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Article

Insecticide Resistance and Plant Virus Status of Bemisia tabaci on Soybean in Suzhou

by
Qi Li
1,2,
Yao Ji
2,
He Du
1,2,
Shufang Ma
3,
Jifei Zhu
3,
Dehui Zhu
3,
Natalia A. Belyakova
4,
Youjun Zhang
1,2,* and
Xin Yang
2,*
1
College of Plant Protection, Hunan Agricultural University, Changsha 410125, China
2
State Key Laboratory of Vegetable Biobreeding, Department of Plant Protection, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, China
3
Suzhou Plant Quarantine and Protection Station, Suzhou 234000, China
4
All-Russia Institute of Plant Protection, Russian Academy of Sciences, Podbelskogo 3, Pushkin, 196608 St. Petersburg, Russia
*
Authors to whom correspondence should be addressed.
Agriculture 2025, 15(10), 1071; https://doi.org/10.3390/agriculture15101071
Submission received: 15 March 2025 / Revised: 9 May 2025 / Accepted: 14 May 2025 / Published: 15 May 2025
(This article belongs to the Special Issue Sustainable Use of Pesticides—2nd Edition)
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Versions Notes

Abstract

:
Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) is a super pest that seriously endangers the development of the agricultural economy worldwide. To prevent and control B. tabaci, insecticides have been used for many years, which has inevitably led to increased tolerance to chemical agents. To elucidate the development of field resistance and more scientifically and efficiently control B. tabaci, in December 2024, we conducted bioassays on B. tabaci on soybeans in Suzhou, Anhui Province, using 14 insecticides. These fourteen insecticides, namely, abamectin, spinetoram, thiamethoxam, flupyradifurone, imidacloprid, dinotefuran, acetamiprid, thiacloprid, nitenpyram, bifenthrin, deltamethrin, pyridaben, flonicamid, and emamectin benzoate, have multiple action sites and have all shown good control effects on B. tabaci. The results revealed that B. tabaci has developed high resistance to many insecticides and that some insecticides have even tended to fail, but B. tabaci is still sensitive to a small number of insecticides. Different biotypes of B. tabaci differ significantly in terms of insecticide resistance. We determined that the population of B. tabaci on soybean in Suzhou was the MED (Q) biotype. It carried the TYLCV virus, with a virus carrying rate of 60%, but did not carry ToCV or CCYV.

1. Introduction

Bemisia tabaci is a stinging insect in the family Aleyrodidae of order Hemiptera with a body length of approximately 1 mm. It is distributed mainly in the tropics and subtropics. However, with increased global warming and the growth of vegetables greenhouse in recent years, it is often found in many temperate climate regions. B. tabaci mainly parasitizes the backs of plant leaves. The main hazards to plants include the sucking of plant juice; reduction in plant activity; the secretion of honeydew, which leads to fungal reproduction inducing coal pollution disease, which then affects plant photosynthesis [1]; and the spread of a variety of plant viruses, causing crop yield reduction or even crop failure. Among the 114 plant viruses that can be transmitted by insects of this family, B. tabaci can transmit 111 [2]. B. tabaci is not only a worldwide pest but also a super pest because of its wide range of hosts: more than 600 plant species [3]. B. tabaci can parasitize so many plants because it steals the plant phenol sugar detoxification enzyme-encoding gene PMAT through horizontal gene transfer; phenol sugar is the substance used by plants to resist foreign enemies [4]. There are three forms of B. tabaci: eggs, nymphs, and adults. B. tabaci can reproduce in two ways: bisexual reproduction and parthenogenesis [5]. In fact, B. tabaci is a complex of 24 morphologically indistinguishable organisms [6], including many different types of biotypes, among which the most harmful and widely distributed are the Middle East-Asia Minor 1 (MEAM1, ‘B’ type) and Mediterranean (MED, ‘Q’ type) types. Although these two biological types cannot be directly distinguished by their appearance, they can be delimited by 3.5% mtCO1 sequence pairwise genetic distance divergence [7]. In China, MEAM1 has gradually replaced the native B. tabaci biotype because of its high resistance to pyrethroid insecticides [8]. MED subsequently replaced MEAM1 as the dominant biotype because of its greater resistance to neonicotinoid insecticides [9,10]. Because different biotypes have significant differences in resistance to different types of insecticides [11,12,13], identification of the biotype is a prerequisite for the prevention of B. tabaci whiteflies. There are various methods for controlling B. tabaci, but chemical control is the most widely used and effective way. Pesticides used in chemical control are diverse, including nicotine insecticides, pyrethroid insecticides and biopesticides. But with the long-term use of pesticides, the tolerance of B. tabaci to pesticides is increasing. B. tabaci populations in Spain have developed high resistance to spirotetramat [14] and cyantraniliprole [15]. B. tabaci populations in both Australia [16] and Israel [17] have developed high resistance to pyriproxyfen. The population of B. tabaci in India has shown significant resistance to organophosphorus, pyrethroid and neonicotinoid insecticides [18]. The annual detection of B. tabaci resistance in China revealed that B. tabaci populations in many provinces presented high levels of resistance to imidacloprid, thiamethoxam, deltamethrin, etc. [19]. In conclusion, resistance to multiple insecticides is a major challenge for the chemical control of Bemisia tabaci.
The resistance of B. tabaci to insecticides is due to the succession of biotypes [11,12] and the massive application of chemical agents [20] and is also related to the presence of a variety of viruses. The most important cause of agricultural economic loss caused by B. tabaci carrying viruses is a reduction in plant production or even death. Among these viruses, tomato yellow leaf curl virus disease (TYLCV) caused by geminivirus is the most serious, and B. tabaci is the only vector insect of TYLCV [21]. B. tabaci and plant viruses have complex interactions. Some studies have noted that the spawning quantity, development duration, female hatching rate, lifespan, etc. of B. tabaci differs before and after carrying the virus [22]. And this change has different effects on different biotypes. Q-type B. tabaci not only adapts to TYLCV better than B-type B. tabaci does but also exhibits increased fitness in diseased plants [9]. Coinfection with TYLCV and ToCV (Tomato chlorosis virus) promoted the transmission of the ToCV virus by the Med-type B. tabaci [23]. Interestingly, feeding on CCYV-infected (Cucurbits chlorotic yellowing virus) plants also significantly changed the sex ratio of the population from the original male to female ratio of 1:1 to 0.5:1, representing a significant decrease in the number of male individuals [24]. Once plants are infected with viral diseases, they are difficult to treat. Thus, preventing and controlling B. tabaci as a viral vector is particularly important. To provide a theoretical basis and data support for the control of B. tabaci in the field, we need to monitor and analyze the changes in biotypes of B. tabaci in the field, the current status and development of resistance to B. tabaci, and the status of a variety of plant viral diseases transmitted by B. tabaci and comprehensively analyze the current status of B. tabaci damage in the field.

