Genetic analysis of abamectin resistance in Tetranychus cinnabarinus

Pesticide Biochemistry and Physiology 95 (2009) 147–151

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Genetic analysis of abamectin resistance in Tetranychus cinnabarinus Lin He a,b,*, Xiwu Gao b, Jinjun Wang a, Zhimo Zhao a, Nannan Liu c a

College of Plant Protection, Southwest University, Chongqing, China Department of Entomology, China Agricultural University, Beijing, China c Department of Entomology and Plant Pathology, Auburn University, Auburn, Alabama, USA b

a r t i c l e

i n f o

Article history: Received 7 January 2009 Accepted 11 August 2009 Available online 15 August 2009 Keywords: Tetranychus cinnabarinus Resistance Selection Abamectin Inheritance model

a b s t r a c t The carmine spider mite is the most serious crop mite pests in China. Abamectin has been used to control insects and mites worldwide but carmine spider mites, Tetranychus cinnabarinus, had developed resistance to it. Genetic research on insecticide resistance has been fundamental for understanding the resistance development, studying resistance mechanisms, and designing appropriate resistance management strategies to control insect pests. A resistant colony of T. cinnabarinus, RRG42, was established to examine the inheritance of abamectin resistance in T. cinnabarinus. The females of T. cinnabarinus were selected for bioassay using a slide dip method. After 42 generations of selection, the RRG42 strain was 8.7-fold resistant to abamectin compared with the susceptible strain (SS). The logarithm (log) concentration–probit response curve for F1s from reciprocal crosses, of F1RS and F1SR, were inclined to that for SS and the degree of dominance (D) values for F1s were 0.81 and 0.17. There was a significant difference in values of LC50 and slope of log concentration–probit lines between F1RS and F1SR. The observed mortalities of BC1 (F1RS$  RRG42#) and BC10 (F1SR$  SS#) were significantly different from the expected mortalities based on a monogenic resistance in the chi-square tests. The inheritance of abamectin resistance in T. cinnabarinus is incompletely recessive and may be controlled by more than one gene. The maternal or cytoplasmic effect may exist in the inheritance of resistance to abamectin in T. cinnabarinus. Ó 2009 Elsevier Inc. All rights reserved.

1. Introduction The carmine spider mite, Tetranychus cinnaberinus (Boisduval), is the most serious crop mite pests and widely distributed in China. It infests many crops, including cotton, tobacco, maize, eggplant, cowpea, and tomatoes. Their phytophagous and strong reproductive nature, short life cycle, limited activity areas, and high exposure rate to acaricides facilitate rapid development of resistance in spider mites to many acaricides [1–3]. The resistance of spider mites (Tetranychus spp.) to acaricides was firstly reported in New York, USA in 1949, with the failure of control cotton mites using parathion in cotton fields. In China, the first case of Tetranychus cinnabarinus resistance to parathion was reported in the beginning of 1960s [4]. Following that, resistance of T. cinnabarinus to different insecticides has been frequently reported. Wu [5] reported that a cotton field population of T. cinnabarinus in Henan province had developed 466.8- and 20.2-fold resistance to parathion and monocrotophos, respectively. Zhan [6] reported that T. cinnabarinus in

* Corresponding author. Address: College of Plant Protection, Southwest University, 216 Tiansheng Road, Beibei, Chongqing 400716, PR China. Fax: +86 23 68251514. E-mail address: [email protected] (L. He). 0048-3575/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.pestbp.2009.08.005

vegetable fields of Zigong city, Sichuan province, had developed resistance to dicofol, isocarbophos, propargite and omethoate with the resistance range from 3.7- to 39.8-fold. Laboratory selections with acaricides, such as omethoate, dicofol, amitraz, pridaben, fenpropathrin and abamectin, on T. cinnabarinus to predict resistance development were also reported [7–9]. Abamectin, macrocyclic lactones isolated from Streptomyces avermitilis [10], acts as agonists of GABA receptors on neuromuscular cells, causing ataxia and paralysis, which is different from the mechanism of action of conventional organophosphate, organochlorine and pyrethroid insecticides. Because of its special mode of action and its environmental friendly nature [11], abamectin has been used to control insects and mites worldwide. Unfortunately, following the application of abamectin, resistance has developed in different insect species, including house flies [12], colorado potato beetles [13], diamondback moths [14], two-spotted spider mites [15–17] and carmine spider mites [8]. Genetic research on insecticide resistance has been fundamental for understanding the resistance development, studying resistance mechanisms, and designing appropriate resistance management strategies to control insect pests [19,20]. In the present study, we examined the genetic inheritance of abamectin resistance in T. cinnabarinus to gain a better understanding of abamectin resistance development in T. cinnabarinus.

