Volatile DMNT directly protects plants against Plutella xylostella by disrupting the peritrophic matrix barrier in insect midgut.

Chen Chen,Chen He,Hongyi Chen,Qingfeng Tang,Chuanhong Wang,Zhen Tao,Taoshan Jiang,Shijie Huang,Peijin Li

doi:10.7554/elife.63938

Abstract

Insect pests negatively affect crop quality and yield; identifying new methods to protect crops against insects therefore has important agricultural applications. Our analysis of transgenic Arabidopsis thaliana plants showed that overexpression of pentacyclic triterpene synthase 1, encoding the key biosynthetic enzyme for the natural plant product (3E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), led to a significant resistance against a major insect pest, Plutella xylostella. DMNT treatment severely damaged the peritrophic matrix (PM), a physical barrier isolating food and pathogens from the midgut wall cells. DMNT repressed the expression of PxMucin in midgut cells, and knocking down PxMucin resulted in PM rupture and P. xylostella death. A 16S RNA survey revealed that DMNT significantly disrupted midgut microbiota populations and that midgut microbes were essential for DMNT-induced killing. Therefore, we propose that the midgut microbiota assists DMNT in killing P. xylostella. These findings may provide a novel approach for plant protection against P. xylostella.

Highlights

Insect pests are one of the major factors affecting plant development and seed production, and cause tremendous global economic losses
While characterizing the function of pentacyclic triterpene synthase 1 (PEN1), an important enzyme catalyzing the production of the volatile metabolite DMNT in Arabidopsis thaliana, we demonstrate that PEN1 and its derived product DMNT play significant roles in pest control
PEN1 has been reported to be a key enzyme in the biosynthesis of the volatile homoterpene DMNT (Sohrabi et al, 2015), which was confirmed by our gas chromatography-mass spectrometry (GC-Murashige and Skoog (MS)) analysis on 35Spro:PEN1 transgenic plants

Summary

Introduction

Insect pests are one of the major factors affecting plant development and seed production, and cause tremendous global economic losses. As part of their defenses, plants can kill or repel insects indirectly; for example, attacked plants emit volatile pheromones that attract insect predators to come and kill the initial pests (Pichersky et al, 2006; Unsicker et al, 2009; Gols, 2014; Liu et al, 2018) This strategy has been successfully adopted for plant protection in the field (Turlings and Ton, 2006; Clavijo McCormick et al, 2012; Li et al, 2018). Pest management by genetic manipulation of volatiles in the plant is not always successful in the field due to its complex context-dependency (Bruce et al, 2015) In another line of defense, plants communicate danger signals to other plants

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Conclusion