Abstract
In recent years, emerging phytoplasma diseases of potato (Solanum tuberosum L.) have increasingly become important in central and eastern Europe. Accurate identification of phytoplasmas and their insect vectors is essential to developing effective management strategies for diseases caused by these plant pathogens. Potato phytoplasma diseases in Europe were for a long time diagnosed only on the basis of visual symptoms. However, this approach is not very reliable and the use of modern molecular techniques such as polymerase chain reaction (PCR) is required in order to accurately determine the etiology of these phytoplasma diseases. A survey and identification of phytoplasmas associated with potato crops in Romania and southern Russia were conducted based on modern molecular techniques. Symptomatic potato plants were collected from several fields and tested for phytoplasmas by PCR. Also, selected crops and weeds in the vicinity of these potato fields were sampled and tested for phytoplasmas. Stolbur (“Candidatus Phytoplasma solani”; 16SrXII-A) was the only phytoplasma detected in potato and adjacent crops, including tomato (Solanum lycopersicum), pepper (Capsicum annuum), eggplant (Solanum melongena), and beet (Beta vulgaris). This phytoplasma was also detected in weeds, particularly Convolvulus arvensis, Cuscuta sp., and Euphorbia falcata. Genotyping of obtained stolbur isolates on tuf genes revealed that they all had the same RFLP profile corresponding to the tuf-type ‘b’ (VK Type II). Stolbur-affected potato plants produced a large number of spongy tubers that resulted in commercially unacceptable potato chips upon processing.
Similar content being viewed by others
References
Banttari, E. E., Ellis, P. J., & Khurana, S. M. P. (1993). Management of diseases caused by viruses and virus-like pathogens. In R. C. Rowe (Ed.), Potato health management (pp. 127–133). St. Paul: APS Press.
Bogoutdinov, D. Z., Valyunas, D., Navalinskene, M., & Samuitene, M. (2008). About specific identification of phytoplasmas in Solanaceae crops. Agricultural Biology, 1, 77–80.
Bojňanský, V. (1959). Ekológia stolburu zemiaka (Ecology of potato stolbur). Zesz. Probl. Postepow. Nauk roln. Zesz., 94, 83–98 (in Slovakian).
Bovey, R. (1956). Une nouvelle maladie á virus de la tomate en Suisse Romande. Annuaire Agricole de la Suisse, 57, 599–611.
Brcak, J., Kralik, O., Limberk, J., & Ulrychova, M. (1969). Mycoplasma-like bodies in plants infected with potato witches’-broom disease and the response of plants to tetracycline treatment. Biologia Plantarum, 11, 470–476.
Cimerman, A., Pacifico, D., Salar, P., Marzachì, C., & Foissac, X. (2009). Striking diversity of vmp1, a variable gene encoding a putative membrane protein of the Stolbur Phytoplasma. Applied and Environmental Microbiology, 75, 2951–2957.
Cousin, M. T., & Moreau, J. P. (1977). Les stolburs des Solanacées. Phytoma, 291, 15–17.
Cousin, M. T., & Smith, I. M. (1988). The aster yellows complex. In I. M. Smith, J. Dunez, R. A. Lelliot, D. H. Phillips, & S. A. Archer (Eds.), European handbook of plant diseases (pp. 121–124). Oxford: Blackwell Scientific Publications.
Crosslin, J. M., Munyaneza, J. E., Brown, J. K., & Liefting, L. W. (2010). Potato zebra chip disease: a phytopathological tale. Plant Health Progress. doi:10.1094/PHP-2010-0317-01-RV.
Daire, X., Clair, D., Reinert, W., & Boudon-Padieu, E. (1997). Detection of grapevine yellows pytoplasmas belonging to elm yellows group and to the Stolbur subgroup by PCR amplification of non-ribosomal DNA. European Journal of Plant Pathology, 103, 504–507.
Davis, R. E., & Sinclair, W. A. (1998). Phytoplasma identity and disease etiology. Phytopathology, 88, 1372–1376.
