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

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.

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

Molecular Biology and Evolution ◽

10.1093/molbev/msab052 ◽

2021 ◽

Cited By ~ 1

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.

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

G3 Genes|Genome|Genetics ◽

10.1534/g3.117.042895 ◽

2017 ◽

Vol 7 (7) ◽

pp. 2227-2234 ◽

Cited By ~ 2

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.

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

Reproduction Fertility and Development ◽

10.1071/rd98056 ◽

1998 ◽

Vol 10 (8) ◽

pp. 593 ◽

Cited By ~ 17

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.

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The discovery and importance of genomic imprinting

eLife ◽

10.7554/elife.42368 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 13

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".

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