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A variably imprinted epiallele impacts seed development

Daniela Pignatta, View ORCID ProfileKatherine Novitzky, View ORCID ProfileP.R. V. Satyaki, View ORCID ProfileMary Gehring
doi: https://doi.org/10.1101/339036
Daniela Pignatta
1Whitehead Institute for Biomedical Research, Cambridge, MA, United States of America
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Katherine Novitzky
1Whitehead Institute for Biomedical Research, Cambridge, MA, United States of America
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P.R. V. Satyaki
1Whitehead Institute for Biomedical Research, Cambridge, MA, United States of America
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Mary Gehring
1Whitehead Institute for Biomedical Research, Cambridge, MA, United States of America
2Dept of Biology, Massachusetts Institute of Technology, Cambridge, MA, United States of America
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  • For correspondence: mgehring@wi.mit.edu
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Abstract

The contribution of epigenetic variation to phenotypic variation is unclear. Imprinted genes, because of their strong association with epigenetic modifications, represent an opportunity for the discovery of such phenomena. In mammals and flowering plants, a subset of genes are expressed from only one parental allele in a process called gene imprinting. Imprinting is associated with differential DNA methylation and chromatin modifications between parental alleles. In flowering plants imprinting occurs in a seed tissue – endosperm. Proper endosperm development is essential for the production of viable seeds. We previously showed that in Arabidopsis thaliana intraspecific imprinting variation is correlated with naturally occurring DNA methylation polymorphisms. Here, we investigated the mechanisms and function of allele-specific imprinting of the class IV homeodomain-Leucine zipper (HD-ZIP) transcription factor HDG3. In imprinted strains, HDG3 is expressed primarily from the methylated paternally inherited allele. We manipulated the methylation state of endogenous HDG3 in a non-imprinted strain and demonstrated that methylation of a proximal transposable element is sufficient to promote HDG3 expression and imprinting. Gain of HDG3 imprinting was associated with earlier endosperm cellularization and changes in seed weight. These results indicate that epigenetic variation alone is sufficient to explain imprinting variation and demonstrate that epialleles can underlie variation in seed development phenotypes.

Author Summary The contribution of genetic variation to phenotypic variation is well-established. By contrast, it is unknown how frequently epigenetic variation causes differences in organismal phenotypes. Epigenetic information is closely associated with but not encoded in the DNA sequence. In practice, it is challenging to disentangle genetic variation from epigenetic variation, as what appears to be epigenetic variation might have an underlying genetic basis. DNA methylation is one form of epigenetic information. HDG3 encodes an endosperm specific transcription factor that exists in two states in A. thaliana natural populations: methylated and expressed and hypomethylated and repressed. We show that pure epigenetic variation is sufficient to explain expression variation of HDG3 – a naturally lowly expressed allele can be switched to a higher expressed state by adding DNA methylation. We also show that expression of HDG3 in strains where it is normally hypomethylated and relatively repressed causes a seed development phenotype. These data indicate that naturally circulating epialleles have consequences for seed phenotypic variation.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted August 21, 2018.
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A variably imprinted epiallele impacts seed development
Daniela Pignatta, Katherine Novitzky, P.R. V. Satyaki, Mary Gehring
bioRxiv 339036; doi: https://doi.org/10.1101/339036
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A variably imprinted epiallele impacts seed development
Daniela Pignatta, Katherine Novitzky, P.R. V. Satyaki, Mary Gehring
bioRxiv 339036; doi: https://doi.org/10.1101/339036

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