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Link to original content: https://pubmed.ncbi.nlm.nih.gov/26169943
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. 2015 Oct;32(10):2749-59.
doi: 10.1093/molbev/msv151. Epub 2015 Jul 13.

Alternative Splice in Alternative Lice

Jaime M Tovar-Corona  1 , Atahualpa Castillo-Morales  1 , Lu Chen  2 , Brett P Olds  3 , John M Clark  4 , Stuart E Reynolds  5 , Barry R Pittendrigh  6 , Edward J Feil  1 , Araxi O Urrutia  7
Affiliations

Alternative Splice in Alternative Lice

Jaime M Tovar-Corona et al. Mol Biol Evol. 2015 Oct.

Abstract

Genomic and transcriptomics analyses have revealed human head and body lice to be almost genetically identical; although con-specific, they nevertheless occupy distinct ecological niches and have differing feeding patterns. Most importantly, while head lice are not known to be vector competent, body lice can transmit three serious bacterial diseases; epidemictyphus, trench fever, and relapsing fever. In order to gain insights into the molecular bases for these differences, we analyzed alternative splicing (AS) using next-generation sequencing data for one strain of head lice and one strain of body lice. We identified a total of 3,598 AS events which were head or body lice specific. Exon skipping AS events were overrepresented among both head and body lice, whereas intron retention events were underrepresented in both. However, both the enrichment of exon skipping and the underrepresentation of intron retention are significantly stronger in body lice compared with head lice. Genes containing body louse-specific AS events were found to be significantly enriched for functions associated with development of the nervous system, salivary gland, trachea, and ovarian follicle cells, as well as regulation of transcription. In contrast, no functional categories were overrepresented among genes with head louse-specific AS events. Together, our results constitute the first evidence for transcript pool differences in head and body lice, providing insights into molecular adaptations that enabled human lice to adapt to clothing, and representing a powerful illustration of the pivotal role AS can play in functional adaptation.

Keywords: alternative splicing; body lice; head lice; human parasite; phenotype evolution; transcriptomics.

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Figures

F<sc>ig</sc>. 1.
Fig. 1.
AS prevalence in human body and head lice as compared with other arthropod species. Bars adjacent to phylogenetic tree represent the proportion alternatively spliced genes in different species (the use of separate bars for head and body lice does not imply them being distinct species). Caenorhabditis elegans is included for reference. See supplementary table S2, Supplementary Material online, for sources of images.
F<sc>ig</sc>. 2.
Fig. 2.
Enrichment and impoverishment of AS event types among head or body louse-specific confirmed AS events. Top left panel shows heat map graph of enrichment analysis of head and body louse-specific AS events compared with the wider pool of AS events in lice. Blocks represent enrichment (checkered blocks) and depletion (solid blocks) for each AS event type in head and body lice. Higher color intensity reflects the statistical significance of enrichment and depletion of each AS event type with yellow tones for less significant deviations from random expectation (P values after Bonferroni correction). All AS types deviate significantly from random expectations in both head and body lice except for 3S5S AS events. Top right panel shows significant enrichment of ES and significant depletion of IR in both head and body lice. Bottom panel shows schematic representation of AS types detected from 454 transcript sequences. AS events can be classified in five main groups ES (ES or cassette exon), 5S (alternative 5′-donor site), 3S5S (alternative 3′-acceptor and 5′-donor sites), 3S (alternative 3′-acceptor site), and I (IR). Constitutive exons are denoted by Cs.
F<sc>ig</sc>. 3.
Fig. 3.
Diagram of alternatively spliced gene counts in head and body lice. The most outer square shows the total number of annotated louse genes. The inner square represents those genes with at least one confirmed AS event in either head or body lice. The left circle includes genes with at least one AS event unique to the head louse. The right set includes genes with at least one AS event unique in the body louse. The intersection includes genes with both at least one unique AS event in head lice and one unique AS event in body lice.
F<sc>ig</sc>. 4.
Fig. 4.
GO enrichment among genes with unique AS events in head or body lice compared with the wider set of alternatively spliced genes in either form of louse. Checkered and solid blocks represent enrichment and depletion respectively. Darker shades represent stronger statistical support for the observed variation. GO categories with fewer than 100 genes were grouped together. Side bar shows the significance threshold for overrepresentation and underrepresentation of GO categories after Benjamini–Hochberg correction.
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