|Expression profiles of Cry1Ab protein and its insecticidal efficacy against the invasive fall armyworm for Chinese domestic GM maize DBN9936
LIANG Jin-gang1, ZHANG Dan-dan2, LI Dong-yang1, 3, ZHAO Sheng-yuan2, WANG Chen-yao1, XIAO Yu-tao4, XU Dong5, YANG Yi-zhong6, LI Guo-ping7, WANG Li-li8, GAO Yu2, YANG Xue-qing9, YUAN Hai-bin10, LIU Jian11, ZHANG Xiu-jie1, WU Kong-ming2
1 Development Center of Science and Technology, Ministry of Agriculture and Rural Affairs, Beijing 100176, P.R.China
2 State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.China
3 State Key Laboratory of Cotton Biology, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang 455000, P.R.China
4 Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518120, P.R.China
5 Institute of Plant Protection and Soil Science, Hubei Academy of Agricultural Sciences, Wuhan 430064, P.R.China
6 College of Horticulture and Plant Protection, Yangzhou University, Yangzhou 225009, P.R.China
7 Institute of Plant Protection, Henan Academy of Agricultural Sciences, Zhengzhou 450002, P.R.China
8 Yantai Academy of Agricultural Sciences, Yantai 265500, P.R.China
9 College of Plant Protection, Shenyang Agricultural University, Shenyang 110866, P.R.China
10 College of Plant Protection, Jilin Agricultural University, Changchun 130118, P.R.China
11 College of Agriculture, Northeast Agricultural University, Harbin 150030, P.R.China
The fall armyworm (FAW) Spodoptera frugiperda, which originated in the Americas, is advancing across China and threatening the nation’s maize crops. Currently, one widely used tool for its control is genetically modified (GM) Bacillus thuringiensis (Bt) maize. Sufficient content of Bt protein in appropriate plant parts is crucial for enhancing resistance against insect pests. In this study, we conducted a systematic investigation of Cry1Ab levels in Chinese domestic GM maize DBN9936, which has recently obtained a biosafety certificate, and evaluated its efficacy against FAW. Quantification of expression levels of Cry1Ab, via ELISA, indicated a spatio-temporal dynamic, with significant variation of mean Cry1Ab, ranging from 0.76 to 8.48 μg g–1 FW with the Cry1Ab protein level ranked as: V6–V8 leaf>R1 leaf>R4 leaf>R1 silk>VT tassel>R4 kernel. Among the nine locations, the Cry1Ab levels in DBN9936 of the Xinxiang, Langfang, and Harbin fields were significantly lower than those from Wuhan and Shenyang, and were slightly, but not significantly lower than those from the other four fields. Furthermore, the artificial diet–Cry1Ab mixture and plant tissue feeding bioassays revealed that DBN9936 has high efficacy against FAW. The insecticidal efficacy of different tissues against FAW larvae reached 34–100% with a descending order of lethality as follows: VT leaf>R4 leaf>R1 husk>R1 silk>VT tassel>R4 kernel. Taken together, our results showed that Bt-Cry1Ab maize DBN9936 has potential as a promising strategy to manage FAW.
Received: 24 June 2020
|Fund: This work was funded by the National Genetically Modified Organism New Variety Breeding Program of China (2019ZX08012-004). We are grateful to Prof. Li Yunhe from Institute of Plant Protection, Chinese Academy of Agricultural Sciences for his helpful comments and suggestions.
Correspondence WU Kong-ming, Tel: +86-10-82105551, E-mail: email@example.com; ZHANG Xiu-jie, Tel: +86-10-59198155, E-mail: firstname.lastname@example.org
|About author: LIANG Jin-gang, Tel: +86-10-59198125, E-mail: email@example.com;
Cite this article:
LIANG Jin-gang, ZHANG Dan-dan, LI Dong-yang, ZHAO Sheng-yuan, WANG Chen-yao, XIAO Yu-tao, XU Dong, YANG Yi-zhong, LI Guo-ping, WANG Li-li, GAO Yu, YANG Xue-qing, YUAN Hai-bin, LIU Jian, ZHANG Xiu-jie, WU Kong-ming .
