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

Genome Research

Volumn 24, Issue 11, 2014, Pages 1821-1829

  Jiang, Caifu ^a,b   Mithani, Aziz ^c   Belfield, Eric J ^b   Mott, Richard ^d   Hurst, Laurence D ^e   Harberd, Nicholas P ^b  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c LAHORE UNIVERSITY OF MANAGEMENT SCIENCES   (Pakistan)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e University of Bath   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSINE; SODIUM CHLORIDE;

ARABIDOPSIS THALIANA; ARTICLE; CONTROLLED STUDY; DNA METHYLATION; DNA SEQUENCE; ENVIRONMENTAL FACTOR; ENVIRONMENTAL STRESS; EPIMUTATION; GENE MUTATION; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC VARIABILITY; INDEL MUTATION; NONHUMAN; PLANT EVOLUTION; PLANT GENETICS; PLANT GENOME; PRIORITY JOURNAL; SALINITY; SALT STRESS; ARABIDOPSIS; BIOLOGICAL MODEL; DRUG EFFECTS; GENETICS; GROWTH, DEVELOPMENT AND AGING; INHERITANCE; MUTATION; NUCLEOTIDE SEQUENCE; PHYSIOLOGICAL STRESS; PLANT SEED; PROCEDURES;

ARABIDOPSIS THALIANA;

ARABIDOPSIS; DNA METHYLATION; DNA MUTATIONAL ANALYSIS; GENOME, PLANT; GENOME-WIDE ASSOCIATION STUDY; INHERITANCE PATTERNS; MODELS, GENETIC; MUTATION; SALINITY; SEEDS; SODIUM CHLORIDE; STRESS, PHYSIOLOGICAL;

EID: 84924405710     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.177659.114     Document Type: Article

References (56)

