The Combined Effect of Elevated O3 Levels and TYLCV Infection Increases the Fitness of Bemisia tabaci Mediterranean on Tomato Plants

Global change and biotic stress, such as tropospheric contamination and virus infection, can individually modify the quality of host plants, thereby altering the palatability of the plant for herbivorous insects. The bottom-up effects of elevated O3 and tomato yellow leaf curl virus (TYLCV) infection on tomato plants and the associated performance of Bemisia tabaci Mediterranean (MED) were determined in open-top chambers. Elevated O3 decreased eight amino acid levels and increased the salicylic acid (SA) and jasmonic acid (JA) content and the gene expression of pathogenesis-related protein (PR1) and proteinase inhibitor (PI1) in both wild-type (CM) and JA defense-deficient tomato genotype (spr2). TYLCV infection and the combination of elevated O3 and TYLCV infection increased eight amino acids levels, SA content and PR1 expression, and decreased JA content and PI1 expression in both tomato genotypes. In uninfected tomato, elevated O3 increased developmental time and decreased fecundity by 6.1 and 18.8% in the CM, respectively, and by 6.8 and 18.9% in the spr2, respectively. In TYLCV-infected tomato, elevated O3 decreased developmental time and increased fecundity by 4.6 and 14.2%, respectively, in the CM and by 4.3 and 16.8%, respectively, in the spr2. These results showed that the interactive effects of elevated O3 and TYLCV infection partially increased the amino acid content and weakened the JA-dependent defense, resulting in increased population fitness of MED on tomato plants. This study suggests that whiteflies would be more successful at TYLCV-infected plants than at uninfected plants in elevated O3 levels.