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Conserved imprinting associated with unique epigenetic signatures in the Arabidopsis genus

Nature Plants volume 2, Article number: 16145 (2016) Cite this article

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Abstract

In plants, imprinted gene expression occurs in endosperm seed tissue and is sometimes associated with differential DNA methylation between maternal and paternal alleles1. Imprinting is theorized to have been selected for because of conflict between parental genomes in offspring2, 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.

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Figure 1: Identification of imprinted genes in A. lyrata and comparison to A. thaliana.
Figure 2: A. lyrata endosperm exhibits an unusual methylation profile.
Figure 3: A. lyrata PEGs are associated with maternal allele CHG gene body hypermethylation.
Figure 4: Conserved PEGs exhibit distinct methylation profiles between species.

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Acknowledgements

M.G. thanks members of the NESCent working group on Testing Theories of Genomic Imprinting for many stimulating discussions. We thank O. Savolainen for kindly providing A. lyrata Karhumäki seeds, the Whitehead Institute Bioinformatics and Research Computing group for assistance, and P.R. Satyaki and B. Williams for comments on the manuscript. This research was funded by NSF grants MCB 1121952 and 1453459 to M.G. C.L.P. is supported by an NSF graduate research fellowship.

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Author notes

  1. Maja Klosinska and Colette L. Picard: These authors contributed equally to this work.

Authors and Affiliations

  1. Whitehead Institute for Biomedical Research, Cambridge, 02142, Massachusetts, USA

    Maja Klosinska, Colette L. Picard & Mary Gehring

  2. Computational and Systems Biology Graduate Program, Massachusetts Institute of Technology, Cambridge, 02139, Massachusetts, USA

    Colette L. Picard

  3. Department of Biology, Massachusetts Institute of Technology, Cambridge, 02139, Massachusetts, USA

    Mary Gehring

Authors
  1. Maja Klosinska
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  2. Colette L. Picard
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  3. Mary Gehring
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Contributions

M.G. conceived the project, M.K. performed experiments, C.L.P. developed and implemented computational analyses, M.K., C.L.P. and M.G. analysed data and wrote the paper.

Corresponding author

Correspondence to Mary Gehring.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Methods, Supplementary References, Supplementary Figure 1-10 (PDF 1904 kb)

Supplementary Table 1

mRNA-seq samples used in this study (XLSX 92 kb)

Supplementary Table 2

Read count and FPKM values for all genes in all samples (XLSX 24948 kb)

Supplementary Table 3

Endosperm imprinting statistics for all genes in all pairwise comparisons (XLSX 29931 kb)

Supplementary Table 4

Endosperm MEGs and PEGs and overlap with DMRs and Tes (XLSX 99 kb)

Supplementary Table 5

Bisulfite-seq samples used in this study and overall methylation data (XLSX 66 kb)

Supplementary Table 6

Features of DMRs and overlap with genes and TEs (XLSX 55 kb)

Supplementary Table 7

Homozygous SNPs identified between Kar and MN47 (XLSX 46 kb)

Supplementary Table 8

Primers used in this study (XLSX 14626 kb)

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Klosinska, M., Picard, C. & Gehring, M. Conserved imprinting associated with unique epigenetic signatures in the Arabidopsis genus. Nature Plants 2, 16145 (2016). https://doi.org/10.1038/nplants.2016.145

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