Abstract
Genetic resistance is a valuable tool in the fight against late blight of potatoes but little is known about the stability and specificity of quantitative resistance including the effect of defeated major resistance genes. In the present study we investigated the effect of different isolates of Phytophthora infestans on the mode of action of R Pi-ber , an R-gene originating from Solanum berthaultii. The experiments were conducted on progenies derived from two reciprocal inter-specific backcrosses of Solanum tuberosum and S. berthaultii. The plant–pathogen interaction was tested in diverse environments including field, greenhouse and growth chamber conditions. The R Pi-ber gene provided complete resistance against a US8 isolate of P. infestans in all trials. When isolates compatible with R Pi-ber were used for inoculation, a smaller, but significant resistance effect was consistently detected in the same map position as the R-gene. This indicates that this R-gene provides a residual resistance effect, and/or that additional resistance loci are located in this genomic region of chromosome X. Additional quantitative resistance loci (QRL) were identified in the analyzed progenies. While some of the QRL (such as those near TG130 on chromosome III) were effective against several isolates of the pathogen, others were isolate specific. With a single exception, the S. berthaultii alleles were associated with a decrease in disease severity. Resistance loci reported in the present study co-locate with previously reported R-genes and QRL to P. infestans and other pathogens.
Similar content being viewed by others
References
Arru L, Francia E, Pecchioni N (2003) Isolate-specific QTLs of resistance to leaf stripe (Pyrenophora graminea) in the ‘Steptoe’ × ‘Morex’ spring barley cross. Theor Appl Genet 106:668–675
Bai Y, Huang CC, Van Der Hulst R, Meijer-Dekens F, Bonnema G, Lindhout P (2003) QTLs for tomato powdery mildew resistance (Oidium lycopersici) in Lycopersicon parviflorum G1.1601 co-localize with two qualitative powdery mildew resistance genes. Mol Plant Microbe Interact 16:169–176
Ballini E, Morel J-B, Droc G, Price A, Courtois B, Notteghem J-L, Tharreau D (2008) A genome-wide meta-analysis of Rice Blast resistance genes and quantitative trait loci provides new insights into partial and complete resistance. Mol Plant Microbe Interact 21:859–868
Ballvora A, Ercolano MR, WeiB J, Meksem K, Bormann CA, Oberhagemann P, Salamini F, Gebhardt C (2002) 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 30:361–371
Bonierbale MW, Plaisted RL, Tanksley SD (1988) RFLP maps based on a common set of clones reveal modes of chromosomal evolution in potato and tomato. Genetics 120:1095–1103
Bonierbale MW, Plaisted RL, Pineda O, Tanksley SD (1994) QTL analysis of trichome-mediated insect resistance in potato. Theor Appl Genet 87:973–987
Bormann CA, Rickert AM, Castillo Ruiz RA, Paal J, Lubeck J, Strahwald J, Buhr K, Gebhardt C (2004) Tagging quantitative trait loci for maturity-corrected late blight resistance in tetraploid potato with PCR-based candidate gene markers. Mol Plant Microbe Interact 17:1126–1138
Büchter R, Strömberg A, Schmelzer E, Kombrink E (1997) Primary structure and expression of acidic (class II) chitinase in potato. Plant Mol Biol 35:749–761
Calenge F, Faure A, Goerre M, Gebhardt C, Van De Weg WE, Parisi L, Durel CE (2004) Quantitative trait loci (QTL) analysis reveals both broad-spectrum and isolate-specific QTL for scab resistance in an apple progeny challenged with eight isolates of Venturia inaequalis. Phytopathology 94:370–379
Caranta C, Lefebvre V, Palloix A (1997) Polygenic resistance of pepper to potyviruses consists of a combination of isolate-specific and broad-spectrum quantitative trait loci. Mol Plant Microbe Interact 10:872–878
