Parent of origin gene expression in the bumblebee, Bombus terrestris, supports Haig’s kinship theory for the evolution of genomic imprinting

AbstractGenomic imprinting is the differential expression of alleles in diploid individuals, with the expression being dependent upon the sex of the parent from which it was inherited. Haig’s kinship theory hypothesizes that genomic imprinting is due to an evolutionary conflict of interest between alleles from the mother and father. In social insects, it has been suggested that genomic imprinting should be widespread. One recent study identified parent-of-origin expression in honeybees and found evidence supporting the kinship theory. However, little is known about genomic imprinting in insects and multiple theoretical predictions must be tested to avoid single-study confirmation bias. We, therefore, tested for parent-of-origin expression in a primitively eusocial bee. We found equal numbers of maternally and paternally biased expressed alleles. The most highly biased alleles were maternally expressed, offering support for the kinship theory. We also found low conservation of potentially imprinted genes with the honeybee, suggesting rapid evolution of genomic imprinting in Hymenoptera.Impact summaryGenomic imprinting is the differential expression of alleles in diploid individuals, with the expression being dependent upon the sex of the parent from which it was inherited. Genomic imprinting is an evolutionary paradox. Natural selection is expected to favour expression of both alleles in order to protect against recessive mutations that render a gene ineffective. What then is the benefit of silencing one copy of a gene, making the organism functionally haploid at that locus? Several explanations for the evolution of genomic imprinting have been proposed. Haig’s kinship theory is the most developed and best supported.Haig’s theory is based on the fact that maternally (matrigene) and paternally (patrigene) inherited genes in the same organism can have different interests. For example, in a species with multiple paternity, a patrigene has a lower probability of being present in siblings that are progeny of the same mother than does a matrigene. As a result, a patrigene will be selected to value the survival of the organism it is in more highly, compared to the survival of siblings. This is not the case for a matrigene.Kinship theory is central to our evolutionary understanding of imprinting effects in human health and plant breeding. Despite this, it still lacks a robust, independent test. Colonies of social bees consist of diploid females (queens and workers) and haploid males created from unfertilised eggs. This along with their social structures allows for novel predictions of Haig’s theory.In this paper, we find parent of origin allele specific expression in the important pollinator, the buff-tailed bumblebee. We also find, as predicted by Haig’s theory, a balanced number of genes showing matrigenic or patrigenic bias with the most extreme bias been found in matrigenically biased genes.

Download Full-text

Allele specific expression in worker reproduction genes in the bumblebee Bombus terrestris

10.7287/peerj.preprints.878 ◽

2015 ◽

Author(s):

Harindra E Amarasinghe ◽

Bradley J Toghill ◽

Eamonn B Mallon

Keyword(s):

Differential Expression ◽

Genomic Imprinting ◽

Bombus Terrestris ◽

Worker Reproduction ◽

Specific Expression ◽

Allele Specific Expression ◽

Potential Models ◽

Allele Specific ◽

Hymenopteran Insects

Genomic imprinting is the differential expression of alleles, with the expression being dependent upon the sex of the parent from which it was inherited. Hymenopteran insects (ants, bees and wasps) are emerging as potential models for genomic imprinting and epigenetics. As a first step in establishing the possibility of genomic imprinting in the bumblebee, Bombus terrestris, we search for allele specific expression in twelve genes associated with worker reproduction. We found that the patrigene (allele from the father) is more expressed than the matrigene (allele from the mother) in Ecdysone 20 monooxygenase. This enzyme catalyses the reaction which turns the ecdysteroid ecdysone into 20-hydroxyecdysone, also an ecdysteroid. Both of these ecdysteroids are important for worker reproduction in the bumblebee.

Download Full-text

Parent of origin DNA methylation as a potential mechanism for genomic imprinting in bees.

10.1101/2021.12.17.473163 ◽

2021 ◽

Author(s):

Hollie Marshall ◽

Moi T Nicholas ◽

Jelle S van Zweden ◽

Felix Wäckers ◽

Laura Ross ◽

...

