Pymetrozine inhibits reproductive behavior of brown planthopper Nilaparvata lugens and fruit fly Drosophila melanogaster

https://doi.org/10.1016/j.pestbp.2020.02.014Get rights and content

Highlights

  • We systematically described the mating process of brown planthopper including 8 steps and explored the optimal mating time.

  • Pymetrozine can both affect the mating behavior and female fecundity of brown planthopper and fruit fly.

  • Nan is essential for reproductive behavior in Drosophila.

  • NlNan protein was functionally conserved in regulating mating behavior and female fertility in Drosophila.

Abstract

Pymetrozine is a promising chemical used to control brown planthopper, which developed resistance to imidacloprid and buprofezin in the past decade. Field efficacy indicates that pymetrozine can reduce the number of offsprings of brown planthopper, but the specific physiological mechanism is unknown. In this study, we systematically described the mating process of brown planthopper including 8 steps (abdominal vibration, following, positioning, wing extension, attempted copulation, copulation, terminated copulation and leaving) and explored the optimal mating time after adult eclosion (3–5 days) and observation time (30 mins). Also, behavioral data showed that pymetrozine can affect the mating behavior and female fecundity of brown planthopper and fruit fly. As one of the target genes for pymetrozine, Nanchung (Nan), the nan36a mutant male courtship index, female receptivity and the number of offsprings were significantly decreased. Behavioral defects in nan36a mutant flies can be rescued by expressed NlNan. Our results indicated that Nan plays essential roles in the mating behavior and female fecundity. These findings provide useful information for demonstrating that pymetrozine effectively reduce the reproduction of brown planthopper and contribute to our understanding of reproductive strategies controlled by pymetrozine in insects.

Introduction

The brown planthopper (BPH), Nilaparvata lugens (Stål) (Hemiptera: Delphacidae), is the most important rice pest in China, and it has a long-range migration habit (Cuong et al., 1997; Garrood et al., 2016; Wu et al., 2019). It can cause serious damage by both directly sucking the phloem-sap, leading to nutrient depletion of nutrients within the plant, and transmitting virus diseases to host plants (Cuong et al., 1997; Murakami et al., 2013). Since the late 1960s, changes in rice varieties and cultivated systems have led to the rapid development of brown planthoppers, making it the main pest on rice in China (Cheng, 2009). It is estimated that annual losses to rice production caused by BPH is more than $300 million in Asia (Min et al., 2014). Brown planthopper is a typical migratory insect with sudden onset, and chemical insecticides remain the emergency method of controlling it. At present, there are 9 insecticides suitable for the control of rice brown planthopper in China, including pymetrozine, nitenpyram, dinotefuran, chlorpyrifos, isoprocarb, clothianidin, sulfoxaflor, triflumezopyrim and cycloxaprid (He et al., 2019; Wu et al., 2018). However, over-reliance on chemical pesticides in rice production, and the large-scale use of the same insecticide multiple times in a single season of rice is more common, resulting in the resistance of brown planthoppers to many major insecticides (Zhang et al., 2014). Since 2008, pymetrozine has been recommended as the main insecticide for controlling BPH in China (Wu et al., 2018).

