入侵云南草地贪夜蛾种群对5种常用Bt蛋白的敏感性评价
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摘要
草地贪夜蛾Spodoptera frugiperda(J. E. Smith)是原分布于美洲大陆热带和亚热带地区的一种重要玉米害虫。在当地,种植抗虫转基因玉米是防控草地贪夜蛾危害的主要手段。该虫于2019年1月入侵我国云南省,为明确入侵我国云南的草地贪夜蛾种群对常用Bt蛋白的敏感性水平,本文通过饲料表面涂抹法测定了瑞丽草地贪夜蛾幼虫对Cry1Ab、Cry1Ac、Cry1F、Cry2Ab以及Vip3A等5种Bt蛋白的敏感性。结果表明:几种常用Bt蛋白对瑞丽草地贪夜蛾致死作用顺序为Vip3A>Cry1Ab>Cry1F>Cry2Ab>Cry1Ac,对草地贪夜蛾抑制生长发育的顺序为Cry1Ab>Cry1F>Vip3A>Cry1Ac>Cry2Ab。此外,与美国相对敏感种群比较,云南瑞丽草地贪夜蛾种群对Cry1Ab、Cry1Ac、Cry1F、Cry2Ab和Vip3A的敏感性指标在0.28～3.76之间,表明该入侵种群对此5种Bt蛋白均未产生抗性。此研究可为将来建立以转Bt基因玉米作为防控草地贪夜蛾的技术体系提供依据。
The fall armyworm, Spodoptera frugiperda(J. E. Smith), is a native major pest of corn in the tropical-subtropical regions of the American continent. Planting transgenic hybrid maize expressing insecticidal protein is the main tool for fall armyworm control in this area. Since January 2019, it has invaded the western part of Yunnan province. In order to determine the susceptibility difference of this invaded fall armyworm population in Ruili of Yunnan province to five Bt proteins, we conducted the susceptibility bioassay to Cry1 Ab, Cry1 Ac, Cry1 F, Cry2 Ab and Vip3 A by using artificial diet overlay method. Based on the LC_(50) and GIC_(50) values, the descending order of lethal was ranked as follows: Vip3 A>Cry1 Ab>Cry1 F>Cry2 Ab>Cry1 Ac, and the descending order of growth inhibition was ranked as follows: Cry1 Ab>Cry1 F>Vip3 A>Cry1 Ac>Cry2 Ab. Compared with susceptible strain of fall armyworm population from USA, the sensitivity indexes of the invaded population to Cry1 Ab, Cry1 Ac, Cry1 F, Cry2 Ab, and Vip3 A proteins ranged from 0.28-3.76, indicating that this invaded population has not significantly developed to resistance to these five Bt proteins. This study will help to construct the strategy of planting transgenic Bt corn for controlling fall armyworm as one of main tactics in the future.
The fall armyworm, Spodoptera frugiperda(J. E. Smith), is a native major pest of corn in the tropical-subtropical regions of the American continent. Planting transgenic hybrid maize expressing insecticidal protein is the main tool for fall armyworm control in this area. Since January 2019, it has invaded the western part of Yunnan province. In order to determine the susceptibility difference of this invaded fall armyworm population in Ruili of Yunnan province to five Bt proteins, we conducted the susceptibility bioassay to Cry1 Ab, Cry1 Ac, Cry1 F, Cry2 Ab and Vip3 A by using artificial diet overlay method. Based on the LC_(50) and GIC_(50) values, the descending order of lethal was ranked as follows: Vip3 A>Cry1 Ab>Cry1 F>Cry2 Ab>Cry1 Ac, and the descending order of growth inhibition was ranked as follows: Cry1 Ab>Cry1 F>Vip3 A>Cry1 Ac>Cry2 Ab. Compared with susceptible strain of fall armyworm population from USA, the sensitivity indexes of the invaded population to Cry1 Ab, Cry1 Ac, Cry1 F, Cry2 Ab, and Vip3 A proteins ranged from 0.28-3.76, indicating that this invaded population has not significantly developed to resistance to these five Bt proteins. This study will help to construct the strategy of planting transgenic Bt corn for controlling fall armyworm as one of main tactics in the future.
引文
[1] SPARKS A N.A review of the biology of the fall armyworm[J].Florida Entomologist,1979,62(2):82-87.
[2] TODD E L,POOLE R W.Keys and illustrations for the armyworm moths of the noctuid genus Spodoptera Guenée from the Western Hemisphere [J].Annals of the Entomological Society of America,1980,73(6):722-738.
