Millennia-long epigenetic fluctuations generate intragenic DNA methylation variance in Arabidopsis populations

Cell Systems, Journal Year: 2023, Volume and Issue: 14(11), P. 953 - 967.e17

Published: Nov. 1, 2023

Methylation of CG dinucleotides (mCGs), which regulates eukaryotic genome functions, is epigenetically propagated by Dnmt1/MET1 methyltransferases. How mCG established and transmitted across generations despite imperfect enzyme fidelity unclear. Whether variation in natural populations governed genetic or epigenetic inheritance also remains mysterious. Here, we show that MET1 de novo activity, enhanced existing proximate methylation, seeds stabilizes Arabidopsis thaliana genes. activity restricted active demethylation suppressed histone variant H2A.Z, producing localized patterns. Based on these observations, develop a stochastic mathematical model precisely recapitulates dynamics predicts intragenic patterns their population-scale given only site spacing. Our results demonstrate establishment, inheritance, variance constitute unified process, revealing undergoes large, millennia-long fluctuations can therefore mediate evolution this timescale.

Language: Английский

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

PLoS Genetics, Journal Year: 2023, Volume and Issue: 19(5), P. e1010728 - e1010728

Published: May 4, 2023

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

Language: Английский

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DNA methylation regulates biosynthesis of tanshinones and phenolic acids during growth of Salvia miltiorrhiza

PLANT PHYSIOLOGY, Journal Year: 2023, Volume and Issue: 194(4), P. 2086 - 2100

Published: Oct. 25, 2023

Abstract DNA methylation plays a crucial role in the regulation of plant growth and biosynthesis secondary metabolites. Danshen (Salvia miltiorrhiza) is valuable Chinese herbal medicine commonly used to treat cardiovascular diseases; its active ingredients are tanshinones phenolic acids, which primarily accumulate roots. Here, we conducted targeted metabolic analysis S. miltiorrhiza roots at 3 distinct stages: 40 d old (r40), 60 (r60), 90 (r90). The contents (cryptotanshinone, tanshinone I, IIA, rosmariquinone) acids (rosmarinic acid salvianolic B) gradually increased during development. Whole-genome bisulfite sequencing transcriptome stages revealed an level CHH context (H represents A, T, or C) r90 compared with r40 r60. Increased levels were associated elevated expression various genes linked epigenetic regulations, including CHROMOMETHYLASE2 (SmCMT2), Decrease Methylation 1 (SmDDM1), Argonaute 4 (SmAGO4), DOMAINS REARRANGED METHYLTRANSFERASE (SmDRM1). Moreover, many involved biosynthesis, such as copalyldiphosphate synthase 5 (SmCPS5), cytochrome P450-related enzyme (SmCYP71D464), geranylgeranyl diphosphate (SmGGPPS1), geranyl (SmGPPS), hydroxyphenylpyruvate reductase (SmHPPR), dioxygenase (SmHPPD), altered owing hyper-methylation, indicating that important regulating accumulation. Our data shed light on root miltiorrhiza, providing clues for further improvement compound production via molecular breeding miltiorrhiza.

Language: Английский

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DNA methylation in clonal duckweed (Lemna minor L.) lineages reflects current and historical environmental exposures

Molecular Ecology, Journal Year: 2022, Volume and Issue: 32(2), P. 428 - 443

Published: Nov. 3, 2022

Environmentally induced DNA methylation variants may mediate gene expression responses to environmental changes. If such are transgenerationally stable, there is potential for persist over multiple generations. Our current knowledge in plants, however, almost exclusively based on studies conducted sexually reproducing species where the majority of changes subject resetting germlines, limiting transgenerational epigenetics stress memory. Asexual reproduction circumvents and therefore be more conducive long-term inheritance epigenetic marks. Taking advantage rapid clonal common duckweed Lemna minor, we hypothesize that long-term, memory from exposure high temperature can detected profiles. Using a reduced representation bisulphite sequencing approach (epiGBS), show induces hypermethylation at many CG CHG cytosine contexts but not CHH. Additionally, differential context was observed still subset cytosines, even after 3-12 generations culturing environment. This demonstrates effect reflected methylome persists Structural annotation revealed this enriched transposable elements. The probably caused by stable persistence temperature-induced across To extent has functional consequences phenotypes, result suggests modulation asexual plants.

