Non-CG DNA methylation-deficiency mutations enhance mutagenesis rates during salt adaptation in cultured Arabidopsis cells

Xiaohong Zhu, Shaojun Xie, Kai Tang, Rajwant K. Kalia, Na Liu, Jinbiao Ma, Ray A. Bressan, Jian-Kang Zhu

Stress Biology ›› 2021, Vol. 1 ›› Issue (1) : 12. DOI: 10.1007/s44154-021-00013-2
Original Paper

Non-CG DNA methylation-deficiency mutations enhance mutagenesis rates during salt adaptation in cultured Arabidopsis cells

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Abstract

Much has been learned about how plants acclimate to stressful environments, but the molecular basis of stress adaptation and the potential involvement of epigenetic regulation remain poorly understood. Here, we examined if salt stress induces mutagenesis in suspension cultured plant cells and if DNA methylation affects the mutagenesis using whole genome resequencing analysis. We generated suspension cell cultures from two Arabidopsis DNA methylation-deficient mutants and wild-type plants, and subjected the cultured cells to stepwise increases in salt stress intensity over 40 culture cycles. We show that ddc (drm1 drm2 cmt3) mutant cells can adapt to grow in 175 mM NaCl-containing growth medium and exhibit higher adaptability compared to wild type Col-0 and nrpe1 cells, which can adapt to grow in only 125 mM NaCl-containing growth medium. Salt treated nrpe1 and ddc cells but not wild type cells accumulate more mutations compared with their respective untreated cells. There is no enrichment of stress responsive genes in the list of mutated genes in salt treated cells compared to the list of mutated genes in untreated cells. Our results suggest that DNA methylation prevents the induction of mutagenesis by salt stress in plant cells during stress adaptation.

Keywords

Salt stress / Cell suspension / DNA methylation-deficient mutants / Stress-induced mutagenesis / Stress adaptation

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Xiaohong Zhu, Shaojun Xie, Kai Tang, Rajwant K. Kalia, Na Liu, Jinbiao Ma, Ray A. Bressan, Jian-Kang Zhu. Non-CG DNA methylation-deficiency mutations enhance mutagenesis rates during salt adaptation in cultured Arabidopsis cells. Stress Biology, 2021, 1(1): 12 https://doi.org/10.1007/s44154-021-00013-2

