Paternally expressed imprinted genes establish postzygotic hybridization barriers in Arabidopsis thaliana

Genomic imprinting is an epigenetic phenomenon causing parent-of-origin specific differential expression of maternally and paternally inherited alleles. While many imprinted genes have been identified in plants, the functional roles of most of them are unknown. In this study, we systematically examine the functional requirement of paternally expressed imprinted genes (PEGs) during seed development in Arabidopsis thaliana. While none of the 15 analyzed peg mutants has qualitative or quantitative abnormalities of seed development, we identify three PEGs that establish postzygotic hybridization barriers in the endosperm, revealing that PEGs have a major role as speciation genes in plants. Our work reveals that a subset of PEGs maintains functional roles in the inbreeding plant Arabidopsis that become evident upon deregulated expression.

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Canonical and Non-canonical Genomic Imprinting in Rodents

Frontiers in Cell and Developmental Biology ◽

10.3389/fcell.2021.713878 ◽

2021 ◽

Vol 9 ◽

Author(s):

Hisato Kobayashi

Keyword(s):

Dna Methylation ◽

Genomic Imprinting ◽

Mouse Genome ◽

Genetic Regulation ◽

Imprinted Genes ◽

Evolutionary Divergence ◽

Chromatin Modifications ◽

Allele Specific ◽

Epigenetic Phenomenon ◽

Parent Of Origin

Genomic imprinting is an epigenetic phenomenon that results in unequal expression of homologous maternal and paternal alleles. This process is initiated in the germline, and the parental epigenetic memories can be maintained following fertilization and induce further allele-specific transcription and chromatin modifications of single or multiple neighboring genes, known as imprinted genes. To date, more than 260 imprinted genes have been identified in the mouse genome, most of which are controlled by imprinted germline differentially methylated regions (gDMRs) that exhibit parent-of-origin specific DNA methylation, which is considered primary imprint. Recent studies provide evidence that a subset of gDMR-less, placenta-specific imprinted genes is controlled by maternal-derived histone modifications. To further understand DNA methylation-dependent (canonical) and -independent (non-canonical) imprints, this review summarizes the loci under the control of each type of imprinting in the mouse and compares them with the respective homologs in other rodents. Understanding epigenetic systems that differ among loci or species may provide new models for exploring genetic regulation and evolutionary divergence.

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Conserved Imprinted Genes between Intra-Subspecies and Inter-Subspecies Are Involved in Energy Metabolism and Seed Development in Rice

International Journal of Molecular Sciences ◽

10.3390/ijms21249618 ◽

2020 ◽

Vol 21 (24) ◽

pp. 9618

Author(s):

Lin Yang ◽

Feng Xing ◽

Qin He ◽

Muhammad Tahir ul Qamar ◽

Ling-Ling Chen ◽

...

Keyword(s):

Energy Metabolism ◽

Seed Development ◽

Genomic Imprinting ◽

Gene Editing ◽

Grain Filling ◽

Imprinted Genes ◽

Rt Pcr ◽

Reciprocal Crosses ◽

Reciprocal Hybrids ◽

Epigenetic Phenomenon

Genomic imprinting is an epigenetic phenomenon in which a subset of genes express dependent on the origin of their parents. In plants, it is unclear whether imprinted genes are conserved between subspecies in rice. Here we identified imprinted genes from embryo and endosperm 5–7 days after pollination from three pairs of reciprocal hybrids, including inter-subspecies, japonica intra-subspecies, and indica intra-subspecies reciprocal hybrids. A total of 914 imprinted genes, including 546 in inter-subspecies hybrids, 211 in japonica intra-subspecies hybrids, and 286 in indica intra-subspecies hybrids. In general, the number of maternally expressed genes (MEGs) is more than paternally expressed genes (PEGs). Moreover, imprinted genes tend to be in mini clusters. The number of shared genes by R9N (reciprocal crosses between 9311 and Nipponbare) and R9Z (reciprocal crosses between 9311 and Zhenshan 97), R9N and RZN (reciprocal crosses between Zhonghua11 and Nipponbare), R9Z and RZN was 72, 46, and 16. These genes frequently involved in energy metabolism and seed development. Five imprinted genes (Os01g0151700, Os07g0103100, Os10g0340600, Os11g0679700, and Os12g0632800) are commonly detected in all three pairs of reciprocal hybrids and were validated by RT-PCR sequencing. Gene editing of two imprinted genes revealed that both genes conferred grain filling. Moreover, 15 and 27 imprinted genes with diverse functions in rice were shared with Arabidopsis and maize, respectively. This study provided valuable resources for identification of imprinting genes in rice or even in cereals.

