Within-plant variation in seed size and inflorescence fecundity is associated with epigenetic mosaicism in the shrub Lavandula latifolia (Lamiaceae)

Alonso, Conchita; Pérez, Rocío Silva; Bazaga, Pilar; Medrano, Mónica; Herrera, Carlos M.

doi:10.1093/aob/mcx140

Cited by 29 publications

(81 citation statements)

References 81 publications

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“…Thus, intra-individual data pooling can indeed obscure interindividual differences. The same conclusion has been drawn recently in other plants [58,59] and mammals [60,26].…”

Section: Discussionsupporting

confidence: 87%

Cell Type-specific Genome Scans of DNA Methylation Diversity Indicate an Important Role for Transposable Elements

Kartal

Schmid

Grossniklaus

2019

Preprint

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The epigenome modulates the activity of genes and supports the stability of the genome. The epigenome can also contain phenotypically relevant, heritable marks that may vary at the organismic and population level. Such non-genetic standing variation may be relevant to ecological and evolutionary processes. To identify loci susceptible to selection, it is common to profile large populations at the genome scale, yet methods to perform such scans for epigenetic diversity are barely tapped. Here, we develop a scalable, information-theoretic approach to assess epigenome diversity based on Jensen-Shannon divergence (JSD) and demonstrate its practicality by measuring cell type-specific methylation diversity in the model plant Arabidopsis thaliana. DNA methylation diversity tends to be increased in the CG as compared to the non-CG (CHG and CHH) sequence context but the tissue or cell type has an impact on diversity at non-CG sites. Less accessible, more heterochromatic states of chromatin exhibit increased diversity. Genes tend to carry more single-methylation polymorphisms when they harbor gene body-like chromatin signatures and flank transposable elements (TEs). In conclusion, the analysis of DNA methylation with JSD in Arabidopsis demonstrates that the genomic location of a gene dominates its methylation diversity, in particular the proximity to TEs which are increasingly viewed as drivers of evolution. Importantly, the JSD-based approach we implemented here is applicable to any population-level epigenomic data set to analyze variation in epigenetic marks among individuals, tissues, or cells of any organism, including the epigenetic heterogeneity of cells in healthy or diseased organs such as tumors.

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“…Thus, intra-individual data pooling can indeed obscure interindividual differences. The same conclusion has been drawn recently in other plants [58,59] and mammals [60,26].…”

Section: Discussionsupporting

confidence: 87%

Cell Type-specific Genome Scans of DNA Methylation Diversity Indicate an Important Role for Transposable Elements

Kartal

Schmid

Grossniklaus

2019

Preprint

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“…It can be analyzed using a method based on high-performance liquid chromatography (HPLC) that does not require a full genome sequence (Alonso et al, 2016b) and provides cost-effective estimates of the proportion of genomic cytosines that are methylated, analogous to flow cytometry for quickly measuring genome size (Dolezel et al, 2007). Within species, global methylation is variable among populations, individuals within populations and different modules of a single plant, and such variation is related to key functional traits such as seed size and seed production (Alonso et al, 2014(Alonso et al, , 2018Herrera et al, 2019), suggesting that its broad interspecific variance could have some ecological relevance. Although data on global methylation (epiphenotype) will be inherently unable to convey information on specific cytosine methylation patterns (epigenotype), it will still provide complementary, interpretable data bearing on the extent of global cytosine methylation that may be functionally linked to other epigenetic features (Vidalis et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Interspecific variation across angiosperms in globalDNAmethylation: phylogeny, ecology and plant features in tropical and Mediterranean communities

et al. 2019

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Summary The interspecific range of epigenetic variation and the degree to which differences between angiosperm species are related to geography, evolutionary history, ecological settings or species‐specific traits, remain essentially unexplored. Genome‐wide global DNA cytosine methylation is a tractable ‘epiphenotypic’ feature suitable for exploring these relationships. Global cytosine methylation was estimated in 279 species from two distant, ecologically disparate geographical regions: Mediterranean Spain and tropical México. At each region, four distinct plant communities were analyzed. Global methylation spanned a 10‐fold range among species (4.8–42.2%). Interspecific differences were related to evolutionary trajectories, as denoted by a strong phylogenetic signal. Genomes of tropical species were on average less methylated than those of Mediterranean ones. Woody plants have genomes with lower methylation than perennial herbs, and genomes of widespread species were less methylated than those of species with restricted geographical distribution. The eight communities studied exhibited broad and overlapping interspecific variances in global cytosine methylation and only two of them differed in average methylation. Altogether, our broad taxonomic survey supported global methylation as a plant ‘epiphenotypic’ trait largely associated with species evolutionary history, genome size, range size and woodiness. Additional studies are required for better understanding the environmental components underlying local and geographical variation.

