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

Handle URI:
http://hdl.handle.net/10754/598206
Title:
Environmentally responsive genome-wide accumulation of de novo Arabidopsis thaliana mutations and epimutations
Authors:
Jiang, Caifu; Mithani, Aziz; Belfield, Eric J.; Mott, Richard; Hurst, Laurence D.; Harberd, Nicholas P.
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.
Citation:
Jiang C, Mithani A, Belfield EJ, Mott R, Hurst LD, et al. (2014) Environmentally responsive genome-wide accumulation of de novo Arabidopsis thaliana mutations and epimutations . Genome Res 24: 1821–1829. Available: http://dx.doi.org/10.1101/gr.177659.114.
Publisher:
Cold Spring Harbor Laboratory Press
Journal:
Genome Research
KAUST Grant Number:
KUK-I1-002-03
Issue Date:
14-Oct-2014
DOI:
10.1101/gr.177659.114
PubMed ID:
25314969
PubMed Central ID:
PMC4216923
Type:
Article
ISSN:
1088-9051; 1549-5469
Sponsors:
This study is based on work supported by King Abdullah University of Science and Technology (KAUST) award no. KUK-I1-002-03; the UK Biotechnological and Biological Sciences Research Council (grants BB/F020759/1 to N.P.H. and BB/F022697/1 to R.M.); St. John's College, Oxford (research support to N.P.H.); the National Natural Science Foundation of China (grant 31470350 to C.J.); LUMS Faculty Startup Grant; and the Wellcome Trust (Core grant 090532/Z/09/Z). We thank Hugh Dickinson (Department of Plant Sciences, University of Oxford, UK), Gilean McVean (Department of Statistics, University of Oxford, UK), and Detlef Weigel (Max Planck Institute for Developmental Biology, Tubingen, Germany) for constructive comments on preliminary versions of our manuscript.
Appears in Collections:
Publications Acknowledging KAUST Support

Full metadata record

DC FieldValue Language
dc.contributor.authorJiang, Caifuen
dc.contributor.authorMithani, Azizen
dc.contributor.authorBelfield, Eric J.en
dc.contributor.authorMott, Richarden
dc.contributor.authorHurst, Laurence D.en
dc.contributor.authorHarberd, Nicholas P.en
dc.date.accessioned2016-02-25T13:14:41Zen
dc.date.available2016-02-25T13:14:41Zen
dc.date.issued2014-10-14en
dc.identifier.citationJiang C, Mithani A, Belfield EJ, Mott R, Hurst LD, et al. (2014) Environmentally responsive genome-wide accumulation of de novo Arabidopsis thaliana mutations and epimutations . Genome Res 24: 1821–1829. Available: http://dx.doi.org/10.1101/gr.177659.114.en
dc.identifier.issn1088-9051en
dc.identifier.issn1549-5469en
dc.identifier.pmid25314969en
dc.identifier.doi10.1101/gr.177659.114en
dc.identifier.urihttp://hdl.handle.net/10754/598206en
dc.description.abstractEvolution 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.en
dc.description.sponsorshipThis study is based on work supported by King Abdullah University of Science and Technology (KAUST) award no. KUK-I1-002-03; the UK Biotechnological and Biological Sciences Research Council (grants BB/F020759/1 to N.P.H. and BB/F022697/1 to R.M.); St. John's College, Oxford (research support to N.P.H.); the National Natural Science Foundation of China (grant 31470350 to C.J.); LUMS Faculty Startup Grant; and the Wellcome Trust (Core grant 090532/Z/09/Z). We thank Hugh Dickinson (Department of Plant Sciences, University of Oxford, UK), Gilean McVean (Department of Statistics, University of Oxford, UK), and Detlef Weigel (Max Planck Institute for Developmental Biology, Tubingen, Germany) for constructive comments on preliminary versions of our manuscript.en
dc.publisherCold Spring Harbor Laboratory Pressen
dc.titleEnvironmentally responsive genome-wide accumulation of de novo Arabidopsis thaliana mutations and epimutationsen
dc.typeArticleen
dc.identifier.journalGenome Researchen
dc.identifier.pmcidPMC4216923en
dc.contributor.institutionState 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.en
dc.contributor.institutionDepartment of Biology, Syed Babar Ali School of Science and Engineering, Lahore University of Management Sciences (LUMS), DHA, Lahore 54792, Pakistan;en
dc.contributor.institutionDepartment of Plant Sciences, University of Oxford, Oxford OX1 3RB, United Kingdom;en
dc.contributor.institutionWellcome Trust Centre for Human Genetics, University of Oxford, Oxford OX3 7BN, United Kingdom;en
dc.contributor.institutionDepartment of Biology and Biochemistry, University of Bath, Bath BA2 7AY, United Kingdom.en
dc.contributor.institutionDepartment of Plant Sciences, University of Oxford, Oxford OX1 3RB, United Kingdom; nicholas.harberd@plants.ox.ac.uk cfjiang@cau.edu.cn.en
kaust.grant.numberKUK-I1-002-03en

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