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Association mapping for soilborne pathogen resistance in synthetic hexaploid wheat

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Abstract

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.

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References

  • Asiedu R, Fisher JM, Driscoll CJ (1990) Resistance to Heterodera avenae in the rye genome of triticale. Theor Appl Genet 79:331–336

    Article  Google Scholar 

  • 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 20:31–40

    Article  CAS  Google Scholar 

  • 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):289–300

    Google Scholar 

  • 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 23:2633–2635

    Article  PubMed  CAS  Google Scholar 

  • Breseghello F, Sorrells MS (2006) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172:1165–1177

    Article  PubMed  Google Scholar 

  • 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 47:887–890

    Article  Google Scholar 

  • 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 47:1018–1030

    Article  CAS  Google Scholar 

  • Cleveland WS (1979) Robust locally weighted regression and smoothing scatterplots. J Am Stat Assoc 74(368):829–836

    Article  Google Scholar 

  • 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 177:1889–1913

    Article  PubMed  CAS  Google Scholar 

  • 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 16:1129–1134

    Article  PubMed  Google Scholar 

  • 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 87:402–408

    Article  Google Scholar 

  • 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, Beijing

  • Eastwood RF (1995) Genetics of resistance to Heterodera avenae in Triticum tauschii and its transfer to bread wheat. PhD thesis, The University of Melbourne, Australia

  • 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 37:311–319

    Article  PubMed  CAS  Google Scholar 

  • 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 26:39–49

    Article  CAS  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  PubMed  CAS  Google Scholar 

  • Flint-Garcia SA, Thornsberry JM, Buckler ES (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374

    Article  PubMed  CAS  Google Scholar 

  • 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 48:1062–1070

    Article  Google Scholar 

  • Goldstein DB, Tate SK, Sisodiya SM (2003) Pharmacogenetics goes genomics. Nat Rev Genet 4:937–947

    Article  PubMed  CAS  Google Scholar 

  • 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 115:282–284

    Article  Google Scholar 

  • 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 120:125–128

    Article  CAS  Google Scholar 

  • Liu K, Muse SV (2005) PowerMarker: integrated analysis environment for for genetic marker data. Bioinformatics 21(9):2128–2129

    Article  PubMed  CAS  Google Scholar 

  • 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 7:6

    Article  PubMed  Google Scholar 

  • 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 55:1205–1211

    Article  CAS  Google Scholar 

  • 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. s.lat. x T. tauschii; 2n = 6x = 42, AABBDD) and its potential utilization for wheat improvement. Genet Resour Crop Evol 43:129–134

    Article  Google Scholar 

  • 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 27:37–58

    Article  Google Scholar 

  • 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 243–287

    Google Scholar 

  • 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 102:623–629

    Article  CAS  Google Scholar 

  • 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 52:1367–1374

    Article  CAS  Google Scholar 

  • 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 59:421–431

    Article  Google Scholar 

  • Park BS, Mori M (2010) Balancing false discovery and false negative rates in selection of differentially expressed genes in microarrays. Open Access Bioinform 2:1–9

    Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Rafalski JA (2002) Novel genetic mapping tools in plants: SNPs and LD-based approaches. Plant Sci 162:329–333

    Article  CAS  Google Scholar 

  • 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 112:738–743

    Article  PubMed  CAS  Google Scholar 

  • Rivoal R, Jahier J, Hulle M (1993) Partial resistance to Heterodera avenae in wheat lines with the 6Mv chromosome from Aegilops ventricosa. J Nematol 25:265–269

    PubMed  CAS  Google Scholar 

  • 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 96:1135–1140

    Article  Google Scholar 

  • Roy JK, Smith KP, Muehlbauer GJ, Chao S, Close TJ, Steffenson BJ (2010) Association mapping of spot blotch resistance in wild barley. Mol Breed 26:243–256

    Article  PubMed  Google Scholar 

  • Sabatti C, Service S, Freimer N (2003) False discovery rate in linkage and association genome screens for complex disorders. Genetics 164:829–833

    PubMed  Google Scholar 

  • 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, Brisbane

  • 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 

  • 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 176:213–222

    Article  CAS  Google Scholar 

  • Slootmaker LAJ, Lange W, Jochemsen G, Schepers J (1974) Monosomic analysis in bread wheat of resistance to cereal root eelworm. Euphytica 23:497–503

    Article  Google Scholar 

  • 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 50:557–567

    Article  PubMed  CAS  Google Scholar 

  • 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 27:77–83

    Article  Google Scholar 

  • 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 59:432–446

    Article  Google Scholar 

  • 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 48:553–559

    Article  Google Scholar 

  • 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 37:235–242

    Article  Google Scholar 

  • 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 115:697–708

    Article  PubMed  CAS  Google Scholar 

  • van Ginkel M, Ogbonnaya F (2007) Novel genetic diversity from synthetic wheats in breeding cultivars for changing production conditions. Field Crops Res 104:86–94

    Article  Google Scholar 

  • vanSlageren MW (1994) Wild wheats: a monograph of Aegilops L. and Ambylopyrum (Jaub. & Spach) Eig (Poaceae). Wageningen Agricultural University Papers, pp 94–97

  • 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 37:220–234

    Article  Google Scholar 

  • 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 112:63–69

    Article  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  PubMed  CAS  Google Scholar 

  • 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 116:439–453

    Article  PubMed  CAS  Google Scholar 

  • 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 104:874–879

    Article  PubMed  CAS  Google Scholar 

  • 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 112:1480–1486

    Article  PubMed  CAS  Google Scholar 

  • Xu SS, Friesen TL, Mujeeb-Kazi A (2004) Seedling resistance to tan spot and Stagonospora nodorum blotch in synthetic hexaploid wheats. Crop Sci 44:2238–2245

    Article  Google Scholar 

  • 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 38:203–208

    Article  PubMed  CAS  Google Scholar 

  • 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.)

  • 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 56:345–352

    Article  CAS  Google Scholar 

  • 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 57:525–530

    Article  Google Scholar 

  • 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 26:107–124

    Article  Google Scholar 

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Acknowledgments

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.

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Correspondence to Francis C. Ogbonnaya.

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Mulki, M.A., Jighly, A., Ye, G. et al. Association mapping for soilborne pathogen resistance in synthetic hexaploid wheat. Mol Breeding 31, 299–311 (2013). https://doi.org/10.1007/s11032-012-9790-z

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