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High-resolution mapping and new marker development for adult plant stripe rust resistance QTL in the wheat cultivar Kariega

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Abstract

Three major quantitative trait loci (QTL) contribute to the durable adult plant stripe rust resistance in the high-quality bread wheat cultivar Kariega; QYr.sgi-2B.1 and QYr.sgi-4A.1, and the pleiotropic resistance gene Lr34/Yr18/Sr57. While marker-assisted selection is currently being used to incorporate the Kariega stripe rust adult plant resistance into new South African wheat breeding lines, effective selection of the large QTL intervals remains a challenging task. In this study, we describe the development of expressed sequence tag (EST)-derived markers as an effective strategy for increasing the marker density in the selected QTL intervals and the conversion of Diversity Arrays Technology (DArT) and EST-derived markers to sequence tagged site (STS) markers to enable high-throughput screening. To reduce the QTL intervals, a high-resolution mapping population was developed, consisting of 1,020 F2 individuals, from the cross Kariega × Avocet S. Through recombinant selection, QYr.sgi-2B.1 was shown to reside within a 6.1 cM interval on the short arm of chromosome 2B, between marker loci Xbarc55 and Xwmc344, a reduction from the previous interval size of 23 cM. Previously, QYr.sgi-4A.1 was poorly defined, but by mapping selected recombinants for the QYr.sgi-4A.1 interval, the QTL region was narrowed to a 16.3-cM interval between marker loci Xbarc78, Xwmc313 and Xwmc219 on the long arm of chromosome 4A. An EST-STS marker, Xufs1-4A, was also developed for QYr.sgi-4A.1, which improved selection for this slow-rusting QTL. The EST marker strategy was useful in increasing marker density and contributed to improved selection for the Kariega QTL in resistance breeding. In addition, BC4F2 families were developed to study the expression of QYr.sgi-2B.1 and QYr.sgi-4A.1 individually, and in combination with Lr34/Yr18/Sr57 in the common, stripe rust susceptible background of Avocet S.

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References

  • Agenbag GM, Pretorius ZA, Boyd LA, Bender CM, Prins R (2012) Identification of adult plant resistance to stripe rust in the wheat cultivar Cappelle-Desprez. Theor Appl Genet 125:109–120

    Article  CAS  PubMed  Google Scholar 

  • Akhunov ED, Sehgal S, Liang H, Wang S, Akhunova AR, Kaur G, Li W, Forrest KL, See D, Šimková H, Ma Y, Hayden MJ, Luo M, Faris JD, Doležel J, Gill BS (2013) Comparative analysis of syntenic genes in grass genome reveals accelerated rates of gene structure and coding sequence evolution in polyploid wheat. Plant Physiol 161:252–265

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Allen AM, Barker GLA, Wilkinson P, Burridge A, Winfield M, Coghill J, Uauy C, Griffiths S, Jack P, Berry S, Werner P, Melichar JPE, McDougall J, Gwilliam R, Robinson P, Edwards KJ (2013) Discovery and development of exome-based, co-dominant single nucleotide polymorphism markers in hexaploid wheat (Triticum aestivum L.). Plant Biotechnol J 11:279–295

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Appels R (2003) A consensus molecular genetic map for wheat—a cooperative international effort. In: Progna N (ed) Proceedings of the 10th international wheat genetics symposium. Paestum, Italy, pp 211–214

    Google Scholar 

  • Baker GLA, Edwards KJ (2009) A genome-wide analysis of single nucleotide polymorphism diversity in the world’s major cereal crops. Plant Biotechnol J 7:318–325

    Article  Google Scholar 

  • Barnard AD, Labuschagne MT, Van Niekerk HA (2002) Heritability estimates of bread wheat quality traits in the Western Cape province of South Africa. Euphytica 127:115–122

    Article  CAS  Google Scholar 

  • Bassam BJ, Caetano-Anollés G, Gresshoff PM (1991) Fast and sensitive silver staining of DNA in polyacrylamide gels. Anal Biochem 196:80–83

