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

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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.

The study was performed within the ‘Characterization of the pinewood nematode/Pinus system: a phytochemical and histopathological approach’ project (PTDC/AGRCFL/120184/2010), funded by Fundação para a Ciência e a Tecnologia (FCT). Additional financial support to AS, LS and RZ came from the Spanish National Research Agency MCIU/AEI/FEDER RESILPINE(RTI2018-094691-B-C33) and PLASTICPINE(PID2022-140521OB-C31) grants; OTR07700, IN607A2021/03, 2022.01903 from Intramural CSIC ref-201640I030 and Xunta de Galicia-GAIN IN607/2023 grant. Also supported by the FCT’s bilateral action Spain-Portugal PRIAIBPT-2011-1152 (NEMARES) and UIDB/50016/2020 R&D Unit.

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