CoChat
Sign Up
Cited by 27Epigenetics and DNA MethylationPlant tissue culture and regenerationPlant Molecular Biology Research

Whole-Genome Bisulfite Sequencing Reveals a Role for DNA Methylation in Variants from Callus Culture of Pineapple (Ananas comosus L.)

Open access
Lin, Wenqiu, Xiao, Xi’ou, Zhang, Hongna, Li, Yunhe, Liu, Shenghui, Sun, Weisheng, Zhang, Xiumei, Wu, Qingsong·2019·Genes
DOI 10.3390/genes10110877PMC PMC6895883
Open this paper in CoChat — free accountOpen PDF

Abstract

DNA methylation changes can occur in some loci during callus culture, resulting in somaclonal variations (SVs). In the present study, we applied whole genome bisulfite sequencing to analyze context-specific DNA methylation changes in the pineapple genome between the cutting seedings and 5 SV plants. In general, SV plants exhibited methylation patterns analogous to those of cutting seedlings (CK). A total of 27.98% of the genomic cytosines of CK were methylcytosines, which was higher than that of 5 SV plants. Moreover, mCG and mCHG was hypermethylated, whereas mCHH was hypomethylated among the 5 SV plants genomic when compared with the CK. Most of the variation of DNA methylation was distributed in gene bodies, thus suggesting that phenotypic differences are probably perturbed by genes methylated from callus culture. In addition, the methylated genes were highly enriched for the Gene Ontology (GO) categories of binding and catalytic activity, cell part and organelle, cellular process, abiotic stimulus, and DNA modification. These results suggest that methylation mediates these pathways in the callus culture of pineapple. The results also suggested that the callus culture induced DNA methylation may result in the SV.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3390/genes10110877

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

No citation lists for this paper

No citation lists for this paper yet — checked again daily.

