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Barley 4H QTL confers NFNB resistance to a global set of P. teres f. teres isolates

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Abstract

Net form net blotch (NFNB), caused by Pyrenophora teres f. teres Drechs., is prevalent in barley-growing regions worldwide. A population of 132 recombinant inbred lines (RILs) developed from a cross of the barley varieties ‘Falcon’ and ‘Azhul’ were used to evaluate resistance to NFNB due to their differential reactions to isolates of P. teres f. teres from Australia, Canada, Japan, and the USA. Falcon is a six-rowed, hulless feed barley harboring resistance to NFNB, while Azhul is a six-rowed, hulless food barley with high levels of susceptibility to many P. teres f. teres isolates. Seedling disease resistance data were collected on seedlings of parents, RILs, and checks in a growth chamber. The population was genotyped using Illumina’s GoldenGate assay, and quantitative trait loci (QTL) were detected on chromosomes 2H, 3H, 4H, and 6H. We identified a single genetic region on barley chromosome 4H that provided varying levels of resistance to all P. teres f. teres isolates evaluated.

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References

  • Abu Qamar M, Liu ZH, Faris JD, Chao S, Edwards MC, Lai Z, Franckowiak JD, Friesen TL (2008) A region of barley chromosome 6H harbors multiple major genes associated with net type net blotch resistance. Theoret Appl Genet 117:1261–1270

    Article  CAS  Google Scholar 

  • Arabi MIE, Al-Safadi B, Charbaji T (2003) Pathogenic variation among isolates of Pyrenophora teres, the causal agent of barley net blotch. J Phytopathology 151:376–382

    Article  Google Scholar 

  • Cakir M, Gupta S, Platz GJ, Ablett GA, Loughman R, Emebiri LC, Poulsen D, Li CD, Lance RCM, Galway NW, Jones MGK, Appels R (2003) Mapping and validation of the genes for resistance to Pyrenophora teres f. teres in barley (Hordeum vulgare L.). Aust J Agric Res 54:1369–1377

    Article  CAS  Google Scholar 

  • Chao S, Zhang W, Dubcovsky J, Sorrells M (2007) Evaluation of genetic diversity and genome-wide linkage disequilibrium among U.S. wheat (Triticum aestivum L.) germplasm representing different market classes. Crop Sci 47:1018–1030

    Article  CAS  Google Scholar 

  • Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chutimanitsakun Y, Cuesta-Marcos A, Chao S, Corey A, Filichkin T, Fisk S, Kolding M, Meints B, Ong YL, Rey JI, Ross AS, Hayes PM (2013) Application of marker-assisted selection and genome-wide association scanning to the development of winter food barley germplasm resources. Plant Breed 132:563–570

    Article  CAS  Google Scholar 

  • Close TJ, Bhat PR, Lonardi S, Wu Y, Rostoks N, Ramsay L, Druka A, Stein N, Svensson JT, Wanamaker S, Bozdag S, Roose ML, Moscou MJ, Chao S, Varshney RK, Szucs P, Sato K, Hayes PM, Matthews DE, Kleinhofs A, Muehlbauer GJ, DeYoung J, Marshall DF, Madishetty K, Fenton RD, Condamine P, Graner A, Waugh R (2009) Development and implementation of high-throughput SNP genotyping in barley. BMC Genomics 10:582

    Article  PubMed  PubMed Central  Google Scholar 

  • Cromey MG, Parks RA (2003) Pathogenic variation in Drechslera teres in New Zealand. NZ Plant Protect 56:251–256

    Google Scholar 

  • Ellwood SR, Liu ZH, Syme R, Hane J, Keiper F, Oliver RP, Friesen TL (2010) A first genome assembly of the barley fungal pathogen Pyrenophora teres f. teres. Genome Biol 11:R109

    Article  PubMed  PubMed Central  Google Scholar 

  • Emebiri LC, Platz G, Moody DB (2005) Disease resistance genes in a doubled haploid population of two-rowed barley segregating for malting quality attributes. Aust J Agric Res 56:49–56

