Abstract
BackgroundHomology-based comparisons of the genes involved in innate immunity across many insect taxa with fully sequenced genomes has revealed a striking pattern of gene gain and loss, particularly among genes that encode proteins involved in clearing pathogens (effectors). However, limited functional annotation in non-model systems has hindered understanding of evolutionary novelties in the insect innate immune system.ResultsWe use short read sequencing technology (Illumina/Solexa) to compare the transcriptional response to infection between the well studied model system Drosophila melanogaster and the distantly related drosophilid D. virilis. We first demonstrate that Illumina/Solexa sequencing of cDNA from infected and uninfected D. melanogaster recapitulates previously published microarray studies of the transcriptional response to infection in this species, validating our approach. We then show that patterns of transcription of homologous genes differ considerably between D. melanogaster and D. virilis, and identify potential candidates for novel components of the D. virilis immune system based on transcriptional data. Finally, we use a proteomic approach to characterize the protein constituents of the D. virilis hemolymph and validate our transcriptional data.ConclusionThese results suggest that the acquisition of novel components of the immune system, and particularly novel effector proteins, may be a common evolutionary phenomenon.
Highlights
Homology-based comparisons of the genes involved in innate immunity across many insect taxa with fully sequenced genomes has revealed a striking pattern of gene gain and loss, among genes that encode proteins involved in clearing pathogens
Aligning sequencing reads to the reference genome and identified genes regulated by infection We generated between 4.8 and 5.2 million 36 bp reads from one lane of Illumina/Solexa sequencing for each of four biological samples: naïve D. melanogaster iso-1 (DmelU), 12 hours post-challenge D. melanogaster iso-1 (DmelI), naïve D. virilis 15010-1051.87 (DvirU), and 12 hourspost challenge D. virilis 15010-1051.87 (DvirI)
We used short read cDNA sequencing to characterize the transcriptional response to infection in D. virilis and D. melanogaster
Summary
Homology-based comparisons of the genes involved in innate immunity across many insect taxa with fully sequenced genomes has revealed a striking pattern of gene gain and loss, among genes that encode proteins involved in clearing pathogens (effectors). BMC Genomics 2009, 10:259 http://www.biomedcentral.com/1471-2164/10/259 ary novelties restricted to D. melanogaster and related species in the Sophophora subgenus of drosophilids [5] This pattern is in contrast to genes encoding components of immune-related signaling pathways, which are typically found as single copy orthologs even among distantly related insects [8,9,13], and have identifiable homologs in mammals [14]. Together, these observations suggest that disruption of stoichiometry, dosage, and other conserved interactions among signaling pathways is usually deleterious, leading to very low tolerance of gene copy variation among signaling pathways and preservation of single-copy orthologs across deep evolutionary time. These observations suggest that pathway outputs retain flexibility, allowing novel effectors to be recruited into the system, potentially leading to rapid, and perhaps advantageous, proliferation of effector components across evolutionary time
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