Quantitative resistance to clubroot infection mediated by transgenerational epigenetic variation in Arabidopsis

Abstract

Summary Quantitative disease resistance, often influenced by environmental factors, is thought to be the result of DNA sequence variants segregating at multiple loci. However, heritable differences in DNA methylation, so‐called transgenerational epigenetic variants, also could contribute to quantitative traits. Here, we tested this possibility using the well‐characterized quantitative resistance of Arabidopsis to clubroot, a Brassica major disease caused by Plasmodiophora brassicae . For that, we used the epigenetic recombinant inbred lines (epi RIL ) derived from the cross ddm1‐2 × Col‐0, which show extensive epigenetic variation but limited DNA sequence variation. Quantitative loci under epigenetic control ( QTL epi ) mapping was carried out on 123 epi RIL infected with P. brassicae and using various disease‐related traits. Epi RIL displayed a wide range of continuous phenotypic responses. Twenty QTL epi were detected across the five chromosomes, with a bona fide epigenetic origin for 16 of them. The effect of five QTL epi was dependent on temperature conditions. Six QTL epi co‐localized with previously identified clubroot resistance genes and QTL in Arabidopsis. Co‐localization of clubroot resistance QTL epi with previously detected DNA ‐based QTL reveals a complex model in which a combination of allelic and epiallelic variations interacts with the environment to lead to variation in clubroot quantitative resistance.

Identification and characterisation of hypomethylated DNA loci controlling quantitative resistance in Arabidopsis

“…Patterns of plant DNA methylation in the plant genome can remain stable over multiple generations and influence heritable phenotypes (Quadrana and Colot, 2016). Recent evidence has suggested that reduced DNA methylation increases the responsiveness of the plant immune system (Espinas et al, 2016) This ‘priming’ of plant defence enables an augmented induction of defence-related genes after pathogen attack, causing increased levels of quantitative resistance (Prime-A-Plant Group et al, 2006; Conrath et al, 2015; Martinez-Medina et al, 2016; Liégard et al, 2018). In some cases, priming of defence-related genes is associated with post-translational histone modifications that mark a more open chromatin structure (Jaskiewicz et al, 2011; Luna et al, 2012).…”

“…Although the epiRILs from the ddm1-2 x Col-0 cross do not carry the ddm1-2 mutation, they contain stably inherited hypomethylated DNA regions from the ddm1-2 parent, which are maintained up to 16 generations of self-pollination (Johannes et al, 2009; Colomé-Tatché et al, 2012; Latzel et al, 2013). A core set of 123 epiRILs from this population at the eight generation of self-pollination in the wild-type (Wt) background has been characterized for differentially methylated region (DMR) markers, enabling linkage mapping of heritable hypomethylated loci controlling root growth, flowering and abiotic stress tolerance (Liégard et al, 2018; Cortijo et al, 2014; Kooke et al, 2015).…”

Epigenetic Mechanisms of Plant Adaptation to Biotic and Abiotic Stresses

“…In a similar experimental setting, 16 epiQTLs were detected that affect resistance of Arabidopsis epiRILs to clubroot–a Brassica disease caused by Plasmodiophora brassicae [ 70 ]. Six epiQTLs were mapped close to the clubroot resistance genes and QTLs.…”

Understanding Host–Pathogen Interactions in Brassica napus in the Omics Era

“…Beyond the gene level, a wider perspective on how epigenetics affects plant responses towards pathogen attack should be considered to enhance our understanding about the resistance mechanisms in Brassica . Examples include how TEs, which are associated with DNA methylation, might contribute towards the resistance and susceptibility of the Brassica crop [ 225 , 226 ] and how epigenetic variability is linked to phenotypic responses towards plant pathogens, as shown in the Arabidopsis – P. brassicae pathosystem, where DNA methylation contributes towards quantitative resistance to Clubroot, based on epigenotyped epigenetic recombinant inbred lines [ 227 ]. In the B. napus – L. maculans pathosystem, promoters of defence genes were differentially methylated during the early stages of infection in the resistant host cultivar compared to the susceptible cultivar [ 228 ].…”