    Article  CAS  PubMed  Google Scholar 

  • Bernardo AN, Bradbury PJ, Ma H, Hu S, Bowden RL, Buckler ES, Bai G (2009) Discovery and mapping of single feature polymorphisms in wheat using Affymetrix arrays. BMC Genomics 10:251

    Article  PubMed Central  PubMed  Google Scholar 

  • Börner A, Schumann E, Fürste A, Cöster H, Leithold B, Röder MS, Weber WE (2002) Mapping of quantitative trait loci determining agronomic important characters in hexaploid wheat (Triticum aestivum L.). Theor Appl Genet 105:921–936

    Article  PubMed  Google Scholar 

  • Boshoff WHP, Pretorius ZA, Van Niekerk BD (2002a) Establishment, distribution, and pathogenicity of Puccinia striiformis f. sp. tritici in South Africa. Plant Dis 86:485–492

    Article  Google Scholar 

  • Boshoff WHP, Pretorius ZA, Van Niekerk BD (2002b) Resistance in South African and foreign wheat cultivars to pathotypes 6E16A− and 6E22A− of Puccinia striiformis f. sp. tritici. S Afr J Plant Soil 19:27–36

    Article  Google Scholar 

  • Boukhatem N, Baret PV, Mingeot D, Jacquemin JM (2002) Quantitative trait loci for resistance against yellow rust in two wheat-derived recombinant inbred line populations. Theor Appl Genet 104:111–118

    Article  CAS  PubMed  Google Scholar 

  • Boyd LA (2005) Can Robigus defeat an old enemy? Yellow rust of wheat. J Agric Sci 143:1–11

    Article  Google Scholar 

  • Carter AH, Chen XM, Garland-Campbell K, Kidwell KK (2009) Identifying QTL for high-temperature adult-plant resistance to stripe rust (Puccinia striiformis f. sp. tritici) in the spring wheat (Triticum aestivum L.) cultivar ‘Louise’. Theor Appl Genet 119:1119–1128

    Article  PubMed  Google Scholar 

  • Chen J, Chu C, Souza EJ, Guttieri MJ, Chen X, Xu S, Hole D, Zemetra R (2012) Genome-wide identification of QTL conferring high-temperature adult-plant (HTAP) resistance to stripe rust (Puccinia striiformis f. sp. tritici) in wheat. Mol Breed 29:791–800

    Article  CAS  Google Scholar 

  • Childs KL, Hamilton JP, Zhu W, Ly E, Cheung F, Wu H, Rabinowicz PD, Town CD, Buell R, Chan AP (2007) The TIGR plant transcript assemblies database. Nucleic Acids Res 35:D846–D851

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Crossa J, Burgueno J, Dreisgacker 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 177:1–25

    Article  Google Scholar 

  • Dedryver F, Paillard S, Mallard S, Robert O, Trottet M, Nègre S, Verplancke G, Jahier J (2009) Characterization of genetic components involved in durable resistance to stripe rust in the bread wheat ‘Renan’. Phytopathology 99:968–973

    Article  CAS  PubMed  Google Scholar 

  • Devos KM, Dubcovsky J, Dvorak J, Chinoy CN, Gale MD (1995) Structural evolution of wheat chromosomes 4A, 5A, and 7B and its impact on recombination. Theor Appl Genet 91:282–288

    Article  CAS  PubMed  Google Scholar 

  • Doerge RW, Churchill GA (1996) Permutation tests for multiple loci affecting a quantitative character. Genetics 142:285–294

    CAS  PubMed Central  PubMed  Google Scholar 

  • Guo Q, Zhang ZJ, Xu YB, Li GH, Feng J, Zhou Y (2008) Quantitative trait loci for high-temperature adult-plant and slow-rusting resistance to Puccinia striiformis f. sp. tritici in wheat cultivars. Phytopathology 98:803–809

    Article  CAS  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hernandez P, Martis M, Dorado G, Pfeifer M, Gálvez S, Schaaf S, Jouve N, Šimková H, Valánik M, Doležel J, Mayer KFX (2012) Next-generation sequencing and syntenic integration of flow-sorted arms of wheat chromosome 4A exposes the chromosome structure and gene content. Plant J 69:377–386