2. Materials and Methods

2.1. Field Populations

The B. tabaci specimens used in this study were collected from Yongqiao District, Suzhou city, Anhui Province, and their host plant was soybean. Anhui is an important soybean planting area in China, and its soybean planting area and output rank second in the country. Suzhou is located in the middle of Anhui Province, with a soybean planting area of more than 134,000 hectares (32,947 acres), accounting for one quarter of the province (Figure 1). Soybean is one of the preferred hosts of B. tabaci, and the warm climate in Suzhou is suitable for its breeding. Therefore, every year, the spread of B. tabaci in Suzhou has caused considerable losses to the agricultural economy. Every August to October, B. tabaci can even attack urban areas, which has a serious adverse impact on the lives of citizens. Clarifying the development of resistance in the B. tabaci population in Suzhou is highly important.

2.2. Insecticides

In this study, we selected the following 14 insecticides with good control effects on B. tabaci adults; the following seven are neonicotinoid pesticides: thiamethoxam [19] 250 g L−1 EC (Syngenta Crop Protection Company, Shanghai, China), a novel second-generation nicotine-based that controls pests through gastric toxicity; flupyradifurone [25] 170 g L−1 SL (Bayer Crop Science, Hangzhou, China), which has almost no cross-resistance with other neonicotinoid insecticides; imidacloprid [26] 700 g L−1 WG (Bayer Crop Science, Hangzhou, China), dinotefuran [27] 200 g L−1 SL (Xinbaihu Biotechnology Co. Ltd., Hefei, China), acetamiprid [28] 100 g L−1 SL (Qingdao Taiyuan Technology Development Co., Ltd., Qingdao, China) and nitenpyram [29] 200 g L−1 WG (Beijing Huarong Kaiwei Plant Protection Biological Technology Co., Ltd., Beijing, China), which have similar effects; thiacloprid [30] 400 g L−1 SC (Limin Group Co., Ltd., Xinyi, China), a new chloronicotinic insecticide that acts on the membrane after the nerve junction of insects; and two types of biological insecticides: avermectin [19] 18 g L−1 EC (Chemical Industry Co. Ltd., Beijing, China), which is a glutamate-gated allosteric modulator of chloride channels; and spinetoram [31] 60 g/L SC (Corteva Agriscience, Indianapolis, IN, USA), which is a broad-spectrum insecticide. The remaining five insecticides were as follows: bifenthrin [31] 45 g L−1 WG (Qingdao Audis Bio-Tech Co. Ltd., Qingdao, China) and deltamethrin [32] 25 g L−1 EW (Bayer Crop Science, Hangzhou, China), pyrethroid insecticides that paralyze insects by prolonging the opening time of sodium ion channels and disturbing the nervous system; pyridaben [33] 150 g L−1 EC (Yifan Biotechnology Group Co. Ltd., Wenzhou, China), which can inhibit the synthesis of glutamate dehydrogenase in insects, resulting in interference with the normal physiological functions of insects or mites; flonicamid [34] 500 g L−1 WG (Shandong Yijia Agrochemical Co., Ltd., Shandong, China), which inhibits the sucking effect of pests, causing them to starve and die; and emamectin benzoate [35] 116 g L−1 SC (Keagio, Shandong, China), which interferes with the nerve conduction system of insects, resulting in their loss of normal motility (Table 1).

