Skip to main content
SpringerLink
Log in

Characterization of the Tolerance against Zebra Chip Disease in Tubers of Advanced Potato Lines from Mexico

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

Abstract

Potato zebra chip disease (ZC), a threat to potato production in the USA, Mexico, New Zealand, and Central America, is associated with the bacterium “Candidatus Liberibacter solanacearum” (Cls) that is vectored by the potato psyllid (Bactericera cockerelli Sulc.). ZC control currently depends on insecticide applications, but sustainable control will require development of resistant and/or tolerant varieties. This study characterized four promising potato lines (246, 865, 510 and NAU) exposed to Cls-positive adult psyllids in choice and no-choice assays for ZC resistance. Psyllids preferred to settle on Atlantic over 246 and 865, and oviposit on Atlantic compared to 510. However, tolerance to ZC appeared more dependent on host responses to Cls infection. All four of these potato genotypes exhibited putative ZC tolerance in raw tubers compared to the susceptible commercial variety Atlantic. Expressed tolerance was associated with reduced concentrations of phenolic compounds in Cls-infected raw tubers with corresponding reductions in freshly-cut symptoms. However, these four genotypes exhibited ZC-linked discoloration of fried tuber slices, which was associated with increased sugar content that occurred following Cls-infection. As a result, these four ZC-tolerant experimental potato lines could be useful if the tubers produced are used for fresh, but not processing, markets.

Resumen

La zebra chip (ZC) o papa rayada, que es una amenaza para la producción de papa en los Estados Unidos, México, Nueva Zelanda y Centroamérica, esta asociada con la bacteria “Candidatus Liberibacter solanacearum” (Cls), que es transmitida por el psílido de la papa (Bactericera cockerelli Sulc.). El control de ZC actualmente depende de aplicaciones de insecticidas, pero un control sustentable requerirá del desarrollo de variedades resistentes y/o tolerantes. Este estudio caracterizó cuatro líneas prometedoras (246, 865, 510 y NAU) expuestas a psílidos adultos positivos a Cls en ensayos de selección y no selección para resistencia a ZC. Los psílidos prefirieron posarse en Atlantic que en 246 y 865, y ovipositaron en Atlantic comparados con 510. No obstante, la tolerancia a ZC parecía más dependiente de las respuestas del hospedante a la infección por Cls. Las cuatro líneas exhibieron tolerancia aparente a ZC en tubérculos crudos en comparación a la variedad comercial susceptible Atlantic. La tolerancia expresada estuvo asociada con concentraciones reducidas de compuestos fenólicos en tubérculos crudos infectados con Cls con las correspondientes reducciones en síntomas en cortes frescos. De todas maneras, estas cuatro líneas exhibieron pigmentación asociada a ZC en hojuelas fritas de tubérculo, lo que estuvo asociado con el aumento en el contenido de azúcar que se presentó después de la infección con Cls. Como resultado, estas cuatro líneas experimentales de papa tolerantes a ZC pudieran ser de utilidad si los tubérculos producidos se utilizan para mercado fresco, no de procesamiento.

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

Similar content being viewed by others

References

  • Alarcón-Rodríguez, N.M., E. Valadéz-Moctezuma, and H. Lozoya-Saldaña. 2014. Molecular analysis of Phytophthora infestans (Mont.) de Bary from Chapingo, Mexico. Phylogeographic referential. American Journal of Potato Research 91(5): 459–466.

    Article  Google Scholar 

  • Anderson, J.A.D., G.P. Walker, P.A. Alspach, M. Jeram, and P.J. Wright. 2012. Assessment of susceptibility to zebra Chip and Bactericera cockerelli of selected potato cultivars under different insecticide regimes in New Zealand. American Journal of Potato Research 90: 58–65.

    Article  Google Scholar 

  • Buchman, J.L., B.E. Heilman, and J.E. Munyaneza. 2011. Effects of liberibacter-infective Bactericera cockerelli (Hemiptera: Triozidae) density on zebra hip potato disease incidence, potato yield, and tuber processing quality. Journal of Economic Entomology 104: 1783–1792.

    Article  PubMed  Google Scholar 

  • Buchman, J.L., T.W. Fisher, V.G. Sengoda, and J.E. Munyaneza. 2012. Zebra chip progression: from inoculation of potato plants with liberibacter to development of disease symptoms in tubers. American Journal of Potato Research 89: 159–168.

