Evolution of the Hox gene fushi tarazu in arthropods

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2012

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Abstract

Homeotic (Hox) genes are important in determining regional identity in virtually all metazoans,and are conserved throughout the animal kingdom. In Drosophila melanogaster, fushi tarazu (ftz) is located within the Hox complex and contains a Hox-like DNA-binding homeodomain, but functions as a pair-rule segmentation gene. At some point(s) during evolution, ftz has undergone three specific changes thought to contribute to its new segmentation function in Drosophila: 1) The gain of an LXXLL motif allowed for interaction with a new co-factor, Ftz-F1; 2) The degeneration of the YPWM motif decreased the ability to interact with the homeotic co-factor Exd; 3) ftz expression switched from Hox-like to seven stripes in Drosophila. Here I isolated ftz sequences and examined expression from arthropods spanning 550 million years of evolutionary time to track these changes in ftz. I found that while the LXXLL motif required for segmentation was stably acquired at the base of the holometabolous insects, the YPWM motif degenerated independently many times in arthropod lineages, and these `degen-YPWMs' vary in their homeotic potential. Additionally, ftz expression in a crustacean is in a weak Hox-like pattern, suggesting a model in which different ftz variants could arise in nature and not be detrimental to organismal development. Given my findings that ftz sequence and expression is so dynamic, I investigated the features that may be preventing ftz fossilization in arthropod genomes. I tested the hypothesis that a broadly conserved role of ftz in the developing central nervous system (CNS) retains ftz in arthropod genomes. This model predicts that the homeodomain, but not variable co-factor interaction motifs, is required for Ftz CNS function. Evidence supporting this model was obtained from CNS-specific rescue experiments in Drosophila. Additionally I examined the expression and function of ftz and ftz-f1 in the short-germ beetle Tribolium castaneum. I found that both genes are expressed in pair-rule patterns, and preliminary results suggest that ftz-f1 is important for proper segmentation and cuticle deposition, and ftz function may be partially redundant with ftz-f1. Taken together, these findings show that variation of a pleiotropic transcription factor is more extensive than previously imagined, and suggest that evolutionary plasticity may be widespread among regulatory genes.

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