Abstract
Powdery mildew is one of the most important wheat diseases in temperate regions of the world. Resistance breeding is considered to be an economical and environmentally benign way to control this disease. The German spring wheat cv. ‘Naxos’ exhibits high levels of partial and race non-specific resistance to powdery mildew in the field and is a valuable source in resistance breeding. The main objective of the present study was to map the genetic factors behind the resistance in Naxos, based on a population of recombinant inbred lines (RIL) from a cross with the susceptible CIMMYT breeding line SHA3/CBRD. Powdery mildew severity was evaluated in six field trials in Norway and four field trials in China. The major quantitative trait locus (QTL) with resistance from Naxos was detected close to the Pm3 locus on 1AS in all environments, and explained up to 35% of the phenotypic variation. Naxos was shown to carry another major QTL on 2DL and minor ones on 2BL and 7DS. QTL with resistance from SHA3/CBRD were detected on 1RS, 2DLc, 6BL and 7AL. The QTL on the 1B/1R translocation showed highly variable effects across environments corresponding to known virulence differences against Pm8. SHA3/CBRD was shown to possess the Pm3 haplotype on 1AS, but none of the known Pm3a-g alleles. The RIL population did not provide any evidence to suggest that the Pm3 allele of SHA3/CBRD acted as a suppressor of Pm8.
Similar content being viewed by others
References
Bjarko ME, Line RF (1988) Heritability and number of genes controlling leaf rust resistance in four cultivars of wheat. Phytopathology 78(4):457–461
Blanco A, Gadaleta A, Cenci A, Carluccio AV, Abdelbacki AMM, Simeone R (2008) Molecular mapping of the novel powdery mildew resistance gene Pm36 introgressed from Triticum turgidum var. dicoccoides in durum wheat. Theor Appl Genet 117(1):135–142
Börner Schumann, Fürste Cöster, Leithold Röder, Weber (2002) Mapping of quantitative trait loci determining agronomic important characters in hexaploid wheat (Triticum aestivum L.). Theor Appl Genet 105(6):921–936. doi:10.1007/s00122-002-0994-1
Bossolini E, Krattinger S, Keller B (2006) Development of simple sequence repeat markers specific for the Lr34 resistance region of wheat using sequence information from rice and Aegilops tauschii. Theor Appl Genet 113(6):1049–1062. doi:10.1007/s00122-006-0364-5
Bougot Y, Lemoine J, Pavoine MT, Guyomar’ch H, Gautier V, Muranty H, Barloy D (2006) A major QTL effect controlling resistance to powdery mildew in winter wheat at the adult plant stage. Plant Breeding 125(6):550–556
Chantret N, Sourdille P, Roder M, Tavaud M, Bernard M, Doussinault G (2000) Location and mapping of the powdery mildew resistance gene MIRE and detection of a resistance QTL by bulked segregant analysis (BSA) with microsatellites in wheat. Theor Appl Genet 100(8):1217–1224
Chantret N, Mingeot D, Sourdille P, Bernard M, Jacquemin JM, Doussinault G (2001) A major QTL for powdery mildew resistance is stable over time and at two development stages in winter wheat. Theor Appl Genet 103(6–7):962–971
Conner RL, Kuzyk AD, Su H (2003) Impact of powdery mildew on the yield of soft white spring wheat cultivars. Can J Plant Sci 83(4):725–728
Duan XY, Sheng BQ (1998) Identification of isolates of Blumeria graminis f. sp. tritici and the monitoring of their virulence frequencies. Acta Phytopathol Sinica 25:31–36
Fu DL, Uauy C, Distelfeld A, Blechl A, Epstein L, Chen XM, Sela HA, Fahima T, Dubcovsky J (2009) A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science 323(5919):1357–1360. doi:10.1126/science.1166289