    Article  CAS  Google Scholar 

  • Fan JB, Oliphant A, Shen R, Kermani BG, Garcia F, Gunderson KL, Hansen M, Steemers F, Butler SL, Deloukas P, Galver L, Hunt S, McBride C, Bibikova M, Rubano T, Chen J, Wickham E, Doucet D, Chang W, Campbell D, Zhang B, Kruglyak S, Bentley D, Haas J, Rigault P, Zhou L, Stuelpnagel J, Chee MS (2003) Highly parallel SNP genotyping. Cold Spring Harb Symp Quant Biol 68:69–78

    Article  CAS  PubMed  Google Scholar 

  • Friesen TL, Faris JD, Lai Z, Steffenson BJ (2006) Identification and chromosomal location of major genes for resistance to Pyrenophora teres in a barley doubled haploid population. Genome 409:855–859

    Article  Google Scholar 

  • Graner A, Foroughi-Wehr B, Tekauz A (1996) RFLP mapping of a gene in barley conferring resistance to net blotch (Pyrenophora teres). Euphytica 91:229–234

    CAS  Google Scholar 

  • Grewal TS, Rossnagel BG, Pozniak C, Scoles GJ (2008) Mapping quantitative trait loci associated with barley net blotch resistance. Theor Appl Genet 116:529–539

    Article  CAS  PubMed  Google Scholar 

  • Grewal TS, Rossnagel BG, Scoles GJ (2012) Mapping quantitative trait loci associated with spot blotch and net blotch resistance in a doubled-haploid barley population. Mol Breed 30:267–279

    Article  CAS  Google Scholar 

  • Gupta S, Loughman R (2001) Current virulence of Pyrenophora teres on barley in Western Australia. Plant Dis 85:960–966

    Article  Google Scholar 

  • Gupta S, Li C, Loughman R, Cakir M, Platz G, Westcott S, Bradley J, Broughton S, Lance R (2010) Quantitative trait loci and epistatic interactions in barley conferring resistance to net type net blotch Pyrenophora teres f. teres isolates. Plant Breed 129:362–368

    CAS  Google Scholar 

  • Hayes PM, Corey AE, Dovel R, Karow R, Mundt C, Rhinart K, Vivar H (2000) Registration of Orca barley. Crop Sci 40:849–851

    Article  Google Scholar 

  • Hearnden PR, Eckermann PJ, McMichael GL, Hayden MJ, Eglinton JK, Chalmers KJ (2007) A genetic map of 1,000 SSR and DArT markers in a wide barley cross. Theor Appl Genet 115:383–391

    Article  CAS  PubMed  Google Scholar 

  • Helm JH, Cortez MJ, Salmon DF, Jedel PE, Stewart WM (1996) Registration of ‘Falcon’ barley. Crop Sci 36:807

    Google Scholar 

  • Islamovic E, Obert DE, Oliver RE, Harrison SA, Ibrahim A, Marshall JM, Miclaus KJ, Hu G, Jackson EW (2013a) Genetic dissection of grain beta-glucan and amylose content in barley (Hordeum vulgare L.). Mol Breeding 31:15–25

    Article  CAS  Google Scholar 

  • Islamovic E, Obert DE, Oliver RE, Marshall JM, Miclaus KJ, Hang A, Chao S, Lazo GR, Harrison SA, Ibrahim A, Jellen EN, Maughan PJ, Brown RH, Jackson EW (2013b) A new genetic linkage map of barley (Hordeum vulgare L.) facilitates genetic dissection of height and spike length and angle. Field Crop Res 154:91–99

    Article  Google Scholar 

  • Jalli M (2004) Suitability of a selected barley differential set for Pyrenophora teres f. teres virulence screening. In, Proceedings of the 9th International Barley Genetics Symposium, Brno Czech Republic, pp. 266–269

  • Jalli M, Robinson J (2000) Stable resistance in barley to Pyrenophora teres f. teres isolates from the Nordic-Baltic region after increase on standard host genotypes. Euphytica 113:71–77

