Identification of DNA methylated regions by using methylated DNA immunoprecipitation sequencing in Brassica rapa
Satoshi Takahashi A H , Naoki Fukushima B H , Kenji Osabe C H , Etsuko Itabashi D , Motoki Shimizu E , Naomi Miyaji B , Takeshi Takasaki-Yasuda B , Yutaka Suzuki F , Motoaki Seki A G and Ryo Fujimoto B IA RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan.
B Graduate School of Agricultural Science, Kobe University, 1-1 Rokkodai, Nada-ku, Kobe 657-8501, Japan.
C Plant Epigenetics Unit, Okinawa Institute of Science and Technology Graduate University, 1919-1 Tancha, Onna-son, Okinawa 904-0495, Japan.
D Institute of Vegetable and Floriculture Science, NARO, 360 Kusawa, Ano, Tsu, Mie 514-2392, Japan.
E Iwate Biotechnology Research Center, 22-174-4 Narita, Kitakami, Iwate 024-0003, Japan.
F Department of Computational Biology, Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-0882, Japan.
G Core Research for Evolutional Science and Technology, Japan Science and Technology, Kawaguchi, Saitama 332-0012, Japan.
H These authors equally contributed to this work.
I Corresponding author. Email: leo@people.kobe-u.ac.jp
Crop and Pasture Science 69(1) 107-120 https://doi.org/10.1071/CP17394
Submitted: 9 December 2016 Accepted: 24 November 2017 Published: 4 January 2018
Abstract
DNA methylation is an epigenetic gene regulatory mechanism that plays an essential role in gene expression, transposon silencing, genome imprinting and plant development. We investigated the influence of DNA methylation on gene expression in Brassica rapa L., to understand whether epigenetic differences exist between inbred lines. Genome-wide DNA methylation was analysed by methylated DNA immunoprecipitation sequencing (MeDIP-seq) of 14-day-old first and second leaves from two inbred lines of Chinese cabbage, one susceptible and one resistant to fusarium yellows caused by Fusarium oxysporum f. sp. conglutinans. MACS (model-based analysis for ChIP-seq) identified DNA methylation peaks in genic regions including 2 kb upstream, exon, intron and 2 kb downstream. More than 65% of genes showed similar patterns of DNA methylation in the genic regions in the two inbred lines. DNA methylation states of the two inbred lines were compared with their transcriptome. Genes having DNA methylation in the intron and in the 200 bp upstream and downstream regions were associated with a lower expression level in both lines. A small number of genes showed a negative correlation between differences in DNA methylation levels and differences in transcriptional levels in the two inbred lines, suggesting that DNA methylation in these genes results in transcriptional suppression.
Additional keywords: epigenetics, fusarium wilt, gene expression, methylome, transposable elements.
References
Amoah S, Kurup S, Rodriguez Lopez CM, Welham SJ, Powers SJ, Hopkins CJ, Wilkinson MJ, King GJ (2012) A hypomethylated population of Brassica rapa for forward and reverse epi-genetics. BMC Plant Biology 12, 193| A hypomethylated population of Brassica rapa for forward and reverse epi-genetics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlGitrs%3D&md5=aa5107c877473c6f5d70c74ecacb118cCAS |
Chalhoub B, Denoeud F, Liu S, Parkin IAP, Tang H, Wang X, Chiquet J, Belcram H, Tong C, Samans B, Corréa M, Da Silva C, Just J, Falentin C, Koh CS, Le Clainche I, Bernard M, Bento P, Noel B, Labadie K, Alberti A, Charles M, Arnaud D, Guo H, Daviaud C, Alamery S, Jabbari K, Zhao M, Edger PP, Chelaifa H, Tack D, Lassalle G, Mestiri I, Schnel N, Le Paslier MC, Fan G, Renault V, Bayer PE, Golicz AA, Manoli S, Lee TH, Thi VHD, Chalabi S, Hu Q, Fan C, Tollenaere R, Lu Y, Battail C, Shen J, Sidebottom CHD, Wang X, Canaguier A, Chauveau A, Bérard A, Deniot G, Guan M, Liu Z, Sun F, Lim YP, Lyons E, Town CD, Bancroft I, Wang X, Meng J, Ma J, Pires JC, King GJ, Brunel D, Delourme R, Renard M, Aury JM, Adams KL, Batley J, Snowdon RJ, Tost J, Edwards D, Zhou Y, Hua W, Sharpe AG, Paterson AH, Guan C, Wincker P (2014) Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345, 950–953.
| Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlOmsr%2FK&md5=dcca79c5ea4e172a9ce1528f02ce5b53CAS |
Chen X, Ge X, Wang J, Tan C, King GJ, Liu K (2015) Genome-wide DNA methylation profiling by modified reduced representation bisulfite sequencing in Brassica rapa suggests that epigenetic modifications play a key role in polyploid genome evolution. Frontiers in Plant Science 6, 836
| Genome-wide DNA methylation profiling by modified reduced representation bisulfite sequencing in Brassica rapa suggests that epigenetic modifications play a key role in polyploid genome evolution.Crossref | GoogleScholarGoogle Scholar |
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.
| Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjt1GnurY%3D&md5=d3df07ce18a2539bd52d8b515ea5b1e4CAS |
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. Proceedings of the National Academy of Sciences of the United States of America 109, E2183–E2191.
| Widespread dynamic DNA methylation in response to biotic stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVWms77L&md5=86b987b8e52681c3524f3fd5571ade2aCAS |
Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: A GO analysis toolkit for the agricultural community. Nucleic Acids Research 38, W64–W70.
| agriGO: A GO analysis toolkit for the agricultural community.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotVSqtL0%3D&md5=2d79f76dbef77bb18fa88d0f2245330eCAS |
Enya J, Togawa M, Takeuchi T, Yoshida S, Tsushima S, Arie T, Sakai T (2008) Biological and phylogenetic characterization of Fusarium oxysporum complex, which causes yellows on Brassica spp., and proposal of F. oxysporum f. sp. rapae, a novel forma specialis pathogenic on B. rapa in Japan. Phytopathology 98, 475–483.
| Biological and phylogenetic characterization of Fusarium oxysporum complex, which causes yellows on Brassica spp., and proposal of F. oxysporum f. sp. rapae, a novel forma specialis pathogenic on B. rapa in Japan.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkslKrs7c%3D&md5=4876b15dbc2f0a4660d99b30dba55a10CAS |
Fujimoto R, Sasaki T, Inoue H, Nishio T (2008a) Hypomethylation and transcriptional reactivation of retrotransposon-like sequences in ddm1 transgenic plants of Brassica rapa. Plant Molecular Biology 66, 463–473.
| Hypomethylation and transcriptional reactivation of retrotransposon-like sequences in ddm1 transgenic plants of Brassica rapa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitVWrtL4%3D&md5=22b86da0351cd5cbf761d01a4ab7614bCAS |
Fujimoto R, Kinoshita Y, Kawabe A, Kinoshita T, Takashima K, Nordborg M, Nasrallah ME, Shimizu KK, Kudoh H, Kakutani T (2008b) Evolution and control of imprinted FWA genes in the genus Arabidopsis. PLoS Genetics 4, e1000048
| Evolution and control of imprinted FWA genes in the genus Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Fujimoto R, Sasaki T, Kudoh H, Taylor JM, Kakutani T, Dennis ES (2011) Epigenetic variation in the FWA gene within the genus Arabidopsis. The Plant Journal 66, 831–843.
| Epigenetic variation in the FWA gene within the genus Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnslahtb4%3D&md5=176976b1d0bafa71c784c773d30c92daCAS |
Fujimoto R, Sasaki T, Ishikawa R, Osabe K, Kawanabe T, Dennis ES (2012) Molecular mechanisms of epigenetic variation in plants. International Journal of Molecular Sciences 13, 9900–9922.
