American Journal of Potato Research

, Volume 96, Issue 1, pp 86–93 | Cite as

Differences in Zebra Chip Severity between ‘Candidatus Liberibacter Solanacearum’ Haplotypes in Texas

  • Kyle Harrison
  • Cecilia TamborindeguyEmail author
  • Douglas C. Scheuring
  • Azucena Mendoza Herrera
  • Adrian Silva
  • Ismael E. Badillo-Vargas
  • J. Creighton MillerJr
  • Julien G. LevyEmail author


Candidatus Liberibacter solanacearum’ (Lso) is a phloem-restricted plant pathogen that is vectored between host plants by the potato psyllid, Bactericera cockerelli. Lso infects solanaceous crops whithin North America and New Zealand and is responsible for causing zebra chip (ZC) in potato. Two Lso haplotypes (A and B) have been identified infecting potato (Solanum tuberosum). Previously, we identified differences in disease severity associated with each Lso haplotype in tomato (Solanum lycopersicum). In this study, the severity of ZC symptoms was evaluated for Lso haplotypes A and B independently or in co-infection in Atlantic variety potato tubers grown in Texas fields. Discolorations in tuber vascular tissues were measured in potato chips using a published 6-point visual scale and compared among plants submitted to five treatments: no psyllids (control), psyllids not infected with Lso (LsoFree), psyllids infected with Lso haplotype A (LsoA), psyllids infected with Lso haplotype B (LsoB), and psyllids infected with both haplotypes (LsoAB). These experiments were performed a total of three times, twice in the Lower Rio Grande Valley (Weslaco, TX) during the winters 2014 and 2018 and once during the spring 2015 in the Texas Panhandle (Springlake, TX). This study showed that significantly lower ZC symptom severity was associated with plants treated with LsoA-infected psyllids compared to plants treated with either LsoB- or LsoAB-infected psyllids; however, this difference was marginal. This difference might be relevant for the disease biology; it has no impact on the tuber suitability for the market. This study also showed that average tuber mass was significantly lower in plants infected with Lso compared with uninfected plants and that this reduction in mass was similar among Lso haplotype treatments. Overall, this study demonstrates that Lso haplotypes A and B cause slightly different ZC symptom severity and that ZC symptom severity in plants treated with psyllids co-infected with both haplotypes is similar to the symptoms associated with Lso haplotype B.


Psyllid Bactericera cockerelli Candidatus Liberibacter solanacearum’ Lso haplotype Potato Zebra chip 


‘Candidatus Liberibacter solanacearum’(Lso) es un fitopatógeno restringido al floema, cuyo vector transmisor entre plantas hospederas es el psílido de la papa Bactericera cockerelli. Lso infecta a cultivos de solanáceas dentro de Norteamérica y Nueva Zelanda, y es responsable de causar la papa rayada (ZC, zebra chip, por sus siglas en inglés). Se han identificado dos haplotipos de Lso (A y B) infectando a la papa (Solanum tuberosum). Previamente, nosotros identificamos diferencias en la severidad de la enfermedad asociadas con cada haplotipo de Lso en tomate (Solanum lycopersicum). En este estudio se evaluó la severidad de los síntomas por ZC para los haplotipos A y B de Lso, independientemente o en co-infección en tubérculos de papa de la variedad Atlantic cultivada en campos de Texas. Se midió la pigmentación en los tejidos vasculares del tubérculo en papas fritas usando una escala visual de seis puntos publicada y se comparó entre plantas sometidas a cinco tratamientos: sin psílidos (testigo), psílidos no infectados con Lso (Libres de Lso, LsoFree), psílidos infectados con el Lso haplotipo A (LsoA), psílidos infectados con el haplotipo B de Lso (LsoB), y psílidos infectados con ambos tipos de haplotipos (LsoAB). Estos experimentos se hicieron tres veces, dos veces en la parte baja del Valle del Río Grande (Weslaco, TX) durante los inviernos de 2014 y 2018, y una vez más durante la primavera de 2015 en la franja de Springlake, TX. Este estudio mostró que más baja severidad significativa del síntoma estuvo asociada con plantas tratadas con psílidos infectados con LsoA en comparación con plantas tratadas ya fuera con psílidos infectados con LsoB o con LsoAB; no obstante, esta diferencia fue marginal. Esta diferencia pudiera ser relevante para la biología de la enfermedad; no tiene impacto en la idoneidad del tubérculo para el mercado. Este estudio también mostró que la masa promedio del tubérculo fue significativamente más baja en plantas infectadas con Lso comparadas con las no infectadas, y que esta reducción en la masa fue similar entre los tratamientos con los haplotipos de Lso. En general, este estudio demuestra que los haplotipos A y B de Lso causan ligeramente diferente severidad de síntoma por ZC, y que esta severidad en plantas tratadas con psílidos co-infectados con ambos haplotipos es similar a los síntomas asociados con el haplotipo B de Lso.