[3] PITRE H N.Relationship of fall armyworm (Lepidoptera:Noctuidae) from Florida,Honduras,Jamaica,and Mississippi:susceptibility to insecticides with reference to migration [J].Florida Entomologist,1988,71:56-61.
[4] CAPINERA J L.Fall armyworm,Spodoptera frugiperda (J E Smith) (Insecta:Lepidoptera:Noctuidae)[R].University of Florida Cooperative Extension Service,Institute of Food and Agricultural Sciences,EDIS,Gainsville,FL,2000.
[5] CASMUZE A,JUáREZ M L,SOCíAS M G,et al.Revisión de los hospederos del gusano cogollero del maíz,Spodoptera frugiperda (Lepidoptera:Noctuidae)[J].Revista de la Sociedad Entomológical Argentina,2010,69:209-231.
[6] GOERGEN G,KUMAR P L,SANKUNG S B,et al.First report of outbreaks of the fall armyworm Spodoptera frugiperda (J E Smith) (Lepidoptera,Noctuidae),a new alien invasive pest in west and central Africa[J/OL].PLoS ONE,2016,11(10):e0165632.
[7] (CABI) Centre for Agriculture and Bioscience International.CABI warns of rapid spread of crop-devastating fall armyworm across Asia [EB/OL].(2018-06-08).https://www.cabi.org/news-and-media/2018/cabi-warns-of-rapid-spreadof-crop-devastating-fall-armyworm-across-asia/.
[8] 姜玉英,刘杰,朱晓明.草地贪夜蛾侵入我国的发生动态和未来趋势分析[J].中国植保导刊,2019,39(2):33-35.
[9] 孙小旭,赵胜园,靳明辉,等.玉米田草地贪夜蛾幼虫的空间分布型与抽样技术[J].植物保护,2019,45(2):13-18.
[10] 张磊,靳明辉,张丹丹,等.入侵云南草地贪夜蛾的分子鉴定[J].植物保护,2019,45(2):19-24.
[11] 郭井菲,赵建周,何康来,等.警惕危险性害虫草地贪夜蛾入侵中国[J].植物保护,2018,44(6):1-10.
[12] HRUSKA A J,GLADSTONE S M.Effect of period and level of infestation of the fall armyworm,Spodoptera frugiperda,on irrigated maize yield [J].Florida Entomologist,1988,71:249-254.
[13] BLANCO C A,CHIARAVALLE W,DALLA-RIZZA M,et al.Current situation of pests targeted by Bt crops in Latin America[J].Current Opinion Insect Science,2016,15:131-138.
[14] (CABI) Centre for Agriculture and Bioscience International.New report reveals cost of fall armyworm to farmers in Africa,provides recommendations for control [EB/OL].2017.https://www.cabi.org/news-and-media/2017/new-report-reveals-cost-of-fall-armyworm-to-farmers-in-africa-providesrecommendations-for-control/.
[15] BLANCO C A,PORTILLA M,JURAT-FUENTES J L,et al.Susceptibility of isofamilies of Spodoptera frugiperda (Lepidoptera:Noctuidae) to Cry1Ac and Cry1Fa proteins of Bacillus thuringiensis [J].Southwestern Entomologist,2010,35:409-415.
[16] STORE N P,BABCOCK J M,SCHLENZ M,et al.Discovery and characterization of field resistance to Bt maize:Spodoptera frugiperda (Lepidoptera:Noctuidae) in Puerto Rico [J].Journal of Economic Entomology,2010,103:1031-1038.
[17] HUANG F,QURESHI J A,HEAD G P,et al.Frequency of Bacillus thuringiensis Cry1A.105 resistance alleles in field populations of the fall armyworm,Spodoptera frugiperda,in Louisiana and Florida [J].Crop Protection,2016,83:83-89.
[18] LI G,REISIG D,MIAO J,et al.Frequency of Cry1F non-recessive resistance alleles in North Carolina field populations of Spodoptera frugiperda (Lepidoptera:Noctuidae)[J/OL].PLoS ONE,2016,11:e0154492.
[19] NIU Y,QURESHI J A,NI X,et al.F2 screen for resistance to Bacillus thuringiensis Cry2Ab2-maize in field populations of Spodoptera frugiperda (Lepidoptera:Noctuidae) from the southern United States [J].Journal of Invertebrate Pathology,2016,138:66-72.
[20] CHANDRASENA D I,SIGNORINI A M,ABRATTI G,et al.Characterization of field-evolved resistance to Bacillus thuringiensis-derived Cry1F δ-endotoxin in Spodoptera frugiperda populations from Argentina [J].Pest Management Science,2018,74:746-754.