Keyword(s):

Dna Methylation ◽

Genomic Imprinting ◽

Bombus Terrestris ◽

Experimental Manipulation ◽

Whole Genome ◽

Specific Expression ◽

Differentially Methylated Genes ◽

Allele Specific ◽

Parent Of Origin ◽

Functional Dna

Genomic imprinting is defined as parent-of-origin allele-specific expression. In order for genes to be expressed in this manner an `imprinting' mark must be present to distinguish the parental alleles within the genome. In mammals imprinted genes are primarily associated with DNA methylation. Genes exhibiting parent-of-origin expression have recently been identified in two species of Hymenoptera with functional DNA methylation systems; Apis mellifera and Bombus terrestris. We carried out whole genome bisulfite sequencing of parents and offspring from reciprocal crosses of two B. terrestris subspecies in order to identify parent-of-origin DNA methylation. We were unable to survey a large enough proportion of the genome to draw a conclusion on the presence of parent-of-origin DNA methylation however we were able to characterise the sex- and caste-specific methylomes of B. terrestris for the first time. We find males differ significantly to the two female castes, with differentially methylated genes involved in many histone modification related processes. We also analysed previously generated honeybee whole genome bisulfite data to see if genes previously identified as showing parent-of-origin DNA methylation in the honeybee show consistent allele-specific methylation in independent data sets. We have identified a core set of 12 genes in female castes which may be used for future experimental manipulation to explore the functional role of parent-of-origin DNA methylation in the honeybee. Finally, we have also identified allele-specific DNA methylation in honeybee male thorax tissue which suggests a role for DNA methylation in ploidy compensation in this species.

Download Full-text

Parent of origin gene expression in the bumblebee, Bombus terrestris , supports Haig's kinship theory for the evolution of genomic imprinting

Evolution Letters ◽

10.1002/evl3.197 ◽

2020 ◽

Vol 4 (6) ◽

pp. 479-490 ◽

Cited By ~ 1

Author(s):

Hollie Marshall ◽

Jelle S. van Zweden ◽

Anneleen Van Geystelen ◽

Kristof Benaets ◽

Felix Wäckers ◽

...

Keyword(s):

Gene Expression ◽

Genomic Imprinting ◽

Bombus Terrestris ◽

Kinship Theory ◽

Parent Of Origin

Download Full-text

Allele specific expression in worker reproduction genes in the bumblebee Bombus terrestris

10.7287/peerj.preprints.878v1 ◽

2015 ◽

Author(s):

Harindra E Amarasinghe ◽

Bradley J Toghill ◽

Eamonn B Mallon

Keyword(s):

Differential Expression ◽

Genomic Imprinting ◽

Bombus Terrestris ◽

Worker Reproduction ◽

Specific Expression ◽

Allele Specific Expression ◽

Potential Models ◽

Allele Specific ◽

Hymenopteran Insects

Download Full-text

Parent-of-origin effects, allele-specific expression, genomic imprinting and paternal manipulation in social insects

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2020.0425 ◽

2021 ◽

Vol 376 (1826) ◽

Cited By ~ 1

Author(s):

Benjamin P. Oldroyd ◽

Boris Yagound

Keyword(s):

Gene Expression ◽

Genomic Imprinting ◽

Social Insects ◽

Social Insect ◽

Specific Gene ◽

Specific Expression ◽

Rna Molecules ◽

Parent Of Origin ◽

Origin Effects ◽

Gene Expression Studies

Haplo-diploidy and the relatedness asymmetries it generates mean that social insects are prime candidates for the evolution of genomic imprinting. In single-mating social insect species, some genes may be selected to evolve genomic mechanisms that enhance reproduction by workers when they are inherited from a female. This situation reverses in multiple mating species, where genes inherited from fathers can be under selection to enhance the reproductive success of daughters. Reciprocal crosses between subspecies of honeybees have shown strong parent-of-origin effects on worker reproductive phenotypes, and this could be evidence of such genomic imprinting affecting genes related to worker reproduction. It is also possible that social insect fathers directly affect gene expression in their daughters, for example, by placing small interfering RNA molecules in semen. Gene expression studies have repeatedly found evidence of parent-specific gene expression in social insects, but it is unclear at this time whether this arises from genomic imprinting, paternal manipulation, an artefact of cyto-nuclear interactions, or all of these. This article is part of the theme issue ‘How does epigenetics influence the course of evolution?’

