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

2020 ◽  
Vol 4 (6) ◽  
pp. 479-490 ◽  
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

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

2020 ◽  
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.

scholarly journals DNA demethylase ROS1 negatively regulates the imprinting of DOGL4 and seed dormancy in Arabidopsis thaliana

2018 ◽  
Vol 115 (42) ◽  
pp. E9962-E9970 ◽  
Author(s):  
Haifeng Zhu ◽  
Wenxiang Xie ◽  
Dachao Xu ◽  
Daisuke Miki ◽  
Kai Tang ◽  
...  
Keyword(s):  
Gene Expression ◽  
Seed Dormancy ◽  
Genomic Imprinting ◽  
Dna Demethylation ◽  
Paternal Allele ◽  
Maternal Allele ◽  
Imprinted Gene ◽  
Differential Gene ◽  
Parent Of Origin ◽  
Dna Demethylase

Genomic imprinting is a form of epigenetic regulation resulting in differential gene expression that reflects the parent of origin. In plants, imprinted gene expression predominantly occurs in the seed endosperm. Maternal-specific DNA demethylation by the DNA demethylase DME frequently underlies genomic imprinting in endosperm. Whether other more ubiquitously expressed DNA demethylases regulate imprinting is unknown. Here, we found that the DNA demethylase ROS1 regulates the imprinting of DOGL4. DOGL4 is expressed from the maternal allele in endosperm and displays preferential methylation and suppression of the paternal allele. We found that ROS1 negatively regulates imprinting by demethylating the paternal allele, preventing its hypermethylation and complete silencing. Furthermore, we found that DOGL4 negatively affects seed dormancy and response to the phytohormone abscisic acid and that ROS1 controls these processes by regulating DOGL4. Our results reveal roles for ROS1 in mitigating imprinted gene expression and regulating seed dormancy.

scholarly journals The discovery and importance of genomic imprinting

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Anne C Ferguson-Smith ◽  
Deborah Bourchis
Keyword(s):  
Gene Expression ◽  
Genomic Imprinting ◽  
Genetic Disorders ◽  
Epigenetic Inheritance ◽  
Specific Gene ◽  
Specific Gene Expression ◽  
Epigenetic Control ◽  
International Award ◽  
Parent Of Origin ◽  
Shed Light

The discovery of genomic imprinting by Davor Solter, Azim Surani and co-workers in the mid-1980s has provided a foundation for the study of epigenetic inheritance and the epigenetic control of gene activity and repression, especially during development. It also has shed light on a range of diseases, including both rare genetic disorders and common diseases. This article is being published to celebrate Solter and Surani receiving a 2018 Canada Gairdner International Award "for the discovery of mammalian genomic imprinting that causes parent-of-origin specific gene expression and its consequences for development and disease".

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

2021 ◽  
Vol 376 (1826) ◽  
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?’

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

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.

scholarly journals A Generalized Linear Model for Decomposing Cis-regulatory, Parent-of-Origin, and Maternal Effects on Allele-Specific Gene Expression

2017 ◽  
Vol 7 (7) ◽  
pp. 2227-2234 ◽  
Author(s):  
Yasuaki Takada ◽  
Ryutaro Miyagi ◽  
Aya Takahashi ◽  
Toshinori Endo ◽  
Naoki Osada
Keyword(s):  
Gene Expression ◽  
Maternal Effects ◽  
Genomic Imprinting ◽  
Whole Body ◽  
Specific Gene ◽  
Rna Seq ◽  
Simple Method ◽  
Specific Gene Expression ◽  
Allele Specific ◽  
Parent Of Origin

Abstract Joint quantification of genetic and epigenetic effects on gene expression is important for understanding the establishment of complex gene regulation systems in living organisms. In particular, genomic imprinting and maternal effects play important roles in the developmental process of mammals and flowering plants. However, the influence of these effects on gene expression are difficult to quantify because they act simultaneously with cis-regulatory mutations. Here we propose a simple method to decompose cis-regulatory (i.e., allelic genotype), genomic imprinting [i.e., parent-of-origin (PO)], and maternal [i.e., maternal genotype (MG)] effects on allele-specific gene expression using RNA-seq data obtained from reciprocal crosses. We evaluated the efficiency of method using a simulated dataset and applied the method to whole-body Drosophila and mouse trophoblast stem cell (TSC) and liver RNA-seq data. Consistent with previous studies, we found little evidence of PO and MG effects in adult Drosophila samples. In contrast, we identified dozens and hundreds of mouse genes with significant PO and MG effects, respectively. Interestingly, a similar number of genes with significant PO effect were detect in mouse TSCs and livers, whereas more genes with significant MG effect were observed in livers. Further application of this method will clarify how these three effects influence gene expression levels in different tissues and developmental stages, and provide novel insight into the evolution of gene expression regulation.

scholarly journals Intrafamily and intragenomic conflicts in human warfare

2017 ◽  
Vol 284 (1849) ◽  
pp. 20162699 ◽  
Author(s):  
Alberto J. C. Micheletti ◽  
Graeme D. Ruxton ◽  
Andy Gardner
Keyword(s):  
Gene Expression ◽  
Mathematical Model ◽  
Genomic Imprinting ◽  
Social Group ◽  
Ecological Study ◽  
Conflicts Of Interest ◽  
Ecological Perspective ◽  
Evolution Of Sex ◽  
Intragenomic Conflict ◽  
Parent Of Origin

