References

vavilov

Вавиловский журнал генетики и селекции

Vavilov Journal of Genetics and Breeding

2500-3259

Institute of Cytology and Genetics of Siberian Branch of the RAS

10.18699/VJ17.223

vavilov-904

Research Article

Генофонд и селекция

Gene pool and breeding

Устойчивость картофеля к карантинным болезням

Potato resistance to quarantine diseases

Хютти

А. В.

Khiutti

A. V.

Санкт-Петербург, Пушкин;

Новосибирск

St. Petersburg, Pushkin;

Novosibirsk

alexanderkhyutti@mail.ru

Антонова

О. Ю.

Antonova

O. Yu.

Новосибирск;

Санкт-Петербург

Novosibirsk;

St. Petersburg

Мироненко

Н. В.

Mironenko

N. V.

Санкт-Петербург, Пушкин;

Новосибирск

St. Petersburg, Pushkin;

Novosibirsk

Гавриленко

Т. А.

Gavrilenko

T. A.

Санкт-Петербург

St. Petersburg

Афанасенко

О. С.

Afanasenko

O. S.

Санкт-Петербург, Пушкин;

Новосибирск

St. Petersburg, Pushkin;

Novosibirsk

Федеральное государственное бюджетное научное учреждение «Всероссийский научно-исследовательский институт защиты растений»; Федеральное государственное бюджетное научное учреждение «Федеральный исследовательский центр Институт цитологии и генетики Сибирского отделения Российской академии наук»РоссияAll-Russian Research Institute of Plant Protection; Institute of Cytology and Genetics SB RASRussian Federation

Федеральное государственное бюджетное научное учреждение «Федеральный исследовательский центр Институт цитологии и генетики Сибирского отделения Российской академии наук»; Федеральное государственное бюджетное научное учреждение «Федеральный исследовательский центр Всероссийский институт генетических ресурсов растений им. Н.И. Вавилова» (ВИР)РоссияInstitute of Cytology and Genetics SB RAS; Federal Research Center the N.I. Vavilov All-Russian Institute of Plant Genetic Resources (VIR)Russian Federation

Федеральное государственное бюджетное научное учреждение «Федеральный исследовательский центр Всероссийский институт генетических ресурсов растений им. Н.И. Вавилова» (ВИР); Федеральное государственное бюджетное образовательное учреждение высшего образования «Санкт-Петербургский государственный университет»РоссияFederal Research Center the N.I. Vavilov All-Russian Institute of Plant Genetic Resources (VIR); St. Petersburg State UniversityRussian Federation

2017

24032017

2115161

2017

Хютти А.В., Антонова О.Ю., Мироненко Н.В., Гавриленко Т.А., Афанасенко О.С.

Khiutti A.V., Antonova O.Y., Mironenko N.V., Gavrilenko T.A., Afanasenko O.S.

This work is licensed under a Creative Commons Attribution 4.0 License.

https://vavilov.elpub.ru/jour/article/view/904

Возбудитель рака картофеля Synchytrium endobioticum (Schilb.) Perc. и золотистая картофельная нематода (ЗКН) Globodera rostochiensis (Wollenweber) Behrens – карантинные виды, раcпространенные на территории Российской Федерации и в большинстве стран мира. Бледная картофельная нематода G. pallida (Stone) Behrens на территории РФ не выявлена, хотя в странах Европейского союза встречается повсеместно. В обзоре приведены сведения о вредоносности S. endobioticum и ЗКН. В настоящее время в мире выявлено 43 патотипа S. endobioticum и 5 патотипов ЗКН. На территории РФ обнаружен только первый (D1) патотип возбудителя рака и Ro1 патотип ЗКН. Представлены современные наборы сортов-дифференциаторов для S. endobioticum и ЗКН и рассмотрены методы определения патотипного состава, в том числе попытки разработать молекулярные маркеры для определения расовой принадлежности S. endobioticum. Приведены данные по устойчивости современного сортимента картофеля к этим карантинным заболеваниям и методы определения устойчивости. Рассмотрены современные данные по генетике устойчивости картофеля к S. endobioticum, G. rostochiensis и G. pallida, включая картирование и клонирование R-генов. Рассмотрены результаты оценки эффективности использования молекулярных маркеров в маркер-вспомогательном отборе (MAS) устойчивых генотипов. Приведены результаты использования мультиплексных систем, позволяющих одновременно выявлять аллельный состав нескольких генов устойчивости к одному или к разным патогенам у образцов картофеля. Рассмотрены механизмы количественной устойчивости картофеля к S. endobioticum и ЗКН и адаптационных процессов в популяциях возбудителей, позволяющие преодолевать уcтойчивость растения-хозяина. Возделывание в производстве слабо повреждаемых ЗКН сортов может стимулировать адаптационную изменчивость возбудителя и приводить к отбору вирулентных патотипов в течение двух-трех генераций патогена.

