Epigenetic variation in plant responses to defence hormones

Latzel, Vít; Zhang, Yuanye; Moritz, Kim Karlsson; Fischer, Markus; Bossdorf, Oliver

doi:10.1093/aob/mcs088

Cited by 74 publications

(65 citation statements)

References 47 publications

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“…Because of this limitation, it has been argued that the epiRILs constitute an ideal system for the study of epigenetic inheritance in Arabidopsis (17,(32)(33)(34). We and others have shown recently that many adaptive phenotypes, such as plant height, flowering time, and growth rate, are highly heritable in this population (12,35,36). Segregating phenotypic effects also have been observed in another epiRIL population which was obtained from a cross between Col(met1) and Col(WT) (37).…”

Section: Discussionmentioning

confidence: 88%

Features of the Arabidopsis recombination landscape resulting from the combined loss of sequence variation and DNA methylation

Colomé-Tatché

Cortijo

Wardenaar

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

136

143

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The rate of meiotic crossing over (CO) varies considerably along chromosomes, leading to marked distortions between physical and genetic distances. The causes underlying this variation are being unraveled, and DNA sequence and chromatin states have emerged as key factors. However, the extent to which the suppression of COs within the repeat-rich pericentromeric regions of plant and mammalian chromosomes results from their high level of DNA polymorphisms and from their heterochromatic state, notably their dense DNA methylation, remains unknown. Here, we test the combined effect of removing sequence polymorphisms and repeat-associated DNA methylation on the meiotic recombination landscape of an Arabidopsis mapping population. To do so, we use genome-wide DNA methylation data from a large panel of isogenic epigenetic recombinant inbred lines (epiRILs) to derive a recombination map based on 126 meiotically stable, differentially methylated regions covering 81.9% of the genome. We demonstrate that the suppression of COs within pericentromeric regions of chromosomes persists in this experimental setting. Moreover, suppression is reinforced within 3-Mb regions flanking pericentromeric boundaries, and this effect appears to be compensated by increased recombination activity in chromosome arms. A direct comparison with 17 classical Arabidopsis crosses shows that these recombination changes place the epiRILs at the boundary of the range of natural variation but are not severe enough to transgress that boundary significantly. This level of robustness is remarkable, considering that this population represents an extreme with key recombination barriers having been forced to a minimum.eiotic recombination is a fundamental process in genetics whereby maternally and paternally inherited homologous chromosomes exchange material, either nonreciprocally by gene conversion or reciprocally by crossing over (CO). COs are not distributed uniformly along the genome but occur more often in chromosome arms and are strongly suppressed in pericentromeric regions (1-3), partly as a result of sequence and chromatin determinants (1,(4)(5)(6)(7)(8). It is commonly believed that in plants and mammals high levels of DNA sequence polymorphisms as well as heterochromatic features associated with repeats, notably dense DNA methylation and transcriptional silencing, play a central role in this suppression (1, 4).Suppression of COs by dense DNA methylation has been demonstrated experimentally in the fungus Ascobolus (7). Specifically, COs were reduced when the recombination interval was methylated on one homolog and were abolished almost completely when methylated on both homologs. In Arabidopsis, two recent mapping studies analyzed F 2 progeny derived from crosses between Columbia ddm1 and met1 [Col(ddm1),Col(met1)] DNA methylation mutants and wild-type Landsberg [Ler(WT)] accessions and showed that loss of DNA methylation could not alleviate the suppression of COs in pericentromeric regions of chromosomes (9, 10). However, as pointed out by the aut...

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Section: Discussionmentioning

confidence: 88%

Features of the Arabidopsis recombination landscape resulting from the combined loss of sequence variation and DNA methylation

Colomé-Tatché

Cortijo

Wardenaar

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

136

143

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“…Recent data show that these DMRs are even stable for over 16 generations in the epiRIL population (Table 4). The epiRILs also show strong heritable differentiation in phenotype [11][12][13]25 , and it is highly likely that these phenotypic differences are the result of DNA methylation differences. Although DNA sequence differences exist in epiRILs (few leftover SNPs or changes in transposable elements that were inherited from the DDM1 parent or occurred during inbreeding), ongoing whole-genome resequencing indicates that differences in DNA sequence among epiRILs are several orders of magnitude smaller than differences in DNA methylation.…”

