High-resolution methylome analysis uncovers stress-responsive genomic hotspots and drought-sensitive transposable element superfamilies in the clonal Lombardy poplar

Cristian Peña-Ponton* (Corresponding author), Barbara Diez-Rodriguez, Paloma Perez-Bello, Claude Becker, Lauren M. McIntyre, Wim H. van der Putten, Emanuele De Paoli, Katrin Heer, Lars Opgenoorth, Koen J.F. Verhoeven* (Corresponding author)

*Corresponding author for this work

Research output: Contribution to journal/periodicalArticleScientificpeer-review

Abstract

DNA methylation is environment-sensitive and can mediate stress responses. In trees, changes in the environment might cumulatively shape the methylome landscape over time. However, because high-resolution methylome studies usually focus on single environmental cues, the stress-specificity and long-term stability of methylation responses remain unclear. Here, we studied the methylome plasticity of a Populus nigra cv. ‘Italica’ clone widely distributed across Europe. Adult trees from different geographic locations were clonally propagated in a common garden experiment and exposed to cold, heat, drought, herbivory, rust infection, and salicylic acid treatments. Whole-genome bisulfite sequencing revealed stress-induced and naturally occurring DNA methylation variants. In CG/CHG contexts, the same genomic regions were often affected by multiple stresses, suggesting a generic methylome response. Moreover, these variants showed striking overlap with naturally occurring methylation variants between trees from different locations. Drought treatment triggered CHH hypermethylation of transposable elements, affecting entire superfamilies near drought-responsive genes. Thus, we revealed genomic hotspots of methylation change that are not stress-specific and that contribute to natural DNA methylation variation, and identified stress-specific hypermethylation of entire transposon superfamilies with possible functional consequences. Our results underscore the importance of studying multiple stressors in a single experiment for recognizing general versus stress-specific methylome responses.

Original languageEnglish
Pages (from-to)5839-5856
Number of pages18
JournalJournal of Experimental Botany
Volume75
Issue number18
DOIs
Publication statusPublished - 27 Sept 2024

Keywords

  • Abiotic stress
  • biotic stress
  • differentially methylated region
  • drought
  • Lombardy poplar
  • Melampsora larici-populina
  • Populus nigra
  • short interspersed nuclear element (SINE)
  • whole genome bisulfite sequencing (WGBS)

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