Resistant inheritance and cross-resistance of cyflumetofen in Tetranychus cinnabarinus (Boisduval)
Graphical abstract
Introduction
Tetranychus cinnabarinus (carmine spider mite) is one of the most important agriculture mite pests in China, which feed on >100 kinds of crops, such as beans, eggplant, pepper, tomato and so on [1,2]. This mite shares many characteristics in morphological, biological, and molecular aspects with T. urticae, and is also considered as red form of two spotted spider mite [3]. However its unique characters make some researchers classify it into a different but very close species with T. urticae [4,5]. Currently, its control has been based on the use of insecticides and acaricides [6]. However, because of the frequent application of acaricides and insecticides, and strong reproductive ability, short generation cycle, arrhenotokous parthenogenesis, highly close relative mating rate of T. cinnabarinus, the mites could develop resistance quickly [1,7].
As a novel benzoyl acetonitrile acaricide, cyflumetofen was developed by Otsuka AgriTechno Co., Ltd., and widely used in many countries since 2007 [8]. Cyflumetofen works as the inhibitor of complex II in the mitochondrial electron transport chain [8,9]. It shows striking activity on kinds of pest mites, such as Tetranychus urticae (two-spotted spider mite), Tetranychus kanzawai (Kanzawa spider mite) and Panonychus citri (citrus red mite), during the whole life span from egg to adult. Besides, cyflumetofen is also effective to a series of mite strains which have developed resistance to other acaricides [9]. Another advantage of this acaricide is its security to mammals, aquatic organisms, beneficial organisms, natural enemies and other non-target organisms. With none occurrence of phytotoxicity to plants, cyflumetofen can be rapidly metabolized in the soil and water [[10], [11], [12]]. At present, many studies focus on chemical synthesis and environmental degradation of cyflumetofen [[13], [14], [15], [16]]. Attentions are also paid to its resistant mechanism in mites, such as overexpression of a GST gene TuGSTd05 enhanced the ability of detoxification against cyflumetofen in T. urticae [17]. However, the resistant inheritance of cyflumetofen in mites has not been fully elucidated. Understanding of the resistant inheritance of insecticide/acaricide is necessary for the sustainability of pest control [18,19]. The inheritance modes of fenpyroximate, pyridaben and abamectin resistance in T. urticae revealed different genetics responses [20,21]. Insecticide/acaricide resistance in natural populations may be monogenic or multiple genes with a major phenotypic effect. Therefore, study on inheritance of mites involved in insecticide/acaricide resistance will aid in our understanding on the development of resistance.
In this study, we demonstrated the same inheritance pattern of cyflumetofen-resistance in both two resistance-selecting strains, as well as its cross-resistance with other five acaricides in T. cinnabarinus. The current study can provide important information for further understanding of cyflumetofen-resistance development in T. cinnabarinus and the reasonable usage of this acaricide.
Section snippets
Susceptible strain (SS)
Carmine spider mite was collected in the field of Beibei District, Chongqing, China, and feed on fresh cowpea seedlings in the indoor illumination constant temperature incubator for >15 years without any pesticide exposure. This population was considered as the relatively susceptible strain (SS) and used for the selection of cyflumetofen resistance. The rearing conditions were as follows: 26 ± 1 °C temperature, 35%–55% relative humidity (RH), and a photoperiod of 14:10 h (L:D).