The casual agent of potato wart Synchytrium endobioticum (Schilb.) Perc. and potato golden nematode (PGN) Globodera rostochiensis (Wollenweber) Behrens are the quarantine species causing the most widespread and destructive diseases of potato in the Russian Federation and other countries of the world. The potato pale nematode Globodera pallida (Stone) Behrens is not found in Russia, although in the European Union it is found everywhere. The review provides information on the harmfulness of S. endobioticum and PGN. To date, 43 pathotypes of S. endobioticum and 5 pathotypes of PGN have been revealed in the world. In the Russian Federation, only the first (D1) pathotype of potato wart and pathotype Ro1 of PGN have been found. Modern sets of differentials for S. endobioticum and PGN and methods of pathotype composition determination, including efforts to develop molecular markers (SSR) to determine the race of S. endobioticum, are presented. Data on the resistance of commercial potato cultivars to these quarantine diseases and methods for resistance determination are reviewed. Modern data on the genetics of potato resistance to S. endobioticum, G. rostochiensis and G. pallida, including mapping and cloning of R-genes, are presented. Available literature data on molecular markers of R-genes for marker assisted selection and the evaluation of their effectiveness are presented. The use of multiplex systems allows the presence of several genes for resistance to one or more pathogens to be analyzed at once. Mechanisms of potato quantitative resistance to S. endobioticum and PGN and adaptation processes in pathogens populations resulting in overcoming resistance of host are discussed. Cultivation of cultivars poorly susceptible to PGN can stimulate the adaptive variability of the pathogen and induce virulent pathotypes for 2–3 pathogen generations.

картофелькарантинные объектыустойчивость растенийSynchytrium endobioticumGlobodera rostochiensisGlobodera pallida

potatoquarantine speciesplant resistanceSynchytrium endobioticumGlobodera rostochiensisGlobodera pallida

Российский научный фонд

References1

Afanasenko O.S., Mironenko N.V., Khyutti A.V. Meeting of the Euphresco expert group (European phytosanitary research cooperation) to improve the analysis methods of the potato wart populations (Synchytrium endobioticum (Schilb.) Perc.). Vestnik zashchity rasteniy = Plant Protection News. 2013;4:77. (in Russian)

Antonova O.Y., Shvachko N.A., Novikova L.Y., Shuvalov O.Y., Kostina L.I., Klimenko N.S., Shuvalova A.R., Gavrilenko T.A. Genetic diversity of potato varieties based on polymorphism of SSR loci and markers associated with R-genes of resistance. Vavilovskiy zhurnal genetiki i selektsii = Vavilov Journal of Genetics and Breeding. 2016;20(5):596-606. (in Russian)

Asano K., Kobayashi A., Tsuda S., Nishinaka M., Tamiya S. DNA marker-assisted evaluation of potato genotypes for potential resistance to potato cyst nematode pathotypes not yet invading into Japan. Breed. Sci. 2012;62(2):142-150. DOI 10.1270/jsbbs.62.142.

Baayen R.P., Cochius G., Hendriks H., Meffert J.P., Bakker J., Bekker M., van den Boogert P.H.J.F., Stachewicz H., van Leeuwen G.C.M. History of potato wart disease in Europe – a proposal for harmonisation in defining pathotypes. Eur. J. Plant Pathology. 2006; 116:21-31. DOI 10.1007/s10658-006-9039-y.

Bakker E., Achenbach U., Bakker J., van Vliet J., Peleman J., Segers B., van der Heijden S., van der Linde P., Graveland R., Hutten R., van Eck H., Coppoolse E., van der Vossen E., Bakker J., Goverse A. A high-resolution map of the H1 locus harboring resistance to the potato cyst nematode Globodera rostochiensis. Theor. Appl. Genet. 2004;109(1):146-152. DOI 10.1007/s00122-004-1606-z.