Deng, S., & Hiruki, C. (1991). Amplification of 16S rRNA genes from culturable and nonculturable Mollicutes. Journal of Microbiology Methods, 14, 53–61.
EPPO/CABI. (1996). Potato purple-top wilt phytoplasma. In I. M. Smith, D. G. McNamara, P. R. Scott, & M. Holdderness (Eds.), Quarantine pests for Europe (pp. 1–5). Wallingford: CAB International.
Fialova, R., Valova, P., Balakishiyeva, G., Danet, J. L., Safarova, D., Foissac, X., et al. (2009). Genetic variability of stolbur phytoplasma in annual crop and wild plant species in south Moravia. Journal of Plant Pathology, 91, 411–416.
Girsova, N., Bottner, K. D., Mozhaeva, K. A., Kastalyeva, T. B., Owens, R. A., & Lee, I.-M. (2008). Molecular detection and identification of group 16SrI and 16SrXII phytoplasmas associated with diseased potatoes in Russia. Plant Disease, 92, 654.
Hansen, A. K., Trumble, J. T., Stouthamer, R., & Paine, T. D. (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.
Harrison, B. D., & Roberts, I. M. (1969). Association of mycoplasma-like bodies with potato witch’s broom disease from Scotland. The Annals of Applied Biology, 63, 347–349.
Hodgson, W.A., Pond, D.D., & Munro, J. (1974). Diseases and pests of potatoes. Canadian Department of Agriculture Publication, No. 1492.
Jones, P., Arocha, Y., Antezana, O., Montellano, E., & Franco, P. (2004). Brotes grandes (big bud) of potato: a new disease associated with a 16SrI-B subgroup phytoplasma in Bolivia. New Disease Reports, 10, 18.
Kaul, C., Seitz, A., Maixner, M., & Johannesen, J. (2009). Infection of Bois-Noir tuf-type-I stolbur phytoplasma in Hyalesthes obsoletus (Hemiptera: Cixiidae) larvae and influence on larval size. Journal of Applied Entomology, 133, 596–601.
Khadhair, A.-H., Hiruki, C., Hwang, S. F., & Wang, K. (1997). Molecular identification and relatedness of potato witches’-broom phytoplasma isolates from four potato cultivars. Microbiology Research, 152, 281–286.
Khadhair, A.-H., Duplessis, H., McAlister, P., Ampong-Nyarko, K., & Bains, P. (2003). Transmission and characterization of phytoplasma diseases associated with infected potato cultivars in Alberta. Acta Horticulturae, 619, 167–176.
Klinkovski, M. (1957, June). Contribution to the knowledge on Stolbur disease of potato. Proceedings of the 3rd Conference on Potato Virus Diseases (pp. 264–277). Lisse-Wageningen, The Netherlands.
Kuroli, G. (1970). Data on the biology of Hyalesthes obsoletus Sign. Agrártud. Egy. Mosonmagyaróvári Mg. Kar Közleményei, 13, 5–22. (in Hungarian).
Langer, M., & Maixner, M. (2004). Molecular characterization of grapevine yellows associated phytoplasmas of the stolbur-group based on RFLP-analysis of non-ribosomal DNA. Vitis, 43, 1919–199.
Lee, I.-M., Bertaccini, A., Vibio, M., & Gundersen, D. E. (1995). Detection of multiple phytoplasmas in perennial fruit trees with decline symptoms in Italy. Phytopathology, 85, 728–735.
Lee, I.-M., Gundersen-Rindal, D. E., Davis, R. E., & Bartoszyk, I. M. (1998). Revised classification scheme of phytoplasmas based on RFLP analyses of 16S rRNA and ribosomal protein gene sequences. International Journal of Systematic Bacteriology, 48, 1153–1169.
Lee, I.-M., Davis, R. E., & Gundersen-Rindal, D. E. (2000). Phytoplasma: phytopathogenic mollicutes. Annual Review of Microbiology, 54, 221–255.