Section: Methodsmentioning

confidence: 99%

“…So far, only DNA sequence variation has been considered capable of generating heritable functional differences between individuals, and therefore such effects of intraspecific diversity have been attributed to DNA sequence variation. However, recent evidence suggests that, even in the absence of DNA sequence variation, within-species variation in functional traits can be created by epigenetic variation [10][11][12][13] .…”

mentioning

confidence: 99%

“…Results of these studies indicate that epigenetic variation is ubiquitous within and among natural plant populations [18][19][20][21][22] , and that epigenetic differences can be independent from DNA sequence variation 10,[23][24] (although rigorous demonstrations of true independence are difficult and still scarce). Moreover, there is increasing evidence that epigenetic variation alone can create heritable variation in ecologically important traits such as the growth, phenology and herbivore defence of plants 11,12,25 , as well as in phenotypic plasticity, niche width and habitat differentiation 13,21,[26][27] .…”

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confidence: 99%

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Epigenetic diversity increases the productivity and stability of plant populations

et al. 2013

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Biological diversity within species can be an important driver of population and ecosystem functioning. Until now, such within-species diversity effects have been attributed to underlying variation in DNA sequence. However, within-species differences, and thus potentially functional biodiversity, can also be created by epigenetic variation. Here, we show that epigenetic diversity increases the productivity and stability of plant populations. Epigenetically diverse populations of Arabidopsis thaliana produce up to 40% more biomass than epigenetically uniform populations. The positive epigenetic diversity effects are strongest when populations are grown together with competitors and infected with pathogens, and they seem to be partly driven by complementarity among epigenotypes. Our study has two implications: first, we may need to re-evaluate previous within-species diversity studies where some effects could reflect epigenetic diversity; second, we need to incorporate epigenetics into basic ecological research, by quantifying natural epigenetic diversity and testing for its ecological consequences across many different species.

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“…The ddm1-2-derived epiRIL population has been analyzed for a number of growth-related morphological traits in both neutral and stressful conditions (Johannes et al, 2009;Reinders et al, 2009;Latzel et al, 2012;Zhang et al, 2013). The observed variation among the lines was found to be highly heritable, and recently, specific differentially methylated regions (DMRs) were shown to act as epigenetic quantitative trait loci accounting for most of the heritable variation in flowering time and root length (Cortijo et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Epigenetic Basis of Morphological Variation and Phenotypic Plasticity inArabidopsis thaliana

et al. 2015

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Epigenetics is receiving growing attention in the plant science community. Epigenetic modifications are thought to play a particularly important role in fluctuating environments. It is hypothesized that epigenetics contributes to plant phenotypic plasticity because epigenetic modifications, in contrast to DNA sequence variation, are more likely to be reversible. The population of decrease in DNA methylation 1-2 (ddm1-2)-derived epigenetic recombinant inbred lines (epiRILs) in Arabidopsis thaliana is well suited for studying this hypothesis, as DNA methylation differences are maximized and DNA sequence variation is minimized. Here, we report on the extensive heritable epigenetic variation in plant growth and morphology in neutral and saline conditions detected among the epiRILs. Plant performance, in terms of branching and leaf area, was both reduced and enhanced by different quantitative trait loci (QTLs) in the ddm1-2 inherited epigenotypes. The variation in plasticity associated significantly with certain genomic regions in which the ddm1-2 inherited epigenotypes caused an increased sensitivity to environmental changes, probably due to impaired genetic regulation in the epiRILs. Many of the QTLs for morphology and plasticity overlapped, suggesting major pleiotropic effects. These findings indicate that epigenetics contributes substantially to variation in plant growth, morphology, and plasticity, especially under stress conditions.

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Epigenetic variation in plant responses to defence hormones

Cited by 74 publications

References 47 publications

Features of the Arabidopsis recombination landscape resulting from the combined loss of sequence variation and DNA methylation

Features of the Arabidopsis recombination landscape resulting from the combined loss of sequence variation and DNA methylation

Epigenetic diversity increases the productivity and stability of plant populations

Epigenetic Basis of Morphological Variation and Phenotypic Plasticity inArabidopsis thaliana

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