    Article  Google Scholar 

  • Jonsson R, Bryngelsson T, Gustafsson M (1997) Virulence studies of Swedish net blotch isolates (Drechslera teres) and identification of resistant barley lines. Euphytica 94:209–218

    Article  Google Scholar 

  • Kandemir N, Jones BL, Wesenberg DM, Ullrich SE, Kleinhofs A (2000a) Marker-assisted analysis of three grain yield QTL in barley (Hordeum vulgare L.) using near isogenic lines. Mol Breed 6:157–167

    Article  CAS  Google Scholar 

  • Kandemir N, Kudrna DA, Ullrich SE, Kleinhofs A (2000b) Molecular marker assisted genetic analysis of head shattering in six-rowed barley. Theor Appl Genet 101:203–210

    Article  CAS  Google Scholar 

  • Kersey PJ, Allen JE, Armean I, Boddu S, Bolt BJ, Carvalho-Silva D, Christensen M, Davis P, Falin LJ, Grabmueller C, Humphrey J, Kerhornou A, Khobova J, Aranganathan NK, Langridge N, Lowy E, McDowall MD, Maheswari U, Nuhn M, Kee Ong C, Overduin B, Paulini M, Pedro H, Perry E, Spundich G, Tapanari E, Walts B, Williams G, Tello-Ruiz M, Stein J, Wei S, Ware D, Bolser DM, Howe KL, Kulesha E, Lawson D, Maslen G, Staines DM (2016) Ensembl Genomes 2016: more genomes, more complexity. Nucleic Acids Res 44:D574–D580

    Article  PubMed  Google Scholar 

  • Khan TN (1982) Changes in barley genotypes grown in Western Australia. Plant Dis 66:655–656

    Article  Google Scholar 

  • Khan TN, Boyd WJR (1969a) Physiologic specialization in Drechslera teres. Aust J Biol Sci 22:1229–1235

    Google Scholar 

  • Kleinhofs A, Kilian A, Saghai Maroof MA, Biyashev RM, Hayes P, Chen FQ, Lapitan N, Fenwick A, Blake TK, Kanazin V, Ananiev E, Dahleen L, Kudrna D, Bollinger J, Knapp SJ, Liu B, Sorrells M, Heun M, Franckowiak JD, Hoffman D, Skadsen R, Steffenson BJ (1993) A molecular, isozyme and morphological map of the barley (Hordeum vulgare) genome. Theor Appl Genet 86:705–712

    Article  CAS  PubMed  Google Scholar 

  • Koladia VM, Faris JD, Brueggeman RS, Chao S, Friesen TL (2016) Genetic analysis of net form net blotch resistance in barley lines CI5791 and Tifang against a global collection of P. teres f. teres isolates. Theoret Appl Genet. doi:10.1007/s00122-016-2801-4

    Google Scholar 

  • Konig J, Perovic D, Kopahnke D, Ordon F (2013) Development of an efficient method for assessing resistance to the net type of net blotch (Pyrenophora teres f. teres) in winter barley and mapping of quantitative trait loci for resistance. Mol Breed 32:641–650

    Article  Google Scholar 

  • Konig J, Perovic D, Kopahnke D, Ordon F (2014) Mapping seedling resistance to net form of net blotch (Pyrenophora teres f. teres) in barley using detached leaf assay. Plant Breed 133:356–365

    Article  Google Scholar 

  • Lai Z, Faris JD, Weiland JJ, Steffenson BJ, Friesen TL (2007) Genetic mapping of Pyrenophora teres f. teres genes conferring avirulence on barley. Fungal Genet Biol 44:323–329

    Article  CAS  PubMed  Google Scholar 

  • Lehmensiek A, Platz GJ, Mace E, Poulsen D, Sutherland MW (2007) Mapping of adult plant resistance to net form of net blotch in three Australian barley populations. Aust J Agric Res 58:1191–1197