1. Agrawal AF, Wang AD. 2008. Increased transmission of mutations by low-condition females: evidence for condition-dependent DNA repair. PLoS Biol 6: e30.
2. Al Mamun AA, Lombardo M-J, Shee C, Lisewski AM, Gonzalez C, Lin D, Nehring RB, Saint-Ruf C, Gibson JL, Frisch RL, et al. 2012. Identity and function of a large gene network underlying mutagenic repair of DNA breaks. Science 338: 1344-1348.
3. The Arabidopsis Genome Initiative. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815.
4. Atwell S, Huang YS, Vilhjalmsson BJ, Willems G, Horton M, Li Y, Meng D, Platt A, Hu TT, Jiang R, et al. 2010. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465: 627-631.
5. Baer CF, Miyamoto MM, Denver DR. 2007. Mutation rate variation in multicellular eukaryotes: causes and consequences. Nat Rev Genet 8: 619-631.
6. Baxter I, Brazelton JN, Yu DN, Huang YS, Lahner B, Yakubova E, Li Y, Bergelson J, Borevitz JO, Nordborg M, et al. 2010. A coastal cline in sodium accumulation in Arabidopsis thaliana is driven by natural variation of the sodium transporter AtHKT1;1. PLoS Genet 6: e1001193.
7. Becker C, Hagmann J, Muller J, Koenig D, Stegle O, Borgwardt K, Weigel D. 2011. Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 480: 245-249.
8. Belfield EJ, Gan X, Mithani A, Brown C, Jiang C, Franklin K, Alvey E, Wibowo A, Jung M, Bailey K, et al. 2012. Genome-wide analysis of mutations in mutant lineages selected following fast-neutron irradiation mutagenesis of Arabidopsis thaliana. Genome Res 22: 1306-1315.
9. Benjamini Y, Hochberg Y 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57: 289-300.
10. Bindra RS, Crosby ME, Glazer PM. 2007. Regulation of DNA repair in hypoxic cancer cells. Cancer Metastasis Rev 26: 249-260.
11. Bjedov I, Tenaillon O, Gerard B, Souza V, Denamur E, Radman M, Taddei F, Matic I. 2003. Stress-induced mutagenesis in bacteria. Science 300: 1404-1409.
12. Bock C. 2012. Analysing and interpreting DNA methylation data. Nat Rev Genet 6: 705-719.
13. Cao X, Jacobsen SE. 2002. Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes. Proc Natl Acad Sci 4: 16491-16498.
14. Cao J, Schneeberger K, Ossowski S, Gunther T, Bender S, Fitz J, Koenig D, Lanz C, Stegle O, Lippert C, et al. 2011. Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat Genet 43: 956-963.
15. Chan SW, Henderson IR, Jacobsen SE. 2005. Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Genet 6: 351-360.
16. Chinnusamy V, Zhu JK. 2009. Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12: 133-139.
17. Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, Pradhan S, Nelson SF, Pellegrini M, Jacobsen SE. 2008. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452: 215-219.
18. Darwin C. 1859. The origin of species by means of natural selection. John Murray, London.
19. Dowen RH, Pelizzola M, Schmitz RJ, Lister R, Dowen JM, Nery JR, Dixon JE, Ecker JR. 2012. Widespread dynamic DNA methylation in response to biotic stress. Proc Natl Acad Sci 109: E2183-E2191.
20. Easterling DR, Meehl GA, Parmesan C, Changnon SA, Karl TR, Mearns LO. 2000. Climate extremes: observations, modeling, and impacts. Science 289: 2068-2074.
21. Gan X, Stegle O, Behr J, Steffen JG, Drewe P, Hildebrand KL, Lyngsoe R, Schultheiss SJ, Osborne EJ, Sreedharan VT, et al. 2011. Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477: 419-423.
22. Gelfman S, Cohen N, Yearim A, Ast G. 2013. DNA-methylation effect on cotranscriptional splicing is dependent on GC architecture of the exon-intron structure. Genome Res 23: 789-799.
23. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ. 2000. Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51: 463-499.
24. Hoffman PD, Leonard JM, Lindberg GE, Bollmann SR, Hays JB. 2004. Rapid accumulation of mutations during seed-to-seed propagation of mismatch-repair-defective Arabidopsis. Genes Dev 18: 2676-2685.
25. Jacobsen SE, Meyerowitz EM. 1997. Hypermethylated SUPERMAN epigenetic alleles in Arabidopsis. Science 277: 1100-1103.
26. Jiang C, Mithani A, Gan X, Belfield EJ, Klingler JP, Zhu JK, Ragoussis J, Mott R, Harberd NP. 2011. Regenerant Arabidopsis lineages display a distinct genome-wide spectrum of mutations conferring variant phenotypes. Curr Biol 21: 1385-1390.
27. Jiang C, Belfield EJ, Mithani A, Visscher A, Ragoussis J, Mott R, Smith JAC, Harberd NP. 2012. ROS-mediated vascular homeostatic control of root-to-shoot soil Na delivery in Arabidopsis. EMBO J 31: 4359-4370.
28. Jiang C, Belfield EJ, Cao Y, Smith JAC, Harberd NP. 2013. An Arabidopsis soil-salinity-tolerance mutation confers ethylene-mediated enhancement of sodium/potassium homeostasis. Plant Cell 25: 3535-3552.
29. Kankel MW, Ramsey DE, Stokes TL, Flowers SK, Haag JR, Jeddeloh JA, Riddle NC, Verbsky ML, Richards EJ. 2003. Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163: 1109-1122.
30. Krueger F, Andrews SR. 2011. Bismark: a flexible aligner and methylation caller for bisulfite-Seq applications. Bioinformatics 27: 1571-1572.
31. Laird W. 2010. Principles and challenges of genome-wide DNA methylation analysis. Nat Rev Genet 11: 191-203.
32. Liu C, Lu F, Cui X, Cao X. 2010. Histone methylation in higher plants. Annu Rev Plant Biol 61: 395-420.
33. Lunter G, Goodson M. 2011. Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res 21: 936-939.
34. Lynch M. 2010. Evolution of the mutation rate. Trends Genet 26: 345-352.
35. Matsuba C, Ostrow DG, Saloman MP, Tolani A, Baer CF. 2013. Temperature, stress and spontaneous mutations in Caenorhabditis briggsae and Caenorhabditis elegans. Biol Lett 9: 20120334.
36. Mitchell-Olds T, Schmitt J. 2006. Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis. Nature 441: 947-952.
37. Mittler R. 2006. Abiotic stress, the field environment and stress combination. Trends Plant Sci 11: 15-19.
38. Munns R, Tester M. 2008. Mechanisms of salinity tolerance. Annu Rev Plant Biol 59: 651-681.
39. Nordborg M, Weigel D. 2008. Next-generation genetics in plants. Nature 456: 720-723.
40. Ossowski S, Schneeberger K, Lucas-Lledo JI, Warthmann N, Clark RM, Shaw RG, Weigel D, Lynch M. 2010. The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327: 92-94.
41. Parmesan C, Yohe G. 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421: 37-42.
42. Rando OJ, Verstrepen KJ. 2007. Timescales of genetic and epigenetic inheritance. Cell 128: 655-668.
43. Ren ZH, Gao JP, Li LG, Cai XL, Huang W, Chao DY, Zhu MZ, Wang ZY, Luan S, Lin HX. 2005. A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat Genet 37: 1141-1146.
44. Richards EJ. 2008. Population epigenetics. Curr Opin Genet Dev 18: 221-226.
45. Rus A, Yokoi S, Sharkhuu A, Reddy M, Lee BH, Matsumoto TK, Koiwa H, Zhu JK, Bressan RA, Hasegawa PM. 2001. AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots. Proc Natl Acad Sci 98: 14150-14155.
46. Schmitz RJ, Ecker JR. 2012. Epigenetic and epigenomic variation in Arabidopsis thaliana. Trends Plant Sci 17: 149-154.
47. Schmitz RJ, Schultz MD, Lewsey MG, O'Malley RC, Urich MA, Libiger O, Schork NJ, Ecker JR. 2011. Transgenerational epigenetic instability is a source of novel methylation variants. Science 334: 369-373.
48. Schmitz RJ, Schultz MD, Urich MA, Nery JR, Pelizzola M, Libiger O, Alix A, McCosh RB, Chen H, Schork NJ, et al. 2013. Patterns of population epigenomic diversity. Nature 495: 193-198.
49. Sharp NP, Agrawal AF. 2013. Male-biased fitness effects of spontaneous mutations in Drosophila melanogaster. Evolution 67: 1189-1195.
50. Shor E, Fox CA, Broach JR. 2013. The yeast environmental stress response regulates mutagenesis induced by proteotoxic stress. PLoS Genet 9: e1003680.
51. Stroud H, Ding B, Simon SA, Feng S, Bellizzi M, Pellegrini M, Wang GL, Meyers BC, Jacobsen SE. 2013. Plants regenerated from tissue culture contain stable epigenome changes in rice. eLife 2: e00354.
52. Zhang J. 2000. Rates of conservative and radical nonsynonymous nucleotide substitutions in mammalian nuclear genes. J Mol Evol 50: 56-68.
53. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE, et al. 2006. Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126: 1189-1201.
54. + antiport activity and serine hydroxymethyltransferase stability. Plant Cell 24: 5106-5122.
55. Zhu JK. 2002. Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53: 247-273.
56. Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S. 2007. Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39: 61-69.