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Imprinting analysis in the Acrodysplasia region of mouse chromosome 12

Bioscience Reports ◽

10.1042/bsr20090009 ◽

2009 ◽

Vol 30 (2) ◽

pp. 119-124 ◽

Cited By ~ 1

Author(s):

Erin N. McMurray ◽

Eric D. Rogers ◽

Jennifer V. Schmidt

Keyword(s):

Mouse Chromosome ◽

Genomic Imprinting ◽

Critical Region ◽

The Other ◽

Chromosome 12 ◽

Imprinted Genes ◽

Skeletal Abnormalities ◽

Mouse Mutation ◽

Parent Of Origin

The insertional mouse mutation Adp (Acrodysplasia) confers a parent-of-origin developmental phenotype, with animals inheriting the mutation from their father showing skeletal abnormalities, whereas those inheriting the mutation from their mother are normal. This parental-specific phenotype, along with mapping of the insertion to a region of chromosome 12 proposed to contain imprinted genes, suggested that disruption of genomic imprinting might underlie the Adp phenotype. Genomic imprinting is the process by which autosomal genes are epigenetically silenced on one of the two parental alleles; imprinting mutation phenotypes manifest after inheritance from one parent but not the other. Imprinted genes typically occur in dense clusters that contain few non-imprinted genes and therefore representative genes from the Adp critical region could be assayed to identify any imprinted domains. None of the genes analysed were found to be imprinted, however, suggesting that other explanations for the Adp phenotype must be considered.

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Imprinted small RNA genes

Biological Chemistry ◽

10.1515/bc.2004.118 ◽

2004 ◽

Vol 385 (10) ◽

pp. 905-911 ◽

Cited By ~ 18

Author(s):

Hervé Seitz ◽

Hélène Royo ◽

Shau-Ping Lin ◽

Neil Youngson ◽

Anne C. Ferguson-Smith ◽

...

Keyword(s):

Genomic Imprinting ◽

Gene Families ◽

Evolutionary Significance ◽

Microrna Gene ◽

Non Coding Rna ◽

Epigenetic Phenomenon ◽

Parent Of Origin ◽

Microrna Genes ◽

Rna Genes

Abstract Genomic imprinting is an epigenetic phenomenon that results in differential expression of both alleles, depending on their parent of origin. We have recently identified many imprinted small non-coding RNA genes belonging to the C/D RNA and microRNA gene families, both of which are usually known to play key roles in post-transcriptional metabolism of specific genes (e.g. C/D RNAs guide ribose methylation of target RNAs while microRNAs elicit either translational repression or RNA interference). Although the functional and evolutionary significance of this association between C/D RNA genes, microRNA genes and genomic imprinting is still highly elusive, these observations provide a framework for further analysis of the potential role of small non-coding RNAs in epigenetic control.

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Identification of imprinted genes subject to parent-of-origin specific expression in Arabidopsis thaliana seeds

BMC Plant Biology ◽

10.1186/1471-2229-11-113 ◽

2011 ◽

Vol 11 (1) ◽

pp. 113 ◽

Cited By ~ 38

Author(s):

Peter C McKeown ◽

Sylvia Laouielle-Duprat ◽

Pjotr Prins ◽

Philip Wolff ◽

Marc W Schmid ◽

...

Keyword(s):

Arabidopsis Thaliana ◽

Imprinted Genes ◽

Specific Expression ◽

Parent Of Origin

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Evolution and function of genomic imprinting in plants

Genes & Development ◽

10.1101/gad.269902.115 ◽

2015 ◽

Vol 29 (24) ◽

pp. 2517-2531 ◽

Cited By ~ 2

Author(s):

Jessica A. Rodrigues ◽

Daniel Zilberman

Keyword(s):

Genomic Imprinting ◽

Histone Methylation ◽

Biological Significance ◽

Flowering Plants ◽

Evolutionary Forces ◽

Plant Genes ◽

Epigenetic Phenomenon ◽

Parent Of Origin ◽

And Function ◽

Genome Scale

Genomic imprinting, an inherently epigenetic phenomenon defined by parent of origin-dependent gene expression, is observed in mammals and flowering plants. Genome-scale surveys of imprinted expression and the underlying differential epigenetic marks have led to the discovery of hundreds of imprinted plant genes and confirmed DNA and histone methylation as key regulators of plant imprinting. However, the biological roles of the vast majority of imprinted plant genes are unknown, and the evolutionary forces shaping plant imprinting remain rather opaque. Here, we review the mechanisms of plant genomic imprinting and discuss theories of imprinting evolution and biological significance in light of recent findings.

