Abstract

Epigenetic variation has been proposed to facilitate adaptation to changing environments, but evidence that natural epialleles contribute to adaptive evolution has been lacking. Here we identify a retrotransposon, named “NMR19” (naturally occurring DNA methylation variation region 19), whose methylation and genomic location vary among Arabidopsis thaliana accessions. We classify NMR19 as NMR19-4 and NMR19-16 based on its location, and uncover NMR19-4 as an epiallele that controls leaf senescence by regulating the expression of PHEOPHYTIN PHEOPHORBIDE HYDROLASE (PPH). We find that the DNA methylation status of NMR19-4 is stably inherited and independent of genetic variation. In addition, further analysis indicates that DNA methylation of NMR19-4 correlates with local climates, implying that NMR19-4 is an environmentally associated epiallele. In summary, we discover a novel epiallele, and provide mechanistic insights into its origin and potential function in local climate adaptation.

Highlights

  • Epigenetic variation has been proposed to facilitate adaptation to changing environments, but evidence that natural epialleles contribute to adaptive evolution has been lacking

  • The methylation status of seven randomly selected loci was confirmed by Chop-PCR assays, suggesting that these naturally occurring differentially methylated regions (NMRs) are differentially methylated in different accessions and that wholegenome bisulfite-sequencing reliably identifies NMRs (Fig. 1a; Supplementary Fig. 1)

  • Identifying natural epigenetic variation and elucidating its role in plant adaptation is important to enhance our understanding of the epigenetic basis of biological diversity

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Summary

Introduction

Epigenetic variation has been proposed to facilitate adaptation to changing environments, but evidence that natural epialleles contribute to adaptive evolution has been lacking. DNA sequence variation is the primary evolutionary force underlying phenotypic variations, DNA methylation changes may affect the expression of genes and can contribute to trait variations that can be inherited to the generations[7] Such stably inherited epigenetic alleles are known as epialleles. Genome-wide DNA methylation analysis of plants identified thousands of naturally occurring differentially methylated regions (NMRs) in various species (e.g., Arabidopsis, soybean and maize) Some of these NMRs are under strong genetic control by cis or trans factors[27]. CHH methylation was found to increase with growth temperature, and a genome-wide association study revealed a strong association between CHH methylation variation and genetic variants[29] These results provide compelling evidence for plant adaption to local environments by genetically dependent epigenetic variations. Detailed functional characterization of such naturally occurring epialleles with a role in environmental adaptation has been limited

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