| Molecular mechanisms of epigenetic variation in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1anurvK&md5=57817355a0b82f16c45224da8076ef14CAS |
Harris RA, Wang T, Coarfa C, Nagarajan RP, Hong C, Downey SL, Johnson BE, Fouse SD, Delaney A, Zhao Y, Olshen A, Ballinger T, Zhou X, Forsberg KJ, Gu J, Echipare L, O’Geen H, Lister R, Pelizzola M, Xi Y, Epstein CB, Bernstein BE, Hawkins RD, Ren B, Chung WY, Gu H, Bock C, Gnirke A, Zhang MQ, Haussler D, Ecker JR, Li W, Farnham PJ, Waterland RA, Meissner A, Marra MA, Hirst M, Milosavljevic A, Costello JF (2010) Comparison of sequencing-based methods to profile DNA methylation and identification of monoallelic epigenetic modifications. Nature Biotechnology 28, 1097–1105.
| Comparison of sequencing-based methods to profile DNA methylation and identification of monoallelic epigenetic modifications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFOht7bN&md5=c954c7cd70af108e7cc57a76d566b58bCAS |
Hauben M, Haesendonckx B, Standaert E, Van Der Kelen K, Azmi A, Akpo H, Van Breusegem F, Guisez Y, Bots M, Lambert B, Laga B, De Block M (2009) Energy use efficiency is characterized by an epigenetic component that can be directed through artificial selection to increase yield. Proceedings of the National Academy of Sciences of the United States of America 106, 20109–20114.
| Energy use efficiency is characterized by an epigenetic component that can be directed through artificial selection to increase yield.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFCrsLvL&md5=9269eef99ace0e48db7571fcd58a7759CAS |
He G, Zhu X, Elling AA, Chen L, Wang X, Guo L, Liang M, He H, Zhang H, Chen F, Qi Y, Chen R, Deng XW (2010) Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. The Plant Cell 22, 17–33.
| Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtlaqtrs%3D&md5=9fcd53a83d9c93e49ffe22449816d768CAS |
Karan R, DeLeon T, Biradar H, Subudhi PK (2012) Salt stress induced variation in DNA methylation pattern and its influence on gene expression in contrasting rice genotypes. PLoS One 7, e40203
| Salt stress induced variation in DNA methylation pattern and its influence on gene expression in contrasting rice genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpvVWrs70%3D&md5=18c68ce0810b53cea1df4a4e6a5c96a4CAS |
Kawamura K, Kawanabe T, Shimizu M, Nagano AJ, Saeki N, Okazaki K, Kaji M, Dennis ES, Osabe K, Fujimoto R (2016) Genetic distance of inbred lines of Chinese cabbage and its relationship to heterosis. Plant Gene 5, 1–7.
| Genetic distance of inbred lines of Chinese cabbage and its relationship to heterosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xht1Oks7fL&md5=88a9a13349e6f6bbf66efb6d68ae2c6dCAS |
Kawanabe T, Fujimoto R, Sasaki T, Taylor JM, Dennis ES (2012) A comparison of transcriptome and epigenetic status between closely related species in the genus Arabidopsis. Gene 506, 301–309.
| A comparison of transcriptome and epigenetic status between closely related species in the genus Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFSqsbvK&md5=abb53deff042a2052b9f4b21e21f678eCAS |
Kawanabe T, Osabe K, Itabashi E, Okazaki K, Dennis ES, Fujimoto R (2016) Development of primer sets that can verify the enrichment of histone modifications, and their application to examining vernalization-mediated chromatin changes in Brassica rapa L. Genes & Genetic Systems 91, 1–10.
