A resilient mutualistic interaction between cucumber mosaic virus and its natural host to adapt to an excess zinc environment and drought stress.

A perennial pseudometallophyte Arabidopsis halleri is frequently infected with cucumber mosaic virus (CMV) in its natural habitat. The purpose of this study was to characterize the effect of CMV infection on the environmental adaptation of its natural host A. halleri. The CMV(Ho) strain isolated from A. halleri was inoculated into clonal virus-free A. halleri plants, and a unique plant-virus system consisting of CMV(Ho) and its natural wild plant host was established. In a control environment with ambient zinc supplementation, CMV(Ho) infection retarded growth in the above-ground part of host plants but conferred strong drought tolerance. On the other hand, in an excess zinc environment, simulating a natural edaphic environment of A halleri, host plants hyperaccumulated zinc and CMV(Ho) infection did not cause any symptoms to host plants while conferring mild drought tolerance. We also demonstrated in Nicotiana benthamiana as another host that similar effects were induced by the combination of excess zinc and CMV(Ho) infection. Transcriptomic analysis indicated that the host plant recognized CMV(Ho) as a mutualistic symbiont rather than a parasitic pathogen. These results suggest a resilient mutualistic interaction between CMV(Ho) and its natural host A. halleri in its natural habitat.