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A role of age-dependent DNA methylation reprogramming in regulating the regeneration capacity of Boea hygrometrica leaves

  • Run-Ze Sun
  • En-Hui Zuo
  • Jin-Feng Qi
  • Yang Liu
  • Chih-Ta Lin
  • Xin DengEmail author
Original Article

Abstract

Plants can regenerate new individuals under appropriate culture conditions. Although the molecular basis of shoot regeneration has steadily been unraveled, the role of age-dependent DNA methylation status in the regulation of explant regeneration remains practically unknown. Here, we established an effective auxin/cytokinin-induced shoot regeneration system for the resurrection plant Boea hygrometrica via direct organogenesis and observed that regeneration was postponed with increasing age of donor plants. Global transcriptome analysis revealed significant upregulation of genes required for hormone signaling and phenylpropanoid biosynthesis and downregulation of photosynthetic genes during regeneration. Transcriptional changes in the positive/negative regulators and cell wall-related proteins involved in plant regeneration, such as ELONGATED HYPOCOTYL5 (HY5), LATERAL ORGAN BOUNDARIES DOMAIN, SHOOT-MERISTEMLESS, and WUSCHEL, were associated with the regeneration process. Comparison of DNA methylation profiling between leaves from young seedlings (YL) and mature plants (ML) revealed increased asymmetrical methylation in ML, which was predominantly distributed in promoter regions of genes, such as HY5 and a member of ABA-responsive element (ABRE) binding protein/ABRE binding factor, as well as genes encoding glycine-rich cell wall structural protein, CENTRORADIALIS-like protein, and beta-glucosidase 40-like essential for shoot meristem and cell wall architecture. Their opposite transcription response in ML explants during regeneration compared with those from YL demonstrated the putative involvement of DNA methylation in regeneration. Moreover, a significant lower expression of DNA glycosylase-lyase required for DNA demethylation in ML was coincident with its postponed regeneration compared with those in YL. Taken together, our results suggest a role of promoter demethylation in B. hygrometrica regeneration.

Keywords

Shoot regeneration Donor plant age DNA methylome Transcriptome Resurrection plant Boea hygrometrica 

Abbreviations

2,4-D

2,4-dichlorophenoxyacetic acid

6-BA

6-benzylaminopurine

ABA

abscisic acid

BSP

bisulfite sequencing PCR

DEG

differentially expressed gene

DMG

differentially methylated gene

DMR

differentially methylated region

GO

Gene Ontology

KEGG

Kyoto Encyclopedia of Genes and Genomes

mC

methylcytosine

ML

leaves from mature plants

qPCR

quantitative real-time PCR

RNA-Seq

high-throughput mRNA sequencing

SIM

shoot-inducing medium

WGBS

whole-genome bisulfite sequencing

YL

leaves from young seedlings

Notes

Author contributions

XD conceived the experiments. EZ, JQ, and YL prepared the plant materials. RS analyzed the data and wrote the manuscript. XD and CL revised the manuscript. All authors have read and approved the manuscript.

Funding

This work was supported by the National Natural Science Foundation of China (grant numbers 31770293 and 31470361).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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Fig. S1

Effects of different compositions and concentrations of plant hormones on shoot regeneration. (PNG 2602 kb)

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High resolution image (TIFF 2343 kb)
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Fig. S2

Young (a) and mature (b) donor plants used for comparison of regeneration capacity. (PNG 2438 kb)

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High resolution image (TIF 635 kb)
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Fig. S3

KEGG pathway enrichment analysis among up- and downregulated DEGs in YL explants during regeneration. (PNG 461 kb)

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High resolution image (TIF 1111 kb)
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Fig. S4

Expression profile of transcription factors in YL explants during regeneration. (PNG 609 kb)

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High resolution image (TIF 1662 kb)
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Fig. S5

Expression profile of genes involved in hormone signaling in YL explants during regeneration. (PNG 3389 kb)

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High resolution image (TIFF 822 kb)
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Fig. S6