Bakker J., Folkertsma R.T., van der Voort R., Boer J.M., Gommers F.J. Changing concepts and molecular approaches in the management of virulence genes in potato cyst nematodes. Annu. Rev. Phytopathol. 1993;31:169-190. DOI 10.1146/annurev.py.31.090193.001125.

Ballvora A., Flath K., Lubeck J., Strahwald J., Tacke E., Hofferbert H.-R., Gebhardt C. Multiple alleles for resistance and susceptibility modulate the defense response in the interaction of tetraploid potato (Solanum tuberosum) with Synchytrium endobioticum pathotypes 1, 2, 6 and 18. Theor. Appl. Genet. 2011;123:1281-1292.

Barone A., Ritter E., Schachtschabel U., Debener T., Salamini F., Gebhardt C. Localization by restriction fragment length polymorphism mapping in potato of a major dominant gene conferring resistance to the potato cyst nematode Globodera rostochiensis. Mol. Gen. Genet. 1990;224(2):177-82. DOI 10.1007/BF00271550.

Biryukova V.A., Shmyglya I.V., Abrosimov S.B., Zapekina T.I., Meleshin A.A., Mityushkin A.V., Manankov V.V. The search for sources of resistance genes to pathogens among the samples of plant breeding and genetics collections of the All-Russia Research Institute of Potato Farming using molecular markers. Zashhita kartofelya = Potato Protection. 2015;1:3-7. (in Russian)

Biryukova V.A., Shmyglya I.V., Meleshin A.A., Mityushkin A.V., Manankov V.V., Abrosimova S.B. Examination of genetic collections of the All-Russia Research Institute of Potato Farming using molecular markers. Dostizheniya nauki i tekhniki APK = Achievements of Science and Technology of AIC. 2016;30(10):22-26. (in Russian)

Biryukova V.A., Zhuravlev A.A., Abrosimova S.B., Kostina L.I., Khromov L.M., Shmyglya I.V., Morozova N.N., Kirsanova S.N. The use of molecular markers of H1 and Gro1 genes of resistance to golden potato cyst nematode. Doklady Rossiyskoy Akademii selskokhozyaystvennykh Nauk = Proceedings of the Russian Academy of Agricultural Sciences. 2008;6:3-6. (in Russian)

Braun H. Biologische Spezialisierung bei Synchytrium endobioticum (Schilb.) Perc. Zeitschr. Pflanzenkrank. u. Pflanzenschutz. 1942; 52(11):481-486.

Brugmans B., Hutten R.G.B., Rookmaker N., Visser R.G.F., van Eck H.J. Exploitation of a marker dense linkage map of potato for positional cloning of a wart disease resistance gene. Theor. Appl. Genet. 2006;112(2):269-277. DOI 10.1007/s00122-005-0125-x.

Bryan G.J., McLean K., Bradshaw J.E., De Jong W.S., Phillips M., Castelli L., Waugh R. Mapping QTLs for resistance to the cyst nematode Globodera pallida derived from the wild potato species Solanum vernei. Theor. Appl. Genet. 2002;105(1):68-77. DOI 10.1007/s00122-002-0873-9.

CABI/EPPO. Globodera rostochiensis. Distribution maps of plant diseases. (2011). Available at http://www.cabi.org.

CABI/EPPO. Synchytrium endobioticum. Distribution maps of plant diseases. (2015). Available at http://www.cabi.org.

Caromel B., Mugniéry D., Kerlan M.-C., Andrzejewski S., Palloix A., Ellissèche D., Rousselle-Bourgeois F., Lefebvre V. Resistance quantitative trait loci originating from Solanum sparsipilum act independently on the sex ratio of Globodera pallida and together for developing a necrotic reaction. Mol. Plant-Microbe Interactions. 2005; 18(11):1186-1194.

Dale M.F.B., Phillips M.S. Variation for the degree of susceptibility to the potato cyst nematode (Globodera pallida) within Solanum tuberosum ssp. tuberosum. Potato Res. 1985;28(1):55-64. DOI 10.1007/BF02357570.

Delmas C.E.L., Fabre F., Jolivet J., Mazet I.D., Cervera S.R., Deliere L., Delmotte F. Adaptation of a plant pathogen to partial host resistance: selection for greater aggressiveness in grapevine downy mildew. Evol. Applications. 2016;9(5):709-725. DOI 10.1111/eva.12368.