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2. Materials and methods 2.1. T. cinnabarinus The SS strain, a reference (relative susceptible) colony of T. cinnabarinus, more than 1500 original mites collected from the cowpea field of Beibei, Chongqing, China, in 1998. This strain has not been exposed to any insecticides since collection. The RRG42 strain, the resistant strain generated from selection with abamectin on the SS strain for 42 generations. T. cinnabarinus was reared with fresh cowpea leaf at 26 ± 1 °C with 55–70% relative humidity under a photoperiod of 14:10 (L:D) h in green house. 2.2. Abamectin selection The 1.8% abamectin EC (trade name: kill insect and mite) was purchased from Xin Bawang chemical Ltd. company (Henan, China). More than 2500 adult mites separated from the T. cinnabarinus SS strain were selected with abamectin using a Changjiang-08 sprayer (Yu Yao plastic product Ltd. company, Zhejiang, China) as described by He et al. [8]. The concentration of abamectin used for each generation selection was sufficient to kill 70% of treated individuals after 24 h. The alive mites were transferred to new leaves of cowpea till laying eggs (1–2 d). The adult mites were then discarded from leaves. The selection on T. cinnabarinus SS was conducted for 42 generations in the laboratory, generating the RRG42 strain. The dipping-slide bioassay was conducted for some generations (Table 1) after selection as described by He et al. [8] and the toxicity of abamectin was analyzed by standard probit analysis [21] using Abbott’s correction for control mortality [22]. 2.3. Genetic crosses To conduct genetic linkage study, we conducted reciprocal crosses between resistant RRG42, and susceptible SS strains of T. cinnabarinu. The virgin female mites used in the crosses were isolated every 8 h before developing into quiescence anaphase. Two F1 reciprocal cross lines, F1RS (RRG42 $  SS #) and F1SR (SS $  RRG42 #), were generated. Backcrosses of the reciprocal progenies of F1RS and F1SR to the parental strains were conducted and two lines of BC1 (F1RS$  RRG42#) and BC10 (F1SR$  SS#) were produced. Because male mites are haploid and inherit their genes only from the maternal side, the BC1 female progeny obtained from the backcrosses is genetically equivalent to the F2 female progeny [23,24]. 2.4. Bioassay and data analyses The bioassay was conducted as described by He et al. [8]. Briefly, each treatment consisted of 30 female mites on slides, dip-

ping in water with an appropriate concentration of abamectin and five to seven concentrations that give >0 and <100% mortality in each experiment. After 24 h treatment, the mortality was examined under dissecting microscope. Each experiment was repeated three times. To estimate the number of genes involving in the resistance, abamectin concentration range was increased to ten for the treatment on back-cross (BC1) progeny. Bioassay data were pooled and probit analysis was conducted [21]. Statistical analysis of LC50s was based on nonoverlap of 95% confidence intervals. The degree of dominance (D) levels of the resistance in the F1s were calculated according to Stone [24] and Liu and Scott [25] using the logarithm of the LC50 values. The degree of dominance values ranged from 1 to +1; D = 1 indicates the completely recessive; 1 < D < 0 indicates incompletely recessive; 0 < D < 1 indicates incompletely dominant, and D = 1 indicates completely dominant. The number of genes that are possibly involved in the resistance of T. cinnabarinus to abamectin was estimated with the responses of back-cross progenies to abamectin. The null hypothesis of monogenic resistance was tested on the basis of chi-square goodness-of-fit between the observed and the theoretical expectation mortality [26–28]. If the observing concentration–response curve and the anticipant concentration–response curve of BC1s have no significant difference, null hypothesis was accepted and the resistance was suggested to be controlled by single factor, and vice versa [1]. The v2 analysis was also performed to compare the expected and observed v2 values for BC1s. Again, if the expected and observed v2 values show significant difference, the resistance was considered as polygenic heredity and vice versa. The v2-tests were performed using two calculation formulas providing by Keena [1] and Preisler [27]. The latter considered the variance factors of increasing v2 besides the variance of binary fluctuation.

