Combined transcriptome and metabolome analyses to understand the dynamic responses of rice plants to attack by the rice stem borer Chilo suppressalis (Lepidoptera: Crambidae).

Qingsong Liu,Yunhe Li,Vered Tzin,Yufa Peng,Jörg Romeis,Xingyun Wang

doi:10.1186/s12870-016-0946-6

Abstract

BackgroundRice (Oryza sativa L.), which is a staple food for more than half of the world’s population, is frequently attacked by herbivorous insects, including the rice stem borer, Chilo suppressalis. C. suppressalis substantially reduces rice yields in temperate regions of Asia, but little is known about how rice plants defend themselves against this herbivore at molecular and biochemical level.ResultsIn the current study, we combined next-generation RNA sequencing and metabolomics techniques to investigate the changes in gene expression and in metabolic processes in rice plants that had been continuously fed by C. suppressalis larvae for different durations (0, 24, 48, 72, and 96 h). Furthermore, the data were validated using quantitative real-time PCR. There were 4,729 genes and 151 metabolites differently regulated when rice plants were damaged by C. suppressalis larvae. Further analyses showed that defense-related phytohormones, transcript factors, shikimate-mediated and terpenoid-related secondary metabolism were activated, whereas the growth-related counterparts were suppressed by C. suppressalis feeding. The activated defense was fueled by catabolism of energy storage compounds such as monosaccharides, which meanwhile resulted in the increased levels of metabolites that were involved in rice plant defense response. Comparable analyses showed a correspondence between transcript patterns and metabolite profiles.ConclusionThe current findings greatly enhance our understanding of the mechanisms of induced defense response in rice plants against C. suppressalis infestation at molecular and biochemical levels, and will provide clues for development of insect-resistant rice varieties.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-016-0946-6) contains supplementary material, which is available to authorized users.

Highlights

Rice (Oryza sativa L.), which is a staple food for more than half of the world’s population, is frequently attacked by herbivorous insects, including the rice stem borer, Chilo suppressalis
Much lower number of Differentially expressed genes (DEG) detected between the time points of 24 h vs. 48 h, 24 h vs. 72 h, or 48 h vs. 72 h and there was no commonality of the DEGs occurred between two of three time points (Fig. 1a, c)
Most DEGs involved in Effects of Chilo Suppressalis feeding on amino acids, organic acids, and nitrogen metabolism Our analyses showed that genes encoding enzymes such as glutamate decarboxylase (GAD), N-carbamoylputrescine amidase (CPA), ornithine decarboxylase (ODC), and Laspartate oxidase (LASPO) were up-regulated; while those encoding adenylosuccinate lyase (ASL), and delta-1-pyrroline-5-carboxylate synthetase (P5CS) were down-regulated over time

Summary

Introduction

Rice (Oryza sativa L.), which is a staple food for more than half of the world’s population, is frequently attacked by herbivorous insects, including the rice stem borer, Chilo suppressalis. Previous results have suggested that plant response to herbivore feeding is a dynamic process, and that the transcript patterns, protein and metabolite profiles are temporally and spatially regulated [1, 10, 12]. This suggests that it is essential to investigate the dynamic at transcriptional, proteomic and metabolic changes associated to insect feeding [6, 7, 9, 11]. The integration of transcriptomic, proteomic, and metabolic approaches can gain a better understanding of plant responses to herbivore feeding [10]

Methods

Results

Discussion

Conclusion