Expression profiles of Cry1Ab protein and its insecticidal efficacy against the invasive fall armyworm for Chinese domestic GM maize DBN9936. Journal of Integrative Agriculture, 20(3): 792-803.
| Abendroth L J, Elmore R W, Boyer M J, Marlay S K. 2011. Corn Growth and Development. Iowa State University of Science and Technology Cooperative Extension Service, Ames, Iowa, USA.
Abrahams P, Beale T, Cock M, Corniani N, Day R, Godwin J, Murphy S, Richards G, Vos J. 2017. Fall armyworm status. In: Impacts and Control Options in Africa: Preliminary Evidence Note (April 2017). Centre for Agriculture and Bioscience International (CABI), UK.
ANZFA (Australia New Zealand Food Authority). 2000. Draft final risk assessment report, application A386, food produced from insect protected, herbicide tolerant Bt-11 corn line. ANZFA. p. 26.
Bakhsh A, Shahzad K, Husnain T. 2011. Variation in the spatio-temporal expression of insecticidal genes in cotton. Czech Journal of Genetics and Plant Breeding, 47, 1–9.
Botha A S, Erasmus A, du Plessis H, Van den Berg J. 2019. Efficacy of Bt maize for control of Spodoptera frugiperda (Lepidoptera: Noctuidae) in South Africa. Journal of Economic Entomology, 112, 1260–1266.
Carzoli A K, Aboobucker S I, Sandall L L, Lübberstedt T T, Suza W P. 2018. Risks and opportunities of GM crops: Bt maize example. Global Food Security, 19, 84–91.
Chandrasena D I, Signorini A M, Abratti G, Storer N P, Olaciregui M L, Alves A P, Pilcher C D. 2018. Characterization of field-evolved resistance to Bacillus thuringiensis-derived Cry1F δ-endotoxin in Spodoptera frugiperda populations from Argentina. Pest Management Science, 74, 746–754.
Cheema H M N, Khan A A, Khan M I, Aslam U, Rana I A, Khan I A. 2016. Assessment of Bt cotton genotypes for the Cry1Ac transgene and its expression. The Journal of Agricultural Science, 154, 109–117.
Chimweta M, Nyakudya I W, Jimu L, Mashingaidze A B. 2020. Fall armyworm [Spodoptera frugiperda (J.E. Smith)] damage in maize: Management options for flood-recession cropping smallholder farmers. International Journal of Pest Management, 66, 142–154.
Deng W J, Zhu S, Zeng L, Liu J, Kang R, Yang M H, Cao L Z, Wang H C, Billiar T R, Jiang J X, Xie M, Tang D L. 2018. The circadian clock controls immune checkpoint pathway in sepsis. Cell Reports, 24, 366–378.
Dong H Z, Li W J. 2007. Variability of endotoxin expression in Bt transgenic cotton. Journal of Agronomy and Crop Science, 193, 21–29.
Dutra C C, Koch R L, Burkness E C, Meissle M, Romeis J, Hutchison W D, Fernandes M G. 2012. Harmonia axyridis (Coleoptera: Coccinellidae) exhibits no preference between Bt and non-Bt maize fed Spodoptera frugiperda (Lepidoptera: Noctuidae). PLoS ONE, 7, e44867.
Eghrari K, de Brito A H, Baldassi A, Balbuena T S, Fernandes O A, Môro G V. 2019. Homozygosis of Bt locus increases Bt protein expression and the control of Spodoptera frugiperda (Lepidoptera: Noctuidae) in maize hybrids. Crop Protection, 124, 104871.
Erasmus R, Pieters R, Du Plessis H, Hilbeck A, Trtikova M, Erasmus A, Van den Berg J. 2019. Introgression of a cry1Ab transgene into open pollinated maize and its effect on Cry protein concentration and target pest survival. PLoS ONE, 14, e0226476.
