A source-sink model explains the difference in the metabolic mechanism of mechanical damage to young and senescing leaves in Catharanthus roseus

Abstract

Background: Mechanical damage is an unavoidable threat to the growth and survival of plants. Although a wound to senescing (lower) leaves improves plant vitality, a wound to younger (upper) leaves often causes damage to or death of the whole plant. Source-sink models are often used to explain how plants respond to biotic or abiotic stresses. In this study, a source-sink model was used to explain the difference in the metabolic mechanism of mechanical damage to young and senescing leaves of Catharanthus roseus.

Results: In our study, GC-MS and LC-QTOF-MS metabolomics techniques were used to explore the differences in source-sink allocation and metabolic regulation in different organs of Catharanthus roseus after mechanical damage to the upper/lower leaves (WUL/WLL). Compared with that of the control group, the energy supplies of the WUL and WLL groups were increased and delivered to the secondary metabolic pathway through the TCA cycle. The two treatment groups adopted different secondary metabolic response strategies. The WLL group increased the input to the defense response after damage by increasing the accumulation of phenolics. A source-sink model was applied to the defensive responses to local (damaged leaves) and systemic (whole plant) damage. In the WUL group, the number of sinks increased due to damage to young leaves, and the tolerance response was emphasized.

Conclusion: The accumulation of primary and secondary metabolites was significantly different between the two mechanical damage treatments. Catharanthus roseus uses different trade-offs between tolerance (repair) and defense to respond to mechanical damage. Repairing damage and chemical defenses are thought to be more energetically expensive than growth development, confirming the trade-offs and allocation of resources seen in this source-sink model.

Keywords: Catharanthus roseus; Mechanical damage; Metabolomics; Resource trade-off; Source-sink model.

Fig. 1

The PCA and PLS-DA score plot of primary metabolism, TIAS, and PCs of mechanical wounding: a: PCA score plot of primary metabolites; b. PLS-DA score plot of primary metabolites; c: PCA score plot of phenolic metabolites; d. PLS-DA score plot of phenolic metabolites; e: PCA score plot of alkaloid metabolites; f. PLS-DA score plot of alkaloid metabolites; CK: Control group, WUL: damaged upper leaf group, WLL: damaged lower leaf group

Fig. 2

The relative content Q-values for major primary metabolites were analyzed using GC-MS: a. Sugars, b. Amino acids, c. fatty acids, d. TCA cycle metabolites; Control group, CK; Damaged upper leaf group, WUL; Damaged lower leaf, WLL

Fig. 3

Significantly different changes in L-phenylalanine, C6C1, and C6C3-type PCs: CK: Control group, WUL: damaged upper leaf group, WLL: damaged lower leaf; group; n = 6, “**” means that there is an extremely significant difference between the treatment group and the control group (p < 0.01), “*” means that there is a significant difference between the treatment group and the control group (p < 0.05)

Fig. 4

Significantly different changes in C6C3C6-type PCs: CK: Control group, WUL: damaged upper leaf group, WLL: damaged lower leaf; group; n = 6, “**” means that there is an extremely significant difference between the treatment group and the control group (p < 0.01), “*” means that there is a significant difference between the treatment group and the control group (p < 0.05)

Fig. 5

Significantly different changes in TIAs: CK: Control group, WUL: damaged upper leaf group, WLL: damaged lower leaf group; n = 6, “**” means that there is an extremely significant difference between the treatment group and the control group (p < 0.01), “*” means that there is a significant difference between the treatment group and the control group (p < 0.05)

Fig. 6

Metabolic allocation map. The grid shows the CK, WUL and WLL groups from left to right; the content from low to high is indicated by the color scale from blue to red, respectively; a solid line represents a one-step reaction, and a dotted line represents a multistep reaction; the TIA Q values and phenol Q values are represented in a histogram; CK: control group, WUL: damaged upper leaf group, WLL: damaged lower leaf group

Fig. 7

Diagram of the network of secondary metabolites. The grid shows the CK, WUL and WLL groups from left to right, respectively; the content of PCs from low to high is indicated by the color scale from red to white, respectively; the content of TIAs from low to high is indicated by the color scale from blue to red, respectively; a solid line represents a one-step reaction, and a dotted line represents a multistep reaction; CK: control group, WUL: damaged upper leaf group, WLL: damaged lower leaf group