3. Results and discussion 3.1. Abamectin resistance in T. cinnabarinus Results of the abamectin selection showed that the resistance in T. cinnabarinus to abamectin increased following the generations of selection. The resistance was increased to 8.7-folds after 42 generations selection, generating a strain of RRG42 (Table1). A previous study of abamectin selection on Panonychus citri (citrus red mite) showed a 7.3-fold resistance development to abamectin only after 12 generations selection [16]. Whereas, our study showed that the resistance to abamectin in T. cinnabarinus reached to a 7.2-fold after 30 generation selection (Table 1), although T. cinnabarinus had the similar susceptibility to abamectin as P. citri before selection. Comparison with the resistance development in P. citri suggests that T. cinnabarinus had a slow rate in resistance development. LC95 and LC99s of abamectin for T. cinnabarinus after

Table 1 Abamectin selection on Tetranychus cinnabarinus.

a b

Number of generation selecteda

Slope (±SE)

v2

LC50 (95% CL) (mg l1)

LC95 (95% CL) (mg l1)

LC99 (95% CL) (mg l1)

RRb

SS (RRG0) RRG4 RRG10 RRG18 RRG22 RRG26 RRG30 RRG34 RRG42

3.3 3.1 3.6 5.2 3.4 3.5 3.2 2.0 3.1

3.01 2.73 0.66 2.99 0.85 1.25 1.34 0.16 1.34

0.017 0.012 0.023 0.055 0.063 0.099 0.122 0.132 0.147

0.054 0.041 0.067 0.115 0.191 0.296 0.398 0.910 0.508

0.088 0.068 0.104 0.155 0.302 0.466 0.648 2.028 0.848

1.0 0.7 1.4 3.2 3.7 5.8 7.2 7.8 8.7

(±0.3) (±0.3) (±0.4) (±0.5) (±0.3) (±0.3) (±0.3) (±0.2) (±0.2)

(0.010–0.024) (0.007–0.017) (0.014–0.032) (0.053–0.057) (0.060–0.066) (0.058–0.140) (0.116–0.128) (0.120–0.144) (0.140–0.154)

(0.044–0.064) (0.032–0.050) (0.055–0.079) (0.108–0.122) (0.181–0.201) (0.260–0.332) (0.385–0.411) (0.710–1.110) (0.494–0.522)

The bioassay was conducted with adult females under 26 ± 1 °C, 55–70% relative humidity, 14 h illumination, 10 h dark conditions. RR, resistance ratio; LC50 of RRG strain/LC50 of SS (RRG0) strain.

(0.074–0.102) (0.049–0.087) (0.084–0.124) (0.142–0.168) (0.284–0.320) (0.426–0.506) (0.627–0.669) (1.778–2.278) (0.826–0.870)

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than the LC50 (0.174 mg l1) observed after the selection for susceptibility [17]. Although the resistance to abamectin in the GGR42 strain of T. cinnabarinus is not high (about 9-fold), the mite showed positive response to the selection of abamectin, e.g. the activity of metabolizing enzymes in the RRG42 was significant higher than that in the SS [28] and the fitness of resistant mites also changed compared that with the susceptible mites [29], which indicated the GGR42 strain had developed real resistance to abamectin and could be used to carry out the genetic analysis.

8.0 SS

RRG42

F1RS

F1SR

Mortality (Probit)

7.0 6.0 5.0 4.0

3.2. Inheritance of the resistance to abamectin in T. cinnabarinus

3.0 2.0 0.015 0.023 0.025 0.028 0.036 0.072 0.113 0.150 0. 25 7 -1 Concentration (mg.L )

Fig. 1. Log concentration–probit lines of abamectin for SS (the parent susceptible strain), parent RRG42 (the abamectin selected resistant strain), and their reciprocal offspring of F1SR (SS$  RRG42#) and F1RS (RRG42$  SS#).

42-generation selection (0.508 and 0.848 mg l1 for LC95 and LC99, respectively) obtained in our study and for P. citri after 12 generation selection (0.692 and 1.670 mg l1 for LC95 and LC99, respectively) obtained by Meng [16] were much lower than the currently recommended concentration (10 mg l1) for the field control of mites in China. These studies suggest that the abamectin’s effect of controlling mites in field was greatly influenced by environmental factors or the field population of mites in China had developed moderate resistance to abamectin. Compared the initial levels of sensitivity to abamectin in T. cinnabarinus and P. citri in China, T. urticae (two-spotted spider mite) in Brazil showed much higher resistance level to abamectin in the field population [17]. A population of T. urticae collected from strawberry field in Atibaia county, state of São Paulo, Brazil, had LC50 of 4.36 mg l1. After 5-generation selections with abamectin, resistance to abamectin in T. urticae was increased 13 times compared with the initial level [17], indicating that this species had a potential for quick development of resistance to abamectin. Abamectin was first registered in China to control vegetable insect and mite in 1991 [18] and not applied in Beibei, from which the susceptible strain of T. cinnabarinus was collected, until 1998. In other words, the SS strain this study is based on had no abamectin exposure history and is really susceptible to abamectin. Compared with T. urticae, the very slow process of resistance development to abamectin in T. cinnabarinus during selection may be related to the initial involvement of the resistant gene(s), because the original population of T. urticae was already moderately resistant to abamectin, even before the selection process in the laboratory. The initial LC50 (4.36 mg l1) of abamectin to T. urticae was 25 times higher