Dong S., Raffaele S., Kamoun S. The two-speed genomes of filamentous pathogens: waltz with plants. Curr. Opin. Genet. Dev. 2015;35: 57-65. DOI 10.1016/j.gde.2015.09.001.

Ellenby C. Resistance to the potato-root eelworm Heterodera rostochiensis Wollenweber. 1952;170(4337):1016.

EPPO A2 List of pests recommended for regulation as quarantine pests. 2003. https://www.eppo.int/.

EPPO. Pest quarantine database. Paris, France. 2014. http://www.eppo.int/.

Eves-van den Akker S., Laetsch D.R., Thorpe P., Lilley C.J., Danchin E.G.J., Da Rocha M., Rancure C., Holroyd N.E., Cotton J.A., Szitenberg A., Grenier E., Montarry J., Mimee B., Duceppe M.-O., BoyesI., Marvin J.M.C., JonesL.M., YusupH.B., Lafond-Lapalme J., Esquibet M., Sabeh M., Rott M., Overmars H., Finkers-Tomczak A., Smant G., Koutsovoulos G., Blok V., Mantelin S., Cock P.J.A., Phillips W., Henrissat B., Urwin P.E., Blaxter M., Jones J.T. The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals insights into the basis of parasitism and virulence. Genome Biology. 2016;17:124. DOI 10.1186/s13059-016-0985-1.

Finkers-Tomczak A., Bakker E., Boer J., Vossen E., Achenbach U., Golas T., Suryaningrat S., Smant G., Bakker J., Goverse A. Comparative sequence analysis of the potato cyst nematode resistance locus H1 reveals a major lack of co-linearity between three haplotypes in potato (Solanum tuberosum ssp.) Theor. Appl. Genet. 2011;122:595608. DOI 10.1007/s00122-010-1472-9.

Finkers-Tomczak A., Danan S. van Dijk T., Beyene A., Bouwman L., Overmars H., van Eck H., Goverse A., Bakker J., Bakker E. A highresolution map of the Grp1 locus on chromosome V of potato harbouring broad-spectrum resistance to the cyst nematode species Globodera pallida and Globodera rostochiensis. Theor. Appl. Genet. 2009;119(1):165-173. DOI 10.1007/s00122-009-1026-1.

Flath K., Przetakiewicz J., van Rijswick P.C.J., Ristau V., van Leeuwen G.C.M. Interlaboratory tests for resistance to Synchytrium endobioticum in potato by the Glynne-Lemmerzahl method. EPPO Bull. 2014;44(3):510-517. DOI 10.1111/epp.12167.

Fournet S., Kerlan M.C., Renault L., Dantec J.P., Rouaux C., Montarry J. Selection of nematodes by resistant plants has implications for local adaptation and cross-virulence. Plant Pathology. 2013;62(1): 184-193. DOI 10.1111/j.1365-3059.2012.02617.x.

Gagnon M.C., van der Lee T.A., Bonants P.J., Smith D.S., Li X., Lé vesque C.A., Bilodeau G.J. Development of polymorphic microsatellite loci for potato wart from next-generation sequence data. Phytopathology. 2016;106(6):636-644. DOI 10.1094/PHYTO-1215-0317-R.

Galanova C.S. Rasprostranenie i vredonosnost’ vozbuditelya raka kartofelya [The prevalence and harmfulness of the potato wart pathogen]. Rak kartofelya i mery bor’by s nim [Potato wart and control measures]. Leningrad, Kolos Publ., 1964;5-22. (in Russian)

Galek R., Rurek M., De Jong W.S., Pietkiewicz G., Augustyniak H., Sawicka-Sienkiewicz E. Application of DNA markers linked to the potato H1 gene conferring resistance to pathotype Ro1 of Globodera rostochiensis. J. Appl. Genetics. 2011;52(4):407-411. DOI 10.1007/s13353-011-0056-y.

Gebhardt C. Bridging the gap between genome analysis and precision breeding in potato. Trends in Genetics. 2013;29(4):248-256. DOI 10.1016/j.tig.2012.11.006.

Gebhardt C., Bellin A., Henselewski A., Lehmann W., Schwarzfischer A., Valkonen J. Marker-assisted combination of major genes for pathogen resistance in potato. Theor. Appl. Genet. 2006;112:14581464. DOI 10.1007/s00122-006-0248-8.

