title: Environmentally responsive genome-wide accumulation of de novo Arabidopsis thaliana mutations and epimutations.
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.
authors.affiliation: State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing 100094, China; Department of Plant Sciences, University of Oxford, Oxford OX1 3RB, United Kingdom; nicholas.harberd@plants.ox.ac.uk cfjiang@cau.edu.cn.
authors.forename: Caifu
authors.initials: C
authors.lastname: Jiang
authors.affiliation: Department of Biology, Syed Babar Ali School of Science and Engineering, Lahore University of Management Sciences (LUMS), DHA, Lahore 54792, Pakistan;
authors.forename: Aziz
authors.initials: A
authors.lastname: Mithani
authors.affiliation: Department of Plant Sciences, University of Oxford, Oxford OX1 3RB, United Kingdom;
authors.forename: Eric J
authors.initials: EJ
authors.lastname: Belfield
authors.affiliation: Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford OX3 7BN, United Kingdom;
authors.forename: Richard
authors.initials: R
authors.lastname: Mott
authors.affiliation: Department of Biology and Biochemistry, University of Bath, Bath BA2 7AY, United Kingdom.
authors.forename: Laurence D
authors.initials: LD
authors.lastname: Hurst
authors.affiliation: Department of Plant Sciences, University of Oxford, Oxford OX1 3RB, United Kingdom; nicholas.harberd@plants.ox.ac.uk cfjiang@cau.edu.cn.
authors.forename: Nicholas P
authors.initials: NP
authors.lastname: Harberd
mesh_terms: D017360:Arabidopsis / Q000187:drug effects* / Q000235:genetics / Q000254:growth & development; D019175:DNA Methylation / Q000187:drug effects*; D004252:DNA Mutational Analysis / Q000379:methods; D018745:Genome, Plant / Q000235:genetics; D055106:Genome-Wide Association Study; D040582:Inheritance Patterns / Q000235:genetics; D008957:Models, Genetic; D009154:Mutation / Q000187:drug effects*; D054712:Salinity; D012639:Seeds / Q000187:drug effects / Q000235:genetics / Q000254:growth & development; D012965:Sodium Chloride / Q000494:pharmacology*; D013312:Stress, Physiological / Q000187:drug effects / Q000235:genetics
chemical_list: D012965:Sodium Chloride