| Development of primer sets that can verify the enrichment of histone modifications, and their application to examining vernalization-mediated chromatin changes in Brassica rapa L.Crossref | GoogleScholarGoogle Scholar |
Kinoshita Y, Saze H, Kinoshita T, Miura A, Soppe WJJ, Koornneef M, Kakutani T (2007) Control of FWA gene silencing in Arabidopsis thaliana by SINE-related direct repeats. The Plant Journal 49, 38–45.
| Control of FWA gene silencing in Arabidopsis thaliana by SINE-related direct repeats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnvVyrug%3D%3D&md5=6b9033a36504678bede0f22c3946cd9eCAS |
Laird PW (2010) Principles and challenges of genome-wide DNA methylation analysis. Nature Reviews Genetics 11, 191–203.
| Principles and challenges of genome-wide DNA methylation analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitFCrsLo%3D&md5=fed719f2260745b30bdfab4d44521451CAS |
Le TN, Schumann U, Smith NA, Tiwari S, Au PC, Zhu QH, Taylor JM, Kazan K, Llewellyn DJ, Zhang R, Dennis ES, Wang MB (2014) DNA demethylases target promoter transposable elements to positively regulate stress responsive genes in Arabidopsis. Genome Biology 15, 458
| DNA demethylases target promoter transposable elements to positively regulate stress responsive genes in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Li X, Zhu J, Hu F, Ge S, Ye M, Xiang H, Zhang G, Zheng X, Zhang H, Zhang S, Li Q, Luo R, Yu C, Yu J, Sun J, Zou X, Cao X, Xie X, Wang J, Wang W (2012) Single-base resolution maps of cultivated and wild rice methylomes and regulatory roles of DNA methylation in plant gene expression. BMC Genomics 13, 300
| Single-base resolution maps of cultivated and wild rice methylomes and regulatory roles of DNA methylation in plant gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslehsL%2FE&md5=a4f64791e206de69d80bb2d6de91edb2CAS |
Lister R, O’Malley RC, Tonti-Filippini J, Gregory BD, Berry CC, Millar AH, Ecker JR (2008) Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133, 523–536.
| Highly integrated single-base resolution maps of the epigenome in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmt1Smur8%3D&md5=32a1069e650f2bd6892a81c079bb70ebCAS |
Liu J, He Y, Amasino R, Chen X (2004) siRNAs targeting an intronic transposon in the regulation of natural flowering behavior in Arabidopsis. Genes & Development 18, 2873–2878.
| siRNAs targeting an intronic transposon in the regulation of natural flowering behavior in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtFShu7nN&md5=09c745cb243c75dd9226d47f4164192cCAS |
Liu S, Liu Y, Yang X, Tong C, Edwards D, Parkin IAP, Zhao M, Ma J, Yu J, Huang S, Wang X, Wang J, Lu K, Fang Z, Bancroft I, Yang TJ, Hu Q, Wang X, Yue Z, Li H, Yang L, Wu J, Zhou Q, Wang W, King GJ, Pires JC, Lu C, Wu Z, Sampath P, Wang Z, Guo H, Pan S, Yang L, Min J, Zhang D, Jin D, Li W, Belcram H, Tu J, Guan M, Qi C, Du D, Li J, Jiang L, Batley J, Sharpe AG, Park BS, Ruperao P, Cheng F, Waminal NE, Huang Y, Dong C, Wang L, Li J, Hu Z, Zhuang M, Huang Y, Huang J, Shi J, Mei D, Liu J, Lee TH, Wang J, Jin H, Li Z, Li X, Zhang J, Xiao L, Zhou Y, Liu Z, Liu X, Qin R, Tang X, Liu W, Wang Y, Zhang Y, Lee J, Kim HH, Denoeud F, Xu X, Liang X, Hua W, Wang X, Wang J, Chalhoub B, Paterson AH (2014) The Brassica oleracea genome reveals the asymmetrical evolution of polyploidy genomes. Nature Communications 5, 3930
Liu R, How-Kit A, Stammitti L, Teyssier E, Rolin D, Mortain-Bertrand A, Halle S, Liu M, Kong J, Wu C, Degraeve-Guibault C, Chapman NH, Maucourt M, Hodgman TC, Tost J, Bouzayen M, Hong Y, Seymour GB, Giovannoni JJ, Gallusci P (2015) A DEMETER-like DNA demethylase governs tomato fruit ripening. Proceedings of the National Academy of Sciences of the United States of America 112, 10804–10809.