Caten CE, Jinks JL (1968) Spontaneous variability of single isolates of Phytophthora infestans. I. Cultural variation. Can J Bot 46:329–348
Celebi-Toprak F, Slack SA, Jahn M (2002) A new gene, Ny tbr , for hypersensitivity to Potato virus Y from Solanum tuberosum maps to chromosome IV. Theor Appl Genet 104:669–674
Chantret N, Pavoine MT, Doussinault G (1999) The race specific resistance gene to powdery mildew, MIRE, has a residual effect on adult plant resistance of winter wheat line RE714. Phytopathology 89:533–539
Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971
Collins A, Milbourne D, Ramsay L, Meyer R, Chatot-Balandras C, Oberhagemann P, Jong WD, Gebhardt C, Bonnel E, Waugh R (1999) QTL for field resistance to late blight in potato are strongly correlated with maturity and vigour. Mol Breed 5:387–398
Dowkiw A, Bastien C (2007) Presence of defeated qualitative resistance genes frequently has major impact on quantitative resistance to Melampsora larici-populina leaf rust in P. × interamericana hybrid poplars. Tree Genetics Genomes 3:261–274
Durel CE, Parisi L, Laurens F, Venisse JS, Jourjon MF (2000) Does the Vf gene maintain a residual resistance to apple scab despite its breakdown by Venturia inequalis race 6 strains. Acta Hortic 539:575–580
Ewing EE, Simko I, Smart CD, Bonierbale MW, Mizubuti ESG, May GD, Fry WE (2000) Genetic mapping of qualitative and quantitative field resistance to Phytophthora infestans in a population derived from Solanum tuberosum and Solanum berthaultii. Mol Breed 6:25–36
Ewing EE, Simko I, Omer EA, Davies PJ (2004) Polygene mapping as a tool to study the physiology of potato tuberization and dormancy. Am J Potato Res 81:281–289
Fry WE (1978) Quantification of general resistance to potato cultivars and fungicide effects for integrated control of potato late blight. Phytopathology 68:1650–1655
Fry W (2008) Phytophthora infestans: the plant (and R-gene) destroyer. Mol Plant Pathol 9:385–402
Fry WE, Goodwin SB (1997) Resurgence of the Irish potato famine fungus. Bioscience 47:363–371
Gebhardt C, Valkonen JPT (2001) Organization of genes controlling disease resistance in the potato genome. Annu Rev Phytopathol 39:79–102
Gebhardt C, Ritter E, Barone A, Debener T, Walkemeier B, Schachtschabel U, Kaufmann H, Thompson RD, Bonierbale MW, Ganal MW, Tanksley SD, Salamini F (1991) RFLP maps of potato and their alignment with the homoeologus tomato genome. Theor Appl Genet 83:49–57
Geffroy V, Sevignac M, De Oliveira JCF, Fouilloux G, Skroch P, Thoquet P, Gepts P, Langin T, Dron M (2000) Inheritance of partial resistance against Colletotrichum lindemuthianum in Phaseolus vulgaris and co-localization of quantitative trait loci with genes involved in specific resistance. Mol Plant Microbe Interact 13:287–296
Ghislain M, Trognitz B, Herrera MDR, Solis J, Casallo G, Vasquez C, Hurtado O, Castillo R, Portal L, Orrillo M (2001) Genetic loci associated with field resistance to late blight in offspring of Solanum phureja and S. tuberosum grown under short-day conditions. Theor Appl Genet 103:433–442
Grube RC, Radwanski ER, Jahn M (2000) Comparative genetics of disease resistance within the Solanaceae. Genetics 155:873–887
Grünwald NJ, Romero Montes G, Lozoya Saldaña H, Rubio Covarrubias OA, Fry WE (2002) Potato late blight management in the Toluca valley: field validation of SimCast modified for cultivars with high field resistance. Plant Dis 86:1163–1168
Guenthner J, Michael K, Nolte P (2001) The economic impact of potato late blight on US growers. Potato Res 44:121–125
