Molecular Breeding

, Volume 31, Issue 2, pp 299–311 | Cite as

Association mapping for soilborne pathogen resistance in synthetic hexaploid wheat

  • Muhammad A. Mulki
  • Abdulqader Jighly
  • Gouyou Ye
  • Livinus C. Emebiri
  • David Moody
  • Omid Ansari
  • Francis C. Ogbonnaya


Soilborne pathogens such as cereal cyst nematode (CCN; Heterodera avenae) and root lesion nematode (Pratylenchus neglectus; PN) cause substantial yield losses in the major cereal-growing regions of the world. Incorporating resistance into wheat cultivars and breeding lines is considered the most cost-effective control measure for reducing nematode populations. To identify loci with molecular markers linked to genes conferring resistance to these pathogens, we employed a genome-wide association approach in which 332 synthetic hexaploid wheat lines previously screened for resistance to CCN and PN were genotyped with 660 Diversity Arrays Technology (DArT) markers. Two sequence-tagged site markers reportedly linked to genes known to confer resistance to CCN were also included in the analysis. Using the mixed linear model corrected for population structure and familial relatedness (Q+K matrices), we were able to confirm previously reported quantitative trait loci (QTL) for resistance to CCN and PN in bi-parental crosses. In addition, we identified other significant markers located in chromosome regions where no CCN and PN resistance genes have been reported. Seventeen DArT marker loci were found to be significantly associated with CCN and twelve to PN resistance. The novel QTL on chromosomes 1D, 4D, 5B, 5D and 7D for resistance to CCN and 4A, 5B and 7B for resistance to PN are suggested to represent new sources of genes which could be deployed in further wheat improvement against these two important root diseases of wheat.


Primary synthetic wheat Cereal cyst nematode Root lesion nematode Genetic resistance Linkage disequilibrium mapping Marker-assisted selection 



We thank all our colleagues from the Australian wheat community for their collaborative spirit and their willingness to share the data consistent with the aims of the synthetic evaluation project. We thank Grain Research and Development Corporation (GRDC), Australia, Department of Primary Industries, Horsham, Victoria and ICARDA, Syria for their financial support. The technical assistance of Jayne Wilson, DPI, Victoria and Professor Rudi Appels for critical review and editorial assistance with the manuscript are gratefully acknowledged.

Supplementary material

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Supplementary material 1 (DOCX 23 kb)
11032_2012_9790_MOESM2_ESM.pdf (21 kb)
Supplementary material 2 (PDF 20 kb)


