Transgenerational tolerance to abiotic stresses induced by plant virus infection

Following pathogen infection, plants have developed diverse mechanisms of defense that enhance their immune system for more robust induction of defense responses against recurrent environmental stresses. This induced resistance can be heritable to the progeny, rendering them more tolerant to stressful events. Although within-generational induction of tolerance to abiotic stress is a well-documented phenomenon in virus-infected plants, the transgenerational inheritance of tolerance to abiotic stresses in their progenies has not been explored. Here, we show that infection of Nicotiana benthamiana plants by Potato virus X (PVX) and by a chimeric Plum pox virus (PPV) expressing the P25 protein of PVX (PPV-P25), but not by PPV, conferred tolerance to both salt and osmotic stresses to the progeny, which correlated with the level of virulence of the pathogen. This transgenerational tolerance to abiotic stresses in the progeny was partially sustained even if the plants experience a virus-free generation. Moreover, progenies from a Dicer-like3 mutant, irrespective whether their parents were infected or not, mimicked the enhanced tolerance to abiotic stress observed in progenies of PVX-infected wild-type plants, suggesting the involvement of 24-nt small interfering RNAs in the transgenerational tolerance to abiotic stress induced by virus infection. RNAseq analysis supported the upregulation of genes related to protein folding and response to stress in the progeny of PVX-infected plants. From an environmental point of view, the significance of virus-induced transgenerational tolerance to abiotic stress could be questionable, as its induction was offset by major reproductive costs arising from a detrimental effect on seed production Comparative gene expression profiling analysis of RNA-seq data for Nicotiana bentamina seeds derived from plants of two different genotypes (Wt and Dcl3) that were either infected with Potato virus X (WtPVX and Dcl3PVX) or mock-inoculated (Dcl3Ctr and WtCtr). Three biological replicates were analyzed for each treatment.