The duck genome and transcriptome provide insight into an avian influenza virus reservoir species

Abstract

The duck (Anas platyrhynchos) is one of the principal natural hosts of influenza A viruses. We present the duck genome sequence and perform deep transcriptome analyses to investigate immune-related genes. Our data indicate that the duck possesses a contractive immune gene repertoire, as in chicken and zebra finch, and this repertoire has been shaped through lineage-specific duplications. We identify genes that are responsive to influenza A viruses using the lung transcriptomes of control ducks and ones that were infected with either a highly pathogenic (A/duck/Hubei/49/05) or a weakly pathogenic (A/goose/Hubei/65/05) H5N1 virus. Further, we show how the duck's defense mechanisms against influenza infection have been optimized through the diversification of its β-defensin and butyrophilin-like repertoires. These analyses, in combination with the genomic and transcriptomic data, provide a resource for characterizing the interaction between host and influenza viruses.

Figure 1

Numbers of gene losses and gains across 17 vertebrates. Data are shown for 17 vertebrates, 3 teleosts, 5 reptilians and 8 mammals. The numbers of gene gains (+) and losses (−) are given on branches or to the right of the taxa. The rates of gene gain and loss for the clades derived from the MRCAR (MRCA of reptiles), MRCAT (MRCA of teleosts) and MRCAM (MRCA of mammals) and for Xenopus tropicalis are 0.0011, 0.0012, 0.0017 and 0.0019 per gene per million years, respectively.

Figure 2

Identification of genes responsive to influenza A viruses in the lungs of ducks infected with one of two H5N1 viruses on days 1, 2 and 3 after inoculation. The genes included here showed significant differences in gene expression (FDR ≤0.001, fold change ≥2) in at least one experiment. Genes shown in red had upregulated expression, and those shown in yellow had downregulated expression in infected ducks relative to controls or in DK/49-infected relative to GS/65-infected ducks. (Full gene names are given in supplementary table 13.) Hierarchical clusters of genes and samples were based on Pearson’s correlation and Spearman’s rank correlation analyses, respectively. (a) Overall gene expression profiles in DK/49- or GS/65-infected ducks compared to control animals. The heatmap was generated from hierarchical cluster analyses of both genes and samples. (b) Expression of 119 innate immune genes in DK/49- or GS/65-infected ducks. The heatmap was generated from hierarchical analysis of genes, showing significant changes in gene expression for 119 innate immune genes in DK/49- or GS/65-infected ducks 1–3 d after inoculation. (c) Expression of two significantly expanded gene families (β-defensins and BTNLs) in DK/49- or GS/65-infected ducks. The heatmap was generated from hierarchical analysis of genes, showing that most of the avian defensin and BTNL genes, including two LSDs of AvDB3 and eight LSDs of BTNL genes, have significantly altered gene expression in DK/49- or GS/65-infected ducks 1–3 d after inoculation.