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

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.

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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.

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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.

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Lineage and Parent-of-Origin Effects in DNA Methylation of Honey Bees (Apis mellifera) Revealed by Reciprocal Crosses and Whole-Genome Bisulfite Sequencing

Genome Biology and Evolution ◽

10.1093/gbe/evaa133 ◽

2020 ◽

Vol 12 (8) ◽

pp. 1482-1492

Author(s):

Xin Wu ◽

David A Galbraith ◽

Paramita Chatterjee ◽

Hyeonsoo Jeong ◽

Christina M Grozinger ◽

...

Keyword(s):

Dna Methylation ◽

Honey Bees ◽

Specific Expression ◽

Africanized Honey Bee ◽

Allele Specific ◽

Parent Of Origin ◽

Origin Effects ◽

Genetic Background Effects ◽

Allele Specific Methylation ◽

Methylation Patterns

Abstract Parent-of-origin methylation arises when the methylation patterns of a particular allele are dependent on the parent it was inherited from. Previous work in honey bees has shown evidence of parent-of-origin-specific expression, yet the mechanisms regulating such pattern remain unknown in honey bees. In mammals and plants, DNA methylation is known to regulate parent-of-origin effects such as genomic imprinting. Here, we utilize genotyping of reciprocal European and Africanized honey bee crosses to study genome-wide allele-specific methylation patterns in sterile and reproductive individuals. Our data confirm the presence of allele-specific methylation in honey bees in lineage-specific contexts but also importantly, though to a lesser degree, parent-of-origin contexts. We show that the majority of allele-specific methylation occurs due to lineage rather than parent-of-origin factors, regardless of the reproductive state. Interestingly, genes affected by allele-specific DNA methylation often exhibit both lineage and parent-of-origin effects, indicating that they are particularly labile in terms of DNA methylation patterns. Additionally, we re-analyzed our previous study on parent-of-origin-specific expression in honey bees and found little association with parent-of-origin-specific methylation. These results indicate strong genetic background effects on allelic DNA methylation and suggest that although parent-of-origin effects are manifested in both DNA methylation and gene expression, they are not directly associated with each other.

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Canonical and Non-canonical Genomic Imprinting in Rodents

Frontiers in Cell and Developmental Biology ◽

10.3389/fcell.2021.713878 ◽

2021 ◽

Vol 9 ◽

Author(s):

Hisato Kobayashi

Keyword(s):

Dna Methylation ◽

Genomic Imprinting ◽

Mouse Genome ◽

Genetic Regulation ◽

Imprinted Genes ◽

Evolutionary Divergence ◽

Chromatin Modifications ◽

Allele Specific ◽

Epigenetic Phenomenon ◽

Parent Of Origin

Genomic imprinting is an epigenetic phenomenon that results in unequal expression of homologous maternal and paternal alleles. This process is initiated in the germline, and the parental epigenetic memories can be maintained following fertilization and induce further allele-specific transcription and chromatin modifications of single or multiple neighboring genes, known as imprinted genes. To date, more than 260 imprinted genes have been identified in the mouse genome, most of which are controlled by imprinted germline differentially methylated regions (gDMRs) that exhibit parent-of-origin specific DNA methylation, which is considered primary imprint. Recent studies provide evidence that a subset of gDMR-less, placenta-specific imprinted genes is controlled by maternal-derived histone modifications. To further understand DNA methylation-dependent (canonical) and -independent (non-canonical) imprints, this review summarizes the loci under the control of each type of imprinting in the mouse and compares them with the respective homologs in other rodents. Understanding epigenetic systems that differ among loci or species may provide new models for exploring genetic regulation and evolutionary divergence.

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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.

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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

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Bumblebee Workers Show Differences in Allele-Specific DNA Methylation and Allele-Specific Expression

Genome Biology and Evolution ◽

10.1093/gbe/evaa132 ◽

2020 ◽

Vol 12 (8) ◽

pp. 1471-1481

Author(s):

Hollie Marshall ◽

Alun R C Jones ◽

Zoë N Lonsdale ◽

Eamonn B Mallon

Keyword(s):

Dna Methylation ◽

Bombus Terrestris ◽

Specific Expression ◽

Allele Specific Expression ◽

Cis Acting ◽

Genome Wide ◽

Expression Bias ◽

Hymenopteran Species ◽

Allele Specific ◽

Allele Specific Methylation

Abstract Allele-specific expression is when one allele of a gene shows higher levels of expression compared with the other allele, in a diploid organism. Recent work has identified allele-specific expression in a number of Hymenopteran species. However, the molecular mechanism which drives this allelic expression bias remains unknown. In mammals, DNA methylation is often associated with genes which show allele-specific expression. DNA methylation systems have been described in species of Hymenoptera, providing a candidate 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 and sterile workers and the proportion of allele-specific expression bias generally varies between genetically distinct colonies. We have also identified genome-wide allele-specific DNA methylation patterns in both reproductive and sterile workers, with reproductive workers showing significantly more genes with allele-specific methylation. Finally, there is no significant overlap between genes showing allele-specific expression and allele-specific methylation. These results indicate that cis-acting DNA methylation does not directly drive genome-wide allele-specific expression in this species.

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Parent of origin gene expression in a founder population identifies two new imprinted genes at known imprinted regions

10.1101/344457 ◽

2018 ◽

Author(s):

Sahar V. Mozaffari ◽

Michelle M. Stein ◽

Kevin M. Magnaye ◽

Dan L. Nicolae ◽

Carole Ober

Keyword(s):

Gene Expression ◽

Dna Methylation ◽

Gene Expression Data ◽

Imprinted Genes ◽

Genotype Data ◽

Expression Data ◽

Rna Seq ◽

Specific Expression ◽

Allele Specific ◽

Parent Of Origin

AbstractGenomic imprinting is the phenomena that leads to silencing of one copy of a gene inherited from a specific parent. Mutations in imprinted regions have been involved in diseases showing parent of origin effects. Identifying genes with evidence of parent of origin expression patterns in family studies allows the detection of more subtle imprinting. Here, we use allele specific expression in lymphoblastoid cell lines from 306 Hutterites related in a single pedigree to provide formal evidence for parent of origin effects. We take advantage of phased genotype data to assign parent of origin to RNA-seq reads in individuals with gene expression data. Our approach identified known imprinted genes, two putative novel imprinted genes, and 14 genes with asymmetrical parent of origin gene expression. We used gene expression in peripheral blood leukocytes (PBL) to validate our findings, and then confirmed imprinting control regions (ICRs) using DNA methylation levels in the PBLs.Author SummaryLarge scale gene expression studies have identified known and novel imprinted genes through allele specific expression without knowing the parental origins of each allele. Here, we take advantage of phased genotype data to assign parent of origin to RNA-seq reads in 306 individuals with gene expression data. We identified known imprinted genes as well as two novel imprinted genes in lymphoblastoid cell line gene expression. We used gene expression in PBLs to validate our findings, and DNA methylation levels in PBLs to confirm previously characterized imprinting control regions that could regulate these imprinted genes.

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

10.1101/2020.01.17.909168 ◽

2020 ◽

Cited By ~ 1

Author(s):

Hollie Marshall ◽

Jelle S. van Zweden ◽

Anneleen Van Geystelen ◽

Kristof Benaets ◽

Felix Wäckers ◽

...

Keyword(s):

Differential Expression ◽

Genomic Imprinting ◽

Bombus Terrestris ◽

Rapid Evolution ◽

Multiple Paternity ◽

Lower Probability ◽

Specific Expression ◽

Social Bees ◽

Kinship Theory ◽

Parent Of Origin

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.

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