Advertisement

Plant Cell Reports

, Volume 38, Issue 11, pp 1439–1448 | Cite as

Improved insect resistance against Spodoptera litura in transgenic sweetpotato by overexpressing Cry1Aa toxin

  • Yingying Zhong
  • Sulaiman Ahmed
  • Gaifang Deng
  • Weijuan Fan
  • Peng ZhangEmail author
  • Hongxia WangEmail author
Original Article

Abstract

Key message

Overexpressing the Cry1Aa gene in sweetpotato significantly reduced pest damage through disrupting the integrity of the midgut of Spodoptera litura larvae for resistance against target Lepidoptera insect pests in sweetpotato.

Abstract

Sweetpotato is susceptible to insect pests and diseases leading to yield losses during pest outbreaks. Lepidoptera insects such as S litura are especially important pests of sweetpotato. The effect of Cry1Aa gene on S. litura was investigated by overexpressing Cry1Aa gene in sweetpotato to relieve symptoms due to pest damage. When transgenic leaves were fed to the larvae of S. litura, the growth of the larvae was reduced, the larval quality decreased, and mortality was increased compared with the larvae that fed on wild-type leaves. Further anatomical analysis revealed that the columnar cells of the midgut epithelium of the BT group were significantly damaged, loosened, or disordered. Furthermore, the integrity of the midgut was destroyed. In addition, when potted seedlings of the wild-type and BT sweetpotato were inoculated with the same number of S. litura larvae, wild-type plants died on the eighth day after infestation, while BT transgenic lines still grew normally. This study showed that transgenic sweetpotato overexpressing Cry1Aa can prevent S. litura infestation, and thus increase the yield of sweetpotato.

Keywords

Ipomoea batatas Spodoptera litura Cry1Aa BT sweetpotato Insect resistance 

Abbreviations

ANOVA

Analysis of variance

FAA

Formaldehyde alcohol acetic acid

qRT-PCR

Quantitative reverse transcription-polymerase chain reaction

TUNEL

Transferase dUTP nick end labeling

WT

Wild type

Notes

Acknowledgements

This work was supported by the grants from the National Natural Science Foundation of China (31771854), China Scholarship Council (201804910055) and the National Key R&D Program of China (2018YFD1000700, 2018YFD1000705), The authors declare no conflict of interest.

Supplementary material

299_2019_2460_MOESM1_ESM.docx (11.7 mb)
Supplementary material 1 (DOCX 11939 kb)

