Unlocking the Arabidopsis epigenome (original) (raw)
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Genes & Development, 2009
Transgenerational epigenetic inheritance has been defined by the study of relatively few loci. We examined a population of recombinant inbred lines with epigenetically mosaic chromosomes consisting of wild-type and CG methylation-depleted segments (epiRILs). Surprisingly, transposons that were immobile in the parental lines displayed stochastic movement in 28% of the epiRILs. Although analysis after eight generations of inbreeding, supported by genome-wide DNA methylation profiling, identified recombined parental chromosomal segments, these were interspersed with unexpectedly high frequencies of nonparental methylation polymorphism. Hence, epigenetic inheritance in hybrids derived from parents with divergent epigenomes permits long-lasting epi-allelic interactions that violate Mendelian expectations. Such persistently ''unstable'' epigenetic states complicate linkage-based epigenomic mapping. Thus, future epigenomic analyses should consider possible genetic instabilities and alternative mapping strategies.
Transgenerational Stability of the Arabidopsis Epigenome Is Coordinated by CG Methylation
Cell, 2007
Maintenance of CG methylation (m CG) patterns is essential for chromatin-mediated epigenetic regulation of transcription in plants and mammals. However, functional links between m CG and other epigenetic mechanisms in vivo remain obscure. Using successive generations of an Arabidopsis thaliana mutant deficient in maintaining m CG, we find that m CG loss triggers genome-wide activation of alternative epigenetic mechanisms. However, these mechanisms, which involve RNA-directed DNA methylation, inhibiting expression of DNA demethylases, and retargeting of histone H3K9 methylation, act in a stochastic and uncoordinated fashion. As a result, new and aberrant epigenetic patterns are progressively formed over several plant generations in the absence of m CG. Interestingly, the unconventional redistribution of epigenetic marks is necessary to ''rescue'' the loss of m CG, since mutant plants impaired in rescue activities are severely dwarfed and sterile. Our results provide evidence that m CG is a central coordinator of epigenetic memory that secures stable transgenerational inheritance in plants.
Journal of Genetics, 2013
Heritable information in plants consists of genomic information in DNA sequence and epigenetic information superimposed on DNA sequence. The latter is in the form of cytosine methylation at CG, CHG and CHH elements (where H = A, T or C) and a variety of histone modifications in nucleosomes. The epialleles arising from cytosine methylation marks on the nuclear genomic loci have better heritability than the epiallelic variation due to chromatin marks. Phenotypic variation is increased manifold by epiallele comprised methylomes. Plants (angiosperms) have highly conserved genetic mechanisms to establish, maintain or erase cytosine methylation from epialleles. The methylation marks in plants fluctuate according to the cell/tissue/organ in the vegetative and reproductive phases of plant life cycle. They also change according to environment. Epialleles arise by gain or loss of cytosine methylation marks on genes. The changes occur due to the imperfection of the processes that establish and maintain the marks and on account of spontaneous and stress imposed removal of marks. Cytosine methylation pattern acquired in response to abiotic or biotic stress is often inherited over one to several subsequent generations. Cytosine methylation marks affect physiological functions of plants via their effect(s) on gene expression levels. They also repress transposable elements that are abundantly present in plant genomes. The density of their distribution along chromosome lengths affects meiotic recombination rate, while their removal increases mutation rate. Transposon activation due to loss of methylation causes rearrangements such that new gene regulatory networks arise and genes for microRNAs may originate. Cytosine methylation dynamics contribute to evolutionary changes. This review presents and discusses the available evidence on origin, removal and roles of cytosine methylation and on related processes, such as RNA directed DNA methylation, imprinting, paramutation and transgenerational memory in plants.
Genetics, 2014
Pure epigenetic variation, or epigenetic variation that is independent of genetic context, may provide a mechanism for phenotypic variation in the absence of DNA mutations. To estimate the extent of pure epigenetic variation within and across generations and to identify the DNA regions targeted, a group of eight plants derived from a highly inbred line of maize (Zea mays) was analyzed by the methylation-sensitive amplified polymorphism (MSAP) technique. We found that cytosine methylation (mC) differences among individuals accounted for up to 7.4% of CCGG sites investigated by MSAP. Of the differentially methylated fragments (DMFs) identified in the S0 generation, 12% were meiotically inherited for at least six generations. We show that meiotically heritable mC variation was consistently generated for an average of 0.5% CCGG sites per generation and that it largely occurred somatically. We provide evidence that mC variation can be established and inherited in a parent-of-origin manner, given that the paternal lineage is more prone to both forward and reverse mC changes. The molecular characterization of selected DMFs revealed that the variation was largely determined by CG methylation changes that map within gene regions. The expression analysis of genes overlapping with DMFs did not reveal an obvious correlation between mC variation and transcription, reinforcing the idea that the primary function of genebody methylation is not to control gene expression. Because this study focuses on epigenetic variation in field-grown plants, the data presented herein pertain to spontaneous epigenetic changes of the maize genome in a natural context.
