Skip to main content
SpringerLink
Log in

Enhanced Resistance to Control Potato Tuberworm by Combining Engineered Resistance, Avidin, and Natural Resistance Derived from, Solanum Chacoense

  • Published:
American Journal of Potato Research Aims and scope Submit manuscript

Abstract

Potato tuberworm, Phthorimaea operculella (Zeller), is a destructive insect pest of potato, Solanum tuberosum (L.), found primarily in tropical and sub-tropical regions. It has recently become established in the northwestern United States. Avidin is a natural protein found in chicken (Gallus gallus L.) egg whites that has insecticidal properties against a number of lepidopteran and coleopteran pests. Biotin is a cofactor of carboxylases that are required for many important processes like lipogenesis, gluconeogensis, fatty acid and amino acid catabolism. Without biotin, an insect’s growth is severely stunted, eventually leading to death. Avidin binds and sequesters biotin, limiting its availability during insect growth and development. Previous studies have demonstrated that avidin is effective against potato tuberworm. We sought to elevate resistance by combining avidin with natural host plant resistance factors from the wild species Solanum chacoense Bitter. We expressed avidin in two potato lines: MSE149-5Y, a susceptible potato line, and ND5873-15, a line with S. chacoense-derived resistance. The avidin expression was determined by ELISA to be 10.6 μM in MSE75.7 (avidin) and 12.5 μM in ND75.3 (avidin + S. chacoense-derived) in the tuber. Potato tuberworm bioassays were performed on MSE149-5Y, MSE75.7, ND5873-15, and ND75.3. Mortality was measured after 28 d. Mortality of larvae fed on MSE149-5Y (susceptible) did not differ significantly compared to the mortality of larvae fed on MSE75.7 (avidin) or ND5873-1 (S. chacoense-derived). Significantly higher mortality (98%) was observed for larvae fed on ND75.3 (avidin + S. chacoense-derived) tubers than for larvae fed on MSE149-5Y (susceptible). The present study is the first report of combining avidin with natural host plant resistance factors against potato tuberworm. Expressing avidin in combination with natural host plant resistance may be of value in managing potato tuberworm.

Resumen

El gusano del tubérculo Phthomaea operculella (Zeller) es una plaga destructiva de papa Solanum tuberosum L., se encuentra principalmente en las regiones tropical y subtropical. Se le ha encontrado recientemente en los estados del noroeste de los EE.UU. La avidina es una proteína que se halla en la clara de huevo de las aves de corral (Gallus gallus L.) que tiene propiedades insecticidas contra ciertos lepidópteros y coleópteros. La biotina es un cofactor de las carboxilasas requerido para muchos procesos importantes como la lipogénesis, gluconogésis y el catabolismo de los ácidos grasos y aminoácidos. Sin la biotina, el crecimiento del insecto es severamente afectado conduciéndolo eventualmente a la muerte. La avidina une y secuestra a la biotina, limitando su disponibilidad durante el crecimiento y desarrollo del insecto. Estudios previos han demostrado que la avidina es efectiva contra el gusano del tubérculo de papa. Buscamos elevar la resistencia mediante la combinación de avidina con factores de resistencia natural de plantas hospedantes provenientes de Solanum chacoense Bitter. Expresamos la avidina en dos líneas de papa: MSE149-5Y, línea susceptible y ND5873-15 línea resistente derivada de S. chacoense. La presencia de avidina fue determinada por ELISA como 10.6 µM en MSE75.7 (avidina) y 12.5 µM en ND75.3 (avidina + derivado de S. chacoense) en los tubérculos. Se realizaron bioensayos del gusano del tubérculo en MSE149-5Y, MSE75.7, ND58.73-15 y ND75.3.. La mortalidad de larvas sobre MSE149-5Y (susceptible) no fue significativamente diferente comparado a la mortalidad de la larva alimentada con MSE75.7 (avidina) o ND5873-1 (derivado de S. chacoense). Se observó una mayor mortalidad (98%) significativa en larvas alimentadas sobre tubérculos de ND75.3 (avidina + derivado de S. chacoense) que en larvas alimentadas sobre tubérculos de MSE149-5Y (susceptible). El presente estudio da el primer informe de una combinación de avidina con factores de resistencia natural de la planta hospedante contra el gusano del tubérculo de papa. La expresión de la avidina en combinación con la resistencia natural de la planta hospedante puede ser una herramienta valiosa para el manejo del gusano del tubérculo de papa.

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

Similar content being viewed by others

References

  • Alvarez, J.M., E. Dotseth and P. Nolte 2005. Potato tuberworm: a threat for Idaho potatoes. University of Idaho Extension Bulletin CIS1125: Jan 2005.