2.3. Adult Bioassays with the Fourteen Pesticides

The adult bioassay method employed was previously described by Zheng [36]. First, the approximate concentration was preset according to the recommended concentration in the field, and six concentration gradients were established using the gradient dilution method, with each gradient reduced one time. The second step involved placing the leaves at the bottom of the biological test tube, using a punch to divide the fresh, flat cotton leaves that had not been exposed to pesticides into small discs with a diameter of 22 mm, and then placing them into the pesticide solution prepared in the first step to soak for 15 s with three replicates for each concentration. The control group was soaked in distilled water. After the leaves were dried on filter paper, they were placed in a glass bioassay tube with 1.5% agar applied in advance to moisten the leaves, and the back of the leaves thus moves upward to simulate the environment of B. tabaci on the back of the leaf. Finally, a sucking tube was used to insert B. tabaci into the bioassay tube, and 20 adults were randomly selected from each tube with three bioassay tubes of one concentration. Then, the bioassay tube was placed upside down at approximately 26 ± 1 °C under a 16 h:8 light:dark photoperiod. After 48 h, the results were observed and recorded, and the mortality was calculated.

2.4. Identification of the Biotypes and Viruses of B. tabaci

2.4.1. Total DNA Extraction from B. tabaci

Forty-eight B. tabaci were randomly selected for DNA extraction. Total DNA was extracted from individual B. tabaci using the Kapa Express Extract DNA Extraction Kit (Beijing PuKaiRui Biotechnology Co., Ltd., Beijing, China,). The specific system was composed of ddH2O (26.5 μL) and buffer (3.0 μL), and 0.5 μL of enzyme, which was premixed. Then, a single B. tabaci was placed at the bottom of a 1.5 mL centrifuge tube, grinding beads were added, the premixed DNA extraction system was added, and the mixture was placed in a grinder until the insect body was completely broken. The mixture was then centrifuged at 8000 rpm for 30 s, and the supernatant was pipetted into a sterilized PCR tube, which was subsequently placed into a PCR instrument for the following enzymatic reaction: protease lysis at 75 °C for 10 min and enzyme inactivation at 95 °C for 5 min.

2.4.2. Identification of B. tabaci Biotypes

Because there is a difference in mtco 1 gene between Med B. tabaci and MEAM1 B. tabaci, mtco1 digestion can be used for biotype identification of B. tabaci [37,38]. First, this 620 bp sequence was amplified, and DNA amplification was performed using 2×EsTaq Master Mix (Beijing ComWin Biotech Co., Ltd., Beijing, China). The amplified product was digested with ASEI endonuclease (Biolink Beijing Blinc Biotechnology Co., Ltd., Beijing, China) upstream primer (Cl-J-2195 5′-TTGATTTTTTGGTCATCCAGAAGT-3′) and downstream primer (R-BQ-2819 5′-CTGAATATCGRCGAGGCATTCC-3′) [36]. The 20.0 μL PCR mixture was as follows: 10.0 μL of PCR mixture, 1.0 μL of upstream and downstream primers, 1.0 μL of DNA template, and 7.0 μL of ddH2O. PCR was performed as follows: predenaturation at 94 °C for 2 min, 30 cycles of denaturation at 94 °C for 30 s, annealing at 55 °C for 30 s, extension at 72 °C for 30 s, and a final extension at 72 °C for 2 min. The PCR products were stored in a refrigerator at 4 °C. The PCR products were subsequently digested with the restriction enzyme ASEI for 2 h. The digestion system included ddH2O (6.5 μL), 10 × buffer (3.1 × 3.0 μL), and ASEI endonuclease (0.5 μL). After premixing, 10.0 μL from each tube was aliquoted and mixed with the PCR products. Enzymolysis was performed at 37 °C for 2 h or left overnight at room temperature. The enzyme digestion product was spotted with 5.0 μL on the prepared 1.5% agarose gel and electrophoresed at 150 V for 20 min, and the size of the enzyme digestion product fragment was determined on a Tanon MINI Sapce 3000 gel imager (Shanghai Tanon Life Science Co., Ltd., Shanghai, China) to identify the biotype of B. tabaci. The target gene amplified by PCR is a 620 bp mtCOI gene fragment, which is digested by the restriction enzyme ASEI. Because there is an ASEI endonuclease site in the Med B. tabaci gene fragment, this site is cut to yield two fragments of different lengths (498 bp, 122 bp), but there is no such enzyme site in the MEAM1 gene fragment, so the MEAM1 gene fragment is still a 620 bp gene fragment after digestion by the ASEI endonuclease (Figure 2).