| A DEMETER-like DNA demethylase governs tomato fruit ripening.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtlSit7vI&md5=e4048c85eeb586b849014918bb2cc1d9CAS |
Long Y, Xia W, Li R, Wang J, Shao M, Feng J, King GJ, Meng J (2011) Epigenetic QTL mapping in Brassica napus. Genetics 189, 1093–1102.
| Epigenetic QTL mapping in Brassica napus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XitFeqt7o%3D&md5=7491ab27a57221014f3aa868aaf0c86aCAS |
Lv H, Fang Z, Yang L, Zhang Y, Wang Q, Liu Y, Zhuang M, Yang Y, Xie B, Liu B, Liu J, Kang J, Wang X (2014) Mapping and analysis of a novel candidate Fusarium wilt resistance gene FOC1 in Brassica oleracea. BMC Genomics 15, 1094
| Mapping and analysis of a novel candidate Fusarium wilt resistance gene FOC1 in Brassica oleracea.Crossref | GoogleScholarGoogle Scholar |
Martin A, Troadec C, Boualem A, Rajab M, Fernandez R, Morin H, Pitrat M, Dogimont C, Bendahmane A (2009) A transposon-induced epigenetic change leads to sex determination in melon. Nature 461, 1135–1138.
| A transposon-induced epigenetic change leads to sex determination in melon.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlKgs7nE&md5=0ff372b489726bc22c5a472a9a84108cCAS |
Matzke MA, Mosher RA (2014) RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nature Reviews Genetics 15, 394–408.
| RNA-directed DNA methylation: an epigenetic pathway of increasing complexity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXns1Wrurg%3D&md5=307c48ee441e1255acee7273a98c31ebCAS |
Miyaji N, Shimizu M, Miyazaki J, Osabe K, Sato M, Ebe Y, Takada S, Kaji M, Dennis ES, Fujimoto R, Okazaki K (2017) Comparison of transcriptome profiles by Fusarium oxysporum inoculation between Fusarium yellows resistant and susceptible lines in Brassica rapa L. Plant Cell Reports 36, 1841–1854.
| Comparison of transcriptome profiles by Fusarium oxysporum inoculation between Fusarium yellows resistant and susceptible lines in Brassica rapa L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhtlGktrnE&md5=286a5d6fa73cffe0208c107056e5a7e5CAS |
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research 8, 4321–4326.
| Rapid isolation of high molecular weight plant DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXmtVSmtL8%3D&md5=e5ac8040c9964b31b77c508d0d22b329CAS |
Niederhuth CE, Bewick AJ, Ji L, Alabady MS, Kim KD, Li Q, Rohr NA, Rambani A, Burke JM, Udall JA, Egesi C, Schmutz J, Grimwood J, Jackson SA, Springer NM, Schmitz RJ (2016) Widespread natural variation of DNA methylation within angiosperms. Genome Biology 17, 194
| Widespread natural variation of DNA methylation within angiosperms.Crossref | GoogleScholarGoogle Scholar |
Osabe K, Sasaki T, Ishikawa R, Fujimoto R (2012) The role of DNA methylation in plants. In ‘DNA methylation: principles, mechanisms and challenges’. (Eds TV Tatarinova, G Sablok) pp. 35–66. (Nova Science Publishers: Hauppauge, NY, USA)
Parkin IAP, Koh C, Tang H, Robinson SJ, Kagale S, Clarke WE, Town CD, Nixon J, Krishnakumar V, Bidwell SL, Denoeud F, Belcram H, Links MG, Just J, Clarke C, Bender T, Huebert T, Mason AS, Pires JC, Barker G, Moore J, Walley PG, Manoli S, Batley J, Edwards D, Nelson MN, Wang X, Paterson AH, King G, Bancroft I, Chalhoub B, Sharpe AG (2014) Transcriptome and methylome profiling reveals relics of genome dominance in the mesopolyploid Brassica oleracea. Genome Biology 15, R77
| Transcriptome and methylome profiling reveals relics of genome dominance in the mesopolyploid Brassica oleracea.Crossref | GoogleScholarGoogle Scholar |
Sasaki T, Fujimoto R, Kishitani S, Nishio T (2011) Analysis of target sequences of DDM1s in Brassica rapa by MSAP. Plant Cell Reports 30, 81–88.