    Article  Google Scholar 

  • Liu ZH, Ellwood SR, Oliver RP, Friesen TL (2011) Pyrenophora teres: profile of an increasingly damaging barley pathogen. Mol Plant Pathol 12:1–19

    Article  PubMed  Google Scholar 

  • Liu ZH, Zhong S, Edwards MC, Friesen TL (2012) Virulence profile and genetic structure of a North Dakota population of Pyrenophora teres f. teres, the causal agent of net form net blotch of barley. Phytopathology 102:539–546

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Holmes DJ, Faris JD, Chao S, Brueggeman R, Edwards MC, Friesen TL (2015) Necrotrophic effector-triggered susceptibility (NETS) underlies the barley-Pyrenophora teres f. teres interaction specific to chromosome 6H. Mol Plant Pathol 16(2):188–200

    Article  CAS  PubMed  Google Scholar 

  • Lu S, Platz GJ, Edwards MC, Friesen TL (2010) Mating type locus -specific polymerase chain reaction markers for differentiation of Pyrenophora teres f. teres and P. teres f. maculata, the causal agents of barley net blotch. Phytopathology 100:1298–1306

    Article  CAS  PubMed  Google Scholar 

  • Ma Z, Steffenson BJ, Prom LK, Lapitan NL (2000) Mapping of quantitative trait loci for Fusarium head blight resistance in barley. Phytopathology 90:1079–1088

    Article  CAS  PubMed  Google Scholar 

  • Manninen OM, Jalli M, Kalendar R, Schulman A, Afanasenko O, Robinson J (2006) Mapping of major spot-type and net-type net-blotch resistance genes in the Ethiopian barley line CI 9819. Genome 49:1564–1571

    Article  CAS  PubMed  Google Scholar 

  • Marcel TC, Varshney RK, Barbieri M, Jafary H, de Kock MJD, Graner A, Niks RE (2007) High-density consensus map of barley to compare the distribution of QTLs for partial resistance of Puccinia hordei A and of defense gene homologues. Theor Appl Genet 114:487–500

    Article  CAS  PubMed  Google Scholar 

  • Mester D, Ronin Y, Minkov D, Nevo E, Korol AB (2003a) Constructing large-scale genetic maps using an evolutionary strategy algorithm. Genetics 165:2269–2282

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mester DI, Ronin YI, Hu Y, Peng J, Nevo E, Korol AB (2003b) Efficient multipoint mapping: making use of dominant repulsion-phase markers. Theor Appl Genet 107:1002–1112

    Article  Google Scholar 

  • Molnar SJ, James LE, Kasha KJ (2000) Inheritance and RAPD tagging of multiple genes for resistance to net blotch in barley. Genome 43:224–231

  • Oliver RE, Islamovic E, Obert DE, Wise ML, Herrin LL, Hang A et al (2014) Comparative systems biology reveals allelic variation modulating tocochromanol profiles in barley (Hordeum vulgare L.). PLoS One 9(5):e96276. doi:10.1371/journal.pone.0096276

    Article  PubMed  PubMed Central  Google Scholar 

  • Potokina E, Druka A, Luo Z, Wise R, Waugh R, Kearsey M (2008) Gene expression quantitative trait locus analysis of 16,000 barley genes reveals a complex pattern of genome-wide transcriptional regulation. Plant J 53:90–101

    Article  CAS  PubMed  Google Scholar 

  • Raman H, Platz GJ, Chalmers KJ, Raman R, Read BJ, Barr AR, Moody DB (2003) Mapping of genetic regions associated with net form of net blotch resistance in barley. Aust J Agric Res 54:1359–1367

    Article  CAS  Google Scholar 

  • Read BJ, Raman H, McMichael G, Chalmers KJ, Ablett GA, Platz GJ, Raman R, Genger RK, Boyd WJR, Li CD, Grime CR, Park RF, Wallwork H, Prangnell R, Lance CM (2003) Mapping and QTL analysis of the barley population Sloop × Halcyon. Aust J Agric Res 54:1145–1153

