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Evolutionary history of x-tox genes in three lepidopteran species: Origin, evolution of primary and secondary structure and alternative splicing, generating a repertoire of immune-related proteins
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The proteins of the X-tox family have imperfectly conserved tandem repeats of several defensin-like motifs known as cysteine-stabilized alpha beta (CS-alpha beta) motifs. These immune-related proteins are inducible and expressed principally in hemocytes, but they have lost the antimicrobial properties of the ancestral defensins from which they evolved. We compared x-tox gene structure and expression in three lepidopteran species (Spodoptera frugiperda, Helicoverpa armigera and Bombyx mori). Synteny and phylogenetic analyses showed that the x-tox exons encoding CS-alpha beta motifs were phylogenetically closely related to defensin genes mapping to chromosomal positions close to the x-tox genes. We were able to define two groups of paralogous x-tox exons (three in Noctuids) that each followed the expected species tree. These results suggest that the ancestor of the three species already possessed an x-tox gene with at least two proto-domains, and an additional duplication/fusion should have occurred in the ancestor of the two noctuid species. An expansion of the number of exons subsequently occurred in each lineage. Alternatively, the proto x-tox gene possessed more copy and each group of x-tox domains might undergo concerted evolution through gene conversion. Accelerated protein evolution was detected in x-tox domains when compared to related defensins, concomitantly to multiplication of exons and/or the possible activation of concerted evolution. The x-tox genes of the three species have similar structural organizations, with repeat motifs composed of CS-alpha beta-encoding exons flanked by introns in phase 1. Diverse mechanisms underlie this organization: (i) the acquisition of new repeat motifs, (ii) the duplication of preexisting repeat motifs and (iii) the duplication of modules. A comparison of gDNA and cDNA structures showed that alternative splicing results in the production of multiple X-tox protein isoforms from the x-fox genes. Differences in the number and sequence of CS-alpha beta motifs in these isoforms were found between species, but also between individuals of the same species. Thus, our analysis of the genetic organization and expression of x-tox genes in three lepidopteran species suggests a rapid evolution of the organization of these genes. (C) 2012 Elsevier Ltd. All rights reserved.
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