We characterized the inheritance of resistance in mites by logarithm (log) concentration–response analyses (bioassays) of abamectin against SS—the susceptible strain, RRG42—the resistant strain, and F1SR (SS$  RR#) and F1RS (RR$  SS#)—the reciprocal crosses of RRG42 and SS. Comparison of the log concentration–response curves in F1 progeny from reciprocal crosses with their parental strains of RRG42 and SS revealed straight parallel log concentration–probit lines (Fig. 1) with similar slopes among RRG42, SS and F1RS strains, and the slope of F1SR strain was smaller than that of the foregoing three strains (Table 2). This result indicates that the RRG42 and SS strains were relatively homogeneous for resistance and susceptibility, respectively, to abamectin [30]. The difference observed between the slopes of log concentration–probit lines for F1RS and F1SR (2.6 and 3.3 for F1RS and F1SR, respectively) suggests that there were more individual heterozygous in F1RS than in F1SR and the resistance to abamectin in T. cinnabarinus may be influenced by the sex of the mites. The LC50 values of abamectin in F1 progeny from reciprocal crosses between SS and RR were significantly different (0.042 (0.039–0.045) and 0.020 (0.019–0.021) mg l1, Table 1), also suggesting that the maternal or cytoplasmic effect may exist in the inheritance of resistance in T. cinnabarinus. These results are not consistent with previous findings in cyhexatin and propargite resistant T. pacificus [31] and pyrethroid resistant house flies [32–34], in which the resistance to insecticides was inherited autosomally. The different findings between our current work on T. cinnabarinus and previous studies on T. pacificus and house flies may suggest the different genetic mechanisms presented between these species for insecticide resistance or mechanisms of inheritance are different between different types of insecticides. The degrees of dominance (D) of resistance for each heterozygous F1s from reciprocal crosses were calculated according to the index used by Stone [24] (Table 2). The D values for the F1 progeny of F1RS and F1SR were 0.17 and the 0.81, respectively, ranged within 1 to 0, indicating that the resistance of T. cinnabarinus to abamectin was incompletely recessive. This suggestion was further supported by the results of the log concentration–probit response lines for F1s from reciprocal crosses, which were inclined to that for SS (Fig. 1) compared with the line for RRG42.

Table 2 Effect of abamectin on susceptible (SS), resistant (RRG42), reciprocal progenies F1RS and F1RS, and backcrosses (F2 or BC) strains of Tetranychus cinnabarinus.

a b c d

Cross

The number of testeda

Slope

LC50 (95% CL) (mg l1)

RRb

Dominance level (D)

Parent SS Parent RRG42 F1RSc F1SRd BC1 (RRG42  F1RS) or F2 BC10 (SS  F1SR)or F20

720 630 720 720 900 900

3.3 3.1 2.6 3.3 4.7 3.2

0.017 0.147 0.042 0.020 0.025 0.012

1.0 8.7 2.5 1.2 1.5 0.7

0.17 0.82

The adult females were tested when conducted the bioassay. RR, resistance ratio; LC50 of each strain/LC50 of SS (RRG0) strain. F1RS is the offspring of RRG42$  SS#. F1SR is the offspring of SS$  RRG42#.

(0.010–0.024) (0.140–0.154) (0.039–0.045) (0.019–0.021) (0.024–0.026) (0.011–0.013)

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Table 3 The chi-square (v2) analysis for monogenic or polygenic inheritance of abamectin resistance in Tetranychus cinnabarinus. Mites of testeda

Back-cross progeny BC1 (F1RS$  RRG42#) BC10 (F1SR$  SS#) **

900 900

15.5 15.5

Anticipant v2 (0.01,8)

v2b

v2c

df **

20.1 20.1

215.5 254.9**

df *

8 8

17.2 90.8**

8 8

Significant difference (p = 0.05) between the observed and the expected v2 values. Significant difference (p = 0.01) between the observed and the expected v2 values. a The adult females were tested when conducted the bioassay. b Show the value of v2 calculated from Keena’s formula. c Show the value of v2 calculated from Preisler’s formula.