Fatoretto J C, Michel A P, Silva Filho M C, Silva N. 2017. Adaptive potential of fall armyworm (Lepidoptera: Noctuidae) limits Bt trait durability in Brazil. Journal of Integrated Pest Management, 8, 17.
Farias J R, Andow D A, Horikoshi R J, Sorgatto R J, Fresia P, dos Santos A C, Omoto C. 2014. Field-evolved resistance to Cry1F maize by Spodoptera frugiperda (Lepidoptera: Noctuidae) in Brazil. Crop Protection, 64, 150–158.
Girón-Calva P S, Twyman R M, Albajes R, Gatehouse A M, Christou P. 2020. The impact of environmental stress on Bt crop performance. Trends in Plant Science, 25, 264–278.
Gonçalves J, Rodrigues J V C, Santos-Amaya O F, Paula-Moraes S V, Pereira E J G. 2020. The oviposition behavior of fall armyworm moths is unlikely to compromise the refuge strategy in genetically modified Bt crops. Journal of Pest Science, 93, 965–977.
Groote H D, Kimenju S C, Munyua B, Palmas S, Kassie M, Bruce A. 2020. Spread and impact of fall armyworm (Spodoptera frugiperda J. E. Smith) in maize production areas of Kenya. Agriculture, Ecosystems & Environment, 292, 106804.
Hardke J T, Leonard B R, Huang F, Jackson R E. 2011. Damage and survivorship of fall armyworm (Lepidoptera: Noctuidae) on transgenic field corn expressing Bacillus thuringiensis Cry proteins. Crop Protection, 30, 168–172.
He K L, Wang Z Y. 2020. Resistance evolution to Bt maize in the fall armyworm and consideration on IRM strategy in China. Plant Protection, 46, 1–15. (in Chinese)
Huang F N, Qureshi J A, Meagher Jr R L, Reisig D D, Head G P, Andow D A, Ni X Z, Kerns D, Buntin G D, Niu Y, Yang F, Dangal V. 2014. Cry1F resistance in fall armyworm Spodoptera frugiperda: single gene versus pyramided Bt maize. PLoS ONE, 9, e112958.
Huang J R, Liu B, Tian C H, Huang B, Zhao W X, Lv G Q, Li G P, Feng H Q. 2020. Spatial distribution of the fall armyworm Spodoptera frugiperda egg masses on corn plant. Plant Protection, doi: 10.16688/j.zwbh.2020240. (in Chinese)
Jeger M, Bragard C, Caffier D, Candresse T, Chatzivassiliou E, Dehnen-Schmutz K, Gilioli G, Gregoire J C, Miret J A J, Navarro M N, Niere B, Parnell S, Potting R, Rafoss T, Rossi V, Urek G, Van Bruggen A, Van der Werf W, West J, Winter S, et al. 2017. Scientific opinion on the pest categorisation of Spodoptera frugiperda. EFSA Journal, 15, 4927.
Koch M S, Ward J M, Levine S L, Baum J A, Vicini J L, Hammond B G. 2015. The food and environmental safety of Bt crops. Frontiers in Plant Science, 6, 283.
Koffi D, Agboka K, Adenka D K, Osae M, Tounou A K, Anani Adjevi M K, Fening K O, Meagher R L. 2020. Maize infestation of fall armyworm (Lepidoptera: Noctuidae) within agro-ecological zones of Togo and Ghana in West Africa 3 yr after its invasion. Environmental Entomology, 49, 645–650.
Kok E J, Pedersen J, Onori R, Sowa S, Schauzu M, De Schrijver A, Teeri T H. 2014. Plants with stacked genetically modified events: To assess or not to assess. Trends in Biotechnology, 32, 70–73.
Kumela T, Simiyu J, Sisay B, Likhayo P, Mendesil E, Gohole L, Tefera T. 2019. Farmers’ knowledge, perceptions, and management practices of the new invasive pest, fall armyworm (Spodoptera frugiperda) in Ethiopia and Kenya. International Journal of Pest Management, 65, 1–9.
