Under the cover of darkness: a transcriptomic exploration of clubroot during the night.

Abstract

Plasmodiophora brassicae (Phytomyxea, Rhizaria) is the etiological agent of clubroot disease, one of the most important diseases of Brassicaceae crops. Alteration of metabolism and hormone homeostasis leads to the formation of tumour-like galls in the roots of affected plants. Host plant energy metabolism, defence and developmental processes are under strong temporal control and the very same processes are affected by clubroot. For the first time, this study uses time-resolved transcriptome analyses to explore how P. brassicae affects Arabidopsis thaliana in the night during intermediate (14 days after inoculation; DAI) and late (21 DAI) infection. Day-night differences in gene expression were more pronounced in younger rather than older plants in our differential gene expression (DGE) analysis. Consequently, intermediate phases of infection showed more day-night differences than later ones. Clustering of differentially expressed genes (DEGs) in functional categories highlighted how some of the typical processes known to be disrupted by clubroot infection are more significantly affected in the night and also uncovered some disrupted exclusively in the night. RNA modification stood out as the most unambiguously upregulated process in infected Arabidopsis roots in the night. Analysis of the interaction between clubroot infection and diel oscillations in gene expression detected modifications in the rhythmicity of central circadian clock components during the infection. We discuss our findings in the context of manipulation of plant defence and metabolism, identifying targets for experimental validation and highlighting potential new lines of investigation of our time-resolved datasets to better understand the interaction between P. brassicae and its host. Significance statementPlasmodiophora brassicae impacts physiological processes under strong temporal control in Brassicaceae hosts: e.g., metabolism, hormone homeostasis and defence. Here, for the first time, we performed a time-resolved transcriptomic exploration of clubroot disease at intermediate and mature stages of infection. We identify a previously unrecognised role for nocturnal manipulation of organellar RNA editing and disruption of rhythmicity in circadian clock components. We provide a dataset enabling further exploration of the impact of clubroot on plant circadian processes.