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

Abstract

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.

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

“…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 ., ) 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 ., ). 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 ., , ; Herrera et al ., ), 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 ., ).…”

Lifetime genealogical divergence within plants leads to epigenetic mosaicism in the long-lived shrubLavandula latifolia(Lamiaceae)

“…Cytosine methylation is a major epigenetic mechanism in plants with roles in gene expression, transposon activity, and plant growth and development (Finnegan et al, 2000;Cokus et al, 2008;Lister et al, 2008), hence subindividual heterogeneity in pattern and level of DNA methylation could also partly account for within-plant variation in organ traits Alonso et al, 2018;Herrera et al, 2019).…”

“…Epigenetic mosaics in which homologous organs in different parts of the same genetic individual differ in extent and/or patterns of DNA methylation have been documented for clonal and non-clonal plants (Bitonti et al, 1996;Gao et al, 2010;Bian et al, 2013;Spens . CC-BY-NC-ND 4.0 International license perpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for this this version posted December 11, 2020. ; https://doi.org/10.1101/2020.12.11.421594 doi: bioRxiv preprint Herrera et al -4 & Douhovnikoff, 2016), and associations between phenotypic heterogeneity and subindividual epigenetic variation, either natural or experimentally induced, have been also found Alonso et al, 2018;Herrera et al, 2019). In adult Lavandula latifolia (Lamiaceae) plants there is substantial subindividual heterogeneity in global DNA cytosine methylation.…”

“…Somatic mutations altering nuclear or plastid DNA sequences are not, however, the only molecular mechanism with a capacity to produce genomic heterogeneity and induce phenotypic variation within individual plants. Cytosine methylation is a major epigenetic mechanism in plants with roles in gene expression, transposon activity, and plant growth and development (Finnegan et al ., 2000; Cokus et al ., 2008; Lister et al ., 2008), hence subindividual heterogeneity in pattern and level of DNA methylation could also partly account for within-plant variation in organ traits (Herrera & Bazaga, 2013; Alonso et al ., 2018; Herrera et al ., 2019).…”

“…Epigenetic mosaics in which homologous organs in different parts of the same genetic individual differ in extent and/or patterns of DNA methylation have been documented for clonal and non-clonal plants (Bitonti et al ., 1996; Gao et al ., 2010; Bian et al ., 2013; Spens & Douhovnikoff, 2016), and associations between phenotypic heterogeneity and subindividual epigenetic variation, either natural or experimentally induced, have been also found (Herrera & Bazaga, 2013; Alonso et al ., 2018; Herrera et al ., 2019). In adult Lavandula latifolia (Lamiaceae) plants there is substantial subindividual heterogeneity in global DNA cytosine methylation.…”