References 34 · Cited by 27

Research works printed but not linked: 30

  1. [1]Papa C.M. Springer N.M. Muszynski M.G. Meeley R. Kaeppler S.M. Maize Chromomethylase Zea methyltransferase2 Is Required for CpNpG Methylation Plant Cell 2001 13 1919 1928 10.1105/TPC.010064 11487702 PMC139128 · DOI
  2. [2]Quinga L.A.P. Fraga H.P.D.F. Vieira L.D.N. Guerra M.P. Epigenetics of long-term somatic embryogenesis in Theobroma cacao L.: DNA methylation and recovery of embryogenic potential Plant Cell Tissue Organ Cult. 2017 131 295 305 10.1007/s11240-017-1284-6 · DOI
  3. [3]Bartels A. Han Q. Nair P. Stacey L. Gaynier H. Mosley M. Huang Q.Q. Pearson J.K. Hsieh T.-F. An Y.-Q.C. Dynamic DNA Methylation in Plant Growth and Development Int. J. Mol. Sci. 2018 19 2144 10.3390/ijms19072144 30041459 PMC6073778 · DOI
  4. [4]Bardini M. Labra M. Winfield M. Sala F. Antibiotic-induced DNA methylation changes in calluses of Arabidopsis thaliana Plant Cell Tissue Organ Cult. 2003 72 157 162 10.1023/A:1022208302819 · DOI
  5. [5]Zhang H. Lang Z. Zhu J.-K. Dynamics and function of DNA methylation in plants Nat. Rev. Mol. Cell Boil. 2018 19 489 506 10.1038/s41580-018-0016-z 29784956 · DOI
  6. [6]Larkin P.J. Scowcroft W.R. Somaclonal variation—A novel source of variability from cell cultures for plant improvement Theor. Appl. Genet. 1981 60 197 214 10.1007/BF02342540 24276737 · DOI
  7. [7]Jaligot E. Rival A. Beule T. Dussert S. Verdeil J.-L. Somaclonal variation in oil palm (Elaeis guineensis Jacq.): The DNA methylation hypothesis Plant Cell Rep. 2000 19 684 690 10.1007/s002999900177 30754806 · DOI · Paper page
  8. [8]Schellenbaum P. Mohler V. Wenzel G. Walter B. Variation in DNA methylation patterns of grapevine somaclones (Vitis vinifera L.) BMC Plant Boil. 2008 8 78 10.1186/1471-2229-8-78 PMC2491626 18627604 · DOI
  9. [10]Landey R.B. Cenci A. Guyot R. Bertrand B. Georget F. Dechamp E. Herrera J.-C. Aribi J. Lashermes P. Etienne H. Assessment of genetic and epigenetic changes during cell culture ageing and relations with somaclonal variation in Coffea arabica Plant Cell Tissue Organ Cult. 2015 122 517 531 10.1007/s11240-015-0772-9 · DOI
  10. [11]Machczyńska J. Orłowska R. Mańkowski D.R. Zimny J. Bednarek P.T. DNA methylation changes in triticale due to in vitro culture plant regeneration and consecutive reproduction Plant Cell Tissue Organ Cult. 2014 119 289 299 10.1007/s11240-014-0533-1 · DOI
  11. [12]González A.I. Saiz A. Acedo A. Ruiz M.L. Polanco C. Analysis of genomic DNA methylation patterns in regenerated and control plants of rye (Secale cereale L.) Plant Growth Regul. 2013 70 227 236 10.1007/s10725-013-9794-7 · DOI
  12. [13]Meilina O. Ordway J.M. Jiang N. Loss of Karma transposon methylation underliesthe mantled somaclonal variant of oil palm Nature 2015 10.1038/nature15365 PMC4857894 26352475 · DOI
  13. [14]Wakasa K. Vaeiation in the plants differentiated from the tissue cuture of pineapple Jpn. J. Breed. 1979 29 13 22 10.1270/jsbbs1951.29.13 · DOI
  14. [17]Soneji J.R. Rao P.S. Mhatre M. Somaclonal variation in micropropagated dormant axillary buds of pineapple (Ananas comosus L., Merr.) J. Hortic. Sci. Biotechnol. 2002 77 28 32 10.1080/14620316.2002.11511452 · DOI
  15. [18]Pérez G. Yanez E. Mbogholi A. Valle B. Sagarra F. Yabor L. Aragon C. Gonzalez J. Isidron M. Lorenzo J.C. New pineapple somaclonal variants: P3R5 and Dwarf Am. J. Plant Sci. 2012 3 1 11 10.4236/ajps.2012.31001 · DOI
  16. [19]Scherer R.F. Fraga H.P.D.F. Klabunde G.F. Da Silva D.A. Guerra M.P. Global DNA Methylation Levels During the Development of Nodule Cluster Cultures and Assessment of Genetic Fidelity of In Vitro-Regenerated Pineapple Plants (Ananas comosus var. comosus) J. Plant Growth Regul. 2015 34 677 683 10.1007/s00344-015-9493-x · DOI
  17. [20]Halim N.A.A. Tan B.C. Midin M.R. Madon M. Khalid N. Yaacob J.S. Abscisic acid and salinity stress induced somaclonal variationand increased histone deacetylase (HDAC) activity in Ananas comosus var. MD2 Plant Cell Tissue Organ Cult. 2018 133 123 135 10.1007/s11240-017-1367-4 · DOI
  18. [21]Coronel C.J. González A.I. Ruiz M.L. Polanco C. Analysis of somaclonal variation in transgenic and regenerated plants of arabidopsis thaliana using methylation related metaflp and tmd markers Plant Cell Rep. 2018 37 137 152 10.1007/s00299-017-2217-x 29038910 · DOI
  19. [22]Ghosh A. Igamberdiev A.U. Debnath S.C. Detection of DNA methylation pattern in thidiazuron-induced blueberry callus using methylation-sensitive amplification polymor-phism Biol. Plant. 2017 61 511 519 10.1007/s10535-016-0678-3 · DOI
  20. [23]Niederhuth C.E. Bewick A.J. Ji L.X. Alabady M.S. Kim K.D. Li Q. Rohr N.A. Rambani A. Burke J.M. Udall J.A. Widespread natural variation of DNA methylation within angiosperms Genome Biol. 2016 17 194 10.1186/s13059-016-1059-0 27671052 PMC5037628 · DOI
  21. [24]Xi Y. Li W. BSMAP: Whole genome bisulfite sequence MAPping program BMC Bioinform. 2009 10 232 10.1186/1471-2105-10-232 19635165 PMC2724425 · DOI
  22. [25]Kaeppler S.M. Phillips R.L. Tissue culture-induced DNA methylation variation in maize Proc. Natl. Acad. Sci. USA 1993 90 8773 8776 10.1073/pnas.90.19.8773 8415605 PMC47442 · DOI · Paper page
  23. [26]Matthes M. Singh R. Cheah S.-C. Karp A. Variation in oil palm (Elaeis guineensis Jacq.) tissue culture-derived regenerants revealed by AFLPs with methylation-sensitive enzymes Theor. Appl. Genet. 2001 102 971 979 10.1007/s001220000491 · DOI
  24. [27]Joyce S.M. Cassells A.C. Variation in potato microplant morphology in vitro and DNA methylation Plant Cell Tissue Organ Cult. 2002 70 125 137 10.1023/A:1016312303320 · DOI
  25. [28]Law J.A. Jacobsen S.E. Establishing; maintaining and modifying DNA methylation patterns in plants and animals Nat. Rev. Genet. 2010 11 204 10.1038/nrg2719 20142834 PMC3034103 · DOI
  26. [29]Chakrabarty D. Yu K. Paek K. Detection of DNA methylation changes during somatic embryogenesis of Siberian ginseng (Eleuterococcus senticosus) Plant Sci. 2003 165 61 68 10.1016/S0168-9452(03)00127-4 · DOI · Paper page
  27. [30]Francischini J. Kemper E. Costa J. Manechini J. Pinto L. DNA methylation in sugarcane somaclonal variants assessed through methylation-sensitive amplified polymorphism Genet. Mol. Res. 2017 16 10.4238/gmr16029585 28481402 · DOI
  28. [31]Stroud H. Ding B. Simon S.A. Feng S. Bellizzi M. Pellegrini M. Wang G.-L. Meyers B.C. Jacobsen S.E. Plants regenerated from tissue culture contain stable epigenome changes in rice eLife 2013 2 10.7554/eLife.00354 23539454 PMC3601819 · DOI
  29. [32]Hsu F.-M. Gohain M. Allishe A. Huang Y.-J. Liao J.-L. Kuang L.-Y. Chen P.-Y. Dynamics of the Methylome and Transcriptome during the Regeneration of Rice Epigenomes 2018 2 14 10.3390/epigenomes2030014 · DOI
  30. [34]West P.T. Li Q. Ji L. Eichten S.R. Song J. Vaughn M.W. Schmitz R.J. Springer N.M. Genomic Distribution of H3K9me2 and DNA Methylation in a Maize Genome PLoS ONE 2014 9 e105267 10.1371/journal.pone.0105267 25122127 PMC4133378 · DOI

