Next Article in Journal
Watering Volume and Growing Design’s Effect on the Productivity and Quality of Cherry Tomato (Solanum lycopersicum cerasiformae) Cultivar Ruby
Next Article in Special Issue
Physiological Response of the Target Stemborer Chilo suppressalis to Elevated CO2 as Reared with Transgenic Bt Rice during Different Plant Growth Stages
Previous Article in Journal
The Molecular Composition of Peat Organic Matter and Prospects for Its Use in Agriculture
Previous Article in Special Issue
RNAi-Mediated Interference with EonuGR1 Affects the Recognition of Phenylacetaldehyde by Empoasca onukii Matsuda (Hemiptera: Cicadellidae)
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Agronomy
Volume 13
Issue 9
10.3390/agronomy13092415
agronomy-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Sensitivities of Fall Armyworm (Spodoptera frugiperda) Populations in Different Regions of China to Four Bt Proteins

by
Yanfang Zhou
1,
Chunmeng Huang
1,
Yi Chen
2,
Lanzhi Han
1,
Jiajian Xie
1 and
Xiuping Chen
1,*
1
Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China
2
Sanya Research Institute, Chinese Academy of Tropical Agricultural Sciences, Sanya 572022, China
*
Author to whom correspondence should be addressed.
Agronomy 2023, 13(9), 2415; https://doi.org/10.3390/agronomy13092415
Submission received: 18 August 2023 / Revised: 15 September 2023 / Accepted: 15 September 2023 / Published: 19 September 2023
(This article belongs to the Special Issue Recent Trends towards Genetics-Based Methods for Pest Management in Agroecosystems)
Browse Figures
Versions Notes

Abstract

:
Fall armyworm (FAW), Spodoptera frugiperda, invaded the south of China in December 2018 and has since posed a huge threat to crop production in China. However, transgenic Bacillus thuringiensis (Bt) corn can efficiently control the damage caused by FAWs. In fact, the Chinese government has issued biosafety certificates for several Bt corn hybrids expressing any one of four Bt proteins, Vip3A, Cry1F, Cry1Ab, and Cry2Ab, or combinations thereof, to control FAWs. These Bt corn events are soon to be commercialized in China. Therefore, it is necessary to monitor and evaluate whether the FAW has developed resistance to any of the Bt corn hybrids planted in fields in China. To address this issue, we collected 11 geographical populations of FAWs and determined the sensitivity of each to the aforementioned four purified Bt proteins as assessed by diet surface overlay bioassays. The ranges for the 50% lethal concentration (LC50) of the four Bt proteins to all FAW populations were as follows: 11.42–88.33 ng/cm2 (for Vip3A), 111.21–517.33 (Cry1F), 135.76–1108.47 (Cry1Ab), and 994.42–5492.50 (Cry2Ab). The corresponding ranges for the 50% growth inhibition concentrations (GIC50) were 1.43–14.86, 2.35–138.97, 1.58–464.86, and 25.01–1266.07 ng/cm2. The lethal effects and growth inhibition effects of the four Bt proteins on FAW were in the same order of Vip3A > Cry1F > Cry1Ab > Cry2Ab. A comparison with published LC50 values of Bt proteins towards sensitive FAW populations revealed that all 11 FAW populations in this study were sensitive to Vip3A, Cry1F, and Cry1Ab. This study provides foundational data for monitoring and controlling the resistance of Bt corn to FAW in China.

1. Introduction

The fall armyworm (FAW) Spodoptera frugiperda is a notoriously polyphagous pest native to tropical and subtropical regions of the American continent, with host plants comprising ~353 species distributed into 76 families [1]. Like other major migratory agricultural pests, FAWs have been described as having the characteristics “international, migratory, explosive, and destructive” [2]. FAW larvae feed on stems, leaves, tassels, ears, and other plant parts. FAW-related damage to seedlings can reduce yield by 10–25% [3]. Indeed, FAW-related damage caused a 20% reduction in corn production in the United States in 2018. In certain South American countries with underdeveloped agricultural technology and relatively low investment in prevention and control, FAW-related damage can reduce corn yield by more than 70% [3]. Therefore, FAW has become a major biological disaster that seriously threatens food security worldwide. Unfortunately, this invasive pest moved into the south of China in December 2018 and quickly spread to 26 provinces by October 2019 [4]. Globally, FAW has two different strains, namely the corn and rice strains; the strain that first invaded China was identified as the corn strain [5]. If left unchecked, FAW has the potential to cause substantial damage to China’s agricultural economy.
Many methods such as synthetic insecticides and biopesticides, cultural control tactics including push–pull, and natural enemies can be used to minimize the damage caused by FAW [6], but some of these methods are time-consuming, laborious, pollute the environment, and can lead to resistance or other problems [7,8]. However, the development of molecular biotechnology techniques has fostered new ways of controlling FAW via the commercial planting of transgenic insect-resistant corn hybrids, which has become a widely adopted means of controlling FAW in the tropical and subtropical regions of the American continent. For example, transgenic Bacillus thuringiensis (Bt) corn events have been commercially planted abroad to control FAW; these hybrids include TC1507, which expresses the Bt protein toxin Cry1F, MON89034, which simultaneously expresses Cry1A.105 and Cry2Ab, and MIR162, which expresses Vip3Aa20, among other hybrids. Most hybrids express an individual Bt protein, i.e., Cry1Ab, Cry1F, Cry1A.105, Cry2Ab, or Vip3A, although some hybrids express two or more proteins [9,10,11,12,13]. With long-term and large-scale planting, however, FAW has developed field resistance to each of Cry1Ab, Cry2Ab, and Cry1F [14,15,16,17,18,19]. In Puerto Rico, for example, the FAW has developed 1000-fold field resistance to TC1507 corn [16]; consequently, TC1507 was voluntarily withdrawn from the territory by the technology’s developers. Since then, many populations of FAW that are field-resistant to Cry1F have been reported in Brazil [17] and Argentina [18] as well as in the states of Florida and North Carolina in the United States [19]. Brazil first introduced the Bt corn MON810 in 2008 and MON89034 in 2010; however, 3 years later, field-resistant FAW populations were found since their first introduction [20]. Although a Vip3A-resistant FAW population (up to 9800-fold resistance) was identified and selected for lab culture [21], no Vip3A-resistant field population has been reported to date. As such, the FAW is still considered to be sensitive to the Bt corn variety expressing Vip3A, and the frequency of resistance is considered low [21,22]. Obviously, resistance monitoring and management are crucial to the successful control of FAW in planting areas.
Since 2019, the Ministry of Agriculture and Rural Affairs of China has issued safety certificates for several genetically modified Bt corn hybrids, such as DBN9936 expressing Cry1Ab, DBN9501 expressing Vip3A, DBN3601T simultaneously expressing Cry1Ab and Vip3A, BLF4-2 simultaneously expressing Cry1Ab and Cry1F, and ND207 expressing Cry1Ab and Cry2Ab. Some bioassay experiments have shown that certain Bt hybrids are highly effective for controlling FAW [23,24,25,26]. In 2022, for example, several hybrids mentioned above were pilot-planted in the provinces of Yunnan and Inner Mongolia, and the results showed significant resistance to FAW and other insects in the field. Currently, the Chinese government is vigorously promoting the commercialization of Bt corn cultivation, and several Bt hybrids will be approved for field planting in China soon. Data from other countries have shown that the long-term commercialization of Bt crops has brought enormous selection pressure to populations of targeted insects, leading to the rapid evolution of the resistance of target pests to Bt corn hybrids, thereby reducing the efficiency of pest control [27,28]. Therefore, it is necessary to monitor and evaluate the resistance of the FAW to specific Bt proteins produced by Bt corn hybrids in China.
In the present study, 11 field populations of FAW were collected from eight cities in seven provinces in four major corn-producing regions in China, i.e., the Northern, Huanghuaihai, Southern, and Southwest regions, from 2021 to 2022. We measured the sensitivity of these field populations to four purified Bt proteins, namely Vip3A, Cry1F, Cry1Ab, and Cry2Ab, which are likely to be approved for large-scale cultivation in China. Our work is expected to provide fundamental data for monitoring and controlling the resistance of transgenic Bt corn to FAW in China and perhaps other countries as well.