Lee, I.-M., Bottner, K. D., Munyaneza, J. E., Secor, G. A., & Gudmestad, N. C. (2004). Clover proliferation group (16SrVI) Subgroup A (16SrVI-A) phytoplasma is a probable causal agent of potato purple top disease in Washington and Oregon. Plant Disease, 88, 429.
Lee, I.-M., Bottner, K. D., Secor, G., & Rivera-Varas, V. (2006). ‘Candidatus phytoplasma americanum’, a phytoplasma associated with a potato purple top disease complex. International Journal of Systematic and Evolutionary Microbiology, 56, 1593–1597.
Leyva-López, N. E., Ochoa-Sánchez, J. C., Leal-Klevezas, D. S., & Martínez-Soriano, J. P. (2002). Multiple phytoplasmas associated with potato diseases in Mexico. Canadian Journal of Microbiology, 48, 1062–1068.
Liefting, L. W., Rez-Egusquiza, Z. C., Clover, G. R. G., & Anderson, J. A. D. (2008). A New ‘Candidatus Liberibacter’ Species in Solanum tuberosum in New Zealand. Plant Disease, 92, 1474.
Liefting, L. W., Veerakone, S., Ward, L. I., & Clover, G. R. G. (2009). First report of ‘Candidatus Phytoplasma australiense’ in potato. Plant Disease, 93, 969.
Lindner, K., & Haase, N. U. (2008). Potato stolbur phytoplasma induced disease of potatoes grown in Romania- II: Low molecular wight carbohydrates. In S. Chiru, G. Olteanu, C. Aldea, & C. Bădărău (Eds.), Potato for a changing world (pp. 595–596). Brasov: Transilvania University of Brasov Publishing House.
Lindner, K., Roman, M., Haase, N. U., & Maixner, M. (2008). Potato stolbur phytoplasma induced disease of potatoes grown in Romania- I: Biology of and potato resistance against the potato stolbur phytoplasma. In S. Chiru, G. Olteanu, C. Aldea, & C. Bădărău (Eds.), Potato for a changing world (pp. 593–594). Brasov: Transilvania University of Brasov Publishing House.
Linhartova, S., Cervana, G., & Rodova, J. (2006). The occurrence of potato stolbur phytoplasma on different hosts in the Czech Republic. Mitteilungen aus der Bundesanstalt Für Land- und Forestwirtschaft Berlin-Dahlem, 400, 456.
Lorenz, K.-H., Schneider, B., Ahrens, U., & Seemüller, E. (1995). Detection of the apple proliferation and pear decline phytoplasmas by PCR amplification of ribosomal and nonribosomal DNA. Phytopathology, 85, 771–776.
Maixner, M., Ahrens, U., & Seemüller, E. (1995). Detection of the German grapevine yellows (Vergilbungskrankheit) MLO in grapevine, alternative hosts and a vector by a specific PCR procedure. European Journal of Plant Pathology, 101, 241–250.
Maramorosch, K., Granados, R. R., & Hirumi, H. (1970). Mycoplasma diseases of plants and insects. Advances in Virus Research, 16, 135–193.
Marchoux, G., & Rougier, J. (1987). Une nouvelle affection des solanées maraichéres: la maladie des proliférations et petites feuilles. Phytoma, 392, 53–54.
Marchoux, G., Giannotti, J., & Laterrot, H. (1969). Le stolbur P, une nouvelle maladie de type jaunisse chez la tomate. Symptomes et examen cytologique des tissus au microscope électronique. Annales de Phytopathologie, 1, 633–640.
Martelli, G. P., Russo, M., & Cirulli, M. (1969). Brevinote sullo stolbur del pomodoro in Puglia. Phytopathologia Mediterranea, 8, 150–154.
