern similar to the situation in chordates.

Conclusions

Our study shows that P. flava ParaHox genes, despite forming an intact cluster, exhibit temporal colinearity but lose spatial colinearity during embryogenesis. During metamorphosis, partial spatial colinearity is retained in the transforming larva. These results strongly suggest that intact ParaHox gene clustering was retained in the deuterostome ancestor and is correlated with temporal colinearity.

Keywords:
Hemichordate; Ptychodera Flava; ParaHox; Colinearity