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Cited by 11Insect-Plant Interactions and ControlInsect Pest Control StrategiesPlant biochemistry and biosynthesis

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Metabolomic Profiling Reveals the Anti-Herbivore Mechanisms of Rice (Oryza sativa)

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Gu, Chengzhen, Zhang, Yujia, Wang, Mengmeng, Lin, Yangzheng, Zeng, Bixue, Zheng, Xinyu, Song, Yuanyuan, Zeng, Rensen·2024·International Journal of Molecular Sciences
DOI 10.3390/ijms25115946PMC PMC11172427
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Abstract

The use of secondary metabolites of rice to control pests has become a research hotspot, but little is known about the mechanism of rice self-resistance. In this study, metabolomics analysis was performed on two groups of rice (T1, with insect pests; T2, without pests), indicating that fatty acids, alkaloids, and phenolic acids were significantly up-regulated in T1. The up-regulated metabolites (p-value < 0.1) were enriched in linoleic acid metabolism, terpene, piperidine, and pyridine alkaloid biosynthesis, α-linolenic acid metabolism, and tryptophan metabolism. Six significantly up-regulated differential metabolites in T1 were screened out: N-trans-feruloyl-3-methoxytyramine (1), N-trans-feruloyltyramine (2), N-trans-p-coumaroyltyramine (3), N-cis-feruloyltyramine (4), N-phenylacetyl-L-glutamine (5), and benzamide (6). The insect growth inhibitory activities of these six different metabolites were determined, and the results show that compound 1 had the highest activity, which significantly inhibited the growth of Chilo suppressalis by 59.63%. Compounds 2–4 also showed a good inhibitory effect on the growth of Chilo suppressalis, while the other compounds had no significant effect. RNA-seq analyses showed that larval exposure to compound 1 up-regulated the genes that were significantly enriched in ribosome biogenesis in eukaryotes, the cell cycle, ribosomes, and other pathways. The down-regulated genes were significantly enriched in metabolic pathways, oxidative phosphorylation, the citrate cycle (TCA cycle), and other pathways. Eighteen up-regulated genes and fifteen down-regulated genes from the above significantly enriched pathways were screened out and verified by real-time quantitative PCR. The activities of detoxification enzymes (glutathione S-transferase (GST); UDP-glucuronosyltransferase (UGT); and carboxylesterase (CarE)) under larval exposure to compound 1 were measured, which indicated that the activity of GST was significantly inhibited by compound 1, while the activities of the UGT and CarE enzymes did not significantly change. As determined by UPLC-MS, the contents of compound 1 in the T1 and T2 groups were 8.55 ng/g and 0.53 ng/g, respectively, which indicated that pest insects significantly induced the synthesis of compound 1. Compound 1 may enhance rice insect resistance by inhibiting the detoxification enzyme activity and metabolism of Chilo suppressalis, as well as promoting cell proliferation to affect its normal growth and development process. The chemical–ecological mechanism of the insect resistance of rice is preliminarily clarified in this paper.

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Crossref · 10.3390/ijms25115946

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Figures

Figure 1 Qualitative, quantitative, and quality control analyses of metabolites. (A) Sample CV distribution map. (B) Heat map of correlation between samples. (C) PCA diagram of T1 and T2 samples. (D) OPLS–DA validation diagram.
Figure 1 Qualitative, quantitative, and quality control analyses of metabolites. (A) Sample CV distribution map. (B) Heat map of correlation between samples. (C) PCA diagram of T1 and T2 samples. (D) OPLS–DA validation diagram.CC BY · PubMed Central
Figure 2 Volcano plot and clustering analysis of differential metabolites. (A) Volcano plot of differential metabolites between T1 and T2 groups. Red dots indicate an up-regulation of metabolite accumulation, while green dots indicate a down-regulation of metabolite accumulation. (B) Differential metabolite clustering heatmap between T1 and T2 groups. Z–score value displays a change in color from high (red) to low (green).
Figure 2 Volcano plot and clustering analysis of differential metabolites. (A) Volcano plot of differential metabolites between T1 and T2 groups. Red dots indicate an up-regulation of metabolite accumulation, while green dots indicate a down-regulation of metabolite accumulation. (B) Differential metabolite clustering heatmap between T1 and T2 groups. Z–score value displays a change in color from high (red) to low (green).CC BY · PubMed Central
Figure 3 KEGG enrichment map and differential abundance score map of differential metabolites in T1 and T2 groups.
Figure 3 KEGG enrichment map and differential abundance score map of differential metabolites in T1 and T2 groups.CC BY · PubMed Central
Figure 4 Cluster heat map of alkaloid differential metabolites in T1 and T2 (* represent the isomer).
Figure 4 Cluster heat map of alkaloid differential metabolites in T1 and T2 (* represent the isomer).CC BY · PubMed Central
Figure 5 Compounds 1–6.
Figure 5 Compounds 1–6.CC BY · PubMed Central
Figure 6 Effect of compounds 1–4 on the body weight of Chilo suppressalis and the change in body weight growth inhibition rate over time (a and b represent a significant difference between the two groups).
Figure 6 Effect of compounds 1–4 on the body weight of Chilo suppressalis and the change in body weight growth inhibition rate over time (a and b represent a significant difference between the two groups).CC BY · PubMed Central
Figure 7 Standard curve of compound 1.
Figure 7 Standard curve of compound 1.CC BY · PubMed Central
Figure 8 Absolute content of compound 1 in two groups of rice materials (a and b represent a significant difference between the two groups).
Figure 8 Absolute content of compound 1 in two groups of rice materials (a and b represent a significant difference between the two groups).CC BY · PubMed Central
Figure 9 The effect of compound 1 on detoxifying enzymes’ activities in Chilo suppressalis. (A) GST enzyme activity, (B) UGT enzyme activity, and (C) CarE enzyme activity. Asterisks indicate significant differences (* p < 0.05; Student’s t-test) (Red represent the treatment group, blue represent the control group).
Figure 9 The effect of compound 1 on detoxifying enzymes’ activities in Chilo suppressalis. (A) GST enzyme activity, (B) UGT enzyme activity, and (C) CarE enzyme activity. Asterisks indicate significant differences (* p < 0.05; Student’s t-test) (Red represent the treatment group, blue represent the control group).CC BY · PubMed Central
Figure 10 BUSCO assessment results.
Figure 10 BUSCO assessment results.CC BY · PubMed Central
Figure 11 Correlation analysis and volcano plot of CK group and RT group.
Figure 11 Correlation analysis and volcano plot of CK group and RT group.CC BY · PubMed Central
Figure 12 GO enrichment histogram and GO enrichment scatterplot of differential genes in CK and RT groups. (A) Enriched GO terms; (B) GO enrichment scatterplot of up–regulated genes in expression levels; and (C) GO enrichment scatterplot of down-regulated genes in expression levels.
Figure 12 GO enrichment histogram and GO enrichment scatterplot of differential genes in CK and RT groups. (A) Enriched GO terms; (B) GO enrichment scatterplot of up–regulated genes in expression levels; and (C) GO enrichment scatterplot of down-regulated genes in expression levels.CC BY · PubMed Central
Figure 13 Scatterplots of KEGG enrichment in CK and RT groups. (A) KEGG enrichment scatterplot of up-regulated genes in expression levels; (B) KEGG enrichment scatterplot of down-regulated genes in expression levels.
Figure 13 Scatterplots of KEGG enrichment in CK and RT groups. (A) KEGG enrichment scatterplot of up-regulated genes in expression levels; (B) KEGG enrichment scatterplot of down-regulated genes in expression levels.CC BY · PubMed Central
Figure 14 Effect of Compound 1 on gene expression of Chilo suppressalis. (A) The expression levels of up-regulated differentially expressed genes. (B) The expression levels of down-regulated differentially expressed genes (* and ** represent a significant difference between the two groups; n.d. represent the gene was not detected).
Figure 14 Effect of Compound 1 on gene expression of Chilo suppressalis. (A) The expression levels of up-regulated differentially expressed genes. (B) The expression levels of down-regulated differentially expressed genes (* and ** represent a significant difference between the two groups; n.d. represent the gene was not detected).CC BY · PubMed Central

