Cited by 55Plant tissue culture and regenerationPlant Genetic and Mutation StudiesGenetically Modified Organisms Research

Tissue culture-induced genetic and epigenetic alterations in rice pure-lines, F1 hybrids and polyploids

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Wang, Xiaoran, Wu, Rui, Lin, Xiuyun, Bai, Yan, Song, Congdi, Yu, Xiaoming, Xu, Chunming, Zhao, Na +2 more·2013·BMC Plant Biology

Abstract

Background: Genetic and epigenetic alterations can be invoked by plant tissue culture, which may result in heritable changes in phenotypes, a phenomenon collectively termed somaclonal variation. Although extensive studies have been conducted on the molecular nature and spectrum of tissue culture-induced genomic alterations, the issue of whether and to what extent distinct plant genotypes, e.g., pure-lines, hybrids and polyploids, may respond differentially to the tissue culture condition remains poorly understood. Results: We investigated tissue culture-induced genetic and epigenetic alterations in a set of rice genotypes including two pure-lines (different subspecies), a pair of reciprocal F1 hybrids parented by the two pure-lines, and a pair of reciprocal tetraploids resulted from the hybrids. Using two molecular markers, amplified fragment length polymorphism (AFLP) and methylation-sensitive amplified polymorphism (MSAP), both genetic and DNA methylation alterations were detected in calli and regenerants from all six genotypes, but genetic alteration is more prominent than epigenetic alteration. While significant genotypic difference was observed in frequencies of both types of alterations, only genetic alteration showed distinctive features among the three types of genomes, with one hybrid (N/9) being exceptionally labile. Surprisingly, difference in genetic alteration frequencies between the pair of reciprocal F1 hybrids is much greater than that between the two pure-line subspecies. Difference also exists in the pair of reciprocal tetraploids, but is to a less extent than that between the hybrids. The steady-state transcript abundance of genes involved in DNA repair and DNA methylation was significantly altered in both calli and regenerants, and some of which were correlated with the genetic and/or epigenetic alterations. Conclusions: Our results, based on molecular marker analysis of ca. 1,000 genomic loci, document that genetic alteration is the major cause of somaclonal variation in rice, which is concomitant with epigenetic alterations. Perturbed expression by tissue culture of a set of 41 genes encoding for enzymes involved in DNA repair and DNA methylation is associated with both genetic and epigenetic alterations. There exist fundamental differences among distinct genotypes, pure-lines, hybrids and tetraploids, in propensities of generating both genetic and epigenetic alterations under the tissue culture condition. Parent-of-origin has a conspicuous effect on the alteration frequencies.

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  • Epigenetic variability observed at the phenotype level reflects adaptations of cellular processes to constraints of in vitro cultivation, which usually implies sequential dedifferentiation and re-differentiation.

    “This epigenetic variability, which frequently is observed at phenotype level, reflects, in reality, the adaptations of the cellular processes to the various constraints of the in vitro cultivation technology, that usually implies sequential dedifferentiation (formation of callus) and re-differentiation (regeneration of plants) [91,95,96,97,98,99,100].”

    From Somaclonal Variation—Advantage or Disadvantage in Micropropagation of the Medicinal Plants (2023) · cites this paper as [99]

    The Background (page unavailable) describes tissue culture as sequential dedifferentiation and re-differentiation, says it provokes genetic and epigenetic instability, and notes that some alterations can appear as phenotypic changes. It does not establish that such changes frequently occur at the phenotype level or that they reflect adaptive cellular processes; the Conclusions instead identify genetic alteration as the major component of somaclonal variation in rice. (LLM, conf=0.86)

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  • Global DNA methylation is the most evaluated epigenetic somaclonal variation; in plants it is at higher levels than in other eukaryotes and is correlated with expression of different genes and changes in mobility of transposable elements.

    “The most evaluated epigenetic somaclonal variation is global DNA methylation, which, in plants, is at higher levels compared with other eukaryotes, and is correlated with the expression of different genes, and changes in the mobility of the numerous transposable elements presented in plant genomes [99,101,102,103,104,105,106,107,108,109].”

    From Somaclonal Variation—Advantage or Disadvantage in Micropropagation of the Medicinal Plants (2023) · cites this paper as [99]

    The Results section on epigenetic alteration in rice calli and regenerants measures changes in DNA methylation patterns as somaclonal variation, and the Discussion describes transposable-element reactivation in plant tissue culture. The paper does not establish that methylation is the most evaluated epigenetic somaclonal variation, that plants have higher methylation levels than other eukaryotes, or that methylation changes correlate with expression of different genes and transposable-element mobility. Its Conclusions instead associate altered expression of genes involved in DNA methylation with genetic and epigenetic alterations in rice; page numbers are unavailable in our copy. (LLM, conf=0.86)

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Cited by

Sorted by citations

Authors
Wang, X., Wu, R., Lin, X., Bai, Y., Song, C., Yu, X., Xu, C., Zhao, N., Dong, Y., & Liu, B.
Affiliations
  • Northeast Normal University (CN)
  • Jilin Academy of Agricultural Sciences (CN)
  • Jilin Agricultural University (CN)
  • Changchun Normal University (CN)
Corresponding author
Dong, Yuzhu
Venue
BMC Plant Biology
Published
2013-05-05
Volume
13
Issue
1
Pages
77-77
ISSN
1471-2229 (ISSN-L)
OpenAlex
W2154584760
Cited by
55
References
0
Citations by year
2026: 1 · 2024: 4 · 2023: 3 · 2022: 5 · 2021: 4 · 2020: 5 · 2019: 2 · 2018: 3 · 2017: 5 · 2016: 5 · 2015: 6 · 2014: 10 · 2013: 1 · 2012: 1
FWCI
3.28
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • BMC Plant Biology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
National Natural Science Foundation of China (31200198)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant tissue culture and regeneration
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Genetic and Mutation Studies
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Genetically Modified Organisms Research
Keywords
somaclonal variation, rice, F1 hybrids, tetraploid, pure lines, DNA methylation, epigenetic modifications, callus, regenerants, DNA repair genes, parent-of-origin effects, genotype-dependent response
MeSH terms
Genotype, Inbreeding, Phenotype, Plant Proteins, Polyploidy, Oryza, DNA, Plant, DNA Methylation, Epigenesis, Genetic, Tissue Culture Techniques

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