WGBS depth and saturation of YL (a) and ML (b). (PNG 382 kb)

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High resolution image (TIF 1842 kb)
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Fig. S7

Distribution of the DNA methylation level in YL (a) and ML (b). (PNG 348 kb)

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High resolution image (TIF 1804 kb)
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Fig. S8

Average mC levels of gene loci in YL (a) and ML (b) and a comparison between samples (c). (PNG 733 kb)

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High resolution image (TIF 3398 kb)
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Fig. S9

Correlation analysis of DEGs in YL explants during regeneration and methylation differences in the corresponding YL and ML regions. (PNG 1254 kb)

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High resolution image (TIF 2998 kb)
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Fig. S10

BSP validation of two representative DMRs between YL and ML. (PNG 279 kb)

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Table S1 (XLSX 13 kb)
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Table S2 (XLSX 10 kb)
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Table S3 (XLSX 519 kb)
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Table S4 (XLSX 58.5 kb)
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Table S5 (XLSX 31 kb)
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Table S10 (XLSX 11 kb)

References

  1. Bao Y, Dharmawardhana P, Mockler TC, Strauss SH (2009) Genome scale transcriptome analysis of shoot organogenesis in Populus. BMC Plant Biol 9:132CrossRefGoogle Scholar
  2. Baskaran P, Moyo M, Van Staden J (2014) In vitro plant regeneration, phenolic compound production and pharmacological activities of Coleonema pulchellum. S Afr J Bot 90:74–79CrossRefGoogle Scholar
  3. Becerra DC, Forero AP, Góngora GA (2004) Age and physiological condition of donor plants affect in vitro morphogenesis in leaf explants of Passiflora edulis f. flavicarpa. Plant Cell Tissue Organ Cult 79:87–90CrossRefGoogle Scholar
  4. Benkirane H, Sabounji K, Chlyah A, Chlyah H (2000) Somatic embryogenesis and plant regeneration from fragments of immature inflorescences and coleoptiles of durum wheat. Plant Cell Tissue Organ Cult 61:107–113CrossRefGoogle Scholar
  5. Berckmans B, Vassileva V, Schmid SPC, Maes S, Parizot B, Naramoto S, Magyar Z, Kamei CLA, Koncz C, Bögre L, Persiau G, de Jaeger G, Friml J, Simon R, Beeckman T, de Veylder L (2011) Auxin-dependent cell cycle reactivation through transcriptional regulation of Arabidopsis E2Fa by lateral organ boundary proteins. Plant Cell 23:3671–3683CrossRefGoogle Scholar
  6. Bouyer D, Kramdi A, Kassam M, Heese M, Schnittger A, Roudier F, Colot V (2017) DNA methylation dynamics during early plant life. Genome Biol 18:179CrossRefGoogle Scholar
  7. Cairns JRK, Esen A (2010) β-Glucosidases. Cell Mol Life Sci 67:3389–3405CrossRefGoogle Scholar
  8. Cardoza V, Stewart CN (2004) Brassica biotechnology: progress in cellular and molecular biology. In Vitro Cell Dev Biol Plant 40:542–551CrossRefGoogle Scholar
  9. Chan SW-L, Henderson IR, Jacobsen SE (2005) Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Genet 6:351–360CrossRefGoogle Scholar
  10. Cheng ZJ, Zhu SS, Gao XQ, Zhang XS (2010) Cytokinin and auxin regulates WUS induction and inflorescence regeneration in vitro in Arabidopsis. Plant Cell Rep 29:927–933CrossRefGoogle Scholar