    Article  CAS  PubMed  Google Scholar 

  • Hovmøller MS, Yahyaoui AH, Milus EA, Justesen AF (2008) Rapid global spread of two aggressive strains of a wheat rust fungus. Mol Ecol 17:3818–3826

    Article  PubMed  Google Scholar 

  • Hovmøller MS, Sørenson CK, Walter S, Justesen AF (2011) Diversity of Puccinia striiformis on cereals and grasses. Annu Rev Phytopathol 49:197–217

    Article  PubMed  Google Scholar 

  • Kent WJ (2002) BLAT—the BLAST-like alignment tool. Genome Res 12:656–664

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, Bossolini E, Selter LL, Keller B (2009) A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323:1360–1363

    Article  CAS  PubMed  Google Scholar 

  • Krattinger SG, Lagudah ES, Wicker T, Risk JM, Ashton AR, Selter LL, Matsumoto T, Keller B (2011) Lr34 multi-pathogen resistance ABC transporter: molecular analysis of homoeologous and orthologous genes in hexaploid wheat and other grass species. Plant J 65:392–403

    Article  CAS  PubMed  Google Scholar 

  • Krattinger SG, Jordan DR, Mace ES, Raqhavan C, Luo MC, Keller B, Lagudah ES (2013) Recent emergence of the wheat Lr34 multi-pathogen resistance: insights from haplotype analysis in wheat, rice, sorghum and Aegilops tauschii. Theor Appl Genet 126:663–672

    Article  CAS  PubMed  Google Scholar 

  • 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 119:889–898

    Article  CAS  PubMed  Google Scholar 

  • Lan C, Liang S, Zhou X, Zhou G, Lu Q, Xia X, He Z (2010) Identification of genomic regions controlling adult-plant stripe rust resistance in Chinese landrace Pinguan 50 through bulked segregant analysis. Phytopathology 100:313–318

    Article  PubMed  Google Scholar 

  • Mallard S, Gaudet D, Aldeia A, Abelard C, Besnard AL, Sourdille P, Dedryver F (2005) Genetic analysis of durable resistance to yellow rust in bread wheat. Theor Appl Genet 110:1401–1409

    Article  CAS  PubMed  Google Scholar 

  • Mammadov J, Chen W, Mingus J, Thompson S, Kumpatla S (2012) Development of versatile gene-based SNP assays in maize (Zea mays L.). Mol Breed 29:779–790

    Article  CAS  Google Scholar 

  • McGrann GRD, Smith PH, Burt C, Mateos GR, Chama TN, McCormack R, Wessels E, Agenbag G, Boyd LA (2014) Genomic and genetic analysis of the wheat race-specific yellow rust resistance gene Yr5. J Plant Sci Mol Breed 3:2

    Article  Google Scholar 

  • McIntosh RA (1992) Close genetic linkage of genes conferring adult-plant resistance to leaf rust and stripe rust in wheat. Plant Pathol 41:523–527

    Article  Google Scholar 

  • McIntosh RA, Wellings CR, Park RF (1995) Wheat rusts: an atlas of resistance genes. CSIRO, Canberra

    Book  Google Scholar 

  • McIntosh RA, Yamazaki Y, Dubcovsky J, Rogers J, Morris C, Appels R, Xia XC (2013) Catalogue of gene symbols for wheat. 12th international wheat genetics symposium, Yokohama, Japan

  • Mickelson-Young L, Endo TR, Gill BS (1995) A cytogenetic ladder-map of the wheat homoeologous group-4 chromosomes. Theor Appl Genet 90:1007–1011

    Article  CAS  PubMed  Google Scholar 

  • Moldenhauer J, Pretorius ZA, Moerschabacher BM, Prins R, Van der Westhuizen AJ (2008) Histopathology and PR-protein markers provide insight into adult plant resistance to stripe rust of wheat. Mol Plant Physiol 9:137–145

    CAS  Google Scholar 

  • Mollinari M, Margarido GRA, Vencovsky R, Carcia AAF (2009) Evaluation of algorithms used to order markers on genetic maps. Heredity 103:494–502