Griffey CA, Das MK, Stromberg EL (1993) Effectiveness of adult-plant resistance in reducing grain yield loss to powdery mildew in winter wheat. Plant Dis 77(6):618–622
Hanusova R, Hsam SLK, Bartos P, Zeller FJ (1996) Suppression of powdery mildew resistance gene Pm8 in Triticum aestivum L. (common wheat) cultivars carrying wheat-rye translocation T1BL.1RS. Heredity 77:383–387
He ZH, Rajaram S, Xin ZY, Huang GZ (2001) A history of wheat breeding in China. CIMMYT, Mexico
He RL, Chang ZJ, Yang ZJ, Yuan ZY, Zhan HX, Zhang XJ, Liu JX (2009) Inheritance and mapping of powdery mildew resistance gene Pm43 introgressed from Thinopyrum intermedium into wheat. Theor Appl Genet 118(6):1173–1180
Herrera-Foessel S, Lagudah E, Huerta-Espino J, Hayden M, Bariana H, Singh D, Singh R (2011) New slow-rusting leaf rust and stripe rust resistance genes Lr67 and Yr46 in wheat are pleiotropic or closely linked. Theor Appl Genet 122(1):239–249. doi:10.1007/s00122-010-1439-x
Hua W, Liu ZJ, Zhu J, Xie CJ, Yang TM, Zhou YL, Duan XY, Sun QX, Liu ZY (2009) Identification and genetic mapping of pm42, a new recessive wheat powdery mildew resistance gene derived from wild emmer (Triticum turgidum var. dicoccoides). Theor Appl Genet 119(2):223–230
Huang XQ, Röder MS (2004) Molecular mapping of powdery mildew resistance genes in wheat: a review. Euphytica 137(2):203–223
Hysing SC, Merker A, Liljeroth E, Koebner RMD, Zeller FJ, Hsam SLK (2007) Powdery mildew resistance in 155 Nordic bread wheat cultivars and landraces. Hereditas 144(3):102–119
Keller M, Keller B, Schachermayr G, Winzeler M, Schmid JE, Stamp P, Messmer MM (1999) Quantitative trait loci for resistance against powdery mildew in a segregating wheat × spelt population. Theor Appl Genet 98(6–7):903–912
Koebner RMD (1995) Generation of PCR-based markers for the detection of rye chromatin in a wheat background. Theor Appl Genet 90(5):740–745
Kolmer JA (1996) Genetics of resistance to wheat leaf rust. Annu Rev Phytopathol 34:435–455
Lagudah ES, Krattinger SG, Herrera-Foessel S, Singh RP, Huerta-Espino J, Spielmeyer W, Brown-Guedira G, Selter LL, Keller B (2009) Gene-specific markers for the wheat gene Lr34/Yr18/Pm38 which confers resistance to multiple fungal pathogens. Theor Appl Genet 119(5):889–898. doi:10.1007/s00122-009-1097-z
Lan CX, Liang SS, Wang ZL, Yan J, Zhang Y, Xia XC, He ZH (2009) Quantitative trait loci mapping for adult-plant resistance to powdery mildew in Chinese wheat cultivar Bainong 64. Phytopathology 99(10):1121–1126. doi:10.1094/phyto-99-10-1121
Lan CX, Ni XW, Yan J, Zhang Y, Xia XC, Chen XM, He ZH (2010) Quantitative trait loci mapping of adult-plant resistance to powdery mildew in Chinese wheat cultivar Lumai 21. Mol Breeding 25(4):615–622
Liang SS, Suenaga K, He ZH, Wang ZL, Liu HY, Wang DS, Singh RP, Sourdille P, Xia XC (2006) Quantitative trait loci mapping for adult-plant resistance to powdery mildew in bread wheat. Phytopathology 96(7):784–789
Lillemo M, Asalf B, Singh RP, Huerta-Espino J, Chen XM, He ZH, Bjornstad A (2008) The adult plant rust resistance loci Lr34/Yr18 and Lr46/Yr29 are important determinants of partial resistance to powdery mildew in bread wheat line Saar. Theor Appl Genet 116(8):1155–1166
Lillemo M, Singh RP, van Ginkel M (2010a) Identification of stable resistance to powdery mildew in wheat based on parametric and nonparametric methods. Crop Sci 50(2):478–485
Lillemo M, Skinnes H, Brown JKM (2010b) Race specific resistance to powdery mildew in Scandinavian wheat cultivars, breeding lines and introduced genotypes with partial resistance. Plant Breeding 129(3):297–303
