Abundant small RNAs in the reproductive tissues of the honey bee, Apis mellifera, are a plausible mechanism for epigenetic inheritance and parental manipulation of gene expression

AbstractPolyandrous social insects such as the honey bee are prime candidates for parental manipulation of gene expression in offspring. Although there is good evidence for parent-of-origin effects in honey bees the epigenetic mechanisms that underlie these effects remain a mystery. Small RNA molecules such as miRNAs, piRNAs and siRNAs play important roles in transgenerational epigenetic inheritance and in the regulation of gene expression during development. Here we present the first characterisation of small RNAs present in honey bee reproductive tissues: ovaries, spermatheca, semen, fertilised and unfertilised eggs, and testes. We show that semen contains fewer piRNAs relative to eggs and ovaries, and that piRNAs and miRNAs which map antisense to genes involved in DNA regulation and developmental processes are differentially expressed between tissues. tRNA fragments are highly abundant in semen and have a similar profile to those seen in semen in other animals. Intriguingly we find abundant piRNAs that target the sex determination locus, suggesting that piRNAs may play a role in honey bee sex determination. We conclude that small RNAs play a fundamental role in honey bee gametogenesis and reproduction and provide a plausible mechanism for parent-of origin-effects on gene expression and reproductive physiology.

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A Search for Parent-of-Origin Effects on Honey Bee Gene Expression

G3 Genes|Genome|Genetics ◽

10.1534/g3.115.017814 ◽

2015 ◽

Vol 5 (8) ◽

pp. 1657-1662 ◽

Cited By ~ 21

Author(s):

Sarah D. Kocher ◽

Jennifer M. Tsuruda ◽

Joshua D. Gibson ◽

Christine M. Emore ◽

Miguel E. Arechavaleta-Velasco ◽

...

Keyword(s):

Gene Expression ◽

Honey Bee ◽

Parent Of Origin ◽

Origin Effects

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Nurse cell-derived small RNAs define paternal epigenetic inheritance in Arabidopsis

10.1101/2021.01.25.428150 ◽

2021 ◽

Author(s):

Jincheng Long ◽

James Walker ◽

Wenjing She ◽

Billy Aldridge ◽

Hongbo Gao ◽

...

Keyword(s):

Gene Expression ◽

Dna Methylation ◽

Small Rnas ◽

Nurse Cell ◽

De Novo ◽

Epigenetic Inheritance ◽

Genome Integrity ◽

Nurse Cells ◽

Male Germline ◽

Methylation Patterns

AbstractThe plant male germline undergoes DNA methylation reprogramming, which methylates genes de novo and thereby alters gene expression and facilitates meiosis. Why reprogramming is limited to the germline and how specific genes are chosen is unknown. Here, we demonstrate that genic methylation in the male germline, from meiocytes to sperm, is established by germline-specific siRNAs transcribed from transposons with imperfect sequence homology. These siRNAs are synthesized by meiocyte nurse cells (tapetum) via activity of the tapetum-specific chromatin remodeler CLASSY3. Remarkably, tapetal siRNAs govern germline methylation throughout the genome, including the inherited methylation patterns in sperm. Finally, we demonstrate that these nurse cell-derived siRNAs (niRNAs) silence germline transposons, thereby safeguarding genome integrity. Our results reveal that tapetal niRNAs are sufficient to reconstitute germline methylation patterns and drive extensive, functional methylation reprogramming analogous to piRNA-mediated reprogramming in animal germlines.

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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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Polymorphism and parent-of-origin effects on gene expression of CAST, leptin and DGAT1 in cattle

Meat Science ◽

10.1016/j.meatsci.2011.08.005 ◽

2012 ◽

Vol 90 (2) ◽

pp. 507-510 ◽

Cited By ~ 3

Author(s):

Simone Cristina Méo Niciura ◽

Adriana Mércia Guaratini Ibelli ◽

Gisele Veneroni Gouveia ◽

Juliana Gracielle Gonzaga Gromboni ◽

Marina Ibelli Pereira Rocha ◽

...

Keyword(s):

Gene Expression ◽

Parent Of Origin ◽

Origin Effects

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

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2020.0425 ◽

2021 ◽

Vol 376 (1826) ◽

Cited By ~ 1

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?’

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RNA Pol IV has antagonistic parent-of-origin effects on Arabidopsis endosperm

10.1101/2021.03.24.436774 ◽

2021 ◽

Author(s):

P.R. V. Satyaki ◽

Mary Gehring

Keyword(s):

Gene Expression ◽

Dna Methylation ◽

Regulatory System ◽

Small Interfering Rnas ◽

Pol Iv ◽

Gene Regulatory System ◽

Rna Polymerase Iv ◽

Parent Of Origin ◽

Origin Effects ◽

Maternal Resources

Gene expression in endosperm, a seed tissue that mediates transfer of maternal resources to offspring, is under complex epigenetic control. We show here that plant-specific RNA Polymerase IV mediates parental control of endosperm gene expression. Pol IV is required for the production of small interfering RNAs that typically direct DNA methylation. We compared small RNAs, DNA methylation, and mRNAs in A. thaliana endosperm from reciprocal heterozygotes produced by crossing wildtype plants to Pol IV mutants. We find that maternally and paternally acting Pol IV have divergent effects on endosperm with loss of maternal and paternal Pol IV impacting sRNAs and DNA methylation at different genomic sites. Strikingly, maternally and paternally-acting Pol IV have antagonistic impacts on gene expression at some loci, divergently promoting or repressing endosperm gene expression. Antagonistic parent-of13 origin effects have only rarely been described and are consistent with a gene regulatory system evolving under parental conflict.

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Multigenerational Regulation of the Caenorhabditis elegans Chromatin Landscape by Germline Small RNAs

Annual Review of Genetics ◽

10.1146/annurev-genet-112618-043505 ◽

2019 ◽

Vol 53 (1) ◽

pp. 289-311 ◽

Cited By ~ 10

Author(s):

Natasha E. Weiser ◽

John K. Kim

Keyword(s):

Gene Expression ◽

Caenorhabditis Elegans ◽

Small Rnas ◽

Model Organism ◽

Epigenetic Inheritance ◽

Small Interfering Rnas ◽

Transgenerational Epigenetic Inheritance ◽

C Elegans ◽

Small Noncoding Rnas ◽

Rna Pathways

In animals, small noncoding RNAs that are expressed in the germline and transmitted to progeny control gene expression to promote fertility. Germline-expressed small RNAs, including endogenous small interfering RNAs (endo-siRNAs) and Piwi-interacting RNAs (piRNAs), drive the repression of deleterious transcripts such as transposons, repetitive elements, and pseudogenes. Recent studies have highlighted an important role for small RNAs in transgenerational epigenetic inheritance via regulation of heritable chromatin marks; therefore, small RNAs are thought to convey an epigenetic memory of genomic self and nonself elements. Small RNA pathways are highly conserved in metazoans and have been best described for the model organism Caenorhabditis elegans. In this review, we describe the biogenesis, regulation, and function of C. elegans endo-siRNAs and piRNAs, along with recent insights into how these distinct pathways are integrated to collectively regulate germline gene expression, transgenerational epigenetic inheritance, and ultimately, animal fertility.

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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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