Network-level dynamics underlie stress memory and shape the intrinsic limits of mechanically induced defense priming.
Khaoula Hadj Amor, Ophélie LégeriD, Sylvain RaffaeleiD, Magdalena Kovacic, Aroune DuclosiD, Pedro Carvalho‐Silva, Frédérick GarçiaiD, Adelin BarbacciiD
Abstract
Repeated environmental stimuli can induce transient immune priming in plants, but how such responses accumulate, persist, and decay remains poorly understood. Here, we used acoustic waves to deliver a controlled oscillatory mechanical stimulus and investigated its effects on quantitative disease resistance in Arabidopsis thaliana. Repeated stimulations progressively increased resistance to Sclerotinia sclerotiorum before reaching a plateau after three stimulations. Transcriptomic analyses showed that priming was not only associated with sustained activation of a restricted set of defense genes, but with progressive reconfiguration of a broad transcriptional response and increased responsiveness to infection. We developed a dynamic network model integrating transcriptional trajectories across repeated stimulations. Modal analysis revealed a distributed dynamical memory composed of rapidly dissipating and slowly relaxing components, providing a basis for the accumulation and transient persistence of priming. The model predicted resistance saturation and rapid relaxation after stimulation ceased, which we experimentally validated. These results support a model in which stress memory is an emergent, multiscale property of transcriptional network dynamics, arising not only from persistent molecular states encoded by a restricted set of genes, but also from their collective dynamics.
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