  1. Asiedu R, Fisher JM, Driscoll CJ (1990) Resistance to Heterodera avenae in the rye genome of triticale. Theor Appl Genet 79:331–336CrossRefGoogle Scholar
  2. Barloy D, Lemoine J, Abelard P, Tanguy AM, Rivoal R, Jahier J (2007) Marker assisted pyramiding of two cereal cyst nematode resistance genes from Aegilops variabilis in wheat. Mol Breed 20:31–40CrossRefGoogle Scholar
  3. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57(1):289–300Google Scholar
  4. Bradbury JC, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635PubMedCrossRefGoogle Scholar
  5. Breseghello F, Sorrells MS (2006) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172:1165–1177PubMedCrossRefGoogle Scholar
  6. Camus-Kulandaivelu L, Veyrieras JB, Gouesnard B, Charcosset A, Manicacci D (2007) Evaluating the reliability of STRUCTURE outputs in case of relatedness between individuals. Crop Sci 47:887–890CrossRefGoogle Scholar
  7. Chao S, Zhang W, Dubcovsky J, Sorrells M (2007) Evaluation of genetic diversity and genome-wide linkage disequilibrium among US wheat (Triticum aestivum L.) germplasm representing different market classes. Crop Sci 47:1018–1030CrossRefGoogle Scholar
  8. Cleveland WS (1979) Robust locally weighted regression and smoothing scatterplots. J Am Stat Assoc 74(368):829–836CrossRefGoogle Scholar
  9. Crossa J, Burgueño J, Dreisigacker S, Vargas M, Herrera-Foessel SA, Lillemo M, Singh RP, Trethowan R, Warburton M, Franco J, Reynolds M, Crouch JH, Ortiz R (2007) Association analysis of historical bread wheat germplasm using additive genetic covariance of relatives and population structure. Genetics 177:1889–1913PubMedCrossRefGoogle Scholar
  10. de Majnik J, Ogbonnaya FC, Moullet O, Lagudah ES (2003) The Cre1 and Cre3 nematode resistance genes are located at homeologous loci in the wheat genome. Mol Plant Microbe Interact 16:1129–1134PubMedCrossRefGoogle Scholar
  11. Delibes A, Romero D, Aguaded S, Duce A, Mena M, Lopez-Brana I, Andres MF, Martin-Sanchez JA, Garcia-Olmedo F (1993) Resistance to cereal cyst nematode (Heterodera avenae Woll.) transferred from the wild grass Aegilops ventricosa to hexaploid wheat by a stepping-stone procedure. Theor Appl Genet 87:402–408CrossRefGoogle Scholar
  12. Detering F, Hunter E, Uszynski G, Wenzl P, Andrzej K (2010) A consensus genetic map of wheat: ordering 5,000 Wheat DArT markers. 20th ITMI & 2nd WGC Workshop, 1–5 September, BeijingGoogle Scholar
  13. Eastwood RF (1995) Genetics of resistance to Heterodera avenae in Triticum tauschii and its transfer to bread wheat. PhD thesis, The University of Melbourne, AustraliaGoogle Scholar
  14. Eastwood RF, Lagudah ES, Appels R (1994) A directed search for DNA sequences tightly linked to cereal cyst nematode resistance genes in Triticum tauschii. Genome 37:311–319PubMedCrossRefGoogle Scholar
  15. Emebiri LC, Oliver JR, Mrva J, Mares D (2010) Association mapping of late maturity α-amylase (LMA) activity in a collection of synthetic hexaploid wheat. Mol Breed 26:39–49CrossRefGoogle Scholar
  16. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  17. Flint-Garcia SA, Thornsberry JM, Buckler ES (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374PubMedCrossRefGoogle Scholar
  18. Friesen TL, Xu SS, Harris MO (2008) Stem rust, tan spot, Stagonospora nodurum blotch, and hessian fly resistance in Langdon durum-Aegilops tauschii synthetic hexaploid wheat lines. Crop Sci 48:1062–1070CrossRefGoogle Scholar
  19. Goldstein DB, Tate SK, Sisodiya SM (2003) Pharmacogenetics goes genomics. Nat Rev Genet 4:937–947PubMedCrossRefGoogle Scholar
  20. Jahier J, Tanguy AM, Abelard P, Rivoal R (1996) Utilization of deletions to localize a gene for resistance to the cereal cyst nematode, Heterodera avenae, on an Aegilops ventricosa chromosome. Plant Breed 115:282–284CrossRefGoogle Scholar
  21. Jahier J, Abelard P, Tanguy AM, Dedryver F, Rivoal R, Bariana HS (2001) The Aegilops ventricosa segment on chromosome 2AS of the wheat cultivar ‘VPM1’ carries the cereal cyst nematode resistance gene Cre5. Plant Breed 120:125–128CrossRefGoogle Scholar
  22. Liu K, Muse SV (2005) PowerMarker: integrated analysis environment for for genetic marker data. Bioinformatics 21(9):2128–2129PubMedCrossRefGoogle Scholar
  23. Malysheva-Otto L, Ganal MW, Röder MS (2006) Analysis of molecular diversity, population structure and linkage disequilibrium in worldwide survey of cultivated barley germplasm (Hordeum vulgare L.). BMC Genet 7:6PubMedCrossRefGoogle Scholar
  24. Martin EM, Eastwood RF, Ogbonnaya FC (2004) Identification of microsatelite markers associated with cereal cyst nematode resistance gene Cre3 in wheat. Aust J Agric Res 55:1205–1211CrossRefGoogle Scholar
