Plant virus evolution under strong drought conditions results in a transition from parasitism to mutualism

Environmental conditions are an important factor driving pathogens’ evolution. Here, we explore the effects of drought stress in plant virus evolution. We evolved turnip mosaic potyvirus in well-watered and drought conditions in Arabidopsis thaliana accessions that differ in their response to virus infection. Virus adaptation occurred in all accessions independently of watering status. Drought-evolved viruses conferred a significantly higher drought tolerance to infected plants. By contrast, nonsignificant increases in tolerance were observed in plants infected with viruses evolved under standard watering. The magnitude of this effect was dependent on the plant accessions. Differences in tolerance were correlated to alterations in the expression of host genes, some involved in regulation of the circadian clock, as well as in deep changes in the balance of phytohormones regulating defense and growth signaling pathways. Our results show that viruses can promote host survival in situations of abiotic stress, with the magnitude of such benefit being a selectable trait.This work was supported by Grants PID2019-103998GB-I00 and BES-2016-077078 (Agencia Estatal de Investigación–Fondo Europeo de Desarrollo Regional) to S.F.E. and R.G., respectively; GRISOLIAP/2018/005 and PROMETEU2019/012 (Generalitat Valenciana) to S.F.E.; and AICO/2019/150 (Generalitat Valenciana) to A.G.-C. Phytohormone measurements were performed at the Servei Central d’Instrumentació Científica of Universitat Jaume I.Peer reviewe