Abstract
The R1 gene for resistance to oomycete Phytophthora infestans (Mont.) de Bary, the causal agent of late blight disease of potato (Solanum tuberosum L.), was initially identified in S. demissum and potato varieties bred by introgressing the S. demissum germplasm. Later a sequence characterized amplified region (SCAR) marker R1-1205 of this gene was also found in S. stoloniferum and S. polytrichon. Here we describe the full-length R1 sequence cloned from S. stoloniferum. This sequence is translatable, and this evidence of structural gene integrity is reinforced by functional characterization of the S. stoloniferum R1 gene in an effectoromics experiment. When screened across a series of S. demissum and S. stoloniferum accessions, the R1 sequences differed by several single nucleotide polymorphisms and an indel; this indel served the basis for constructing SCAR markers R1-517 and R1-513 that reliably discerned two R1 orthologs. The demissum-specific marker R1-517 was found in all S. demissum accessions under study; it was also present in many demissum-derived potato varieties and hybrids. The stoloniferum-specific marker R1-513 was found in 27% of S. stoloniferum and S. polytrichon accessions; however, we failed to discern this marker in the genotypes of cultivated potato listing S. stoloniferum in their pedigrees. Most probably, such absence of R1-513 is best explained by an opportunistic breeding history of stoloniferum-derived founder lines, which were employed first and foremost in breeding for resistance to potato virus Y: eventually, these founder lines are devoid of the R1 gene.
Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.Abbreviations
- bp:
-
base pairs
- LB:
-
late blight
- PVY:
-
potato virus Y
- SCAR:
-
Sequence Characterized Amplified Region
References
Śliwka, J. and Zimnoch-Guzowska, E., Resistance to late blight in potato, in Translational Genomics for Crop Breeding, vol. 1: Biotic Stress, Varshney, R.K. and Tuberosa, R., Eds., Wiley-Blackwell, 2013, pp. 221–240.
Jo, R.R., Zhu, S., Bai, Y., Hutten, R.C.B., Kessel, G.J.T., Vleeshouwers, V.G.A.A., Jacobsen, E., Visser, R.G.F., and Vossen, J.H., Problematic crops. 1. Potatoes: towards sustainable potato late blight resistance by cisgenic R gene pyramiding, in Plant Pathogen Resistance Biotechnology, Collinge, D.B., Ed., New York: Wiley, 2016, pp. 171–191.
Cooke, D.E.L., Cano, L.M., Raffaele, S., Bain, R.A., Cooke, L.R., Etherington, G.J., Deahl, K.L., Farrer, R.A., Gilroy, E.M., Goss, E.M., Grünwald, N.J., Hein, I., MacLean, D., McNicol, J.W., Randall, E., et al., Genome analyses of an aggressive and invasive lineage of the Irish Potato Famine pathogen, PLoS Pathog., 2012, vol. 8, p. e1002940. doi 10.1371/journal.ppat.1002940
Ballvora, A., Ercolano, M.R., Weiss, J., Meksem, K., Bormann, C.A., Oberhagemann, P., Salamini, F., and Gebhardt, C., The R1 gene for potato resistance to late blight (Phytophthora infestans) belongs to the leucine zipper/NBS/LRR class of plant resistance genes, Plant J., 2002, vol. 30, pp. 361–371.
Leonards-Schippers, C., Gieffers, W., Gebhardt, C., and Salamini, F., The R1 gene conferring race-specific resistance to Phytophtora infestans in potato is located on potato chromosome V, Mol. Gen. Genet., 1992, vol. 233, pp. 278–283.
Kuang, H., Wei, F., Marano, M.R., Wirtz, U., Wang, X., Liu, J., Shum, W.P., Zaborsky, J., Tallon, L.J., Rensink, W., Lobst, S., Zhang, P., Tornqvist, C.E., Tek, A., Bamberg, J., et al., The R1 resistance gene cluster contains three groups of independently evolving, type I R1 homologues and shows substantial structural variation among haplotypes of Solanum demissum, Plant J., 2005, vol. 44, pp. 37–51.
Ballvora, A., Jocker, A., Viehover, P., Ishihara, H., Paal, J., Meksem, K., Bruggmann, R., Schoof, H., Weisshaar, B., and Gebhardt, C., Comparative sequence analysis of Solanum and Arabidopsis in a hot spot for pathogen resistance on potato chromosome V reveals a patchwork of conserved and rapidly evolving genome segments, BMC Genomics, 2007, vol. 8, p. 112. doi 10.1186/1471-2164-8-112
Gyetvai, G., Sønderkær, M., Göbel, U., Basekow, R., Ballvora, A., Imhoff, M., Kersten, B., Nielsen, K.-M., and Gebhardt, C., The transcriptome of compatible and incompatible interactions of potato (Solanum tuberosum) with Phytophthora infestans revealed by DeepSAGE analysis, PLoS One, 2012, vol. 7, p. e31526. doi 10.1371/journal.pone.0031526
Gebhardt, C., Ballvora, A., Walkemeier, B., Oberhagemann, P., and Schüler, K., Assessing genetic potential in germplasm collections of crop plants by marker-trait association: a case study for potatoes with quantitative variation of resistance to late blight and maturity type, Mol. Breed., 2004, vol. 13, pp. 93–102.
Beketova, M.P., Drobyazina, P.E., and Khavkin, E.E., The R1 gene for late blight resistance in early and late maturing potato cultivars, Russ. J. Plant Physiol., 2006, vol. 53, pp. 384–389.
Ross, H., Potato Breeding Problems and Perspectives, Hamburg: Paul Parey, 1986.
Świeżyński, K.M. and Zimnoch-Guzowska, E., Breeding potato cultivars with tubers resistant to Phytophthora infestans, Potato Res., 2001, vol. 44, pp. 97–117.