References

  1. Abegunde OK, Mu TH, Chen JW, Deng FM (2013) Physicochemical characterization of sweetpotato starches popularly used in Chinese starch industry. Food Hydrocoll 33:169–177CrossRefGoogle Scholar
  2. Bernardi D, Salmeron E, Horikoshi RJ, Bernardi O, Dourado PM, Carvalho RA, Martinelli S, Head GP, Omoto C (2015) Cross-Resistance between Cry1 proteins in fall armyworm (Spodoptera frugiperda) may affect the durability of current pyramided BT maize hybrids in Brazil. PLoS One 10:130–140Google Scholar
  3. Bravo A, Likitvivatanavong S, Gill SS, Soberón M (2011) Bacillus thuringiensis: a story of a successful bioinsecticide. Insect Biochem Mol Biol 41:423–431CrossRefGoogle Scholar
  4. Chalfant RB, Jansson RK, Seal DR (1990) Ecology and management of sweetpotato insects. Annu Rev Entomol 35:157–180CrossRefGoogle Scholar
  5. CIP Annual Report (2010) Putting strategy into action: implementing the CIP corporate and strategic plan to enhance pro-poor research impacts. International Potato Center, LimaGoogle Scholar
  6. Deml R, Meise T, Dettner K (1999) Effects of Bacillus thuringiensis delta endotoxins on food utilization, growth and survival of phytophagous insects. J Appl Entomol 123:55–64CrossRefGoogle Scholar
  7. Deng C, Peng Q, Song F, Lereclus D (2014) Regulation of Cry gene expression in Bacillus thuringiensis. Toxins 6:2194–2209CrossRefGoogle Scholar
  8. Duan X, Xu J, Ling E, Zhang P (2013) Expression of Cry1Aa in cassava improves its insect resistance against Helicoverpa armigera. Plant Mol Biol 83:131–141CrossRefGoogle Scholar
  9. Hilbeck A, Defarge N, Bøhn T, Krautter M, Conradin C, Amiel C, Panoff JM, Trtikova M (2018) Impact of antibiotics on efficacy of Cry toxins produced in two different genetically modified BT maize varieties in two Lepidopteran Herbivore species, Ostrinia nubilalis and Spodoptera littoralis. Toxins (Basel) 10:489CrossRefGoogle Scholar
  10. Horikoshi RJ, Bernardi D, Bernardi O, Malaquias JB, Okuma DM, Miraldo LL, Amaral FSA, Omoto C (2016) Effective dominance of resistance of Spodoptera frugiperda to BT maize and cotton varieties: implications for resistance management. Sci Rep 6:34864CrossRefGoogle Scholar
  11. James C (2016) Global status of commercialized Biotech/GM Crops: 2016. ISAAA Brief No. 52. ISAAA, Ithaca, NYGoogle Scholar
  12. Janmaat AF, Bergmann L, Ericsson J (2014) Effect of low levels of Bacillus thuringiensis exposure on the growth, food consumption and digestion efficiencies of Trichoplusia ni resistant and susceptible to BT. J Invertebr Pathol 119:32–39CrossRefGoogle Scholar
  13. Koo HN, Yun SH, Kim HK, Kim GH (2018) Elucidation of molecular expression associated with abnormal development and sterility caused by electron beam irradiation in Spodoptera litura (F.) (Lepidoptera: Noctuidae). Int J Radiat Biol 95:1–8Google Scholar
  14. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-DDCt method. Methods 25:402–408CrossRefGoogle Scholar
  15. Matten SR, Frederick RJ, Reynolds AH (2012) United States Environmental Protection Agency insect resistance management programs for plant-incorporated protectants and use of simulation modeling. In: Wozniak CA, McHughen A (eds) Regulation of agricultural biotechnology. Springer, New York, pp 175–267Google Scholar
  16. Morán R, Garcıa R, López A, Zaldúa Z, Mena J, Garcıa M, Armas R, Somonte D, Rodrı́guezc J, Gómez M, Pimentel E (1998) Transgenic sweetpotato plants carrying the delta-endotoxin gene from Bacillus thuringiensis var. tenebrionis. Plant Sci 139:175–184CrossRefGoogle Scholar
  17. Muddanuru T, Polumetla AK, Maddukuri L, Mulpuri S (2019) Development and evaluation of transgenic castor (Ricinus communis L.) expressing the insecticidal protein Cry1Aa of Bacillus thuringiensis against lepidopteran insect pests. Crop Protect 119:113–125CrossRefGoogle Scholar
  18. Nathan SS, Chung PG, Murugan K (2005) Effect of biopesticides applied separately or together on nutritional indices of the rice leaffolder, Cnaphalocrocis medinalis. Phytoparasitica 33:187–195CrossRefGoogle Scholar
  19. Okonya J, Ocimati W, Nduwayezu A, Kantungeko D, Niko N, Blomme G, Legg JP, Kroschel J (2019) Farmer reported pest and disease impacts on root, tuber, and banana crops and livelihoods in Rwanda and Burundi. Sustainability 11:6–20Google Scholar
