Roles of LsCYP4DE1 in wheat adaptation and ethiprole tolerance in Laodelphax striatellus

Highlights

• Only a few P450 genes participated in host adaption in SBPH.

• LsCYP4DE1 was up-regulated in wSBPH and can be induced by wheat plant.

• LsCYP4DE1 was important for SBPHs rearing on wheat plant.

Abstract

The cytochrome P450 monooxygenase (P450) gene family has an important role in detoxifying host plant allelochemicals and pesticides. In this study, we screened differentially expressed genes of the small brown planthopper (Laodelphax striatellus, SBPHs) that were reared for more than ten generations on rice and wheat plants, and found that only a few P450s were associated with host adaptation. LsCYP4DE1, whose expression was 9.5-fold higher in the wheat-adapted SBPH (wSBPH) than in the rice-adapted SBPH (rSBPH), appeared to have an important role in the colonization of wheat plants. Knocking down the expression of LsCYP4DE1 led to increased mortality, as well as decreased performance of SBPHs reared on wheat. However, no significant difference was found in dsLsCYP4DE1-treated SBPHs on rice plants. In addition, LsCYP4DE1 was potentially associated with pesticide tolerance, and suppression of its expression led to increased sensitivity to the pesticide ethiprole. Our results revealed potential roles of LsCYP4DE1 in wheat adaptation and ethiprole tolerance, and provide useful information for pest management.

Introduction

Through millions of years of evolution, insects have developed sophisticated defense systems to detoxify or tolerate various toxic compounds from plants or other sources (Feyereisen, 2005; Li et al., 2007; Tao et al., 2012). The cytochrome monooxygenase P450s (P450s), which represent the largest and most diverse superfamily of multifunctional enzymes, play important roles in the metabolism of endogenous and exogenous compounds (Li et al., 2007). Recently, with the development of genomic sequencing, P450 enzymes have been identified in numerous insect species. Although insect P450 can be divided into four major clades (three microsomal cytochrome P450 clades (CYP2–CYP4) and one mitochondrial cytochrome P450 clade), their total number in each species varied, which ranged from 34 in Ceratosolen solmsi (Xiao et al., 2013) to 170 in Culex quinquefasciatus (Arensburger et al., 2010). The detoxification-related P450s that participated in plant toxins or synthetic pesticides metabolism have been well documented (reviewed in Cui et al., 2016; Feyereisen, 2012), and the current studies indicated that CYP3 and CYP4 clades showed large variation and the majority of detoxification-related P450 genes belonged to these two clades (Feyereisen, 2012).

Insecticide adaptation is a specific form of insect adapting to toxic compounds. The targets, transporters, and enzymes that involved in the adaptation of insects to host plant and pesticides are basically the same (Dermauw et al., 2018). In many cases, plant allelochemicals influence pesticide tolerance in insects, but the underlying mechanisms are not fully understood. In Tetranychus urticae, the transcriptional profiles of tomato-adapted mites resemble those of multipesticide-resistant strains, and adaptation to tomato decreased the susceptibility to unrelated pesticide classes (Dermauw et al., 2013). In Helicoverpa insects, P450s induced by allelochemicals from their major host plants contributed to increased tolerance to other toxic chemicals (Tao et al., 2012). In Myzus persicae, overexpression of CYP6CY3 allows tobacco-adapted aphids to efficiently detoxify nicotine and adapt to neonicotinoid insecticides (Bass et al., 2013). Despite the attractiveness of pre-adaptation hypothesis (Alyokhin and Chen, 2017; Gordon, 1961), Dermauw et al. (2018) proposed that the host range of herbivores is neither necessary nor sufficient to drive the dynamics of pesticide resistance. In the wild, insects encounter a variety of xenobiotics from host plants and synthetic pesticides. Genetic, biological/ecological, and operational factors might cooperatively influence insect adaptations to such xenobiotics (Georghiou and Taylor, 1986), although the underlying mechanisms remain unclear.

The small brown planthopper (Laodelphax striatellus, SBPH) is a destructive pest that is distributed from the Philippines to Siberia and Europe. As oligophagous plant-feeders, SBPHs attack a variety of crops, including rice, wheat, and maize, causing serious damage by feeding and transmitting viruses (Otuka et al., 2010). In East Asia, a wheat–rice rotation system provides ideal food resources for SBPHs, which transfer to different host plants every year. The host plants are the most important factors that affect insect life cycles, and SBPHs are better sustained on rice than wheat plants (Li et al., 2009). Differences in host plant fitness might be closely associated with the detoxification system, which helps insects overcome the hurdle of plant toxins in their diets (Schoonhoven et al., 2005). SBPHs have developed resistance to various insecticides (Gao et al., 2008). Studies of planthopper responses to xenobiotics mainly focused on the pesticides, and several detoxification-related genes have been identified, such as CYP6CW1, LsCYP4DE1, and CYP353D1v2 (Elzaki et al., 2015, 2016; Zhang et al., 2012). However, the influence of host transference on SBPH detoxification systems remain largely unknown. It was interesting to unveil the relationship between host adaptation and pesticide tolerance in this important agriculture pest.

In this study, we profiled the global gene expression change of a wheat-adapted SBPH (wSBPH) and rice-adapted SBPH (rSBPH) by Illumina sequencing. Two P450 genes were identified. LsCYP4DE1, whose expression was significantly influenced by the host plant, was associated with wheat adaptation. LsCYP4DE1 knockdown resulted in decreased performance of wheat-reared SBPHs and increased sensitivity to the pesticide ethiprole. Our results provide evidence that P450 genes might contribute to wheat adaptation and ethiprole tolerance in L. striatellus.