2.4.3. Detection of B. tabaci Viruses

The main reason why B. tabaci harms the agricultural economy is the reduction in production or even a lack of harvest caused by the spread of viral diseases. We detected three kinds of plant viruses carried by B. tabaci on the soybean population in Suzhou, including the DNA virus TYLCV (accession numbers: NC_004005), the RNA virus ToCV (accession numbers: NC_007340), and CCYV (accession numbers: OQ285911). TYLCV and ToCV are harmful mainly to tomatoes, whereas CCYV is harmful mainly to melons and Cucurbitaceae plants. The previously extracted total DNA of a single B. tabaci was used as a template. The 20.0 μL PCR system was as follows: 10.0 μL of PCR mix, 7.0 μL of ddH2O, 1.0 μL of upstream and downstream primers and 1.0 μL of DNA sample. The specific primers TYLCV-61 (5′-ATACTTGGACACCTAATGGC-3′) and TYLCV-473 (5′-AGTCACGGGCCCTTACAA-3′) were used [39]. The PCR amplification conditions were as follows: 94 °C for 2 min; 32 cycles of 94 °C for 30 s, 60 °C for 30 s, and 72 °C for 30 s; and 72 °C for 2 min. The PCR product was directly detected by gel electrophoresis, and the target band was 412 bp in length. The lack of an amplification band indicates that a single B. tabaci does not carry TYLCV.
The RNA of B. tabaci was extracted using the FastPure Cell/Tissue Total RNA Isolation Kit V2 (Vazyme Biotech Co., Ltd., Nanjing, China). RNA was reverse transcribed using the FastKing RT Kit (with gDNase) (Tiangen Biotech (Beijing) Co., Ltd., Beijing, China), and the cDNA obtained was used for subsequent detection. The synthesized cDNA of B. tabaci was used as a template. The 20.0 μL PCR system was as follows: PCR mixture, 10.0 μL; ddH2O, 7.0 μL; upstream and downstream primers, 1.0 μL each; and a single whitefly DNA sample, 1.0 μL. The specific primers ToCv-172 (5′-GCTTCCGAAACTCCGTCTTG-3′) and ToCV-610 (5′-TGTCGAAAGTACCGCCACC-3′) were used. The PCR amplification conditions were as follows: 95 °C for 2 min; 35 cycles of 94 °C for 30 s, 55 °C for 30 s, and 72 °C for 30 s; and 72 °C for 2 min. The PCR product was directly detected by gel electrophoresis, and the target band was 439 bp. The absence of an amplified band indicated that the single B. tabaci did not carry TOCV.
The synthesized cDNA of B. tabaci was used as a template. The 20 μL PCR system was as follows: 10.0 μL of PCR mix, 7.0 μL of ddH2O, 1.0 μL of upstream and downstream primers and 1.0 μL of a DNA sample from a single B. tabaci. The specific primers CPF (5′-CGCAATCAATAAGGCGGCGACC-3′) and CPR (5′-ACTACAACCTCCCGGTGCCAACT-3′) were used. The PCR amplification conditions were as follows: 95 °C for 5 min; 35 cycles of 94 °C for 1 min, 58 °C for 30 s, and 72 °C for 1 min; and 72 °C for 7 min. The PCR product was directly detected by gel electrophoresis, and the target band was 804 bp in length. If there was no amplified band, the single B. tabaci did not carry CCYV.

