Shaping animal body plans in development and evolution by modulation of Hox expression patterns

Abstract

Most animals exhibit distinctive and diverse morphological features on their anterior‐posterior body axis. However, underneath the variation in design and developmental strategies lies a shared ancient structural blueprint that is based on the expression patterns of Hox genes. Both the establishment and maintenance of the spatial and temporal distribution of Hox transcripts play an important role in determining axial pattern. The study of many animal systems, both vertebrate and invertebrate, suggests that the mechanisms used to establish Hox transcription are nearly as diverse as the body plans they specify. The strategies for maintenance of Hox expression pattern seem more conserved among different phyla, and rely on the action of Pc and trx group genes as well as auto‐ and cross‐regulation among Hox genes. In mice, the sharing of regulatory elements coupled with auto‐ and cross‐regulation could explain the conservation of the clustered arrangement of Hox genes. In contrast, fly Hox genes seem to have evolved insulators or boundary elements to avoid sharing regulatory regions. Differences in Hox transcription patterns can be correlated with morphological modifications in different species, and it seems likely that evolutionary variation of Hox cis‐regulatory elements has played a major role in the emergence of novel body plans in different taxa of the animal kingdom. BioEssays 20:116–125, 1998.© 1998 John Wiley & Sons, Inc.

Cell fate specification along the anterior–posterior axis of the intermediate mesoderm

“…The anterior expression border of Hox genes is probably the most discussed phenomenon along the A-P axis, yet little is known regarding the complex cellular and molecular regulatory mechanisms of these anterior borders (Gellon and McGinnis, 1998;Burke and Nowicki, 2001). Burke (2000) distinguishes between two types of "positional information" (as termed by Wolpert, 1969).…”

Evolution of Double Positive Autoregulatory Feedback Loops in CYCLOIDEA2 Clade Genes Is Associated with the Origin of Floral Zygomorphy

“…It is suggested that the establishment and maintenance of Hox gene asymmetric expression, relying on auto-and crossregulation, might have been associated with the evolutionary switch from the primary oral-aboral axis to the elaborated anterior-posterior axis of Metazoans and subsequent rapid diversification of the bilaterian lineages, thus implicated in the Cambrian explosion ;520 million years ago (Gellon and McGinnis, 1998;Knoll and Carroll, 1999;Valentine et al, 1999;Pearson et al, 2005). The double positive autoregulatory feedback loop as a novel mechanism maintaining and strengthening CYC2 gene expression in later developmental stages, co-opted with the regulation for their dorsal-specific location evolved previously or subsequently, might have driven the shift of floral symmetry from actinomorphy to zygomorphy.…”

Hox, ParaHox, ProtoHox: facts and guesses

“…1978), the Hox gene cluster has fascinated evolutionary and developmental biologists alike. Hox genes belong to a class of homeobox genes, a major class of transcription factors regulating many aspects of development (Gellon and McGinnis, 1998). The discovery of the homeobox in 1984 (McGinnis et al, 1984) and the finding that similar genes act in similar ways in animals as diverse as flies and mice facilitated the reconciliation of developmental and evolutionary biologists.…”

“…The conservation of Hox genes galvanized the Evo-Devo community and served to define the concept of the metazoan 'zootype', a conserved set of genes patterning the antero-posterior body axis (Slack et al, 1993). Soon after that, changes in Hox gene numbers, sequence, and regulation were invoked for body plan evolution and diversification (eg Gellon and McGinnis, 1998;Wagner et al, 2003;Amores et al, 2004).…”