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Duplication, concerted evolution and purifying selection drive the evolution of mosquito vitellogenin genes.

ABSTRACT: Mosquito vitellogenin (Vtg) genes belong to a small multiple gene family that encodes the major yolk protein precursors required for egg production. Multiple Vtg genes have been cloned and characterized from several mosquito species, but their origin and molecular evolution are poorly understood.Here we used in silico and molecular cloning techniques to identify and characterize the evolution of the Vtg gene family from the genera Culex, Aedes/Ochlerotatus, and Anopheles. We identified the probable ancestral Vtg gene among different mosquito species by its conserved association with a novel gene approximately one kilobase upstream of the start codon. Phylogenetic analysis indicated that the Vtg gene family arose by duplication events, but that the pattern of duplication was different in each mosquito genera. Signatures of purifying selection were detected in Culex, Aedes and Anopheles. Gene conversion is a major driver of concerted evolution in Culex, while unequal crossover is likely the major driver of concerted evolution in Anopheles. In Aedes, smaller fragments have undergone gene conversion events.The study shows concerted evolution and purifying selection shaped the evolution of mosquito Vtg genes following gene duplication. Additionally, similar evolutionary patterns were observed in the Vtg genes from other invertebrate and vertebrate organisms, suggesting that duplication, concerted evolution and purifying selection may be the major evolutionary forces driving Vtg gene evolution across highly divergent taxa.

SUBMITTER: Chen S

PROVIDER: S-EPMC2875236 | biostudies-literature | 2010 May

REPOSITORIES: biostudies-literature

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Duplication, concerted evolution and purifying selection drive the evolution of mosquito vitellogenin genes.

Chen Song S Armistead Jennifer S JS Provost-Javier Katie N KN Sakamoto Joyce M JM Rasgon Jason L JL

BMC evolutionary biology 20100513

<h4>Background</h4>Mosquito vitellogenin (Vtg) genes belong to a small multiple gene family that encodes the major yolk protein precursors required for egg production. Multiple Vtg genes have been cloned and characterized from several mosquito species, but their origin and molecular evolution are poorly understood.<h4>Results</h4>Here we used in silico and molecular cloning techniques to identify and characterize the evolution of the Vtg gene family from the genera Culex, Aedes/Ochlerotatus, and ...[more]

PMID: 20465817

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Project description:Comparative sequence analysis of mosquito vitellogenin (Vg) genes was carried out to gain a better understanding of their evolution. The genomic clones of vitellogenin genes were isolated and sequenced from all three subfamilies of the family Culicidae including Culicinae (Aedes aegypti, Ochlerotatus atropalpus, Ae. polynesiensis, Ae. albopictus, Ochlerotatus triseriatus and Culex quinquefasciatus), Toxorhynchitinae (Toxorhynchites amboinensis), and Anophelinae (Anopheles albimanus). Genomic clones of vitellogenin genes Vg-B and Vg-C were isolated from Ae. aegypti and sequenced. A comparison of Vg-B and Vg-C, with the previously characterized vitellogenin gene, Vg-A1, suggests that Vg-A1 and Vg-B probably arose by a recent gene duplication, and Vg-C apparently diverged from the two other members of the gene family in an earlier gene duplication event. Two vitellogenin genes orthologous to Vg-C were cloned from a Cx. quinquefasciatus DNA library, one of which is truncated at the N-terminal end. Single vitellogenin genes, orthologous to Vg-C, were cloned from the An. albimanus and Tx. amboinensis libraries. Incomplete sequences orthologous to Vg-B and Vg-C were isolated from the Oc. atropalpus library. Only partial sequences were isolated from Ae. polynesiensis, Ae. albopictus and Oc. triseriatus. Inferred phylogenetic relationships based on analysis of these sequences suggest that Vg-C was the ancestral gene and that a recent gene duplication gave rise to Vg-A1 and Vg-B after the separation of the genus Aedes. The deduced amino acid composition of mosquito vitellogenin proteins exhibits higher tyrosine and phenylalanine composition than other mosquito proteins except for the hexamerin storage proteins. Analysis of vitellogenin coding sequences showed that a majority of amino acid substitutions were due to conserved and moderately conserved changes suggesting that the vitellogenins are under moderately selective constrains to maintain tertiary structure. The vitellogenin genes of the three anautogenous mosquitoes, that require a blood meal to develop eggs, had very high synonymous codon usage biases similar to highly expressed genes of other organisms. On the other hand, the vitellogenin genes of autogenous mosquitoes, that develop at least one batch of eggs without a blood meal, exhibited low synonymous codon usage bias. An unusual pattern of synonymous codon usage was observed in the first 15 amino acid residues encoding the signal peptide in the vitellogenin genes, where a high number of rarely used synonymous codons are present. It is hypothesized that rare synonymous codons have selectively accumulated in the signal peptide region to down-regulate the rate of translation initiation in the absence of a blood meal. Real-time PCR gene expression experiments showed that all three Ae. aegypti vitellogenin genes were highly expressed after a blood meal, and expressed in non-blood-fed females, males, larvae and pupae at trace levels. Sequences were deposited in GenBank (accession numbers: Ae. aegypti Vg-B, AY380797, Vg-C, AY373377; Oc. atropalpus Vg-B, AY691321, Vg-C, AY691322; Ae. polynesiensis Vg-A1, AY691318, Vg-B, AY691319, Vg-C, AY691320; Ae. albopictus Vg-A1, AY691316, Vg-C, AY691317; Oc. triseriatus Vg-C, AY691323; Cx. quinquefasciatus Vg-C1, AY691324, Vg-C2, AY691325; Tx. amboinensis Vg-C, AY691326; An. albimanus Vg-C, AY691327).

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Duplication, concerted evolution and purifying selection drive the evolution of mosquito vitellogenin genes.

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Duplication, concerted evolution and purifying selection drive the evolution of mosquito vitellogenin genes.

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