Virulence determines beneficial trade‐offs in the response of virus‐infected plants to drought via induction of salicylic acid

Abstract

It has been hypothesized that plants can get beneficial trade-offs from viral infections when grown under drought conditions. However, experimental support for a positive correlation between virus-induced drought tolerance and increased host fitness is scarce. We investigated whether increased virulence exhibited by the synergistic interaction involving Potato virus X (PVX) and Plum pox virus (PPV) improves tolerance to drought and host fitness in Nicotiana benthamiana and Arabidopsis thaliana. Infection by the pair PPV/PVX and by PPV expressing the virulence protein P25 of PVX conferred an enhanced drought-tolerant phenotype compared with single infections with either PPV or PVX. Decreased transpiration rates in virus-infected plants were correlated with drought tolerance in N. benthamiana but not in Arabidopsis. Metabolite and hormonal profiles of Arabidopsis plants infected with the different viruses showed a range of changes that positively correlated with a greater impact on drought tolerance. Virus infection enhanced drought tolerance in both species by increasing salicylic acid accumulation in an abscisic acid-independent manner. Viable offspring derived from Arabidopsis plants infected with PPV increased relative to non-infected plants, when exposed to drought. By contrast, the detrimental effect caused by the more virulent viruses overcame potential benefits associated with increased drought tolerance on host fitness.

Exploring how viruses enhance plants' resilience to drought and the limits to this form of viral payback

“…Aguilar et al () have expanded on previous studies by examining drought resistance in N. benthamiana plants following infection with plum pox virus (PPV, the causative agent of Sharka disease in Prunus spp. : Damsteegt et al, ), potato virus X (PVX), a genetically engineered PPV recombinant expressing the PVX RNA silencing suppressor molecule P25 (PPV‐P25), and mixed PPV/PVX infection.…”

“…They also examined the effects of PPV, PPV‐25, and PPV/PVX mixed infections on drought resistance in A. thaliana (note that PVX alone is not able to infect this host: Brosseau & Moffett, ). In all cases it was found that virus infection could to some extent relieve the symptoms of drought (Aguilar et al, ).…”

“…Another interesting phenomenon discovered from studies of stressed plants, is that virus‐infected plants can display increased resilience to cold and drought (Xu et al, ; Davis et al, ). In this issue of Plant, Cell and Environment , Aguilar et al () explore to what extent increased drought resistance may be a payback to the host, and the mechanistic basis of virus‐induced drought resistance, focusing on changes in levels of osmoprotective metabolites and the potential role of the plant phytohormone salicylic acid (SA).…”

The C4 protein from the geminivirus Tomato yellow leaf curl virus confers drought tolerance in Arabidopsis through an ABA‐independent mechanism

“…Viruses have been shown to enhance drought tolerance through the promotion of salicylic acid (SA) signalling (Aguilar et al , ). C4‐expressing plants, however, do not overaccumulate SA and do not display increased expression of SA marker genes (data not shown), indicating that the events underlying the effect of C4 on drought stress tolerance are different to the ones previously described for other viruses (Aguilar et al , ; Westwood et al , ; Xu et al , ).…”

“…Plants have adopted a wide range of strategies to confront the negative effects of drought, including increasing water uptake by optimizing the root system, closing stomata to limit the water loss caused by transpiration, accumulating osmoprotectants, or producing the hormone abscisic acid (ABA). This intricate scenario makes drought resistance a highly complex trait, with polygenic nature, low heritability, and vastly influenced by genotypeenvironment interactions (Fang and Xiong, 2014).A growing body of evidence indicates that viral infections can result in improved plant tolerance to abiotic stresses (see, among others: Aguilar et al, 2017;Anfoka et al, 2016;Westwood et al, 2012;Xu et al, 2008), raising the tantalizing idea that the identification of the molecular mechanisms underlying these viral effects could unlock yet-unknown stress tolerance strategies and pave the way for the generation of stress-resilient plants. Geminiviruses are viruses with small circular, single-stranded DNA genomes that infect a broad range of plants.…”