Phytophthora alni Infection Reinforces the Defense Reactions in Alnus glutinosa-Frankia Roots to the Detriment of Nodules

Alnus glutinosa, able to establish symbiosis with mutualistic bacteria of the genus Frankia, is one of the main species in European riparian environments, where it performs numerous biological and socioeconomic functions. However, riparian ecosystems face a growing threat from Phytophthora alni, a highly aggressive waterborne pathogen causing severe dieback in A. glutinosa. To date, the tripartite interaction between the host plant, the symbiont Frankia, and the pathogen remains unexplored but is critical for understanding how pathogen-induced stress influences the nodule molecular machinery and thus the host-symbiont metabolism. In the present study, we aimed to explore for the first time how P. alni affects the overall molecular processes of Alnus glutinosa-Frankia nodules, with a special focus on unraveling the spatial expression of defense mechanisms within these tissues. We conducted a laboratory experiment based on P. alni infection of young A. glutinosa seedlings nodulated with Frankia alni ACN14a, noninfected or infected with the pathogen P. alni. Multi-omics analyses (i.e., transcriptomics, proteomics, and metabolomics) were carried out on nodules (N) and associated roots (AR) of the same plant to underline the impact on the nodule molecular processes (i.e., N/AR markers) when the host plant is infected compared with noninfected plants. Our results revealed that P. alni infection modified the molecular nodule processes and induced reprograming of defense-related markers by a shift in associated roots to the detriment of nodules. These findings suggest that A. glutinosa reinforces locally its immune responses in roots but moderates this activation in nodules to preserve its Frankia symbiont. [Figure: see text] Copyright © 2025 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.