Li G P, Ji T J, Sun X X, Jiang Y Y, Wu K M, Feng H Q. 2019. Susceptibility evaluation of invaded Spodoptera frugiperda population in Yunnan Province to five Bt proteins. Plant Protection, 45, 15–20. (in Chinese)
Li P G, Yang C, Yue R, Zhen Y P, Zhuo Q, Piao J H, Yang X G, Xiao R. 2018. Modulation of the fecal microbiota in sprague-dawley rats using genetically modified and isogenic corn lines. Journal of Agricultural and Food Chemistry, 66, 551–561.
Li X J, Wu M F, Ma J, Gao B Y, Wu Q L, Chen A D, Liu J, Jiang Y Y, Zhai B P, Early R, Chapman J W, Hu G. 2019. Prediction of migratory routes of the invasive fall armyworm in eastern China using a trajectory analytical approach. Pest Management Science, 76, 454–463.
Li Y H, Hallerman E M, Peng Y F. 2018. How can China prepare for the domestic cultivation of Bt maize. Trends in Food Science & Technology, 73, 87–88.
Li Y H, Hallerman E M, Wu K M, Peng Y F. 2020a. Insect-resistant genetically engineered crops in China: Development, application, and prospects for use. Annual Review of Entomology, 65, 273–292.
Li Y H, Wang Z Y, Romeis J. 2020b. Managing the invasive fall armyworm through biotech crops: A Chinese perspective. Trends in Biotechnology, doi: 10.1016/j.tibtech.2020.07.001.
Liu Q S, Hallerman E, Peng Y F, Li Y H. 2016. Development of Bt rice and Bt maize in China and their efficacy in target pest control. International Journal of Molecular Sciences, 17, 1561.
Lohn A F, Trtikova M, Chapela I, den Berg J V, du Plessis H, Hilbeck A. 2020. Transgene behavior in Zea mays L. crosses across different genetic backgrounds: Segregation patterns, cry1Ab transgene expression, insecticidal protein concentration and bioactivity against insect pests. PLoS ONE, 15, e0238523.
Monsanto. 2002. Safety assessment of YieldGard insect-protected event MON810. Monsanto. p. 4.
Moscardini V F, Marques L H, Santos A C, Rossetto J, Silva O A B N, Rampazzo P E, Castro B A. 2020. Efficacy of Bacillus thuringiensis (Bt) maize expressing Cry1F, Cry1A.105, Cry2Ab2 and Vip3Aa20 proteins to manage the fall armyworm (Lepidoptera: Noctuidae) in Brazil. Crop Protection, 137, 105269.
Murúa M G, Vera M A, Michel A, Casmuz A S, Fatoretto J, Gastaminza G. 2019. Performance of field-collected Spodoptera frugiperda (Lepidoptera: Noctuidae) strains exposed to different transgenic and refuge maize hybrids in Argentina. Journal of Insect Science, 19, 21.
Nagoshi R N, Meagher R L, Hay-Roe M. 2012. Inferring the annual migration patterns of fall armyworm (Lepidoptera: Noctuidae) in the United States from mitochondrial haplotypes. Ecology and Evolution, 2, 1458–1467.
Nguyen H T, Jehle J A. 2007. Quantitative analysis of the seasonal and tissue-specific expression of Cry1Ab in transgenic maize Mon810. Journal of Plant Diseases and Protection, 114, 82–87.
Nguyen H T, Jehle J A. 2009. Expression of Cry3Bb1 in transgenic corn MON88017. Journal of Agricultural and Food Chemistry, 57, 9990–9996.
Obrist L B, Dutton A, Romeis J, Bigler F. 2006. Biological activity of Cry1Ab toxin expressed by Bt maize following ingestion by herbivorous arthropods and exposure of the predator Chrysoperla carnea. BioControl, 51, 31–48.
Omoto C, Bernardi O, Salmeron E, Sorgatto R J, Dourado P M, Crivellari A, Carvalho R A, Willse A, Martinelli S, Head G P. 2016. Field-evolved resistance to Cry1Ab maize by Spodoptera frugiperda in Brazil. Pest Management Science, 72, 1727–1736.