Gebhardt C., Mugniery D., Ritter E., Salamini F., Bonnel E. Identification of RFLP markers closely linked to the H1 gene conferring resistance to Globodera rostochiensis in potato. Theor. Appl. Genet. 1993;85:541-544. DOI 10.1007/BF00220911.

Glynne M.D. Infection experiments with wart disease of potatoes Synchytrium endobioticum (Schilb.) Perc. Annals Appl. Biology. 1925; 12:34-60.

Guskova A.A. Diseases caused by nematodes. Diseases of cultivated plants. St.-Petersburg, 2005;204-215. (in Russian)

Hamilton J., Hansey C., Whitty B., Stoffel K., Massa A., Van Deynze A., De Jong W., Douches D., Buell C.R. Single nucleotide polymorphism discovery in elite North American potato germplasm. BMC Genom. 2011;12(1):302. DOI 10.1186/1471-2164-12-302.

Hampson M.C. A bioassay for Synchytrium endobioticum using micropropagated potato plantlets. Can. J. Plant Pathol. 1992;14:289-292.

Hampson М.С. History, biology and control of potato wart disease in Canada. Can. J. Plant Pathol. 1993;15:223-244.

Hawkes J.G. The Potato, Evolution, Biodiversity and Genetic Resources. Oxford, UK: Belhaven Press, 1990.

Hehl R., Faurie E., Hesselbach J., Salamini F., Witham S., Baker B., Gebhardt C. TMV resistance gene N homologues are linked to Synchytrium endobioticum resistance in potato. Theor. Appl. Genet. 1999;98:379-386. DOI 10.1007/s001220051083.

Jacobs J.M.E., van Eck H.J., Horsman K., Arens P.F.P., Verkerk-Bakker B., Jacobsen E., Pereira A., Stiekema W.J. Mapping of resistance to the potato cyst nematode Globodera rostochiensis from the wild potato species Solanum vernei. Mol. Breeding. 1996;2:51-60. DOI 10.1007/BF0017135.

Khiutti A., Afanasenko O., Antonova O., Shuvalov O., Novikova L., Krylova E., Chalaya N., Mironenko N., Spooner D., Gavrilenko T. Characterization of resistance to Synchytrium endobioticum in cultivated potato accessions from the collection of Vavilov Institute of Plant Industry. Plant Breeding. 2012;131(6):744-750. DOI 10.1111/j.1439-0523.2012.02005.x.

Köhler E. Methodische Bemerkungen zum Infektionsverfahren nach Spieckermann. Fortschritte der Landwirtschaft. 1927;2:115-118.

Kort J., Ross H., Rumpenhorst R.J., Stone A.R. An International scheme for identifying and classifying pathotypes of potato cystnematodes Globodera rostochiensis and G. pallida. Nematologica. 1977;23(3):333-339.

Kreike C.M., de Koning J.R.A., Vinke J.H., van Ooijen J.W., Gebhardt C., Stiekema W.J. Mapping of loci involved in quantitatively inherited resistance to the potato cyst-nematode Globodera rostochiensis pathotype Ro1. Theor. Appl. Genet. 1993;87:464-470.

Kreike C.M., Kok-Westeneng A.A., Vinke J.H., Stiekema W.J. Mapping of QTLs involved in nematode resistance, tuber yield and root development in Solanum sp. Theor. Appl. Genet. 1996;92:463-470.

Kubich A. Pytanie matwiku ziemniaczanum w Hollandui. Ochrona Roslin. 1963;4:11-13.

Kuzminova O.A., Staszewski Z. Vologin S.G., Gimaeva E.A. The study of potato breeding material using a molecular genetic analysis for the presence of genes for resistance to Globodera rostochiensis. Materialy Vseross. zaochnoj nauchno-prakt. konferencii molodyh uchenyh, posvjashhennoj pamjati R.G. Gareeva “Sovremennye tehnologii vyrashhivanija s/h kul’tur”. Kazan’ [Proceedings of the scientific-practical conference of young scientists dedicated to the memory of R.G.Gareev “Modern technologies of growing crops”], Kazan. 2015;88-97.

Laidlaw W.M.R. A method for the detection of the resting sporangia of potato wart disease (Synchytrium endobioticum) in the soil of old outbreak sites. Potato Res. 1985;28:223-232.