Language: Английский

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Hybridization and gene expression: Beyond differentially expressed genes

Molecular Ecology, Journal Year: 2024, Volume and Issue: unknown

Published: Feb. 27, 2024

Gene expression has a key role in reproductive isolation, and studies of hybrid gene have identified mechanisms causing sterility. Here, we review the evidence for altered following hybridization outline shown to contribute hybrids. Transgressive expression, transcending that both parental species, is pervasive early generation sterile hybrids, but also frequently observed viable, fertile We highlight showing can result transgressive established lineages or species. Such extreme patterns stabilized taxa suggest may hybridization-derived evolutionary novelty. conclude while misexpression hybrids are well documented, understanding lagging. argue jointly assessing differences cell composition cell-specific changes addition chromatin methylation, will significantly advance our basis expression. Moreover, uncovering what extent evolution results individual genes, entire networks how selection moulds Finally, studying dual roles serving as mechanism isolation substrate ecological adaptation, lead significant advances

Language: Английский

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The regulatory potential of transposable elements in maize

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: July 14, 2024

The genomes of flowering plants consist largely transposable elements (TEs), some which modulate gene regulation and function. However, the repetitive nature TEs difficulty mapping individual by short-read-sequencing have hindered our understanding their regulatory potential. We demonstrate that long-read chromatin fiber sequencing (Fiber-seq) comprehensively identifies accessible regions (ACRs) CpG methylation across maize genome. uncover stereotypical ACR patterns at young degenerate with evolutionary age, resulting in TE-enhancers preferentially marked a novel plant-specific epigenetic feature: simultaneous hyper-CpG accessibility. show TE ACRs are co-opted as promoters ACR-containing can facilitate amplification. Lastly, we pervasive signature - hypo-5mCpG diffuse accessibility directing to specific loci, including loci sparked McClintock's discovery TEs.

Language: Английский

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Climate change and epigenetics: Unraveling the role of methylation in response to thermal instability in the Antarctic plant Colobanthus quitensis

Physiologia Plantarum, Journal Year: 2025, Volume and Issue: 177(1)

Published: Jan. 1, 2025

Abstract Low temperatures are one of the critical conditions affecting performance and distribution plants. Exposure to cooling results in reprogramming gene expression, which turn would be mediated by epigenetic regulation. Antarctica is known as most severe ecosystems, but several climate models predict an increase average temperature, may positively impact development Antarctic plants; however, under warmer temperatures, plants' vulnerability damages from low‐temperature events increases. Here, we evaluated these on acclimation process, with a focus how methylation influences induction cold response genes. According results, number methylations promoter regions associated lower expression Similarly, populations where this relationship observed, individuals acclimated projected change condition more vulnerable, their temperature face event compared current antarctic condition. This research first report highlighting role its influence transcriptional responses plant Colobanthus quitensis facing projections.

Language: Английский

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Climatic and stress memory in trees - and how to study it

Elsevier eBooks, Journal Year: 2025, Volume and Issue: unknown, P. 399 - 418

Published: Jan. 1, 2025

Language: Английский

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The genomic and epigenomic landscapes of hemizygous genes across crops with contrasting reproductive systems

Proceedings of the National Academy of Sciences, Journal Year: 2025, Volume and Issue: 122(6)

Published: Feb. 7, 2025

Hemizygous genes, which are present on only one of the two homologous chromosomes diploid organisms, have been mainly studied in context sex and sex-linked genes. However, these genes can also occur autosomes plants due to structural variants (SVs), such as a deletion/insertion allele, this phenomenon largely unexplored plants. Here, we investigated genomic epigenomic landscapes hemizygous across 22 genomes with varying propagation histories: eleven clonal lineages, seven outcrossed samples, four inbred putatively homozygous genomes. We identified SVs leading genic hemizygosity. As expected, very few (0.01 1.2%) were genomes, representing negative controls. Hemizygosity was appreciable among averaging 8.7% but consistently elevated for samples at 13.8% likely reflecting heterozygous SV accumulation during propagation. Compared more often situated centromeric than telomeric regions experienced weaker purifying selection. They had reduced levels expression, ~20% expression violating evolutionary model dosage compensation. detected higher DNA methylation transposable elements, may contribute their expression. Finally, profiles showed that specifically expressed contexts related fruit development, organ differentiation, stress responses. Overall, accumulate clonally propagated lineages display distinct genetic epigenetic features compared shedding unique insights into studies breeding programs crops.

Language: Английский

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Independent mechanisms of benzimidazole resistance across Caenorhabditis nematodes

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2025, Volume and Issue: unknown

Published: March 15, 2025

Benzimidazoles (BZs), a widely used class of anthelmintic drugs, target beta-tubulin proteins, disrupt microtubule formation, and cause nematode death. In parasitic species, mutations in genes ( e.g. , isotype-1 beta-tubulin) are predicted to inhibit BZ binding associated with resistance. Similarly, the free-living Caenorhabditis elegans an ortholog, ben-1 primary drivers The recurrent association resistance beta-tubulins suggests that is repeatedly caused by genes, example repeated evolution drug across species. To evaluate hypothesis mediated beta-tubulin, we identified alleles wild strains from three species: C. briggsae tropicalis . We hypothesized that, if these species experienced similar selective pressures, they would evolve BZs any tbb-1 tbb-2 ). Using high-throughput development assays, tested found heterogeneous set variants were only two encode premature stop codon (W21stop) missense substitution (Q134H), but neither was might have evolved other or not Our findings reveal lack highlight importance defining mechanisms outside beta-tubulins.

Language: Английский

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