Lifetime genealogical divergence within plants leads to epigenetic mosaicism in the shrub Lavandula latifolia (Lamiaceae)

Abstract

 Epigenetic mosaicism is a possible source of within-plant phenotypic heterogeneity, yet its frequency and developmental origin remain unexplored. This study examines whether the extant epigenetic heterogeneity within long-lived Lavandula latifolia (Lamiaceae) shrubs reflects recent epigenetic modifications experienced independently by different plant parts or, alternatively, it is the cumulative outcome of a steady lifetime process. Leaf samples from different architectural modules were collected from three L. latifolia plants and characterized epigenetically by global DNA cytosine methylation and methylation state of methylation-sensitive amplified fragment length polymorphism markers (MS-AFLP). Epigenetic characteristics of modules were then assembled with information on the branching history of plants. Methods borrowed from phylogenetic research were used to assess genealogical signal of extant epigenetic variation and reconstruct within-plant genealogical trajectory of epigenetic traits. Plants were epigenetically heterogeneous, as shown by differences among modules in global DNA methylation and variation in the methylation states of 6-8% of MS-AFLP markers. All epigenetic features exhibited significant genealogical signal within plants.Events of epigenetic divergence occurred throughout the lifespan of individuals and were subsequently propagated by branch divisions. Internal epigenetic diversification of L. latifolia individuals took place steadily during their development, a process which eventually led to persistent epigenetic mosaicism.

DNA Methylation Can Mediate Local Adaptation and Response to Climate Change in the Clonal Plant Fragaria vesca: Evidence From a European-Scale Reciprocal Transplant Experiment

“…Finally, it is also likely that the role of epigenetic variation plays different roles at the level of individual ramet and whole clone. It is known that epigenetic variation can be greatly variable even within individual non-clonal plants (e.g., Herrera and Bazaga, 2013 ; Herrera et al, 2021 ). Considering clonal plants, it was proposed that differences in DNA methylation among communicating ramets could enhance whole genet functioning ( Latzel et al, 2016 ), suggesting that the observed responses of single ramets may not be scalable to whole plant generalizations.…”

Ecological significance of intraplant variation: Epigenetic mosaicism in Lavandula latifolia plants predicts extant and transgenerational variability of fecundity‐related traits

“…Individual plants' ontogenies add a temporal dimension to the preceding ecological and evolutionary effects. Extant epigenetic mosaics exhibited by adult plants at a given point in their lifetimes, such as those studied here, are the instantaneous manifestation of a dynamic lifelong process of internal epigenetic diversification which takes place steadily, apparently at a constant epimutation rate (Herrera et al, 2021;Yao et al, 2021).…”

“…Simplifying from Gill et al (1995), the GMH rests on the simultaneous fulfilment of four central premises: (a) spontaneous mutations occur among the proliferating meristems; (b) the meristematic and modular basis of plant development assures that many of these mutations are preserved and expanded hierarchically among modules as the plant grows; (c) the differential growth and survival of ramets, branches and shoots should alter the genotypic configuration of the plant as it grows; and (d) intraplant trait heterogeneity arising from genotypic heterogeneity will affect individual fitness through effects on progeny traits, plant responses to the environment and/or responses of animal consumers (Herrera et al, 2021).…”

Plants as epigenetic mosaics: harnessing variability to thrive in a variable world

“…Our understanding of how plants cope with external variability by developing trait variability within themselves – known as subindividual variability – has advanced dramatically over the last decade, thanks in large part to work by Carlos Herrera and colleagues, including the recent article published in this issue of New Phytologist , Herrera et al . (2021; pp. 2065–2076).

‘A key lesson from this research is that plants are more than the sum – or mean – of their parts.

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“…Most plasticity research has examined how plants optimize their whole or average phenotypes, but environmental factors also vary significantly within plantslight and herbivore attack, for example, often vary among leaves within plants. Our understanding of how plants cope with external variability by developing trait variability within themselvesknown as subindividual variabilityhas advanced dramatically over the last decade, thanks in large part to work by Carlos Herrera and colleagues, including the recent article published in New Phytologist, Herrera et al (2021;doi: 10.1111/ nph.17257).…”