Tissue Culture-Induced Novel Epialleles of a<i>Myb</i>Transcription Factor Encoded by<i>pericarp color1</i>in Maize

Rhee, Yong; Sekhon, Rajandeep S.; Chopra, Surinder; Kaeppler, Shawn M.

doi:10.1534/genetics.110.117929

Cited by 46 publications

(43 citation statements)

References 59 publications

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“…The rate of occurrence of aberrant phenotypes is higher than observed for normally propagated plants and appears to reflect a higher "mutagenic" rate during tissue culture. Detailed characterization of particular somaclonal variants has revealed evidence for novel TE insertions as well as epigenetic changes (Rhee et al 2009(Rhee et al , 2010. It is worth noting that the consistent DNA methylation changes observed in this study and in a prior study in rice (Stroud et al 2013) would predict a tissue culture "syndrome" that would be observed in many of the plants regenerated from culture.…”

Section: Discussionsupporting

confidence: 69%

“…Somaclonal variation has been well characterized in a number of plants species, and generally results in the occurrence of unexpected phenotypes in progeny that arise from tissue culture (Kaeppler and Phillips 1993;Kaeppler et al 2000;Thorpe 2006;Rhee et al 2010;Miguel and Marum 2011;Neelakandan and Wang 2012). The rate of occurrence of aberrant phenotypes is higher than observed for normally propagated plants and appears to reflect a higher "mutagenic" rate during tissue culture.…”

Section: Discussionmentioning

confidence: 99%

“…Heritable epialleles have been characterized in progeny of regenerated plants. For instance, epialleles of the P locus, which controls cob color in maize, were associated with reversible hypermethylation of the second intron (Rhee et al 2010). Interestingly, a naturally occurring epiallele at P has also been reported (Sekhon et al 2007), indicating that similar epigenetic responses to stress that occur in tissue cultured cells may also occur in plants grown in the field.…”

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Consistent and Heritable Alterations of DNA Methylation Are Induced by Tissue Culture in Maize

et al. 2014

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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 regenerantderived 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. C LONAL propagation of plants and animals is expected to produce individuals identical to the donor. However, this is often not the case. Plant tissue culture involves dedifferentiation, or return to a "stem-cell-like" state, which involves dynamic reprogramming at the chromatin level to induce the formation of callus. Subsequently, proliferating cells start to redifferentiate when specific changes in the balance of growth regulators are introduced in the culture medium, ultimately leading to organogenesis or regeneration into whole plants (Grafi et al. 2011;Miguel and Marum 2011). This process represents a traumatic stress to plant cells and often provokes an array of genetic and epigenetic instabilities that are somatically and meiotically heritable (Phillips et al. 1994;Kaeppler et al. 2000). This suite of molecular and phenotypic phenomena is collectively termed somaclonal variation (Larkin and Scowcroft 1981).At the cellular and molecular levels, somaclonal variation is composed of chromosome rearrangements, polyploidy and aneuploidy, DNA sequence changes, activation of quiescent transposable elements (TEs), and epigenetic variation reflected by altered DNA methylation patterns (Karp and Maddock 1984;Brettell et al. 1986;Dennis et al. 1987;Pe...

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Section: Discussionsupporting

confidence: 69%

Section: Discussionmentioning

confidence: 99%

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confidence: 99%

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Consistent and Heritable Alterations of DNA Methylation Are Induced by Tissue Culture in Maize

et al. 2014

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“…Tissue culture-induced epigenetic somaclonal variation of an endogenous gene was demonstrated in maize by identifying novel epialleles of a myb transcription factor, pericarp color 1, which affects the flavonoid biosynthesis pathway in maize seeds (Rhee et al 2010). The progenitor allele, P1-wr, consists of tandem copies of the gene and produces brick-red color in the cob glume.…”

Section: Dna Methylationmentioning

confidence: 99%

Recent progress in the understanding of tissue culture-induced genome level changes in plants and potential applications

2011

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In vitro cell and tissue-based systems have tremendous potential in fundamental research and for commercial applications such as clonal propagation, genetic engineering and production of valuable metabolites. Since the invention of plant cell and tissue culture techniques more than half a century ago, scientists have been trying to understand the morphological, physiological, biochemical and molecular changes associated with tissue culture responses. Establishment of de novo developmental cell fate in vitro is governed by factors such as genetic make-up, stress and plant growth regulators. In vitro culture is believed to destabilize the genetic and epigenetic program of intact plant tissue and can lead to chromosomal and DNA sequence variations, methylation changes, transposon activation, and generation of somaclonal variants. In this review, we discuss the current status of understanding the genomic and epigenomic changes that take place under in vitro conditions. It is hoped that a precise and comprehensive knowledge of the molecular basis of these variations and acquisition of developmental cell fate would help to devise strategies to improve the totipotency and embryogenic capability in recalcitrant species and genotypes, and to address bottlenecks associated with clonal propagation.

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“…1. It has been suggested that such epigenetic changes during tissue culture are a major source of somaclonal variation (Kaeppler et al, 2000;Rhee et al, 2010;Miguel & Marum, 2011;Neelakandan & Wang, 2012;Stelpflug et al, 2014;Ong-Abdullah et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Importance of DNA and histone methylation in in vitro plant propagation for crop improvement: a review

Karim

Nuruzzaman

Khalid

et al. 2016

Annals of Applied Biology

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Epigenetic changes including DNA and histone methylation may reorganise the nuclear architecture during in vitro culture. The states of methylation resulting from in vitro cultures are often related to control the somatic embryogenesis and regeneration process via modulating gene expression. By changing the methylation profile, it is possible to alter gene expression which may be applicable to produce large number of high quality planting materials or to improve agronomic traits leading to crop improvement. Understanding the molecular mechanisms of methylation alterations and acquisition of developmental cell fate during in vitro cultures can help in the development of strategies to enhance the embryogenic capability and totipotency in recalcitrant plant species and genotypes. Moreover, the methylation profile may also be useful to adapt crops under adverse environment as the plants undergo through various stresses during in vitro cultures. In this article, we review the literature on the role of DNA and histone methylation in plant variation and discuss the potential of targeted epigenetic variation for crop improvement.

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Tissue Culture-Induced Novel Epialleles of aMybTranscription Factor Encoded bypericarp color1in Maize

Cited by 46 publications

References 59 publications

Consistent and Heritable Alterations of DNA Methylation Are Induced by Tissue Culture in Maize

Consistent and Heritable Alterations of DNA Methylation Are Induced by Tissue Culture in Maize

Recent progress in the understanding of tissue culture-induced genome level changes in plants and potential applications

Importance of DNA and histone methylation in in vitro plant propagation for crop improvement: a review

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