Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica

Tunicate embryos and larvae have small cell numbers and simple anatomical features in comparison with other chordates, including vertebrates. Although they branch near the base of chordate phylogenetic trees, their degree of divergence from the common chordate ancestor remains difficult to evaluate. Here we show that the tunicate Oikopleura dioica has a complement of nine Hox genes in which all central genes are lacking but a full vertebrate-like set of posterior genes is present. In contrast to all bilaterians studied so far, Hox genes are not clustered in the Oikopleura genome. Their expression occurs mostly in the tail, with some tissue preference, and a strong partition of expression domains in the nerve cord, in the notochord and in the muscle. In each tissue of the tail, the anteroposterior order of Hox gene expression evokes spatial collinearity, with several alterations. We propose a relationship between the Hox cluster breakdown, the separation of Hox expression domains, and a transition to a determinative mode of development.

[1]  J. Postlethwait,et al.  Brachyury (T) expression in embryos of a larvacean urochordate, Oikopleura dioica, and the ancestral role of T. , 2000, Developmental biology.

[2]  P. Holland,et al.  The amphioxus Hox cluster: deuterostome posterior flexibility and Hox14 , 2000, Evolution & development.

[3]  M. Akam,et al.  Hox genes and the diversification of insect and crustacean body plans , 1995, Nature.

[4]  M. P. Cummings,et al.  PAUP* Phylogenetic analysis using parsimony (*and other methods) Version 4 , 2000 .

[5]  Paul Richardson,et al.  The Draft Genome of Ciona intestinalis: Insights into Chordate and Vertebrate Origins , 2002, Science.

[6]  T R Bürglin,et al.  The Caenorhabditis elegans homeobox gene cluster. , 1993, Current opinion in genetics & development.

[7]  E. Lewis,et al.  Splits in fruitfly Hox gene complexes , 1996, Nature.

[8]  P. Holland,et al.  Ciona intestinalis ParaHox genes: evolution of Hox/ParaHox cluster integrity, developmental mode, and temporal colinearity. , 2002, Molecular phylogenetics and evolution.

[9]  C. Kenyon,et al.  Correct Hox gene expression established independently of position in Caenorhabditis elegans , 1996, Nature.

[10]  C. Amemiya,et al.  Evidence for a Hox14 paralog group in vertebrates , 2004, Current Biology.

[11]  R. Krumlauf,et al.  Patterning the ascidian nervous system: structure, expression and transgenic analysis of the CiHox3 gene. , 1999, Development.

[12]  S. Fujiwara,et al.  Expression of Raldh2, Cyp26 and Hox-1 in normal and retinoic acid-treated Ciona intestinalis embryos. , 2003, Gene expression patterns : GEP.

[13]  J. Mappes,et al.  Tracking the evolution of warning signals , 1996, Nature.

[14]  D. Duboule,et al.  Gene Transpositions in the HoxD Complex Reveal a Hierarchy of Regulatory Controls , 1996, Cell.

[15]  D. Duboule,et al.  Organizing Axes in Time and Space; 25 Years of Colinear Tinkering , 2003, Science.

[16]  G. A. Miller.  THE PSYCHOLOGICAL REVIEW THE MAGICAL NUMBER SEVEN, PLUS OR MINUS TWO: SOME LIMITS ON OUR CAPACITY FOR PROCESSING INFORMATION 1 , 1956 .

[17]  Martin Vingron,et al.  TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing , 2002, Bioinform..

[18]  R. Dukas,et al.  Behavioural and ecological consequences of limited attention. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[19]  G. Balavoine,et al.  Hox clusters and bilaterian phylogeny. , 2002, Molecular phylogenetics and evolution.

[20]  Roderick S. Bain,et al.  The evolution of aggregation in profitable and unprofitable prey , 2005, Animal Behaviour.

[21]  J. Finnerty,et al.  The origins of axial patterning in the metazoa: how old is bilateral symmetry? , 2003, The International journal of developmental biology.

[22]  D. Swofford.  PAUP*: Phylogenetic analysis using parsimony (*and other methods), Version 4.0b10 , 2002 .

[23]  John A. Allen,et al.  Protective polymorphism in populations of computer-simulated moth-like prey , 1997 .

[24]  T. Lacalli.  Tunicate tails, stolons, and the origin of the vertebrate trunk , 1999, Biological reviews of the Cambridge Philosophical Society.

[25]  M. Blaxter,et al.  Hox Gene Loss during Dynamic Evolution of the Nematode Cluster , 2003, Current Biology.

[26]  H. Lehrach,et al.  Miniature genome in the marine chordate Oikopleura dioica. , 2001, Science.

[27]  R. di Lauro,et al.  Cihox5, a new Ciona intestinalisHox-related gene, is involved in regionalization of the spinal cord , 1998, Development Genes and Evolution.

[28]  M. Mann,et al.  Molecular Patterning of the Oikoplastic Epithelium of the Larvacean Tunicate Oikopleura dioica * , 2001, The Journal of Biological Chemistry.

[29]  Yuri Y. Shevelyov,et al.  Large clusters of co-expressed genes in the Drosophila genome , 2002, Nature.

[30]  V. Storch,et al.  Zur feinstruktur der Chorda dorsalis niederer Chordaten [Dendrodoa grossularia (v. Beneden) und Oikopleura dioica Fol] , 1968, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[31]  T. Sherratt,et al.  The Evolution of Warning Signals as Reliable Indicators of Prey Defense , 2003, The American Naturalist.

[32]  M. Akam.  Hox and HOM: Homologous gene clusters in insects and vertebrates , 1989, Cell.

[33]  A. Spagnuolo,et al.  Unusual number and genomic organization of Hox genes in the tunicate Ciona intestinalis. , 2003, Gene.

[34]  Joshua M. Stuart,et al.  Chromosomal clustering of muscle-expressed genes in Caenorhabditis elegans , 2002, Nature.

[35]  H. Wada.  Evolutionary history of free-swimming and sessile lifestyles in urochordates as deduced from 18S rDNA molecular phylogeny. , 1998, Molecular biology and evolution.

[36]  F. Götmark,et al.  Bright Male Plumage and Predation Risk in Passerine Birds: Are Males Easier to Detect Than Females? , 1995 .