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Genetic organization and embryonic expression of the ParaHox genes in the sea urchin S. purpuratus: Insights into the relationship between clustering and colinearity

Amone, Maria I. and Rizzo, Francesca and Annunciata, Rosella and Cameron, R. Andrew and Peterson, Kevin J. and Martínez, Pedro (2006) Genetic organization and embryonic expression of the ParaHox genes in the sea urchin S. purpuratus: Insights into the relationship between clustering and colinearity. Developmental Biology, 300 (1). pp. 63-73. ISSN 0012-1606. https://resolver.caltech.edu/CaltechAUTHORS:20121031-073253328

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Abstract

The ANTP family of homeodomain transcription factors consists of three major groups, the NKL, the extended Hox, and the Hox/ParaHox family. Hox genes and ParaHox genes are often linked in the genome forming two clusters of genes, the Hox cluster and the ParaHox cluster, and are expressed along the major body axis in a nested fashion, following the relative positions of the genes within these clusters, a property called colinearity. While the presences of a Hox cluster and a ParaHox cluster appear to be primitive for bilaterians, few taxa have actually been examined for spatial and temporal colinearity, and, aside from chordates, even fewer still manifest it. Here we show that the ParaHox genes of the sea urchin Strongylocentrotus purpuratus show both spatial and temporal colinearity, but with peculiarities. Specifically, two of the three ParaHox genes-discovered through the S. purpuratus genome project-Sp-lox and Sp-Cdx, are expressed in the developing gut with nested domains in a spatially colinear manner. However, transcripts of Sp-Gsx, although anterior of Sp-lox, are detected in the ectoderm and not in the gut. Strikingly, the expression of the three ParaHox genes would follow temporal colinearity if they were clustered in the same order as in chordates, but each ParaHox gene is actually found on a different genomic scaffold (> 300 kb each), which suggests that they are not linked into a single coherent cluster. Therefore, ParaHox genes are dispersed in the genome and are used during embryogenesis in a temporally and spatially coherent manner, whereas the Hox genes, now fully sequenced and annotated, are still linked and are employed as a complex only during the emergence of the adult body plan in the larva.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1016/j.ydbio.2006.07.037DOIArticle
http://www.sciencedirect.com/science/article/pii/S0012160606010670PublisherArticle
ORCID:
AuthorORCID
Cameron, R. Andrew0000-0003-3947-6041
Additional Information:© 2006 Elsevier Inc. Received for publication 30 May 2006; revised 20 July 2006; accepted 27 July 2006. Available online 4 August 2006. We thank Michael Thorndyke (Kristineberg Marine Station, Sweden) and Jordi Garcia-Fernández (Universitat de Barcelona, Spain) for their very helpful comments on the manuscript. We would also like to thank Marco Borra and Elvira Mauriello of the SZN Molecular Biology Service for their assistance with QPCR and sequencing. We are very grateful to the European Network of Excellence “Marine Genomics Europe” (GOCE-04-505403) for supporting the organization of the S. purpuratus Annotation Workshop, held at the Stazione Zoologica di Napoli, Italy, in January 2006. National Science Foundation Grant IBN9604454 and the Beckman Institute, California Institute of Technology supported the work on this project contributed by R. A. Cameron. NASA-Ames, NSF, and the Dartmouth College support K. J. Peterson.
Funders:
Funding AgencyGrant Number
European Network of ExcellenceGOCE-04-505403
NSFIBN9604454
Caltech Beckman InstituteUNSPECIFIED
NASAUNSPECIFIED
Dartmouth CollegeUNSPECIFIED
Subject Keywords:Hox; ParaHox; Colinearity; Gsx; lox; Cdx; Cluster; S. purpuratus; Evolution
Issue or Number:1
Record Number:CaltechAUTHORS:20121031-073253328
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20121031-073253328
Official Citation:Maria I. Arnone, Francesca Rizzo, Rosella Annunciata, R. Andrew Cameron, Kevin J. Peterson, Pedro Martínez, Genetic organization and embryonic expression of the ParaHox genes in the sea urchin S. purpuratus: Insights into the relationship between clustering and colinearity, Developmental Biology, Volume 300, Issue 1, 1 December 2006, Pages 63-73, ISSN 0012-1606, 10.1016/j.ydbio.2006.07.037. (http://www.sciencedirect.com/science/article/pii/S0012160606010670)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:35192
Collection:CaltechAUTHORS
Deposited By: Ruth Sustaita
Deposited On:31 Oct 2012 14:50
Last Modified:03 Oct 2019 04:26

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