  11. Choi Y, Gehring M, Johnson L, Hannon M, Harada JJ, Goldberg RB, Jacobsen SE, Fischer RL (2002) DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell 110:33–42CrossRefGoogle Scholar
  12. Conti L, Bradley D (2007) TERMINAL FLOWER1 is a mobile signal controlling Arabidopsis architecture. Plant Cell 19:767–778CrossRefGoogle Scholar
  13. Devaiah BN, Karthikeyan AS, Raghothama KG (2007) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 143:1789–1801CrossRefGoogle Scholar
  14. Ding C-J, Liang L-X, Diao S, Su X-H, Zhang B-Y (2018) Genome-wide analysis of day/night DNA methylation differences in Populus nigra. PLoS One 13:e0190299CrossRefGoogle Scholar
  15. Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085–1097CrossRefGoogle Scholar
  16. Fan M, Xu C, Xu K, Hu Y (2012) LATERAL ORGAN BOUNDARIES DOMAIN transcription factors direct callus formation in Arabidopsis regeneration. Cell Res 22:1169–1180CrossRefGoogle Scholar
  17. Fujita Y, Yoshida T, Yamaguchi-Shinozaki K (2013) Pivotal role of the AREB/ABF-SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants. Physiol Plant 147:15–27CrossRefGoogle Scholar
  18. Gaj MD (2004) Factors influencing somatic embryogenesis induction and plant regeneration with particular reference to Arabidopsis thaliana (L.) Heynh. Plant Growth Regul 43:27–47CrossRefGoogle Scholar
  19. Gao F, Xia Y, Wang J, Lin Z, Ou Y, Liu X, Liu W, Zhou B, Luo H, Zhou B, Wen B, Zhang X, Huang J (2014) Integrated analyses of DNA methylation and hydroxymethylation reveal tumor suppressive roles of ECM1, ATF5, and EOMES in human hepatocellular carcinoma. Genome Biol 15:533CrossRefGoogle Scholar
  20. Gong Z, Morales-Ruiz T, Ariza RR, Roldán-Arjona T, David L, Zhu J-K (2002) ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell 111:803–814CrossRefGoogle Scholar
  21. Ikeuchi M, Ogawa Y, Iwase A, Sugimoto K (2016) Plant regeneration: cellular origins and molecular mechanisms. Development 143:1442–1451CrossRefGoogle Scholar
  22. Ikeuchi M, Sugimoto K, Iwase A (2013) Plant callus: mechanisms of induction and repression. Plant Cell 25:3159–3173CrossRefGoogle Scholar
  23. Iwase A, Harashima H, Ikeuchi M, Rymen B, Ohnuma M, Komaki S, Morohashi K, Kurata T, Nakata M, Ohme-Takagi M, Grotewold E, Sugimoto K (2017) WIND1 promotes shoot regeneration through transcriptional activation of ENHANCER OF SHOOT REGENERATION1 in Arabidopsis. Plant Cell 29:54–69CrossRefGoogle Scholar
  24. Iwase A, Mitsuda N, Koyama T, Hiratsu K, Kojima M, Arai T, Inoue Y, Seki M, Sakakibara H, Sugimoto K, Ohme-Takagi M (2011) The AP2/ERF transcription factor WIND1 controls cell dedifferentiation in Arabidopsis. Curr Biol 21:508–514CrossRefGoogle Scholar
  25. Jiménez VM (2005) Involvement of plant hormones and plant growth regulators on in vitro somatic embryogenesis. Plant Growth Regul 47:91–110CrossRefGoogle Scholar
  26. Jones AMP, Saxena PK (2013) Inhibition of phenylpropanoid biosynthesis in Artemisia annua L.: a novel approach to reduce oxidative browning in plant tissue culture. PLoS One 8:e76802CrossRefGoogle Scholar
  27. Jones PA (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 13:484–492CrossRefGoogle Scholar
  28. Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357–360CrossRefGoogle Scholar
  29. Kong L, Zhang Y, Ye Z-Q, Liu X-Q, Zhao S-Q, Wei L, Gao G (2007) CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res 35:W345–W349CrossRefGoogle Scholar
