Resistance of Pinus pinea to Bursaphelenchus xylophilus explained by the dynamic response of phytohormones, antioxidant activity, and stress-related gene expression

Key message

The effects of MJ on pine trees are species-specific and trigger a resistant phenotype to the PWN. A more dynamic response of hormones and gene expression in Pinus pinea explains the high resistance to Bursaphelenchus xylophilus of this species.

Abstract

Knowledge on hormonal and genetic mechanisms of pine trees in response to the pinewood nematode (PWN; Bursaphelenchus xylophilus) is limited. To describe tree defence strategies against B. xylophilus, this study used the plant stress hormone methyl jasmonate (MJ) on four pine species with different susceptibility (Pinus pinaster < P. radiata ≈ P. sylvestris < P. pinea). Three-year-old trees were sprayed with MJ at 0, 25, and 50 mM, and 2 months later challenged with the PWN. Multiple samples were taken to assess nematode content, oxidative stress, secondary metabolites, phytohormone levels, and stress-related gene expression. Nematode infestation in trees correlated negatively with the water content of needles and phenolics of stems, and positively with the concentration of indole-3-carboxylic acid in stems. MJ spray reduced in a dose-dependent manner the nematode content in P. pinaster and P. sylvestris. The effects of MJ were species-specific, although a more pronounced impact was observed in the susceptible P. pinaster species, leading to a decrease of chlorophyll and water loss and to the upregulation of the gene involved in the biosynthesis of terpenoids (AFS). After MJ spray, increased levels of JA-Ile were observed in P. pinea only. Hormone profiling, predisposition to activate antioxidant response, and gene expression in P. pinea trees provide evidence of why this species is highly resistant to B. xylophilus. On the contrary, the lack of effective hormonal changes in P. pinaster explained the lack of defence responses to B. xylophilus of this susceptible species. This study is a first approach to explore biochemical, molecular, and hormonal interactions between Pinus species and the PWN, and presents unprecedented insights into alterations induced by exogenous MJ in regulating defence mechanisms in pine trees.