References

[1]
AkiyamaK, KurotaniA, IidaK, KuromoriT, ShinozakiK, SakuraiT. RARGE II: an integrated phenotype database of Arabidopsis mutant traits using a controlled vocabulary. Plant Cell Physiol, 2014, 55(1):e4
CrossRef Google scholar
[2]
AmanoT, HirasawaK, O'DonohueMJ, PernolleJC, ShioiY. A versatile assay for the accurate, time-resolved determination of cellular viability. Anal Biochem, 2003, 314(1):1-7
CrossRef Google scholar
[3]
Azman AS, Mhiri C, Grandbastien, MA, Tam SM (2014) Transposable elements and the detection of somaclonal variation in plant tissue culture: A review. Malays Appl Biol 43(1):1–12
[4]
BaerCF, MiyamotoMM, DenverDR. Mutation rate variation in multicellular eukaryotes: causes and consequences. Nat Rev Genet, 2007, 8(8):619-631
CrossRef Google scholar
[5]
BarrettT, WilhiteSE, LedouxP, EvangelistaC, KimIF, TomashevskyM, MarshallKA, PhillippyKH, ShermanPM, HolkoM, YefanovA, LeeH, ZhangN, RobertsonCL, SerovaN, DavisS, SobolevaA. NCBI GEO: archive for functional genomics data sets—update. Nucleic Acids Res, 2013, 41(Database issue):D991-D995
CrossRef Google scholar
[6]
Binzel ML, Hasegawa PM, Handa AK, Bressan RA (1985) Adaptation of tobacco cells to NaCI. Plant Physiology 79:118–125
[7]
BjedovI, TenaillonO, GerardB, SouzaV, DenamurE, RadmanM, TaddeiF, MaticI. Stress-induced mutagenesis in bacteria. Science, 2003, 300(5624):1404-1409
CrossRef Google scholar
[8]
Braun AC (1959) A demonstration of the recovery of the crown-gall tumor cell with the use of complex tumors of single-cell origin. Proc Natl Acad Sci USA 45:932–938
[9]
BristowRG, HillRP. Hypoxia and metabolism. Hypoxia, DNA repair and genetic instability. Nat Rev Cancer, 2008, 8(3):180-192
CrossRef Google scholar
[10]
ButtonDK, GartlandKMA, BallLD, NatansonL, GartlandJS, LyonGD. DRASTIC—INSIGHTS: querying information in a plant gene expression database. Nucleic Acids Res, 2006, 34(Database issue):D712-D716
CrossRef Google scholar
[11]
CaoXF, JacobsenSE. Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol, 2002, 12(13):1138-1144
CrossRef Google scholar
[12]
CingolaniP, PlattsA, Wang leL, CoonM, NguyenT, WangL, LandSJ, LuX, RudenDM. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly, 2012, 6(2):80-92
CrossRef Google scholar
[13]
EhrlichM, NorrisKF, WangRY, KuoKC, GehrkeCW. DNA cytosine methylation and heat-induced deamination. Biosci Rep, 1986, 6(4):387-393
CrossRef Google scholar
[14]
Encina CL, Constantin M, Botella J (2001) An easy and reliable method for establishment and maintenance of leaf and root cell cultures of Arabidopsis thaliana. Plant Mol Biol Report 19(3):245–248. https://doi.org/10.1007/BF02772896
[15]
FosterPL. Stress-induced mutagenesis in bacteria. Crit Rev Biochem Mol Biol, 2007, 42(5):373-397
CrossRef Google scholar
[16]
FurnerIJ, MatzkeM. Methylation and demethylation of the Arabidopsis genome. Curr Opin Plant Biol, 2011, 14(2):137-141
CrossRef Google scholar
[17]
Gunther T, Schmid KJ (2010) Deleterious amino acid polymorphisms in Arabidopsis thaliana and rice. Theor Appl Genet 121(1):157–168. https://doi.org/10.1007/s00122-010-1299-4
[18]
HasegawaPM, BressanRA, ZhuJK, BohnertHJ. Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol, 2000, 51(1):463-499
CrossRef Google scholar
[19]
HeidenreichE. Adaptive mutation in Saccharomyces cerevisiae. Crit Rev Biochem Mol Biol, 2007, 42(4):285-311
CrossRef Google scholar
[20]
HenicsT, WheatleyDN. Cytoplasmic vacuolation, adaptation and cell death: a view on new perspectives and features. Biol Cell, 1999, 91(7):485-498
CrossRef Google scholar
[21]
HollidayR, GriggGW. DNA methylation and mutation. Mutat Res, 1993, 285(1):61-67
CrossRef Google scholar
[22]
JiangC, BelfieldEJ, MithaniA, VisscherA, RagoussisJ, MottR, SmithJA, HarberdNP. ROS-mediated vascular homeostatic control of root-to-shoot soil Na delivery in Arabidopsis. EMBO J, 2012, 31(22):4359-4370
CrossRef Google scholar
[23]
Jiang C, Mithani A, Belfield EJ, Mott R, Hurst LD, Harberd NP (2014) Environmentally responsive genome-wide accumulation of de novo Arabidopsis thaliana mutations and epimutations. Genome Res 24(11):1821–1829. https://doi.org/10.1101/gr.177659.114
[24]