  • Berthon, H. 1855. On the potato moth. Proceeding of the Royal Society of Van Diemen’s Land 3: 76–80.

    Google Scholar 

  • Beuning, L., D.S. Mitra, N. Markwick, and P. Gleave. 2001. Minor modifications to the cry1Ac9 nucleotide sequence are sufficient to generate transgenic plants resistant to Phthorimaea operculella. Annals of Applied Biology 138: 281–291.

    Article  CAS  Google Scholar 

  • Burgess, E.P.J., L.A. Malone, J.T. Christeller, M.T. Lester, C. Murray, B.A. Phillip, M.M. Phung, and E.L. Tregidga. 2002. Avidin expressed in transgenic tobacco leaves confers resistance to two noctuid pests, H. armigera and S. litura. Transgenic Research 11: 185–189.

    Article  PubMed  CAS  Google Scholar 

  • Chavez, R., P.E. Schmiediche, M.T. Jackson, and K.V. Raman. 1998. The breeding potential of wild potato species resistant to the potato tubermoth, Phthorimaea operculella (Zeller). Euphytica 39: 123–132.

    Article  Google Scholar 

  • Chittenden, F.H. 1912. The potato tubermoth (Phthorimaea operculella (Zell.). United States Department of Agricultural Bureau of Entomology, Circ 162: 7.

    Google Scholar 

  • Christeller, J.T., L.A. Malone, J.H. Todd, R.M. Marshall, E.P. Burgess, and B.A. Philip. 2005. Distribution and residual activity of two insecticidal proteins, avidin and aprotinin, expressed in transgenic tobacco plants, in the bodies and frass of Spodoptera litura larvae following feeding. Journal of Insect Physiology 51: 1117–1126.

    Article  PubMed  CAS  Google Scholar 

  • Coll, M., S. Gavish, and I. Dori. 2000. Population biology of the potato tuber moth, Phthorimaea operculella (Lepidoptera : Gelechiidae), in two potato cropping systems in Israel. Bulletin of Entomological Research 90: 309–315.

    Article  PubMed  CAS  Google Scholar 

  • Coombs, J.J., D.S. Douches, W.B. Li, E.J. Grafius, and W.L. Pett. 2002. Combining engineered (Bt-cry3a) and natural resistance mechanism in potato for control of Colorado potato beetle. Journal of the American Society for Horticultural Science 127: 62–68.

    CAS  Google Scholar 

  • Cooper, S.G., D.S. Douches, and E.J. Grafius. 2006. Insecticidal activity of avidin combined with genetically engineered and traditional host plant resistance against Colorado potato beetle (Coleoptera: Chrysomelidae) larvae. Journal of Economic Entomology 99: 527–536.

    PubMed  CAS  Google Scholar 

  • Cooper, S.G., D.S. Douches and E.J. Grafius 2007. Combining engineered resistance, avidin, and natural resistance derived from Solanum chacoense Bitter to control Colorado potato beetle. Journal of Economic Entomology (submitted).

  • Das, G.P., and K.V. Raman. 1994. Alternative hosts of the potato tubermoth, Phthorimaea operculella (Zeller). Crop Protection 13: 83–86.

    Article  Google Scholar 

  • Davidson, M.M., R.C. Butler, S.D. Wratten, and A.J. Conner. 2004. Resistance of potatoes transgenic for a cry1Ac9 gene, to Phthorimaea operculella (Lepidoptera: Gelechiidae) over field seasons and between plant organs. Annals of Applied Biology 145: 271–277.

    Article  CAS  Google Scholar 

  • Douches, D.S., A.L. Westedt, K. Zarka, and B. Schroeter. 1998. Potato transformation to combine natural and engineered resistance for controlling tuber moth. HortScience 336: 1053–1056.

    CAS  Google Scholar 

  • Douches, D.S., W. Pett, F. Santos, J. Coombs, E. Grafius, W. Li, E.A. Metry, T. Nasr El-din, and M. Madkour. 2004. Field and storage testing Bt potatoes for resistance to potato tuberworm (Lepidoptera: Gelichiidae). Journal of Economic Entomology 97: 1425–1431.

    PubMed  CAS  Google Scholar 

  • Durance, T.D. 1991. Residual avidin activity in cooked egg white assayed with improved sensitivity. Journal of Food Science 56: 707.

    Article  CAS  Google Scholar 

  • Gould, F. 1998. Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annual Review of Entomology 43: 701–726.

    Article  PubMed  CAS  Google Scholar 

  • Graf, J.E. 1917. The potato tubermoth. Technical Bulletin of the United States Department of Agriculture 427: 56.

    Google Scholar 

  • Green, N.M. 1990. Avidin and streptavidin. Methods in Enzymology 184: 51–67.

