"Out of sight, out of mind". The antagonistic role of the transcriptional memory associated with repeated acoustic stimuli on the priming of plant defense.

Abstract

BackgroundPriming plant immunity offers a powerful and sustainable strategy for crop protection, enabling plants to respond faster and more efficiently to threats. This increased readiness is driven by transcriptional memory--molecular mechanisms that store and recall stress responses, including protein accumulation, transcription factor activity, and epigenetic modifications. However, the interplay among transcriptional stress memory, its stability, and its broader impact on plant resistance remain poorly understood. ResultsHere, we reveal a tight link between transcriptional memory and defense priming in Arabidopsis thaliana exposed to repeated acoustic stimulations. Using a combination of experiments and computational modeling, we show that enhanced resistance to Sclerotinia sclerotiorum after three stimulations arises from three key mechanisms: (1) preemptive activation of defense pathways in noninoculated plants, (2) increased diversification of defense-related genes, and (3) gene priming. This heightened defense state is sustained by transcriptional stress memory across thousands of genes, which is likely orchestrated by transcription factor cascades. Challenging the conventional view that priming involves stepwise activation of distinct pathways, our findings suggest that priming instead results from the simultaneous modulation of a broad spectrum of defense pathways. This built-in redundancy enhances resilience, shielding primed plants from the genetic variability-driven resistance loss observed in naive plants. However, this same redundancy imposes strict limits on further enhancing the resistance. More frequent acoustic stimulations did not amplify the protective effect, and transcriptional memory faded within 1.5 days after stimulation ceased. ConclusionsBy integrating experimental and computational approaches, we present a genome-scale quantitative model of stress-induced gene regulation. Our results highlight the trade-offs inherent in transcriptional memory-driven priming, revealing both its potential and its limitations in optimizing plant immunity.