scholarly journals Males That Silence Their Father’s Genes: Genomic Imprinting of a Complete Haploid Genome

2021 ◽  
Author(s):  
Andrés G de la Filia ◽  
Andrew J Mongue ◽  
Jennifer Dorrens ◽  
Hannah Lemon ◽  
Dominik R Laetsch ◽  
...  
Keyword(s):  
Genomic Imprinting ◽  
Reproductive Tract ◽  
Expression Patterns ◽  
Mendelian Inheritance ◽  
Specific Gene ◽  
Paternal Genome ◽  
Genetic Conflict ◽  
Maternal Genome ◽  
Allele Specific ◽  
Parent Of Origin

AbstractGenetic conflict is considered a key driver in the evolution of reproductive systems 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, while the paternally inherited homologues are excluded from sperm. This asymmetric inheritance is thought to have evolved through an evolutionary arms race between the paternal and maternal genomes over transmission to future generations. In several PGE clades, such as the mealybugs (Hemiptera: Pseudococcidae), paternal chromosomes are not only eliminated from sperm, but also heterochromatinized early in development and thought to remain inactive, which could result from genetic conflict between parental genomes. Here, we present a parent-of-origin allele-specific transcriptome analysis in male mealybugs showing that expression is globally biased toward the maternal genome. However, up to 70% of somatically expressed genes are to some degree paternally expressed, while paternal genome expression is much more restricted in the male reproductive tract, with only 20% of genes showing paternal contribution. We also show that parent-of-origin-specific gene expression patterns are remarkably similar across genotypes, and that genes with completely biparental expression show elevated rates of molecular evolution. Our results provide the clearest example yet of genome-wide genomic imprinting in insects and enhance our understanding of PGE, which will aid future empirical tests of evolutionary theory regarding the origin of this unusual reproductive strategy.

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 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.

Influence of epigenetic changes during oocyte growth on nuclear reprogramming after nuclear transfer

1998 ◽  
Vol 10 (8) ◽  
pp. 593 ◽  
Author(s):  
Tomohiro Kono
Keyword(s):  
Gene Expression ◽  
Genomic Imprinting ◽  
Epigenetic Mechanism ◽  
Specific Gene ◽  
Paternal Genome ◽  
Specific Expression ◽  
Oocyte Growth ◽  
Specific Gene Expression ◽  
Mammalian Embryos ◽  
Allele Specific

Genomic imprinting is the epigenetic mechanism that distinguishes whether the loci that are inherited from the maternal or paternal genome lead to parent-specific gene expression. The mechanism also regulates development in mammalian embryos. Genomic imprinting is established after implantation according to the specific markers that are imposed on the genome during gametogenesis; the allele-specific gene expression is then maintained throughout embryogenesis. The genomic imprinting markers are erased and renewed on an own-sex basis only in cells that differentiate into germline cells. This report shows that the epigenetic modifications that occur during oogenesis perform the crucial function of establishing the allele-specific expression of imprinted genes, and also suggests that the epigenetic DNA modification is related to the reprogramming and aberrant development seen in manipulated embryos.

scholarly journals 106 GENOMIC IMPRINTING OF IGF2R IN TISSUES OF BOVINE FETUSES GENERATED BY ARTIFICIAL INSEMINATION OR IN VITRO FERTILIZATION

2005 ◽  
Vol 17 (2) ◽  
pp. 204 ◽  
Author(s):  
S. Hiendleder ◽  
D. Bebbere ◽  
S. Bauersachs ◽  
M. Stojkovic ◽  
H. Wenigerkind ◽  
...  
Keyword(s):  
In Vitro Fertilization ◽  
Artificial Insemination ◽  
Expression Patterns ◽  
Allelic Expression ◽  
Paternal Allele ◽  
Specific Gene ◽  
Vitro Fertilization ◽  
Bovine Fetuses ◽  
Parent Of Origin

