Abstract
ABSTRACTDifferential intragenic methylation in social insects has been hailed as a prime mover of environmentally driven organismal plasticity and even as evidence for genomic imprinting. However, very little experimental work has been done to test these ideas and to prove the validity of such claims. Here we analyze in detail differentially methylated obligatory epialleles of a conserved gene encoding lysosomal α-mannosidase (AmLAM) in the honeybee. We combined genotyping of progenies derived from colonies founded by single drone inseminated queens, ultra-deep allele-specific bisulfite DNA sequencing, and gene expression to reveal how sequence variants, DNA methylation, and transcription interrelate. We show that both methylated and non-methylated states of AmLAM follow Mendelian inheritance patterns and are strongly influenced by polymorphic changes in DNA. Increased methylation of a given allele correlates with higher levels of context-dependent AmLAM expression and appears to affect the transcription of an antisense long noncoding RNA. No evidence of allelic imbalance or imprinting involved in this process has been found. Our data suggest that by generating alternate methylation states that affect gene expression, sequence variants provide organisms with a high level of epigenetic flexibility that can be used to select appropriate responses in various contexts. This study represents the first effort to integrate DNA sequence variants, gene expression, and methylation in a social insect to advance our understanding of their relationships in the context of causality.
Highlights
The transcriptional events that lead to the development of a multicellular organism result from interactions between the underlying genetic sequence and an array of epigenomic marks that are modulated, in part, by environmental signals
Recent work has shown that genetic variation is associated with altered chromatin states 5,6 and differential DNA methylation, 7 which appear to modify gene expression primarily through altered transcription factor binding.[7,8]
In the process of comparing genome-wide methylation profiles in the honeybee haploid and diploid embryos we have come across a »0.8 kb region, located on Linkage Group 4, containing 20 CpGs that are highly methylated only in the diploid sample. We identified this region as exons 16 to 18 of the gene coding for lysosomal a-mannosidase (AmLAM GB44223, Fig. 1), and noticed that 2 sequence variants correlated with a particular methylation pattern (Fig. S1)
Summary
The transcriptional events that lead to the development of a multicellular organism result from interactions between the underlying genetic sequence and an array of epigenomic marks that are modulated, in part, by environmental signals. Central to these processes are a variety of epigenetic pathways contributing to phenotypic plasticity and environmental adaptation.[1,2,3] One of the key challenges in understanding what drives phenotypic variation lies in determining the extent to which the nucleotide sequence influences epigenetic states. Defining the exact mechanisms whereby a given epiallele can influence transcription and, subsequently, phenotype remains a challenge
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