[21] VéLEZ A M,SPENCER T A,ALVES A P,et al.Inheritance of Cry1F resistance,cross resistance and frequency of resistant alleles in Spodoptera frugiperda (Lepidoptera:Noctuidae)[J].Bulletin of Entomological Research,2013,103:700-713.
[22] HARRISON F P.Oviposition and subsequent infestations of corn by fall armyworm [J].Florida Entomologist,1986,69:588-592.
[23] SIEBERT M W,TINDALL K V,LEONARD B R,et al.Evaluation of corn hybrids expressing Cry1F (Herculex? I Insect Protection) against fall armyworm (Lepidoptera:Noctuidae) in southern United States [J].Journal of Entomology Science,2008,43:41-51.
[24] ADAMCZYK J R,HOLLOWAY J J,LEONARD J W,et al.Susceptibility of fall armyworm collected from different plant hosts to selected insecticides and transgenic Bt cotton [J].Journal of Cotton Science,1997,1:21-28.
[25] YU S J,NGUYEN S N,ABO-ELGHAR G E.Biochemical characteristics of insecticide resistance in the fall armyworm,Spodoptera frugiperda (J.E.Smith)[J].Pesticide Biochemistry and Physiology,2003,77:1-11.
[26] BUNTIN G D.Corn expressing Cry1Ab or Cry1F endotoxin for fall armyworm and corn earworm (Lepidoptera:Noctuidae) management in field corn for grain production [J].Florida Entomologist,2008,91:523-530.
[27] SIEBERT M W,BABOCK J M,NOLTING S,et al.Efficacy of Cry1F insecticidal protein in maize and cotton for control of fall armyworm (Lepidoptera:Noctuidae)[J].Florida Entomologist,2008,91:555-565.
[28] HARDKE J T,LEONARD B R,HUANG F,et al.Damage and survivorship of fall armyworm (Lepidoptera:Noctuidae) on transgenic field corn expressing Bacillus thuringiensis Cry proteins [J].Crop Protection,2011,30:168-172.
[29] FARIAS J R,ANDOW D A,HORIKOSHI R J,et al.Field-evolved resistance to Cry1F maize by Spodoptera frugiperda (Lepidoptera:Noctuidae) in Brazil [J].Crop Protection,2014,64:150-158.
[30] HERNáNDEZ-RODRíGUEZ C S,HERNáNDEZ-MARTíNEZ P,VAN RIE J,et al.Shared midgut binding sites for Cry1A.105,Cry1Aa,Cry1Ab,Cry1Ac and Cry1Fa proteins from Bacillus thuringiensis in two important corn pests,Ostrinia nubilalis and Spodoptera frugiperda [J/OL].PLoS ONE,2013,8(7):e68164.
[31] GOUFFON C,VAN V A,VAN R J,et al.Binding sites for Bacillus thuringiensis Cry2Ae toxin on heliothine brush border membrane vesicles are not shared with Cry1A,Cry1F,or Vip3A toxin [J].Applied Environmental Microbiology,2011,77(10):3182-3188.
[32] BERNARDI O,BERNARDI D,AMADO D,et al.Resistance risk assessment of Spodoptera frugiperda (Lepidoptera:Noctuidae) and Diatraea saccharalis (Lepidoptera:Crambidae) to Vip3A20 insecticidal protein expressed in corn [J].Journal of Economic Entomology,2015,108(6):2711-2719.
[33] STORER N P,KUBISZAK M E,KING E,et al.Status of resistance to Bt maize in Spodoptera frugiperda:lessons from Puerto Rico [J].Journal of Invertebrate Pathology,2012,110:294-300.
[34] 江幸福,张蕾,程云霞,等.草地贪夜蛾迁飞行为与监测技术研究进展[J].植物保护,2019,45(1):12-18.
[35] DANGAL V,HUANG F.Fitness costs of Cry1F resistance in two populations of fall armyworm,Spodoptera frugiperda (J.E.Smith),collected from Puerto Rico and Florida [J].Journal of Invertebrate Pathology,2015,127:81-86.
[36] CAMARGO A M,CASTA?ERA P,FARINóS G P,et al.Comparative analysis of the genetic basis of Cry1F resistance in two strains of Spodoptera frugiperda originated from Puerto Rico and Florida [J].Journal of Invertebrate Pathology,2017,146:47-52.
[37] 吴秋琳,姜玉英,吴孔明,等.草地贪夜蛾缅甸虫源迁入中国的路径分析[J].植物保护,2019,45(2):1-6.
[2] TODD E L,POOLE R W.Keys and illustrations for the armyworm moths of the noctuid genus Spodoptera Guenée from the Western Hemisphere [J].Annals of the Entomological Society of America,1980,73(6):722-738.