Miles, G. P., Samuel, M. A., Chen, J., Civerolo, E. L., & Munyaneza, J. E. (2010). Evidence that cell death is associated with zebra chip disease in potato tubers. American Journal of Potato Research, 87, 337–349.
Munyaneza, J. E. (2005). Purple top disease and beet leafhopper-transmitted virescence agent (BLTVA) phytoplasma in potatoes of the Pacific Northwest of the United States. In A. J. Haverkort & P. C. Struik (Eds.), Potato in progress: Science meets practice (pp. 211–220). Wageningen: Wageningen Academic Publishers.
Munyaneza, J. E., Crosslin, J. M., & Upton, J. E. (2006). The beet leafhopper (Hemiptera: Cicadellidae) transmits the Columbia Basin potato purple top phytoplasma to potatoes, beets, and weeds. Journal of Economic Entomology, 99, 268–272.
Munyaneza, J. E., Crosslin, J. M., & Lee, I.-M. (2007). Phytoplasmas diseases and insect vectors in potatoes of the Pacific Northwest of the United States. Bulletin of Insectology, 60, 181–182.
Munyaneza, J. E., Crosslin, J. M., & Upton, J. E. (2007). Association of Bactericera cockerelli (Homoptera: Psyllidae) with “zebra chip”, a new potato disease in southwestern United States and Mexico. Journal of Economic Entomology, 100, 656–663.
Munyaneza, J. E., Goolsby, J. A., Crosslin, J. M., & Upton, J. E. (2007). Further evidence that zebra chip potato disease in the lower Rio Grande Valley of Texas is associated with Bactericera cockerelli. Subtropical Plant Science, 59, 30–37.
Munyaneza, J. E., Buchman, J. L., Upton, J. E., Goolsby, J. A., Crosslin, J. M., Bester, G., et al. (2008). Impact of different potato psyllid populations on zebra chip disease incidence, severity, and potato yield. Subtropical Plant Science, 60, 27–37.
Munyaneza, J. E., Jensen, A. S., Hamm, P. B., & Upton, J. E. (2008). Seasonal occurrence and abundance of beet leafhopper in the potato growing region of Washington and Oregon Columbia Basin and Yakima Valley. American Journal of Potato Research, 85, 77–84.
Munyaneza, J. E., Crosslin, J. M., & Buchman, J. L. (2009). Susceptibility of different potato cultivars to purple top disease. American Journal of Potato Research, 86, 499–503.
Munyaneza, J. E., Crosslin, J. M., Buchman, J. L., & Sengoda, V. G. (2010). Susceptibility of different potato plant growth stages to purple top disease. American Journal of Potato Research, 87, 60–66.
Munyaneza, J.E., Crosslin, J.M., Upton, J.E., Buchman, J.L. (2010b). Incidence of beet leafhopper-transmitted virescene agent phytoplasma in local populations of the beet leafhopper, Circulifer tenellus, in Washington State 10pp. Journal of Insect Science 10: 18 available online: insectscience.org/10.18.
Olivier, C. Y., Lowery, D. T., & Stobbs, L. W. (2009). Phytoplasma diseases and their relationship with insect and plant hosts in Canadian horticultural and field crops. The Canadian Entomologist, 141, 425–462.
Paltrinieri, S., & Bertaccini, A. (2007). Detection of phytoplasmas in plantlets grown from different batches of seed-potatoes. Bulletin of Insectology, 60, 379–380.
Petróczy, I. (1962). Stolbur and Stolbur-like diseases on the potato growing areas in West Hungary. Növénytermelés, 2, 183–190.
Radonjic, S., Snjezana, H., Jovic, J., Cvrkovic, T., Kristic, O., Krnjajic, S., et al. (2009). Occurrence and distribution of grapevine yellows caused by stolbur phytoplasma in Montenegro. Journal of Phytopathology, 157, 682–685.
Rich, A. E. (1983). Potato diseases. New York: Academic.
