Crosstalk of DNA Methylation Triggered by Pathogen in Poplars With Different Resistances

Abstract

DNA methylation plays crucial roles in responses to environmental stimuli. Modification of DNA methylation during development and abiotic stress responses has been confirmed in increasing numbers of plants, mainly annual plants. However, the epigenetic regulation mechanism underlying the immune response to pathogens remains largely unknown in plants, especially trees. To investigate whether DNA methylation is involved in the response to infection process or is related to the resistance differences among poplars, we performed comprehensive whole-genome bisulfite sequencing of the infected stem of the susceptible type Populus × euramerican ‘74/76’ and resistant type Populus tomentosa ‘henan’ upon Lonsdalea populi infection. The results revealed that DNA methylation changed dynamically in poplars during the infection process with a remarkable decrease seen in the DNA methylation ratio. Intriguingly, the resistant P. tomentosa ‘henan’ had a much lower basal DNA methylation ratio than the susceptible P. × euramerican ‘74/76’. Compared to mock-inoculation, both poplar types underwent post-inoculation CHH hypomethylation; however, significant decreases in mC and mCHH proportions were found in resistant poplar. In addition, most differentially CHH-hypomethylated regions were distributed in repeat and promoter regions. Based on comparison of DNA methylation modification with the expression profiles of genes, DNA methylation occurred in resistance genes, pathogenesis-related genes, and phytohormone genes in poplars during pathogen infection. Additionally, transcript levels of genes encoding methylation-related enzymes changed during pathogen infection. Interestingly, small-regulator miRNAs were subject to DNA methylation in poplars experiencing pathogen infection. This investigation highlights the critical role of DNA methylation in the poplar immune response to pathogen infection and provides new insights into epigenetic regulation in perennial plants in response to biotic stress.

Transcriptomic and methylation analysis of susceptible and tolerant grapevine genotypes following Plasmopara viticola infection

“…In accordance with that, global methylation presented a lower increase in the tolerant genotype. Analysis of global DNA methylation pattern modification on several species after infection with different pathogens has been reported on tomato roots, Poplar bark and Arabidopsis leaves (Leonetti & Molinari, 2020 ; Xiao et al, 2021 ). Often, resistant species showed DNA hypomethylation patterns while susceptible ones presented hypermethylated DNA after pathogens attack (Leonetti & Molinari, 2020 ; Xiao et al, 2021 ).…”

“…Analysis of global DNA methylation pattern modification on several species after infection with different pathogens has been reported on tomato roots, Poplar bark and Arabidopsis leaves (Leonetti & Molinari, 2020;Xiao et al, 2021). Often, resistant species showed DNA hypomethylation patterns while susceptible ones presented hypermethylated DNA after pathogens attack (Leonetti & Molinari, 2020;Xiao et al, 2021). Also, studies have observed that altering DNA methylation levels (hypo-or hypermethylation) on genomic regions could influence gene and phenotypic responses to plant diseases (Geng et al, 2019;Leonetti & Molinari, 2020) Wang, 2015;Espinas et al, 2016;Ramirez-Prado, Piquerez, et al, 2018;Song et al, 2021;Wang et al, 2020;Zhi & Chang, 2021).…”

Multi-Omics Techniques for Forest Plant Breeding

“…The dynamics of DNA methylation play important roles in the epigenetic regulation of plant growth, development, and response to environmental stresses [116]. For instance, several studies have revealed the potential role of DNA methylation in flower development [117], drought tolerance [118], wood formation [119], and immune response to pathogen infection [120] in Populus species. Since DNA methylation alters gene expression, transcriptome analysis is usually combined with methylation analysis to investigate the functional relationship between the epigenome and transcriptome [114].…”

The Ups and Downs of Plant NLR Expression During Pathogen Infection

“…Demethylation of promoters leads to cis elements being more accessible to TFs, ultimately leading to increased NLR gene expression and disease resistance. In poplar trees infected with Lonsdalea populi , hypomethylation occurred at CH sites within promoter regions of defense-related genes ( Xiao et al, 2021 ). Higher levels of hypomethylation were particularly noted in poplar trees with increased resistance toward L. populi when compared to susceptible trees.…”