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Conserved imprinting associated with unique epigenetic signatures in the Arabidopsis genus.

ABSTRACT: In plants, imprinted gene expression occurs in endosperm seed tissue and is sometimes associated with differential DNA methylation between maternal and paternal alleles(1). Imprinting is theorized to have been selected for because of conflict between parental genomes in offspring(2), but most studies of imprinting have been conducted in Arabidopsis thaliana, an inbred primarily self-fertilizing species that should have limited parental conflict. We examined embryo and endosperm allele-specific expression and DNA methylation genome-wide in the wild outcrossing species Arabidopsis lyrata. Here we show that the majority of A. lyrata imprinted genes also exhibit parentally biased expression in A. thaliana, suggesting that there is evolutionary conservation in gene imprinting. Surprisingly, we discovered substantial interspecies differences in methylation features associated with paternally expressed imprinted genes (PEGs). Unlike in A. thaliana, the maternal allele of many A. lyrata PEGs was hypermethylated in the CHG context. Increased maternal allele CHG methylation was associated with increased expression bias in favour of the paternal allele. We propose that CHG methylation maintains or reinforces repression of maternal alleles of PEGs. These data suggest that the genes subject to imprinting are largely conserved, but there is flexibility in the epigenetic mechanisms employed between closely related species to maintain monoallelic expression. This supports the idea that imprinting of specific genes is a functional phenomenon, and not simply a byproduct of seed epigenomic reprogramming.

SUBMITTER: Klosinska M

PROVIDER: S-EPMC5367468 | biostudies-literature | 2016 Sep

REPOSITORIES: biostudies-literature

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Conserved imprinting associated with unique epigenetic signatures in the Arabidopsis genus.

Klosinska Maja M Picard Colette L CL Gehring Mary M

Nature plants 20160919

In plants, imprinted gene expression occurs in endosperm seed tissue and is sometimes associated with differential DNA methylation between maternal and paternal alleles(1). Imprinting is theorized to have been selected for because of conflict between parental genomes in offspring(2), but most studies of imprinting have been conducted in Arabidopsis thaliana, an inbred primarily self-fertilizing species that should have limited parental conflict. We examined embryo and endosperm allele-specific e ...[more]

PMID: 27643534

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Project description:In plants, imprinted gene expression occurs in endosperm seed tissue and can be associated with differential DNA methylation between maternal and paternal alleles. Imprinting is theorized to have been selected for because of conflict between parental genomes in offspring, but most studies of imprinting have been conducted in Arabidopsis thaliana, an inbred primarily self-fertilizing species that should have limited parental conflict. We examined embryo and endosperm allele-specific expression and DNA methylation genome-wide in the wild outcrossing species Arabidopsis lyrata. Here we show that the majority of A. lyrata imprinted genes exhibit parentally-biased expression in A. thaliana, suggesting that there is evolutionary conservation in gene imprinting. Surprisingly, we discovered substantial interspecies differences in methylation features associated with paternally expressed imprinted genes (PEGs). Unlike A. thaliana, the maternal allele of many A. lyrata PEGs was hypermethylated in the CHG context. Increased maternal allele CHG methylation was associated with increased expression bias in favor of the paternal allele. We propose that CHG methylation maintains or reinforces repression of maternal alleles of PEGs. These data suggest that while the genes subject to imprinting are largely conserved, there is flexibility in the epigenetic mechanisms employed between closely related species to maintain monoallelic expression. This supports the idea that imprinting of specific genes is a functional phenomenon, and not simply a byproduct of seed epigenomic reprogramming. Examination of total gene expression, parent-of-origin specific allelic bias, or DNA methylation in embryo, endosperm, flower bud or seedcoat tissue from Arabidopsis lyrata accessions MN47 (MN), Karhumaki (Kar or KA), and crosses between them. High-throughput Illumina poly-A-selected mRNA-seq was used to identify imprinted genes in A. lyrata, and high-throughput Illumina whole genome bisulfite-sequencing was used to examine DNA methylation. mRNA-seq samples are designated MMxFF_T# where MM is the mother of the cross (either MN for MN47 or KA for Kar), FF is the father, T is the tissue (E for embryo, N for endosperm, S for seedcoat, b for buds), and # is the replicate numbers. Samples obtained from bisulfite sequencing follow the same naming but have suffix _BS and indicate cytosine methylation context (CpG, CHG, or CHH). For KAxMN bisulfite sequencing, additional files MMxFF_T#_BS_P_C.txt follow the same naming scheme but contain context-specific methylation data (C) from reads that mapped preferentially to one parent strain (P).

Project description:BACKGROUND: The epsilon proteobacteria, which include many important human pathogens, are presently recognized solely on the basis of their branching in rRNA trees. No unique molecular or biochemical characteristics specific for this group are known. RESULTS: Comparative analyses of proteins in the genomes of Wolinella succinogenes DSM 1740 and Campylobacter jejuni RM1221 against all available sequences have identified a large number of proteins that are unique to various epsilon proteobacteria (Campylobacterales), but whose homologs are not detected in other organisms. Of these proteins, 49 are uniquely found in nearly all sequenced epsilon-proteobacteria (viz. Helicobacter pylori (26695 and J99), H. hepaticus, C. jejuni (NCTC 11168, RM1221, HB93-13, 84-25, CF93-6, 260.94, 11168 and 81-176), C. lari, C. coli, C. upsaliensis, C. fetus, W. succinogenes DSM 1740 and Thiomicrospira denitrificans ATCC 33889), 11 are unique for the Wolinella and Helicobacter species (i.e. Helicobacteraceae family) and many others are specific for either some or all of the species within the Campylobacter genus. The primary sequences of many of these proteins are highly conserved and provide novel resources for diagnostics and therapeutics. We also report four conserved indels (i.e. inserts or deletions) in widely distributed proteins (viz. B subunit of exinuclease ABC, phenylalanyl-tRNA synthetase, RNA polymerase beta '-subunit and FtsH protein) that are specific for either all epsilon proteobacteria or different subgroups. In addition, a rare genetic event that caused fusion of the genes for the largest subunits of RNA polymerase (rpoB and rpoC) in Wolinella and Helicobacter is also described. The inter-relationships amongst Campylobacterales as deduced from these molecular signatures are in accordance with the phylogenetic trees based on the 16S rRNA and concatenated sequences for nine conserved proteins. CONCLUSION: These molecular signatures provide novel tools for identifying and circumscribing species from the Campylobacterales order and its subgroups in molecular terms. Although sequence information for these signatures is presently limited to Campylobacterales species, it is likely that many of them will also be found in other epsilon proteobacteria. Functional studies on these proteins and conserved indels should reveal novel biochemical or physiological characteristics that are unique to these groups of epsilon proteobacteria.

Dataset Information

Conserved imprinting associated with unique epigenetic signatures in the Arabidopsis genus.

Publications

Conserved imprinting associated with unique epigenetic signatures in the Arabidopsis genus.

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