Aphid feeding induces the relaxation of epigenetic control and the associated regulation of the defense response in Arabidopsis

Abstract

Environmentally induced changes in the epigenome help individuals to quickly adapt to fluctuations in the conditions of their habitats. We explored those changes in Arabidopsis thaliana plants subjected to multiple biotic and abiotic stresses, and identified transposable element (TE) activation in plants infested with the green peach aphid, Myzus persicae. We performed a genome-wide analysis mRNA expression, small RNA accumulation and DNA methylation Our results demonstrate that aphid feeding induces loss of methylation of hundreds of loci, mainly TEs. This loss of methylation has the potential to regulate gene expression and we found evidence that it is involved in the control of plant immunity genes. Accordingly, mutant plants deficient in DNA and H3K9 methylation (kyp) showed increased resistance to M. persicae infestation. Collectively, our results show that changes in DNA methylation play a significant role in the regulation of the plant transcriptional response and induction of defense response against aphid feeding.

Exploiting Epigenetic Variations for Crop Disease Resistance Improvement

“…A similar DNA hypomethylation is observed upon application of bacterial PAMP flg22, nematode PAMP "NemaWater, " and plant defense hormone salicylic acid (SA) in model and crop plants (Ngom et al, 2017;Atighi et al, 2020). High-resolution DNA methylation profiling revealed that this pathogen-induced DNA hypomethylation occurs in many chromatin regions proximal to defense-related genes, including promoters, gene bodies, and nearby transposable elements (TEs) (Dowen et al, 2012;Yu et al, 2013;Rambani et al, 2015;Kellenberger et al, 2016;López Sánchez et al, 2016;Ngom et al, 2017;Wang C. et al, 2018;Geng et al, 2019;Sun et al, 2019;Atighi et al, 2020;Annacondia et al, 2021). Although combined analysis of DNA methylation and gene expression revealed that this pathogen-induced DNA hypomethylation is generally correlated with transcriptional activation of proximal defense-related genes, specific regulation of defense-related gene transcription by nearby DNA hypomethylation varies among plant species and genes (Yu et al, 2013;López Sánchez et al, 2016;Geng et al, 2019;Atighi et al, 2020).…”

“…With the contribution of DNA (de)methylation mutants and advanced DNA methylation profiling techniques such as methylation-sensitive amplified fragment length polymorphism (MSAP) analysis, whole-genome bisulfite sequencing (WGBS), methylated DNA immunoprecipitation sequencing (MeDIPseq), and methyl-CpG binding domain protein capture sequencing (MBDCap-seq), dynamics and biological functions of DNA (de)methylation in plant-pathogen interactions have been extensively studied in model and crop plants (Clark et al, 1994;Guevara et al, 2017;Li et al, 2018;Feng and Lou, 2019;Tirnaz and Jacqueline, 2019;Hsu et al, 2020). As a part of plant defense response, DNA hypomethylation is induced by pathogen infections in many plant species such as Arabidopsis thaliana, Oryza sativa, Nicotiana tabacum, Glycine max, Brassica rapa, Citrullus lanatus, and Aegilops tauschii (Dowen et al, 2012;Yu et al, 2013;Rambani et al, 2015;Kellenberger et al, 2016;López Sánchez et al, 2016;Wang C. et al, 2018;Geng et al, 2019;Sun et al, 2019;Atighi et al, 2020;Annacondia et al, 2021). A similar DNA hypomethylation is observed upon application of bacterial PAMP flg22, nematode PAMP "NemaWater, " and plant defense hormone salicylic acid (SA) in model and crop plants (Ngom et al, 2017;Atighi et al, 2020).…”

“…Increasing evidence revealed that DNA (de)methylation also gets involved in the regulation of plant defense response to pests and nematodes (Leonetti and Molinari, 2020). For instance, Arabidopsis mutant plants deficient in methylation of DNA and H3K9 (kyp) showed increased resistance to the infestation of green peach aphid Myzus persicae (Annacondia et al, 2021). Similarily, rice RdDM and DDM1 mutants dcl3, ago4, drm2, and ddm1 exhibited attenuated susceptibility to the infection of nematode Meloidogyne graminicola, confirming a central role of DNA (de)methylation in the regulation of plant defense against pathogenic microbes, pests, and nematodes (Table 1, Atighi et al, 2020).…”

Epigenome and Epitranscriptome: Potential Resources for Crop Improvement

“…Epigenetic variations in response to biotic stress have also been reported. DNA methylation and histone modification dynamics have been monitored upon plant exposure to pathogens and changes in plant–pathogen interactions of some DNA methylation and histone modification factor mutants [ 86 , 87 , 88 ]. Pathogen-induced DNA demethylation occurs in promoters, gene bodies, and nearby TEs of defense-related genes, and the DNA demethylation is generally correlated with transcriptional activation of these genes [ 88 ].…”

“…DNA methylation and histone modification dynamics have been monitored upon plant exposure to pathogens and changes in plant–pathogen interactions of some DNA methylation and histone modification factor mutants [ 86 , 87 , 88 ]. Pathogen-induced DNA demethylation occurs in promoters, gene bodies, and nearby TEs of defense-related genes, and the DNA demethylation is generally correlated with transcriptional activation of these genes [ 88 ]. For instance, Arabidopsis mutants ( met1 and ddc ), which cause global cytosine methylation depletion, are more resistant to the bacterial pathogen Pseudomonas syringae pv.…”