Genomic evidence of paternal genome elimination in globular springtails

Paternal genome elimination (PGE) - a type of reproduction in which males inherit but fail to pass on the genome of their father - evolved independently in six to eight arthropod clades. Thousands of species, including several important for agriculture, reproduce via this mode of reproduction. While some of the clades are well established PGE systems, the evidence in globular springtails (Symphypleona) remains elusive, even though they represent the oldest and most species rich clade putatively reproducing via PGE. We sequenced genomic DNA from whole bodies of Allacma fusca males with sufficiently high fractions (31 - 38%) of sperm to conclusively confirm that all the sperm carry one parental haplotype only. Although it is suggestive that the single haplotype present in sperm is maternally inherited, definitive genetic proof of the parent of origin is still needed. The genomic approach we developed allows for detection of genotypic differences between germline and soma in all species with sufficiently high fraction of germline in their bodies. This opens new opportunities for scans for reproductive modes in small animals.

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A chimeric gene paternally instructs female sex determination in the haplodiploid wasp Nasonia

Science ◽

10.1126/science.abb8949 ◽

2020 ◽

Vol 370 (6520) ◽

pp. 1115-1118

Author(s):

Yuan Zou ◽

Elzemiek Geuverink ◽

Leo W. Beukeboom ◽

Eveline C. Verhulst ◽

Louis van de Zande

Keyword(s):

Sex Determination ◽

Genomic Rearrangements ◽

Coding Region ◽

Female Development ◽

Paternal Genome ◽

Zygotic Transcription ◽

Parent Of Origin ◽

Haploid Embryos ◽

Origin Effect ◽

Insect Sex

Various primary signals direct insect sex determination. In hymenopteran insects, the presence of a paternal genome is needed to initiate female development. When absent, uniparental haploid males develop. We molecularly and functionally identified the instructor sex-determination gene, wasp overruler of masculinization (wom), of the haplodiploid wasp Nasonia vitripennis. This gene contains a P53-like domain coding region and arose by gene duplication and genomic rearrangements. Maternal silencing of wom results in male development of haploid embryos. Upon fertilization, early zygotic transcription from the paternal wom allele is initiated, followed by a timely zygotic expression of transformer (tra), leading to female development. Wom is an instructor gene with a parent-of-origin effect in sex determination.

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Gamete imprinting: setting epigenetic patterns for the next generation

Reproduction Fertility and Development ◽

10.1071/rd05118 ◽

2006 ◽

Vol 18 (2) ◽

pp. 63 ◽

Cited By ~ 90

Author(s):

Jacquetta M. Trasler

Keyword(s):

Dna Methylation ◽

Genomic Dna ◽

Germ Line ◽

Imprinted Genes ◽

Specific Expression ◽

Placental Function ◽

Early Embryos ◽

Parent Of Origin ◽

Methylation Patterns ◽

Epigenetic Patterns

The acquisition of genomic DNA methylation patterns, including those important for development, begins in the germ line. In particular, imprinted genes are differentially marked in the developing male and female germ cells to ensure parent-of-origin-specific expression in the offspring. Abnormalities in imprints are associated with perturbations in growth, placental function, neurobehavioural processes and carcinogenesis. Based, for the most part, on data from the well-characterised mouse model, the present review will describe recent studies on the timing and mechanisms underlying the acquisition and maintenance of DNA methylation patterns in gametes and early embryos, as well as the consequences of altering these patterns.

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

10.1101/2020.04.27.063396 ◽

2020 ◽

Cited By ~ 1

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.