Harborne JB (1986) Systematic significance of variations in defense chemistry in the Solanaceae. In: D’Arcy WG (ed) Solanaceae: biology and systematics. Columbia University Press, New York, pp 328–344
Harrison JG, Lowe R (1994) Effects of temperature and light on non-race-specific resistance of potato leaflets to late blight. Plant Pathol 43:733–739
Hein I, Birch PRJ, Danan S, Lefebvre V, Odeny DA, Gebhardt C, Trognitz F, Bryan GJ (2009) Progress in mapping and cloning qualitative and quantitative resistance against Phytophthora infestans and its wild relatives. Potato Res 52:215–227
Huang L, Backhouse D (2005) Induction of defence responses in roots and mesocotyls of sorghum seedlings by inoculation with Fusarium thapsinum and F. proliferatum, wounding and light. J Phytopathol 153:522–529
Joehanes R, Nelson JC (2008) QGene 4.0, an extensible Java QTL-analysis platform. Bioinformatics. doi:10.1093/bioinformatics/btn523
Johnson ET, Berhow MA, Dowd PF (2008) Colored and white sectors from star-patterned petunia flowers display differential resistance to corn earworm and cabbage looper larvae. J Chem Ecol 34:757–765
Jung CS, Griffiths HM, De Jong DM, Cheng S, Bodis M, De Jong WS (2005) The potato P locus codes for flavonoid 3′,5′-hydroxylase. Theor Appl Genet 110:269–275
Konieczny A, Ausubel FM (1993) A procedure for mapping Arabidopsis mutations using codominant ecotype-specific PCR-based markers. Plant J 4:403–410
Kover PX, Caicedo AL (2001) The genetic architecture of disease resistance in plants and the maintenance of recombination by parasites. Mol Ecol 10:1–16
Leonards-Schippers C, Gieffers W, Schafer-Pregl R, Ritter E, Knapp S, Salamini F, Gebhardt C (1994) Quantitative resistance to Phytophthora infestans in Potato: a case study for QTL mapping in an allogamous plant species. Genetics 137:67–77
Lorenzen JH, Ewing EE (1990) Changes in tuberization and assimilate partitioning in potato (Solanum tuberosum) during the first 18 days of photoperiod treatment. Ann Bot 66:457–464
Mackay TFC (2001) The genetic architecture of quantitative traits. Annu Rev Genet 35:303–339
Manly KF, Cudmore JRH, Meer JM (2001) Map Manager QTX, cross platform software for genetic mapping. Mamm Genome 12:930–932
Marcel TC, Gorguet B, Ta MT, Kohutova Z, Vels A, Niks RE (2008) Isolate specificity of quantitative trait loci for partial resistance of barley to Puccinia hordei confirmed in mapping populations and near-isogenic lines. New Phytol 177:743–755
Marczewski W, Hennig J, Gebhardt C (2002) The Potato virus S resistance gene Ns maps to potato chromosome VIII. Theor Appl Genet 105:564–567
Marczewski W, Strzelczyk-Zyta D, Hennig J, Witek K, Gebhardt C (2006) Potato chromosomes IX and XI carry genes for resistance to Potato virus M. Theor Appl Genet 112:1232–1238
Meksem K, Leister D, Peleman J, Zabeau M, Salamini F, Gebhardt C (1995) A high resolution map of the vicinity of the R1 locus on chromosome V of potato based on RFLP and AFLP markers. Mol Gen Genet 249:74–81
Mihovilovich E, Munive S, Bonierbale M (2010) Influence of day-length and isolates of Phytophthora infestans on field resistance to late blight of potato. Theor Appl Genet 120:1265–1278
Nelson RR (1978) Genetics of horizontal resistance to plant diseases. Annu Rev Phytopathol 16:359–378
Oberhagemann P, Chatot-Balandras C, Schafer-Pregl R, Wegener D, Palomino C, Salamini F, Bonnel E, Gebhardt C (1999) A genetic analysis of quantitative resistance to late blight in potato: towards marker-assisted selection. Mol Breed 5:399–415
Park TH, Vleeshouwers VGAA, Jacobsen E, van der Vossen E, Visser RGF (2009) Molecular breeding for resistance to Phytophthora infestans (Mont.) de Bary in potato (Solanum tuberosum L.): a perspective of cisgenesis. Plant Breed 128:109–117
