Skip to main page content
U.S. flag

An official website of the United States government

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2016 Jun 29;283(1833):20160558.
doi: 10.1098/rspb.2016.0558.

A possible role of DNA methylation in functional divergence of a fast evolving duplicate gene encoding odorant binding protein 11 in the honeybee

R Kucharski  1 , J Maleszka  1 , R Maleszka  2
Affiliations

A possible role of DNA methylation in functional divergence of a fast evolving duplicate gene encoding odorant binding protein 11 in the honeybee

R Kucharski et al. Proc Biol Sci. .

Abstract

Although gene duplication is seen as the main path to evolution of new functions, molecular mechanisms by which selection favours the gain versus loss of newly duplicated genes and minimizes the fixation of pseudo-genes are not well understood. Here, we investigate in detail a duplicate honeybee gene obp11 belonging to a fast evolving insect gene family encoding odorant binding proteins (OBPs). We report that obp11 is expressed only in female bees in rare antennal sensilla basiconica in contrast to its tandem partner obp10 that is expressed in the brain in both females and males (drones). Unlike all other obp genes in the honeybee, obp11 is methylated suggesting that functional diversification of obp11 and obp10 may have been driven by an epigenetic mechanism. We also show that increased methylation in drones near one donor splice site that correlates with higher abundance of a transcript variant encoding a truncated OBP11 protein is one way of controlling its contrasting expression. Our data suggest that like in mammals and plants, DNA methylation in insects may contribute to functional diversification of proteins produced from duplicated genes, in particular to their subfunctionalization by generating complementary patterns of expression.

Keywords: Apis mellifera; epialleles; genome evolution; insect epigenomics; insect olfaction.

PubMed Disclaimer

Figures

Figure 1.
Figure 1.
A snapshot of a genomic landscape shows the tandem arrangement of obp10 and obp11. The level of individual CpGs methylation for each gene is shown at the top, and the transcript variants deduced from the available transcriptomes at the bottom. Extracted from the honeybee genome browser (BeeBase, dna.anu.edu.au). (Online version in colour.)
Figure 2.
Figure 2.
Analysis of obp11 expression in the worker honeybee antenna. (a) Scanning electron microscopy image shows the localization of sensilla basiconica on the antennal tip (segments 3–10). (b) In situ analysis on a longitudinal section of the antenna showing the expression in the nuclei of basiconica. (c) PCR detection of a 250 bp obp11 amplicon in antennal segments 3–10. (d) In situ hybridization on a cross section of the antenna with the same antisense probe as in panel (b). (Online version in colour.)
Figure 3.
Figure 3.
Effect of methylation on obp11 alternative splicing. (a) Alternative splice acceptor site in intron 3 generates transcripts with a premature stop codon resulting in truncated peptide. Primers used to examine the expression of full-length (FL) and truncated (T) transcripts are shown below the exon/intron map. (b) Expression of obp11 alternatively spliced variant shown as percentage of total obp11 expression. In drone antennae, the spliced variant with the premature stop codon constitutes a much higher proportion of obp11 transcripts. This result is based on five replicates. (c) Increased methylation of three CpG sites in exon 3 correlates with higher abundance of the spliced variant encoding the truncated obp11. Based on three libraries. **p < 0.01, Student's t-test. (Online version in colour.)
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Rodin SN, Riggs AD. 2003. Epigenetic silencing may aid evolution by gene duplication. J. Mol. Evol. 56, 718–729. (10.1007/s00239-002-2446-6) - DOI - PubMed
    1. Lynch M, Conery JS. 2000. The evolutionary fate and consequences of duplicate genes. Science 290, 1151–1155. (10.1126/science.290.5494.1151) - DOI - PubMed
    1. Flores K, Wolschin F, Corneveaux JJ, Allen AN, Huentelman MJ, Amdam GV. 2012. Genome-wide association between DNA methylation and alternative splicing in an invertebrate. BMC Genomics 13, 480 (10.1186/1471-2164-13-480) - DOI - PMC - PubMed
    1. Lyko F, Foret S, Kucharski R, Wolf S, Falckenhayn C, Maleszka R. 2010. The honey bee epigenomes: differential methylation of brain DNA in queens and workers. PLoS Biol. 8, e1000506 (10.1371/journal.pbio.1000506) - DOI - PMC - PubMed
    1. Foret S, Kucharski R, Pittelkow Y, Lockett GA, Maleszka R. 2009. Epigenetic regulation of the honey bee transcriptome: unravelling the nature of methylated genes. BMC Genomics 10, 472 (10.1186/1471-2164-10-472) - DOI - PMC - PubMed

Substances

LinkOut - more resources