Sirex noctilio infestation led to inevitable pine death despite activating pathways involved in tolerance

Defense-related metabolome traits in pine species after infestation by Sirex noctilio are largely unknown, despite, in most cases, trees being overwhelmed. Using LC-MS-based untargeted metabolomics, we revealed the systemic metabolic changes induced by this insect in 14-year-old Pinus radiata trees, the most affected species worldwide. An immediate metabolome alteration was expressed in needles after infestation, including the up-regulation of flavonols, flavan-3-ols, oxyneolignans, auxins, proline, and tryptophan, among others. The flavan-3-ols (catechin and procyanidin B1) suggested a rapidly induced photoprotection mechanism aided by diverting proline as an alternative substrate for respiration to compensate for the progressive chlorosis that degrades photosystems. Meanwhile, glutathione, glutamate, and ascorbate levels significantly dropped in needles, which may indicate the critical oxidative stress that trees had to face since the onset of the infestation. They were not fully replenished after long-term infestation, and redox homeostasis was probably not achieved, compromising tree survival. Nevertheless, a huge auxins overexpression detected in needles throughout the infestation may reflect tolerance against the premature senescence caused by the woodwasp venom. In contrast, the metabolome of wood tissues remained initially unchanged, although it seems to collapse after three months. Overall, the metabolomics strategy adopted in this work evidenced its usefulness in uncovering the fundamental roles of plants’ chemical defense that govern interactions with specific stressors. Metabolomics uncovered the P. radiata response to S. noctilio infestation, highlighting photoprotection and auxin expression as tolerance traits and the oxidative stress causing death. [Display omitted] •Metabolomics revealed the whole picture of P. radiata chemical response to woodwasp.•Photoprotection was immediately induced in needles by up-regulating catechins.•Proline biosynthesis initially increased to be then catabolized to fuel respiration.•Persistent ascorbate deficit suggested severe oxidative stress as a cause of death.•Auxins overexpression throughout the infestation evidenced an attempt of tolerance.