Perception of volatiles produced by UVC-irradiated plants alters the response to viral infection in naïve neighboring plants

Abstract

Interplant communication of stress via volatile signals is a well-known phenomenon. It has been shown that plants undergoing stress caused by pathogenic bacteria or insects generate volatile signals that elicit defense response in neighboring naïve plants. Similarly, we have recently shown that naïve plants sharing the same gaseous environment with UVC-exposed plants exhibit similar changes in genome instability as UVC-exposed plants. We found that methyl salicylate (MeSA) and methyl jasmonate (MeJA) serve as volatile signals communicating genome instability (as measured by an increase in the homologous recombination frequency). UVC-exposed plants produce high levels of MeSA and MeJA, a response that is missing in an npr1 mutant. Concomitantly, npr1 mutants are impaired in communicating the signal leading to genome instability, presumably because this mutant does not develop new necrotic lesion after UVC irradiation as observed in wt plants. To analyze the potential biological significance of such plant-plant communication, we have now determined whether bystander plants that receive volatile signals from UVC-irradiated plants, become more resistant to UVC irradiation or infection with oilseed rape mosaic virus (ORMV). Specifically, we analyzed the number of UVC-elicited necrotic lesions, the level of anthocyanin pigments, and the mRNA levels corresponding to ORMV coat protein and the NPR1-regulated pathogenesis-related protein PR1 in the irradiated or virus-infected bystander plants that have been previously exposed to volatiles produced by UVC-irradiated plants. These experiments showed that the bystander plants responded similarly to control plants following UVC irradiation. Interestingly, however, the bystander plants appeared to be more susceptible to ORMV infection, even though PR1 mRNA levels in systemic tissue were significantly higher than in the control plants, which indicates that bystander plants could be primed to strongly respond to bacterial infection.

Figure 1. Levels of anthocyanin and number of necrotic lesions in UV irradiated plants. Analysis of anthocyanin levels (A) and the number of necrotic lesions (B) was done as described in methods section. Ct, control non-exposed plants; ct-UV, UV-irradiate control plants; UV-UV, UV-irradiated plants previously exposed to UV; BS-UV, UV-irradiated bystander plants. Different letters indicated significantly different data points (p < 0.05).

Figure 2. Levels of anthocyanin and number of necrotic lesions in ORMV infection plants. Analysis of anthocyanin levels (A) and the number of necrotic lesions (B) was done as described in methods section. Ct, control non-exposed plants; ct-ORMV, ORMV-infected control plants; UV-ORMV, ORMV-infected plants previously exposed to UV; BS-ORMV, ORMV-infected bystander plants. Different letters indicated significantly different data points (p < 0.05).

Figure 3. Quantification of ORMV infection and PR1 gene expression. Steady-state mRNA level of ORMV coat protein (A) and PR1 mRNA (B) was done as described in methods section. Ct, control non-exposed plants; ct-ORMV, ORMV-infected tissue of control plants; ct-distal, non-infected tissue of ORMV-infected control plants; UV-ORMV, ORMV-infected tissues of plants previously exposed to UV; UV-distal, non-infected tissue of ORMV-infected plants previously exposed to UV; BS-ORMV, ORMV-infected tissue of bystander plants; BS-distal, non-infected tissue of ORMV-infected bystander plants. Different letters indicated significantly different data points (p < 0.05).

Figure 4. Model explaining changes in bystander plants.