2. Materials and Methods

2.1. Purified Bt Proteins

Purified Cry1Ab and Cry1F proteins were purchased from Envirotest-China (agent for EnviroLogix Inc., Portland, ME, USA; www.envirotest-china.com; accessed on 10 March 2021). The protoxin from Bt had been expressed as a single-gene product in Escherichia coli at Case Western Reserve University (Cleveland, OH, USA). The protoxin inclusion bodies were then dissolved, isolated, and purified, and the pure fractions were desalted and lyophilized. The purity was 94–96% (Marianne P. Carey, Case Western Reserve University, personal communication). Cry2Ab and Vip3A were purchased from Beijing Meiyan Agricultural Technology Co., Ltd. (Beijing, China; www.caasbuy.com/platform/shop.lf?shopid=2972; accessed on 10 March 2021). The production process of Cry2Ab and Vip3A was the same as that of Cry1Ab and Cry1F, and the purity was >90%. All protein samples were dissolved in distilled water at a concentration of 5 mg/mL and stored at −80 °C before use in the bioassay.

2.2. FAW Populations

Eleven different geographical populations of FAW were collected from eight cities in seven provinces in the four major corn production regions of China from 2021 to 2022 (Figure 1 and Table 1). These four regions make up more than 90% of the total corn acreage of China [29]. Information pertaining to FAW collection is given in Table 1.
The larvae were fed an artificial diet [30], which was cut into small pieces of ~1 g. Each well in a 24-well plate contained one piece of the diet and one larva. When the larvae grew to the 4th to 5th instar stage, they were transferred to a glass tube with an artificial diet; the tube was then closed with a cotton plug for pupation and adult emergence. The adults were placed in cages (4 × 25 × 25 cm) and fed a 10% w/v sugar solution to supplement nutrition and water. The top of each cage was covered with medical gauze for oviposition, which was changed every day and put into a zip-lock bag, and then the bag was placed in a climatic chamber at 26 ± 1 °C, 60 ± 10% relative humidity, with a photoperiod of 16 h:8 h (L:D). The resulting 0 to 24 h-old neonates after 2~3 generations were used for bioassays.

2.3. Bioassay

The sensitivity of each FAW population to each Bt protein was determined by a diet surface overlay bioassay. Briefly, approximately 1 mL of liquefied diet was poured into each well of a 24-well plate. After the diet solidified, 50 µL Bt protein solution was added onto the diet surface in each well; each Bt protein was tested at 10 concentrations: 625, 312.50, 156.25, 78.13, 39.06, 19.53, 9.77, 4.88, 2.44, and 0 ng/cm2 for Vip3A, or 5000, 2500, 1250, 625, 312.50, 156.25, 78.13, 39.06, 19.53, and 0 ng/cm2 for Cry1F, Cry1Ab, and Cry2Ab. Once all wells on a plate had been treated, the plate was tilted from front to back and from left to right to ensure that the protein solution was evenly distributed on the diet surface. After the diet surface dried, a single 0 to 24 h-old neonate was transferred to each well with a fine brush (24 neonates per concentration of Bt protein). After infestation, the plate was covered with a sheet of blow-molded paper pad and then fastened with four rubber bands to prevent escape. The infested plates were placed in a climatic chamber under the following conditions: temperature, 26 ± 1 °C; light/dark cycle, 16/8 h; relative humidity, 60 ± 10%. The bioassays were technically repeated three times (insects from the same generation) for each Bt protein toxin, and thus the total number of neonates used was 720 for each FAW population and for each protein. Mortality was recorded at 7 days after treatment. Larvae that remained in the first instar stage throughout the experiment were counted as dead. The weight of surviving larvae was measured and recorded at the end of each experiment.

2.4. Data Analysis

The growth inhibitory rate of FAW larvae was calculated as growth inhibitory rate (%) = [(body weight of control group − body weight of treated group)/body weight of control group] × 100. The fold of 50% lethal concentration (LC50) and 50% growth inhibition concentration (GIC50) between the most susceptible and least susceptible populations for each Bt protein = LC50 or GIC50 of the least susceptible populations/LC50 or GIC50 of the most susceptible. The susceptibility of different populations to Bt protein toxins was analyzed by probit and logit analysis using PoloPlus [31], which generated LC50 and GIC50 values with 95% fiducial limits, chi-square (χ2) data, slope with standard error (slope ± SE), and degrees of freedom. The difference between LC50 values was considered significant if the 95% fiducial limits of the values did not overlap. One-way analysis of variance followed by Duncan’s multiple range test was used to compare the statistical significance of differences among the average values of LC50 or GIC50 among the 11 FAW populations for the four Bt proteins by using the SPSS software package (version 13, 2004); p < 0.05 was considered to reflect a statistically significant difference between values.

3. Results

3.1. Sensitivity of Different FAW Populations to Vip3A Protein

Table 2 lists dose-mortality data for FAW populations exposed to Bt Vip3A. Among the 11 FAW populations, the LC50 values ranged from 11.42 ng/cm2 (Nanchang2021) to 88.33 ng/cm2 (Dehong2021), and the GIC50 values ranged from 1.43 ng/cm2 (Langfang2021) to 14.86 ng/cm2 (Jinan2021). There were significant differences in susceptibility among some of the populations involved. The fold difference between the most susceptible and least susceptible populations was 7.73 (for LC50) and 10.39 (for GIC50).

