Uncovering the novel characteristics of Asian honey bee, Apis cerana, by whole genome sequencing

Abstract

Background: The honey bee is an important model system for increasing understanding of molecular and neural mechanisms underlying social behaviors relevant to the agricultural industry and basic science. The western honey bee, Apis mellifera, has served as a model species, and its genome sequence has been published. In contrast, the genome of the Asian honey bee, Apis cerana, has not yet been sequenced. A. cerana has been raised in Asian countries for thousands of years and has brought considerable economic benefits to the apicultural industry. A cerana has divergent biological traits compared to A. mellifera and it has played a key role in maintaining biodiversity in eastern and southern Asia. Here we report the first whole genome sequence of A. cerana.

Results: Using de novo assembly methods, we produced a 238 Mbp draft of the A. cerana genome and generated 10,651 genes. A.cerana-specific genes were analyzed to better understand the novel characteristics of this honey bee species. Seventy-two percent of the A. cerana-specific genes had more than one GO term, and 1,696 enzymes were categorized into 125 pathways. Genes involved in chemoreception and immunity were carefully identified and compared to those from other sequenced insect models. These included 10 gustatory receptors, 119 odorant receptors, 10 ionotropic receptors, and 160 immune-related genes.

Conclusions: This first report of the whole genome sequence of A. cerana provides resources for comparative sociogenomics, especially in the field of social insect communication. These important tools will contribute to a better understanding of the complex behaviors and natural biology of the Asian honey bee and to anticipate its future evolutionary trajectory.

Figure 1

CpG analysis of protein sequence of A. mellifera and A. cerana. Distributions of normalized CpG o/e content of the (A) A. cerana and (B) A. mellifera. Bimodal distributions of honey bee protein-coding sequences indicate that the genome of honey bee encoded two distinct classes of genes which are targeted by DNA methylation.

Figure 2

Comparative analysis of orthologous protein groups among the four insect genomes. Orthology analysis of the proteins of A. cerana (orange oval) with three well known insect models, D. melanogaster (blue oval), N. vitripennis (purple oval), and A. mellifera (red oval). Both D. melanogaster and N. vitripennis are non-social and A. mellifera and A. cerana are social insect species. *indicates A. cerana-specific proteins.

Figure 3

Phylogenetic tree of the gustatory receptor ( Gr ) family. (A) Phylogenetic tree constructed using A. cerana (red), A. mellifera (blue), and D. melanogaster gustatory receptor proteins (B) Relative Gr gene expression profiling using RPKM values in A. cerana (left) and A. mellfera (right). Red color indicates high expression compared to blue.

Figure 4

Phylogenetic tree of the odorant receptor ( Or ) family. (A) Phylogenetic tree constructed using A. cerana (red), A. mellifera (blue), and D. melanogaster odorant receptor proteins. (B) Relative Or gene expression profiling using RPKM values in A. cerana (left) and A. mellfera (right). Red color indicates high expression compared to blue. (C) Microsynteny between A. cerana and A. mellfera Or genes. Orthologous and paralogous of A. cerana (red) and A. mellifera (blue) Ors were analyzed with BLASTZ. A. cerana scaffold number and A. mellifera chromosome number are on the left and right side, respectively.

Figure 5

Phylogenetic tree of the ionotropic receptor ( Ir ) family. (A) Phylogenetic tree constructed using A. cerana (red), A. mellifera (blue), and D. melanogaster ionotropic receptor proteins. (B) Relative Ir gene expression profiling using RPKM values in A. cerana (left) and A. mellfera (right). Red color indicates high expression compared to blue.

Figure 6

Candidate genes of immune-related pathways in A. cerana. Colored boxes indicate counterparts of immune pathway components in the A. cerana genome. Schematic drawing adapted from immune pathways in A. mellifera[90].