Pannuti L E R, Baldin E L L, Hunt T E, Paula-Moraes S V. 2016. On-plant larval movement and feeding behavior of fall armyworm (Lepidoptera: Noctuidae) on reproductive corn stages. Environmental Entomology, 45, 192–200.
Prasanna B M, Huesing J E, Eddy R, Peschke V M. 2018. Fall Armyworm in Africa: A Guide for Integrated Pest Managemen. 1st ed. CDMX: CIMMYT, Mexico. p. 75.
Ramirez-Romero R, Desneux N, Chaufaux J, Kaiser L. 2008. Bt-maize effects on biological parameters of the non-target aphid Sitobion avenae (Homoptera: Aphididae) and Cry1Ab toxin detection. Pesticide Biochemistry and Physiology, 91, 110–115.
Romeis J, Naranjo S E, Meissle M, Shelton A M. 2019. Genetically engineered crops help support conservation biological control. Biological Control, 130, 136–154.
Silver A. 2019. China seeks predator to stop voracious caterpillar. Nature, 570, 286–287.
Silva C L T, Paiva L A, Correa F, Silva F C, Pelosi A P, da Silva Araujo M, de Sousa Almeida A C, Jesus F G. 2020. Interaction between corn genotypes with Bt protein and management strategies for Spodoptera frugiperda (Lepidoptera: Noctuidae). Florida Entomologist, 102, 725–730.
Silva G A, Picanço M C, Ferreira L R, Ferreira D O, Farias E S, Souza T C, Rodrigues-Silva N, Pereira E J G. 2018. Yield losses in transgenic Cry1Ab and non-Bt corn as assessed using a crop-life-table approach. Journal of Economic Entomology, 111, 218–226.
Sisay B, Tefera T, Wakgari M, Ayalew G, Mendesil E. 2019. The efficacy of selected synthetic insecticides and botanicals against fall armyworm, Spodoptera frugiperda, in maize. Insects, 10, 45.
Souza C S F, Silveira L C P, Pitta R M, Waquil J M, Pereira E J G, Mendes S M. 2019. Response of field populations and Cry-resistant strains of fall armyworm to Bt maize hybrids and Bt-based bioinsecticides. Crop Protection, 120, 1–6.
Souza C S F, Silveira L C P, Souza B H S, Nascimento P T, Damasceno N C R, Mendes S M. 2020. Efficiency of biological control for fall armyworm resistant to the protein Cry1F. Brazilian Journal of Biology, doi: 10.1590/1519-6984.224774.
Storer N P, Babcock J M, Schlenz M, Meade T, Thompson G D, Bing J W, Huckaba R M. 2010. Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. Journal of Economic Entomology, 103, 1031–1038.
Storer N P, Kubiszak M E, King J E, Thompson G D, Santos A C. 2012. Status of resistance to Bt maize in Spodoptera frugiperda: Lessons from Puerto Rico. Journal of Invertebrate Pathology, 110, 294–300.
Sun H W, Li F, Gao R, Xu X H, Yang S K, Lu X B. 2018. Bt protein spatial-temporal expression and evaluation for resistance of transgenic cry1Ab/cry2Aj and G10evo-epsps maize. Journal of Biosafety, 27, 63–68. (in Chinese)
Sun X X, Hu C X, Jia H R, Wu Q L, Shen X J, Zhao S Y, Jiang Y Y, Wu K M. 2021. Case study on the first immigration of fall armyworm, Spodoptera frugiperda invading into China. Journal of Integrative Agriculture, 20, 664–672.
Svobodová Z, Burkness E C, Habuštová O S, Hutchison W D. 2017a. Predator preference for Bt-fed Spodoptera frugiperda (Lepidoptera: Noctuidae) prey: Implications for insect resistance management in Bt maize seed blends. Journal of Economic Entomology, 110, 1317–1325.
Svobodová Z, Shu Y H, Habuštová O S, Romeis J, Meissle M. 2017b. Stacked Bt maize and arthropod predators: Exposure to insecticidal Cry proteins and potential hazards. Proceedings of the Royal Society (B: Biological Sciences), 284, 20170440.