2.5. Statistical Analysis

As early as 2008, we collected a sensitive population of B. tabaci and named it Strain THS, which has been cultivated in an environment without pesticide contamination. This population is used for biological testing as the sensitive baseline of each agent to observe the development of insecticide resistance and maintain the consistency of internal experiments. The raw data for each bioassays result were recorded. At the same time, the data of the control group were also included to eliminate the influence of objective factors such as natural death on the results, and POLO PLUS 2.0 software was used to calculate the median lethal concentration. The resistance factor (RF) was calculated as follows: the LC50 of the resistant population in the field was divided by the LC50 of the baseline. While some sensitive baselines refer to those used in other experiments, the sensitive baseline of pyridaben was 0.52 mg L−1 [35], that of emamectin benzoate was 2.92 mg L−1 [35], that of spinetoram was 1.38 mg L−1 [31], that of nitenpyram was 2.68 mg L−1 [40], that of flupyradifurone was 18.63 mg L−1 [40], that of dinotefuran was 6.01 mg L−1 [41], that of flonicamid was 7.52 mg L−1 [42], that of thiamethoxam was 1.19 mg L−1 [43], that of imidacloprid was 0.99 mg L−1 [43], that of abamectin was 0.06 mg L−1 [44] and that of acetamiprid was 1.80 mg L−1 [44]. The resistance levels were categorized as very high (RF > 100), high (RF = 30–100), medium (RF = 10–30), low (RF = 1–10), and susceptible (RF < 1).

3. Results

3.1. Resistance of Adult B. tabaci to Fourteen Pesticides

The damage caused by B. tabaci in Suzhou is extremely serious. The local soybean planting area is more than 134,000 hectares (32,947 acres), accounting for one quarter of the planting area in the province. Soybean leaves are one of the favorite crops of B. tabaci. Dense fourth-instar nymphs of B. tabaci that are about to emerge, white pupal shells that have been successfully shed, and adult B. tabaci can be observed on the backs of soybean leaves. Patches of yellow spots appear on the front of leaves, which consume many plant nutrients, resulting in plant weakness and even plant death in serious cases, resulting in considerable losses to the extensive local soybean planting areas.
For abamectin, both the sensitivity baseline and the bioassay results of the soybean B. tabaci population in Suzhou were very low, and the resistance factor was 0.33. For spinetoram, the median lethal concentration and resistance factor are also very low, and the RF was only 0.41.
For thiamethoxam, the median lethal concentration was very high, reaching 2169.316 ppm, and the resistance factor reached 1845.64. For flupyradifurone, dinotefuran and deltamethrin, a moderate level of resistance was observed. The resistance level of imidacloprid, another insecticide with a long history, was relatively high with a median lethal concentration of 4572.568 ppm and a resistance factor of 4618.75. For acetamiprid, the sensitivity baseline was very low, at only 1.80 ppm, but the biological test results for the Suzhou population reached 786.568 ppm, and the resistance factor was 436.98. For thiacloprid, the resistance factor was also high, reaching 116.43. For nitenpyram and bifenthrin, the resistance factor was very low, but because the sensitivity baseline of bifenthrin is relatively high, its median lethal concentration also reached 144.085 ppm. Among all insecticides, imidacloprid had the highest resistance factor, reaching 4618.75. Finally, for flonicamid and emamectin benzoate, the former Suzhou population presented a high level of resistance, with a resistance factor of 37.16, whereas the latter population was sensitive with a resistance factor of 0.22 (Table 2).

3.2. Results of the Determination of B. tabaci Biotypes and Viruses

We randomly selected 20 B. tabaci individuals and extracted total DNA from each, and further detection revealed that 14 of them were TYLCV positive. This finding revealed that the soybean population of B. tabaci in Suzhou carries TYLCV with a virus-carrying rate of 70%. However, the target band was not detected for CCYV or ToCV, which indicated that the population of soybean B. tabaci in Suzhou does not carry ToCV or CCYV.