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Citations

Cites

Research works printed but not linked: 5

  1. Yang, 2021, The insect-resistance physiology of plants: A review, Chin. Agr. Sci. Bull., 37, 130
  2. Li, 2018, Research progress of chemical interactions between rice and brown planthopper, Plant Physiol. J., 54, 528
  3. Lv, Y.H. (2007). Comparision of Defense Chemicals of Rice Plants Infested by Different Herbivores and Setup of Rice Lines with Antisense Inhibition of Defense-Related Gene OPR1 or PLD3. [Master’s Thesis, Zhejiang University].
  4. Luo, T., Lu, H.P., and Shu, Q.Y. (2015, January 27–30). The pathway of tryptophan metabolism influences the defense response of rice to brown planthopper. Proceedings of the 7th Symposium on Plant Allelopathy in China, Kunming, China.
  5. Cheng, Y.B. (2021). Mechanisms of ROS-CncC Pathway Regulating Insecticide Tolerance in Response to Phytochemicals in Spodoptera litura. [Master’s Thesis, Fujian Agriculture and Forestry University].

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Metadata

Authors
Gu, C., Zhang, Y., Wang, M., Lin, Y., Zeng, B., Zheng, X., Song, Y., & Zeng, R.
Affiliations
Fujian Agriculture and Forestry University (CN)
Corresponding author
  • Song, Yuanyuan
  • Zeng, Rensen
ORCID
Venue
International Journal of Molecular Sciences
Publisher
MDPI AG
Published
2024-05-29
Volume
25
Issue
11
Pages
5946
ISSN
1422-0067 (ISSN-L)
DOI
10.3390/ijms25115946
PMC
PMC11172427
OpenAlex
W4399174257
Cited by
11
References
30
Citations by year
2026: 3 · 2025: 8
FWCI
3.56
Type
journal article
Language
en
Open access
Licence
Locations
  • International Journal of Molecular Sciences (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • National Natural Science Foundation of China (31800332, 32371588, XJQ201922, 2021J01095, 2021J01075, 2022J01591, GBMUC-2019-007)
  • Distinguished Youth Talent Program of the Fujian Agriculture and Forestry University (31800332, 32371588, XJQ201922, 2021J01095, 2021J01075, 2022J01591, GBMUC-2019-007)
  • Natural Science Foundation of Fujian Province (31800332, 32371588, XJQ201922, 2021J01095, 2021J01075, 2022J01591, GBMUC-2019-007)
  • Fujian Agriculture and Forestry University (31800332, 32371588, XJQ201922, 2021J01095, 2021J01075, 2022J01591, GBMUC-2019-007)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Insect Pest Control Strategies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant biochemistry and biosynthesis
Keywords
plant defense against herbivores, Chilo suppressalis, secondary metabolites, N-trans-feruloyltyramine, benzamide, insect growth inhibition, phenolic acids, fatty acids, glutathione S-transferase, detoxification enzymes
MeSH terms
Alkaloids, Animals, Coumaric Acids, Oryza, Tyramine, Gene Expression Regulation, Plant, Metabolomics, Metabolome, Herbivory

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