3.2. Sensitivity of Different FAW Populations to Cry1F Protein

Table 3 lists the sensitivities of 11 FAW populations exposed to Cry1F. The LC50 values ranged from 111.21 ng/cm2 (Jinan2021) to 517.33 ng/cm2 (Langfang2021), and the GIC50 values ranged from 2.35 ng/cm2 (Nanchang2022) to 138.97 ng/cm2 (Dehong2021). The fold difference between the most susceptible and most tolerant populations with respect to LC50 and GIC50 was 4.65 and 59.14, respectively.

3.3. Sensitivities of Different FAW Populations to Cry1Ab Protein

As for Cry1Ab, the LC50 values for the 11 FAW populations ranged from 135.76 ng/cm2 (Yuanyan2021) to 1108.47 ng/cm2 (Tongzhou2022), and the GIC50 values ranged from 1.58 ng/cm2 (Sanya2022) to 464.86 ng/cm2 (Tongzhou2022) (Table 4). The fold difference between the most susceptible and least susceptible populations at the LC50 and GIC50 levels was 8.16 and 294.22, respectively.

3.4. Sensitivity of Different FAW Populations to Cry2Ab Protein

As for Cry2Ab, the LC50 values for the 11 FAW populations ranged from 994.42 ng/cm2 (Nangchan2021) to 5492.50 ng/cm2 (Dali2022), and the GIC50 values ranged from 24.17 ng/cm2 (Langfang2022) to 1266.07 ng/cm2 (Yuanyan2021) (Table 5). The fold difference between the most susceptible and most tolerant populations with respect to LC50 and GIC50 was 5.52 and 50.62 respectively.

3.5. Sensitivity Comparison of the Three Populations from the Same Location Collected in Different Years

We also compared the sensitivity of the three populations (Sanya, Nanchang, and Langfang) collected from the same locations in different years. The LC50 values of the three populations of the four proteins in 2022 did not increase or decrease simultaneously when compared with those of 2021 (Figure 2). There were no significant differences between most of the LC50 values of the same protein for the different years except those of Vip3A (Sanya), Cry1F (Langfang), and Cry1Ab (Langfang).

3.6. Sensitivity Comparison among the Four Bt Proteins

We next compared the sensitivity differences among the four Bt proteins (Figure 3). The mean ± SE values of LC50 for all 11 FAW populations for each Bt protein were as follows: 44.00 ± 8.05 ng/cm2 (Vip3A), 275.88 ± 37.53 (Cry1F), 502.73 ± 102.17 (Cry1Ab), and 2381.87 ± 130.05 (Cry2Ab), and the corresponding GIC50 values were 6.80 ± 1.55, 37.32 ± 3.75, 86.86 ± 49.94, and 278.67 ± 30.92 ng/cm2. Significant differences were apparent among the average LC50 or GIC50 values for the four Bt proteins (Figure 3). The lethal effects and growth inhibition effects of the four Bt proteins on FAW were in the same order: Vip3A > Cry1F > Cry1Ab > Cry2Ab.

4. Discussion

Using genetically modified crops is one of the most effective ways of controlling FAW in the Western Hemisphere. Results from Chinese researchers showed that the larval density, the percentage of damaged plants, and the average damage ratings of GM corn (expressing Cry1Ab) were significantly lower than those of the control group [32]. At present, insect-resistant corn used to control FAW mainly expresses Cry1 proteins such as Cry1Ab, Cry1A.105, and Cry1F, Cry2 proteins such as Cry2Ab, or Vip3 proteins such as Vip3Aa [9,10,11,12,13]. Although some of these proteins have been expressed alone, they are now typically expressed in combinations with each other. Therefore, in the present study, we evaluated the sensitivity of FAW to these four commonly used and likely commercially applicable Bt proteins in China. China has six main corn production regions [29], and we collected 11 FAW populations from four of these regions (Table 1), which together comprise more than 90% of the total corn acreage of China. A diet incorporation assay [15,17,25,33] or surface overlay bioassay [11,18,34,35,36,37,38,39] is generally used to determine the sensitivity of FAW to Bt proteins. In our present study, we evaluated the sensitivity of 11 FAW populations to four Bt proteins based on results from a diet surface overlay method.
Among the various FAW populations we tested, the LC50 values for Vip3A, Cry1F, Cry1Ab, and Cry2Ab proteins ranged from 11.42 to 88.33, 111.21 to 517.33, 135.76 to 1108.47, and 994.42 to 5492.50 ng/cm2, respectively, representing fold differences of 7.73, 4.65, 8.16, and 5.52 among several populations. This indicated clear inter-population variation in susceptibility to the same Bt protein. In fact, variations between FAW populations [13,14,25,39]—and between certain populations of other Lepidoptera pests [40,41]—have been frequently reported. For example, the median effective concentration (i.e., EC50) of Cry1Ab in field populations of FAW in Brazil was reported to range from 0.30 to 3.67 µg/mL, implying a 12.23-fold difference among populations [14]. The LC50 for Vip3Aa20 varied from 92.38 to 611.65 ng/cm2, implying a 6.6-fold difference among populations [22]. It was assumed that the broad range of EC50 and LC50 values reflects natural variability among populations rather than selection pressure [25,41].
In our study, the smallest and largest LC50 values for Vip3A among the different FAW populations were 11.42 (range 4.59–21.30) and 88.33 (41.64–139.19) ng/cm2, respectively. Some studies reported that the LC50 values for the most Vip3A-sensitive FAW population ranged from 8.96 to 611.65 ng/cm2 [21,22,42,43]. Compared with values in this range, our FAW populations were highly susceptible to Vip3A.
Based on reported studies, the LC50 values for Cry1F ranged from 10.64 to 420 ng/cm2 among susceptible FAW populations [11,18,35,36,37,38,39,43]. In our present study, the smallest and largest LC50 values for Cry1F were 111.21 (range 49.42–196.63) and 308.56 (209.88–406.54) ng/cm2, respectively, which fall within the aforementioned reported range; this indicates that the FAW populations we studied were also susceptible to Cry1F.
Xu et al. measured the susceptibility of FAW populations collected from different planting areas of the Anhui Province of China to Cry1Ab, and the LC50 values ranged from 17.99 to 537.60 ng/cm2 [39]. Results from Ingber et al. indicated that LC50 values for Cry1Ab exceeded 2000 ng/cm2 with two “corn” strain FAW populations, whereas Cry1Ab LC50 values for the rice strain and their hybrid populations ranged from 1341 to 1912 ng/cm2 [44]. In our present study, the LC50 values for Cry1Ab ranged from 135.76 to 1108.47 ng/cm2, which is consistent with the aforementioned ranges. Many reports have confirmed that Cry1Ab has relatively low toxicity for Noctuidae pests such as FAW, which generally is not regarded as a target pest for this Bt protein [45,46]. For example, Bt corn hybrids such as “Bt11”, “Bt176”, and “MON810”, which express Cry1Ab, are highly toxic to the corn borer, with field control efficiencies exceeding 99%; however, these hybrids also can help control FAW by reducing the damage rate of corn at the heart-leaf stage by 90% and at the ear stage by 50–80% [47,48].
As for Cry2Ab, the reported LC50 values for susceptible FAW populations ranged from 160.35 to 840 ng/cm2 [15,36,43]. In the present study, the LC50 values for Cry2Ab ranged from 994.42 to 5492.50 ng/cm2. Thus, the Cry2Ab LC50 values measured in our study are larger than those reported previously. The difference may be attributable to differences in the activity of Cry2Ab from different sources.
Our results also revealed that the lethality and growth inhibition effects of the four Bt proteins on FAW were in the same order, i.e., Vip3A > Cry1F > Cry1Ab > Cry2Ab. Li et al. determined the lethality and growth inhibition effects of five Bt proteins on FAW collected from Yunnan province and found that the relative lethality was Vip3A > Cry1Ab > Cry1F > Cry2Ab > Cry1Ac and that growth inhibition was Cry1Ab > Cry1F > Vip3A > Cry1Ac > Cry2Ab [41]. Our results are partially consistent with these results. Many reports have confirmed that Cry1Ab has relatively low toxicity toward Noctuidae pests such as FAW [43,44], whereas Cry1F is more toxic and thus can better control FAW [12]. Xu et al. [39] and Zhang et al. [49] conducted a bioassay on a susceptible FAW population and found that the activity of Cry1F was superior to that of Cry1Ab. Thus, their results tend to support ours.
In summary, our results indicate that Vip3A, Cry1F, Cry1Ab, and Cry2Ab are clearly effective for controlling FAW, yet their effectiveness varied among different FAW populations. Based on reported LC50 values for Bt proteins toward susceptible and resistant FAW populations, we infer that the FAW populations tested in the present study are indeed susceptible to Vip3A, Cry1F, and Cry1Ab. To date, there has been no report of the emergence of Bt-resistant FAW populations in China [25,39,43]. Existing studies suggest that the population of FAWs that invaded China is likely to have originated from the United States [32], and this population is relatively sensitive to Bt biopesticides and Bt plants [32,50].
Based on the experience of Bt corn planting and FAW control in countries other than China, a multi-gene strategy should be followed to avoid planting corn hybrids that express a single Bt gene, especially Bt corn that only expresses Cry1Ab [14]. Multivalent Bt maize with a high-dose expression of Cry1 and Vip3A should be planted to control the number of FAWs at their source. The FAW has completed the colonization process in China and surrounding Southeast Asian countries. Bt corn or Bt cotton has been approved for planting in Vietnam, the Philippines, Myanmar, and other FAW source countries. If FAW develops resistance locally, individuals with resistance genes will likely invade the southern corn-producing areas of China, which is bound to pose a threat to the effectiveness and yield of Bt maize in China. Therefore, we recommend that the Bt protein bioassay be augmented for use in assessing the effectiveness of Bt proteins and that a unified resistance monitoring standard be formulated to facilitate the continued monitoring of the sensitivity of different geographical populations of FAWs to different Bt proteins and the frequency of the appearance of resistance genes [4], which will have important theoretical and practical significance for the rational layout and long-term use of transgenic corn in China.