4. Discussion

There are many ways to control B. tabaci in the field, including physical, chemical, biological, and agricultural control [19]. However, the most frequently used and most effective method is chemical control. Chemical control involves a variety of pesticides with different modes and sites of action [45]. There is a significant difference in the resistance of different biotypes of B. tabaci to insecticides. For example, the resistance of MEAM1 to pyrethroid insecticides has been widely reported [46], whereas Med is highly resistant to neonicotinoid insecticides, which is also why, with the extensive use of neonicotinoid insecticides in China, Med has gradually replaced MEAM1, making it the dominant biotype in China [43]. Therefore, while monitoring the development of resistance, we also identified its biotype and determined that the B. tabaci biotype in Suzhou was Med (Figure 2), which is also consistent with the current dominant biotype in China, and we found from the bioassay results that this population was indeed highly resistant to the neonicotinoid insecticides imidacloprid and thiamethoxam. While Med B. tabaci is a better carrier of TYLCV, TYLCV is not only detected in tomato populations. The presence of TYLCV was detected in the soybean population of B. tabaci in Suzhou, but the target signal was relatively weak and the virus carrier rate was relatively low, indicating that the occurrence of TYLCV in this area was relatively mild.
The median lethal concentration of all the pesticides was very low (Table 3); the lowest was observed for abamectin (0.06 ppm), the highest was observed for bifenthrin (20.61 ppm), and the majority of the median lethal concentrations were less than 10 ppm, which indicates that the 14 selected pesticides initially had good control effects on B. tabaci. However, with respect to current B. tabaci resistance, the toxicity of some pesticides to B. tabaci has been greatly reduced, and some effects have been minimal. Nevertheless, some biological insecticides and second-generation insecticides still have good control effects on B. tabaci. Resistance to biopesticides does not evolve easily because of the diversity of action sites [47], whereas resistance to second-generation insecticides evolves relatively quickly [48].
Figure 3 shows that the concentrations of the two selected biological pesticides abamectin and spinetoram are very low in terms of both the median lethal concentration and the resistance ratio, which indicates that biological pesticides are not only very effective in the control of B. tabaci but also do not easily produce resistance, and biological pesticides have little impact on the environment or other organisms, which is more in line with the requirements of green and low-toxicity pesticides [47]. The research on and development of neonicotinoid insecticides can be traced back to 1991 and gradually became the most effective insecticide for the control of pests with piercing and sucking mouthparts [49]. In this study, eight new nicotine insecticides were assessed. Except for the relatively short launch time of flupirfuranone and flupirimid, the other six have been used for many years, which has led to high resistance to some nicotine insecticides. For example, thiamethoxam (RF = 1845.64), acetamiprid (RF = 244.27), and imidacloprid (RF = 4618.75) all presented very high resistance levels. The highest median lethal concentration even reached 4572.568 ppm, which was not suitable for the long-term control of B. tabaci. The two new nicotine insecticides also produced moderate to high levels of resistance, indicating that the resistance of the Q-biotype B. tabaci to nicotine insecticides has developed rapidly [43]. However, the resistance levels of dinotefuran (RF = 13.08) and nitenpyram (RF = 2.88) are relatively low—far lower than those of other neonicotinoid insecticides. It can be used for the subsequent chemical control of Bemisia tabaci in Suzhou. Among the pyrethroid insecticides, bifenthrin (RF = 6.99) has a lower resistance ratio, which is more suitable for controlling the field population of Bemisia tabaci in Suzhou when insecticides are used in rotation. Finally, emamectin benzoate, which is a combination of two insecticides, has a good control effect on B. tabaci with a median lethal concentration of only 0.667 ppm (Figure 3). The insecticides with a good control effect on Bemisia tabaci screened by bioassay experiments can be used for the chemical control of Bemisia tabaci in this area in the future. The selected insecticides with severe resistance development can provide basic data and theoretical support for the study of the resistance mechanism of Bemisia tabaci.

5. Conclusions

Anhui, China, is an important soybean-planting province. The soybean-planting area in the Suzhou area constitutes one quarter of the province. The damage caused by B. tabaci to soybean is very severe. In the face of the large gap between soybean production and demand, reducing the harm caused by B. tabaci to important crops such as soybeans is highly important for bioassay experiments involving a variety of insecticides of B. tabaci in Suzhou. Faced with the huge gap between soybean production and demand, in order to reduce the harm of Bemisia tabaci to important crops such as soybeans, 14 kinds of insecticide bioassay tests were carried out on soybean Bemisia tabaci population in Suzhou area. According to the results, abamectin, acetamiprid, bifenthrin, nitenpyram, and emamectin benzoate, which have good control effects and low resistance factors, are recommended for chemical control of Bemisia tabaci in Suzhou area. At the same time, we also detected that the local population of Bemisia tabaci was Q biotype and carried TYLCV, which was consistent with the current biotype distribution of Bemisia tabaci in China and the background of TYLCV outbreaks across the country

Author Contributions

Conceptualization, Y.Z., X.Y. and Q.L.; methodology, X.Y. and Q.L.; software, Q.L.; validation, Q.L. and H.D.; formal analysis Y.Z., X.Y. and Q.L.; investigation, Q.L., S.M., J.Z. and D.Z.; resources, Y.Z. and X.Y.; data curation, Q.L.; writing—original draft preparation, Q.L.; writing—review and editing, X.Y. and N.A.B.; visualization, Q.L., Y.J. and H.D.; supervision, X.Y.; project administration, X.Y.; funding acquisition, Y.Z. and X.Y. All authors have read and agreed to the published version of the manuscript.

Funding

The National Natural Science Foundation of China (grant no. 32361133558, 32272598, 32221004), the China Agriculture Research System (grant no. CARS-24-C-02), the Beijing Key Laboratory for Pest Control and Sustainable Cultivation of Vegetables and the Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences (grant no. CAAS-ASTIP-IVFCAAS), and the Central Public-interest Scientific Institution Basal Research Fund (Y2023XK15; Y2024XK01).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Conflicts of Interest

The authors declare that no competing interests exist.