We would like to thank Dr. Elizabeth A. Pierson for scientific discussion, J. W. Koym and Angel Chappel for technical support. The authors gratefully acknowledge the constructive effort from anonymous reviewers in improving our manuscript. This project is supported by Agriculture and Food Research Initiative competitive award no. 2017-67013-26564 from the USDA National Institute of Food and Agriculture, and by the Texas A&M AgriLife Research Insect Vector Disease Grant Program (award number 06-L701774).

Supplementary material

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ESM 1 (DOCX 168 kb)


  1. Crosslin, J.M., J.E. Munyaneza, J.K. Brown, and L.L. W. 2010. Potato zebra chip disease: A phytopathological tale. Plant Health Progress 17: 33. Scholar
  2. Glynn, J.M., M. Islam, Y. Bai, S. Lan, A. Wen, N.C. Gudmestad, E.L. Civerolo, and H. Lin. 2012. Multilocus sequence typing of ‘Candidatus Liberibacter solanacearum’ isolates from North America and New Zealand. Journal of Plant Pathology 94: 223–228.Google Scholar
  3. Haapalainen, M. 2014. Biology and epidemics of Candidatus Liberibacter species, psyllid-transmitted plant-pathogenic bacteria. Annals of Applied Biology 165: 172–198. Scholar
  4. Haapalainen, M.L., J. Wang, S. Latvala, M.T. Lehtonen, M. Pirhonen, and A.I. Nissinen. 2018. Genetic variation of ‘Candidatus Liberibacter solanacearum’haplotype C and identification of a novel haplotype from Trioza urticae and stinging nettle. Phytopathology 108: 925–934. Scholar
  5. Hansen, A.K., J.T. Trumble, R. Stouthamer, and T.D. Paine. 2008. A new Huanglongbing species, "Candidatus Liberibacter psyllaurous," found to infect tomato and potato, is vectored by the psyllid Bactericera cockerelli (Sulc). Applied and Environmental Microbiology 74: 5862–5865. Scholar
  6. Hernández-Deheza, M.G., R.I. Rojas-Martínez, A. Rivera-Peña, E. Zavaleta-Mejía, D.L. Ochoa-Martínez, and A. Carrillo-Salazar. 2018. Resistance in potato to two haplotypes of ‘Candidatus Liberibacter solanacearum. Journal of Plant Pathology: 1–6.Google Scholar
  7. Levy, J., D.C. Scheuring, J.W. Koym, D.C. Henne, C. Tamborindeguy, E. Pierson, and J.C. Miller Jr. 2015. Investigations on putative zebra chip tolerant potato selections. American Journal of Potato Research 92: 417–425.CrossRefGoogle Scholar
  8. Li, W., J.A. Abad, R.D. French-Monar, J. Rascoe, A. Wen, N.C. Gudmestad, G.A. Secor, I.M. Lee, Y. Duan, and L. Levy. 2009. Multiplex real-time PCR for detection, identification and quantification of 'Candidatus Liberibacter solanacearum' in potato plants with zebra chip. Journal of Microbiological Methods 78: 59–65. Scholar
  9. Liefting, L.W., Z.C. Perez-Egusquiza, G.R. Clover, and J.A.D. Anderson. 2008. A new ‘Candidatus Liberibacter’ species in Solanum tuberosum in New Zealand. Plant Disease 92: 1474.CrossRefGoogle Scholar
  10. Lin, H., M.S. Islam, Y. Bai, A. Wen, S. Lan, N.C. Gudmestad, and E.L. Civerolo. 2012. Genetic diversity of ‘Cadidatus Liberibacter solanacearum’ strains in the United States and Mexico revealed by simple sequence repeat markers. European Journal of Plant Pathology 132: 297–308. Scholar
  11. Mawassi, M., O. Dror, M. Bar-Joseph, A. Piasetzky, J. Sjölund, N. Levitzky, N. Shoshana, L. Meslenin, S. Haviv, and C. Porat. 2018. 'Candidatus Liberibacter solanacearum'is tightly associated with carrot yellows symptoms in Israel and transmitted by the prevalent psyllid vector Bactericera trigonica. Phytopathology 108: 1056–1066. Scholar