    Article  CAS  PubMed  Google Scholar 

  • Navabi A, Tewari JP, Singh RP, McCallum B, Laroche A, Briggs KG (2005) Inheritance and QTL analysis of durable resistance to stripe and leaf rusts in an Australian cultivar, Triticum aestivum ‘Cook’. Genome 48:97–107

    Article  CAS  PubMed  Google Scholar 

  • Pallotta MA, Warner P, Fox RL, Kuchel H, Jefferies SP, Langridge P (2003) Marker assisted wheat breeding in the southern region of Australia. In: Progna N (ed) Proceedings of the 10th international wheat genetics symposium. Paestum, Italy, pp 789–791

    Google Scholar 

  • Payne TS, Wanjama JK, Girma B (2001) Eastern Africa wheat pool. In: Bonjean AP, Angus WJ (eds) The world wheat book. A history of wheat breeding. Lavoisier, Paris, pp 901–922

    Google Scholar 

  • Pretorius ZA, Boshoff WHP, Kema GHJ (1997) First report of Puccinia striiformis f. sp. tritici on wheat in South Africa. Plant Dis 81:424

    Article  Google Scholar 

  • Pretorius ZA, Pakendorf KW, Marais GF, Prins R, Komen JS (2007) Challenges for sustainable cereal rust control in South Africa. Aust J Agric Res 58:593–601

    Article  Google Scholar 

  • Prins R, Ramburan VP, Pretorius ZA, Boyd LA, Boshoff WHP, Smith PH, Louw JH (2005) Development of a doubled haploid mapping population and linkage map for the bread wheat cross Kariega × Avocet S. S Afr J Plant Soil 22:1–8

    Article  CAS  Google Scholar 

  • Prins R, Pretorius ZA, Bender CM, Lehmensiek A (2011) QTL mapping of stripe, leaf and stem rust resistance genes in a Kariega × Avocet S doubled haploid wheat population. Mol Breed 270:259–270

    Article  Google Scholar 

  • Ramburan VP, Pretorius ZA, Louw JH, Boyd LA, Smith PH, Boshoff WHP, Prins R (2004) A genetic analysis of adult plant resistance to stripe rust in the wheat cultivar Kariega. Theor Appl Genet 108:1426–1433

    Article  CAS  PubMed  Google Scholar 

  • Röder MS, Korzun V, Wendehake K, Plaschke J, Tixier M-H, Leroy P, Ganal MW (1998) A microsatellite map of wheat. Genetics 149:2007–2023

    PubMed Central  PubMed  Google Scholar 

  • Rosewarne GM, Herrera-Foessel SA, Singh RP, Huerta-Espino J, Lan CX, He ZH (2013) Quantitative trait loci of stripe rust resistance in wheat. Theor Appl Genet 126:2427–2449

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rustgi S, Bandopadhyay R, Balyan HS, Gupta PK (2009) EST-SNPs in bread wheat: discovery, validation, genotyping and haplotype structure. Czech J Plant Breed 45:106–116

    CAS  Google Scholar 

  • Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234

    Article  CAS  PubMed  Google Scholar 

  • Semagn K, Bjørnstad A, Xu Y (2010) The genetic dissection of quantitative traits in crops. Electron J Biotechnol 13:16–17

    Article  Google Scholar 

  • Semagn K, Babu R, Hearne S, Olsen M (2014) Single nucleotide polymorphism genotyping using competitive Allele Specific PCR (KASP): overview of the technology and its application in crop improvement. Mol Breed 33:1–14

    Article  CAS  Google Scholar 

  • Singh RP, Nelson JC, Sorrells ME (2000) Mapping Yr28 and other genes for resistance to stripe rust in wheat. Crop Sci 40:1148–1155

    Article  CAS  Google Scholar 

  • Singh RP, Huerta-Espino J, William HM (2005) Genetics and breeding for durable resistance to leaf and stripe rusts in wheat. Turk J Agric For 29:121–127

    CAS  Google Scholar 

  • Somers DJ, Kirkpatrick R, Moniwa M, Walsh A (2003) Mining single-nucleotide polymorphisms from hexaploid wheat ESTs. Genome 49:431–437