    Article  PubMed  CAS  Google Scholar 

  • Hardinge, M.G. 1961. Lesser known vitamins in food. Journal of the American Dietetic Association 38: 240–245.

    PubMed  CAS  Google Scholar 

  • James, D.P. 1952. Nicotinic acid, pantothenic acid and biotin in fruits, vegetables and nuts. British Journal of Nutrition 6: 341–356.

    Article  PubMed  CAS  Google Scholar 

  • Kramer, K.J., T.D. Morgan, J.E. Throne, F.E. Dowell, M. Bailey, and J.A. Howard. 2000. Transgenic avidin maize is resistant to storage insect pests. Nature Biotechnology 18: 670–674.

    Article  PubMed  CAS  Google Scholar 

  • Kroschel, J., and W. Koch. 1994. Studies on the population dynamics of the potato tubermoth in the republic of Yemen. Journal of Applied Entomology 118: 327–341.

    Article  Google Scholar 

  • Levinson, H.Z., and E.D. Bergmann. 1959. Vitamin deficiencies in the housefly produced by antivitamins. Journal of Insect Physiology 3: 293–305.

    Article  CAS  Google Scholar 

  • Levinson, H.Z., A.R. Levinson, and M. Offenberger. 1992. Effect of dietary antagonists and corresponding nutrients on growth and reproduction of the flour mite (Acarus siro L). Experientia 48: 721–729.

    Article  CAS  Google Scholar 

  • Maga, J.A. 1994. Glycoalkaloids in Solanaceae. Food Reviews International 10: 385–418.

    CAS  Google Scholar 

  • Malakar, R., and W.M. Tingey. 1999. Resistance of Solanum berthaultii foliage to potato tuberworm (Lepidoptera: Gelechiidae). Journal of Economic Entomology 92: 497–502.

    Google Scholar 

  • Malone, L.A., E.P.J. Burgess, C.F. Mercer, J.T. Christeller, M.T. Lester, C. Murray, M.M. Phung, B.A. Philip, E.L. Tregidga, and J.H. Todd. 2002. Effects of biotin-binding proteins on eight species of pasture invertebrates. New Zealand Plant Protection 55: 411–415.

    Google Scholar 

  • Malone, L.A., J.H. Todd, E.P.J. Burgess, and J.T. Christeller. 2004. Development of hypopharyngeal glands in adult honey bees fed with a Bt toxin, a biotin-binding protein and a protease inhibitor. Apidologie 35: 655–664.

    Article  CAS  Google Scholar 

  • Markwick, N.P., J.T. Christeller, L.C. Dochterty, and C.M. Lilley. 2001. Insecticidal activity of avidin and streptavidin against four species of pest lepidoptera. Entomologia Experimentalis et Applicata 98: 59–66.

    Article  CAS  Google Scholar 

  • Marwick, N.P., L.C. Docherty, M.M. Phung, M.T. Lester, C. Murray, J.L. Yao, D.S. Mitra, D. Cohen, L.L. Beuning, S. Kutty-Amma, and J.T. Christeller. 2003. Transgenic tobacco and apple plants expressing biotin-binding proteins are resistant to two cosmopolitan insect pests, potato tuber moth, and lightbrown apple moth, respectively. Transgenic Research 12: 671–681.

    Article  Google Scholar 

  • Mistry, S.P., and K. Dakshinamurti. 1964. Biochemistry of biotin. Vitamins and Hormones 22: 1–55.

    Article  PubMed  CAS  Google Scholar 

  • Miura, K., T. Takaya, and K. Koshiba. 1967. The effect of biotin deficiency on the biosynthesis of fatty acids in a blowfly, Aldrichina grahami, during metamorphosis under aseptic conditions. Archives Internationales de Physiologie, de Biochemie et de Biophysique 75: 65–76.

    Article  CAS  Google Scholar 

  • Morgan, T.D., B. Oppert, T.H. Czapla, and K.J. Kramer. 1993. Avidin and streptavidin as insecticidal and growth inhibiting dietary proteins. Entomologia Experimentalis et Applicata 69: 97–108.

    Article  CAS  Google Scholar 

  • Mohammed, A., D.S. Douches, W. Pett, E. Grafius, J. Coombs, Liswidowati, W. Li, and M.A. Madkour. 2000. Evaluation of potato tuber moth (Lepidoptera: Gelechiidae) resistance in tubers of Bt-cry5 transgenic potato lines. Journal of Economic Entomology 932: 472–476.

    Article  PubMed  CAS  Google Scholar 

  • Naimov, S., S. Dukiandjiev, and R.A. de Maagd. 2003. A hybrid Bacillus thuringiensis delta-endotoxin gives resistance against a coleopteran and a lepidopteran pest in transgenic potato. Plant Biotechnology Journal 1: 51–57.

