Comparative analysis of hox gene expression in the polychaete Chaetopterus: Implications for the evolution of body plan regionalization

American Zoologist, Jun 2001 by Irvine, Steven Q, Martindale, Mark Q

Three major findings emerged from these gene expression studies. First, we discovered an unexpected and apparently novel pattern of very early expression of all five of the Hox genes examined in the putative growth zone of the larva, as compared with other taxa with teloblastic growth. This expression appears well before any segmentation occurs and obeys the paradigm of temporal colinearity. Second, we observed basic spatial colinearity of anterior expression boundaries like those seen in other taxa (with some important exceptions). Third, we found that some of the genes have posterior expression boundaries that relate to transitions in the tagmatized body plan of Chaetopterus.

Each of these findings will be discussed in relation to Hox expression data from other segmented protostomes, namely the leeches within the annelid group, and insects, crustaceans and chelicerates among the arthropods. We will pay special attention to the issue of whether changes in the domains of Hox gene expression between animal groups relate to differences in body plan morphology, and argue that posterior boundaries of expression may deserve special attention.

COMPARISON OF Hox GENE EXPRESSION PATrERNs

Chaetopterus Hox gene expression patterns

We have examined the expression patterns of five Chaetopterus Hox genes by whole-mount in situ hybridization (Irvine and Martindale, 2000) (Fig. 2A). By phylogenetic and sequence analysis these were determined to be orthologs of labial, proboscipedia, zen, Deformed, and sex combs reduced, and have been termed CH-Hox], CH-Hox2, CH-Hox3, CH-Hox4, and CHHox5 respectively, to reflect the orthologous vertebrate paralogy groups (1-5). A major finding was robust early expression at the posterior of the larva for each of the genes which begins well before overt segmentation has occurred, and continues throughout the entire course of larval life. As mentioned above, this posterior region has been described as a growth zone from which all the segmental tissues of the adult trunk are derived. The five genes show a clear temporal colinearity, with the exception of CH-Hox2, whose gene products are present prior to zygotic transcription (Peterson et al., 2000). This early phase of expression in proliferating segmental precursors may impart basic positional information which the expressing cell "remembers" during later morphogenesis (Akam, 1998a; Garcia-Bellido and Capdevila, 1978). It is notable that in other taxa with teloblastic growth, such as leeches, crustaceans, and (in a modified form) short germ band insects, this very early and persistent expression in the growth zone has not been reported (Abzhanov and Kaufman, 1999a; Averof and Akam, 1995; Kelsh et al., 1994; Kourakis et al., 1997; Nardelli-Haefliger and Shankland, 1992; Peterson et al., 1999; Tear et al., 1990; Wong et al., 1995), suggesting that the early Chaetopterus expression may be unique to polychaetes, or lost in other taxa sampled. Further study of the early Chaetopterus pattern is warranted to understand the involvement of Hox gene expression in the initiation of segment identity.