  30. Kubo H, Peeters AJM, Aarts MGM, Pereira A, Koornneef M (1999) ANTHOCYANINLESS2, a homeobox gene affecting anthocyanin distribution and root development in Arabidopsis. Plant Cell 11:1217–1226CrossRefGoogle Scholar
  31. Lai Y-S, Zhang X, Zhang W, Shen D, Wang H, Xia Y, Qiu Y, Song J, Wang C, Li X (2017) The association of changes in DNA methylation with temperature-dependent sex determination in cucumber. J Exp Bot 68:2899–2912CrossRefGoogle Scholar
  32. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359CrossRefGoogle Scholar
  33. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12:323CrossRefGoogle Scholar
  34. Li W, Liu H, Cheng ZJ, Su YH, Han HN, Zhang Y, Zhang XS (2011) DNA methylation and histone modifications regulate de novo shoot regeneration in Arabidopsis by modulating WUSCHEL expression and auxin signaling. PLoS Genet 7:e1002243CrossRefGoogle Scholar
  35. 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 133:523–536CrossRefGoogle Scholar
  36. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo QM, Edsall L, Antosiewicz-Bourget J, Stewart R, Ruotti V, Millar AH, Thomson JA, Ren B, Ecker JR (2009) Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462:315–322CrossRefGoogle Scholar
  37. Liu J, Hu X, Qin P, Prasad K, Hu Y, Xu L (2018) The WOX11–LBD16 pathway promotes pluripotency acquisition in callus cells during de novo shoot regeneration in tissue culture. Plant Cell Physiol 59:739–748CrossRefGoogle Scholar
  38. Liu Z, Li J, Wang L, Li Q, Lu Q, Yu Y, Li S, Bai My HY, Xiang F (2016) Repression of callus initiation by the miRNA-directed interaction of auxin–cytokinin in Arabidopsis thaliana. Plant J 87:391–402CrossRefGoogle Scholar
  39. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-Seq data with DESeq2. Genome Biol 15:550CrossRefGoogle Scholar
  40. Mangeon A, Junqueira RM, Sachetto-Martins G (2010) Functional diversity of the plant glycine-rich proteins superfamily. Plant Signal Behav 5:99–104CrossRefGoogle Scholar
  41. Matzke MA, Mosher RA (2014) RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet 15:394–408CrossRefGoogle Scholar
  42. Mitra J, Xu G, Wang B, Li M, Deng X (2013) Understanding desiccation tolerance using the resurrection plant Boea hygrometrica as a model system. Front Plant Sci 4:446CrossRefGoogle Scholar
  43. Mohebodini M, Mokhtar JJ, Mahboudi F, Alizadeh H (2011) Effects of genotype, explant age and growth regulators on callus induction and direct shoot regeneration of lettuce (Lactuca sativa L.). Aust J Crop Sci 5:92–95Google Scholar
  44. Motte H, Vereecke D, Geelen D, Werbrouck S (2014) The molecular path to in vitro shoot regeneration. Biotechnol Adv 32:107–121CrossRefGoogle Scholar
  45. Muday GK, Rahman A, Binder BM (2012) Auxin and ethylene: collaborators or competitors? Trends Plant Sci 17:181–195CrossRefGoogle Scholar
  46. Naing AH, Park KI, Chung MY, Lim KB, Kim CK (2015) Optimization of factors affecting efficient shoot regeneration in chrysanthemum cv. Shinma. Rev Bras Bot 39:975–984CrossRefGoogle Scholar
  47. Nameth B, Dinka SJ, Chatfield SP, Morris A, English J, Lewis D, Oro R, Raizada MN (2013) The shoot regeneration capacity of excised Arabidopsis cotyledons is established during the initial hours after injury and is modulated by a complex genetic network of light signalling. Plant Cell Environ 36:68–86CrossRefGoogle Scholar
