The green peach aphid Myzus persicae perform better on pre-infested Chinese cabbage Brassica pekinensis by enhancing host plant nutritional quality

Abstract

The green peach aphid, Myzus persicae Sulzer, is a notorious pest on vegetables, which often aggregates in high densities on crop leaves. In this study, we investigated whether M. persicae could suppress the resistance level of Chinese cabbage Brassica pekinensis. M. persicae performed better in terms of weight gain (~33% increase) and population growth (~110% increase) when feeding on previously infested (pre-infested) Chinese cabbage compared with those on non-infested plants. However, when given a choice, 64% of the aphids preferred to settle on non-infested leaves, while 29% of aphids chose pre-infested leaves that had a 2.9 times higher concentration of glucosinolates. Aphid feeding significantly enhanced the amino acid:sugar ratio of phloem sap and the absolute amino acid concentration in plant leaves. Aphid infestation significantly increased the expression levels of salicylic acid (SA) marker genes, while it had marginal effects on the expression of jasmonate marker genes. Exogenously applied SA or methyl jasmonate had no significant effects on M. persicae performance, although these chemicals increased glucosinolates concentration in plant leaves. M. persicae infestation increase amino acid:sugar ratio and activate plant defenses, but aphid performed better on pre-infested plants, suggesting that both nutrition and toxics should be considered in insect-plant interaction.

Figure 1. The performance of M. persicae on pre-infested plants and control plants.

(a) Aphid weight after feeding for five days on non-infested plants (Control) and previously infested plants (Pre-infested). (b) Number of nymphs produced by per aphid after feeding for seven days. Aphids were born on treated Chinese cabbage plants and their weight or nymphs produced were examined after indicated time. Values shown are mean ± SE. *P < 0.05; Student’s t-test (Fig. 1a) or Mann-Whitney U test (Fig. 1b).

Figure 2. Settling preference of M. persicae on Chinese cabbage leaves.

Proportion of responding M. persicae adults settled on non-infested plants (Control) and previously infested plants (Pre-infested). **P < 0.001; chi-square test. Values shown are mean ± SE.

Figure 3

Relative expression levels of salicylic acid (a,b) and jasmonate (c,d) marker genes in M. persicae infested plants (Infested) or non-infested plants (Control). Leaves were collected and analysed after aphid feeding for one, three, and five days. The gene expression ratio of Chinese cabbage leaves infested by M. persicae was calculated relative to the control group, using actin gene expression for normalization. Values shown are mean ± SE. *P < 0.05. Gene abbreviations: β-1, 3-GLUCANASE 2 (BrBGL2), PATHOGENESIS-RELATED 1 (BrPR1), LIPOXYGENASE 2 (BrLOX2), VEGETATIVE STORAGE PROTEIN 2 (BrVSP2).

Figure 4

Relative expression levels of salicylic acid (SA) (a,b) and jasmonate (c,d) marker genes in SA and methyl jasmonate (MeJA) treated leaves. Leaves were collected two days after treatment. The gene expression ratio of Chinese cabbage leaves treated by MeJA or SA was calculated relative to the control group, using actin gene expression for normalization. Values shown are mean ± SE. *P < 0.05; **P < 0.01. Gene abbreviations: β-1, 3-GLUCANASE 2 (BrBGL2), PATHOGENESIS-RELATED 1 (BrPR1), LIPOXYGENASE 2 (BrLOX2), VEGETATIVE STORAGE PROTEIN 2 (BrVSP2).

Figure 5. M. persicae feeding changed the nutritional quality of its host plants.

(a) Relative amino acid concentration in phloem sap of non-infested plants (Control) and M. persicae infested plants (Infested). (b) The amino acid:sugar (sucrose, fructose, and glucose) ratio in phloem sap of control and aphid infested plants. (c) Relative sugar concentration in phloem sap of control and aphid infested plants. (d) Amino acid concentration and (e) sugar concentration in non-infested control and aphid infested (Infested) plant leaves. Values shown are mean ± SE. *P < 0.05, **P < 0.01; Student’s t-test.

Figure 6. The effects of M. persicae feeding and methyl jasmonate (MeJA) or salicylic acid (SA) treatment on glucosinolate concentration in plant leaves.

(a,b) M. persicae feeding increased indole glucosinolate concentration in plant leaves. **P < 0.01; Student’s t-test. (c,d) MeJA and SA treatment on glucosinolate concentration in plant leaves. Kruskal-Wallis test. Different letters above bars indicate significant difference at P < 0.05. Values shown are mean ± SE. Glucosinolate side chain abbreviations: 4MTB, 4-methylsulfinylbutyl; I3M, indol-3-ylmethyl; 4MI3M, 4-methoxyindol-3-ylmethyl; 4OHI3M, 4-hydroxyindol-3-ylmethyl; 1MI3M, 1-methoxyindol-3-ylmethyl.

Figure 7. Model of the interaction between M. persicae and Chinese cabbage plants.

M. persicae infestation activated salicylic acid (SA) signaling pathway and increase accumulation of glucosinolates in Chinese cabbage leaves, which have antibiotic and antixenotic effects to M. persicae. SA is a positive regulator of glucosinolates and SA possibly promote plant senescence that may contribute to the increase of free amino acid in plant leaves. Amino acid is a key nutrition for aphids. Thus, M persicae reduce direct resistance of Chinese cabbage likely contributes to the higher nutritional quality in infested leaves. Solid arrows indicate promotion or positive modulation of the processes and dashed arrows indicate possible promotion of the processes. Vertical bar indicates negative modulation of the process.