American Journal of Botany, 2018
PREMISE OF THE STUDY: The ecological and evolutionary significance of natural epigenetic variation (i.e., not based on DNA sequence variants) variation will depend critically on whether epigenetic states are transmitted from parents to offspring, but little is known on epigenetic inheritance in non-model plants. METHODS: We present a quantitative analysis of transgenerational transmission of global DNA cytosine methylation (= proportion of all genomic cytosines that are methylated) and individual epigenetic markers (= methylation status of anonymous MSAP markers) in the shrub Lavandula latifolia. Methods based on parent-offspring correlations and parental variance component estimation were applied to epigenetic features of field-growing plants ('maternal parents') and greenhouse-grown progenies. Transmission of genetic markers (AFLP) was also assessed for reference. KEY RESULTS: Maternal parents differed significantly in global DNA cytosine methylation (range = 21.7-36.7%). Greenhouse-grown maternal families differed significantly in global methylation, and their differences were significantly related to maternal origin. MSAP markers exhibited significant transgenerational transmission, as denoted by significant maternal variance component of marker scores in greenhouse families and significant mother-offspring correlations of marker scores. CONCLUSIONS: Although transmission-related measurements for global methylation and MSAP markers were quantitatively lower than those for AFLP markers taken as reference, this study has revealed extensive transgenerational transmission of genomewide global cytosine methylation and anonymous epigenetic markers in L. latifolia. Similarity of results for global cytosine methylation and epigenetic markers lends robustness to this conclusion, and stresses the value of considering both types of information in epigenetic studies of non-model plants.
From epigenetics to epigenomics and their implications in plant breeding
2012
Higher organisms, including plants, use three systems to initiate and sustain epigenetic gene regulation: DNA methylation, histone modification, and RNA-interference. Unraveling the relationships between these epigenetic components has led to surprising and rapidly evolving new concepts, showing how they interact and stabilize each other. These interacting systems can regulate expression or silencing of genes, resulting in epigenetically controlled phenotypes that can be meiotically or mitotically heritable. In this review we discuss issues relevant to the involvement of epigenetic inheritance as a source of polymorphism generating useful variation for selecting superior genotypes. The role of methylation in hybrid vigor and stability of performance, and aspects of epigenetic transgene silencing in elite transgenic varieties will also be addressed.
Evolutionary Ecology, 2010
Heritable phenotypic variation in plants can be caused not only by underlying genetic differences, but also by variation in epigenetic modifications such as DNA methylation. However, we still know very little about how relevant such epigenetic variation is to the ecology and evolution of natural populations. We conducted a greenhouse experiment in which we treated a set of natural genotypes of Arabidopsis thaliana with the demethylating agent 5-azacytidine and examined the consequences of this treatment for plant traits and their phenotypic plasticity. Experimental demethylation strongly reduced the growth and fitness of plants and delayed their flowering, but the degree of this response varied significantly among genotypes. Differences in genotypes’ responses to demethylation were only weakly related to their genetic relatedness, which is consistent with the idea that natural epigenetic variation is independent of genetic variation. Demethylation also altered patterns of phenotypic plasticity, as well as the amount of phenotypic variation observed among plant individuals and genotype means. We have demonstrated that epigenetic variation can have a dramatic impact on ecologically important plant traits and their variability, as well as on the fitness of plants and their ecological interactions. Epigenetic variation may thus be an overlooked factor in the evolutionary ecology of plant populations.
Epigenetic mechanisms in plants and their implications in plant breeding
In the wake of the …, 2005
Higher organisms, including plants, use three systems to initiate and sustain epigenetic gene regulation: DNA methylation, histone modification and RNA-interference. Unraveling the relationships between these epigenetic components has led to surprising and rapidly evolving new concepts, showing how they interact and stabilize each other. These interacting systems can regulate expression or silencing of genes, resulting in epigenetically controlled phenotypes that can be meiotically or mitotically heritable. In this review we discuss issues relevant to the involvement of epigenetic inheritance as a source of polymorphism generating useful variation for selecting superior genotypes. The role of methylation in hybrid vigor and stability of performance, and aspects of epigenetic transgene silencing in elite transgenic varieties will also be addressed.