Nutrition versus defense: Why Myzus persicae (green peach aphid) prefers and performs better on young leaves of cabbage

Abstract

Plant leaves of different ages differ in nutrients and toxic metabolites and thus exhibit various resistance levels against insect herbivores. However, little is known about the influence of leaf ontogeny on plant resistance to phloem-feeding insects. In this study, we found that the green peach aphid, Myzus persicae, preferred to settle on young cabbage leaves compared with mature or old leaves, although young leaves contained the highest concentration of glucosinolates. Furthermore, aphids feeding on young leaves had higher levels of glucosinolates in their body, but aphids performed better on young leaves in terms of body weight and population growth. Phloem sap of young leaves had higher amino acid:sugar molar ratio than mature leaves, and aphids feeding on young leaves showed two times longer phloem feeding time and five times more honeydew excretion than on other leaves. These results indicate that aphids acquired the highest amount of nutrients and defensive metabolites when feeding on young cabbage leaves that are strong natural plant sinks. Accordingly, we propose that aphids generally prefer to obtain more nutrition rather than avoiding host plant defense, and total amount of nutrition that aphids could obtain is significantly influenced by leaf ontogeny or source-sink status of feeding sites.

Fig 1

Preference of M. persicae for pairs of different-aged leaves (A-C) (paired t-test: *P < 0.05); and performance of M. persicae in terms of body weight (D), nymph production (E), and number of adults (F). Different letters above the bars indicate significant differences (P < 0.05). Values are means ± SE (n = 10).

Fig 2. Nutrition quality in cabbage leaves for Myzus persicae.

Amino acid contents in different-aged leaves (A-C), and the amino acid concentrations (D) and amino acid:sugar molar ratios (E) in the phloem sap. Different letters above the bars indicate significant differences (P < 0.05). Values are means ± SE (n = 8).

Fig 3. Myzus persicae preference for glutamine, methionine, and valine.

Number of adult M. persicae settled on the 15% sucrose solution (control) or the sucrose solution containing glutamine (A), methionine (B), or valine (C). (Paired t-test: *P < 0.05, **P < 0.01). Values are means ± SE (n = 10).

Fig 4. Concentrations of glucosinolates in different-aged cabbage leaves and aphids feeding on them.

Glucosinolates concentrations in different-aged cabbage leaves (A-B), and in Myzus persicae feeding on these leaves (C-D). Different letters above the bars indicate significant differences (P < 0.05). Values are means ± SE (n = 8). 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; 4MSB, 4-Methylsuphinylbutyl.

Fig 5. Myzus persicae phloem feeding activities and honeydew production rate on different-aged cabbage leaves.

Total probing time (A), mean phloem feeding duration (B), total phloem feeding duration (C), and honeydew production (D) by M. persicae on cabbage leaves. Different letters above the bars indicate significant differences (P < 0.05). Values are means ± SE (n = 22–25 for figs A-C; n = 5 for fig D).

Fig 6. Source-sink status of plant leaves influence host plant resistance to aphids.

Young leaves have higher growth capacity than older ones and contain more defensive metabolites. However, aphids can obtain more phloem sap when feeding on young leaves that are natural plant sinks where phloem sap flows to. In contrast, aphids feeding on mature or old leaves compete for phloem sap with natural plant sinks and may thus ingest less phloem sap. To maximize their fitness, aphids generally prefer to obtain more nutrients by feeding on plant sinks rather than avoiding ingesting more plant defense metabolites in these tissues. Red arrows indicate phloem flow direction.