Székács A, Lauber É, Juracsek J, Darvas B. 2010a. Cry1Ab toxin production of MON 810 transgenic maize. Environmental Toxicology and Chemistry, 29, 182–190.
Székács A, Lauber É, Takács E, Darvas B. 2010b. Detection of Cry1Ab toxin in the leaves of MON 810 transgenic maize. Analytical and Bioanalytical Chemistry, 396, 2203–2211.
Székács A, Weiss G, Quist D, Takács E, Darvas B, Meier M, Swain T, Hilbeck A. 2012. Inter-laboratory comparison of Cry1Ab toxin quantification in MON 810 maize by enzyme-immunoassay. Food and Agricultural Immunology, 23, 99–121.
Trtikova M, Wikmark O G, Zemp N, Widmer A, Hilbeck A. 2015. Transgene expression and Bt protein content in transgenic Bt maize (MON810) under optimal and stressful environmental conditions. PLoS ONE, 10, e0123011.
US-EPA (U.S. Environmental Protection Agency). 2010. Biopesticide Registration Action Document: Cry1Ab and Cry1F Bacillus thuringiensis (Bt) corn plant-incorporated protectants. US-EPA, Office of Pesticide Programs, Biopesticides and Pollution Prevention Division. p. 20.
Vélez A M, Vellichirammal N N, Jurat-Fuentes J L, Siegfried B D. 2016. Cry1F resistance among lepidopteran pests: A model for improved resistance management? Current Opinion in Insect Science, 15, 116–124.
Wang F, Peng S B, Cui K H, Nie L X, Huang J L. 2014a. Field performance of Bt transgenic crops: A review. Australian Journal of Crop Science, 8, 18–26.
Wang L, Lu Y Y. 2020. Spreading trend predication of fall armyworm, Spodoptera frugiperda, in year of 2020 in China. Journal of Environmental Entomology, 42, 1139–1145. (in Chinese)
Wang Y N, Ke K Q, Li Y H, Han L Z, Liu Y M, Hua H X, Peng Y F. 2016. Comparison of three transgenic Bt rice lines for insecticidal protein expression and resistance against a target pest, Chilo suppressalis (Lepidoptera: Crambidae). Insect Science, 23, 78–87.
Wang Y N, Zhang L, Li Y H, Liu Y M, Han L Z, Zhu Z, Wang F, Peng Y F. 2014b. Expression of Cry1Ab protein in a marker-free transgenic Bt rice line and its efficacy in controlling a target pest, Chilo suppressalis (Lepidoptera: Crambidae). Environmental Entomology, 43, 528–536.
Wu C, Zhang L, Liao C Y, Wu K M, Xiao Y T. 2019. Research progress of resistance mechanism and management techniques of fall armyworm Spodoptera frugiperda to insecticides and Bt crops. Journal of Plant Protection, 46, 503–513.
Wu K M. 2020. Management strategies of fall armyworm (Spodoptera frugiperda) in China. Plant Protection, 46, 1–5. (in Chinese)
Xiao Y T, Wu K M. 2019. Recent progress on the interaction between insects and Bacillus thuringiensis crops. Philosophical Transactions of the Royal Society (B: Biological Sciences), 374, 20180316.
Zhang D D, Wu K M. 2019. The bioassay of Chinese domestic Bt-Cry1Ab and Bt-(Cry1Ab+Vip3Aa) maize against the fall armyworm, Spodoptera frugiperda. Plant Protection, 45, 54–60. (in Chinese)
Zhang L, Liu B, Zheng W G, Liu C H, Zhang D D, Zhao S Y, Li Z Y, Xu P J, Wilson K, Withers A, Jones C M, Smith J A, Chipabika G, Kachigamba D L, Nam K, d’Alençon E, Liu B, Liang X Y, Jin M H, Wu C, et al. 2020. Genetic structure and insecticide resistance characteristics of fall armyworm populations invading China. Molecular Ecology Resources, 20, 1682–1696.
|No Suggested Reading articles found!