The insulin-like growth factor 2 receptor gene (IGF2R) is involved in fetal growth regulation. A study in sheep associated fetal overgrowth after in vitro embryo culture with abnormal DNA methylation and expression of IGF2R (Young et al. 2001 Nat. Genet. 27, 153–154). This suggested that abnormal IGF2R imprinting is a major cause of fetal overgrowth. To test this hypothesis in bovine fetuses, we developed a microsatellite marker for IGF2R from cDNA sequence data and screened 45 Day-80 fetuses generated in vivo, by artificial insemination (AI), or in vitro, by in vitro fertilization (IVF) procedures, for parent-of-origin-specific gene expression. A total of 17 fetuses were heterozygous, but available parental DNA samples showed that only 12 (8 AI, 4 IVF) allowed unambiguous discrimination of parental alleles. Parent-of-origin-specific allelic expression patterns indicated that bovine IGF2R was expressed predominantly from the maternal allele and thus imprinted in fetal heart, kidney, liver, lung, muscle, and cotyledon tissue. However, the relative amount of expression from the paternal allele was tissue-specific and ranged from 6.4 ± 0.8% in skeletal muscle up to 27.4 ± 0.9% in cotyledon (SPSS or 11.5, ANOVA, P < 0.001). Tissues that originated from the same germ layer showed similar allelic expression ratios whereas significantly different expression ratios (P < 0.05) were observed between tissues originating from different germ layers. Contrary to expectations from sheep data, there was no evidence for gross abnormalities in IGF2R imprinting in tissues from overgrown (n = 2) or normal sized (n = 2) IVF fetuses. However, relative paternal expression levels in several tissues showed significant relationships (P < 0.05–0.001) with growth parameters and pointed to subtle changes in paternal IGF2R expression in overgrown IVF fetuses. We thank W. Scholz and M. Weppert for excellent technical assistance.

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".

97 MAGNITUDE AND SPECIFICITY OF EFFECTS OF MATERNAL AND PATERNAL GENOMES ON THE FETO-PLACENTAL UNIT

2015 ◽  
Vol 27 (1) ◽  
pp. 141 ◽  
Author(s):  
R. Xiang ◽  
C. A. S. Estrella ◽  
C. J. Fitzsimmons ◽  
Z. A. Kruk ◽  
D. A. Thomsen ◽  
...  
Keyword(s):  
Umbilical Cord ◽  
Maternal Effects ◽  
Linear Models ◽  
Bos Taurus ◽  
Expression Patterns ◽  
Maternal Weight ◽  
Paternal Genome ◽  
Fetal Sex ◽  
Maternal Genome ◽  
Fetal Fluid

The placenta, a major determinant of fetal growth in eutherians, facilitates maternal-fetal cross talk and mediates programming of postnatal phenotype via genetic and epigenetic mechanisms. However, magnitude and specificity of effects of maternal and paternal genomes on placental and fetal phenotype and their relationships are unclear. Using an outbred bovine intra-species model with well-defined Bos taurus taurus and Bos taurus indicus maternal and paternal genetics, we generated purebred and reciprocal cross fetuses (Animal Ethics No. S-094-2005) to dissect and quantify effects of parental genomes, fetal sex, and nongenetic maternal effects (maternal weight and post-conception maternal weight gain) on 41 gross and histomorphological feto-placental parameters. Analysis of data from 73 fetuses recovered at midgestation (Day 153) with general linear models (Xiang et al. 2014 JBMR http://dx.doi.org/10.1002/jbmr.2263) using the GLM procedure of R version 22.14 (R Development Core Team, Vienna, Austria) revealed that maternal and paternal genome combined explained the highest proportion of variation (47.2–99.5%) in 30 investigated parameters with significant (P < 0.05–0.0001) models. Fetal sex accounted for up to 32.2% (P < 0.05–0.0001) and nongenetic maternal effects for up to 25.1% (P < 0.05–0.001) of variation in 11 and 14 parameters, respectively. Partitioning of parental (epi)genome variation showed that the maternal genome predominantly contributed to variation in gross (80.3–95.7%; P < 0.05–0.0001) and histomorphological (51.5–82.1%; P < 0.05–0.0001) placental parameters, fetal weight (54.1%; P < 0.0001), and fetal organ weights (43.7–73.1%; P < 0.05–0.0001), whereas the paternal genome predominantly contributed to fetal fluids weight (73.0%; P < 0.001), umbilical cord weight (73.9%; P < 0.05) and length (73.2%; P < 0.01), and placental (69.6%; P < 0.05) and umbilical cord (83.2%; P < 0.0001) efficiency. Our finding that the maternal genome determined placental phenotype (i.e. nutrient source) and the paternal genome determined umbilical cord and fetal fluid phenotype (i.e. nutrient flow) is in line with predicted expression patterns of genomic imprinting effects by both maternal-offspring coadaptation (Wolf and Hager 2006 PLoS Biol. 4, e380) and conflict-of-interest (Moore and Haig 1991 Trends Genet 7, 45–49) hypotheses in the feto-placental unit. Furthermore, there were 4 maternal genome determined relationships between placental weights and umbilical cord phenotype (P < 0.05–0.0001) and 28 paternal genome and/or fetal sex-determined relationships between fetus-, organ- and fetal fluid weights and umbilical cord phenotype (P < 0.05–0.0001). The finding of specific relationships between placenta and fetus merging in clusters differentiated by maternal and paternal genome effects suggests the existence of (epi)genetic-regulated morphological modules within the feto-placental unit.Funded by the JS Davies Bequest.

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.

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