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Parent-of-origin effects on seed development in Arabidopsis thaliana

Development ◽

10.1242/dev.125.17.3329 ◽

1998 ◽

Vol 125 (17) ◽

pp. 3329-3341 ◽

Cited By ~ 20

Author(s):

R.J. Scott ◽

M. Spielman ◽

J. Bailey ◽

H.G. Dickinson

Keyword(s):

Arabidopsis Thaliana ◽

Seed Development ◽

Endosperm Development ◽

Double Dose ◽

Extreme Phenotypes ◽

Interploidy Crosses ◽

Parent Of Origin ◽

Viable Seeds ◽

Different Doses ◽

Triple Dose

Many flowering plants are polyploid, but crosses between individuals of different ploidies produce seeds that develop abnormally and usually abort. Often, seeds from interploidy crosses develop differently depending on whether the mother or father contributes more chromosome sets, suggesting that maternal and paternal genomes are not functionally equivalent. Here we present the first cytological investigation of seed development following interploidy crosses in Arabidopsis thaliana. We find that crosses between diploid and tetraploid plants in either direction, resulting in double the normal dose of maternal or paternal genomes in the seed, produce viable seeds containing triploid embryos. However, development of the seed and in particular the endosperm is abnormal, with maternal and paternal genomic excess producing complementary phenotypes. A double dose of maternal genomes with respect to paternal contribution inhibits endosperm development and ultimately produces a smaller embryo. In contrast, a double dose of paternal genomes promotes growth of the endosperm and embryo. Reciprocal crosses between diploids and hexaploids, resulting in a triple dose of maternal or paternal genomes, produce seeds that begin development with similar but more extreme phenotypes than those with a double dose, but these invariably abort. One explanation of our observations is that seeds with maternal or paternal excess contain different doses of maternally or paternally expressed imprinted loci affecting endosperm development.

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Genomic imprinting in marsupial placentation

Reproduction ◽

10.1530/rep-08-0264 ◽

2008 ◽

Vol 136 (5) ◽

pp. 523-531 ◽

Cited By ~ 38

Author(s):

Marilyn B Renfree ◽

Eleanor I Ager ◽

Geoff Shaw ◽

Andrew J Pask

Keyword(s):

Genomic Imprinting ◽

Direct Evidence ◽

Egg Laying ◽

Common Mechanism ◽

Parental Conflict ◽

Imprinted Genes ◽

Nutrient Transfer ◽

Epigenetic Phenomenon ◽

Selection For ◽

Shed Light

Genomic imprinting is a widespread epigenetic phenomenon in eutherian mammals, which regulates many aspects of growth and development. Parental conflict over the degree of maternal nutrient transfer is the favoured hypothesis for the evolution of imprinting. Marsupials, like eutherian mammals, are viviparous but deliver an altricial young after a short gestation supported by a fully functional placenta, so can shed light on the evolution and time of acquisition of genomic imprinting. All orthologues of eutherian imprinted genes examined have a conserved expression in the marsupial placenta regardless of their imprint status. Differentially methylated regions (DMRs) are the most common mechanism controlling genomic imprinting in eutherian mammals, but none were found in the marsupial imprinted orthologues of IGF2 receptor (IGF2R), INS or mesoderm-specific transcript (MEST). Instead, histone modification appears to be the mechanism used to silence these genes. At least three genes in marsupials have DMRs: H19, IGF2 and PEG10. PEG10 is particularly interesting as it is derived from a retrotransposon, providing the first direct evidence that retrotransposon insertion can drive the evolution of an imprinted region and of a DMR in mammals. The insertion occurred after the prototherian–therian mammal divergence, suggesting that there may have been strong selection for the retention of imprinted regions that arose during the evolution of placentation. There is currently no evidence for genomic imprinting in the egg-laying monotreme mammals. However, since these mammals do have a short-lived placenta, imprinting appears to be correlated with viviparity but not placentation.

