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


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.


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



2,4-dichlorophenoxyacetic acid




abscisic acid


bisulfite sequencing PCR


differentially expressed gene


differentially methylated gene


differentially methylated region


Gene Ontology


Kyoto Encyclopedia of Genes and Genomes




leaves from mature plants


quantitative real-time PCR


high-throughput mRNA sequencing


shoot-inducing medium


whole-genome bisulfite sequencing


leaves from young seedlings


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.


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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High resolution image (TIF 2606 kb)
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Table S10 (XLSX 11 kb)


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© 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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