Rubio-Covarrubias, O. A., Almeyda-Leon, I. H., Moreno, J. I., Sanchez-Salas, J. A., Sosa, R. F., Borbon-Soto, J. T., et al. (2006). Distribution of potato purple top and Bactericera cockerelli Sulc. in the main potato production zones in Mexico. Agricultura Técnica en México, 32, 201–211.
Salazar, L., & Javasinghe, U. (2001). Diseases caused by phytoplasmas in potato. In CIP (Ed.), Techniques in plant virology. Lima: International Potato Center (CIP).
Santos-Cervantes, M. E., Chávez-Medina, J. A., Acosta-Pardini, J., Flores-Zamora, G. L., Méndez-Lozano, J., & Leyva-Lopez, N. E. (2010). Genetic diversity and geographical distribution of phytoplasmas associated with potato purple top disease in Mexico. Plant Disease, 94, 388–395.
Savulescu, A., & Pop, I. (1956). Contribution to the study of Stolbur in Romania. Buletinul Stiintifie, Sectia de Biologie si Stiite Agricola, 8, 723–737.
Secor, G. A., & Rivera-Varas, V. V. (2004). Emerging diseases of cultivated potato and their impact on Latin America. Revista Latinoamericana de la Papa (Suplemento), 1, 1–8.
Secor, G. A., Lee, I.-M., Bottner, K. D., Rivera-Varas, V., & Gudmestad, N. C. (2006). First report of a defect of processing potatoes in Texas and Nebraska associated with a new phytoplasma. Plant Disease, 90, 377.
Secor, G. A., Rivera, V. V., Abad, J. A., Lee, I.-M., Clover, G. R. G., Liefting, L. W., et al. (2009). Association of ‘Candidatus Liberibacter solanacearum’ with Zebra chip disease of potato established by graft and psyllid transmission, electron microscopy, and PCR. Plant Disease, 93, 574–583.
Seemüller, E., Marcone, C., Lauer, U., Ragozzino, A., & Göschl, M. (1998). Current status of molecular classification of the phytoplasmas. Journal of Plant Pathology, 80, 3–26.
Slack, S. A. (2001). Diseases caused by phytoplasmas. In W. R. Stevenson, R. Loria, G. D. Franc, & D. P. Weingartner (Eds.), Compendium of potato diseases (pp. 56–57). St Paul: APS Press.
Smart, C. D., Schneider, B., Blomquist, C. L., Guerra, L. J., Harrison, N. A., Ahrens, U., et al. (1996). Phytoplasma-specific PCR primers based on sequences of the 16S-23S rRNA spacer region. Applied and Environmental Microbiology, 62, 2988–2993.
Suhov, K.S., & Vovk, A.A. (1949). Stolbur rasienovüh. (Izd. Akad.Nauk. SSSR,Moskva-Leningrad) (in Russian).
Szirmai, J. (1956). New disease in Hungary. Agrártudomány, 8, 351–353. (in Hungarian).
Valenta, V., Musil, M., & Misiga, S. (1961). Investigation on European yellows-type viruses: the stolbur virus. Phytopathologische Zeitschrift, 42, 1–38.
Acknowledgements
We thank Zita Nagy and Agnes Mike (FITOLAB, Budapest, Hungary), Sergey Marchenko, Valery Gonchar and Igor Kiselev (Pepsico International Frito Lay Manufacturing, Rostov, Russia), as well as Alexandra Lupascu, Marius Munteanu and Neli Filip (Star Foods E.M. Ltd/Frito-Lay, Ilfov, Romania) for their invaluable technical assistance. We are also grateful to A. Bertaccini, I.-M. Lee, and M. Maixner for providing reference controls used in the study. Funding for this research was provided by Pepsico International, Inc.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ember, I., Acs, Z., Munyaneza, J.E. et al. Survey and molecular detection of phytoplasmas associated with potato in Romania and southern Russia. Eur J Plant Pathol 130, 367–377 (2011). https://doi.org/10.1007/s10658-011-9759-5
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10658-011-9759-5