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A small RNA pathway mediates global allelic dosage in endosperm

10.1101/138750 ◽

2017 ◽

Cited By ~ 1

Author(s):

Robert M. Erdmann ◽

P.R. V. Satyaki ◽

Maja Klosinska ◽

Mary Gehring

Keyword(s):

Small Rna ◽

Small Rnas ◽

Inverse Relationship ◽

Paternal Genome ◽

Pol Iv ◽

Genome Wide ◽

A Genome ◽

Normal Seed ◽

Wide Scale ◽

Parent Of Origin

SummaryBalance between maternal and paternal genomes within the triploid endosperm is necessary for normal seed development. The majority of genes in Arabidopsis endosperm are expressed in a 2:1 maternal:paternal ratio, reflecting endosperm genomic DNA content. Here we find that the 2:1 transcriptional ratio is not, unexpectedly, a passive default but is actively regulated. We describe an inverse relationship between the parent-of-origin of small RNAs and mRNAs in endosperm on a genome-wide scale. Disruption of the Pol IV small RNA pathway causes the entire transcriptome to become more maternally biased. Furthermore, paternal inheritance of a RNA Pol IV mutation is sufficient to rescue seed abortion caused by excess paternal genome dosage. These results indicate that maintenance of the maternal:paternal transcriptome ratio in endosperm is an active process and reveal a function for RNA Pol IV in mediating the global transcriptional balance between maternally and paternally inherited genomes in endosperm.

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Autophagy and apoptosis: parent-of-origin genome-dependent mechanisms of cellular self-destruction

Open Biology ◽

10.1098/rsob.140027 ◽

2014 ◽

Vol 4 (6) ◽

pp. 140027 ◽

Cited By ~ 2

Author(s):

Grazyna E. Ptak ◽

Paola Toschi ◽

Antonella Fidanza ◽

Marta Czernik ◽

Federica Zacchini ◽

...

Keyword(s):

Cellular Response ◽

Resource Limitation ◽

Parental Origin ◽

Paternal Genome ◽

Cell Death Pathways ◽

Starting Point ◽

Mammalian Embryos ◽

Parent Of Origin ◽

The Difference ◽

Maternal Resources

Functional genomic imprinting is necessary for the transfer of maternal resources to mammalian embryos. Imprint-free embryos are unable to establish a viable placental vascular network necessary for the transfer of resources such as nutrients and oxygen. How the parental origin of inherited genes influences cellular response to resource limitation is currently not well understood. Because such limitations are initially realized by the placenta, we studied how maternal and paternal genomes influence the cellular self-destruction responses of this organ specifically. Here, we show that cellular autophagy is prevalent in androgenetic (i.e. having only a paternal genome) placentae, while apoptosis is prevalent in parthenogenetic (i.e. having only a maternal genome) placentae. Our findings indicate that the parental origin of inherited genes determines the placenta's cellular death pathway: autophagy for androgenotes and apoptosis for parthenogenotes. The difference in time of arrest between androgenotes and parthenogenotes can be attributed, at least in part, to their placentae's selective use of these two cell death pathways. We anticipate our findings to be a starting point for general studies on the parent-of-origin regulation of autophagy. Furthermore, our work opens the door to new studies on the involvement of autophagy in pathologies of pregnancy in which the restricted transfer of maternal resources is diagnosed.

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Modes of Reproduction and the Accumulation of Deleterious Mutations With Multiplicative Fitness Effects

Genetics ◽

10.1093/genetics/166.2.1093 ◽

2004 ◽

Vol 166 (2) ◽

pp. 1093-1104

Author(s):

Patsy Haccou ◽

Maria Victoria Schneider

Keyword(s):

