Norway spruce (Picea abies) is an economically and ecologically important tree species that grows across northern and central Europe. Treating Norway spruce with jasmonate has long-lasting beneficial effects on tree resistance to damaging pests, such as the European spruce bark beetle Ips typographus and its fungal associates. The potential involvement of (epi)genetic mechanisms in this long-lasting jasmonate-induced resistance (IR) has gained much recent interest, but remains largely unknown. In this study, we treated 2-year-old spruce seedlings with methyl jasmonate (MeJA) and challenged them with the I. typographus vectored necrotrophic fungus Grosmannia penicillata. MeJA treatment reduced the extent of necrotic lesions in the bark and thus elicited IR to the fungus. The transcriptional response of spruce bark to MeJA treatment was analyzed over a 4-week time course using mRNA-seq. This analysis provided evidence that MeJA treatment induced a transient upregulation of jasmonic acid, salicylic acid and ethylene biosynthesis and downstream signaling genes. Additionally, genes encoding components of the RNA-directed DNA methylation pathway showed long-term repression, suggesting a possible role of DNA demethylation in the maintenance of MeJA-IR. These results provide new clues about the potential mechanisms underpinning long-term MeJA-IR in Norway spruce.

Abstract Recent evidence suggests that stressed plants employ epigenetic mechanisms to transmit acquired resistance to their progeny. However, little is known about the evolutionary and ecological significance of this transgenerational acquired resistance (TAR). In this study, we have used a full factorial design to study the specificity, costs and stability of TAR following exposure of Arabidopsis thaliana to increasing stress intensities by a biotrophic pathogen, a necrotrophic pathogen, and soil salinity. All stresses incrementally reduced parental growth, while salt stress additionally impacted reproductive success. Biotrophic and necrotrophic pathogens, but not salt, increased resistance of progeny against the stress experienced by their parents (i.e., in matched environments). In mis-matched environments, however, pathogen-elicited TAR was associated with costs from increased susceptibility to other stresses. Furthermore, the stability of pathogen-elicited TAR over one stress-free generation and its associated costs were proportional to parental disease severity, suggesting that plants use stress intensity as an environmental proxy to adjust TAR investment. We conclude that pathogen-elicited TAR is an adaptive and deterministic parental effect that is associated with ecological costs. Accordingly, our study provides evolutionary and ecological context to the epigenetic TAR response. Key words: Adaptive parental effects; Arabidopsis; Phenotypic plasticity; Plant stress; Transgenerational acquired resistance.