Pymetrozine is a highly active insecticide for sucking pests, including aphids, whiteflies and planthoppers (Fuog et al., 1998). As a representative of pyridine azomethine insecticides, it inhibited insects from feeding in a unique way. Pymetrozine-treated aphids eventually died due to starvation (Harrewijn and Kayser, 1997). In fact, this finding demonstrated that pymetrozine is not generally toxic to aphids, but immediately withdraw the aphids stylet from the plant vascular system to stop feeding. Although locusts are not insects that feeding plant sap, pymetrozine could also interfere with its feeding behavior. In addition, the hindlegs of locusts injected with pymetrozine did not stretch normally. Comparably to pymetrozine, 5-hydroxytryptamine (5-HT) applied to the ganglion increased the spontaneous spiking activity (Kaufmann et al., 2004). However, further investigation showed that pymetrozine could selectively affect the femoral chordotonal organ responsible for femur–tibia joint control (Ausborn et al., 2005). The normal anti-gravitaxis behavior of Drosophila melanogaster could be destroyed by pymetrozine, and the transient receptor potential vanilloid (TRPV) mutant fruit flies (nan36a and iav1) that kept on pymetrozine or dimethyl sulfoxide (DMSO) both displayed gravitaxis defects. Analysis of physiological functions of pymetrozine on Drosophila confirmed that the target of pymetrozine are the TRPV channels (Nesterov et al., 2015). Subsequent experiments indicated that pymetrozine can activate the TRPV channels of the pea aphid (Kandasamy et al., 2017) and brown planthopper (Wang et al., 2019).

It is unreasonable to judge the susceptibility of pymetrozine by calculating the mortality (LC50 or LD50) in N. lugens resistance monitoring because there is no apparent lethal effect after pymetrozine treatment (Tsujimoto et al., 2016). Therefore, the Insecticide Resistance Action Committee (IRAC) sued a standard method (no.005) of measuring the number of offsprings. An improved method for monitoring the susceptibility of the brown planthopper to pymetrozine is also to assess the number of offspring (Tsujimoto et al., 2016). But how pymetrozine decreased the number of offsprings is still unknown. Mating behavior is the most fundamental and important process to produce offspring, often biotic and abiotic conditions such as wind, temperature, rainfall, daylight, insect age, and predator population plays a critical role that results in the development of specialized niche conditions (Ahmed et al., 2016; Long et al., 2012). There are also many reports on the effects of insecticides on female fertility (Ge et al., 2011, 2010; Li et al., 2015; Xu et al., 2019).

Understanding the effects of pymetrozine on the reproductive behavior of brown planthopper is essential for management of this pest and could better explain the reasonability of the bioassay method recommend by IRAC. In this study, we systematically described the mating process of brown planthopper and explored the optimal mating time and observation time. Furthermore, mating behavior and female fertility analysis confirmed that pymetrozine affects reproductive behavior of N. lugens and D. melanogaster. Our results reinforce strongly evidence on the function of nan in the mating behavior.

Section snippets

Insects and reagents

The BPH used in this study were obtained from a laboratory population. The insects were maintained indoors on fresh rice seedlings (Taichung Native 1, TN1) under standard conditions of 27 ± 1 °C and 70% ± 10% relative humidity with a 16 h:8 h (Light: Dark) photoperiod.

Canton S were used as a wild-type flies. Nan-GAL4 (BDSC: 24903) and nan36a mutants (BDSC: 24902) were obtained from the Bloomington Drosophila Stock Center. UAS-NlNan was constructed fruit fly we reported before (Wang et al., 2019

Pymetrozine reduces the number of offsprings of brown planthopper

To show that pymetrozine can reduce the number of progenies of brown planthopper, we used a slightly modified no.5 method to study the effect of pymetrozine on brown planthopper. The results adopted the rice seedling dipping test method combined with counting the number of offsprings showed an obvious dose-response in the suppression ratio of N. lugens (Table 1). The EC50 value in this experiment was 3.055 mg/L. From this result, we confirmed that pymetrozine can significantly affect the number

Discussion

In this paper, we systematically described the mating process of brown planthopper, using clear pictures, including 8 steps (abdominal vibration, following, positioning, wing extension, attempted copulation, copulation, terminated copulation and leaving) (Fig. 1A). Virgin female brown planthoppers attract males through abdominal vibration before successful mating (Ichikawa and Ishii, 1974). Male planthoppers will produce courtship signals within five minutes, regardless of the presence or

Acknowledgements

This research was supported by the National Natural Science Foundation of China (No. 31672068, 31830075 & 31471804) and the Postgraduate Research & Practice Innovation Program of Jiangsu Province (KYCX18_0671).

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    These authors contributed equally to this work.

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