“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

Facilitating plant defense through priming holds significant promise for advancing sustainable crop health practices. The primed state of plants is correlated with a more rapid and efficient response, achievable by subjecting plants to recurrent stressors. Consequently, priming constitutes a dynamic transitional process between two distinct biological states, necessitating the establishment and maintenance of transcriptional memory mechanisms. Research on transcriptional memory has revealed molecular mechanisms including protein and transcription factor accumulation, as well as epigenetic modulations. Nonetheless, there remains a dearth of understanding regarding the interplay among the dynamics of transcriptional stress memory, its preservation, and the resultant emergent properties conferred upon the organism once primed. Here, we found that the robustness of transcriptional memory associated with repeated mechanical stimuli played an antagonistic role in the priming of plant defense. Incorporating experiments and computational modeling, we have analyzed the transcriptional stress memory of Arabidopsis thaliana subjected to daily acoustic stimulations. The observed enhanced resistance to the pathogen Sclerotinia sclerotiorum following three rounds of repeated acoustic stimulations is attributed to three primary mechanisms: the activation of a first line of defense in non-inoculated plants, an increase defense-associated gene diversification, and gene priming. These mechanisms are sustained by a transcriptional stress memory involving thousands of genes, likely regulated mostly by transcription factor cascades. Upon comparing the predictions of the transcriptional stress memory model with experimental outcomes, we propose that priming does not arise from the sequential activation of different pathways but rather from the simultaneous modulation of a broad spectrum of pathways. Pathway redundancy in the transcriptional memory topology imparts robustness to plant defense priming. Consequently, primed plants exhibit independence from limited genetic variations, preventing critical loss of resistance observed in naive plants. Pathway redundancies also imply strong limitations in increasing plant defense. Thus, plants remain unaffected by an increase in the daily rate of RAS and exhibited a stress memorization time limited to 1.5 days.