Author Contributions

X.C. and J.X. conceived and designed the experiment; Y.Z. performed most of the experiment; C.H. and Y.C., performed some of the experiment; Y.Z. and C.H. analyzed the data; X.C. wrote the manuscript; Y.C., C.H., L.H. and J.X. reviewed and edited the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Science and Technology Innovation 2030-Major projects on Agricultural Biotechnology Breeding (Construction of Environmental Safety Evaluation Support System) and the Scientific and Technological Innovation Project of the Chinese Academy of Agricultural Science.

Data Availability Statement

All data generated or analyzed during this study are included in this published article.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Todd, E.L.; Poole, R.W. Keys and illustrations for the armyworm moths of the noctuid genus Spodoptera Guenée from the western hemisphere. Ann. Entomol. Soc. Am. 1980, 6, 722–738. [Google Scholar] [CrossRef]
  2. Montezano, D.G.; Specht, A.; Sosa-Gómez, D.R.; Roque-Specht, V.F.; Sousa-Silva, J.C.; Paula-Moraes, S.V.; Peterson, J.A.; Hunt, T.E. Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas. Afr. Entomol. 2018, 26, 286–300. [Google Scholar] [CrossRef]
  3. FAO. Integrated Management of the Fall Armyworm on Maize; Food and Agriculture Organization of the United Nations: Rome, Italy, 2017. [Google Scholar]
  4. Wu, K.M. Management strategies of fall armyworm (Spodoptera frugiperda) in China. Plant Prot. 2020, 46, 1–5. [Google Scholar]
  5. Zhang, L.; Jin, M.H.; Zhang, D.D.; Jiang, Y.Y.; Liu, J.; Wu, K.M.; Xiao, Y.T. Molecular identification of invasive fall armyworm Spodoptera frugiperda in Yunan province. Plant Prot. 2019, 45, 19–24. [Google Scholar]
  6. Van den Berg, J.; Prasanna, B.M.; Midega, C.A.O.; Ronald, P.C.; Carrière, Y.; Tabashnik, B.E. Managing fall armyworm in Africa: Can Bt maize sustainably improve control? J. Econ. Entomol. 2021, 114, 1934–1949. [Google Scholar] [CrossRef]
  7. Gutirrez-Moreno, R.; Mota-Sanchez, D.; Blanco, C.A.; Whalon, M.E.; Terán-Santofimio, H.; Rodriguez-Maciel, J.C.; Difonzo, C. Field-evolved resistance of the fall armyworm (Lepidoptera: Noctuidae) to synthetic insecticides in Puerto Rico and Mexico. J. Econ. Entomol. 2019, 112, 792–802. [Google Scholar] [CrossRef]
  8. Zhang, D.D.; Xiao, Y.T.; Xu, P.J.; Yang, X.M.; Wu, Q.L.; Wu, K.M. Insecticide resistance monitoring for the invasive populations of fall armyworm, Spodoptera frugiperda in China. J. Integr. Agric. 2021, 20, 783–791. [Google Scholar] [CrossRef]
  9. Buntin, G.D. Assessment of experimental Bt events against fall armyworm and corn earworm in field corn. J. Econ. Ento. 2004, 97, 259–264. [Google Scholar] [CrossRef]
  10. Siebert, M.; Leonard, S.; Stewart, J. Evaluation of corn hybrids expressing Cry1F, cry1A.105, Cry2Ab2, Cry34Ab1/Cry35Ab1, and Cry3Bb1 against southern United States insect pests. Econ. Entomol. 2012, 105, 1825–1834. [Google Scholar] [CrossRef]
  11. Storer, N.P.; Babcock, J.M.; Schlenz, M.; Meade, T.; Thompson, G.D.; Bing, J.W.; Huckaba, R.M. Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. J. Econ. Entomol. 2010, 103, 1031–1038. [Google Scholar] [CrossRef]
  12. Buntin, G.D. Corn expressing Cry1Ab or Cry1F endotoxin for fall armyworm and corn earworm management in field corn for grain production. FLA Entomol. 2008, 91, 523–530. [Google Scholar]
  13. Bernardi, O. Biological activity of Bt proteins expressed in different structures of transgenic corn against Spodoptera frugiperda. Ciênc. Rural 2016, 46, 1019–1024. [Google Scholar] [CrossRef]
  14. Omoto, C.; Bernardi, O.; Salmeron, E.; Sorgatto, R.J.; Dourado, P.M.; Crivellari, A.; Carvalho, R.A.; Willse, A.; Martinelli, S.; Head, G.P. Field-evolved resistance to Cry1Ab maize by Spodoptera frugiperda in Brazil. Pest Manag. Sci. 2016, 72, 1727–1736. [Google Scholar] [CrossRef]
  15. Yang, F.; Kerens, D.L.; Head, G.P.; Price, P.; Huang, F. Cross-Resistance to purified Bt proteins, Bt corn and Bt cotton in a Cry2Ab2-corn resistant strain of Spodoptera frugiperda. Pest Manag. Sci. 2017, 73, 2495–2503. [Google Scholar] [CrossRef]
  16. Storer, N.P. Status of resistance to Bt maize in Spodoptera frugiperda: Lessons from Puerto Rico. Invertebr. Pathol. 2012, 110, 294–300. [Google Scholar] [CrossRef]
  17. Farias, J.R.; Andow, D.A.; Horikoshi, R.J.; Sorgatto, R.J.; Fresia, P.; Dos Santos, A.C.; Omoto, C. Field-Evolved resistance to Cry1F maize by Spodoptera frugiperda (Lepidoptera: Noctuidae) in Brazil. Crop Prot. 2014, 64, 150–158. [Google Scholar] [CrossRef]