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“…Epigenetic mosaicism, in which different parts of the same genetic individual differ in the pattern (distribution across specific sites or regions in the genome) or level (proportion of total cytosines that are methylated) of genomic DNA methylation, has been recently suggested as one possible mechanism contributing to the appearance of within‐plant variation in organ traits (Herrera and Bazaga, ; Herrera, ; Alonso et al., ). This hypothesis was initially motivated by results of a handful of studies showing that the genomes of homologous, yet phenotypically distinct organs in the same genetic individual may differ in pattern or level of DNA cytosine methylation (Bitonti et al., , ; Gao et al., ; Bian et al., ; Herrera and Bazaga, ).…”

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confidence: 99%

“…For example, prickly and nonprickly leaves borne by the same individual of the heterophyllous tree Ilex aquifolium differed in DNA methylation, the genomes of nonprickly leaves being significantly more methylated than those of prickly ones (Herrera and Bazaga, ). In the shrub Lavandula latifolia , leaves from different branchlets in the same individual differed significantly in global DNA cytosine methylation, and such epigenetic mosaicism was correlated with within‐plant variation in seed number and size (Alonso et al., ). Cytosine methylation is a major epigenetic mechanism in plants with significant roles in gene expression, transposon activity, and plant growth and development (Finnegan et al., ; Cokus et al., ; Lister et al., ), and DNA methylation variants independent of DNA sequences are causally related to individual differences in continuous traits (Zhang et al., ; Cortijo et al., ; Hu et al., ; Kooke et al., ).…”

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confidence: 99%

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Within‐plant heterogeneity in fecundity and herbivory induced by localizedDNAhypomethylation in the perennial herbHelleborus foetidus

Herrera

Medrano

Pérez

et al. 2019

American J of Botany

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Premise Phenotypic heterogeneity of reiterated, homologous structures produced by individual plants has ecological consequences for plants and their animal consumers. This paper examines experimentally the epigenetic mosaicism hypothesis, which postulates that within‐plant variation in traits of reiterated structures may partly arise from different parts of the same genetic individual differing in patterns or extent of genomic DNA methylation. Methods Leaves of paired ramets borne by field‐growing Helleborus foetidus plants were infiltrated periodically over the entire flowering period with either a water solution of the demethylating agent zebularine or just water as the control. The effects of the zebularine treatment were assessed by quantifying genome‐wide DNA cytosine methylation in leaves and monitoring inflorescence growth and flower production, number of ovules per flower, pollination success, fruit set, seed set, seed size, and distribution of sap‐feeding insects. Results Genomic DNA from leaves in zebularine‐treated ramets was significantly less methylated than DNA from leaves in control ones. Inflorescences in treated ramets grew smaller and produced fewer flowers, with fewer ovules and lower follicle and seed set, but did not differ from inflorescences in untreated ramets in pollination success or seed size. The zebularine treatment influenced the within‐plant distribution of sap‐feeding insects. Conclusions Experimental manipulation of genomic DNA methylation level in leaves of wild‐growing H. foetidus plants induced considerable within‐plant heterogeneity in phenotypic (inflorescences, flowers, fecundity) and ecologically relevant traits (herbivore distribution), which supports the hypothesis that epigenetic mosaicism may partly account for within‐plant variation.

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Within-plant variation in seed size and inflorescence fecundity is associated with epigenetic mosaicism in the shrub Lavandula latifolia (Lamiaceae)

Cited by 29 publications

References 81 publications

Cell Type-specific Genome Scans of DNA Methylation Diversity Indicate an Important Role for Transposable Elements

Cell Type-specific Genome Scans of DNA Methylation Diversity Indicate an Important Role for Transposable Elements

Interspecific variation across angiosperms in globalDNAmethylation: phylogeny, ecology and plant features in tropical and Mediterranean communities

Within‐plant heterogeneity in fecundity and herbivory induced by localizedDNAhypomethylation in the perennial herbHelleborus foetidus

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