Under the cover of darkness: how clubroot disease affects Arabidopsis thaliana physiology during the night

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Abstract

Background

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 tumor-like galls in the root system of affected plants. Host plant energy metabolism and developmental processes are under strong temporal control exhibiting differences between day and night. The very same processes are affected by clubroot, but the effect of the infection on the host plant in the night has never been investigated. This study uses time-resolved transcriptome analyses to explore how P. brassicae affects A. thaliana in the night during intermediate (14 DAI) and late (21 DAI) infection.

Results

Day-night differences in gene expression were more pronounced in younger rather than older plants in our differential gene expression (DGE) analysis, regardless of infection status. 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. Among these, RNA modification stood out as the most unambiguously highly upregulated process in infected Arabidopsis roots in the night. Analysis of the interaction between clubroot infection and diel oscillations in gene expression also showed a higher interplay between clubroot and time in younger plants, where many genes lost their normal day/night oscillations during the infection. Interestingly, few genes central to the plant circadian clock were found to be affected and lost their normal rhythmicity with the infection.

Conclusions

P. brassicae induces night time specific changes in gene expression during the metabolically active phases of the infection. In addition, the infection does affect rhythmic gene expression in plants including core genes of the circadian clock. Time-resolved datasets could help to better understand the interaction between P. brassicae and its hosts and constitute the first step for the investigation of clubroot-induced changes in rhythmic gene expression.

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