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

Comparative Analysis of Hox Gene Expression in the Polychaete Chaetopterus: Implications for the Evolution of Body Plan Regionalization'

SYNOPSIS. The Hox genes are widely regarded as candidates for involvement in major evolutionary changes in body plan organization. We examine Hox gene expression data for several taxa, in relation to recent work on the polychaete annelid Chaetopterus. The work in Chaetopterus shows the basic conservation of colinearity of anterior expression boundaries seen in other groups. It also reveals novel patterns including early expression in the larval growth zone and later formation of posterior boundaries that correlate with morphological transitions in the polychaete body plan. The polychaete gene expression pattern is compared with those of Hox gene homologs in other taxa to reveal differences that represent evolutionary changes in Hox gene regulation between lineages. Correlations between Hox gene expression differences and morphological differences are examined, focussing on a number of cases in which posterior Hox gene expression boundaries correlate with morphological transitions. Differential regulation of these posterior expression boundaries is proposed as a possible mechanism for changes body plan regionalization.

INTRODUCTION

Hox genes in body plan evolution: the paradigm

Mutational studies in flies and mice have clearly shown that Hox genes play an important role in the development of discrete regions of the adult body plan (Carroll, 1995). If Hox genes are involved in the evolution of animal body plans, one must argue that the spatial and temporal regulation of these genes must play a role in body plan regionalization because Hox genes do not code directly for any unique morphological structures (Carroll, 1995; Gellon and McGinnis, 1998). One way to look for the significance of these changes in body plan evolution is to compare patterns in various taxa with different morphologies to determine the extent of variation and how it might relate to these differences.

In a very simplified view (to be elaborated below), metazoans are armed with a complement of Hox genes clustered together in a contiguous region of their genomes. The spatial and temporal expression of these genes is regulated by the position of the genes from 3' to 5' along the chromosome, a feature termed colinearity.

For example, in vertebrates the temporal onset of expression of Hox genes is largely colinear with chromosomal location, i.e., 3' genes are expressed earlier than more 5' genes (De Robertis, 1994). There also appears to be a biphasic temporal pattern of expression in which the morphogenetic function of Hox genes changes during development. Early expression has been characterized as imparting positional information to cells which "remember" the initial Hox code (Gonzalez-Reyes and Morata, 1990). Expression during later stages of development involves the fine tuning of Hox gene expression within and between segments to transduce complex morphogenetic information and specify unique cell fates (Akam, 1998b).

The hallmark of Hox gene expression is their coordinated nested spatial patterns. Individual Hox genes are generally expressed from an anterior boundary along the body axis caudally-with or without a defined posterior boundary. The anterior boundaries of consecutive genes in the cluster are arranged in rank order from anterior to posterior in the same register as their 3' to 5' positions along the chromosome.

The paradigmatic view of Hox gene expression is that the most significant feature of the expression pattern is the anterior boundary. Ectopic expression of Hox genes in segments anterior to their normal domain generally results in posteriorization of the affected segment, i.e., the more anterior segment acquires the "Hox code" of the ectopically expressed gene. Similarly if a Hox gene anterior boundary is shifted caudally, the segment losing that gene product takes on the more anterior identity. This general principle is called "posterior dominance" (reviewed in Manak and Scott [1994]).

In the case of posterior boundaries, shifting the expression domain may or may not affect segmental identity. Gene overexpression studies in flies and mice indicate that in some cases posterior boundaries of expression do have functional significance. Ubiquitous expression of a heat-shock-Dfd transgene causes a partial transformation of the more posterior labial and thoracic segments towards a maxillary identity (Kuziora and McGinnis, 1988) and ectopic expression of Scr results in the cuticle in the second and third thoracic segments being converted to the form of the first thoracic segment (Andrew et al., 1994; Pederson et al., 1996). In the mouse, overexpression of Hoxc-6 results in one or more supernumerary ribs in the lumbar region, caudal to the normal posterior expression boundary of this gene (Jegalian and DeRobertis, 1992). Similarly, overexpression of Hoxb-8 and Hoxc-8 posterior to their normal domains result in 'atavistic' changes in posterior vertebral morphology (Pollock et al., 1995). These experiments indicate that in certain cases of genes with defined posterior boundaries of expression, dominance by more posteriorly expressed genes does not hold and therefore changes in posterior expression boundaries could be a mechanism of morphological change.