JohnB, SaliA. Detection of homologous proteins by an intermediate sequence search. Protein Sci, 2004, 13(1):54-62
CrossRef Google scholar
[25]
KimS, JeongK, BhutaniK, LeeJ, PatelA, ScottE, NamH, LeeH, GleesonJG, BafnaV. Virmid: accurate detection of somatic mutations with sample impurity inference. Genome Biol, 2013, 14(8):R90
CrossRef Google scholar
[26]
KoboldtDC, ZhangQ, LarsonDE, ShenD, McLellanMD, LinL, MillerCA, MardisER, DingL, WilsonRK. VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res, 2012, 22(3):568-576
CrossRef Google scholar
[27]
Larkin P, Scowcroft W (1981) Somaclonal variation—a novel source of variability from cell cultures for plant improvement. Theor Appl Genet 60:197–214.
[28]
LawJA, JacobsenSE. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet, 2010, 11(3):204-220
CrossRef Google scholar
[29]
LiH, HandsakerB, WysokerA, FennellT, RuanJ, HomerN, MarthG, AbecasisG, DurbinR Genome Project Data Processing S. The sequence alignment/map format and SAMtools. Bioinformatics, 2009, 25(16):2078-2079
CrossRef Google scholar
[30]
MatzkeMA, MosherRA. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet, 2014, 15(6):394-408
CrossRef Google scholar
[31]
MillerG, SuzukiN, Ciftci-YilmazS, MittlerR. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ, 2010, 33(4):453-467
CrossRef Google scholar
[32]
MugalCF, EllegrenH. Substitution rate variation at human CpG sites correlates with non-CpG divergence, methylation level and GC content. Genome Biol, 2011, 12(6):R58-R58
CrossRef Google scholar
[33]
MunnsR, TesterM. Mechanisms of salinity tolerance. Annu Rev Plant Biol, 2008, 59(1):651-681
CrossRef Google scholar
[34]
Ng PC, Henikoff S (2001) Predicting deleterious amino acid substitutions. Genome Research 11:863–874
[35]
NgPC, HenikoffS. SIFT: predicting amino acid changes that affect protein function. Nucleic Acids Res, 2003, 31(13):3812-3814
CrossRef Google scholar
[36]
OhashiE, OgiT, KusumotoR, IwaiS, MasutaniC, HanaokaF, OhmoriH. Error-prone bypass of certain DNA lesions by the human DNA polymerase kappa. Genes Dev, 2000, 14(13):1589-1594
CrossRef Google scholar
[37]
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(5961):92–94. https://doi.org/10.1126/science.1180677
[38]
RamY, HadanyL. Stress-induced mutagenesis and complex adaptation. Proc Biol Sci, 2014, 281(1792):20141025
CrossRef Google scholar
[39]
RosenbergSM. Evolving responsively: adaptive mutation. Nat Rev Genet, 2001, 2(7):504-515
CrossRef Google scholar
[40]
SharpNP, AgrawalAF. Evidence for elevated mutation rates in low-quality genotypes. Proc Natl Acad Sci U S A, 2012, 109(16):6142-6146
CrossRef Google scholar
[41]
SrivastavaAK, LuYM, ZintaG, LangZB, ZhuJK. UTR-dependent control of gene expression in plants. Trends Plant Sci, 2018, 23(3):248-259
CrossRef Google scholar
[42]
StroudH, GreenbergMV, FengS, BernatavichuteYV, JacobsenSE. Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell, 2013, 152(1–2):352-364
CrossRef Google scholar
[43]
TenaillonO, DenamurE, MaticI. Evolutionary significance of stress-induced mutagenesis in bacteria. Trends Microbiol, 2004, 12(6):264-270
CrossRef Google scholar
[44]
XiaJ, HanL, ZhaoZ. Investigating the relationship of DNA methylation with mutation rate and allele frequency in the human genome. BMC Genomics, 2012, 13(Suppl 8):S7
CrossRef Google scholar
[45]
ZemachA, KimMY, HsiehPH, Coleman-DerrD, Eshed-WilliamsL, ThaoK, HarmerSL, ZilbermanD. The arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell, 2013, 153(1):193-205
CrossRef Google scholar
[46]
ZhangH, MaZY, ZengL, TanakaK, ZhangCJ, MaJ, BaiG, WangP, ZhangSW, LiuZW, CaiT, TangK, LiuR, ShiX, HeXJ, ZhuJK. DTF1 is a core component of RNA-directed DNA methylation and may assist in the recruitment of pol IV. Proc Natl Acad Sci U S A, 2013, 110(20):8290-8295
CrossRef Google scholar
[47]
ZhuJK. Salt and drought stress signal transduction in plants. Annu Rev Plant Biol, 2002, 53(1):247-273
CrossRef Google scholar
[48]
ZhuJK. Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol, 2003, 6(5):441-445
CrossRef Google scholar
Funding
National Natural Science Foundation of China(31872807); CAS Strategic Priority Research Program(XDB27040101)

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