Reproductive Mode ◽

Deleterious Mutations ◽

Paternal Genome ◽

Evolutionary Transitions ◽

Synergistic Interactions ◽

Fitness Effects ◽

Maintenance Of Sex ◽

Reproductive Modes ◽

Large Populations ◽

Lower Load

Abstract Mutational load depends not only on the number and nature of mutations but also on the reproductive mode. Traditionally, only a few specific reproductive modes are considered in the search of explanations for the maintenance of sex. There are, however, many alternatives. Including these may give radically different conclusions. The theory on deterministic deleterious mutations states that in large populations segregation and recombination may lead to a lower load of deleterious mutations, provided that there are synergistic interactions. Empirical research suggests that effects of deleterious mutations are often multiplicative. Such situations have largely been ignored in the literature, since recombination and segregation have no effect on mutation load in the absence of epistasis. However, this is true only when clonal reproduction and sexual reproduction with equal male and female ploidy are considered. We consider several alternative reproductive modes that are all known to occur in insects: arrhenotoky, paternal genome elimination, apomictic thelytoky, and automictic thelytoky with different cytological mechanisms to restore diploidy. We give a method that is based on probability-generating functions, which provides analytical and numerical results on the distributions of deleterious mutations. Using this, we show that segregation and recombination do make a difference. Furthermore, we prove that a modified form of Haldane’s principle holds more generally for thelytokous reproduction. We discuss the implications of our results for evolutionary transitions between different reproductive modes in insects. Since the strength of Muller’s ratchet is reduced considerably for several forms of automictic thelytoky, many of our results are expected to be also valid for initially small populations.

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Novel imprints in mouse blastocysts are predominantly DNA methylation independent

10.1101/2020.11.03.366948 ◽

2020 ◽

Author(s):

Laura Santini ◽

Florian Halbritter ◽

Fabian Titz-Teixeira ◽

Toru Suzuki ◽

Maki Asami ◽

...

Keyword(s):

Gene Expression ◽

Genomic Dna ◽

Bisulfite Sequencing ◽

Preimplantation Embryos ◽

Imprinted Genes ◽

Whole Genome ◽

Specific Expression ◽

Complex Program ◽

Genome Bisulfite Sequencing ◽

Parent Of Origin

ABSTRACTIn mammals, chromatin marks at imprinted genes are asymmetrically inherited to control parentally-biased gene expression. This control is thought predominantly to involve parent-specific differentially methylated regions (DMR) in genomic DNA. However, neither parent-of-origin-specific transcription nor DMRs have been comprehensively mapped. We here address this by integrating transcriptomic and epigenomic approaches in mouse preimplantation embryos (blastocysts). Transcriptome-analysis identified 71 genes expressed with previously unknown parent-of-origin-specific expression in blastocysts (nBiX: novel blastocyst-imprinted expression). Uniparental expression of nBiX genes disappeared soon after implantation. Micro-whole-genome bisulfite sequencing (μWGBS) of individual uniparental blastocysts detected 859 DMRs. Only 18% of nBiXs were associated with a DMR, whereas 60% were associated with parentally-biased H3K27me3. This suggests a major role for Polycomb-mediated imprinting in blastocysts. Five nBiX-clusters contained at least one known imprinted gene, and five novel clusters contained exclusively nBiX-genes. These data suggest a complex program of stage-specific imprinting involving different tiers of regulation.

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64 MACROGLOSSIA IN CLONED PIGLETS IS ASSOCIATED WITH HYPOMETHYLATION AT THE KCNQ-OT1 CpG ISLAND

Reproduction Fertility and Development ◽

10.1071/rdv23n1ab64 ◽

2011 ◽

Vol 23 (1) ◽

pp. 138

Author(s):

C. Li ◽

C. O'Gorman ◽

R. S. Prather ◽

J. A. Green ◽

K. D. Wells

Keyword(s):

