Abstract
Hox genes define regional identities along the anterior–posterior axis in many animals. In a number of species, Hox genes are clustered in the genome, and the relative order of genes corresponds with position of expression in the body. Previous Hox gene studies in lophotrochozoans have reported expression for only a subset of the Hox gene complement and/or lack detailed genomic organization information, limiting interpretations of spatial and temporal colinearity in this diverse animal clade. We studied expression and genomic organization of the single Hox gene complement in the segmented polychaete annelid Capitella sp. I. Total genome searches identified 11 Hox genes in Capitella, representing 11 distinct paralog groups thought to represent the ancestral lophotrochozoan complement. At least 8 of the 11 Capitella Hox genes are genomically linked in a single cluster, have the same transcriptional orientation, and lack interspersed non-Hox genes. Studying their expression by situ hybridization, we find that the 11 Capitella Hox genes generally exhibit spatial and temporal colinearity. With the exception of CapI-Post1, Capitella Hox genes are all expressed in broad ectodermal domains during larval development, consistent with providing positional information along the anterior–posterior axis. The anterior genes CapI-lab, CapI-pb, and CapI-Hox3 initiate expression prior to the appearance of segments, while more posterior genes appear at or soon after segments appear. Many of the Capitella Hox genes have either an anterior or posterior expression boundary coinciding with the thoracic–abdomen transition, a major body tagma boundary. Following metamorphosis, several expression patterns change, including appearance of distinct posterior boundaries and restriction to the central nervous system. Capitella Hox genes have maintained a clustered organization, are expressed in the canonical anterior–posterior order found in other metazoans, and exhibit spatial and temporal colinearity, reflecting Hox gene characteristics that likely existed in the protostome–deuterostome ancestor.
Highlights
Hox genes have represented one of the major paradigms of developmental biology for nearly three decades
Among the most fascinating characteristics of these genes are that Hox genes are organized into clusters in the genome in some animals, and there is a precise relationship between the order of genes in the cluster and the relative postions of expression domains along the anterior– posterior axis of the body, a phenomenon called spatial colinearity
These models have been largely based on studies limited to deuterostomes and ecdysozoans, limiting the inferences that can be made about Hox genes in the protostome/deuterostome ancestor
Summary
Hox genes have represented one of the major paradigms of developmental biology for nearly three decades (reviewed in [1,2]) These homeodomain genes encode transcription factors that, via regulation of various downstream genes, are capable of imprinting positional identities on to distinct body domains along the anterior-posterior axis of the animal. The species-specific repertoire, genomic organization, presence or absence of clusters and, in the case of vertebrates, numbers of clusters, and their deployment have formed the basis of models of animal body plan evolution and diversification [5,6] These models have been largely based on studies limited to deuterostomes and ecdysozoans, limiting the inferences that can be made about Hox genes in the protostome/deuterostome ancestor. There is significant variation in genomic organization of Hox genes even within deuterostomes
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