Langerfeld E., Stachewicz H. Assessment of varietal reactions to potato wart (Synchytrium endobioticum) in Germany. Bull. OEPP/EPPO Bull. 1994;24:793-798.

Lellbach H., Effmert M. Ergebnisse einer Diallelanalyse zur Vererung der Resistenz gegen Synchytrium endobioticum (Schilb.) Perc., pathotyp 1 (D1) bei Kartoffeln (Solanum tuberosum L.). Potato Res. 1990;33(2):251-256.

Lemmerzahl J. Neues vereinfachtes infektionsverfahren zur Prüfung von Kartoffelsorten auf Krebsfestigkeit. J. Lemmerzahl. Züchter. 1930;2:288-297.

Lemmerzahl J. Zur Methodik der Krebsprüfung von Kartoffelstämmen. Züchter. 1931;3:138-152.

Limantseva L., Mironenko N., Shuvalov O., Antonova O., Khiutti A., Novikova L., Afanasenko O., Spooner D., Gavrilenko T. Characterization of resistance to Globodera rostochiensis pathotype Ro1 in cultivated and wild potato species accessions from the Vavilov Institute of Plant Industry. Plant Breeding. 2014;133(5):660-665.

Lopez-Pardo R., Barandalla L., Ritter E., Ruiz de Galarreta J.I. Validation of molecular markers for pathogen resistance in potato. Plant Breeding. 2013;132(3):246-251. DOI 10.1111/pbr.12062.

Luksha V.I., Voronkova E.V., Gukasjan O.N., Ermishin A.P. Otsenka pervichnykh digaploidov S. tuberosum na nalichie genov ustoychivosti k boleznyam i vreditelyam metodom PTsR-analiza [Evaluation of primary dihaploids S. tuberosum for the presence of genes for resistance to diseases and pests by PCR analysis]. Molekulyarnaya i prikladnaya genetika. Sbornik nauchnyh trudov Instituta genetiki i citologii nacional’noj akademii nauk Belarusi. [Molecular and Applied Genetics. Bulletin of the Institute of Genetics and Cytology, National Academy of Sciences of Belarus]. Minsk, 2012;13:82-87.

Melnik P.A. Wart disease of potato, Synchytrium endobioticum (Schilbersky) Percival. 1998; EPPO Tech. Docum. No. 1032.

Milczarek D. A multiplex PCR method of detecting markers linked to genes conferring resistance to Globodera rostochiensis. Am. J. Potato Res. 2012;89(2):169-171. DOI 10.1007/s12230-011-9227-y.

Milczarek D., Flis B., Przetakiewicz А. Suitability of molecular markers for selection of potatoes resistant to Globodera spp. Am. J. Potato Res. 2011;88:245-255. DOI 10.1007/s12230-011-9189-0.

Milczarek D., Przetakiewicz A., Kaminski P., Flis B. Early selection of potato clones with the H1 resistance gene – the relation of nematode resistance to quality characteristics. Czech J. Genet. Plant Breeding. 2014;50(4):278-284.

Mimee B., Duceppe M-O., Véronneau P.-Y., Lafond-Lapalme J., Jean M., Belzile F., Bélair G. A new method for studying population genetics of cyst nematodes based on Pool-Seq and genomewide allele frequency analysis. Mol. Ecol. Res. 2015; DOI 10.1111/17550998.12412.

Mironenko N.V., Afanasenko O.S., Rogozina E.V. Variability of gene pool of Globodera rostochiensis Woll. population as a result of selection on weakly resistant potato hybrid clones. Vestnik zashchity rasteniy=Plant Protection News. 2015;2(84):24-28.

Mironenko N.V., Afanasenko O.S., Rogozina E.V., Limantseva L.A., Khyutti A.V., Antonova O.Yu., Shuvalov O.Yu., Novikova L.Yu., Gavrilenko T.A. Mechanisms of interaction of Globodera rostochiensis with the partially resistant interspecific potato hybrids. Vestnik zashchity rasteniy = Plant Protection News. 2013;4:37-42.

Mironenko N.V., Khyutti A.V., Afanasenko O.S. Characteristics of Synchytrium endobioticum populations on virulence, aggressiveness and DNA-markers. Mikologiya i fitopatologiya = Mycology and Phytopathology. 2009;43(5):460-469.