  25. Mujeeb-Kazi A, Rosas V, Roldan S (1996) Conservation of the genetic variation of Triticum tauschii (Coss.) Schmalh. (Aegilops squarrosa auct. non L.) in synthetic hexaploid wheats (T. turgidum L. x T. tauschii; 2n = 6x = 42, AABBDD) and its potential utilization for wheat improvement. Genet Resour Crop Evol 43:129–134CrossRefGoogle Scholar
  26. Neumann K, Kobiljski B, Denčić S, Varshney RK, Börner A (2011) Genome-wide association mapping: a case study in bread wheat (Triticum aestivum L.). Mol Breed 27:37–58CrossRefGoogle Scholar
  27. Nicol JM, Rivoal R (2008) Global knowledge and its application for the integrated control and management of nematodes on wheat. In: Ciancio A, Mukerji KG (eds) Integrated management and biocontrol of vegetable and grain crops nematodes. Springer, The Netherlands, pp 243–287Google Scholar
  28. Ogbonnaya FC, Seah S, Delibes A, Jahier J, Lopez-Brana I, Eastwood RF, Lagudah ES (2001a) Molecular-genetic characterisation of a new nematode resistance gene in wheat. Theor Appl Genet 102:623–629CrossRefGoogle Scholar
  29. Ogbonnaya FC, Subrahmanyam NC, Moullet O, de Majnik J, Eagles HA, Brown JS, Eastwood RF, Kollmorgen J, Appels R, Lagudah ES (2001b) Diagnostic DNA markers for cereal cyst nematode resistance in bread wheat. Aust J Agric Res 52:1367–1374CrossRefGoogle Scholar
  30. Ogbonnaya FC, Imtiaz M, Bariana HS, McLean M, Shankar M, Hollaway GJ, Trethowan R, Lagudah ES, van Ginkel M (2008) Mining synthetic hexaploids for multiple disease resistance to improve wheat. Aust J Agric Res 59:421–431CrossRefGoogle Scholar
  31. Park BS, Mori M (2010) Balancing false discovery and false negative rates in selection of differentially expressed genes in microarrays. Open Access Bioinform 2:1–9Google Scholar
  32. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  33. Rafalski JA (2002) Novel genetic mapping tools in plants: SNPs and LD-based approaches. Plant Sci 162:329–333CrossRefGoogle Scholar
  34. Ravel C, Praud S, Murigneux A, Linossier L, Dardevet M, Balfourier F, Dufour P, Brunel D, Charmet G (2006) Identification of Glu-B1-1 as a candidate gene for the quantity of high-molecular-weight gluten in in bread wheat (Triticum aestivum L.) by means of an association study. Theor Appl Genet 112:738–743PubMedCrossRefGoogle Scholar
  35. Rivoal R, Jahier J, Hulle M (1993) Partial resistance to Heterodera avenae in wheat lines with the 6Mv chromosome from Aegilops ventricosa. J Nematol 25:265–269PubMedGoogle Scholar
  36. Romero M, Montes MJ, Sin E, López-Brana I, Duce A, Martin-Sanchez JA, Andres MF, Delibes A (1998) A cereal cyst nematode (Heterodera avenae) resistance gene transferred from Aegilops triuncialisto hexaploid wheat. Theor Appl Genet 96:1135–1140CrossRefGoogle Scholar
  37. Roy JK, Smith KP, Muehlbauer GJ, Chao S, Close TJ, Steffenson BJ (2010) Association mapping of spot blotch resistance in wild barley. Mol Breed 26:243–256PubMedCrossRefGoogle Scholar
  38. Sabatti C, Service S, Freimer N (2003) False discovery rate in linkage and association genome screens for complex disorders. Genetics 164:829–833PubMedGoogle Scholar
  39. Sheedy JS (2004) Resistance to root-lesion nematode (Pratylenchus thornei) in wild relatives of bread wheat (Triticum aestivum) and Iranian landrace wheats. M. Agric. Sc. Thesis, University of Queensland, BrisbaneGoogle Scholar
  40. Sheedy JG, Thompson JP, Kelly A (2012) Diploid and tetraploid progenitors of wheat are valuable sources of resistance to the root lesion nematode Pratylenchus thornei. Euphytica. doi: 10.1007/s10681-011-0617-5 Google Scholar
  41. Singh K, Chhuneja P, Singh I, Sharma SK, Garg T, Garg M, Keeler B, Dhaliwal H (2010) Molecular mapping of cereal cyst nematode resistance in Triticum monococcum L. and its transfer to the genetic background of cultivated wheat. Euphytica 176:213–222CrossRefGoogle Scholar
  42. Slootmaker LAJ, Lange W, Jochemsen G, Schepers J (1974) Monosomic analysis in bread wheat of resistance to cereal root eelworm. Euphytica 23:497–503CrossRefGoogle Scholar
  43. Somers DJ, Banks T, DePauw R, Fox S, Clarke J, Pozniak C, McCartney C (2007) Genome-wide linkage disequilibrium analysis in bread wheat and durum wheat. Genome 50:557–567PubMedCrossRefGoogle Scholar
  44. Steinberg L, Kuang D (2002) Quick and easy implementation of the Benjamini-Hochberg procedure for controlling the false positive rate in multiple comparisons. J Educ Behav Stat 27:77–83CrossRefGoogle Scholar
  45. Thompson JP (2008) Resistance to root-lesion nematodes (Pratylenchus thornei and P. neglectus) in synthetic hexaploid wheats and their durum and Aegilops tauschii parents. Aust J Agric Res 59:432–446CrossRefGoogle Scholar