  18. Chandrasena, D.I.; Signorini, A.M.; Abratti, G.; Storer, N.P.; Olaciegui, M.L.; Alves, A.P.; Pilcher, C.D. Characterization of field-evolved resistance to Bacillus thuringiensis-derived Cry1F δ-Endotoxin in Spodoptera frugiperda populations from Argentina. Pest Manag. Sci. 2018, 74, 746–754. [Google Scholar] [CrossRef]
  19. Li, G.P.; Reifig, D.; Miao, J.; Gould, F.; Huang, F.N.; Feng, H.Q. Frequency of Cry1F non-recessive resistance alleles in North Carolina field populations of Spodoptera frugiperda (Lepidoptera: Noctuidae). PLoS ONE 2016, 11, e0154492. [Google Scholar] [CrossRef]
  20. Fatoretto, J.C.; Michel, A.P.; Filho, M.C.S.; Silva, N. Adaptive potential of fall armyworm (Lepidoptera: Noctuidae) limits bt trait durability in Brazil. J. Integr. Pest Manag. 2017, 8, 17. [Google Scholar] [CrossRef]
  21. Wen, Z.; Conville, J.; Matthews, P.; Hootman, T.; Himes, J.; Wong, S.; Huang, F.; Ni, X.; Chen, J.S.; Bramlett, M. More than 10 years after commercialization, Vip3A-expressing MIR162 remains highly efficacious in controlling major lepidopteran maize pests: Laboratory resistance selection versus field reality. Pestic. Biochem. Physiol. 2023, 192, 105385. [Google Scholar] [CrossRef]
  22. Bernardi, O.; Bernardi, D.; Ribeiro, R.S.; Okuma, D.M.; Salmeron, E.; Fatoretto, J.; Medeiros, F.C.L.; Burd, T.; Omoto, C. Frequency of resistance to Vip3Aa20 toxin from Bacillus thuringiensis in Spodoptera frugiperda (Lepidoptera: Noctuidae) populations in Brazil. Crop Prot. 2015, 76, 7–14. [Google Scholar] [CrossRef]
  23. Zhang, D.D.; Wu, K.M. The bioassay of Chinese domestic Bt-Cry1Ab and Bt-(Cry1Ab+Vip3Aa) maize against the fall armyworm (Spodoptera frugiperda). Plant Prot. 2019, 45, 54–60. [Google Scholar]
  24. Liang, J.G.; Zhang, D.D.; Li, D.Y.; Zhao, S.Y.; Wang, C.Y.; Xiao, Y.T.; Xu, D.; Yang, Y.Z.; Li, G.P.; Wang, L.L.; et al. Expression profiles of Cry1Ab protein and its insecticidal efficacy against the invasive Fall Armyworm for Chinese domestic GM maize DBN9936. J. Integr. Agric. 2021, 20, 792–803. [Google Scholar] [CrossRef]
  25. Wang, W.; Zhang, D.; Zhao, S.; Wu, K. Susceptibilities of the invasive fall armyworm (Spodoptera frugiperda) to the insecticidal proteins of Bt maize in China. Toxins 2022, 14, 507. [Google Scholar] [CrossRef]
  26. Hu, J.; Ding, D.; Bai, S.Y.; Jing, T.X.; Yang, Y.Z. Effect of two transgenic maize on population increase of Spodoptera frugiperda. J. Yangzhou Univ. Agric. Life Sci. Ed. 2023, 44, 75–81. [Google Scholar]
  27. Tabashnik, B.E.; Mota-Scanchez, D.; Whalon, M.E.; Hollingworth, R.M.; Carrière, Y. Defining terms for proactive management of resistance to Bt crops and pesticides. J. Econ. Entomol. 2014, 107, 496–507. [Google Scholar] [CrossRef]
  28. Tabashnik, B.E.; Carrière, Y. Surge in insect resistance to transgenic crops and prospects for sustainability. Nat. Biotechnol. 2017, 35, 926–935. [Google Scholar] [CrossRef]
  29. Yue, D.R. Quality Zoning and Industrial Layout of Corn in China; China Agriculture Press: Beijing, China, 2004. [Google Scholar]
  30. Liang, G.M.; Tan, W.J.; Guo, Y.Y. Improvement of artificial feeding technology of cotton bollworm. Plant Prot. 1999, 25, 16–18. [Google Scholar]
  31. Robertson, J.L.; Preisler, H.K.; Russell, R.M. PoloPlus, Probit and Logit Analysis: User’s Guide, version 1.0, LeOra Software: Petaluma, CA, USA, 2003.
  32. Zhang, L.; Liu, B.; Zheng, W.; Liu, C.; Zhang, D.; Zhao, S.; Li, Z.; Xu, P.; Wilson, K.; Withers, A.; et al. Genetic structure and insecticide resistance characteristics of fall armyworm populations invading China. Mol. Ecol. Resour. 2020, 20, 1682–1696. [Google Scholar] [CrossRef]
  33. Huang, F.N.; Qureshi, J.A.; Meagher, R.L., Jr.; Reisig, D.D.; Head, G.P.; Andow, D.A.; Ni, X.Z.; Kerns, D.; Buntin, G.D.; Niu, Y.; et al. Cry1F resistance in fall armyworm Spodoptera frugiperda: Single gene versus pyramided Bt maize. PLoS ONE 2014, 9, e112958. [Google Scholar] [CrossRef]
  34. Leite, N.A.; Mendes, S.M.; Santos-Amaya, O.F.; Santos, C.A.; Teixeira, T.P.M.; Guedes, R.N.C.; Pereira, E.J.G. Rapid selection and characterization of Cry1F resistance in a Brazilian strain of fall armyworm. Entomol. Exp. Appl. 2016, 158, 236–247. [Google Scholar] [CrossRef]
  35. Flagel, L.; Lee, Y.W.; Wanjugi, H.; Swarup, S.; Brown, A.; Wang, J.; Kraft, E.; Greenplate, J.; Simmons, J.; Adams, N.; et al. Mutational disruption of the ABCC2 gene in fall armyworm, Spodoptera frugiperda, confers resistance to the Cry1Fa and Cry1A.105 insecticidal proteins. Sci. Rep. 2018, 8, 7255. [Google Scholar] [CrossRef]
  36. Figueiredo, C.S.; Lemes, A.R.N.; Sebastião, I.; Desidério, J.A. Synergism of the Bacillus thuringiensis Cry1, Cry2, and Vip3 proteins in Spodoptera frugiperda control. Appl. Biochem. Biotechnol. 2019, 188, 798–809. [Google Scholar] [CrossRef]
