The Stress Response of Aphids to the Accumulation of Heavy Metals Along Vicia faba L. Under Cadmium Treatment

Abstract

Due to the intensification of human activities, the ecosystems are being polluted by heavy metals. The pollution of heavy metals in agricultural systems has become a serious issue of global concern. This study detected the bioaccumulation of cadmium (Cd) in broad beans and aphids through continuous exposure to varying concentrations of Cd pollution (0, 3.125, 6.25, 12.5, 25, 50 mg/L) and subsequently examined its effects on aphid energy metabolism and reproductive ability. The results showed that Cd can be transmitted and accumulated between Vicia faba L. and aphids along the food chain, and the amount of accumulation was related to the Cd treatment concentration. Quantitative real-time PCR results showed that the expression levels of trehalase (TRE) and trehalose-6-phosphate synthase (TPS) in F1 were significantly upregulated, and those of vitellogenin (Vg) were varied across the five generations of aphids after Cd treatment, which were up-regulated, and others down-regulated. Compared with the control group, the glycogen content and two types of trehalase activities of the first-generation Cd-treatment aphids were decreased, while trehalose content increased; there was no significant change in the carbohydrate content and trehalase activity of the fourth and fifth generations of aphids. In addition, the reproduction of female aphids was inhibited. This research is helpful for studying the toxic effects of heavy metals on insects and the adaptation mechanisms of insects to extreme environments. It also provides a theoretical basis for further exploring the molecular mechanisms of Cd homeostasis in plants and insects under Cd stress.

Keywords: Megoura crassicauda; Vicia faba L.; bioaccumulation; cadmium; energy metabolism; food chain.

Figure 1

Cd²⁺ content in soaked seeds (A), roots (B), stems (C), and leaves (D) of broad beans and five batches of aphids (E). Bars represent means (±SD) of three replicate experiments. Bars with different letters indicate significant differences (Tukey method, p < 0.05). Note: Tukey method analysis was performed on different groups of aphids from the same batch, with different letters indicating significant differences between the two.

Figure 2

Contents of glycogen (A), glucose (B), and trehalose (C) in different groups of aphids. Bars represent means (±SE) of three replicate experiments. Bars with different letters indicate significant differences (Tukey method, p < 0.05). Note: Tukey method analysis was performed on different groups of aphids from the same batch, with different letters indicating significant differences between the two.

Figure 3

Changes in the activity of two trehalase enzymes in adult aphids of different generations under different Cd concentrations. (A) Soluble trehalase activity. (B) Membrane-bound trehalase activity. Bars represent means (±SE) of three replicate experiments. Three biological replicates were performed on 10 adult aphids of M. crassicauda in each treatment. Bars with different letters indicate significant differences (Tukey method, p < 0.05). Note: Tukey method analysis was performed on different groups of aphids from the same batch, with different letters indicating significant differences between the two.

Figure 4

Relative expression levels of trehalase and trehalose-6-phosphate synthase genes in adult aphids of different generations under different cadmium concentrations. (A) Trehalase gene, TRE. (B) Trehalose-6-phosphate synthase gene, TPS. Three biological replicates were performed on 10 adult aphids of M. crassicauda in each treatment. Bars represent means (±SE) of three replicate experiments. Bars with different letters indicate significant differences (Tukey method, p < 0.05). Note: Tukey method analysis was performed on different groups of aphids from the same batch, with different letters indicating significant differences between the two.

Figure 5

Changes in the number of offspring and vitellogenin gene expression levels of adult aphids from different generations under different Cd concentrations. The number of offspring produced by female aphids from the first generation within 7 days and the expression level of vitellogenin (Vg) gene in the aphid on the first day of aphid production statistics (A). The number of offspring produced by female aphids from the second generation within 7 days and the expression level of vitellogenin (Vg) gene in the aphid on the first day of aphid production statistics (B). The number of offspring produced by female aphids from the third generation within 7 days and the expression level of vitellogenin (Vg) gene in the aphid on the first day of aphid production statistics (C). The number of offspring produced by female aphids from the fourth generation within 7 days and the expression level of vitellogenin (Vg) gene in the aphid on the first day of aphid production statistics (D). The number of offspring produced by female aphids from the fifth generation within 7 days and the expression level of vitellogenin (Vg) gene in the aphid on the first day of aphid production statistics (E). Three biological replicates were performed on 8 adult aphids of M. crassicauda in each treatment. Bars represent means (±SE) of three replicate experiments. Bars with different letters indicate significant differences (Tukey method, p < 0.05). Note: Tukey method analysis was performed on different groups of aphids from the same batch, with different letters indicating significant differences between the two.