Skip to main content
SpringerLink
Log in

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

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

A Correction to this article was published on 29 November 2019

This article has been updated

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Change history

  • 29 November 2019

    In Materials and method section, a sweetpotato variety “Taizhong-6” (China national number 2013003) should be renamed as Ayamurasaki”.

  • 29 November 2019

    In Materials and method section, a sweetpotato variety ���Taizhong-6��� (China national number 2013003) should be renamed as Ayamurasaki���.

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

References

  • Abegunde OK, Mu TH, Chen JW, Deng FM (2013) Physicochemical characterization of sweetpotato starches popularly used in Chinese starch industry. Food Hydrocoll 33:169–177

    Article  CAS  Google Scholar 

  • 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 10:130–140

    Google Scholar 

  • Bravo A, Likitvivatanavong S, Gill SS, Soberón M (2011) Bacillus thuringiensis: a story of a successful bioinsecticide. Insect Biochem Mol Biol 41:423–431

    Article  CAS  Google Scholar 

  • Chalfant RB, Jansson RK, Seal DR (1990) Ecology and management of sweetpotato insects. Annu Rev Entomol 35:157–180

    Article  Google Scholar 

  • CIP Annual Report (2010) Putting strategy into action: implementing the CIP corporate and strategic plan to enhance pro-poor research impacts. International Potato Center, Lima

    Google Scholar 

  • 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 123:55–64

    Article  CAS  Google Scholar 

  • Deng C, Peng Q, Song F, Lereclus D (2014) Regulation of Cry gene expression in Bacillus thuringiensis. Toxins 6:2194–2209

    Article  Google Scholar 

  • Duan X, Xu J, Ling E, Zhang P (2013) Expression of Cry1Aa in cassava improves its insect resistance against Helicoverpa armigera. Plant Mol Biol 83:131–141

    Article  CAS  Google Scholar 

  • 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) 10:489

    Article  CAS  Google Scholar 

  • 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 6:34864

    Article  CAS  Google Scholar 

  • James C (2016) Global status of commercialized Biotech/GM Crops: 2016. ISAAA Brief No. 52. ISAAA, Ithaca, NY

  • 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 119:32–39

    Article  CAS  Google Scholar 

  • 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 95:1–8

    Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-DDCt method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • 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 175–267

    Google Scholar 

  • 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 139:175–184

    Article  Google Scholar 

  • 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 119:113–125

    Article  CAS  Google Scholar 

  • Nathan SS, Chung PG, Murugan K (2005) Effect of biopesticides applied separately or together on nutritional indices of the rice leaffolder, Cnaphalocrocis medinalis. Phytoparasitica 33:187–195

    Article  Google Scholar 

  • 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 11:6–20

    Google Scholar 

  • 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. Paul

    Google Scholar 

  • 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 33:467–479

    Article  Google Scholar 

  • 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 5:18243

    Article  CAS  Google Scholar 

  • 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 62:775–806

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 2014:135675

    Article  Google Scholar 

  • 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 4:361–365

    Article  Google Scholar 

  • Tabashnik BE, Brévault T, Carrière Y (2013) Insect resistance to BT crops: lessons from the first billion acres. Nat Biotechnol 31:510

    Article  CAS  Google Scholar 

  • 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 279:1071–1079

    Article  CAS  Google Scholar 

  • 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 111:1–12

    Article  CAS  Google Scholar 

  • Vinodh R (2013) Genetic transformation of sorghum for stem borer resistance using Cry1Aa gene via Agrobacterium-mediated approach. Ph.D Thesis, Andhra University, Visakhapatnam, India

  • 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 50:176–189

    Article  CAS  Google Scholar 

  • 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 10:277–289

    Article  Google Scholar 

  • Whalon ME, Wingerd BA (2003) BT: mode of action and use. Arch Insect Biochem Physiol 54:200–211

    Article  CAS  Google Scholar 

  • 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 66:1273–1274

    Article  CAS  Google Scholar 

  • 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 181:701–711

    Article  CAS  Google Scholar 

  • 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 69:1326–1333

    Article  CAS  Google Scholar 

  • 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 115:84–91

    Article  CAS  Google Scholar 

Download references

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.

Author information

Author notes

  1. Yingying Zhong and Sulaiman Ahmed: equal contribution.

Authors and Affiliations

  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 Sciences, Chinese Academy of Science, Shanghai, 200032, China

    Yingying Zhong, Sulaiman Ahmed, Gaifang Deng, Peng Zhang & Hongxia Wang

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Yingying Zhong, Gaifang Deng & Peng Zhang

  3. Shanghai Key Laboratory of Plant Functional Genomics and Resources, Shanghai Chenshan Plant Science Research Center, Chinese Academy of Science, Shanghai Chenshan Botanical Garden, Shanghai, 201602, China

    Weijuan Fan

  4. Department of Plant and Soil Sciences and Kentucky Tobacco Research and Development Center, University of Kentucky, Lexington, KY, 40546, USA

    Hongxia Wang

Authors
  1. Yingying Zhong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sulaiman Ahmed
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gaifang Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Weijuan Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Peng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hongxia Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Peng Zhang or Hongxia Wang.

Additional information

Communicated by Sang-Soo Kwak.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 11939 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhong, Y., Ahmed, S., Deng, G. et al. Improved insect resistance against Spodoptera litura in transgenic sweetpotato by overexpressing Cry1Aa toxin. Plant Cell Rep 38, 1439–1448 (2019). https://doi.org/10.1007/s00299-019-02460-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-019-02460-8

Keywords

Search

Navigation