    Article  PubMed  CAS  Google Scholar 

  • Robbins, W.J., and R. Ma. 1941. Biotin and the Growth of Fusarium avenaceum. Bulletin of the Torrey Botanical Club 70: 372–377.

    Google Scholar 

  • Rondon, S.I. 2007. New Emerging Pests in the Pacific Northwest. Oregon State UniversityIntegrated Pest Management. http://oregonstate.edu/potatoes/ipm/insects/emerging.htm. (15 March 2007).

  • Roush, R.T. 1998. Two-toxin strategies for management of insecticidal transgenic crops: can pyramiding succeed where pesticide mixtures have not? Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 353: 1777–1786.

    Article  CAS  Google Scholar 

  • Roux, O., R. Von Arx, and J. Baumgaertner. 1992. Estimating potato tuberworm (Lepidoptera: Gelechiidae) damage in stored potatoes in Tunisia. Journal of Economic Entomology 85: 2246–2250.

    Google Scholar 

  • Shelton, A.M., and J.M. Wyman. 1979. Potato tuber worm damage under different irrigation and cultural practices. Journal of Economic Entomology 72: 261–264.

    Google Scholar 

  • Sileshi, G., and J. Teriessa. 2001. Tuber damage by potato tuber moth, Phthorimaea operculella Zeller (Lepidoptera: Gelechiidae), in the field in eastern Ethiopia. International Journal of Pest Management 47: 109–113.

    Article  Google Scholar 

  • Sinden, S.L., L.L. Sanford, W.W. Cantelo, and K.L. Deahl. 1986. Leptine glycoalkaloids and resistance to the Colorado potato beetle (Coleoptera: Chrysomelidae) in Solanum chacoense. Environmental Entomology 15: 1057–1062.

    CAS  Google Scholar 

  • Stevens, L. 1991. Egg white proteins. Comparative Biochemistry and Physiology 100B: 1–9.

    CAS  Google Scholar 

  • Subramanian, N., and P.R. Adiga. 1997. Mapping the common antigenic determinants in avidin and streptavidin. Biochemistry and Molecular Biology International 43: 375–382.

    PubMed  CAS  Google Scholar 

  • Trager, W. 1948. Biotin and fat-soluble materials with biotin activity in the nutrition of mosquito larvae. Journal of Biological Chemistry 176: 1211–1223.

    PubMed  CAS  Google Scholar 

  • Trivedi, T.P., and D. Rajagopal. 1991. Efffect of different temperature on the development, longevity, and fecundity of potato tubermoth, Phthorimaea operculela (Zell). Journal of Applied Zoological Researches 2: 43–46.

    Google Scholar 

  • Whalon, M.E., and B.A. Wingerd. 2003. Bt: Mode of action and use. Archives of Insect Biochemistry and Physiology 54: 200–211.

    Article  PubMed  CAS  Google Scholar 

  • Yoshida, S., and A. Shirata. 2000. Biotin induces sporulation of mulberry anthracnose fungus, Colletotrichum dematium. Journal of General Plant Pathology 66: 117–122.

    Article  CAS  Google Scholar 

  • Yoza, K., T. Imamura, K.J. Kramer, T.D. Morgan, S. Nakamura, K. Akiyama, S. Kawasaki, F. Takaiwa, and K. Ohtsubo. 2005. Avidin expressed in transgenic rice confers resistance to the stored-product insect pests Tribolium confusum and Sitotroga cerealella. Bioscience Biotechnology and Biochemistry 69: 966–971.

    Article  CAS  Google Scholar 

  • Zhao, J., J. Cao, H.L. Collins, S.L. Bates, R.T. Roush, E.D. Earle, and A.M. Shelton. 2005. Concurrent use of transgenic plants expressing a single and two Bacillus thuringiensis genes speeds insect adaptation to pyramided plants. Proceedings of the National Academy of Science 102: 8426–8430.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Crop and Soil Sciences, Michigan State University, East Lansing, MI, 48824, USA

    Susannah G. Cooper, David S. Douches & Kelly Zarka

  2. Department of Entomology, Michigan State University, East Lansing, MI, 48824, USA

    Edward J. Grafius

Authors
  1. Susannah G. Cooper
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David S. Douches
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kelly Zarka
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Edward J. Grafius
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David S. Douches.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cooper, S.G., Douches, D.S., Zarka, K. et al. Enhanced Resistance to Control Potato Tuberworm by Combining Engineered Resistance, Avidin, and Natural Resistance Derived from, Solanum Chacoense . Am. J. Pot Res 86, 24–30 (2009). https://doi.org/10.1007/s12230-008-9057-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12230-008-9057-8

Keywords

Search

Navigation