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Lipid profiles reveal different responses to brown planthopper infestation for pest susceptible and resistant rice plants

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Abstract

Introduction

Brown planthopper (BPH) is the most destructive insect pest for rice, causing major reductions in rice yield and large economic losses. More than 31 BPH-resistance genes have been located, and several of them have been isolated. Nevertheless, the metabolic mechanism related to BPH-resistance genes remain uncharacterized.

Objectives

To elucidate the resistance mechanism of the BPH-resistance gene Bph6 at the metabolic level, a Bph6-transgenic line R6 (BPH-resistant) and the wild-type Nipponbare (BPH-susceptible) were used to investigate their lipid profiles under control and BPH treatments.

Methods

In conjunction with multivariate statistical analysis and quantitative real-time PCR, BPH-induced lipid changes in leaf blade and leaf sheath were investigated by GC–MS-based lipidomics.

Results

Forty-five lipids were identified in leaf sheath extracts. Leaf sheath lipidomics analysis results show that BPH infestation induces significant differences in the lipid profiles of Nipponbare and R6. The levels of hexadecanoic acid, methyl ester, linoleic acid, methyl ester, linolenic acid, methyl ester, glycidyl palmitate, eicosanoic acid, methyl ester, docosanoic acid, methyl ester, beta-monolinolein, campesterol, beta-sitosterol, cycloartenol, phytol and phytyl acetate had undergone enormous changes after BPH feeding. These results illustrate that BPH feeding enhances sterol biosynthetic pathway in Nipponbare plants, and strengthens wax biosynthesis and phytol metabolism in R6 plants. The results of quantitative real-time PCR of 5 relevant genes were consistent with the changes in metabolic level. Forty-five lipids were identified in the leaf blade extracts. BPH infestation induces distinct changes in the lipid profiles of the leaf blade samples of Nipponbare and R6. Although the lipid changes in Nipponbare are more drastic, the changes within the two varieties are similar. Lipid profiles in leaf sheath brought out significant differences than in leaf blade within Nipponbare and R6. We propose that Bph6 mainly affects the levels of lipids in leaf sheath, and mediates resistance by deploying metabolic re-programming during BPH feeding.

Conclusion

The results indicate that wax biosynthesis, sterol biosynthetic pathway and phytol metabolism play vital roles in rice response to BPH infestation. This finding demonstrated that the combination of lipidomics and quantitative real-time PCR is an effective approach to elucidating the interactions between brown planthopper and rice mediated by resistance genes.

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Acknowledgements

This work was supported by grants from the National Program on Research and Development of Transgenic Plants (2016ZX08009-003-001), and the National Key Research and Development Program (2016YFD0100600 and 2016YFD0100900).

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  1. State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, 430072, China

    Jiajiao Zhang, Yi Li, Jianping Guo, Bo Du, Guangcun He, Rongzhi Chen & Jiaru Li

  2. State Key Laboratory of Phytochemistry and Plant Resources in West China, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, China

    Yingjun Zhang

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JRL, RZC and YJZ conceived and designed the study. JJZ, YL, JPG and BD performed the experiments and analyzed experimental data. JJZ wrote the paper. GCH reviewed and edited the manuscript.

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Zhang, J., Li, Y., Guo, J. et al. Lipid profiles reveal different responses to brown planthopper infestation for pest susceptible and resistant rice plants. Metabolomics 14, 120 (2018). https://doi.org/10.1007/s11306-018-1422-0

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