Root gene regulatory network analysis reveals roles for defense hormones and secondary metabolites in establishment of disease-suppressive soil

Abstract

Plants recruit beneficial microbiota in their rhizosphere to alleviate stresses. In Arabidopsis thaliana, foliar infection by Hyaloperonospora arabidopsidis (Hpa) has been shown to establish a disease-suppressive microbiome that promotes protection against Hpa infection of the subsequent plant generation grown in this conditioned soil - a phenomenon known as soil-borne legacy (SBL). The root responses involved in SBL establishment have remained largely unclear. In this study, time-series RNA-seq of roots from Hpa-infected plants grown in natural soil was conducted over seven days post-inoculation. A gene regulatory network of the responding roots was constructed. The role of predicted key components was verified in follow-up assays. Root transcriptional reprogramming started within one day after foliar infection. Genes associated with salicylic acid (SA)-mediated defense were upregulated, while those linked to secondary metabolism and jasmonic acid (JA) responsiveness were downregulated. SA accumulation increased at 1 dpi, and JA decreased by 3 dpi. Transcriptional regulation occurred primarily in the tips of the roots. Mutant analyses confirmed that SA, JA, indole glucosinolates, camalexin, and flavonoids contribute to SBL establishment. Our findings reveal rapid systemic transcriptional reprogramming in roots upon foliar pathogen attack, uncovering novel roles of hormone signaling and secondary metabolism in shaping a disease-suppressive soil beyond their known defense functions.