Pel MA, Foster SJ, Park T-H, Rietman H, van Arkel G, Jones JDG, Van Eck HJ, Jacobsen E, Visser RGF, Van der Vossen EAG (2009) Mapping and cloning of late blight resistance genes from Solanum venturii using an interspecific candidate gene approach. Mol Plant Microbe Interact 22:601–615
Perchepied L, Bardin M, Dogimont C, Pitrat M (2005a) Relationship between loci conferring downy mildew and powdery mildew resistance in melon assessed by quantitative trait loci mapping. Phytopathology 95:556–565
Perchepied L, Dogimont C, Pitrat M (2005b) Strain-specific and recessive QTLs involved in the control of partial resistance to Fusarium oxysporum f. sp. melonis race 1.2 in a recombinant inbred line population of melon. Theor Appl Genet 111:65–74
Pilet F, Pelle R, Ellisseche D, Andrivon D (2005) Efficacy of the R2 resistance gene as a component for the durable management of potato late blight in France. Plant Pathol 54:723–732
Rauscher GM, Smart CD, Simko I, Bonierbale M, Mayton H, Greenland A, Fry WE (2006) Characterization and mapping of R Pi-ber , a novel potato late blight resistance gene from Solanum berthaultii. Theor Appl Genet 112:674–687
Robertson DS (1985) A possible technique for isolating genomic DNA for quantitative traits in plants. J Theor Biol 117:1–10
Sato M, Nishikawa K, Komura K, Hosaka K (2006) Potato virus Y resistance gene, Ry chc , mapped to the distal end of potato chromosome 9. Euphytica 149:367–372
Shaner G, Finney RE (1977) The effect of nitrogen fertilization on the expression of slow-mildewing resistance in Knowx wheat. Phytopathology 67:1051–1056
Simko I (2002) Comparative analysis of quantitative trait loci for foliage resistance to Phytophthora infestans in tuber-bearing Solanum species. Am J Potato Res 79:125–132
Simko I, Vreugdenhil D, Jung CS, May GD (1999) Similarity of QTLs detected for in vitro and greenhouse development of potato plants. Mol Breed 5:417–428
Śliwka J, Jakuczun H, Lebecka R, Marczewski W, Gebhardt C, Zimnoch-Guzowska E (2007) Tagging QTLs for late blight resistance and plant maturity from diploid wild relatives in a cultivated potato (Solanum tuberosum) background. Theor Appl Genet 115:101–112
Smilde WD, Brigneti G, Jagger L, Perkins S, Jones JDG (2005) Solanum mochiquense chromosome IX carries a novel late blight resistance gene Rpi-moc1. Theor Appl Genet 110:252–258
Song Y, Hepting L, Schweizer G, Hartl L, Wenzel G, Schwarzfischer A (2005) Mapping of extreme resistance to PVY (Ry sto ) on chromosome XII using anther-culture-derived primary dihaploid potato lines. Theor Appl Genet 111:879–887
Stewart HE, Bradshaw JE, Pande B (2003) The effect of the presence of R-genes for resistance to late blight (Phytophthora infestans) of potato (Solanum tuberosum) on the underlying level of field resistance. Plant Pathol 52:193–198
Szajko K, Chrzanowska M, Witek K, Strzelczyk-Zyta D, Zagorska H, Gebhardt C, Hennig J, Marczewski W (2008) The novel gene Ny-1 on potato chromosome IX confers hypersensitive resistance to Potato virus Y and is an alternative to Ry genes in potato breeding for PVY resistance. Theor Appl Genet 116:297–303
Talukder ZI, Tharreau D, Price AH (2004) Quantitative trait loci analysis suggests that partial resistance to rice blast is mostly determined by race-specific interactions. New Phytol 162:197–209
Tan MYA, Hutten RCB, Celis C, Park TH, Niks RE, Visser RGF, van Eck HJ (2008) The R Pi-mcd1 locus from Solanum microdontum involved in resistance to Phytophthora infestans, causing a delay in infection, maps on potato chromosome 4 in a cluster of NBS-LRR genes. Mol Plant Microbe Interact 21:909–918