  37. Rivero-Borja, M.; Rodríguez-Maciel, J.C.; Urzúa Gutiérrez, J.A.; Silva-Aguayo, G.; Chandrasena, D.I.; Felix-Bermudez, N.C.; Storer, N.P. Baseline of susceptibility to the Cry1F protein in Mexican populations of fall armyworm. J. Econ. Entomol. 2020, 113, 390–398. [Google Scholar] [CrossRef]
  38. Abdelgaffar, H.; Perera, O.P.; Jurat-Fuentes, J.L. ABC transpoter mutations in Cry1F-resistant Spodoptera frugiperda do not result in altered susceptibility to selected samll molecule pesticides. Pest Manag. Sci. 2021, 77, 949–955. [Google Scholar] [CrossRef]
  39. Xu, T.T.; Wang, Y.Q.; Hu, F.; Bi, S.J.; Hu, B.J.; Wang, Z.Y.; Xu, L.N. Susceptibility of different geographical populations of fall armyworm Spodoptera frugiperda in Anhui Province to Bt proteins. J. Plant Prot. 2022, 49, 1521–1527. [Google Scholar]
  40. Siegfried, B.D.; Spencer, T.; Nearman, J. Baseline susceptibility of the corn earworm (Lepidoptera: Noctuidae) to the Cry1Ab toxin from Bacillus thuringiensis. J. Econ. Entomol. 2000, 93, 1265–1268. [Google Scholar] [CrossRef]
  41. He, K.; Wang, Z.; Wen, L.; Bai, S.; Ma, X.; Yao, Z. Determination of baseline susceptibility to Cry1Ab protein for Asian corn borer (Lep., Crambidae). J. Appl. Entomol. 2005, 129, 407–412. [Google Scholar] [CrossRef]
  42. Yang, F.; Morsello, S.; Head, G.P.; Sansone, C.; Huang, F.; Gilreath, R.T.; Kerns, D.L. F2 screen, ingeritance and cross-resistance of field derived Vip3A resistance in Spodoptera frugiperda collected from Louisiana USA. Pest Manag. Sci. 2018, 74, 1769–1778. [Google Scholar] [CrossRef]
  43. Li, G.P.; Ji, T.J.; Sun, X.X.; Jiang, Y.Y.; Wu, K.M.; Feng, H.Q. Susceptibility evaluation of invaded Spodoptera frugiperda population in Yunnan province to five Bt proteins. Plant Prot. 2019, 45, 15–20. [Google Scholar]
  44. Ingber, D.A.; Mason, C.E.; Flexner, L. Cry1 Bt susceptibilities of fall armyworm (Lepidoptera: Noctuidae) host strains. J. Econ. Entomol. 2018, 111, 361–368. [Google Scholar] [CrossRef] [PubMed]
  45. Luttrell, R.G.; Wan, L.; Knighten, K. Variation in susceptibility of Noctuid (Lepidoptera) larvae attacking cotton and soybean to purified endotoxin proteins and commercial formulations of Bacillus thuringiensis. J. Econ. Entomol. 1999, 92, 21–32. [Google Scholar] [CrossRef]
  46. Archer, T.L.; Patrick, C.; Schuster, G.; Cronholm, G.; Bynum, E.D., Jr.; Morrison, W.P. Ear and shank damage by corn borers and corn earworms to four events of Bacillus thuriengiensis transgenic maize. Crop Prot. 2001, 20, 139–144. [Google Scholar] [CrossRef]
  47. Buntin, G.D.; Lee, R.D.; Willson, D.M.; McPherson, R.M. Evaluation of yieldgard transgenic resistance for control of fall armywom and corn earworm (Lepidoptera: Noctuidae) on corn. FLA Entomol. 2001, 84, 37–42. [Google Scholar] [CrossRef]
  48. Buntin, G.D. Corn expressing CrylAb endotoxin for management of fall armywom and corn earwrorm (Lepidoptera: Noctuidae) in silage production. J. Entomol. Sci. 2010, 45, 283–295. [Google Scholar]
  49. Zhang, J.F.; Jin, M.H.; Yang, Y.C.; Liu, L.L.; Yang, Y.B.; Gómez, I.; Bravo, A.; Soberón, M.; Xiao, Y.T.; Liu, K.Y. The cadherin protein is not involved in susceptibility to Bacillus thuringiensis Cry1Ab or Cry1Fa toxins in Spodoptera frugiperda. Toxins 2020, 12, 375. [Google Scholar] [CrossRef]
  50. Guan, F.; Zhang, J.; Shen, H.; Wang, X.; Padovan, A.; Walsh, T.K.; Tay, W.T.; Gordon, K.H.J.; James, W.; Czepak, C.; et al. Wholegenome sequencing to detect mutations associated with resistance to insecticides and Bt proteins in Spodoptera frugiperda. Insect Sci. 2021, 28, 627–638. [Google Scholar] [CrossRef]
Agronomy 13 02415 g001
Figure 1. Corn production regions and sampling locations where FAWs were collected. Percentage of corn grown in each region for the total area: I. Northern Spring Corn Region, 30%; Ⅱ. Huang–Huai–Hai Summer Corn Region, 40%; Ⅲ: Southwest Hilly Corn Region, 20%; Ⅳ: Southern Hilly Corn Region, 5%; Ⅴ. Northwest Inland Corn Region, 3%; and Ⅵ. Qiang-Zang Plateau Corn Region, 2%. 1. Dehong; 2. Dali; 3. Sanya; 4. Nanchang; 5. Yuanyan; 6. Jinan; 7. Langfang; 8. Tongzhou.
Figure 1. Corn production regions and sampling locations where FAWs were collected. Percentage of corn grown in each region for the total area: I. Northern Spring Corn Region, 30%; Ⅱ. Huang–Huai–Hai Summer Corn Region, 40%; Ⅲ: Southwest Hilly Corn Region, 20%; Ⅳ: Southern Hilly Corn Region, 5%; Ⅴ. Northwest Inland Corn Region, 3%; and Ⅵ. Qiang-Zang Plateau Corn Region, 2%. 1. Dehong; 2. Dali; 3. Sanya; 4. Nanchang; 5. Yuanyan; 6. Jinan; 7. Langfang; 8. Tongzhou.
Agronomy 13 02415 g001
Agronomy 13 02415 g002