    Article  Google Scholar 

  • Somers DJ, Isaac P, Edwards K (2004) A high-density microsatellite consensus map for bread wheat (Triticum austivum L.). Theor Appl Genet 109:1105–1114

    Article  CAS  PubMed  Google Scholar 

  • Sourdille P, Singh S, Cadalen T, Brown-Guedira GL, Gay G, Qi L, Gill BS, Dufour P, Murigneux A, Bernard M (2004) Microsatellite-based deletion bin system for the establishment of genetic-physical map relationships in wheat (Triticum aestivum L.). Funct Integr Genomics 4:12–25

    Article  CAS  PubMed  Google Scholar 

  • Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JAM (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35:W71–W74

    Article  PubMed Central  PubMed  Google Scholar 

  • Valesco E, Infante M, Durán M, Pèrez-Cabornero L, Sanz DJ, Esteban-Cardeñosa E, Miner C (2007) Heteroduplex analysis by capillary array electrophoresis for rapid mutation detection in large multiexon genes. Nat Protoc 2:237–246

    Article  Google Scholar 

  • Van Ooijen JW (2006) JoinMap® 4, software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen

    Google Scholar 

  • Van Ooijen JW (2009) MapQTL® 6, software for mapping of quantitative trait loci in experimental populations of diploid species. Kyazma BV, Wageningen

    Google Scholar 

  • Van Ooijen JW (2011) Multipoint maximum likelihood mapping in a full-sib family of an outbreeding species. Genet Res 93:343–349

    Article  Google Scholar 

  • Wang S, Basten CJ, Zeng Z-B (2012) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, North Carolina (http://statgen.ncsu.edu/qtlcart/WQTLCart.htm)

  • Xue S, Zhang Z, Lin F, Kong Z, Cao Y, Li C, Yi H, Mei M, Zhu H, Wu J, Xu H, Zhao D, Tian D, Zhang C, Ma Z (2008) A high-density intervarietal map of the wheat genome enriched with markers derived from expressed sequence tags. Theor Appl Genet 117:181–189

    Article  CAS  PubMed  Google Scholar 

  • Yan J-B, Tang J-H, Meng Y-J, Ma X-Q, Teng W-T, Subhash C, Li L, Li J-S (2006) Improving QTL mapping resolution based on genotypic sampling—a case using a RIL population. Acta Genet Sin 33:617–624

    Article  PubMed  Google Scholar 

  • Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Cereal Rusts Bull 3:14–23

    Google Scholar 

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Acknowledgments

We would like to thank F. J. Kloppers (PANNAR) for the trial site and stewardship of the field plot. Chrisna Steyn, Debbie Snyman, Denise Liebenberg, Mauritz Venter and Graham McGrann are thanked for technical assistance. The South African Winter Cereal Research Trust, National Research Foundation and the Biotechnology and Biological Sciences Research Council (BBSRC) and the Department for International Development (DFID), UK, are acknowledged for financial support. The BBSRC and DFID are also thanked for the PhD scholarship of GM Agenbag provided through the Sustainable Agriculture Research for International Development special initiative: SARID.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Plant Sciences, University of the Free State, PO Box 339, Bloemfontein, 9300, South Africa

    G. M. Agenbag, Z. A. Pretorius, C. M. Bender & R. Prins

  2. CenGen (Pty) Ltd, 78 Fairbairn Street, Worcester, 6850, South Africa

    G. M. Agenbag & R. Prins

  3. National Institute of Agricultural Botany, Huntingdon Road, Cambridge, CB3 0LE, UK

    L. A. Boyd

  4. Department of Life and Medical Sciences, University of Hertfordshire, Hatfield, AL10 9AB, Hertfordshire, UK

    L. A. Boyd

  5. Department of Disease and Stress Biology, John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK

    R. MacCormack

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  1. G. M. Agenbag
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  2. Z. A. Pretorius
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  3. L. A. Boyd
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Correspondence to R. Prins.

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Agenbag, G.M., Pretorius, Z.A., Boyd, L.A. et al. High-resolution mapping and new marker development for adult plant stripe rust resistance QTL in the wheat cultivar Kariega. Mol Breeding 34, 2005–2020 (2014). https://doi.org/10.1007/s11032-014-0158-4

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