[3] PITRE H N.Relationship of fall armyworm (Lepidoptera:Noctuidae) from Florida,Honduras,Jamaica,and Mississippi:susceptibility to insecticides with reference to migration [J].Florida Entomologist,1988,71:56-61.
[4] CAPINERA J L.Fall armyworm,Spodoptera frugiperda (J E Smith) (Insecta:Lepidoptera:Noctuidae)[R].University of Florida Cooperative Extension Service,Institute of Food and Agricultural Sciences,EDIS,Gainsville,FL,2000.
[5] CASMUZE A,JUáREZ M L,SOCíAS M G,et al.Revisión de los hospederos del gusano cogollero del maíz,Spodoptera frugiperda (Lepidoptera:Noctuidae)[J].Revista de la Sociedad Entomológical Argentina,2010,69:209-231.
[6] GOERGEN G,KUMAR P L,SANKUNG S B,et al.First report of outbreaks of the fall armyworm Spodoptera frugiperda (J E Smith) (Lepidoptera,Noctuidae),a new alien invasive pest in west and central Africa[J/OL].PLoS ONE,2016,11(10):e0165632.
[7] (CABI) Centre for Agriculture and Bioscience International.CABI warns of rapid spread of crop-devastating fall armyworm across Asia [EB/OL].(2018-06-08).https://www.cabi.org/news-and-media/2018/cabi-warns-of-rapid-spreadof-crop-devastating-fall-armyworm-across-asia/.
[8] 姜玉英,刘杰,朱晓明.草地贪夜蛾侵入我国的发生动态和未来趋势分析[J].中国植保导刊,2019,39(2):33-35.
[9] 孙小旭,赵胜园,靳明辉,等.玉米田草地贪夜蛾幼虫的空间分布型与抽样技术[J].植物保护,2019,45(2):13-18.
[10] 张磊,靳明辉,张丹丹,等.入侵云南草地贪夜蛾的分子鉴定[J].植物保护,2019,45(2):19-24.
[11] 郭井菲,赵建周,何康来,等.警惕危险性害虫草地贪夜蛾入侵中国[J].植物保护,2018,44(6):1-10.
[12] HRUSKA A J,GLADSTONE S M.Effect of period and level of infestation of the fall armyworm,Spodoptera frugiperda,on irrigated maize yield [J].Florida Entomologist,1988,71:249-254.
[13] BLANCO C A,CHIARAVALLE W,DALLA-RIZZA M,et al.Current situation of pests targeted by Bt crops in Latin America[J].Current Opinion Insect Science,2016,15:131-138.
[14] (CABI) Centre for Agriculture and Bioscience International.New report reveals cost of fall armyworm to farmers in Africa,provides recommendations for control [EB/OL].2017.https://www.cabi.org/news-and-media/2017/new-report-reveals-cost-of-fall-armyworm-to-farmers-in-africa-providesrecommendations-for-control/.
[15] BLANCO C A,PORTILLA M,JURAT-FUENTES J L,et al.Susceptibility of isofamilies of Spodoptera frugiperda (Lepidoptera:Noctuidae) to Cry1Ac and Cry1Fa proteins of Bacillus thuringiensis [J].Southwestern Entomologist,2010,35:409-415.
[16] STORE N P,BABCOCK J M,SCHLENZ M,et al.Discovery and characterization of field resistance to Bt maize:Spodoptera frugiperda (Lepidoptera:Noctuidae) in Puerto Rico [J].Journal of Economic Entomology,2010,103:1031-1038.
[17] HUANG F,QURESHI J A,HEAD G P,et al.Frequency of Bacillus thuringiensis Cry1A.105 resistance alleles in field populations of the fall armyworm,Spodoptera frugiperda,in Louisiana and Florida [J].Crop Protection,2016,83:83-89.
[18] LI G,REISIG D,MIAO J,et al.Frequency of Cry1F non-recessive resistance alleles in North Carolina field populations of Spodoptera frugiperda (Lepidoptera:Noctuidae)[J/OL].PLoS ONE,2016,11:e0154492.
[19] NIU Y,QURESHI J A,NI X,et al.F2 screen for resistance to Bacillus thuringiensis Cry2Ab2-maize in field populations of Spodoptera frugiperda (Lepidoptera:Noctuidae) from the southern United States [J].Journal of Invertebrate Pathology,2016,138:66-72.
[20] CHANDRASENA D I,SIGNORINI A M,ABRATTI G,et al.Characterization of field-evolved resistance to Bacillus thuringiensis-derived Cry1F δ-endotoxin in Spodoptera frugiperda populations from Argentina [J].Pest Management Science,2018,74:746-754.