Mori K., Sakamoto Y., Mukojima N., Tamiya S., Naka T., Ishii T., Hosaka K. Development of a multiplex PCR method for simultaneous detection of diagnostic DNA markers of five disease and pest resistance genes in potato. Euphytica. 2011;18(3):347-355. DOI 10.1007/s10681-011-0381-6.

Mundt C.C. Durable resistance: a key to sustainable management of pathogens and pests. Infection, Genet. Evolution. 2014;27:446-455. DOI 10.1016/j.meegid.2014.01.011.

Niewöhner J., Salamini F., Gebhardt C. Development of PCR assays diagnostic for RFLP marker alleles closely linked to alleles Gro1 and H1, conferring resistance to the root cyst nematode Globodera rostochiensis in potato. Mol. Breeding. 1995;1(1):65-78.

Noble M., Glynne M.D. Wart disease of potatoes. FAO Plant Protection Bull. 1970;18(6):125-135.

Obidiegwu J.E., Flath K., Gebhardt C. Managing potato wart: a review of present research status and future perspective. Theor. Appl. Genet. 2014;127(4):763-780.

OEPP/EPPO. EPPO Standards PM 7/28. Diagnostic protocols for regulated pests: Synchytrium endobioticum. Bull. OEPP/EPPO Bull. 2004;34:213-218.

OEPP/EPPO. Testing of potato varieties to assess resistance to Globodera rostochiensis and Globodera pallida. Bull. OEPP/EPPO Bull. 2006;36:419-420.

Paal J., Henselewski H., Muth J., Meksem K., Menéndez C.M., Salamini F., Ballvora A., Gebhardt C. Molecular cloning of the potato Gro1-4 gene conferring resistance to pathotype Ro1 of the root cyst nematode Globodera rostochiensis, based on a candidate gene approach. Plant J. 2004;38(2):285-297.

Pariaud B., Ravigné V., Halkett F., Goyeau H., Carlier J., Lannou C. Aggressiveness and its role in the adaptation of plant pathogens. Plant Pathol. 2009;58(3):409-424. DOI 10.1111/j.1365-3059.2009.02039.x.

Parlevliet J.E., Zadoks J.C. The integrated concept of disease resistance: a new view including horizontal and vertical resistance in plants. Euphytica. 1977;26(1):5-21. DOI 10.1007/BF00032062.

Phillips M.S., Trudgill D.L. Variation in virulence, in terms of quantitative reproduction of Globodera pallida populations, from Europe and South America, in relation to resistance from Solanum vernei and S. tuberosum ssp. andigena CPC 2802. Nematologica. 1998;44: 409-423.

Pineda O., Bonierbale M.W., Plaisted R.L., Brodie B.B., Tanksley S.D. Identification of RFLP markers linked to the H1 gene conferring resistance to the potato cyst nematode Globodera rostochiensis. Genome. 1993;36(1):152-156.

Ponin I.Ya. K metodike ispytaniya sortov i seyantsev kartofelya na ustoychivost’ k kartofel’noy nematode [A method of testing varieties and potato seedlings for resistance to potato cyst nematode]. Materialy I Resp. konf. molodykh uchenykh [Proceedings of the First Republican Conference of Young Scientists]. Minsk, 1974;141-146.

Raffaele S., Kamoun S. Genome evolution in filamentous plant pathogens: why bigger can be better. Nature Reviews. Microbiology. 2012;10(6):417-430. DOI 10.1038/nrmicro2790.

Ramakrishnan A.P., Ritland C.E., Blas Sevillano R.H., Riseman A. Review of potato molecular markers to enhance trait selection. Am. J. Potato Res. 2015;92(4):455-472. DOI 10.1007/s12230-015-9455-7.

Rice S.L., Leadbeater B.S.C., Stone A.R. Changes in cell structure in roots of resistant potatoes parasitized by potato cyst-nematodes. I. Potatoes with resistance gene H1 derived from Solanum tuberosum ssp. andigena. Physiol. Plant Pathol. 1985;27(2):219-234. DOI 10.1016/0048-4059(85)90069-4.

Sattarzadeh A., Achenbach U., Lübeck J., Strahwald J., Tacke E., Hofferbert H.-R., Rothsteyn T., Gebhardt C. Single nucleotide polymorphism (SNP) genotyping as basis for developing a PCR based marker highly diagnostic for potato varieties with high resistance to Globodera pallida pathotype Pa2/3. Mol. Breeding. 2006;18(4):301-312. DOI 10.1007/s11032-006-9026-1.