Lillemo M, Bjørnstad Å, Skinnes H (2012) Molecular mapping of partial resistance to powdery mildew in winter wheat cultivar Folke. Euphytica doi:10.1007/s10681-011-0620-x (online)
Liu SX, Griffey CA, Maroof MAS (2001) Identification of molecular markers associated with adult plant resistance to powdery mildew in common wheat cultivar Massey. Crop Sci 41(4):1268–1275
Ma H, Kong Z, Fu B, Li N, Zhang L, Jia H, Ma Z (2011) Identification and mapping of a new powdery mildew resistance gene on chromosome 6D of common wheat. Theor Appl Genet 123(7):1099–1106
McDonald BA, Linde C (2002) The population genetics of plant pathogens and breeding strategies for durable resistance. Euphytica 124(2):163–180
McIntosh R, Zhang P, Cowger C, Parks R, Lagudah E, Hoxha S (2011) Rye-derived powdery mildew resistance gene Pm8 in wheat is suppressed by the Pm3 locus. Theor Appl Genet 123(3):359–367
Mingeot D, Chantret N, Baret PV, Dekeyser A, Boukhatem N, Sourdille P, Doussinault G, Jacquemin JM (2002) Mapping QTL involved in adult plant resistance to powdery mildew in the winter wheat line RE714 in two susceptible genetic backgrounds. Plant Breeding 121(2):133–140
Miranda LM, Murphy JP, Marshall D, Leath S (2006) Pm34: a new powdery mildew resistance gene transferred from Aegilops tauschii Coss. to common wheat (Triticum aestivum L.). Theor Appl Genet 113(8):1497–1504
Miranda LM, Murphy JP, Marshall D, Cowger C, Leath S (2007) Chromosomal location of Pm35, a novel Aegilops tauschii derived powdery mildew resistance gene introgressed into common wheat (Triticum aestivum L.). Theor Appl Genet 114(8):1451–1456
Mohler V, Bauer A, Bauer C, Flath K, Schweizer G, Hartl L (2011) Genetic analysis of powdery mildew resistance in German winter wheat cultivar Cortez. Plant Breeding 130(1):35–40. doi:10.1111/j.1439-0523.2010.01824.x
Muranty H, Pavoine MT, Jaudeau B, Radek W, Doussinault G, Barloy D (2009) Two stable QTL involved in adult plant resistance to powdery mildew in the winter wheat line RE714 are expressed at different times along the growing season. Mol Breeding 23(3):445–461
Ren SX, McIntosh RA, Lu ZJ (1997) Genetic suppression of the cereal rye-derived gene Pm8 in wheat. Euphytica 93(3):353–360
Rosewarne G, Singh R, Huerta-Espino J, William H, Bouchet S, Cloutier S, McFadden H, Lagudah E (2006) Leaf tip necrosis, molecular markers and β1-proteasome subunits associated with the slow rusting resistance genes Lr46/Yr29. Theor Appl Genet 112(3):500–508. doi:10.1007/s00122-005-0153-6
Saal B, Wricke G (1999) Development of simple sequence repeat markers in rye (Secale cereale L.). Genome 42(5):964–972
Schneider A, Molnár-Láng M (2009) Detection of the 1RS chromosome arm in Martonvásár wheat genotypes containing 1BL.1RS or 1AL.1RS translocations using SSR and STS markers. Acta Agron Hung 57(4):409–416
Singh RP (1992) Association between gene Lr34 for leaf rust resistance and leaf tip necrosis in wheat. Crop Sci 32(4):874–878
Singh RP, Mujeeb-Kazi A, Huerta-Espino J (1998) Lr46: a gene conferring slow-rusting resistance to leaf rust in wheat. Phytopathology 88(9):890–894
Singh RP, Nelson JC, Sorrells ME (2000) Mapping Yr28 and other genes for resistance to stripe rust in wheat. Crop Sci 40(4):1148–1155. doi:10.2135/cropsci2000.4041148x
Skinnes H (2002) Breakdown of race specific resistance to powdery mildew in Norwegian wheat. Cereal Rusts and Powdery Mildews Bulletin 30. Available at http://www.crpmb.org/2002/1201skinnes/
Somers DJ, Isaac P, Edwards K (2004) A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theor Appl Genet 109(6):1105–1114