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Agriculture 15 01071 g001
Figure 1. The left photograph shows the soybean field, and many yellow leaves can be observed. The middle photograph shows the yellow board for monitoring the control of B. tabaci with more than 10,000 B. tabaci on a single board. White pupal shells left by the emergence of B. tabaci, yellow fourth-instar nymph pseudopupae, and white adults can be seen on the back of the soybean leaf in the right photograph.
Figure 1. The left photograph shows the soybean field, and many yellow leaves can be observed. The middle photograph shows the yellow board for monitoring the control of B. tabaci with more than 10,000 B. tabaci on a single board. White pupal shells left by the emergence of B. tabaci, yellow fourth-instar nymph pseudopupae, and white adults can be seen on the back of the soybean leaf in the right photograph.
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Agriculture 15 01071 g002
Figure 2. M: marker D2000: (a) Identification of B. tabaci biotypes; (b) detection of TYLCV in B. tabaci. Lane 21 is the TYLCV bacterial mixture positive control.
Figure 2. M: marker D2000: (a) Identification of B. tabaci biotypes; (b) detection of TYLCV in B. tabaci. Lane 21 is the TYLCV bacterial mixture positive control.
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Agriculture 15 01071 g003
Figure 3. (a) Histogram showing the median lethal concentration of the 14 insecticides in the population of B. tabaci in Suzhou, Anhui Province; the abscissa is arranged in descending order according to the median lethal concentration. (b) Histogram showing the resistance factors of the 14 insecticides in the population of B. tabaci in Suzhou, Anhui Province. The abscissa is arranged from small to large according to the resistance factor.
Figure 3. (a) Histogram showing the median lethal concentration of the 14 insecticides in the population of B. tabaci in Suzhou, Anhui Province; the abscissa is arranged in descending order according to the median lethal concentration. (b) Histogram showing the resistance factors of the 14 insecticides in the population of B. tabaci in Suzhou, Anhui Province. The abscissa is arranged from small to large according to the resistance factor.
Agriculture 15 01071 g003
Table 1. Background information on the insecticides used in this study.
Table 1. Background information on the insecticides used in this study.
InsecticideFormulationClass of
Insecticide		Active
Ingredient		ManufacturerRecommended Field Concentration (mg L−1)
AbamectinEmulsifiable
Concentrate (EC)		Biological1.8%Chemical Industry
Co. Ltd.		10.8–14.4
SpinetoramSuspension Concentrate (SC)Biological6%Corteva Agriscience10–20
ThiamethoxamWater-Dispersible
Granule (WG)		Neonicotinoid25%Syngenta35–75
FlupyradifuroneSoluble
Concentrate (SL)		Neonicotinoid17%Bayer (China) Limited333–666
ImidaclopridWater-Dispersible
Granule (WG)		Neonicotinoid70%Bayer (China) Limited133.3–200
DinotefuranSuspension Concentrate (SC)Neonicotinoid20%Xinbaihu Biotechnology Co. Ltd.666.6–1333.2
AcetamipridEmulsifiable
Concentrate (EC)		Neonicotinoid10%Qingdao Taiyuan Technology Development Co., Ltd.50–100
ThiaclopridSuspension Concentrate (SC)Neonicotinoid40%Limin Group Co. Ltd.0.33–0.66
NitenpyramWater-Dispersible
Granule (WG)		Neonicotinoid20%Beijing Huarong Kaiwei Plant Protection Biological Technology Co., Ltd.0.5–1
BifenthrinWater-Dispersible
Granule (WG)		pyrethroid4.5%Qingdao Audis
Bio-Tech Co. Ltd.		0.66–1.66
DeltamethrinEmulsion in Water (EW)pyrethroid2.5%Bayer (China) Limited20–30
PyridabenEmulsifiable
Concentrate (EC)		Pyridazine ketone15%Yifan Biotechnology
Group Co. Ltd.		50–70
FlonicamidWater dispersible
Granule (WG)		Pyridine amide50%Shandong Yijia Agrochemical Co., Ltd.140–233.3
Emamectin benzoateSuspension Concentrate (SC)Organophosphorus11.6%Keagio17–20
Recommended field concentration (mg L−1): recommended by the manufacturer.
Table 2. Susceptibility of field populations of B. tabaci adults to fourteen insecticides.