    Article  Google Scholar 

  • Butler, C.D., and J.T. Trumble. 2012. The potato psyllid, Bactericera cockerelli (Sulc) (Hemiptera: Triozidae): life history, relationship to plant diseases, and management strategies. Terrestrial Arthropod Reviews. 5: 87–111.

    Article  Google Scholar 

  • Butler, C.D., B. Gonzalez, K.L. Manjunath, R.F. Lee, R.G. Novy, J.C. Miller, and J.T. Trumble. 2011a. Behavioral responses of adult potato psyllid, Bactericera cockerelli (Hemiptera: Triozidae), to potato germplasm and transmission of Candidatus liberibacter psyllaurous. Crop Protection. 30: 1233–1238.

    Article  Google Scholar 

  • Butler, C.D., F.J. Byrne, M.L. Keremane, R.F. Lee, and J.T. Trumble. 2011b. Effects of insecticides on behavior of adult Bactericera cockerelli (Hemiptera: Triozidae) and transmission of Candidatus liberibacter psyllaurous. Journal Economic Entomology 104: 586–594.

    Article  CAS  Google Scholar 

  • Cadena-Hinojosa, M.A., I.R. Guzmán-P, M. Díaz-V, T.E. Zavala-Q, O.S. Magaña-T, I.H. Almeyda-L, H. López-D, A. Rivera-P, and O.A. Rubio-Covarrubias. 2003. Distribución, incidencia y severidad del pardeamiento y la brotación anormal en los tubérculos de papa en Valles Altos y Sierras de los estados de México, Tlaxcala y el Distrito Federal, México. Revista Mexicana de Fitopatología 21: 248–259.

    Google Scholar 

  • CNSPP. 2013. Comité Nacional del Sistema Producto Papa. CNSPP: Monografía del sector papa. México D.F.

    Google Scholar 

  • Cooper, W.R., and J.B. Bamberg. 2014. Variation in Bactericera cockerelli (Hemiptera:Trioidae) oviposition, survival, and development on Solanum bulbocastanum germplasm. American Journal of Potato Research. 91: 523–537.

    Article  Google Scholar 

  • de Alfonso, I., S. Vacas, and J. Primo. 2014. Role of alpha-copaene in the susceptibility of olive fruits to Bactrocera oleae (Rossi). Journal of Agriculture and Food Chemistry 62: 11979–11979.

    Article  Google Scholar 

  • Diaz-Montano, J., B.G. Vindiola, N. Drew, R.G. Novy, J.C. Miller, and J.T. Trumble. 2014. Resistance of selected potato genotypes to the potato psyllid (Hemiptera: Triozidae). American Journal of Potato Research. 91: 363–367.

    Article  CAS  Google Scholar 

  • Dunn, O.J. 1964. Multiple comparisons using rank sums. Technometrics 6(3): 241–252.

    Article  Google Scholar 

  • Dwelle, R. B. 2003. In Potato production systems. Stark, J.C. and S. L. Love (eds). p 246. University of Idaho, Agricultural Communications, Moscow.

  • Gao, F., J. Jifon, X. Yang, and T.X. Liu. 2009. Zebra chip disease incidence on potato is influenced by timing of potato psyllid infestation, but not by the host plants on which they were reared. Insect Science 15(5): 399–408.

    Article  Google Scholar 

  • Guenthner, J., J. Goolsby, and G. Greenway. 2012. Use and cost of insecticides to control potato psyllids and zebra chip on potatoes. South West Entomology 37: 263–270.

    Article  Google Scholar 

  • Holm, S. 1979. A simple sequentially rejective multiple test procedure. Scandinavian J. Statistics 6(2): 65–70.

    Google Scholar 

  • Kendra, P.E., W.S. Montgomery, M.A. Deyrup, and D. Wakarchuk. 2016. Improved lure for redbay ambrosia beetle developed by enrichment of alpha-copaene content. Jounral Pest Science 89: 427–438.

    Article  Google Scholar 

  • Leszkowiat, M.J., V. Barichello, R.Y. Yada, R.H. Coffin, E.C. Lougheed, and D.W. Stanley. 1990. Contribution of sucrose to nonenzymatic browning in potato chips. Journal Food Science 55(1): 281–284.

    Article  CAS  Google Scholar 

  • Liu, D., and J.T. Trumble. 2004. Tomato psyllid behavioral responses to tomato plant lines and interactions of plant lines with insecticides. Journal Economic Entomology 97: 1078–1085.

