Differentially methylated obligatory epialleles modulate context-dependent LAM gene expression in the honeybee Apis mellifera

Laura Wedd, Robert Kucharski, Ryszard Maleszka

Research output: Contribution to journalArticle

21 Citations (Scopus)

Abstract

Differential 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.

Original languageEnglish
Pages (from-to)1-10
Number of pages10
JournalEpigenetics
Volume11
Issue number1
DOIs
Publication statusPublished - 2 Jan 2016
Externally publishedYes

Cite this

Wedd, Laura ; Kucharski, Robert ; Maleszka, Ryszard. / Differentially methylated obligatory epialleles modulate context-dependent LAM gene expression in the honeybee Apis mellifera. In: Epigenetics. 2016 ; Vol. 11, No. 1. pp. 1-10.
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Differentially methylated obligatory epialleles modulate context-dependent LAM gene expression in the honeybee Apis mellifera. / Wedd, Laura; Kucharski, Robert; Maleszka, Ryszard.

In: Epigenetics, Vol. 11, No. 1, 02.01.2016, p. 1-10.

Research output: Contribution to journalArticle

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T1 - Differentially methylated obligatory epialleles modulate context-dependent LAM gene expression in the honeybee Apis mellifera

AU - Wedd, Laura

AU - Kucharski, Robert

AU - Maleszka, Ryszard

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AB - Differential 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.

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KW - Epigenesis, Genetic

KW - Genotype

KW - Male

KW - Sequence Analysis, DNA

KW - Inheritance Patterns

KW - DNA Methylation

KW - RNA, Long Noncoding/genetics

KW - Animals

KW - Alleles

KW - Bees/genetics

KW - Female

KW - Transcription, Genetic

KW - High-Throughput Nucleotide Sequencing

KW - RNA, Antisense/genetics

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DO - 10.1080/15592294.2015.1107695

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