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Global DNA cytosine methylation as an evolving trait: phylogenetic signal and correlated evolution with genome size in angiosperms.

ABSTRACT: DNA cytosine methylation is a widespread epigenetic mechanism in eukaryotes, and plant genomes commonly are densely methylated. Genomic methylation can be associated with functional consequences such as mutational events, genomic instability or altered gene expression, but little is known on interspecific variation in global cytosine methylation in plants. In this paper, we compare global cytosine methylation estimates obtained by HPLC and use a phylogenetically-informed analytical approach to test for significance of evolutionary signatures of this trait across 54 angiosperm species in 25 families. We evaluate whether interspecific variation in global cytosine methylation is statistically related to phylogenetic distance and also whether it is evolutionarily correlated with genome size (C-value). Global cytosine methylation varied widely between species, ranging between 5.3% (Arabidopsis) and 39.2% (Narcissus). Differences between species were related to their evolutionary trajectories, as denoted by the strong phylogenetic signal underlying interspecific variation. Global cytosine methylation and genome size were evolutionarily correlated, as revealed by the significant relationship between the corresponding phylogenetically independent contrasts. On average, a ten-fold increase in genome size entailed an increase of about 10% in global cytosine methylation. Results show that global cytosine methylation is an evolving trait in angiosperms whose evolutionary trajectory is significantly linked to changes in genome size, and suggest that the evolutionary implications of epigenetic mechanisms are likely to vary between plant lineages.

SUBMITTER: Alonso C

PROVIDER: S-EPMC4310347 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Global DNA cytosine methylation as an evolving trait: phylogenetic signal and correlated evolution with genome size in angiosperms.

Alonso Conchita C Pérez Ricardo R Bazaga Pilar P Herrera Carlos M CM

Frontiers in genetics 20150129

DNA cytosine methylation is a widespread epigenetic mechanism in eukaryotes, and plant genomes commonly are densely methylated. Genomic methylation can be associated with functional consequences such as mutational events, genomic instability or altered gene expression, but little is known on interspecific variation in global cytosine methylation in plants. In this paper, we compare global cytosine methylation estimates obtained by HPLC and use a phylogenetically-informed analytical approach to t ...[more]

PMID: 25688257

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Project description:Spartina alterniflora, marsh grass, is a vegetative apomicticly-reproducing halophyte native to marshes along the east coast of the United States and invasive across the world. S. alterniflora provides many ecosystem services including, but not limited to, water filtration, habitats for invertebrates, and sediment retention. Widespread diebacks of longstanding marsh grass colonies launched extensive investigations into probable mechanisms leading to patchy diebacks. There is still current debate as to the causes of a marsh dieback but environmental stress is acknowledged as a constant. Spatial epigenetic variation could contribute to variation of stress susceptibility, but the scale and structure of epigenetic variation is unknown. The current study investigates patterns of epigenetic variation in a natural population of S. alterniflora. This study examines variation of global DNA methylation within and among clones of the marsh grass Spartina alterniflora using an ELISA-like microplate reaction and observed significant heterogeneity of global DNA methylation within and among clones of S. alterniflora across the North Inlet basin, as well as significant differences of global methylation between adults and sexually produced seedlings. The present study also characterized differences for plants in a section of the population that experienced an acute marsh dieback in the year 2001 and have subsequently recolonized, finding a significant positive correlation between cytosine methylation and time period of colonization. The significant heterogeneity of global DNA methylation both within and among clones observed within this natural population of S. alterniflora and potential impacts from hypersaline environments at North Inlet suggests the need for more in-depth epigenetic studies to fully understand DNA methylation within an ecological context. Future studies should consider the effects of varying saline conditions on both global DNA and gene specific methylation.

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Project description:Cytosine DNA methylation (CDM) is a stable epigenetic modification to the genome and a widespread regulatory process in living organisms that involves multicomponent molecular machines. Genome-wide cytosine methylation patterning participates in the epigenetic reprogramming of a cell, suggesting that the biological information contained within methylation positions may be amenable to decoding. Adaptation to a new cellular or organismal environment also implies the potential for genome-wide redistribution of CDM changes that will ensure the stability of DNA molecules. This raises the question of whether or not we would be able to sort out the regulatory methylation signals from the CDM background ("noise") induced by thermal fluctuations. Here, we propose a novel statistical and information thermodynamic description of the CDM changes to address the last question. The physical basis of our statistical mechanical model was evaluated in two respects: 1) the adherence to Landauer's principle, according to which molecular machines must dissipate a minimum energy ? = kBT ln2 at each logic operation, where kB is the Boltzmann constant, and T is the absolute temperature and 2) whether or not the binary stretch of methylation marks on the DNA molecule comprise a language of sorts, properly constrained by thermodynamic principles. The study was performed for genome-wide methylation data from 152 ecotypes and 40 trans-generational variations of Arabidopsis thaliana and 93 human tissues. The DNA persistence length, a basic mechanical property altered by CDM, was estimated with values from 39 to 66.9 nm. Classical methylome analysis can be retrieved by applying information thermodynamic modelling, which is able to discriminate signal from noise. Our finding suggests that the CDM signal comprises a language scheme properly constrained by molecular thermodynamic principles, which is part of an epigenomic communication system that obeys the same thermodynamic rules as do current human communication systems.

Dataset Information

Global DNA cytosine methylation as an evolving trait: phylogenetic signal and correlated evolution with genome size in angiosperms.

Publications

Global DNA cytosine methylation as an evolving trait: phylogenetic signal and correlated evolution with genome size in angiosperms.

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