    Article  CAS  Google Scholar 

  • Matkin OA, and PA Chandler. 1957. The U.C.-type soil mixes. In K. Baker (ed.), The U.C. system for producing healthy container-grown plants through the use of clean soil, clean stock and sanitation. California Agricultural Experiment Station, Berkeley pp. 68–85.

  • Miles, G.P., M.A. Samuel, J. Chen, E.L. Civerolo, and J.E. Munyaneza. 2010. Evidence that cell death is associated with zebra chip disease in potato tubers. American Journal of Potato Research 87: 337–349.

    Article  CAS  Google Scholar 

  • Mottram, D.S., B.L. Wedzicha, and A.T. Dodson. 2002. Acrilamide is formed in the Millard reaction. Nature 419: 448–449.

    Article  CAS  PubMed  Google Scholar 

  • Munyaneza, J.E. 2012. Zebra chip disease of potato: biology, epidemiology, and management. American Journal Potato Research 89: 329–350.

    Article  Google Scholar 

  • Munyaneza JE., Novy R., Bester G., Nordgaard J., van Hest P., Thompson A., and C. Wallis. 2013. Research update on potato germplasm screening for zebra chip disease. Proceedings of the 13th annual 2013 zebra chip reporting session. ed Workneh, F. and Rush, C.M., 44–46.

  • Mustafa, T., D.R. Horton, W.R. Cooper, K.D. Swisher, R.S. Zack, H.R. Pappu, and J.E. Munyaneza. 2015. Use of electrical penetration graph technology to examine transmission of ‘Candidatus liberibacter solanacearum’ to potato by three haplotypes of potato psyllid (Bactericera cockerelli; Hemiptera: Triozidae). PloS One 10(9): e0138946. doi:10.1371/journal.pone.0138946.

    Article  PubMed  PubMed Central  Google Scholar 

  • Navarre, D.A., R. Shakya, J. Holden, and J.M. Crosslin. 2009. LC-MS analysis of phenolic compounds in tubers showing zebra chip symptoms. American Journal of Potato Research 86: 88–95.

    Article  CAS  Google Scholar 

  • Novy RG, Prager SM, Miller Jr. J. C., Vindeola B, and JT Trumble. 2013. characterization of potato breeding clones to determine mechanisms conferring observed resistance/tolerance to zebra chip disease. Proceedings of the 13th annual 2013 zebra chip reporting session. ed. Workneh, F. and Rush, C.M., 39–43.

  • Parker, J.K., D.P. Balagiannis, J. Higley, G. Smith, B.L. Wedzicka, and D.S. Mottram. 2012. Kinetic model for the formation of acrylamide during the finish-frying of commercial French fries. Journal Agricultural and Food Chemistry 60: 9321–9331.

    Article  CAS  Google Scholar 

  • Prager, S.M., O.M. Lewis, and C. Nansen. 2013. Oviposition and feeding by Bactericera cockerelli (Homoptera: Psyllidae) in response to a limestone particle film or a plant growth regulator applied to potato plants. Crop Protection 45: 57–62.

    Article  CAS  Google Scholar 

  • Rashed A., Wallis C.M., Paetzold, L., Workneh, F., and C. M. Rush. 2013. Zebra chip disease and potato biochemistry: tuber physiological changes in response to 'Candidatus liberibacter solanacearum' infection over time. Phytopathology 103(5):419–426.

  • Rubio-Covarrubias, O.A., I.H. Almeyda-León, A.M. Cadena-Hinojosa, and R. Lobato-Sánchez. 2011. Relación entre Bactericera cockerelli y la presencia de Candidatus Liberibacter psyllaurous en lotes comerciales de papa. Revista Mexicana de Ciencias Agrícolas 2(1): 17–28.

    Google Scholar 

  • Rubio-Covarrubias O. A., Cadena-Hinojosa M. A., and Vázquez-Carrillo G. 2013. Manejo integrado de la punta morada de la papa en el Estado de México. Folleto Técnico No. 2. Sitio Experimental Metepec INIFAP. México.

  • Rubio-Covarrubias, O.A., M.A. Cadena-Hinojosa, R. Flores-López, J. Munyaneza, S. Prager, and J. Trumble. 2015. Assessing zebra chip resistance of advanced potato breeding lines under field conditions in the Toluca Valley, Mexico. Revista de la Sociedad Latino Americana de la papa. 19(2): 20–30.

    Google Scholar 

  • SAS Institute. 2012. SAS release 9.3 ed. SAS Institute, SAS, Cary.