  12. Mendoza Herrera, A., J. Levy, K. Harrison, J. Yao, F. Ibanez, and C. Tamborindeguy. 2018. Infection by 'Candidatus Liberibacter solanacearum’ haplotypes a and B in Solanum lycopersicum 'Moneymaker. Plant Disease 102: 2009–2015. Scholar
  13. Munyaneza, J.E., J.L. Buchman, J.E. Upton, J.A. Goolsby, J.M. Crosslin, B. Gerhard, G.P. Miles, and V.G. Sengoda. 2008. Impact of different potato psyllid populations on zebra chip disease incidence, severity, and potato yield. Subtropical Plant Science v. 60: 27–37.Google Scholar
  14. Munyaneza, J.E., T.W. Fisher, V.G. Sengoda, S.F. Garczynski, A. Nissinen, and A. Lemmetty. 2010. First report of “Candidatus Liberibacter solanacearum” associated with psyllid-affected carrots in Europe. Plant Disease 94: 639–639. Scholar
  15. Nachappa, P., J. Levy, E. Pierson, and C. Tamborindeguy. 2011. Diversity of endosymbionts in the potato psyllid, Bactericera cockerelli (Hemiptera: Triozidae), vector of zebra chip disease of potato. Current Microbiology 62: 1510–1520. Scholar
  16. Nelson, W.R., T.W. Fisher, and J.E. Munyaneza. 2011. Haplotypes of "Candidatus Liberibacter solanacearum" suggest long-standing separation. European Journal of Plant Pathology 130: 5–12. Scholar
  17. Rashed, A., F. Workneh, L. Paetzold, J. Gray, and C.M. Rush. 2014. Zebra chip disease development in relation to plant age and time of 'Candidatus Liberibacter solanacearum' infection. Plant Disease 98: 24–31. Scholar
  18. Secor, G.A., and V.V. Rivera-Varas. 2004. Emerging diseases of cultivated potato and their impact on Latin America. Revista Latinoamericana de la Papa (Suplemento) 1: 1–8.Google Scholar
  19. Sengoda, V.G., J.E. Munyaneza, J.M. Crosslin, J.L. Buchman, and H.R. Pappu. 2010. Phenotypic and etiological differences between psyllid yellows and zebra chip diseases of potato. American Journal of Potato Research 87: 41–49. Scholar
  20. Swisher Grimm, K.D., T. Mustafa, W. Rodney Cooper, and J.E. Munyaneza. 2018. Role of ‘Candidatus Liberibacter solanacearum’ and Bactericera cockerelli haplotypes in zebra chip incidence and symptom severity. American Journal of Potato Research 95: 709–719. Scholar
  21. Tahzima, R., M. Maes, E.H. Achbani, K.D. Swisher, J.E. Munyaneza, and K. De Jonghe. 2014. First report of ‘Candidatus Liberibacter solanacearum’ on carrot in Africa. Plant Disease 98: 1426–1426. Scholar
  22. Thomas, J.E., A.D.W. Geering, and G. Maynard. 2018. Detection of “Candidatus Liberibacter solanacearum” in tomato on Norfolk Island, Australia. Australasian Plant Disease Notes 13: 7. Scholar
  23. Wen, A., C. Johnson, and N.C. Gudmestad. 2013. Development of a PCR assay for the rapid detection and differentiation of 'Candidatus Liberibacter solanacearum' haplotypes and their spatiotemporal distribution in the United States. American Journal of Potato Research 90: 229–236. Scholar
  24. Yao, J., P. Saenkham, J. Levy, F. Ibanez, C. Noroy, A. Mendoza, O. Huot, D.F. Meyer, and C. Tamborindeguy. 2016. Interactions ‘Candidatus Liberibacter solanacearum’ – Bactericera cockerelli: Haplotype effect on vector fitness and gene expression analyses. Frontiers in Cellular and Infection Microbiology 6: 62. Scholar

Copyright information

© The Potato Association of America 2018

Authors and Affiliations

  1. 1.Department of Horticultural SciencesTexas A&M UniversityCollege StationUSA
  2. 2.Department of EntomologyTexas A&M UniversityCollege StationUSA
  3. 3.Department of EntomologyTexas A&M AgriLife ResearchWeslacoUSA

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