Authors
Lin, W., Xiao, X., Zhang, H., Li, Y., Liu, S., Sun, W., Zhang, X., & Wu, Q.
Affiliations
Chinese Academy of Tropical Agricultural Sciences (CN)
Corresponding author
Wu, Qingsong
ORCID
Venue
Genes
Publisher
MDPI AG
Published
2019-11-01
Volume
10
Issue
11
Pages
877
ISSN
2073-4425 (ISSN-L)
DOI
10.3390/genes10110877
PMC
PMC6895883
OpenAlex
W2989271678
Cited by
27
References
34
Citations by year
2026: 5 · 2025: 4 · 2024: 4 · 2023: 3 · 2022: 6 · 2021: 3 · 2020: 2
FWCI
0.91
Type
journal article
Language
en
Open access
Licence
Locations
  • Genes (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Greater South Information System
Funders
  • Natural Science Foundation of Hainan Province (No. 317244)
  • Central Public-interest Scientific Institution Basal Research Fund for Chinese Academy of Tropical Agricultural Sciences (No. 1630062019025)
  • the Natural Science Foundation of Guangdong Province (No. 2017A030307003)
  • the National Natural Science Foundation of China (No. 31601733)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant tissue culture and regeneration
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
Keywords
DNA methylation, somaclonal variation, pineapple, callus culture, whole-genome bisulfite sequencing, gene body methylation, methylated genes, epigenetic regulation
MeSH terms
Whole Genome Sequencing, Gene Expression Regulation, Plant, Genome, Plant, DNA Methylation, Ananas, Plant Somatic Embryogenesis Techniques

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review