Spielmeyer W, McIntosh RA, Kolmer J, Lagudah ES (2005) Powdery mildew resistance and Lr34/Yr18 genes for durable resistance to leaf and stripe rust cosegregate at a locus on the short arm of chromosome 7D of wheat. Theor Appl Genet 111(4):731–735
Tommasini L, Yahiaoui N, Srichumpa P, Keller B (2006) Development of functional markers specific for seven seven Pm3 resistance alleles and their validation in the bread wheat gene pool. Theor Appl Genet 114(1):165–175. doi:10.1007/s00122-006-0420-1
Tucker DM, Griffey CA, Liu S, Brown-Guedira G, Marshall DS, Maroof MAS (2007) Confirmation of three quantitative trait loci conferring adult plant resistance to powdery mildew in two winter wheat populations. Euphytica 155(1–2):1–13
Uauy C, Brevis JC, Chen XM, Khan I, Jackson L, Chicaiza O, Distelfeld A, Fahima T, Dubcovsky J (2005) High-temperature adult-plant (HTAP) stripe rust resistance gene Yr36 from Triticum turgidum ssp. dicoccoides is closely linked to the grain protein content locus Gpc-B1. Theor Appl Genet 112(1):97–105. doi:10.1007/s00122-005-0109-x
Utz HF, Melchinger AE (1996) PLABQTL: a computer program to map QTL. Institute of plant breeding, seed science and population genetics, University of Hohenheim, Stuttgart
Van Ooijen J, Voorrips R (2001) Joinmap 3.0 software for the calculation of genetic linkage maps. Plant Research International, Wageningen
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93(1):77–78
Wang ZL, Li LH, He ZH, Duan XY, Zhou YL, Chen XM, Lillemo M, Singh RP, Wang H, Xia XC (2005) Seedling and adult plant resistance to powdery mildew in Chinese bread wheat cultivars and lines. Plant Dis 89(5):457–463
William M, Singh RP, Huerta-Espino J, Islas SO, Hoisington D (2003) Molecular marker mapping of leaf rust resistance gene Lr46 and its association with stripe rust resistance gene Yr29 in wheat. Phytopathology 93(2):153–159
Xu WG, Li CX, Hu L, Zhang L, Zhang JZ, Dong HB, Wang GS (2010) Molecular mapping of powdery mildew resistance gene PmHNK in winter wheat (Triticum aestivum L.) cultivar Zhoumai 22. Mol Breeding 26(1):31–38
Yahiaoui N, Brunner S, Keller B (2006) Rapid generation of new powdery mildew resistance genes after wheat domestication. Plant J 47(1):85–98
Yu DZ (2000) Wheat powdery mildew in Central China: pathogen population structure and host resistance. PhD thesis, Wageningen University and Research Centre, Wageningen
Zhou Y, He ZH, Zhang GS, Xia LQ, M. CX, C. GY, B. JZ, J. YG (2004) Utilization of 1BL/1RS translocation in wheat breeding in China. Acta Agronomica Sinica 30(6):531–535
Zhu ZD, Zhou RH, Kong XY, Dong YC, Jia JZ (2005) Microsatellite markers linked to 2 powdery mildew resistance genes introgressed from Triticum carthlicum accession PS5 into common wheat. Genome 48(4):585–590
Acknowledgments
The PhD scholarship of the first author was funded by the Norwegian University of Life Sciences, and the research was supported by grants from the Research Council of Norway (projects 178273 and 185046), and the National Science Foundation of China (projects 30821140351 and 30671294). Additionally, we gratefully acknowledge the technical contributions from Anne Guri Marøy in the lab and Yalew Tarkegne in the field.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by J. Snape.
Rights and permissions
About this article
Cite this article
Lu, Q., Bjørnstad, Å., Ren, Y. et al. Partial resistance to powdery mildew in German spring wheat ‘Naxos’ is based on multiple genes with stable effects in diverse environments. Theor Appl Genet 125, 297–309 (2012). https://doi.org/10.1007/s00122-012-1834-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-012-1834-6