Table 2. Susceptibility of field populations of B. tabaci adults to fourteen insecticides.
InsecticideN aSlope (±SE)LC50
(mg L−1)		95% FL bDf cχ2RFResistance Level
Abamectin3001.529 ± 0.2220.0200.004–0.03535.24780.33Susceptible
Spinetoram3001.142 ± 0.1850.5780.364–0.80031.9390.41Susceptible
Thiamethoxam3570.786 ± 0.1412169.3161346.905–4890.11640.1481845.64Very high
Flupyradifurone3560.949 ± 0.143313.435221.359–504.02840.33016.82Moderate
Imidacloprid4180.780 ± 0.1234572.5682769.194–10398.84650.9074618.75Very high
Dinotefuran3541.027 ± 0.14578.64137.725–193.04248.72413.08Moderate
Acetamiprid3710.922 ± 0.142786.568543.991–1331.09940.394436.98Very high
Thiacloprid3500.786 ± 0.1441875.5881156.237–4337.33640.345116.43Very high
Nitenpyram2941.654 ± 0.2117.7204.239–12.55734.8202.88Low
Bifenthrin3690.916 ± 0.138144.08599.432–201.97643.6876.99Low
Deltamethrin3520.832 ± 0.138281.181192.966–452.26542.63727.11Moderate
Pyridaben3580.787 ± 0.139476.117319.227–802.67140.237915.60Very high
Flonicamid3570.725 ± 0.139279.454177.446–571.76140.20837.16high
Emamectin benzoate3621.414 ± 0.1530.6670.519–0.84440.3130.22Susceptible
N a: total number of adults in bioassay. SE: standard error. LC50: concentration of insecticide killing 50% of adults. 95% FL b: 95% fiducial limits. Df c:degree of freedom. χ2: chi-square testing linearity of dose–mortality responses. RF: resistance ratio = the LC50 value of the field population divided by the LC50 value of the baseline.
Table 3. Baseline susceptibilities of the reference strain of B. tabaci to fourteen insecticides.
Table 3. Baseline susceptibilities of the reference strain of B. tabaci to fourteen insecticides.
InsecticideN aSlope (±SE)LC50
(mg L−1)		95% FL bDf cχ2Ref
Abamectin4981.95 ± 0.120.060.03–0.1432.33Yang et al. [44]
Spinetoram5161.96 ± 0.161.381.03–1.8631.85Wang et al. [31]
Thiamethoxam-1.54 ± 0.151.190.95–1.46--Wang et al. [43]
Flupyradifurone3561.35 ± 0.1118.6315.98–21.5032.35Wang et al. [40]
Imidacloprid-2.34 ± 0.210.990.83–1.17--Wang et al. [43]
Dinotefuran2851.67 ± 0.286.014.13–8.4331.92Li et al. [41]
Acetamiprid3281.57± 0.251.800.80–3.8042.46Yang et al. [44]
Thiacloprid2941.38 ± 0.45416.1010.139–20.63141.441Strain THS
Nitenpyram6632.78 ± 0.202.682.21–3.2634.820Wang et al. [40]
Bifenthrin2791.11 ± 0.19320.6110.473–76.81344.559Strain THS
Deltamethrin2851.11 ± 0.19110.374.865–35.82545.074Strain THS
Pyridaben7001.52 ± 0.120.520.32–0.7740.237Ahmad and Akhtar [35]
flonicamid-2.44 ± 0.187.526.64–8.54--Moustafa et al. [42]
Emamectin benzoate6001.46 ± 0.122.922.30–3.654-Ahmad and Akhtar [35]
N a: total number of adults in bioassay. SE: standard error. LC50: concentration of insecticide killing 50% of adults. 95% FL b: 95% fiducial limits. Df c:degree of freedom. χ2: chi-square testing linearity of dose-mortality responses. Ref: References.
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Li, Q.; Ji, Y.; Du, H.; Ma, S.; Zhu, J.; Zhu, D.; Belyakova, N.A.; Zhang, Y.; Yang, X. Insecticide Resistance and Plant Virus Status of Bemisia tabaci on Soybean in Suzhou. Agriculture 2025, 15, 1071. https://doi.org/10.3390/agriculture15101071

AMA Style

Li Q, Ji Y, Du H, Ma S, Zhu J, Zhu D, Belyakova NA, Zhang Y, Yang X. Insecticide Resistance and Plant Virus Status of Bemisia tabaci on Soybean in Suzhou. Agriculture. 2025; 15(10):1071. https://doi.org/10.3390/agriculture15101071

Chicago/Turabian Style

Li, Qi, Yao Ji, He Du, Shufang Ma, Jifei Zhu, Dehui Zhu, Natalia A. Belyakova, Youjun Zhang, and Xin Yang. 2025. "Insecticide Resistance and Plant Virus Status of Bemisia tabaci on Soybean in Suzhou" Agriculture 15, no. 10: 1071. https://doi.org/10.3390/agriculture15101071

APA Style

Li, Q., Ji, Y., Du, H., Ma, S., Zhu, J., Zhu, D., Belyakova, N. A., Zhang, Y., & Yang, X. (2025). Insecticide Resistance and Plant Virus Status of Bemisia tabaci on Soybean in Suzhou. Agriculture, 15(10), 1071. https://doi.org/10.3390/agriculture15101071

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