| Analysis of target sequences of DDM1s in Brassica rapa by MSAP.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmvV2r&md5=a7af628dd6c8149e2afc7d355e116471CAS |
Saze H, Kakutani T (2007) Heritable epigenetic mutation of a transposon-flanked Arabidopsis gene due to lack of the chromatin-remodeling factor DDM1. The EMBO Journal 26, 3641–3652.
| Heritable epigenetic mutation of a transposon-flanked Arabidopsis gene due to lack of the chromatin-remodeling factor DDM1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXos1eqtb8%3D&md5=ab18eb7a1e9ed095d160ce446dc6df10CAS |
Saze H, Sasaki T, Kakutani T (2008) Negative regulation of DNA methylation in plants. Epigenetics 3, 122–124.
| Negative regulation of DNA methylation in plants.Crossref | GoogleScholarGoogle Scholar |
Schield DR, Walsh MR, Card DC, Andrew AL, Adams RH, Castoe TA (2016) EpiRADseq: scalable analysis of genomewide patterns of methylation using next-generation sequencing. Methods in Ecology and Evolution 7, 60–69.
| EpiRADseq: scalable analysis of genomewide patterns of methylation using next-generation sequencing.Crossref | GoogleScholarGoogle Scholar |
Shimizu M, Fujimoto R, Ying H, Pu ZJ, Ebe Y, Kawanabe T, Saeki N, Taylor JM, Kaji M, Dennis ES, Okazaki K (2014) Identification of candidate genes for fusarium yellows resistance in Chinese cabbage by differential expression analysis. Plant Molecular Biology 85, 247–257.
| Identification of candidate genes for fusarium yellows resistance in Chinese cabbage by differential expression analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXkvVGrt78%3D&md5=f79302090f7f3d7106e81edb3ab66ab7CAS |
Shimizu M, Pu Z, Kawanabe T, Kitashiba H, Matsumoto S, Ebe Y, Sano M, Funaki T, Fukai E, Fujimoto R, Okazaki K (2015) Map-based cloning of a candidate gene conferring Fusarium yellows resistance in Brassica oleracea. Theoretical and Applied Genetics 128, 119–130.
| Map-based cloning of a candidate gene conferring Fusarium yellows resistance in Brassica oleracea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvFWhur3E&md5=bbd5cd38353c8a8333bed6daac82eae4CAS |
Tarutani Y, Shiba H, Iwano M, Kakizaki T, Suzuki G, Watanabe M, Isogai A, Takayama S (2010) Trans-acting small RNA determines dominance relationships in Brassica self-incompatibility. Nature 466, 983–986.
| Trans-acting small RNA determines dominance relationships in Brassica self-incompatibility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVyks7nI&md5=e0681044e0974bd3ab7ae6a2336b7104CAS |
Vaughn MW, Tanurdžić M, Lippman Z, Jiang H, Carrasquillo R, Rabinowicz PD, Dedhia N, McCombie WR, Agier N, Bulski A, Colot V, Doerge RW, Martienssen RA (2007) Epigenetic natural variation in Arabidopsis thaliana. PLoS Biology 5, e174
| Epigenetic natural variation in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Verkest A, Byzova M, Martens C, Willems P, Verwulgen T, Slabbinck B, Rombaut D, Van de Velde J, Vandepoele K, Standaert E, Peeters M, Van Lijsebettens M, Van Breusegem F, De Block M (2015) Selection for improved energy use efficiency and drought tolerance in canola results in distinct transcriptome and epigenome changes. Plant Physiology 168, 1338–1350.
