title: 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.
abstract: The proteins of the X-tox family have imperfectly conserved tandem repeats of several defensin-like motifs known as cysteine-stabilized αβ (CS-αβ) 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-αβ 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-αβ-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-tox genes. Differences in the number and sequence of CS-αβ 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.
authors.affiliation: INRA, UMR 1333 Laboratoire Diversité, Génomes & Interactions Microorganismes - Insectes (DGIMI), CC54, 2 place E. Bataillon, 34095 Montpellier, France.
authors.forename: Emmanuelle
authors.initials: E
authors.lastname: d'Alençon
authors.forename: Nicolas
authors.initials: N
authors.lastname: Bierne
authors.forename: Pierre-Alain
authors.initials: PA
authors.lastname: Girard
authors.forename: Ghislaine
authors.initials: G
authors.lastname: Magdelenat
authors.forename: Sylvie
authors.initials: S
authors.lastname: Gimenez
authors.forename: Imène
authors.initials: I
authors.lastname: Seninet
authors.forename: Jean-Michel
authors.initials: JM
authors.lastname: Escoubas
mesh_terms: D017398:Alternative Splicing; D000818:Animals; D001483:Base Sequence; D012831:Bombyx / Q000235:genetics* / Q000276:immunology; D023082:Defensins / Q000235:genetics; D019143:Evolution, Molecular; D040461:Gene Components; D015870:Gene Expression; D049750:Genome, Insect; D019476:Insect Proteins / Q000235:genetics*; D008969:Molecular Sequence Data; D009690:Nucleic Acid Conformation; D010802:Phylogeny; D020033:Protein Isoforms; D018411:Spodoptera / Q000235:genetics* / Q000276:immunology; D026801:Synteny
chemical_list: D023082:Defensins; D019476:Insect Proteins; D020033:Protein Isoforms