  46. Thompson JP, Haak MI (1997) Resistance to root-lesion nematode (Pratylenchus thornei) in Aegilops tauschii Coss., the D-genome donor to wheat. Aust J Agric Res 48:553–559CrossRefGoogle Scholar
  47. Thompson JP, Owen KJ, Stirling GR, Bell MJ (2008) Root-lesion nematodes (Pratylenchus thornei and P. neglectus): a review of recent progress in managing a significant pest of grain crops in northern Australia. Aust Plant Pathol 37:235–242CrossRefGoogle Scholar
  48. Tommasini L, Schnurbusch T, Fossati D, Mascher F, Keller B (2007) Association mapping of Stagonospora nodorum blotch resistance in modern European winter wheat varieties. Theor Appl Genet 115:697–708PubMedCrossRefGoogle Scholar
  49. van Ginkel M, Ogbonnaya F (2007) Novel genetic diversity from synthetic wheats in breeding cultivars for changing production conditions. Field Crops Res 104:86–94CrossRefGoogle Scholar
  50. vanSlageren MW (1994) Wild wheats: a monograph of Aegilops L. and Ambylopyrum (Jaub. & Spach) Eig (Poaceae). Wageningen Agricultural University Papers, pp 94–97Google Scholar
  51. Vanstone VA, Hollaway GJ, Stirling GR (2008) Managing nematode pests in the southern and western regions of the Australian cereal industry: continuing progress in a challenging environment. Aust Plant Pathol 37:220–234CrossRefGoogle Scholar
  52. Villareal RL, Mujeeb-Kazi A, Fuentes-Davila G, Rajaram S, Del Toro E (1994) Resistance to karnal bunt (Tilletia indica Mitra) in synthetic hexaploid wheats derived from Triticum turgidum x T. tauschii. Plant Breed 112:63–69CrossRefGoogle Scholar
  53. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78PubMedCrossRefGoogle Scholar
  54. White J, Law JR, Mackay I, Chalmers KJ, Smith JSC, Kilian A, Powell W (2008) The genetic diversity of UK, US and Australian cultivars of Triticum aestivum measured by DArT markers and considered by genome. Theor Appl Genet 116:439–453PubMedCrossRefGoogle Scholar
  55. Williams KJ, Taylor SP, Bogacki P, Pallotta M, Bariana HS, Wallwork H (2002) Mapping of the root lesion nematode (Pratylenchus neglectus) resistance gene Rlnn1 in wheat. Theor Appl Genet 104:874–879PubMedCrossRefGoogle Scholar
  56. Williams KJ, Willsmore KL, Olson S, Matic M, Kuchel H (2006) Mapping of a novel QTL for resistance to cereal cyst nematode in wheat. Theor Appl Genet 112:1480–1486PubMedCrossRefGoogle Scholar
  57. Xu SS, Friesen TL, Mujeeb-Kazi A (2004) Seedling resistance to tan spot and Stagonospora nodorum blotch in synthetic hexaploid wheats. Crop Sci 44:2238–2245CrossRefGoogle Scholar
  58. Yu J, Pressoir G, Briggs WH, Vroh Bi I, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2006) A unified mixed-model 24 method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208PubMedCrossRefGoogle Scholar
  59. Zwart RS, Thompson JP, Williamson PM, Seymour NP (2004) Elite sources of resistance in wheat to root-lesion nematodes (Pratylenchus thornei and P. neglectus) and yellow spot (Pyrenophoratritici-repentis). In: Proceedings of the 3rd Australasian Soilborne Diseases Symposium, p 220. (South Australian Research and Development Institute: Adelaide, S. Aust.)Google Scholar
  60. Zwart RS, Thompson JP, Godwin ID (2005) Identification of quantitative trait loci for resistance to two species of root-lesion nematode (Pratylenchus thornei and P. neglectus) in wheat. Aust J Agric Res 56:345–352CrossRefGoogle Scholar
  61. Zwart RS, Thompson JP, Sheedy JG, Nelson JC (2006) Mapping quantitative trait loci for resistance to Pratylenchus thornei from synthetic hexaploid wheat in the international triticeae mapping initiative (ITMI) population. Aust J Agric Res 57:525–530CrossRefGoogle Scholar
  62. Zwart RS, Thompson JP, Milgate AW, Bansal UK, Williamson PM, Raman H, Bariana HS (2010) QTL mapping of multiple foliar disease and root-lesion nematode resistances in wheat. Mol Breed 26:107–124CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Muhammad A. Mulki
    • 1
    • 6
  • Abdulqader Jighly
    • 1
  • Gouyou Ye
    • 2
  • Livinus C. Emebiri
    • 3
  • David Moody
    • 4
  • Omid Ansari
    • 5
  • Francis C. Ogbonnaya
    • 1
    • 5
  1. 1.International Center for Agricultural Research in the Dry Areas (ICARDA)AleppoSyria
  2. 2.International Rice Research Institute (IRRI)Los Banos, LagunaPhilippines
  3. 3.EH Graham Centre for Agricultural InnovationWaggaWaggaAustralia
  4. 4.InterGrain Pty LtdBibra LakeAustralia
  5. 5.Grains Research and Development CorporationKingstonAustralia
  6. 6.Max Planck Institute for Plant Breeding ResearchCologneGermany

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