| Selection for improved energy use efficiency and drought tolerance in canola results in distinct transcriptome and epigenome changes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsVSrt77J&md5=718b603569fb167029897ebc222747e5CAS |
Wang X, Wang H, Wang J, Sun R, Wu J, Liu S, Bai Y, Mun JH, Bancroft I, Cheng F, Huang S, Li X, Hua W, Wang J, Wang X, Freeling M, Pires JC, Paterson AH, Chalhoub B, Wang B, Hayward A, Sharpe AG, Park BS, Weisshaar B, Liu B, Li B, Liu B, Tong C, Song C, Duran C, Peng C, Geng C, Koh C, Lin C, Edwards D, Mu D, Shen D, Soumpourou E, Li F, Fraser F, Conant G, Lassalle G, King GJ, Bonnema G, Tang H, Wang H, Belcram H, Zhou H, Hirakawa H, Abe H, Guo H, Wang H, Jin H, Parkin IAP, Batley J, Kim JS, Just J, Li J, Xu J, Deng J, Kim JA, Li J, Yu J, Meng J, Wang J, Min J, Poulain J, Wang J, Hatakeyama K, Wu K, Wang L, Fang L, Trick M, Links MG, Zhao M, Jin M, Ramchiary N, Drou N, Berkman PJ, Cai Q, Huang Q, Li R, Tabata S, Cheng S, Zhang S, Zhang S, Huang S, Sato S, Sun S, Kwon SJ, Choi SR, Lee TH, Fan W, Zhao X, Tan X, Xu X, Wang Y, Qiu Y, Yin Y, Li Y, Du Y, Liao Y, Lim Y, Narusaka Y, Wang Y, Wang Z, Li Z, Wang Z, Xiong Z, Zhang Z (2011) The genome of the mesopolyploid crop species Brassica rapa. Nature Genetics 43, 1035–1039.
| The genome of the mesopolyploid crop species Brassica rapa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtV2gtrbL&md5=1fb5a1ac9e4a79b545aadd1a310f8fa9CAS |
Wang M, Qin L, Xie C, Li W, Yuan J, Kong L, Yu W, Xia G, Liu S (2014) Induced and constitutive DNA methylation in a salinity-tolerant wheat introgression line. Plant & Cell Physiology 55, 1354–1365.
| Induced and constitutive DNA methylation in a salinity-tolerant wheat introgression line.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFCru7nP&md5=b1bc30bc95679a3efcac60823003d3efCAS |
Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SWL, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE, Ecker JR (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126, 1189–1201.
| Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVCnsrvP&md5=72c0fa8a17d5861ef58864aa8cce53cdCAS |
Zhang X, Shiu SH, Cal A, Borevitz JO (2008) Global analysis of genetic, epigenetic and transcriptional polymorphisms in Arabidopsis thaliana using whole genome tiling arrays. PLoS Genetics 4, e1000032
| Global analysis of genetic, epigenetic and transcriptional polymorphisms in Arabidopsis thaliana using whole genome tiling arrays.Crossref | GoogleScholarGoogle Scholar |
Zhu QH, Shan WX, Ayliffe MA, Wang MB (2016) Epigenetic mechanisms: an emerging player in plant-microbe interactions. Molecular Plant-Microbe Interactions 29, 187–196.
| Epigenetic mechanisms: an emerging player in plant-microbe interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XpsFOrs7Y%3D&md5=8d8bc510e2a816b811863d4b766918b6CAS |