Genomic Dna ◽

Cpg Island ◽

Methylation Status ◽

Differentially Methylated Region ◽

Sequencing Data ◽

Chi Square ◽

Cpg Sites ◽

Loss Of Imprinting ◽

Parent Of Origin ◽

Cloned Pig

Beckwith-Wiedeman Syndrome (BWS) is a loss of imprinting (LOI) condition that is associated with macroglossia, midline abdominal defects, and neonatal gigantism among other symptoms. These symptoms have also been seen in animals produced by SCNT. A common feature of BWS is the loss of methylation at the KCNQ-OT1 differentially methylated region. We hypothesised that this locus would show a similar LOI in cloned piglets that display macroglossia. DNA sequence for the porcine KCNQ-OT1 region was assembled in silico from public genome sequencing data. A CpG island was noted as being similarly located in the swine sequence as one which has been described for the human differentially differentiated region. Primers were designed to amplify a portion of this region from bisulfite converted genomic DNA. The amplimer spanned 32 CpG sites. To confirm imprinting status of KCNQ-OT1 in swine, a non-cloned pig was evaluated as to the methylation status across this region using DNA isolated from muscle (M) and the proportion hypermethylated was evaluated by chi-square tests. As seen in humans, this region was hypermethylated in approximately half (12 of 24, P = 1) of the cloned, sequenced amplimers. This observation is consistent with a parent of origin imprint at this locus. Next, 2 cloned piglets that appeared normal were assessed for methylation at KCNQ-OT1. M DNA from each of these animals was consistent with normal methylation at this locus, (7 of 16 and 8 of 18 cloned, sequenced amplimers, P > 0.40). Next, M DNA was isolated from 2 cloned litter mates where 1 piglet presented with macroglossia and the other did not. The non-presenting piglet’s M DNA was methylated in approximately half of the cloned sequenced amplimers (9 of 17, P = 0.67) whereas the macroglossia piglet M DNA was devoid of the methylated allele (0 of 14, P < 0.001). An additional pair of macroglossia presenting and non-presenting cloned littermates was identified. In this pair, the non-presenting piglet showed a normal distribution of methylation at this allele (8 of 19, P = 0.77) and the macroglossia piglet deviated somewhat from normal (6 of 20, P < 0.05). These 2 case studies are consistent with the conclusion that the appearance of macroglossia in cloned pigs may be associated with hypomethylation at KCNQ-OT1 and may model BSW. However, additional abnormal pigs will need to be assessed to completely characterise the LOI in cloned piglets.

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Ribosomal DNA, peroxidase and extensin variation in genomic DNA of Medicago laciniata (L.) Miller from Australia and Africa

Australian Journal of Agricultural Research ◽

10.1071/ar9941013 ◽

1994 ◽

Vol 45 (5) ◽

pp. 1013 ◽

Cited By ~ 1

Author(s):

RR Young ◽

ES Lagudah

Keyword(s):

Restriction Endonuclease ◽

South African ◽

Ribosomal Dna ◽

Genomic Dna ◽

Repeat Unit ◽

Cdna Clones ◽

Genotypic Differences ◽

Rdna Repeat ◽

Eastern Australia ◽

Rdna Repeat Unit

Fifty-four Medicago laciniata (L.) Miller accessions from diverse locations in eastern Australia, Africa and Israel were characterized for genotypic differences by restriction endonuclease cleavage of genomic DNA and probing with radio-labelled DNA sequences to detect restriction fragment length polymorphisms (RFLP). Digestion of the genomic DNA with the restriction endonuclease, Bam HI, and probing with the complete ribosomal DNA (rDNA) repeat unit of soybean (pGmrl) and its subclones revealed that the variable region in M. laciniata spans the Bam H1 sites of the intergenic spacer region between the 18s and 26s DNA. The length variation in the rDNA repeat unit clearly distinguished South African from Australian accessions. The rDNA variants from SA1847 (Morocco) and SA7750 (Tunisia) were the same as the Australian accessions and slightly larger than the rDNA spacer variant unique to SA3428 (Israel). When Eco R1 digested M. laciniata genomic DNA was probed with peroxidase and extensin cDNA clones, all Australian accessions were again characterized by the same RFLP genotype with further differentiation between African and Israeli accessions. An accession of unknown origin, SA3412, possessed the same RFLP genotype as the Australian accessions for all endonuclease and probe combinations. For the African accessions, differences in RFLP genotype were more frequent than differences in phenotype (leaflet laciniation and colour). However, of three South African accessions with the same RFLP genotype, SA26844, SA26847, and SA26848, SA26847 had more pronounced leaflet laciniation.

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