Turnip mosaic virus alters phosphorus metabolism and shoot-root allocation without resource competition.

Abstract

Plant viruses affect production through symptom induction in host plants. These symptoms could partially arise from nutrient deprivation: The resource competition hypothesis posits that massive viral replication deprives hosts of essential nutrients, yet direct evidence for phosphorus (P) competition is lacking. Moreover, it is reported that biotic stresses can lead to alterations on P metabolism. Using a hydroponic system enabling separate analysis of shoots and roots in adult Arabidopsis thaliana plants, we investigated whether Turnip mosaic virus (TuMV) drawed significant P internal pools leading to P competition or altered P metabolism. TuMV genomic RNA represented < 0.3% of the P pool allocated to 18S rRNA, refuting the resource competition hypothesis. Instead, TuMV induced a marked shoot-to-root P redistribution: Shoot/Root Pi and Porg changed from 1.7 to 1.04 to 0.71 and 0.68, respectively. This altered partitioning correlated with organ-specific gene expression changes: high-affinity transporters PHT1; 4 and PHT1; 5 were co-induced in shoots, whereas immunity-related PHT1; 4 was uniquely repressed in roots. The senescence-associated gene SEN1 showed opposite regulation between organs (repressed in shoots, induced in roots), distinguishing virus-induced responses from canonical senescence. Multivariate analysis revealed that shoots and roots only partially share physiological and molecular responses to TuMV. The virus reprograms phosphorus metabolism through organ-specific changes, not through resource depletion, and roots act as a distinct hub integrating infection response, senescence, and nutrient dynamics. This study advances the understanding of growth-defense trade-offs in plant mineral nutrition and identifies new targets for maintaining crop productivity under biotic stress.