Parental experience modifies the Mimulus methylome

Abstract

BackgroundTransgenerational plasticity occurs when the environmental experience of an organism modifies the growth and development of its progeny. Leaf damage in Mimulus guttatus exhibits transgenerational plasticity mediated through differential expression of hundreds of genes. The epigenetic mechanisms that facilitate this response have yet to be described.ResultsWe performed whole genome bisulfite sequencing in the progeny of genetically identical damaged and control plants and developed a pipeline to compare differences in the mean and variance of methylation between treatment groups. We find that parental damage increases the variability of CG and CHG methylation among progeny, but does not alter the overall mean methylation. Instead it has positive effects in some regions and negative in others. We find 3,396 CHH, 203 CG, and 54 CHG Differentially Methylated Regions (DMRs) ranging from tens to thousands of base pairs scattered across the genome. CHG and CHH DMRs tended to overlap with transposable elements. CG DMRs tended to overlap with gene coding regions, many of which were previously found to be differentially expressed.ConclusionsGenome-wide increases in methylome variation suggest that parental conditions can increase epigenetic diversity in response to stress. Additionally, the potential association between CG DMRs and differentially expressed genes supports the hypothesis that differential methylation is a mechanistic component of transgenerational plasticity in M. guttatus.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-5087-x) contains supplementary material, which is available to authorized users.

Genotypic variation in the persistence of transgenerational responses to seasonal cues*

“…Genomic analysis may provide clarity as to whether these traits, and the genes responsible for them, are under selection in nature, or are evolving by drift. Likely candidates include genes regulating DNA methylation (e.g., Colicchio et al 2018;Rendina González et al 2018;Van Dooren et al 2020), or small RNAs (Zhong et al 2013), both of which have been implicated in the regulation of transgenerational plasticity.…”

Mimulus sRNAs Are Wound Responsive and Associated with Transgenerationally Plastic Genes but Rarely Both

“…Previous experimental work in this same M. guttatus RIL94 genotype identified 3731 differentially methylated genomic regions (DMRs) [ 13 ] and 919 differentially expressed genes (DEGs) [ 14 ] in the progeny of leaf wounded plants. To test component (2) of our working model, whether proximity of sRNA loci increases the probability that protein coding regions will be differentially methylated or differentially expressed in progeny of leaf wounded plants, we tested whether genomic regions that overlapped with sRNA loci were more likely to have previously been identified as transgenerationally labile.…”

“…In M. guttatus , altered trichome production in the progeny of wounded plants [ 54 ] has inspired a number of follow-up experiments designed to elucidate the underlying molecular mechanisms for the transmission of non-genetic information between generations. Past work has demonstrated the genotype specificity of this response [ 54 , 55 ], pointed at substantial differential gene expression associated with parental wounding [ 14 , 56 ] and suggested that the majority of differential methylation associated with parental wounding is associated with transposon CHH methylation but that genic CG methylation is also impacted [ 13 ]. Additionally, recent work has demonstrated transgenerational trichome plasticity transmitted through both the maternal and paternal germline, with maternal but not paternal transmission likely involving DNA methylation [ 9 ].…”

“…Meiotic transmission of epigenetic markings resulting from environmental cues provides a mechanism through which plastic responses to the environment can be transmitted from one generation to the next (transgenerational plasticity [ 6 ]). While plant germline cells do undergo a number of rounds of epigenetic reprogramming prior to the formation of a new seed [ 7 ], it is clear that environmental conditions experienced by parents can alter phenotypes [ 8 , 9 , 10 , 11 ], epigenetic profiles [ 4 , 10 , 12 , 13 ] and gene expression [ 14 , 15 , 16 ] in the next generation. Importantly, autocorrelation between offspring and parent environment can favor mechanisms that establish such patterns of transgenerational plasticity [ 17 , 18 ], perhaps leading to natural selection that either favors or disfavors this transmission depending on local environmental patterns [ 11 ].…”

“…Mimulus guttatus is a well-known system for studies in ecological and evolutionary genetics and in recent years has also become a plant model for transgenerational plasticity in response to wounding. Offspring of leaf-wounded parents exhibit phenotypic [ 9 , 54 , 55 ], gene expression [ 14 , 56 ] and DNA methylation [ 13 ] differences compared to control plants. There is substantial genetic variation within M. guttatus for the transgenerational induction of trichomes [ 54 , 55 ] but the mechanisms that mediate this response remain unclear.…”