Figure 2. Sensitivity comparison of the 3 populations from the same locations collected in different years. The difference between LC50 values was considered significant if the 95% fiducial limits of the values did not overlap. The data of the 95% fiducial limits are shown in Table 2, Table 3, Table 4 and Table 5. N.S., not significant. An asterisk indicates a significant difference between two groups.
Figure 2. Sensitivity comparison of the 3 populations from the same locations collected in different years. The difference between LC50 values was considered significant if the 95% fiducial limits of the values did not overlap. The data of the 95% fiducial limits are shown in Table 2, Table 3, Table 4 and Table 5. N.S., not significant. An asterisk indicates a significant difference between two groups.
Agronomy 13 02415 g002
Agronomy 13 02415 g003
Figure 3. Mean ± SE values of LC50 and GIC50 for 11 FAW populations for four Bt proteins. Different letters indicate significant differences among LC50 values (uppercase letters) and among GIC50 values (lowercase letters) for different Bt proteins (p < 0.05, Duncan’s test).
Figure 3. Mean ± SE values of LC50 and GIC50 for 11 FAW populations for four Bt proteins. Different letters indicate significant differences among LC50 values (uppercase letters) and among GIC50 values (lowercase letters) for different Bt proteins (p < 0.05, Duncan’s test).
Agronomy 13 02415 g003
Table 1. Collection information for the studied FAW populations from corn fields in primary corn production regions in China.
Table 1. Collection information for the studied FAW populations from corn fields in primary corn production regions in China.
LocationCoordinatesMap Ref. No.Collection DateNo. of Larvae Collected
Production RegionProvinceCity
Southwest Hilly Corn RegionYunnanDehong24.01° N, 97.82° E1August 2021120
Dali25.23° N, 100.24° E2May 2022183
Southern Hilly Corn RegionHainanSanya18.38° N, 109.20° E3July 2021, July 2022159, 188
JiangxiNanchang28.33° N, 115.56° E4August 2021, August 2022239
Huang–Huai–Hai Summer Corn RegionHenanYuanyan35.06° N, 113.96° E5August 2021130
ShandongJinan36.39° N, 117.01° E6August 2021218
Northern Spring Corn RegionHebeiLangfang39.53° N, 116.70° E7September 2021, July 202276, 65
BeijingTongzhou39.90° N, 116.65° E8September 2022138
Table 2. Susceptibility of S. frugiperda populations in different regions to Vip3A protein.
Table 2. Susceptibility of S. frugiperda populations in different regions to Vip3A protein.
PopulationN *LC50 (95% FL, ng/cm2) §Slope ± SEχ2GIC50 (95% FL, ng/cm2) §Slope ± SEχ2
Dehong202172088.33 (41.64–139.19) a2.42 ± 0.3219.112.36 (1.21–3.79) de0.85 ± 0.087.08
Dali202272046.52 (24.54–79.45) abc1.88 ± 0.1828.267.05 (4.12–10.54) abc1.26 ± 0.0819.96
Sanya202172061.94 (40.34–86.91) ab2.49 ± 0.2514.384.91 (0.37–13.34) abcde0.78 ± 0.0756.65
Sanya202272013.63 (7.75–19.05) e2.70 ± 0.3510.0913.66 (8.27–21.40) ab1.64 ± 0.1041.14
Nangchan202172011.42 (4.59–21.30) ce1.28 ± 0.1033.037.37 (4.70–10.49) abc1.07 ± 0.0814.91
Nanchang202272051.07 (20.81–77.24) abc3.91 ± 0.5524.441.94 (0.40–4.25) de0.88 ± 0.0822.08
Yuanyan202172068.07(39.44–96.71) ab2.25 ± 0.3010.422.09 (0.98–3.51) de1.24 ± 0.097.28
Jinan202172020.12 (9.62–33.40) cde1.96 ± 0.1729.4614.86 (9.16–22.53) a1.43 ± 0.0930.96
Tongzhou202272073.83 (43.91–122.63) a1.07 ± 0.137.1914.03 (6.35–25.03) ac0.66 ± 0.0617.06
Langfang202172025.73 (11.10–42.78) bcde1.70 ± 0.1720.711.43 (0.77–2.21) e0.96 ± 0.105.75
Langfang202272023.30 (7.26–40.11) cde1.75 ± 0.2314.335.06 (2.80–7.76) cd0.98 ± 0.0712.11
* Total number of larvae tested in the bioassay. § Values followed by different letters within the same column imply statistically significant differences (p < 0.05). 95% FL, 95% fiducial limits; LC50, 50% lethal concentration; GIC50, 50% growth inhibition concentration.
Table 3. Susceptibility of S. frugiperda populations in different regions to Cry1F protein.
Table 3. Susceptibility of S. frugiperda populations in different regions to Cry1F protein.
PopulationN *LC50 (95% FL, ng/cm2) §Slope ± SEχ2GIC50 (95% FL, ng/cm2) §Slope ± SEχ2
Dehong2021720262.11 (109.78–469.77) abc1.16 ± 0.148.77138.97 (26.27–316.84) a0.81 ± 0.1435.41
Dali2022720174.71 (96.42–289.03) bc1.19 ± 0.0922.903.24 (0.25–10.61) bc0.65 ± 0.0810.59
Sanya2021720347.64 (196.91–547.35) ab1.38 ± 0.1214.502.50 (0.14–9.38) bc0.53 ± 0.0710.52
Sanya2022720445.59 (75.93–1017.25) abc1.03 ± 0.1422.4667.65 (35.92–108.02) a0.82 ± 0.0713.59
Nangchan2021720281.19 (185.73–382.71) abc1.61 ± 0.194.1882.83 (41.98–137.16) a1.21 ± 0.0833.45
Nanchang2022720232.56 (61.70–551.02) abc0.93 ± 0.0928.422.35 (0.25–7.86) c0.65 ± 0.086.39
Yuanyan2021720141.23 (51.50–283.01) bc1.13 ± 0.0933.1617.05 (7.54–29.55) abc0.76 ± 0.077.57