  • Scheuring D. C., Levy J., Pierson J., Koym J. W., Henne D. C., Novy R. G., and J.C. Miller Jr. 2013. ZC expression in several caged potato populations following infestation with the potato psyllid. Proceedings of the 13th annual 2013 zebra chip reporting session. eds. F. Workneh and C. M. Rush, pp 34–38.

  • Smith C. M. 2005. Plant resistance to arthropods: molecular and conventional approaches. Springer, Dordrecht pp. 19–65.

  • Wallis, C.M., J. Chen, and E.L. Civerolo. 2012. Zebra chip-diseased potato tubers are characterized by increased levels of host phenolics, amino acids, and defense-related proteins. Physiological and Molecular Plant Pathology. 78: 66–72.

    Article  CAS  Google Scholar 

  • Wallis, C.M., A. Rashed, A.K. Wallingford, L. Paetzold, F. Workneh, and C.M. Rush. 2014. Similarities and differences in physiological responses to ‘Candidatus liberibacter solanacearum’ infection among different potato cultivars. Phytopathology 104: 126–133.

    Article  CAS  PubMed  Google Scholar 

  • Wallis, C.M., J.E. Munyaneza, J. Chen, R. Novy, G. Bester, J.L. Buchman, J. Nordgaard, and P. van Hest. 2015a. ‘Candidatus liberibacter solanacearum’ titers in and infection effects on potato tuber chemistry on promising germplasm exhibiting tolerance to zebra chip disease. Phytopathology 105: 1573–1584.

    Article  CAS  PubMed  Google Scholar 

  • Wallis, C.M., A. Rashed, J. Chen, L. Paezold, F. Workneh, and C.M. Rush. 2015b. Effects of potato-psyllid-vectored ‘Candidatus liberibacter solanacearum’ infection of potato leaf and stem physiology. Phytopathology 105: 189–198.

    Article  CAS  PubMed  Google Scholar 

  • Will, T., and J.A.E. van Bel. 2006. Physical and chemical interactions between aphids and plants. Journal Experimental Botany 57(4): 729–737.

  • Yang, X.B., Y.M. Zhang, L. Hua, L.N. Peng, J.E. Munyaneza, J.T. Trumble, and T.X. Liu. 2010. Repellency of selected biorational insecticides to potato psyllid, Bactericera cockerelli (Hemiptera: Psyllidae). Crop Protection 29(11): 1320–1324.

    Article  Google Scholar 

  • Zhang, M., S.K. Chaduri, and I. Kubo. 1993. Quantification of insect growth and its use in screening naturally occurring insect control agents. Journal Chemical Ecology 19: 1109–1118.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture. USDA is an equal opportunity provider and employer. The authors thank Beatriz Vindiola and K. Gilbert for assistance in the lab and greenhouse, and Julie Pedraza for assistance in preparing samples. They also thank Emily Dorff for helpful editorial comments.

Author information

Author notes

  1. S. M. Prager

    Present address: Department of Plant Sciences, University of Saskatchewan, 51 Campus Drive , Saskatoon, Saskatchewan, S7N 5A8, Canada

Authors and Affiliations

  1. Instituto Nacional de Investigaciones Forestales Agrícolas y Pecuarias (INIFAP), Programa de Papa, Conjunto SEDAGRO s/n, 52140, Metepec, Estado de México, C.P, Mexico

    O. A. Rubio-Covarrubias & M. A. Cadena-Hinojosa

  2. Department of Entomology, University of California Riverside, 900 University Ave, Riverside, CA, 92521, USA

    S. M. Prager & J. T. Trumble

  3. USDA-ARS San Joaquin Valley Agricultural Sciences Center, Crop Diseases, Pests and Genetics Research Unit, 9611 S. Riverbend Ave, Parlier, CA, 93648, USA

    C. M. Wallis

Authors
  1. O. A. Rubio-Covarrubias
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. A. Cadena-Hinojosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. M. Prager
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. M. Wallis
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. T. Trumble
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. M. Prager.

Electronic supplementary material

ESM 1

(DOCX 98 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rubio-Covarrubias, O.A., Cadena-Hinojosa, M.A., Prager, S.M. et al. Characterization of the Tolerance against Zebra Chip Disease in Tubers of Advanced Potato Lines from Mexico. Am. J. Potato Res. 94, 342–356 (2017). https://doi.org/10.1007/s12230-017-9570-8

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12230-017-9570-8

Keywords

Search

Navigation