Abstract
BackgroundHox genes play a central role in axial patterning during animal development. They are clustered in the genome and specify cell fate in sequential domains along the anteroposterior (A-P) body axis in a conserved order that is co-linear with their relative genomic position. In the soil worm Caenorhabditis elegans, this striking rule of co-linearity is broken by the anterior Hox gene ceh-13, which is located between the two middle Hox paralogs, lin-39 and mab-5, within the loosely organized nematode Hox cluster. Despite its evolutionary and developmental significance, the functional consequence of this unusual genomic organization remains unresolved.ResultsIn this study we have investigated the role of ceh-13 in different developmental processes, and found that its expression and function are not restricted to the anterior body part. We show that ceh-13 affects cell migration and fusion as well as tissue patterning in the middle and posterior body regions too. These data reveal novel roles for ceh-13 in developmental processes known to be under the control of middle Hox paralogs. Consistently, enhanced activity of lin-39 and mab-5 can suppress developmental arrest and morphologic malformation in ceh-13 deficient animals.ConclusionOur findings presented here show that, unlike other Hox genes in C. elegans which display region-specific accumulation and function along the A-P axis, the expression and functional domain of the anterior Hox paralog ceh-13 extends beyond the anterior region of the worm. Furthermore, ceh-13 and the middle Hox paralogs share several developmental functions. Together, these results suggest the emergence of the middle-group Hox genes from a ceh-13-like primordial Hox ancestor.
Highlights
Hox genes play a central role in axial patterning during animal development
These findings suggest that in the nematode lineage the middle Hox genes emerged from a primordial ceh-13-like Hox paralog, and that the ancestor of this anterior Hox paralog might have given raise the primitive Hox cluster through tandem gene duplications during an early phase of animal evolution
The migration of Q neuroblasts is influenced by ceh-20 and unc-62, Figure 2 ceh-13 deficiency causes defects in cell migration
Summary
Hox genes play a central role in axial patterning during animal development. They are clustered in the genome and specify cell fate in sequential domains along the anteroposterior (A-P) body axis in a conserved order that is co-linear with their relative genomic position. Embryonic patterning and viability in C. elegans require only the anterior and the two most posterior Hox genes; triple loss-of-function (lf) mutant worms defective for lin-39, mab-5 and egl-5 can develop into fertile adults [3,15], raising interesting questions about the evolutionary status of these dispensable Hox genes They control various developmental processes, including the migration of Q neuroblasts, cell fusion in Pn.p cell lineages, cell fate specification during vulval patterning, and programmed cell death [11,12,16,17,18]. The functional consequence of this unusual genomic organization and the role of ceh-13 in development remain largely unknown
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