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Deletion of the Imprinted Phlda2 Gene Increases Placental Passive Permeability in the Mouse

Genes ◽

10.3390/genes12050639 ◽

2021 ◽

Vol 12 (5) ◽

pp. 639

Author(s):

Emily Angiolini ◽

Ionel Sandovici ◽

Philip M. Coan ◽

Graham J. Burton ◽

Colin P. Sibley ◽

...

Keyword(s):

Fetal Growth ◽

Placental Transfer ◽

Structural Characteristics ◽

Imprinted Genes ◽

Passive Permeability ◽

Small Set ◽

Epigenetic Phenomenon ◽

Catch Up ◽

Parent Of Origin

Genomic imprinting, an epigenetic phenomenon that causes the expression of a small set of genes in a parent-of-origin-specific manner, is thought to have co-evolved with placentation. Many imprinted genes are expressed in the placenta, where they play diverse roles related to development and nutrient supply function. However, only a small number of imprinted genes have been functionally tested for a role in nutrient transfer capacity in relation to the structural characteristics of the exchange labyrinthine zone. Here, we examine the transfer capacity in a mouse model deficient for the maternally expressed Phlda2 gene, which results in placental overgrowth and a transient reduction in fetal growth. Using stereology, we show that the morphology of the labyrinthine zone in Phlda2−/+ mutants is normal at E16 and E19. In vivo placental transfer of radiolabeled solutes 14C-methyl-D-glucose and 14C-MeAIB remains unaffected at both gestational time points. However, placental passive permeability, as measured using two inert hydrophilic solutes (14C-mannitol; 14C-inulin), is significantly higher in mutants. Importantly, this increase in passive permeability is associated with fetal catch-up growth. Our findings uncover a key role played by the imprinted Phlda2 gene in modifying placental passive permeability that may be important for determining fetal growth.

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Genomic imprinted genes in reciprocal hybrid endosperm of Brassica napus

BMC Plant Biology ◽

10.1186/s12870-021-02908-8 ◽

2021 ◽

Vol 21 (1) ◽

Author(s):

Hao Rong ◽

Wenjing Yang ◽

Haotian Zhu ◽

Bo Jiang ◽

Jinjin Jiang ◽

...

Keyword(s):

Brassica Napus ◽

Genomic Imprinting ◽

Castor Bean ◽

Imprinted Genes ◽

Reciprocal Hybrid ◽

Rna Seq ◽

Flower Bud ◽

Gene Imprinting ◽

Parent Of Origin ◽

Stem Leaf

Abstract Background Genomic imprinting results in the expression of parent-of-origin-specific alleles in the offspring. Brassica napus is an oil crop with research values in polyploidization. Identification of imprinted genes in B. napus will enrich the knowledge of genomic imprinting in dicotyledon plants. Results In this study, we performed reciprocal crosses between B. napus L. cultivars Yangyou 6 (Y6) and Zhongshuang 11 (ZS11) to collect endosperm at 20 and 25 days after pollination (DAP) for RNA-seq. In total, we identified 297 imprinted genes, including 283 maternal expressed genes (MEGs) and 14 paternal expressed genes (PEGs) according to the SNPs between Y6 and ZS11. Only 36 genes (35 MEGs and 1 PEG) were continuously imprinted in 20 and 25 DAP endosperm. We found 15, 2, 5, 3, 10, and 25 imprinted genes in this study were also imprinted in Arabidopsis, rice, castor bean, maize, B. rapa, and other B. napus lines, respectively. Only 26 imprinted genes were specifically expressed in endosperm, while other genes were also expressed in root, stem, leaf and flower bud of B. napus. A total of 109 imprinted genes were clustered on rapeseed chromosomes. We found the LTR/Copia transposable elements (TEs) were most enriched in both upstream and downstream of the imprinted genes, and the TEs enriched around imprinted genes were more than non-imprinted genes. Moreover, the expression of 5 AGLs and 6 pectin-related genes in hybrid endosperm were significantly changed comparing with that in parent endosperm. Conclusion This research provided a comprehensive identification of imprinted genes in B. napus, and enriched the gene imprinting in dicotyledon plants, which would be useful in further researches on how gene imprinting regulates seed development.

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