Recent years have seen an explosion of multidisciplinary interest in ancient human warfare. Theory has emphasized a key role for kin-selected cooperation, modulated by sex-specific demography, in explaining intergroup violence. However, conflicts of interest remain a relatively underexplored factor in the evolutionary-ecological study of warfare, with little consideration given to which parties influence the decision to go to war and how their motivations may differ. We develop a mathematical model to investigate the interplay between sex-specific demography and human warfare, showing that: the ecology of warfare drives the evolution of sex-biased dispersal; sex-biased dispersal modulates intrafamily and intragenomic conflicts in relation to warfare; intragenomic conflict drives parent-of-origin-specific patterns of gene expression—i.e. ‘genomic imprinting’—in relation to warfare phenotypes; and an ecological perspective of conflicts at the levels of the gene, individual, and social group yields novel predictions as to pathologies associated with mutations and epimutations at loci underpinning human violence.

scholarly journals Males that silence their father’s genes: genomic imprinting of a complete haploid genome

2020 ◽  
Author(s):  
Andrés G. de la Filia ◽  
Andrew J. Mongue ◽  
Jennifer Dorrens ◽  
Hannah Lemon ◽  
Dominik R. Laetsch ◽  
...  
Keyword(s):  
Gene Expression ◽  
Genomic Imprinting ◽  
Mendelian Inheritance ◽  
Specific Gene ◽  
Paternal Genome ◽  
Genetic Conflict ◽  
Specific Gene Expression ◽  
Maternal Genome ◽  
Allele Specific ◽  
Parent Of Origin

AbstractGenetic conflict is considered a key driver in the evolution of new reproductive and sex determining systems. In particular, reproductive strategies with non-Mendelian inheritance, where parents do not contribute equally to the genetic makeup of their offspring. One of the most extraordinary examples of non-Mendelian inheritance is paternal genome elimination (PGE), a form of haplodiploidy which has evolved repeatedly across arthropods. Under PGE, males are diploid but only transmit maternally-inherited chromosomes to their offspring, while the paternal homologues are excluded from sperm. This asymmetric inheritance is thought to have evolved through an evolutionary arms race between paternal and maternal genomes over transmission to future generations. In several clades with PGE, such as the mealybugs (Hemiptera: Pseudococcidae), paternal chromosomes are not just eliminated from sperm, but also heterochromatinised early in development and thought to remain inactive. Such paternal genome silencing could alleviate genetic conflict between paternal alleles over transmission. However, it is unclear if paternal chromosomes are indeed genetically inert in both soma and germline. Here, we present a parent-of-origin allele-specific transcriptome analysis in male mealybugs. We show that expression is globally biased towards the maternal genome, but detect activity of paternal chromosomes in both somatic and reproductive tissues. Up to 70% of somatically-expressed genes are to some degree paternally-expressed. However, paternal genome expression is much more restricted in the testis, with only 20% of genes showing paternal contribution. Finally, we show that the patterns of parent-of-origin-specific gene expression are remarkably similar across genotypes and that those genes with biparental expression show elevated rates of molecular evolution. Our results provide the clearest example yet of genome-wide genomic imprinting (parent-of-origin specific gene expression) in insects. Furthermore, it enhances our understanding of PGE, which will aid future empirical tests of evolutionary theory regarding the origin of this unusual reproductive strategy.

scholarly journals Associations between imprinted gene expression in the placenta, human fetal growth and preeclampsia

2017 ◽  
Vol 13 (11) ◽  
pp. 20170643 ◽  
Author(s):  
Julian K. Christians ◽  
Katherine Leavey ◽  
Brian J. Cox
Keyword(s):  
Gene Expression ◽  
Genomic Imprinting ◽  
Fetal Growth ◽  
Placental Insufficiency ◽  
Imprinted Genes ◽  
Nutrient Allocation ◽  
Imprinted Gene ◽  
Expression Levels ◽  
Kinship Theory ◽  
Coordinated Regulation

Genomic imprinting is essential for normal placental and fetal growth. One theory to explain the evolution of imprinting is the kinship theory (KT), which predicts that genes that are paternally expressed will promote fetal growth, whereas maternally expressed genes will suppress growth. We investigated the expression of imprinted genes using microarray measurements of expression in term placentae. Correlations between birthweight and the expression levels of imprinted genes were more significant than for non-imprinted genes, but did not tend to be positive for paternally expressed genes and negative for maternally expressed genes. Imprinted genes were more dysregulated in preeclampsia (a disorder associated with placental insufficiency) than randomly selected genes, and we observed an excess of patterns of dysregulation in preeclampsia that would be expected to reduce nutrient allocation to the fetus, given the predictions of the KT. However, we found no evidence of coordinated regulation among these imprinted genes. A few imprinted genes have previously been shown to be associated with fetal growth and preeclampsia, and our results indicate that this is true for a broader set of imprinted genes.

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

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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