Tan MYA, Park TH, Alles R, Hutten RCB, Visser RGF, van Eck HJ (2009) GpaXI l tar originating from Solanum tarijense is a major resistance locus to Globodera pallida and is localised on chromosome 11 of potato. Theor Appl Genet 119:1477–1487
Tanksley SD (1993) Mapping polygenes. Annu Rev Genet 27:205–233
Tanksley SD, Ganal MW, Prince JP, de Vicente MC, Bonierbale MW, Broun P, Fulton TM, Giovanoni JJ, Grandillo S, Martin GB, Messenger R, Miller JC, Miller L, Paterson AH, Pineda O, Roder MS, Wing RA, Wu W, Young ND (1992) High density molecular linkage maps of the tomato and potato genomes. Genetics 132:1141–1160
Tian ZD, Liu J, Wang BL, Xie CH (2006) Screening and expression analysis of Phytophthora infestans induced genes in potato leaves with horizontal resistance. Plant Cell Rep 25:1094–1103
Trognitz F, Manosalva P, Gysin R, Nino-Liu D, Simon R, Herrera MD, Trognitz B, Ghislain M, Nelson R (2002) Plant defense genes associated with quantitative resistance to potato late blight in Solanum phureja × dihaploid S. tuberosum hybrids. Mol Plant Microbe Interact 15:587–597
Umaerus V, Umaerus M (1994) Inheritance of resistance to late blight. In: Bradshaw JE, Mackay GR (eds) Potato genetics. CAB International, Oxon, pp 365–401
USDA, ARS (1999) National Germplasm Resources Laboratory, Beltsville, Maryland. National genetic resources program. Germplasm Resources information network (GRIN). Available at http://www.ars-grin.gov/cgi-bin/npgs/html/taxgenform.pl
van den Berg JH, Ewing EE, Plaisted RL, McMurry S, Bonierbale MW (1996) QTL analysis of potato tuberization. Theor Appl Genet 93:307–316
van Eck HJ, Jacobs JME, van Dijk J, Skitema WJ, Jacobsen E (1993) Identification and mapping of three flower colour loci of potato (S. tuberosum L.) by RFLP analysis. Theor Appl Genet 86:295–300
van Eck HJ, Jacobs JME, van den Berg PMMM, Skitema WJ, Jacobsen E (1994) The inheritance of anthocyanin pigmentation in potato (Solanum tuberosum L.) and mapping of tuber skin colour using loci using RFLPs. Heredity 73:410–421
van Ooijen J (1999) LOD significance thresholds for QTL analysis in experimental populations of diploid species. Heredity 83:613–624
Velásquez AC, Mihovilovich E, Bonierbale M (2007) Genetic characterization and mapping of major gene resistance to Potato leafroll virus in Solanum tuberosum ssp. andigena. Theor Appl Genet 114:1051–1058
Visker M, Keizer LCP, Van Eck HJ, Jacobsen E, Colon LT, Struik PC (2003) Can the QTL for late blight resistance on potato chromosome 5 be attributed to foliage maturity type? Theor Appl Genet 106:317–325
Wastie RL (1991) Breeding for resistance. Adv Plant Pathol 7:193–223
Wernham CC (1946) Mineral oil as a fungus preservative. Mycologia 38:691–692
Woo KS, Newcombe G (2003) Absence of residual effects of a defeated resistance gene in poplar. Forest Pathol 33:81–89
Young ND (1996) QTL mapping and quantitative disease resistance in plants. Annu Rev Phytopathol 34:479–501
Acknowledgments
This study was supported by Syngenta. We want to thank John Cianchietti, Kevin Myers, Barbara Esposito, Phoi Tran, and Karen Moravec for their help on the field experiments. Clare Nelson provided valuable insight on data analyses. We also wish to thank Jason Rauscher for critical reading and suggestions on the manuscript. Thanks also to Hector Lozoya-Saldaña and PICTIPAPA for supporting field research in Mexico.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by R. Visser.
Rights and permissions
About this article
Cite this article
Rauscher, G., Simko, I., Mayton, H. et al. Quantitative resistance to late blight from Solanum berthaultii cosegregates with R Pi-ber : insights in stability through isolates and environment. Theor Appl Genet 121, 1553–1567 (2010). https://doi.org/10.1007/s00122-010-1410-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-010-1410-x