    Article  CAS  Google Scholar 

  • Richter K, Schondelmaier J, Jung C (1998) Mapping of quantitative trait loci affecting Drechslera teres resistance in barley with molecular markers. Theor Appl Genet 97:1225–1234

    Article  CAS  Google Scholar 

  • Romagosa I, Han F, Ullrich SE, Hayes PM, Wesenberg DM (1999) Verification of yield QTL through realized molecular marker-assisted selection response in a barley cross. Mol Breed 5:143–152

    Article  Google Scholar 

  • Ronin Y, Mester D, Minkov D, Korol A (2010) Building reliable genetic maps: different mapping strategies may result in different maps. Nat Sci 2:576–589

    CAS  Google Scholar 

  • Rostoks N, Mudie S, Cardle L, Russell J, Ramsay L, Booth A, Svensson JT, Wanamaker SI, Walia H, Rodriguez EM, Hedley PE, Liu H, Morris J, Close TJ, Marshall DF, Robbie Waugh R (2005) Genome-wide SNP discovery and linkage analysis in barley based on genes responsive to abiotic stress. Mol Genet Genom 274:515–527

    Article  CAS  Google Scholar 

  • Sato K, Takeda K (1993) Pathogenic variation of Pyrenophora teres isolates collected from Japanese and Canadian spring barley. Bull Res Inst Bioresour Okayama Univ 1:147–158

    Google Scholar 

  • Sato K, Nankaku N, Takeda K (2009) A high density transcript linkage map of barley derived from a single population. Heredity 103:110–117

    Article  CAS  PubMed  Google Scholar 

  • Schmierer DA, Kandemir N, Kudrna DA, Jones BL, Ullrich SE, Kleinhofs A (2005) Molecular marker-assisted selection for enhanced yield in malting barley. Mol Breed 14:463–473

    Article  Google Scholar 

  • Shjerve RA, Faris JD, Brueggeman RS, Yan C, Zhu Y, Koladia V, Friesen TL (2014) Evaluation of a Pyrenophora teres f. teres mapping population reveals multiple independent interactions with a region barley chromosome 6H. Fungal Genet Biol 70:104–112

    Article  CAS  PubMed  Google Scholar 

  • Spaner D, Shugar LP, Choo TM, Falak I, Briggs KG, Legge WG, Falk DE, Ullrich SE, Tinker NA, Steffenson BJ, Mather DE (1998) Mapping of disease resistance loci in barley on the basis of visual assessment of naturally occurring symptoms. Crop Sci 38:843–850

    Article  Google Scholar 

  • St. Pierre S, Gustus C, Steffenson BJ, Dill-Macky R, Smith KP (2010) Mapping net form net blotch and Septoria speckled leaf blotch resistance loci in barley. Phytopathology 100:80–84

    Article  CAS  PubMed  Google Scholar 

  • Steffenson BJ, Webster RK (1992) Pathotype diversity of Pyrenophora teres f. teres on barley. Phytopathology 82:170–177

    Article  Google Scholar 

  • Steffenson BJ, Hayes PM, Kleinhofs A (1996) Genetics of seedling and adult plant resistance to net blotch (Pyrenophora teres f. teres) and spot blotch (Cochliobolus sativus) in barley. Theor Appl Genet 92(5):552–558

    Article  CAS  PubMed  Google Scholar 

  • Stein N, Prasad M, Scholz U, Thiel T, Zhang H, Wolf M, Kota R, Varshney RK, Perovic D, Grosse I, Graner A (2007) A 1,000-loci transcript map of the barley genome: new anchoring points for integrative grass genomics. Theor Appl Genet 114:823–839

    Article  CAS  PubMed  Google Scholar 

  • Szűcs P, Blake VC, Bhat PR, Close TJ, Cuesta-Marcos A, Muehlbauer GJ, Ramsay LV, Waugh R, Hayes PM (2009) An integrated resource for barley linkage map and malting quality QTL alignment. Plant Genome 2:134–140

