The White Mountains in Eastern California are home to some of the oldest living trees in the world. According to tree-ring data, a Great Basin bristlecone pine known as Methuselah dates back almost 5,000 years, and when this little pine seedling emerged from the soil, mammoths were still wandering the Earth, the historic landmark Stonehenge was under heavy construction, and writing paper had just been invented in Ancient Egypt. Methuselah has weathered storms, endured temperature fluctuations and survived drought periods during its long lifetime, and as the saying goes, with age comes wisdom. This accumulated “wisdom” is stored on a cellular level in the form of epigenetic modifications induced by exposure to environmental stress. As sessile, long-lived organisms, trees have evolved sophisticated adaptation mechanisms to constantly changing environmental conditions, and epigenetic memory may enable them to respond to recurring stress events more quickly. Since some epigenetic variations are heritable, they can even pass this “knowledge” on to following generations which raises hope that epigenetic mechanisms may help trees to adapt to climate change more efficiently than genetic adaptation would allow. Correlative studies indicate a role of epigenetics in phenotypic plasticity but evidence that unequivocally links the distribution of epigenetic marks to gene expression and phenotypes is rare.
A common epigenetic modification is DNA methylation of cytosine residues which can occur in different contexts: CG, CHG, and CHH, where H is A, T, or C. The non-CG DNA methylation contexts are typical for plants but very rare in other organisms. DNA methylation analysis has mainly been conducted in the model species Arabidopsis and only few studies have addressed this process in long-lived tree species. The team lead by Peña-Ponton have now provided unprecedented insight into DNA methylation variations in trees in response to environmental stressors. The authors analysed clonally propagated Lombardy poplar from several European countries exposed to different abiotic and biotic stress conditions for 20 days under experimental conditions and then analysed their DNA methylation profiles. Lombardy poplars are derived from a single clonal lineage that likely originated in the 17th century in Italy and is now grown worldwide. As it is a clonally propagated plant, the authors were able to minimising the effect of genetic variation and maximising the effect of epigenetic differences to phenotypic plasticity.
The authors showed that genome-wide methylation changes, especially in the CG and CHG contexts, could be explained by the trees’ origin rather than the experimentally induced short-term stress, and these changes thus reflect how the trees’ growth history has shaped their DNA methylation landscape. These differentially methylated regions were also shown to be stress-agnostic for the most part and responding to multiple stressors, which ties in with the fact that different stresses share general response components on a physiological level. However, the DNA methylation response also showed certain specificity, with drought treatment having the strongest stress-specific epigenetic effect and inducing hypermethylation in the CHH context, mostly in gene-flanking regions, particularly on so-called transposable elements or transposons. Transposons are genetic elements that can create copies of themselves and move between genomic regions, which gave them the nickname “jumping genes”. Environmental stress can activate transposon activity, and certain transposon families preferentially insert near stress-responsive genes. DNA methylation within these regions can silence their mobilisation and keep their disruptive effects on the genome at bay. The results by Peña-Ponton and colleagues reveal hypermethylation of entire transposon superfamilies in response to stress, especially drought, and based on gene ontology enrichment data the authors speculate that this methylation-mediated transposon silencing may have regulatory effects on nearby drought-responsive genes.
We are only at the beginning of understanding the functional consequences of DNA methylation in response to environmental change, yet more profound insight is urgently needed if the epigenetic “wisdom” held by trees such as Methuselah may indeed be useful for adaptation to climate change. Large-scale studies like the one presented by Peña-Ponton et al., however, are unfortunately rare. The authors used whole-genome bisulfite sequencing, which is considered the gold standard for methylome profiling since it provides high-resolution data, but it also comes with certain drawbacks, such as high sequencing costs and output of large amounts of data that require major computing and storage capacities. In another JXB study, Isabelle Lesur and colleagues offer an alternative approach to address these shortcomings. The authors have developed and validated a technique that identifies and focuses on regions of highly variable DNA methylation, which may be more suitable for population-scale epigenetic studies both in plants and animals. Interested readers can find the detailed workflow and the corresponding data in their recent Technical Innovation paper in the Journal of Experimental Botany.
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Peña-Ponton, C., Diez-Rodriguez, B., Perez-Bello, P., Becker, C., McIntyre, L.M., van der Putten, W.H., De Paoli, E., Heer, K., Opgenoorth, L. and Verhoeven, K.J., 2024. High-resolution methylome analysis uncovers stress-responsive genomic hotspots and drought-sensitive TE superfamilies in the clonal Lombardy poplar. Journal of Experimental Botany, https://doi.org/10.1093/jxb/erae262.
Mareike Jezek
Dr. Jezek is an Assistant Editor at the Journal of Experimental Botany, one of the official journals of the Society for Experimental Biology.
Featured Image by Alun Salt
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