The genome of the sea urchin Strongylocentrotus purpuratus

Abstract

We report the sequence and analysis of the 814-megabase genome of the sea urchin Strongylocentrotus purpuratus, a model for developmental and systems biology. The sequencing strategy combined whole-genome shotgun and bacterial artificial chromosome (BAC) sequences. This use of BAC clones, aided by a pooling strategy, overcame difficulties associated with high heterozygosity of the genome. The genome encodes about 23,300 genes, including many previously thought to be vertebrate innovations or known only outside the deuterostomes. This echinoderm genome provides an evolutionary outgroup for the chordates and yields insights into the evolution of deuterostomes.

Fig. 1

The phylogenetic position of the sea urchin relative to other model systems and humans. The chordates are shown on the darker blue background overlapping the deuterostomes as a whole on a lighter blue background. Organisms for which genome projects have been initiated or finished are shown across the top.

Fig. 2

Orthologs among the Bilateria. The number of 1:1 orthologs captured by BLAST alignments at a match value of e = 1 × 10⁻⁶ in comparisons of sequenced genomes among the Bilateria. The number of orthologs is indicated in the boxes along the arrows, and the total number of International Protein Index database sequences is shown under the species symbol. Hs, Homo sapiens; Mm, Mus musculus; Ci, Ciona intestinalis; Sp, S. purpuratus; Dm, Drosophila melanogaster; Ce, Caenorhabditis elegans.

Fig. 3

Protein kinase evolution: Invention and loss of protein kinase subfamilies in metazoan lineages. Deuterostomes share 9 protein kinase subfamilies absent from C. elegans and Drosophila, and the sea urchin has not lost any of the 158 metazoan primordial kinase classes, unlike insects or nematodes. [From (23)]

Fig. 4

Partial phylogenies of the Rho (A) and the Rab families (B)ofsmallGTPases. The pink boxes highlight gene-specific duplications that increased sea urchin GTPase numbers, resulting in a complexity comparable to vertebrates. Numbers at each junction represent confidence values obtained via three independent phylogenetic methods [neighbor-joining (green), maximum parsimony (blue), and Bayesian (black)]; red stars indicate nodes retained by maximum likelihood. [From (28)]

Fig. 5

Survey of the Wnt family of secreted signaling molecules in selected metazoans. Each square indicates a single Wnt gene identified either through genome analyses or independent studies, and squares with a question mark indicate uncertainty of the orthology. Letter X’s represent absence of members of that subfamily in the corresponding annotated genome; empty spaces have been left for species for which genomic databases are not yet available. [From (30)]

Fig. 6

Presence of Wnt signaling machinery components (A) and target genes (B) in the S. purpuratus genome. (A) The 126 genes involved in the transduction of the Wnt signals have been separated into four categories from the extracellular compartment to the nucleus. Sea urchin homologs are identified by the lighter shade (indicated by both the number and the percentage of homologs that were identified within the chart); the total number of known genes is indicated in the chart legend. (B) The 93 reported Wnt targets have been divided into three categories: signaling molecules, transcription factors, and cell adhesion molecules. Colors and numbers are as in (A).

Fig. 7

Gene families encoding important innate immune receptors and complement factors in animals with sequenced genomes. For some key receptor classes, gene numbers in the sea urchin exceeds other animals by more than an order of magnitude. Representative animals include H.s., Homo sapiens; C.i., Ciona intestinalis; S.p. Strongylocentrotus purpuratus; D.m. Drosophila melanogaster; and C.e. Caenorhabditis elegans. Indicated gene families include TLR, toll-like receptors; NLR, NACHT and leucine-rich repeat (LRR) domain–containing proteins similar to the vertebrate Nod/NALP genes; SRCR, Scavenger receptor cysteine-rich domain genes; PGRP, peptidoglycan recognition protein domain genes; and GNBP, Gram-negative binding proteins. C3/4/5, thioester proteins homologous to vertebrate C3, C4, and C5; Bf/C2, complement factors homologous to vertebrate C2 and factor B; C1q/MBP, homologs of vertebrate lectin pathway receptors; and Terminal pathway, homologs of vertebrate C6, C7, C8, and C9. SRCR gene statistics are given as domain number/gene number for multiple SRCR-containing proteins (numbers for C. intestinalis includes all SRCR proteins). Asterisk in the D. melanogaster C3/4/5 column is meant to denote the presence of related thioester genes (TEPs) and a true C3/4/5 homolog from another arthropod. +/− for C. intestinalis Terminal pathway column indicates the presence of genes with similarity to C6 only (Nonaka and Yoshizaki 2004). Phylogenetic relations among species are indicated by a cladogram at the left.