Since 1956, the inheritance of resistance in mites, such as T. urticae, T. pacificus, Panonychus citri, P. ulmi (European red mite), T. kanzawai kishida (Kanzawa spider mite), Amblyseius nichols [35], A. Pseudolongispinosus [36] and T. cinnabarinus [37,38] were reported. Croft [39] reported that inheritance of resistance of T. urticae to formatanate appeared to be dominant whereas to cyhexatin may be intermediate to recessive. Hoy [23] reported that resistance of T. pacificus to cyhexatin and propargite was semi-recessive. Keena [1] reported that propargite resistance in T. pacificus was nearly completely recessive. Wu [37,38] reported the inheritance of organophosphate and monocrotophos resistance in T. cinnabarinus was incompletely dominant. The present study is for first time to report the inheritance of abamectin resistance in T. cinnabarinus with an incomplete recessive inheritance. The inheritance of abamectin resistance in house fly and diamondback moth were highly recessive [12] and incomplete recessive [43], respectively. These studies suggest the resistance to abamectin in insect and mite were controlled by recessive gene or genes.

SS

RRG42

0.012

0.020

F1SR

BC'-O

BC'-E

8.0 7.0 6.0 5.0 4.0 3.0 2.0 0.006

0.026

0.060

0.113

0.200

-1

Concentration (mg.L ) Fig. 3. Abamectin log concentration–probit lines for susceptible SS, resistant RRG42, their F1 progeny of F1SR (SS$  RRG42#), and back-cross progeny BC10 (F1SR$  SS#). BC10 -O: observed; BC10 -E expected.

4.0

lower concentration, BC10 -E was significantly separated from BC10 -O at the higher concentration (Fig. 3). The results of both chi-square test and log concentration–probit analysis strongly disagree with monogenic inheritance model [40], indicating the inheritance of T. cinnabarinus resistance to abamectin might be controlled by more than one gene. It has been reported that the inheritance of formatanate resistance in T. urticae, appeared to be monofactorial [39]. It also reported that cyhexatin and propargite resistance in T. pacificus was primarily determined by a major semi-recessive gene [23,31]. Nevertheless, propargite resistance in T. urticae was probable controlled by more than one gene [1]. Wu also reported that inheritance of resistance to organophosphorus insecticides, omethoate and monocrotophos, in T. cinnabarinus, was determined by a single incompletely dominant gene [37,38]. The present study is the first time to report the inheritance of abamectin resistance in T. cinnabarinus, which was polygenic non-complete recessive. The result was consistent with the resistant inheritance model of Leptinotarsa decemlineata [41], Musca domestica and Plutella xylostella to abamectin [42,43]. In conclusion, the inheritance of abamectin resistance in T. cinnabarinus may be controlled by more than one incompletely recessive factors and the resistance was developed slowly in the laboratory conditions. These results would provide the valuable information for designing appropriate the strategies for managing T. cinnabarinus and delaying resistance development.

3.0

Acknowledgments

3.3. Characterization of the possible number of genes involved in resistance To characterize the possible number of the genes involved in the resistance, we conducted bioassay with females of back-cross progeny of BC1 (F1RS$  RRG42#, or F2) and BC10 (F1SR$  SS#, or F20 ) with abamectin. Our results of the goodness-of-fit chisquare test (Table 3) showed that the observed mortalities of BC1 and BC10 were significantly different from the expected mortalities based on a monogenic resistance in the chi-square tests. Further, plots of the observed and expected concentration–response data for the back-cross progenies showed that within all tested dosage range, the expected log concentration–probit lines for BC1, i.e., BC1-E were completely separated from 95% confidential limit of the observed lines of BC1-O (Fig. 2); although overlapped at the

8.0 S

R

RS

BC1-O

BC1-E

7.0

Mortality (Probit)

9.0

Mortality (Probit)

*

Anticipant v2 (0.05,8)

6.0 5.0

2.0 0.009 0.018 0.023 0.030 0.060 0.090 0.129 0.200 0.360 -1

Concentration (mg.L ) Fig. 2. Abamectin log concentration–probit lines for susceptible SS, resistant RRG42, their F1 progeny of F1RS (RRG42$  SS#), and back-cross progeny BC1 (F1RS$  RRG42#). BC1-O: observed; BC1-E expected.

This research was funded in part by the National Nature Sciences Foundation of China(30571239 and 30600059). The research facility was kindly provided by the Key Laboratory of Entomology and Pest Control Engineering, Ministry of Agriculture, PR China and College of Plant Protection, Southwest University, Chongqing, PR China.

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