O3-Induced Leaf Senescence in Tomato Plants Is Ethylene Signaling-Dependent and Enhances the Population Abundance of Bemisia tabaci

Abstract

Elevated ozone (O₃) can alter the phenotypes of host plants particularly in induction of leaf senescence, but few reports examine the involvement of phytohormone in O₃-induced changes in host phenotypes that influence the foraging quality for insects. Here, we used an ethylene (ET) receptor mutant Nr and its wild-type to determine the function of the ET signaling pathway in O₃-induced leaf senescence, and bottom-up effects on the performance of Bemisia tabaci in field open-top chambers (OTCs). Our results showed that elevated O₃ reduced photosynthetic efficiency and chlorophyll content and induced leaf senescence of plant regardless of plant genotype. Leaf senescence in Nr plants was alleviated relative to wild-type under elevated O₃. Further analyses of foliar quality showed that elevated O₃ had little effect on phytohormone-mediated defenses, but significantly increased the concentration of amino acids in two plant genotypes. Furthermore, Nr plants had lower amino acid content relative to wild-type under elevated O₃. These results provided an explanation of O₃-induced increase in abundance of B. tabaci. We concluded that O₃-induced senescence of plant was ET signal-dependent, and positive effects of O₃-induced leaf senescence on the performance of B. tabaci largely resulted from changes of nutritional quality of host plants.

Keywords: Bemisia tabaci; amino acid; elevated O3; ethylene; hormone-dependent defense; leaf senescence.

FIGURE 1

The ET production rate and fold-change in the expression of ET synthesis genes of wild-type AC plants spraying with ACC, 1-MCP, and H₂O, and of ET-insensitive Nr mutants spraying with H₂O grown under ambient O₃ and elevated O₃. (A) ET production rate. (B) ACS. (C) ACO. Each value represents the mean (±SE) of four OTCs (10 plants for each treatment per OTC). Different lowercase letters indicate significant differences between ambient O₃ and elevated O₃ within the same genotype. Different uppercase letters indicate significant differences between genotypes following with ACC, 1-MCP, or H₂O applications within the same O₃ treatment.

FIGURE 2

The phenotype of wild-type AC plants spraying with ACC, 1-MCP, and H₂O, and of ET-insensitive Nr mutants spraying with H₂O grown under ambient O₃ and elevated O₃. (A) Biomass. (B) Photosynthetic rate. (C) Chlorophyll content. (D) ROS. (E) O₃-damaged stippled leaves. (F) Curl leaves. (G) Deciduous leaves. Each value represents the mean (±SE) of four OTCs (10 plants for each treatment per OTC). Different lowercase letters indicate significant differences between ambient O₃ and elevated O₃ within the same genotype. Different uppercase letters indicate significant differences between genotypes following with ACC, 1-MCP, or H₂O applications within the same O₃ treatment.

FIGURE 3

Abundance of B. tabaci when fed on two tomato genotypes grown under ambient O₃ and elevated O₃. Each value represents the mean (±SE) of four OTCs (eight plants for each genotype per OTC). Different lowercase letters indicate significant differences between ambient O₃ and elevated O₃ within the same genotype. Different uppercase letters indicate significant differences between genotypes within the same O₃ treatment.

FIGURE 4

SA content and fold-change in the expression of related genes involved in the SA-dependent signaling pathway in two tomato genotypes grown under ambient O₃ and elevated O₃ with and without B. tabaci infestation. (A) SA content. (B) PR. (C) GLU. Each value represents the mean (±SE) of four OTCs (eight plants for each genotype per OTC). Different lowercase letters indicate significant differences among the combinations of B. tabaci treatment and O₃ concentrations within the same genotype. Different uppercase letters indicate significant differences between genotypes within the same O₃ treatment and B. tabaci treatment.

FIGURE 5

JA content and fold-change in the expression of related genes involved in the JA-dependent signaling pathway in two tomato genotypes grown under ambient O₃ and elevated O₃ with and without B. tabaci infestation. (A) JA content. (B) LOX. (C) PI. Each value represents the mean (±SE) of four OTCs (eight plants for each genotype per OTC). Different lowercase letters indicate significant differences among the combinations of B. tabaci treatment and O₃ concentrations within the same genotype. Different uppercase letters indicate significant differences between genotypes within the same O₃ treatment and B. tabaci treatment.

FIGURE 6

Ethylene emission and fold-change in the expression of related genes involved in the ET-dependent signaling pathway in two tomato genotypes grown under ambient O₃ and elevated O₃ with and without B. tabaci infestation. (A) ET emission. (B) ERF1. (C) ERF2. Each value represents the mean (±SE) of four OTCs (eight plants for each genotype per OTC). Different lowercase letters indicate significant differences among the combinations of B. tabaci treatment and O₃ concentrations within the same genotype. Different uppercase letters indicate significant differences between genotypes within the same O₃ treatment and B. tabaci treatment.

FIGURE 7

Total nitrogen concentration for two tomato genotypes grown under ambient O₃ and elevated O₃ without B. tabaci infestation. Different lowercase letters indicate significant differences between ambient O₃ and elevated O₃ within the same genotype. Different uppercase letters indicate significant differences between genotypes within the same O₃ treatment.

FIGURE 8

Total and individual amino acid concentration for two tomato genotypes grown under ambient O₃ and elevated O₃ without B. tabaci infestation. (A) Total amino acid concentration. (B) The activity of protease. (C) Individual amino acid concentration in AC plants. (D) Individual amino acid concentration in Nr plants. Different lowercase letters indicate significant differences at P < 0.05.