Schultz L., Cogan N.О.I., McLean K., Dale M.F.B., Bryan G.J., Forster J.W., Slater A.T. Evaluation and implementation of a potential diagnostic molecular marker for H1-conferred potato cyst nematode resistance in potato (Solanum tuberosum L.). Plant Breeding. 2012;131:315-321. DOI 10.1111/j.1439-0523.2012.01949.x.

Spieckermann A., Kothoff P. Die Prüfung von Kartoffeln auf Krebsfestigkeit. Deutsche Landwirtschaftliche Presse. 1924;51:114-115.

Stone A.R. Co-evolution of potato cyst nematodes and their hosts: implications for pathotypes and resistance. Bull. OEPP/EPPO Bull. 1985;15:131-131. DOI 10.1111/j.1365-2338.1985.tb00212.x.

Takeuchi T., Sasaki J., Suzuki T., Horita H., Iketani S. High-resolution maps and DNA markers of the Potato virus Y resistance gene Rychc and the potato cyst nematode resistance gene H1. Breed. Res. 2008;10(1):148.

Toxopeus H.J., Huijsman C.A. Breeding for resistance to potato root eelworm. I. Preliminary data concerning the inheritance and the nature of resistance. Euphytica. 1953;2(3):180-186. DOI 10.1007/BF00053725.

Turner S.J., Fleming C.C. Multiple selection of potato cyst nematode Globodera pallida virulence on a range of potato species. I. Serial selection on Solanum-hybrids. Eur. J. Plant Pathol. 2002;108(5):461467. DOI 10.1023/A:1016018002152.

Van der Voort J.R., Wolters P., Folkertsma R., Hutten R., van Zandvoort P., Vinke H., Kanyuka K., Bendahmane A., Jacobsen E., Janssen R., Bakker J. Mapping of the cyst nematode resistance locus Gpa2 in potato using a strategy based on comigrating AFLP markers. Theor. Appl. Genet. 1997;95(5):874-880. DOI 10.1007/s001220050638.

Van der Vossen E.A.G., van der Voort J.R., Kanyuka K., Bendahmane A., Sandbrink H., Baulcombe D.C., Bakker J., Stiekema W.J., Klein-Lankhorst R.M. Homologues of a single resistance-gene cluster in potato confer resistance to distinct pathogens: a virus and a nematode. Plant J. 2000;23(5):567-576. DOI 10.1046/j.1365313x.2000.00814.x.

Whitehead A.G. Selection for virulence in the potato cyst-nematode, Globodera pallida. Annals Appl. Biology. 1991;118(2):395-402. DOI 10.1111/j.1744-7348.1991.tb05639.x.

Winslow R.D., Willis R.J. Nematode diseases of potatoes. II. Potato cyst nematode, Heterodera rostochiensis. Economic Nematology. Ed. J. Webster. N.Y.: Acad. Press, 1972;18-34.

Yakovleva V.I. Ispol’zovanie dikikh i kul’turnykh vidov pri vyvedenii rakoustoychivykh sortov kartofelya [The use of wild and cultivated species in breeding resistant potato varieties]. Rak kartofelya i mery bor’by s nim [Potato wart and control measures]. Leningrad, Kolos, 1964;62-77.

Yakovleva V.A., Dolyagin A.B. (Eds.). Polozhenie o poryadke ispytaniya sortov i gibridov kartofelya na ustoychivost’ k vozbuditelyu raka kartofelya (patotip I) i zolotistoy kartofel’noy nematode (patotip RoI) [Regulations on the testing of varieties and hybrids of potatoes for resistance to the agent of potato wart (pathotype I) and golden potato cyst nematode (pathotype Ro I)]. Moscow, 1993.

Yakovleva V.I., Saltykova L.P. The aggressiveness of the potato wart agent. Zaschita rasteniy = Plant Protection. 1966;7:51.

Yakovleva V.I., Saltykova L.P. (Eds.) Laboratornaya diagnostika rakoustoychivosti kartofelya metodom zarazheniya rostkov ot svezhikh rakovykh narostov (metodicheskie ukazaniya) [Laboratory diagnostics of wart resistance in potato by inoculation of sprouts with fresh wart material: guidelines]. Moscow, VASKhNIL Publ., 1979.

The authors declare that there are no conflicts of interest present.