Conserved imprinting associated with unique epigenetic signatures in the Arabidopsis genus

  • Nature Plants 2, Article number: 16145 (2016)
  • doi:10.1038/nplants.2016.145
  • Download Citation
Published online:


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.

  • Subscribe to Nature Plants for full access:



Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.


  1. 1.

    Genomic imprinting: insights from plants. Annu. Rev. Genet. 47, 187–208 (2013).

  2. 2.

    & Parent-specific gene expression and the triploid endosperm. Am. Nat. 134, 147–155 (1989).

  3. 3.

    et al. Regulation of imprinted gene expression in Arabidopsis endosperm. Proc. Natl Acad. Sci. USA 108, 1755–1762 (2011).

  4. 4.

    et al. High-resolution analysis of parent-of-origin allelic expression in the Arabidopsis Endosperm. PLoS Genet. 7, e1002126 (2011).

  5. 5.

    , & Genomic analysis of parent-of-origin allelic expression in Arabidopsis thaliana seeds. PLoS ONE 6, e23687 (2011).

  6. 6.

    et al. Natural epigenetic polymorphisms lead to intraspecific variation in Arabidopsis gene imprinting. eLife e03198 (2014).

  7. 7.

    et al. A genome-wide survey of imprinted genes in rice seeds reveals imprinting primarily occurs in the endosperm. PLoS Genet. 7, e1002125 (2011).

  8. 8.

    et al. Parent-of-origin effects on gene expression and DNA methylation in the maize endosperm. Plant Cell 23, 4221–4233 (2012).

  9. 9.

    et al. Dynamic expression of imprinted genes associates with maternally controlled nutrient allocation during maize endosperm development. Plant Cell 25, 3212–3227 (2013).

  10. 10.

    et al. Extensive, clustered parental imprinting of protein-coding and noncoding RNAs in developing maize endosperm. Proc. Natl Acad. Sci. USA 108, 20042–20047 (2011).

  11. 11.

    et al. Genome-wide high resolution parental-specific DNA and histone methylation maps uncover patterns of imprinting regulation in maize. Genome Res. 24, 167–176 (2014).

  12. 12.

    , , & Parental epigenetic asymmetry of PRC2-mediated histone modifications in the Arabidopsis endosperm. EMBO J. 35, 1298–1311 (2016).

  13. 13.

    et al. The evolution of genomic imprinting: theories, predictions and empirical tests. Heredity 113, 119–128 (2014).

  14. 14.

    et al. Comprehensive analysis of imprinted genes in maize reveals allelic variation for imprinting and limited conservation with other species. Proc. Natl Acad. Sci. USA 110, 19639–19644 (2013).

  15. 15.

    , , & Hypothesis: selection of imprinted genes is driven by silencing deleterious gene activity in somatic tissues. Cold Spring Harb. Symp. Quant. Biol. 77, 23–29 (2012).

  16. 16.

    & Epigenetic reprogramming in plant sexual reproduction. Nat. Rev. Genet. 15, 613–624 (2014).

  17. 17.

    , , , & Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 107, 18724–18728 (2010).

  18. 18.

    & A catalogue of imprinted genes and parent-of-origin effects in humans and animals. Hum. Mol. Genet. 7, 1599–1609 (1998).

  19. 19.

    et al. Duplicated fie genes in maize: expression pattern and imprinting suggest distinct functions. Plant Cell 15, 425–438 (2003).

  20. 20.

    & RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat. Rev. Genet. 15, 394–408 (2014).

  21. 21.

    , & Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science 324, 1447–1451 (2009).

  22. 22.

    et al. Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science 337, 1360–1364 (2012).

  23. 23.

    et al. Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants. Cell 151, 167–180 (2012).

  24. 24.

    , , & Control of genic DNA methylation by a jmjC domain-containing protein in Arabidopsis thaliana. Science 319, 462–465 (2008).

  25. 25.

    , , & DNA methylation in an intron of the IBM1 histone demethylase gene stabilizes chromatin modification patterns. EMBO J. 31, 2981–2993 (2012).

  26. 26.

    et al. Hypomethylated pollen bypasses the interploidy hybridization barrier in Arabidopsis. Plant Cell 26, 3556–3568 (2014).

  27. 27.

    et al. Loss of the DNA methyltransferase MET1 induces H3K9 hypermethylation at PcG target genes and redistribution of H3K27 trimethylation to transposons in Arabidopsis thaliana. PLoS Genet. 8, e1003062 (2012).

  28. 28.

    et al. The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat. Genet. 43, 476–481 (2011).

  29. 29.

    et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).

  30. 30.

    & Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics 27, 1571–1572 (2011).

Download references


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.

Author information

Author notes

    • Maja Klosinska
    •  & Colette L. Picard

    These authors contributed equally to this work.


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

    • Maja Klosinska
    • , Colette L. Picard
    •  & Mary Gehring
  2. Computational and Systems Biology Graduate Program, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA

    • Colette L. Picard
  3. Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA

    • Mary Gehring


  1. Search for Maja Klosinska in:

  2. Search for Colette L. Picard in:

  3. Search for Mary Gehring in:


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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Mary Gehring.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    Supplementary Methods, Supplementary References, Supplementary Figure 1-10

Excel files

  1. 1.

    Supplementary Table 1

    mRNA-seq samples used in this study

  2. 2.

    Supplementary Table 2

    Read count and FPKM values for all genes in all samples

  3. 3.

    Supplementary Table 3

    Endosperm imprinting statistics for all genes in all pairwise comparisons

  4. 4.

    Supplementary Table 4

    Endosperm MEGs and PEGs and overlap with DMRs and Tes

  5. 5.

    Supplementary Table 5

    Bisulfite-seq samples used in this study and overall methylation data

  6. 6.

    Supplementary Table 6

    Features of DMRs and overlap with genes and TEs

  7. 7.

    Supplementary Table 7

    Homozygous SNPs identified between Kar and MN47

  8. 8.

    Supplementary Table 8

    Primers used in this study