Download Full-text

Bumblebee worker castes show differences in allele-specific DNA methylation and allele-specific expression

10.1101/2020.02.07.938423 ◽

2020 ◽

Author(s):

H. Marshall ◽

A.R.C. Jones ◽

Z.N. Lonsdale ◽

E.B. Mallon

Keyword(s):

Dna Methylation ◽

Bombus Terrestris ◽

Imprinted Genes ◽

Specific Expression ◽

Allele Specific Expression ◽

Genome Wide ◽

Expression Bias ◽

Allele Specific ◽

Parent Of Origin ◽

Worker Castes

AbstractAllele-specific expression is when one allele of a gene shows higher levels of expression compared to the other allele, in a diploid organism. Genomic imprinting is an extreme example of this, where some genes exhibit allele-specific expression in a parent-of-origin manner. Recent work has identified potentially imprinted genes in species of Hymenoptera. However, the molecular mechanism which drives this allelic expression bias remains unknown. In mammals DNA methylation is often associated with imprinted genes. DNA methylation systems have been described in species of Hymenoptera, providing a candidate imprinting mechanism. Using previously generated RNA-Seq and whole genome bisulfite sequencing from reproductive and sterile bumblebee (Bombus terrestris) workers we have identified genome-wide allele-specific expression and allele-specific DNA methylation. The majority of genes displaying allele-specific expression are common between reproductive castes and the proportion of allele-specific expression bias generally varies between colonies. We have also identified genome-wide allele-specific DNA methylation patterns in both castes. There is no significant overlap between genes showing allele-specific expression and allele-specific methylation. These results indicate that DNA methylation does not directly drive genome-wide allele-specific expression in this species. Only a small number of the genes identified may be ‘imprinted’ and it may be these genes which are associated with allele-specific DNA methylation. Future work utilising reciprocal crosses to identify parent-of-origin DNA methylation will further clarify the role of DNA methylation in parent-of-origin allele-specific expression.

Download Full-text

Divergence among rice cultivars reveals roles for transposition and epimutation in ongoing evolution of genomic imprinting

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2104445118 ◽

2021 ◽

Vol 118 (29) ◽

pp. e2104445118

Author(s):

Jessica A. Rodrigues ◽

Ping-Hung Hsieh ◽

Deling Ruan ◽

Toshiro Nishimura ◽

Manoj K. Sharma ◽

...

Keyword(s):

Gene Expression ◽

Dna Methylation ◽

Genomic Imprinting ◽

Small Rnas ◽

Imprinted Genes ◽

Dna Hypomethylation ◽

Transcription Start ◽

Specific Expression ◽

Parent Of Origin

Parent-of-origin–dependent gene expression in mammals and flowering plants results from differing chromatin imprints (genomic imprinting) between maternally and paternally inherited alleles. Imprinted gene expression in the endosperm of seeds is associated with localized hypomethylation of maternally but not paternally inherited DNA, with certain small RNAs also displaying parent-of-origin–specific expression. To understand the evolution of imprinting mechanisms in Oryza sativa (rice), we analyzed imprinting divergence among four cultivars that span both japonica and indica subspecies: Nipponbare, Kitaake, 93-11, and IR64. Most imprinted genes are imprinted across cultivars and enriched for functions in chromatin and transcriptional regulation, development, and signaling. However, 4 to 11% of imprinted genes display divergent imprinting. Analyses of DNA methylation and small RNAs revealed that endosperm-specific 24-nt small RNA–producing loci show weak RNA-directed DNA methylation, frequently overlap genes, and are imprinted four times more often than genes. However, imprinting divergence most often correlated with local DNA methylation epimutations (9 of 17 assessable loci), which were largely stable within subspecies. Small insertion/deletion events and transposable element insertions accompanied 4 of the 9 locally epimutated loci and associated with imprinting divergence at another 4 of the remaining 8 loci. Correlating epigenetic and genetic variation occurred at key regulatory regions—the promoter and transcription start site of maternally biased genes, and the promoter and gene body of paternally biased genes. Our results reinforce models for the role of maternal-specific DNA hypomethylation in imprinting of both maternally and paternally biased genes, and highlight the role of transposition and epimutation in rice imprinting evolution.

