Elsevier

Gene

Volume 317, 23 October 2003, Pages 165-185
Gene

A genome-wide survey of the genes for planar polarity signaling or convergent extension-related genes in Ciona intestinalis and phylogenetic comparisons of evolutionary conserved signaling components

https://doi.org/10.1016/S0378-1119(03)00700-5Get rights and content

Abstract

Non-canonical Wnt signals similar to planar cell polarity (PCP) signaling in the fly control convergent extension (CE) of the dorsal mesoderm during gastrulation in vertebrates. Using the Ciona complete genome sequence and EST sequence data, we present here an initial and exhaustive search in non-vertebrate chordates, Ciona intestinalis for the family members as well as homologs or orthologs that are involved in PCP/CE signaling cascades. We clarified 7 cardinal gene families, including the MAPK, STE20 group kinase, Rho small GTPase, STAT, Glypican, Fz and Wnt gene families, as well as gene homologs or orthologs for known PCP/CE signaling components with their phylogenetic nature. As a result, we characterized 62 Ciona component genes. Among them, 59 genes were novel and functional genes which were supported by EST expressions and 15 genes belonged to PCP/CE component orthologs of other organisms or common ancestor genes. Moreover, from the phylogenetic point of view, we compared these components genome-widely with the PCP signaling components of fly and the CE signaling components of vertebrates. We then discovered not only that ascidians contain the basic ancestral signaling pathway components in chordates but also that several signaling components have not found in ascidian, indicating that ascidian CE pathway might have several gaps from vertebrate CE pathway. The present study provides an initial step for the subsequent analysis of CE in the non-vertebrate chordates, ascidians. In addition, this phylogenetic approach will help to facilitate understanding of the relationship between fly PCP signaling and the vertebrate CE pathway.

Introduction

Recent reports have shown that homologs of genes controlling polarized cell shape changes in flies also control the polarized cell motility underlying the morphogenetic movements that shape the vertebrate body plan Keller, 2002, Wallingford et al., 2002. These movements are known as “convergence and extension” or “convergent extension” (CE). CE by cell intercalation is a common, if not universal, mechanism of shaping the large features of metazoan embryos. It occurs during gastrulation and axis elongation of ascidians, teleost fish, birds, and mammals, and during Drosophila germ band extension and echinoderm gut elongation Keller, 2002, Wallingford et al., 2002.

The notochord is one of the characteristic features of the phylum Chordata. It is of particular interest to study the notochord when considering chordate evolution. We have focused on the evolution and development of the ascidian notochord. Previously, we isolated 20 Ciona intestinalis notochord-specific genes in the tailbud-stage embryo Hotta et al., 1999, Hotta et al., 2000, Takahashi et al., 1999. One of these genes, prickle (pk), is known as a gene which is expressed in cells undergoing CE Wallingford et al., 2002, Takeuchi et al., 2003. In addition, it has been reported that a few homologs of genes related to Planar Cell Polarity (PCP) signaling in Drosophila or CE in vertebrates serve a similar function in the ascidian notochord intercalation. For example, the ascidian Wnt5 homolog is expressed in the notochord and involved in the morphogenetic movement of notochord cells (Sasakura and Makabe, 2001). It was also shown that the expression of mutant Dishevelled (Dsh) in the ascidian notochord severely disrupted notochord cell intercalation without disrupting notochord cell fate (Keys et al., 2002). These data imply that signaling similar to the PCP/CE pathway plays an important role in the notochord of the non-vertebrate chordates, ascidians. There has been special interest in the study of the relationship between notochord development and CE, especially in ascidians.

To study the CE pathway in ascidians, an appropriate approach is to investigate orthologs of the known PCP/CE components in flies or vertebrates. In addition, since the numbers of components related to both pathways are growing and continuously being updated, we need to clarify not only the Ciona PCP/CE-related gene orthologs but also the families to which these genes belong. In this study, we focused on the principal participants of the components and downstream effectors in the known PCP/CE signal transduction pathway in flies or vertebrates, or both animals (Table 1). We selected PCP/CE-related genes (Table 1) according to Mlodzik (2002), Keller (2002) and Wallingford et al. (2002). A more detailed relationship of each gene to the PCP/CE pathway will be shown in each section later. Table 1 is constantly growing and is likely to include more components in the near future.

From the complete C. intestinalis whole-genome shotgun sequence (Dehal et al., 2002), EST sequences and assembled EST sequence data (Satou et al., 2002a), we present here an initial, exhaustive search in C. intestinalis for the family members as well as homologs or orthologs that are involved in PCP/CE signaling cascades. We then clarified and characterized the unique and simple features of ascidian signaling molecules in selected pathways. The present study should help the subsequent analysis of CE in ascidians. In addition, we made a comparison between the two mechanisms, fly PCP and vertebrate CE, from the phylogenetic point of view.

Section snippets

Ciona genome project

Department of Energy Joint Genome Institute (Walnut Creek, CA, USA) (http://genome.jgi-psf.org/ciona4/ciona4.home.html). On this website, we could access the genomic sequence data for C. intestinalis obtained by whole-genome shotgun sequencing, which has been annotated and integrated with the comparative data of homology, cDNA, EST and genome sequences of other organisms. Ciona gene products predicted from the Ciona genome sequence were attached to a gene product ID (e.g., ci01001512,

Frizzled (Fz/Smo family, CRD-containing proteins)

The seven-path transmembrane receptor Frizzled (Fz) is a key primary component of PCP signaling, and Fz receptors have also been reported in vertebrate CE. Five, three and twelve members of the frizzled family are known in Drosophila, C. elegans and humans, respectively. In ascidians, Ciona savignyi Cs-frizzled3 (AB057741.1) and C. intestinalis Cifrz (AB031542) have been found. Structurally, each Fz protein is composed of an extracellular cysteine-rich domain (CR), a seven transmembrane region,

Acknowledgements

We thank the members of the Center for Information Biology, National Institute of Genetics, in particular J.S. Hwang, and the members of the Division of Morphogenesis, Department of Developmental Biology, National Institute for Basic Biology, in particular S. Yamada, for their support in this work.

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