Cold suppresses virus accumulation and alters the host transcriptomic response in the turnip mosaic virus - Arabidopsis halleri system

Abstract

Since plant viruses cause lifelong infections, virus–plant interactions are exposed to large temperature fluctuations in evergreen perennials. In such circumstances, virus–plant interactions are expected to change significantly between the warm and cold seasons. However, few studies have investigated the effects of cold temperatures on virus–plant interactions. Here, we show that in a persistent infection system of the turnip mosaic virus (TuMV)–Arabidopsis halleri, cold temperatures lead to slow viral replication/spreading within the host, attenuated host symptoms, and cold-specific transcriptomic responses. Many differentially expressed genes (DEGs) were detected between virus-inoculated and mock-inoculated plants under warm and cold conditions; however, the sets of DEGs and response timings were temperature-dependent. At cold temperatures, the expression of photosynthesis-related genes decreased in the early stages of infection. However, it recovered to the same level as that in uninfected plants in the later stages. In contrast, the transcriptomic changes under warm conditions suggest that viral infections cause auxin signaling disruption. These responses coincided with the inhibition of host growth. We identified 6 cold- and 38 warm-specific DEGs, which changed their expression in response to TuMV infection under more than half of the conditions for either cold or warm temperatures. Further validation of the putative relationships between transcriptomic and phenotypic responses of the host is required. Our findings on temperature-dependent host responses at both symptomatic and transcriptomic levels help us understand how warm and cold temperatures affect virus–plant interactions in seasonal environments.