  20. Ostlie KR, Hutchison WD, Hellmich RL (1997) BT-corn and European corn borer, long term success through resistance management. North Central Region Extension Publication 602, University of Minnesota, St. PaulGoogle Scholar
  21. Prutz G, Dettner K (2005) Effects of various concentrations of Bacillus thuringiensis corn leaf material on food utilization by Chilo partellus larvae of different ages. Phytoparasitica 33:467–479CrossRefGoogle Scholar
  22. Santos-Amaya OF, Rodrigues JV, Souza TC, Tavares CS, Campos SO, Guedes RN, Pereira EJ (2015) Resistance to dual-gene BT maize in Spodoptera frugiperda: selection, inheritance, and cross-resistance to other transgenic events. Sci Rep 5:18243CrossRefGoogle Scholar
  23. Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J, Feitelson J, Zeigler DR, Dean DH (1998) Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol Mol Biol Rev 62:775–806PubMedPubMedCentralGoogle Scholar
  24. Schünemann R, Knaak N, Fiuza LM (2014) Mode of action and specificity of Bacillus thuringiensis toxins in the control of caterpillars and stink bugs in soybean culture. ISRN Microbiol 2014:135675CrossRefGoogle Scholar
  25. Suzuki N, Hori H, Tachibana M, Asano S (1994) Bacillus thuringiensis strain Buibui for control of cupreous chafer, Anomala cuprea (Coleoptera: Scarabaeidae), in turfgrass and sweetpotato. Biol Contr 4:361–365CrossRefGoogle Scholar
  26. Tabashnik BE, Brévault T, Carrière Y (2013) Insect resistance to BT crops: lessons from the first billion acres. Nat Biotechnol 31:510CrossRefGoogle Scholar
  27. Tanaka S, Yoshizawa Y, Sato R (2012) Response of midgut epithelial cells to Cry1Aa is toxin-dependent and depends on the interplay between toxic action and the host apoptotic response. FEBS J 279:1071–1079CrossRefGoogle Scholar
  28. Vachon V, Laprade R, Schwartz JL (2012) Current models of the mode of action of Bacillus thuringiensis insecticidal crystal proteins: a critical review. J Invertebr Pathol 111:1–12CrossRefGoogle Scholar
  29. Vinodh R (2013) Genetic transformation of sorghum for stem borer resistance using Cry1Aa gene via Agrobacterium-mediated approach. Ph.D Thesis, Andhra University, Visakhapatnam, IndiaGoogle Scholar
  30. Visarada KBRS, Padmaja PG, Saikishore N, Pashupatinath E, Royer M, Seetharama N, Patil JV (2014) Production and evaluation of transgenic sorghum for resistance to stem borer. Vitro Cell Dev Biol Plant 50:176–189CrossRefGoogle Scholar
  31. Visarada KBRS, Prasad GS, Royer M (2016) Genetic transformation and evaluation of two sweet sorghum genotypes for resistance to spotted stemborer, Chilo partellus (Swinhoe). Plant Biotechnol Rep 10:277–289CrossRefGoogle Scholar
  32. Whalon ME, Wingerd BA (2003) BT: mode of action and use. Arch Insect Biochem Physiol 54:200–211CrossRefGoogle Scholar
  33. Xue M, Pang YH, Li QL, Liu TX (2010) Effects of four host plants on susceptibility of Spodoptera litura (Lepidoptera: Noctuidae) larvae to five insecticides and activities of detoxification esterases. Pest Manag Sci 66:1273–1274CrossRefGoogle Scholar
  34. Yang J, Bi HP, Fan WJ, Zhang M, Wang HX, Zhang P (2011) Efficient embryogenic suspension culturing and rapid transformation of a range of elite genotypes of sweetpotato (Ipomoea batatas [L.] Lam.). Plant Sci 181:701–711CrossRefGoogle Scholar
  35. Yu H, Li Y, Li X, Romeis J, Wu K (2013) Expression of Cry1Ac in transgenic Bt soybean lines and their efficiency in controlling lepidopteran pests. Pest Manag Sci 69:1326–1333CrossRefGoogle Scholar
  36. Zhu C, Niu Y, Zhou Y, Guo J, Head GP, Price PA, Wen X, Huang F (2019) Survival and effective dominance level of a Cry1A.105/Cry2Ab2-dual gene resistant population of Spodoptera frugiperda (JE Smith) on common pyramided Bt corn traits. Crop Protect 115:84–91CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological SciencesChinese Academy of ScienceShanghaiChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Shanghai Key Laboratory of Plant Functional Genomics and Resources, Shanghai Chenshan Plant Science Research CenterChinese Academy of Science, Shanghai Chenshan Botanical GardenShanghaiChina
  4. 4.Department of Plant and Soil Sciences and Kentucky Tobacco Research and Development CenterUniversity of KentuckyLexingtonUSA

Personalised recommendations