Abstract

BackgroundThe cereal weevil, Sitophilus zeamais is one of the most destructive pests of stored cereals worldwide. Frequent use of fumigants for managing stored-product insects has led to the development of resistance in insects. Essential oils from aromatic plants including the tea oil plant, Melaleuca alternifolia may provide environmentally friendly alternatives to currently used pest control agents. However, little is known about molecular events involved in stored-product insects in response to plant essential oil fumigation.ResultsM. alternifolia essential oil was shown to possess the fumigant toxicity against S. zeamais. The constituent, terpinen-4-ol was the most effective compound for fumigant toxicity. M. alternifolia essential oil significantly inhibited the activity of three enzymes in S. zeamais, including two detoxifying enzymes, glutathione S-transferase (GST), and carboxylesterase (CarE), as well as a nerve conduction enzyme, acetylcholinesterase (AChE). Comparative transcriptome analysis of S. zeamais through RNA-Seq identified a total of 3,562 differentially expressed genes (DEGs), of which 2,836 and 726 were up-regulated and down-regulated in response to M. alternifolia essential oil fumigation, respectively. Based on gene ontology (GO) analysis, the majority of DEGs were involved in insecticide detoxification and mitochondrial function. Furthermore, an abundance of DEGs mapped into the metabolism pathway in the Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway database were associated with respiration and metabolism of xenobiotics, including cytochrome P450s, CarEs, GSTs, and ATP-binding cassette transporters (ABC transporters). Some DEGs mapped into the proteasome and phagosome pathway were found to be significantly enriched. These results led us to propose a model of insecticide action that M. alternifolia essential oil likely directly affects the hydrogen carrier to block the electron flow and interfere energy synthesis in mitochondrial respiratory chain.ConclusionThis is the first study to perform a comparative transcriptome analysis of S. zeamais in response to M. alternifolia essential oil fumigation. Our results provide new insights into the insecticidal mechanism of M. alternifolia essential oil fumigation against S. zeamais and eventually contribute to the management of this important agricultural pest.

Highlights

  • As one of the most destructive pests in stored cereals in the world, the cereal weevil, Sitophilus zeamais causes extensive quantitative loss in stored grains, and alters the quality of grains and grain products, resulting in seed viability deterioration [1, 2]

  • M. alternifolia essential oil significantly inhibited the activity of three enzymes in S. zeamais, including two detoxifying enzymes, glutathione S-transferase (GST), and carboxylesterase (CarE), as well as a nerve conduction enzyme, acetylcholinesterase (AChE)

  • An abundance of differentially expressed genes (DEGs) mapped into the metabolism pathway in the Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway database were associated with respiration and metabolism of xenobiotics, including cytochrome P450s, CarEs, GSTs, and ATP-binding cassette transporters (ABC transporters)

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Summary

Introduction

As one of the most destructive pests in stored cereals in the world, the cereal weevil, Sitophilus zeamais causes extensive quantitative loss in stored grains, and alters the quality of grains and grain products, resulting in seed viability deterioration [1, 2]. Frequent and widespread use of chemical fumigants has led to the development of resistance in stored-product insects [5]. It is critical to search for novel fumigants for combating stored-product insects Another prominent alternative for chemical fumigants is plant natural products, such as plant essential oils. Plant natural products are known for their properties of low residue formation, high selectivity, and difficulty to generate cross-resistance, etc [8]. It is mainly because of their complex constituents and novel modes of action against insects [9]. Frequent use of fumigants for managing stored-product insects has led to the development of resistance in insects. Little is known about molecular events involved in stored-product insects in response to plant essential oil fumigation.

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