    Article  Google Scholar 

  • Tekauz A (1985) A numerical scale to classify reactions of barley to Pyrenophora teres. Can J Plant Pathol 7:181–183

    Article  Google Scholar 

  • Tekauz A (1990) Characterization and distribution of pathogenic variation in Pyrenophora teres f. teres and P. teres f. maculata from western Canada. Can J Plant Pathol 12:141–148

    Article  Google Scholar 

  • Toojinda T, Baird E, Booth A, Broers L, Hayes P, Powell W, Thomas W, Vivar H, Young G (1998) Introgression of quantitative trait loci (QTLs) determining stripe rust resistance in barley: an example of marker-assisted line development. Theor Appl Genet 96:123–131

    Article  CAS  Google Scholar 

  • van Ooijen JW (1999) LOD significance thresholds for QTL analysis in experimental populations of diploid species. Heredity 83:613–624

    Article  PubMed  Google Scholar 

  • Varshney RK, Marcel TC, Ramsay L, Russell J, Roder MS, Stein N, Waugh R, Langridge P, Niks RE, Graner A (2007) A high density barley microsatellite consensus map with 775 SSR loci. Theor Appl Genet 114:1091–1103

    Article  CAS  PubMed  Google Scholar 

  • Verhoeven EC, Bonman M, Bregitzer P, Brunick B, Cooper B, Corey AE, Cuesta-Marcos A, Filichkina T, Mundt CC, Obert D, Rossnagel B, Richardson K, Hayes PM (2011) Registration of the BISON genetic stocks in Hordeum vulgare. L J Plant Reg 5:135–150

    Article  Google Scholar 

  • Wang S, Basten CJ, Zeng Z-B (2005) Windows QTL Cartographer 2.5. Available at statgen.ncsu.edu/qtlcart/WQTL-Cart.htm. Dept. Statistics, North Carolina State University, Raleigh

  • Weiland JJ, Steffenson BJ, Cartwright RD, Webster RK (1999) Identification of molecular genetic markers in Pyrenophora teres f. teres associated with low virulence on ‘Harbin’ barley. Phytopathology 89:176–181. doi:10.1094/PHYTO.1999.89.2.176

  • Wenzl P, Li H, Carling J, Zhou M, Raman H, Paul E, Hearnden P, Maier C, Xia L, Caig V, Ovesná J, Cakir M, Poulsen D, Wang J, Raman R, Smith KP, Muehlbauer GJ, Chalmers KJ, Kleinhofs A, Huttner E, Kilian A (2006) A high-density consensus map of barley linking DArT markers to SSR, RFLP and STS loci and agricultural traits. BMC Genomics 7:206

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu HL, Steffenson BJ, Zhong S (2003) Genetic variation for virulence and RFLP markers in Pyrenophora teres. Can J Plant Pathol 25:82–90

    Article  CAS  Google Scholar 

  • Zeng Z (1994) Precision mapping of quantitative trait loci. Genetics 136:1457–1468

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank and recognize the efforts of Danielle Holmes for fungal inoculations and her management of the greenhouse projects. This work was funded by the USDA-NIFA-AFRI grant number 2011-68002-30029 (T-CAP), USDA Barley for Rural Development Grant, The Idaho Barley Commission, and USDA ARS CRIS Projects 5442-22000-048-00D and 2050-21000-031-00. The USDA ARS is an equal opportunity employer.

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  1. Emir Islamovic

    Present address: BASF, Research Triangle Park, NC, 27709, USA

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  1. USDA ARS, 1691 S. 2700 W., Aberdeen, ID, 83210, USA

    Emir Islamovic & Phil Bregitzer

  2. Cereal Crops Research Unit, Northern Crop Science Laboratory, USDA ARS, Fargo, ND, 58105, USA

    Timothy L Friesen

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Islamovic, E., Bregitzer, P. & Friesen, T.L. Barley 4H QTL confers NFNB resistance to a global set of P. teres f. teres isolates. Mol Breeding 37, 29 (2017). https://doi.org/10.1007/s11032-017-0621-0

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