Jinan2021720111.21 (49.42–196.63) c1.22 ± 0.1118.6642.73 (8.91–80.74) ab1.07 ± 0.0855.98
Tongzhou2022720308.56 (209.88–406.54) ab2.24 ± 0.267.8427.90 (7.66–57.27) abc0.77 ± 0.0720.52
Langfang2021720517.33 (379.99–699.84) a1.38 ± 0.113.8717.22 (9.94–25.94) b0.86 ± 0.085.83
Langfang2022720212.57 (122.11–336.49) bc1.08 ± 0.0910.048.09 (3.59–14.23) bc0.77 ± 0.085.30
* Total number of larvae tested in the bioassay. § Values followed by different letters within the same column imply statistically significant differences (p < 0.05). 95% FL, 95% fiducial limits; LC50, 50% lethal concentration; GIC50, 50% growth inhibition concentration.
Table 4. Susceptibility of S. frugiperda populations in different regions to Cry1Ab protein.
Table 4. Susceptibility of S. frugiperda populations in different regions to Cry1Ab protein.
PopulationN *LC50 (95% FL, ng/cm2) §Slope ± SEχ2GIC50 (95% FL, ng/cm2) §Slope ± SEχ2
Dehong2021720541.85 (273.04–1059.28) abc0.96 ± 0.1117.402.59 (0.25–8.88) b0.36 ± 0.064.88
Dali2022720434.79 (300.40–594.88) bc2.18 ± 0.1916.4314.22 (3.45–31.35) b0.71 ± 0.0714.31
Sanya2021720148.07 (68.38–255.29) de1.13 ± 0.128.8212.56 (3.28–27.40) b0.65 ± 0.0710.83
Sanya2022720179.58 (127.54–240.41) e1.82 ± 0.263.281.58 (0.038–7.65) b0.42 ± 0.684.83
Nangchan2021720758.16 (496.30–1039.59) ab1.40 ± 0.194.114.85 (0.10–34.08) b0.31 ± 0.079.12
Nanchang2022720697.35 (492.16–926.19) ab1.56 ± 0.231.5211.77 (1.33–33.58) b0.51 ± 0.086.66
Yuanyan2021720135.76 (71.85–212.63) e1.11 ± 0.118.4010.34 (0.99–35.52) b0.69 ± 0.104.88
Jinan2021720401.30 (240.87–642.05) bcd1.61 ± 0.1228.3631.72 (5.87–77.57) b0.70 ± 0.0812.41
Tongzhou20227201108.47 (780.35–1438.36) a2.15 ± 0.328.08464.86 (323.66–635.77) a0.90 ± 0.078.38
Langfang2021720943.00 (457.67–1474.74) ab1.61 ± 0.1217.64372.56 (203.35–602.15) a1.26 ± 0.0833.53
Langfang2022720181.74 (32.08–406.36) cde1.12 ± 0.1418.4628.36 (0.10–134.23) b0.60 ± 0.0628.46
* Total number of larvae tested in the bioassay. § Values followed by different letters within the same column imply statistically significant differences (p < 0.05). 95% FL, 95% fiducial limits; LC50, 50% lethal concentration; GIC50, 50% growth inhibition concentration.
Table 5. Susceptibility of S. frugiperda populations in different regions to Cry2Ab protein.
Table 5. Susceptibility of S. frugiperda populations in different regions to Cry2Ab protein.
PopulationN *LC50 (95% FL, ng/cm2) §Slope ± SEχ2GIC50 (95% FL, ng/cm2) §Slope ± SEχ2
Dehong20217202781.24 (1557.35–7184.05) abc1.27 ± 0.1718.35296.41 (178.72–440.95) bc0.85 ± 0.0710.69
Dali20227205492.50 (4087.30–9106.10) a1.86 ± 0.345.72304.57 (221.58–419.87) bc1.19 ± 0.0915.45
Sanya20217201008.61 (54.11–1357.48) de2.02 ± 0.297.46117.94 (82.22–161.32) de0.89 ± 0.068.16
Sanya20227201506.56 (1231.76–1776.26) cde2.95 ± 0.395.2367.33 (48.86–88.39) de1.14 ± 0.087.77
Nangchan2021720994.42 (725.19–1290.45) e2.86 ± 0.2814.3396.18 (67.49–118.71) de1.16 ± 0.088.42
Nanchang20227202380.72 (1033.92–4711.16) abcde1.81 ± 0.3615.22490.15 (326.75–693.32) b0.76 ± 0.067.74
Yuanyan20217204489.60 (2067.40–22081.00) ab1.02 ± 0.1025.671266.07 (877.72–1817.75) a1.27 ± 0.0730.75
Jinan20217203231.40 (1905.90–7364.20) ab1.10 ± 0.1014.55224.54 (52.33–493.20) bcd0.75 ± 0.0635.06
Tongzhou20227201409.79 (990.00–1871.47) cde1.59 ± 0.266.99152.95 (60.22–277.95) ce0.75 ± 0.0715.36
Langfang20217201089.20 (382.21–2194.60) cde1.19 ± 0.1719.4925.01 (6.42–54.09) df0.55 ± 0.0612.08
Langfang20227201816.53 (1350.92–2782.32) bcd2.17 ± 0.396.8624.17 (13.35–37.12) f0.77 ± 0.078.47
* Total number of larvae tested in the bioassay. § Values followed by different letters within the same column imply statistically significant differences (p < 0.05). 95% FL, 95% fiducial limits; LC50, 50% lethal concentration; GIC50, 50% growth inhibition concentration.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Zhou, Y.; Huang, C.; Chen, Y.; Han, L.; Xie, J.; Chen, X. Sensitivities of Fall Armyworm (Spodoptera frugiperda) Populations in Different Regions of China to Four Bt Proteins. Agronomy 2023, 13, 2415. https://doi.org/10.3390/agronomy13092415

AMA Style

Zhou Y, Huang C, Chen Y, Han L, Xie J, Chen X. Sensitivities of Fall Armyworm (Spodoptera frugiperda) Populations in Different Regions of China to Four Bt Proteins. Agronomy. 2023; 13(9):2415. https://doi.org/10.3390/agronomy13092415

Chicago/Turabian Style

Zhou, Yanfang, Chunmeng Huang, Yi Chen, Lanzhi Han, Jiajian Xie, and Xiuping Chen. 2023. "Sensitivities of Fall Armyworm (Spodoptera frugiperda) Populations in Different Regions of China to Four Bt Proteins" Agronomy 13, no. 9: 2415. https://doi.org/10.3390/agronomy13092415

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop