Parental pericentromeric methylation status drives methylome remodelling and heterosis in epigenetic hybrids

Kakoulidou, Ioanna; Piecyk, Robert S.; Meyer, Rhonda C.; Kuhlmann, Markus; Altmann, Thomas; Gutjahr, Caroline; Johannes, Frank

doi:10.1101/2022.09.29.510107

Cited by 3 publications

(25 citation statements)

References 61 publications

(94 reference statements)

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“…That this spreading is monoallelic could not be directly verified in the isogenic hybrid system used by the authors. However, in many cases, SMR gain events flanking TCM loci display clear intermediate methylation levels (Kakoulidou et al, 2022), which is at least consistent with this idea. Further support for this comes from the fact that many SMR gain events show a correlative gain in sRNA abundance in the flanking regions relative to the parents.…”

Section: A Trans-chromosomal Demethylation Model For Dmr Loss Eventssupporting

confidence: 74%

“…The remodeling of DNA methylation patterns co-occurs with other chromatin modifications, which together reshape the regulatory landscape of hybrid genomes and could thus provide a molecular basis for heterosis. The fact that similar epigenetic changes have been observed in F1 offspring from isogenic parents that had been engineered to differ in their DNA methylation profiles (Dapp et al, 2015;Kakoulidou et al, 2022;Lauss et al, 2018) underlines that these events are not just consequences of genetic variation, and thus call for independent mechanistic explanations.…”

Section: Introductionmentioning

confidence: 86%

“…This has led to the hypothesis that mostly epigenetic, rather than genetic, differences between the parents trigger these heterotic phenotypes. More concerted attempts to delineate the role of parental epigenetic differences in facilitating DNA methylation remodeling and heterosis in F1 hybrids have been made by Dapp et al (2015), Rigal et al (2016), Lauss et al (2018), andKakoulidou et al (2022). These latter studies examined F1 hybrids from crosses between isogenic parents that had been engineered to differ only in their epigenetic profiles.…”

Section: Overview Of F1 Experimental Systemsmentioning

confidence: 99%

“…The trigger to initiate remodeling events in SMRs must therefore come from 'distal' regions outside of homologous alleles. Kakoulidou et al (2022) recently provided evidence that many SMR gain events could possibly be fitted into what may be called a 'TCM proximity model' (Figure 3). They found that many such events occur nearby TCM sites (about 350 bp), suggesting that they are simply a byproduct of a TCM process in the genomic 'neighborhood'.…”

Section: A Trans-chromosomal Demethylation Model For Dmr Loss Eventsmentioning

confidence: 99%

“…One intriguing model proposes that epigenetic, rather than genetic, differences serve as a trigger for heterosis (Groszmann et al, 2013;Lauss et al, 2018). This model is backed by observations that F1 hybrids undergo substantial DNA methylation remodeling relative to their parents (Greaves et al, 2012;Kakoulidou et al, 2022;Shen et al, 2012;Zhang et al, 2016) and that experimental perturbations of DNA methylation pathways alter the heterotic potential of hybrids (Kakoulidou et al, 2022;Kawanabe et al, 2016;Lauss et al, 2018;Rigal et al, 2016;Shen et al, 2012). The remodeling of DNA methylation patterns co-occurs with other chromatin modifications, which together reshape the regulatory landscape of hybrid genomes and could thus provide a molecular basis for heterosis.…”

Section: Introductionmentioning

confidence: 99%

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DNA methylation remodeling in F1 hybrids

Kakoulidou

Johannes

2023

The Plant Journal

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SUMMARYF1 hybrids derived from a cross between two inbred parental lines often display widespread changes in DNA methylation patterns relative to their parents. To which extent these changes drive non‐additive gene expression levels and phenotypic heterosis in F1 individuals is not fully resolved. Current mechanistic models propose that DNA methylation remodeling in hybrids is the result of epigenetic interactions between parental alleles via small interfering RNA (sRNA). These models have strong empirical support but are limited to genomic regions where the two parental lines differ in DNA methylation status. However, most remodeling events occur in parental regions with similar methylation patterns, and seem to be strongly conditioned by distally acting factors, even in isogenic hybrid systems. The molecular basis of these distal interactions is currently unknown, and will likely emerge as an active area of research in the future. Despite these gaps in our molecular understanding, parental DNA methylation states are statistically associated with heterosis, independent of genetic information, and may serve as biomarkers in crop breeding.

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Section: A Trans-chromosomal Demethylation Model For Dmr Loss Eventssupporting

confidence: 74%

Section: Introductionmentioning

confidence: 86%

Section: Overview Of F1 Experimental Systemsmentioning

confidence: 99%

Section: A Trans-chromosomal Demethylation Model For Dmr Loss Eventsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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DNA methylation remodeling in F1 hybrids

Kakoulidou

Johannes

2023

The Plant Journal

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On the Causes of Gene-Body Methylation Variation inArabidopsis thaliana

Nizhynska

Morales

Nordborg

2022

Preprint

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Gene-body methylation (gbM) refers to sparse CG methylation of coding regions, in particular of evolutionarily conserved house-keeping genes. It is found in both plants and animals, but is directly and stably (epigenetically) inherited over multiple generations in the former. Studies inArabidopsis thalianahave demonstrated that plants originating from different parts of the world exhibit large differences in gbM, which presumably reflects an epigenetic memory of ancestral genetic and/or environmental factors. Here we look for evidence of such factors in F2 plants resulting from a cross between a southern Swedish line with low gbM and a northern Swedish line with high gbM, grown at two different temperatures. Using bisulfite-sequencing data with nucleotide-level resolution on hundreds of individuals, we confirm that CG sites are either methylated (nearly 100% methylation across sampled cells) or unmethylated (approximately 0% methylation across sampled cells), and show that the higher level of gbM in the northern line is due to more sites being methylated. Furthermore, methylation variants almost always show Mendelian segregation, consistent with their being directly and stably inherited through meiosis. To explore how the differences between the parental lines could have arisen, we focused on somatic deviations from the inherited state, distinguishing between gains (relative to the inherited 0% methylation) and losses (relative to the inherited 100% methylation) at each site in the F2 generation. We demonstrate that deviations predominantly affect sites that differ between the parental lines, consistent with these sites being more mutable. Gains and losses behave very differently in terms of the genomic distribution, and are influenced by the local chromatin state. We find clear evidence for different trans-acting genetic polymorphism affecting both gains and losses, with those affecting gains showing strong environmental interactions (G x E). Direct effects of the environment were minimal. In conclusion, we show that genetic and environmental factors can change gbM at a cellular level, and hypothesize that these factors can also lead to trans-generational differences between individuals via the inclusion of such changes in the zygote.

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On the causes of gene-body methylation variation in Arabidopsis thaliana

2023

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Gene-body methylation (gbM) refers to sparse CG methylation of coding regions, which is especially prominent in evolutionarily conserved house-keeping genes. It is found in both plants and animals, but is directly and stably (epigenetically) inherited over multiple generations in the former. Studies in Arabidopsis thaliana have demonstrated that plants originating from different parts of the world exhibit genome-wide differences in gbM, which could reflect direct selection on gbM, but which could also reflect an epigenetic memory of ancestral genetic and/or environmental factors. Here we look for evidence of such factors in F2 plants resulting from a cross between a southern Swedish line with low gbM and a northern Swedish line with high gbM, grown at two different temperatures. Using bisulfite-sequencing data with nucleotide-level resolution on hundreds of individuals, we confirm that CG sites are either methylated (nearly 100% methylation across sampled cells) or unmethylated (approximately 0% methylation across sampled cells), and show that the higher level of gbM in the northern line is due to more sites being methylated. Furthermore, methylation variants almost always show Mendelian segregation, consistent with their being directly and stably inherited through meiosis. To explore how the differences between the parental lines could have arisen, we focused on somatic deviations from the inherited state, distinguishing between gains (relative to the inherited 0% methylation) and losses (relative to the inherited 100% methylation) at each site in the F2 generation. We demonstrate that deviations predominantly affect sites that differ between the parental lines, consistent with these sites being more mutable. Gains and losses behave very differently in terms of the genomic distribution, and are influenced by the local chromatin state. We find clear evidence for different trans-acting genetic polymorphism affecting gains and losses, with those affecting gains showing strong environmental interactions (G×E). Direct effects of the environment were minimal. In conclusion, we show that genetic and environmental factors can change gbM at a cellular level, and hypothesize that these factors can also lead to transgenerational differences between individuals via the inclusion of such changes in the zygote. If true, this could explain genographic pattern of gbM with selection, and would cast doubt on estimates of epimutation rates from inbred lines in constant environments.

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Parental pericentromeric methylation status drives methylome remodelling and heterosis in epigenetic hybrids

Cited by 3 publications

References 61 publications

DNA methylation remodeling in F1 hybrids

DNA methylation remodeling in F1 hybrids

On the Causes of Gene-Body Methylation Variation inArabidopsis thaliana

On the causes of gene-body methylation variation in Arabidopsis thaliana

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