Choosing the right signaling pathway: hormone responses to Phytophthora cinnamomi during compatible and incompatible interactions with chestnut (Castanea spp.).

Ink disease caused by the hemibiotrophic root pathogen Phytophthora cinnamomi (Pc) is devastating for the European chestnut (Castanea sativa), unlike Asian chestnuts and interspecific hybrids, which are resistant to Pc. The role that hormone responses play for Pc resistance remains little understood, especially regarding the temporal regulation of hormone responses. We explored the relationship between changes in tree health and physiology and alterations in leaf and root phytohormones and primary and secondary metabolites during compatible and incompatible Castanea spp.-Pc interactions. Susceptible (S) C. sativa and resistant (R) C. sativa × C. crenata ramets were inoculated with Pc in roots and assessed for disease progression, leaf physiology and biochemistry at 1, 3, 5 and 8 days after inoculation (d.a.i.). In S chestnuts, Pc increasingly deteriorated the leaf physiological functioning by decreasing leaf CO2 assimilation, stomatal conductance, transpiration rate, chlorophylls content and the maximum quantum yield of the photosystem II over time, triggering aerial symptoms (leaf wilting and chlorosis) 8 d.a.i. Pc had little impact on the leaf physiological functioning of R chestnuts, which remained asymptomatic. In roots of S chestnuts, Pc transiently induced jasmonates signaling (5 d.a.i.) while impairing root carbohydrates metabolism over time. In leaves, a transient antioxidant burst (5 d.a.i.) followed by abscisic acid (ABA) accumulation (8 d.a.i.) was observed. R chestnuts responded to Pc by up-regulating root salicylic acid (SA) at early (1 d.a.i.) and late (8 d.a.i.) infection stages, in an antagonistic crosstalk with root ABA. Overall, the results pinpoint an important role of SA in mediating the resistant response of chestnuts to Pc, but also show that the specific hormone pathways induced by Pc are genotype dependent. The study also highlights that the dynamic nature of hormone responses over time must be considered when elucidating hormone-regulated responses to Pc.