[21] VéLEZ A M,SPENCER T A,ALVES A P,et al.Inheritance of Cry1F resistance,cross resistance and frequency of resistant alleles in Spodoptera frugiperda (Lepidoptera:Noctuidae)[J].Bulletin of Entomological Research,2013,103:700-713.
[22] HARRISON F P.Oviposition and subsequent infestations of corn by fall armyworm [J].Florida Entomologist,1986,69:588-592.
[23] SIEBERT M W,TINDALL K V,LEONARD B R,et al.Evaluation of corn hybrids expressing Cry1F (Herculex? I Insect Protection) against fall armyworm (Lepidoptera:Noctuidae) in southern United States [J].Journal of Entomology Science,2008,43:41-51.
[24] ADAMCZYK J R,HOLLOWAY J J,LEONARD J W,et al.Susceptibility of fall armyworm collected from different plant hosts to selected insecticides and transgenic Bt cotton [J].Journal of Cotton Science,1997,1:21-28.
[25] YU S J,NGUYEN S N,ABO-ELGHAR G E.Biochemical characteristics of insecticide resistance in the fall armyworm,Spodoptera frugiperda (J.E.Smith)[J].Pesticide Biochemistry and Physiology,2003,77:1-11.
[26] BUNTIN G D.Corn expressing Cry1Ab or Cry1F endotoxin for fall armyworm and corn earworm (Lepidoptera:Noctuidae) management in field corn for grain production [J].Florida Entomologist,2008,91:523-530.
[27] SIEBERT M W,BABOCK J M,NOLTING S,et al.Efficacy of Cry1F insecticidal protein in maize and cotton for control of fall armyworm (Lepidoptera:Noctuidae)[J].Florida Entomologist,2008,91:555-565.
[28] HARDKE J T,LEONARD B R,HUANG F,et al.Damage and survivorship of fall armyworm (Lepidoptera:Noctuidae) on transgenic field corn expressing Bacillus thuringiensis Cry proteins [J].Crop Protection,2011,30:168-172.
[29] FARIAS J R,ANDOW D A,HORIKOSHI R J,et al.Field-evolved resistance to Cry1F maize by Spodoptera frugiperda (Lepidoptera:Noctuidae) in Brazil [J].Crop Protection,2014,64:150-158.
[30] HERNáNDEZ-RODRíGUEZ C S,HERNáNDEZ-MARTíNEZ P,VAN RIE J,et al.Shared midgut binding sites for Cry1A.105,Cry1Aa,Cry1Ab,Cry1Ac and Cry1Fa proteins from Bacillus thuringiensis in two important corn pests,Ostrinia nubilalis and Spodoptera frugiperda [J/OL].PLoS ONE,2013,8(7):e68164.
[31] GOUFFON C,VAN V A,VAN R J,et al.Binding sites for Bacillus thuringiensis Cry2Ae toxin on heliothine brush border membrane vesicles are not shared with Cry1A,Cry1F,or Vip3A toxin [J].Applied Environmental Microbiology,2011,77(10):3182-3188.
[32] BERNARDI O,BERNARDI D,AMADO D,et al.Resistance risk assessment of Spodoptera frugiperda (Lepidoptera:Noctuidae) and Diatraea saccharalis (Lepidoptera:Crambidae) to Vip3A20 insecticidal protein expressed in corn [J].Journal of Economic Entomology,2015,108(6):2711-2719.
[33] STORER N P,KUBISZAK M E,KING E,et al.Status of resistance to Bt maize in Spodoptera frugiperda:lessons from Puerto Rico [J].Journal of Invertebrate Pathology,2012,110:294-300.
[34] 江幸福,张蕾,程云霞,等.草地贪夜蛾迁飞行为与监测技术研究进展[J].植物保护,2019,45(1):12-18.
[35] DANGAL V,HUANG F.Fitness costs of Cry1F resistance in two populations of fall armyworm,Spodoptera frugiperda (J.E.Smith),collected from Puerto Rico and Florida [J].Journal of Invertebrate Pathology,2015,127:81-86.
[36] CAMARGO A M,CASTA?ERA P,FARINóS G P,et al.Comparative analysis of the genetic basis of Cry1F resistance in two strains of Spodoptera frugiperda originated from Puerto Rico and Florida [J].Journal of Invertebrate Pathology,2017,146:47-52.
[37] 吴秋琳,姜玉英,吴孔明,等.草地贪夜蛾缅甸虫源迁入中国的路径分析[J].植物保护,2019,45(2):1-6.