The interplay between virus infection and water-related stress is mediated by the plant metabolism of ascorbic acid

Plants are often subjected to environmental variations in the context of infection such that virus-induced and abiotic stresses co-occur. One such environmental variation is water stress, which strongly impacts plant fitness. Although there is ample evidence of the beneficial effects of plant viruses under drought, the consequences of infection under water excess and its molecular basis are unknown. We analyze the effect of cucumber mosaic virus (CMV) infection on Arabidopsis thaliana growth and reproduction across a reaction norm of watering conditions: from drought to waterlogging. The role of the stress-induced ascorbate-glutathione (AsA-GSH) pathway in modulating the outcome of the plant-virus-environment interaction is explored by quantifying gene expression and by using plants overexpressing monodehydroascorbate reductase (MDHAR), a key component of the pathway. Results show that CMV infection is detrimental to plant fitness under standard watering, nearly neutral under waterlogging, and beneficial under drought. Virus-derived compensation for the negative effects of drought is associated with increased expression of MDHAR. Consistent with this, under water stress plants constitutively overexpressing MDHAR reproduced the phenotypes of CMV-infected plants. This work provides novel information on how the interplay between virus infection and watering conditions shapes plant fitness and highlights the plasticity of the resulting outcome.

This work was funded by Plan Estatal de I+D+i, Agencia Estatal de Investigación, Spain (grant PID2022-141836OB-I00) to IP. GD is Universidad Politecnica de Madrid contracted Doctor under the María Zambrano programme (Ministerio de Universidades, Spain), cofounded by Severo Ochoa CBGP-Mission WALLADAPT (CEX2020-000999-S). We are grateful for the Gender Identity Grant from ASACTEI (Santa Fe, Argentina), which enabled CJ to carry out part of this work.

With funding from the Spanish government through the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2020-000999-S)

Peer reviewed