Download Full-text

Paternally expressed imprinted genes establish postzygotic hybridization barriers in Arabidopsis thaliana

eLife ◽

10.7554/elife.10074 ◽

2015 ◽

Vol 4 ◽

Cited By ~ 53

Author(s):

Philip Wolff ◽

Hua Jiang ◽

Guifeng Wang ◽

Juan Santos-González ◽

Claudia Köhler

Keyword(s):

Arabidopsis Thaliana ◽

Differential Expression ◽

Seed Development ◽

Genomic Imprinting ◽

Imprinted Genes ◽

Functional Requirement ◽

Functional Roles ◽

Epigenetic Phenomenon ◽

Parent Of Origin

Genomic imprinting is an epigenetic phenomenon causing parent-of-origin specific differential expression of maternally and paternally inherited alleles. While many imprinted genes have been identified in plants, the functional roles of most of them are unknown. In this study, we systematically examine the functional requirement of paternally expressed imprinted genes (PEGs) during seed development in Arabidopsis thaliana. While none of the 15 analyzed peg mutants has qualitative or quantitative abnormalities of seed development, we identify three PEGs that establish postzygotic hybridization barriers in the endosperm, revealing that PEGs have a major role as speciation genes in plants. Our work reveals that a subset of PEGs maintains functional roles in the inbreeding plant Arabidopsis that become evident upon deregulated expression.

Download Full-text

Genomic imprinting in mouse blastocysts is predominantly associated with H3K27me3

Nature Communications ◽

10.1038/s41467-021-23510-4 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Laura Santini ◽

Florian Halbritter ◽

Fabian Titz-Teixeira ◽

Toru Suzuki ◽

Maki Asami ◽

...

Keyword(s):

Bisulfite Sequencing ◽

Blastocyst Stage ◽

Preimplantation Embryos ◽

Imprinted Genes ◽

Specific Expression ◽

Histone 3 ◽

Complex Program ◽

Genome Bisulfite Sequencing ◽

Mammalian Genomes ◽

Parent Of Origin

AbstractIn mammalian genomes, differentially methylated regions (DMRs) and histone marks including trimethylation of histone 3 lysine 27 (H3K27me3) at imprinted genes are asymmetrically inherited to control parentally-biased gene expression. However, neither parent-of-origin-specific transcription nor imprints have been comprehensively mapped at the blastocyst stage of preimplantation development. Here, we address this by integrating transcriptomic and epigenomic approaches in mouse preimplantation embryos. We find that seventy-one genes exhibit previously unreported parent-of-origin-specific expression in blastocysts (nBiX: novel blastocyst-imprinted expressed). Uniparental expression of nBiX genes disappears soon after implantation. Micro-whole-genome bisulfite sequencing (µWGBS) of individual uniparental blastocysts detects 859 DMRs. We further find that 16% of nBiX genes are associated with a DMR, whereas most are associated with parentally-biased H3K27me3, suggesting a role for Polycomb-mediated imprinting in blastocysts. nBiX genes are clustered: five clusters contained at least one published imprinted gene, and five clusters exclusively contained nBiX genes. These data suggest that early development undergoes a complex program of stage-specific imprinting involving different tiers of regulation.

Download Full-text