  48. Ortega-Galisteo AP, Morales-Ruiz T, Ariza RR, Roldán-Arjona T (2008) Arabidopsis DEMETER-LIKE proteins DML2 and DML3 are required for appropriate distribution of DNA methylation marks. Plant Mol Biol 67:671–681CrossRefGoogle Scholar
  49. Oyama T, Shimura Y, Okada K (1997) The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. Genes Dev 11:2983–2995CrossRefGoogle Scholar
  50. Pertea M, Pertea GM, Antonescu CM, Chang T-C, Mendell JT, Salzberg SL (2015) StringTie enables improved reconstruction of a transcriptome from RNA-Seq reads. Nat Biotechnol 33:290–295CrossRefGoogle Scholar
  51. Radhakrishnan D, Kareem A, Durgaprasad K, Sreeraj E, Sugimoto K, Prasad K (2018) Shoot regeneration: a journey from acquisition of competence to completion. Curr Opin Plant Biol 41:23–31CrossRefGoogle Scholar
  52. Sahrawat AK, Chand S (2001) High-frequency plant regeneration from coleoptile tissue of indica rice (Oryza sativa L.). In Vitro Cell Dev Biol Plant 37:55–61CrossRefGoogle Scholar
  53. Schmid MW, Giraldo-Fonseca A, Rövekamp M, Smetanin D, Bowman JL, Grossniklaus U (2018) Extensive epigenetic reprogramming during the life cycle of Marchantia polymorpha. Genome Biol 19:9CrossRefGoogle Scholar
  54. Shang B, Xu C, Zhang X, Cao H, Xin W, Hu Y (2016) Very-long-chain fatty acids restrict regeneration capacity by confining pericycle competence for callus formation in Arabidopsis. Proc Natl Acad Sci U S A 113:5101–5106CrossRefGoogle Scholar
  55. Shemer O, Landau U, Candela H, Zemach A, Eshed Williams L (2015) Competency for shoot regeneration from Arabidopsis root explants is regulated by DNA methylation. Plant Sci 238:251–261CrossRefGoogle Scholar
  56. Shin DH, Choi M, Kim K, Bang G, Cho M, Choi S-B, Choi G, Park Y-I (2013) HY5 regulates anthocyanin biosynthesis by inducing the transcriptional activation of the MYB75/PAP1 transcription factor in Arabidopsis. FEBS Lett 587:1543–1547CrossRefGoogle Scholar
  57. Skoog F, Miller CO (1957) Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp Soc Exp Biol 11:118–130Google Scholar
  58. Stelpflug SC, Eichten SR, Hermanson PJ, Springer NM, Kaeppler SM (2014) Consistent and heritable alterations of DNA methylation are induced by tissue culture in maize. Genetics 198:209–218CrossRefGoogle Scholar
  59. Stroud H, Ding B, Simon SA, Feng S, Bellizzi M, Pellegrini M, Wang G-L, Meyers BC, Jacobsen SE (2013) Plants regenerated from tissue culture contain stable epigenome changes in rice. Elife 2:e00354CrossRefGoogle Scholar
  60. Su N, He K, Jiao Y, Chen C, Zhou J, Li L, Bai S, Li X, Deng XW (2007) Distinct reorganization of the genome transcription associates with organogenesis of somatic embryo, shoots, and roots in rice. Plant Mol Biol 63:337–349CrossRefGoogle Scholar
  61. Sudan J, Raina M, Singh R (2018) Plant epigenetic mechanisms: role in abiotic stress and their generational heritability. 3 Biotech 8:172CrossRefGoogle Scholar
  62. Sugimoto K, Jiao Y, Meyerowitz EM (2010) Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Dev Cell 18:463–471CrossRefGoogle Scholar
  63. Sun R-Z, Cheng G, Li Q, He Y-N, Wang Y, Lan Y-B, Li S-Y, Zhu Y-R, Song W-F, Zhang X, Cui X-D, Chen W, Wang J (2017) Light-induced variation in phenolic compounds in Cabernet Sauvignon grapes (Vitis vinifera L.) involves extensive transcriptome reprogramming of biosynthetic enzymes, transcription factors, and phytohormonal regulators. Front Plant Sci 8:547CrossRefGoogle Scholar
