Environmentally responsive genome-wide accumulation of de novo Arabidopsis thaliana mutations and epimutations

Caifu Jiang, Aziz Mithani, Eric J. Belfield, Richard Mott, Laurence D. Hurst, Nicholas P. Harberd

Research output: Contribution to journalArticlepeer-review

107 Citations (Scopus)

Abstract

Evolution is fueled by phenotypic diversity, which is in turn due to underlying heritable genetic (and potentially epigenetic) variation. While environmental factors are well known to influence the accumulation of novel variation in microorganisms and human cancer cells, the extent to which the natural environment influences the accumulation of novel variation in plants is relatively unknown. Here we use whole-genome and whole-methylome sequencing to test if a specific environmental stress (high-salinity soil) changes the frequency and molecular profile of accumulated mutations and epimutations (changes in cytosine methylation status) in mutation accumulation (MA) lineages of Arabidopsis thaliana. We first show that stressed lineages accumulate ∼100% more mutations, and that these mutations exhibit a distinctive molecular mutational spectrum (specific increases in relative frequency of transversion and insertion/deletion [indel] mutations). We next show that stressed lineages accumulate ∼45% more differentially methylated cytosine positions (DMPs) at CG sites (CG-DMPs) than controls, and also show that while many (∼75%) of these CG-DMPs are inherited, some can be lost in subsequent generations. Finally, we show that stress-associated CG-DMPs arise more frequently in genic than in nongenic regions of the genome. We suggest that commonly encountered natural environmental stresses can accelerate the accumulation and change the profiles of novel inherited variants in plants. Our findings are significant because stress exposure is common among plants in the wild, and they suggest that environmental factors may significantly alter the rates and patterns of incidence of the inherited novel variants that fuel plant evolution.

Original languageEnglish
Pages (from-to)1821-1829
Number of pages9
JournalGenome Research
Volume24
Issue number11
Early online date14 Oct 2014
DOIs
Publication statusPublished - 30 Nov 2014

ASJC Scopus subject areas

  • Genetics
  • Genetics(clinical)
  • Medicine(all)

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