Bradshaw, J.E., Bryan, G.J., and Ramsay, G., Genetic resources (including wild and cultivated Solanum species) and progress in their utilization in potato breeding, Potato Res., 2006, vol. 49, pp. 49–65.
Kiru, S.D., Gavrilenko, T.A., Kostina, L.I., Rogozina, E.V., Antonova, O.Y., Truskinov, E.V., Shvachko, N.A., Krylova, E.A., and Smirnova, A.B., Conservation, evaluation and use in breeding of potato genetic diversity at the N.I. Vavilov Institute of Plant Industry (VIR), in Potato Production and Innovative Technologies, Havercort, A. and Anisimov, B., Eds., Wageningen: Wageningen Acad. Publ., 2007, pp. 353–363.
Sokolova, E., Pankin, A., Beketova, M., Kuznetsova, M., Spiglazova, S., Rogozina, E., Yashina, I., and Khavkin, E., SCAR markers of the R-genes and germplasm of wild Solanum species for breeding late blightresistant potato cultivars, Plant Genet. Res., 2011, vol. 9, pp. 309–312.
Solomon-Blackburn, R.M. and Barker, H., Breeding virus resistant potatoes (Solanum tuberosum): a review of traditional and molecular approaches, Heredity, 2001, vol. 86, pp. 17–35.
Valkonen, J.P.T., Wiegmann, K., Hämäläinen, J.H., Marczewski, W., and Watanabe, K.N., Evidence for utility of the same PCR based markers for selection of extreme resistance to Potato virus Y controlled by Ry sto of Solanum stoloniferum derived from different sources, Ann. Appl. Biol., 2008, vol. 152, pp. 121–130.
Flis, B., Hennig, J., Strzelczyk-Zyta, D., Gebhardt, C., and Marczewski, W., The Ry-f sto gene from Solanum stoloniferum for extreme resistance to Potato virus Y maps to potato chromosome XII and is diagnosed by PCR marker GP122718 in PVY resistant potato cultivars, Mol. Breed., 2005, vol. 15, pp. 95–101.
Song, Y.S. and Schwarzfischer, A., Development of STS markers for selection of extreme resistance (Ry sto) to PVY and maternal pedigree analysis of extremely resistant cultivars, Am. J. Potato Res., 2008, vol. 85, pp. 159–170.
Zimnoch-Guzowska, E., Yin, Z., Chrzanowska, M., and Flis, B., Sources and effectiveness of potato PVY resistance in IHAR’s breeding research, Am. J. Potato Res., 2013, vol. 90, pp. 21–27.
Fadina, O.A., Beketova, M.P., Sokolova, E.A., Kuznetsova, M.A., Smetanina, T.I., Rogozina, E.V., and Khavkin, E.E., Anticipatory breeding: molecular markers as a tool in developing donors of potato late blight resistance from complex interspecific hybrids, Sel’skokhozyaistvennaya Biologiya (Agric. Biol.), 2017, vol. 52, pp. 84–94.
Simakov, E.A., Sklyarova, N.P., and Yashina, I.M., Manual in Potato Breeding Technologies, Moscow: Dostizheniya Nauki i Tekhniki APK, 2006.
Doyle, J.J. and Doyle, J.L., A rapid DNA isolation procedure for small quantities of fresh leaf tissue, Phytochem. Bull., 1987, vol. 19, pp. 11–15.
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S., MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods, Mol. Biol. Evol., 2011, vol. 28, pp. 2731–2739.
Rietman, H., Putting the Phytophthora infestans genome sequence at work; multiple novel avirulence and potato resistance gene candidates revealed, PhD Thesis, Wageningen: Wageningen Univ., 2011.
Spooner, D.M., Ghislain, M., Simon, R., and Gavrilenko, T.F., Systematics, diversity, genetics, and evolution of wild and cultivated potatoes, Bot. Rev., 2014, vol. 80, pp. 283–383.
Hanneman, R. and Bamberg, J., Inventory of Tuber-Bearing Solanum Species, Wisconsin: Potato Introduction Station, 1986.
Aversano, R., Contaldi, F., Ercolano, M.R., Grosso, V., Iorizzo, M., Tatino, F., Xumerle, L., Dal, M.A., Avanzato, C., Ferrarini, A., Delledonne, M., Sanseverino, W., Cigliano, R.A., Capella-Gutierrez, S., Gabaldón, T., et al., The Solanum commersonii genome sequence provides insights into adaptation to stress conditions and genome evolution of wild potato relatives, Plant Cell, 2015, vol. 27, pp. 954–968.
Bradshaw, J.E., Potato breeding at the Scottish Plant Breeding Station and the Scottish Crop Research Institute: 1920–2008, Potato Res., 2009, vol. 52, pp. 141–172.
Palmgren, M.G., Edenbrandt, A.K., Vedel, S.E., Andersen, M.M., Landes, X., Østerberg, J.T., Falhof, J., Olsen, L.I., Christensen, S.B., Sandøe, P., Gamborg, C., Kappel, K., Thorsen, B.J., and Pagh, P., Are we ready for back-to-nature crop breeding? Trends Plant Sci., 2015, vol. 20, pp. 155–164.
Author information
Authors and Affiliations
Corresponding author
Additional information
Published in Russian in Fiziologiya Rastenii, 2017, Vol. 64, No. 5, pp. 372–382.
The article was translated by the authors.
Rights and permissions
About this article
Cite this article
Beketova, M.P., Sokolova, E.A., Rogozina, E.V. et al. Two orthologs of late blight resistance gene R1 in wild and cultivated potato. Russ J Plant Physiol 64, 718–727 (2017). https://doi.org/10.1134/S1021443717050028
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1021443717050028