  64. Sun R-Z, Lin C-T, Zhang X-F, Duan L-X, Qi X-Q, Gong Y-H, Deng X (2018) Acclimation-induced metabolic reprogramming contributes to rapid desiccation tolerance acquisition in Boea hygrometrica. Environ Exp Bot 148:70–84CrossRefGoogle Scholar
  65. Sun R, He F, Lan Y, Xing R, Liu R, Pan Q, Wang J, Duan C (2015) Transcriptome comparison of Cabernet Sauvignon grape berries from two regions with distinct climate. J Plant Physiol 178:43–54CrossRefGoogle Scholar
  66. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-Seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578CrossRefGoogle Scholar
  67. Vaillant I, Paszkowski J (2007) Role of histone and DNA methylation in gene regulation. Curr Opin Plant Biol 10:528–533CrossRefGoogle Scholar
  68. Vandenbussche F, Habricot Y, Condiff AS, Maldiney R, Straeten DVD, Ahmad M (2007) HY5 is a point of convergence between cryptochrome and cytokinin signalling pathways in Arabidopsis thaliana. Plant J 49:428–441CrossRefGoogle Scholar
  69. Vining K, Pomraning KR, Wilhelm LJ, Ma C, Pellegrini M, Di Y, Mockler TC, Freitag M, Strauss SH (2013) Methylome reorganization during in vitro dedifferentiation and regeneration of Populus trichocarpa. BMC Plant Biol 13:92CrossRefGoogle Scholar
  70. Wang L, Long C-L (2003) Tissue culture of Boea hygrometrica. Plant Physiol Commun 39:233Google Scholar
  71. Wang W, Li H, Lin X, Yang S, Wang Z, Fang B (2015) Transcriptome analysis identifies genes involved in adventitious branches formation of Gracilaria lichenoides in vitro. Sci Rep 5:17099CrossRefGoogle Scholar
  72. Xi Y, Li W (2009) BSMAP: whole genome bisulfite sequence MAPping program. BMC Bioinformatics 10:232CrossRefGoogle Scholar
  73. Xu C, Cao H, Zhang Q, Wang H, Xin W, Xu E, Zhang S, Yu R, Yu D, Hu Y (2018a) Control of auxin-induced callus formation by bZIP59–LBD complex in Arabidopsis regeneration. Nat Plants 4:108–115CrossRefGoogle Scholar
  74. Xu J, Zhou S, Gong X, Song Y, Nocker S, Ma F, Guan Q (2018b) Single-base methylome analysis reveals dynamic epigenomic differences associated with water deficit in apple. Plant Biotechnol J 16:672–687CrossRefGoogle Scholar
  75. Xu K, Liu J, Fan M, Xin W, Hu Y, Xu C (2012) A genome-wide transcriptome profiling reveals the early molecular events during callus initiation in Arabidopsis multiple organs. Genomics 100:116–124CrossRefGoogle Scholar
  76. Xu W, Yang T, Dong X, Li D-Z, Liu A (2016) Genomic DNA methylation analyses reveal the distinct profiles in castor bean seeds with persistent endosperms. Plant Physiol 171:1242–1258Google Scholar
  77. Yang H, Chang F, You C, Cui J, Zhu G, Wang L, Zheng Y, Qi J, Ma H (2015) Whole-genome DNA methylation patterns and complex associations with gene structure and expression during flower development in Arabidopsis. Plant J 81:268–281CrossRefGoogle Scholar
  78. Zhang T-Q, Lian H, Zhou C-M, Xu L, Jiao Y, Wang J-W (2017) A two-step model for de novo activation of WUSCHEL during plant shoot regeneration. Plant Cell 29:1073–1087CrossRefGoogle Scholar
  79. Zhong S, Fei Z, Chen Y-R, Zheng Y, Huang M, Vrebalov J, McQuinn R, Gapper N, Liu B, Xiang J, Shao Y, Giovannoni JJ (2013) Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat Biotechnol 31:154–159CrossRefGoogle Scholar
  80. 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 39:61–69CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory of Plant Resources, Institute of BotanyChinese Academy of SciencesBeijingChina

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