Developmentally regulated generation of a systemic signal for long‐lasting defence priming in tomato

Summary: Tomato is a major global crop. However, its production is limited by Botrytis cinerea. Due to the toxicity of postharvest pesticide application, alternative control methods such as priming are being investigated. Plants were treated with β‐aminobutyric acid (BABA) at two developmental stages and resistance against B. cinerea was tested in fruit tissue and in progenies. DNA methylation and RNA sequencing were conducted to characterise the (epi)genetic changes associated with long‐lasting resistance. Grafting experiments were done to assess the systemic nature of this signal, which was further characterised by small RNA (sRNA) sequencing of scions. Only BABA‐treated seedlings displayed induced resistance (IR). DNA methylation analysis revealed seedling‐specific changes, which occurred in the context of lower basal methylation. BABA‐IR was found to be transmissible from primed rootstock to grafted unprimed scions. In these scions, we identified a subset of mobile 24 nt sRNAs associated with genes showing primed expression during infection in fruit. Our results demonstrate the functional association of a systemic signal with long‐lasting IR and priming. Through integrated omics approaches, we have identified markers of long‐lasting priming in tomato fruit which could also serve as targets for durable resistance in other crops.