Consistent and Heritable Alterations of DNA Methylation Are Induced by Tissue Culture in Maize
Open accessAbstract
Plants regenerated from tissue culture and their progenies are expected to be identical clones, but often display heritable molecular and phenotypic variation. We characterized DNA methylation patterns in callus, primary regenerants, and regenerant-derived progenies of maize using immunoprecipitation of methylated DNA (meDIP) to assess the genome-wide frequency, pattern, and heritability of DNA methylation changes. Although genome-wide DNA methylation levels remained similar following tissue culture, numerous regions exhibited altered DNA methylation levels. Hypomethylation events were observed more frequently than hypermethylation following tissue culture. Many of the hypomethylation events occur at the same genomic sites across independent regenerants and cell lines. The DNA methylation changes were often heritable in progenies produced from self-pollination of primary regenerants. Methylation changes were enriched in regions upstream of genes and loss of DNA methylation at promoters was associated with altered expression at a subset of loci. Differentially methylated regions (DMRs) found in tissue culture regenerants overlap with the position of naturally occurring DMRs more often than expected by chance with 8% of tissue culture hypomethylated DMRs overlapping with DMRs identified by profiling natural variation, consistent with the hypotheses that genomic stresses similar to those causing somaclonal variation may also occur in nature, and that certain loci are particularly susceptible to epigenetic change in response to these stresses. The consistency of methylation changes across regenerants from independent cultures suggests a mechanistic response to the culture environment as opposed to an overall loss of fidelity in the maintenance of epigenetic states.
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Tissue culture induces consistent homozygous DNA methylation changes inherited across multiple independent lines.
“For example, the study found that tissue culture induces consistent homozygous DNA methylation changes inherited across multiple independent lines.”
From Somaclonal Variation and Clonal Fidelity in Commercial Micropropagation: Challenges and Perspectives (2025) · cites this paper as [152]
The Discussion reports methylation changes at the same regions in many independent maize lines and says most hypomethylation events were heritable in progeny. It says those changes “appear to reflect” changes to both alleles, however, so the claim presents inferred homozygosity as a definitive finding. Page numbers are unavailable in our copy. (LLM, conf=0.84)
Experimental — accuracy not yet measuredWGBS revealed methylation changes in several micropropagated species of maize.
“WGBS has revealed methylation changes in several micropropagated species of maize [152].”
From Somaclonal Variation and Clonal Fidelity in Commercial Micropropagation: Challenges and Perspectives (2025) · cites this paper as [152]
The Methods section ('meDIP-Chip Epigenomic Profiling and qPCR Assays'; page unavailable) says the authors detected methylation changes using methylated-DNA immunoprecipitation followed by a microarray, not WGBS. 'Discovery of tissue culture induced DMRs' (page unavailable) describes regenerated plants from four cultures of one maize genotype, A188, rather than several maize species. The Discussion mentions WGBS data from other maize studies, but not as the method used to detect these tissue-culture changes. (LLM, conf=0.90)
Experimental — accuracy not yet measuredWhile not all changes in callus plants are observed in primary regenerants, most methylation alterations in primary regenerants are passed onto subsequent generations.
“While not all changes in callus plants are observed in primary regenerants, most methylation alterations in primary regenerants are passed onto subsequent generations.”
From Somaclonal Variation and Clonal Fidelity in Commercial Micropropagation: Challenges and Perspectives (2025) · cites this paper as [152]
In “Many tissue culture DMRs are heritable” (page unavailable), the paper reports that about 60% of hypomethylated regions in the primary regenerants were detected in both tested offspring, but only 7% of hypermethylated regions were stably inherited. Thus, “most methylation alterations” overstates the result. The section also says most changes observed in regenerants were already present in callus; it does not establish the converse claim that some changes in callus were absent from primary regenerants. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThese changes, including both gains and losses of DNA methylation in CG and CHG contexts, suggest that specific loci may act as hotspots for epigenetic variation.
“These changes, including both gains and losses of DNA methylation in CG and CHG contexts, suggest that specific loci may act as hotspots for epigenetic variation.”
From Somaclonal Variation and Clonal Fidelity in Commercial Micropropagation: Challenges and Perspectives (2025) · cites this paper as [152]
The Discovery of tissue culture induced DMRs section reports both gains and losses of methylation and finds that some genomic regions change consistently across independent cultures. The Discussion says specific regions are sensitive to tissue-culture stress. But it also states that the study’s meDIP-array profiling cannot distinguish methylation contexts, so it does not establish that both gains and losses occurred in CG and CHG contexts. Page numbers are not available in our copy. (LLM, conf=0.88)
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- Authors
- Stelpflug, S. C., Eichten, S. R., Hermanson, P. J., Springer, N. M., & Kaeppler, S. M.
- Affiliations
- University of Wisconsin–Madison (US)
- University of Minnesota (US)
- Corresponding author
- Kaeppler, Shawn M
- Venue
- Genetics
- Publisher
- Oxford University Press (OUP)
- Published
- 2014-07-14
- Volume
- 198
- Issue
- 1
- Pages
- 209-218
- ISSN
- 0016-6731 (ISSN-L)
- 1943-2631
- PMC
- PMC4174933
- OpenAlex
- W2086334204
- Cited by
- 90
- References
- 44
- Citations by year
- 2026: 6 · 2025: 3 · 2024: 6 · 2023: 8 · 2022: 12 · 2021: 15 · 2020: 5 · 2019: 8 · 2018: 9 · 2017: 6 · 2016: 5 · 2015: 7
- FWCI
- 2.46
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- Genetics (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- ANU Open Research (Australian National University) (submittedVersion)
- Funders
- Division of Materials Research
- 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, maize, tissue culture, somaclonal variation, epigenetic inheritance, differentially methylated regions, promoter hypomethylation, gene expression, callus, regenerants, methylated DNA immunoprecipitation
- MeSH terms
- Cells, Cultured, Zea mays, Seeds, Plant Leaves, Genome, Plant, DNA Methylation, Epigenesis, Genetic
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