Cyflumetofen-resistant strain (CyR and YN-CyR)
The
Resistance selection and bioassay of cyflumetofen
The LC50 of cyflumetofen against SS and CyR was 2.19 mg/L and 229.31 mg/L, separately, from which the relative resistance-ratio of CyR was calculated as 104.7-fold. When compared with another susceptible strain (CyS) [22], the relative resistance-ratio of CyR could be higher as 290.3-fold. Besides, the toxicity of cyflumetofen against YN-CyR was from 8.39 to 56.09 mg/L after 12 generations' slection with cyflumetofen, from which the relative resistance ratio was 25.6- and 71.0-fold when
Discussion
Cyflumetofen is a novel acaricide which noted for very high efficiency to spider mites and safe for the environment, so it could be a main acaricide in future. After 104 generations' selection with increasing concentrations of cyflumetofen under laboratory condition, the resistance ratio reached to 104.7-fold (CyR_104/SS). A more cyflumetofen-susceptible strain (CyS) had also been selected from susceptible strain (SS) in our previous study [22], and the resistance for CyR_104 should be as high
Acknowledgments
This research is partially funded by Chongqing Research Program of Basic Research and Frontier Technology (No. cstc2017jcyjBX0061) and the National Natural Sciences Foundation of China (31672085).
References (43)
- et al.
Acaricide resistance mechanisms in the two-spotted spider mite Tetranychus urticae and other important Acari: a review
Insect Biochem. Mol. Biol.
(2010) - et al.
A glutathione-S-transferase (TuGSTd05) associated with acaricide resistance in Tetranychus urticae directly metabolizes the complex II inhibitor cyflumetofen
Insect Biochem. Mol. Biol.
(2017) - et al.
Resistance in field populations of Tetranychus urticae to acaricides and characterization of the inheritance of abamectin resistance
Crop Prot.
(2015) - et al.
Resistance selection and biochemical mechanism of resistance against cyflumetofen in Tetranychus cinnabarinus (Boisduval)
Pestic. Biochem. Physiol.
(2014) - et al.
Complete maternal inheritance of bifenazate resistance in Tetranychus urticae Koch (Acari: Tetranychidae) and its implications in mode of action considerations
Insect Biochem. Mol. Biol.
(2006) - et al.
Genetic analysis of abamectin resistance in Tetranychus cinnabarinus
Pestic. Biochem. Physiol.
(2009) - et al.
Fenazaquin acaricide specific binding sites in NADH: ubiquinone oxidoreductase and apparently the ATP synthase stalk
Pestic. Biochem. Physiol.
(1996) - et al.
Spider mite (Acari: Tetranychidae) on various crops in Taiwan
J. Agric. Res. China.
(1997) - et al.
Some observations on the biology and behaviour of carmine spider mite Tetranychus cinnabarinus(Boisduval) (Acarina: Terranychidae): a pest of brinjal vegetable
J. Adv. Zool.
(1999) - et al.
Evidence for synonymy between Tetranychus urticae and Tetranychus cinnabarinus (Acari, Prostigmata, Tetranychidae): review and new data
Acarologia
(2013)
Population genetic structure of Tetranychus urticae and its sibling species Tetranychus cinnabarinus (Acari: Tetranychidae) in China as inferred from microsatellite data
Ann. Entomol. Soc. Am.
Studies on the differentiation of two sibling species, Tetranychus cinnabarinus (Boisduval) and T. urticae Koch
Acta Entomol. Sin.
Incidence and inheritance of resistance to METIFacaricides in European strains of the two-spotted spider mite (Tetranychus urticae) (Acari: Tetranychidae)
Pest Manag. Sci.
Development of a new acaricide, cyflumetofen
J. Pestic. Sci.
Cyflumetofen, a novel acaricide–its mode of action and selectivity
Pest Manag. Sci.
Comparative toxicity of acaricides to Tetranychus merganser Boudreaux and Tetranychus kanzawai Kishida (Acari: Tetranychidae)
Int. J. Acarol.
Synthesis and acaricidal activities of Cyflumetofen
Agrochemicals
Cross-resistance risk of the novel complex II inhibitors cyenopyrafen and cyflumetofen in resistant strains of the two-spotted spider mite Tetranychus urticae
Pest Manag. Sci.
Synthesis of acaricide cyflumetofen
Modern Agrochem.
Chiral determination of a novel acaricide cyflumetofen enantiomers in cucumber, tomato, and apple by HPLC
J. Sep. Sci.
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