Herbivore-Induced DNA Demethylation Changes Floral Signalling and Attractiveness to Pollinators in Brassica rapa

Abstract

Plants have to fine-tune their signals to optimise the trade-off between herbivore deterrence and pollinator attraction. An important mechanism in mediating plant-insect interactions is the regulation of gene expression via DNA methylation. However, the effect of herbivore-induced DNA methylation changes on pollinator-relevant plant signalling has not been systematically investigated. Here, we assessed the impact of foliar herbivory on DNA methylation and floral traits in the model crop plant Brassica rapa. Methylation-sensitive amplified fragment length polymorphism (MSAP) analysis showed that leaf damage by the caterpillar Pieris brassicae was associated with genome-wide methylation changes in both leaves and flowers of B. rapa as well as a downturn in flower number, morphology and scent. A comparison to plants with jasmonic acid-induced defence showed similar demethylation patterns in leaves, but both the floral methylome and phenotype differed significantly from P. brassicae infested plants. Standardised genome-wide demethylation with 5-azacytidine in five different B. rapa full-sib groups further resulted in a genotype-specific downturn of floral morphology and scent, which significantly reduced the attractiveness of the plants to the pollinator bee Bombus terrestris. These results suggest that DNA methylation plays an important role in adjusting plant signalling in response to changing insect communities.

Within‐plant heterogeneity in fecundity and herbivory induced by localized DNA hypomethylation in the perennial herb Helleborus foetidus

“…This result contrasts with those obtained by Kellenberger et al. () for Brassica plants treated with 5‐azacytidine, in which the demethylation treatment reduced the attractiveness of plants to pollinators. Experimental insect exclusion and hand‐pollination, combined with experimental localized demethylation, would be valuable to elucidate the possible relationships between biotic interactions and the plant epigenome which may affect plant fitness (Alonso et al., )…”

“…Experiments designed to reveal possible epigenetic effects on ecologically relevant plant traits have often relied on interfering with developmental processes by using some DNA demethylating agent (Fieldes et al., ; Kondo et al., ; Bossdorf et al., ; Verhoeven and Van Gurp, ; Kellenberger et al., ; Alonso et al., ). The demethylating agent chosen in most of these earlier investigations was the cytidine analogue 5‐azacytidine, applied to germinating seeds or young seedlings using immersion or, less often, spraying procedures (Puy et al., ).…”

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

“…This observation is in agreement with previous results obtained by Kellenberger et al . () and Sharma et al . () in the Brassica genus, which linked plant responses to biotic and abiotic stress to epigenetic regulations.…”

Do native and invasive herbivores have an effect on Brassica rapa pollination?

“…; Kellenberger et al . ). However, these studies were conducted in an experimental setup including only one pollinator type ( i.e .…”