Skip to main content
SpringerLink
Log in

Identification of quantitative trait loci for net form net blotch resistance in contemporary barley breeding germplasm from the USA using genome-wide association mapping

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

Association mapping study conducted in a population of 3490 elite barley breeding lines from ten barley breeding programs of the USA identified 12 QTLs for resistance/susceptibility to net form of net blotch.

Abstract

Breeding resistant varieties is the best management strategy for net form of net blotch (NFNB) in barley (Hordeum vulgare L.) caused by Pyrenophora teres f. teres (Ptt). Several resistance QTL have been previously identified in barley via linkage mapping and genome-wide association studies (GWAS). A GWAS conducted in a collection of advanced breeding lines (n = 3490) representing elite germplasm from ten barley breeding programs of the USA identified 42 unique marker-trait associations (MTA) for NFNB resistance. The lines were genotyped with 3072 SNP markers and phenotyped with four Ptt isolates in controlled environment. The lines were used to construct 13 different GWAS panels. Efficient mixed model association method with principal components and kinship was used for GWAS. Significance threshold for MTA was set at a false discovery rate of 0.05. Two, eight, six, one and 25 MTA were identified in chromosomes 1H, 3H, 4H, 5H and 6H, respectively. Based on genetic positions and linkage disequilibrium, these MTA’s correspond to two, three, two, one and four QTLs in chromosome 1H, 3H, 4H, 5H and 6H, respectively. A comparison with previous linkage and GWAS studies revealed several previously identified and novel QTLs. Moreover, different genomic regions were found to be responsible for NFNB resistance in two-row versus six-row germplasm. The germplasm-specific SNP markers with additive effects and allelic distribution is reported to facilitate breeders in selection of markers for MAS to introgress novel net blotch resistance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adhikari A, Steffenson BJ, Smith MJ, Dill-Macky R (2019) Genome-wide association mapping of seedling net form net blotch resistance in an Ethiopian and Eritrean Barley Collection. Crop Sci 59:1625–1638

    CAS  Google Scholar 

  • Afanasenko OS, Marja J, Pinnschmidt HO, Filatova O, Platz GJ (2009) Development of an international standard set of barley differential genotypes for Pyrenophora teres f. teres. Plant Pathol 58:665–676

    Google Scholar 

  • Amezrou R, Verma RPS, Chao S, Brueggeman RS, Belqadi L, Arbaoui M, Rehman S, Gyawali S (2018) Genome-wide association studies of net form of net blotch resistance at seedling and adult plant stages in spring barley collection. Mol Breed 38:1–14

    Google Scholar 

  • Barleymap. http://floresta.eead.csic.es/barleymap

  • Berger GL, Liu S, Hall MD, Brooks WS, Chao S, Muehlbauer GJ, Baik B-K, Steffenson B, Griffey CA (2013) Marker-trait associations in Virginia Tech winter barley identified using genome-wide mapping. Theor Appl Genet 126:693–710

    CAS  PubMed  Google Scholar 

  • Bockelman H, Sharp E, Eslick R (1977) Trisomic analysis of genes for resistance to scald and net blotch in several barley cultivars. Can J Bot 55:2142–2148

    Google Scholar 

  • Cakir M, Gupta S, Platz G, Ablett GA, Loughman R, Emebiri L, Poulsen D, Li C, Lance R, Galwey N (2003) Mapping and validation of the genes for resistance to Pyrenophora teres f. teres in barley (Hordeum vulgare L.). Crop Pasture Sci 54:1369–1377

    CAS  Google Scholar 

  • Cantalapiedra CP, Boudiar R, Casas AM, Igartua E, Contreras-Moreira B (2015) BARLEYMAP: physical and genetic mapping of nucleotide sequences and annotation of surrounding loci in barley. Mol Breed 35:13

    Google Scholar 

  • Close TJ, Bhat PR, Lonardi S, Wu Y, Rostoks N, Ramsay L, Druka A, Stein N, Svensson JT, Wanamaker S (2009) Development and implementation of high-throughput SNP genotyping in barley. BMC Genom 10:582

    Google Scholar 

  • Daba SD, Horsley R, Brueggeman R, Chao S, Mohammadi M (2019) Genome-wide association studies and candidate gene identification for leaf scald and net blotch in barley (L.) Plant Dis 103:880–889

    PubMed  Google Scholar 

  • Endelman JB (2011) Ridge regression and other kernels for genomic selection with R package rrBLUP. Plant Genome 4:250–255

    Google Scholar 

  • Friesen T, Faris J, Lai Z, Steffenson B (2006) Identification and chromosomal location of major genes for resistance to Pyrenophora teres in a doubled-haploid barley population. Genome 49:855–859

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Hamblin MT, Close TJ, Bhat PR, Chao S, Kling JG, Abraham KJ, Blake T, Brooks WS, Cooper B, Griffey CA, Hayes PM, Hole DJ, Horsley RD, Obert DE, Smith KP, Ullrich SE, Muehlbauer GJ, Jannink J-L (2010) Population structure and linkage disequilibrium in US barley germplasm: implications for association mapping. Crop Sci 50:556–566

    CAS  Google Scholar 

  • Jordan V (1981) Aetiology of barley net blotch caused by Pyrenophora teres and some effects on yield. Plant Pathol 30:77–87

    Google Scholar 

  • Kang HM, Zaitlen NA, Wade CM, Kirby A, Heckerman D, Daly MJ, Eskin E (2008) Efficient control of population structure in model organism association mapping. Genetics 178:1709–1723

    PubMed  PubMed Central  Google Scholar 

  • Khan T (1987) Relationship between net blotch (Drechslera teres) and losses in grain yield of barley in Western Australia. Crop Pasture Sci 38:671–679

    Google Scholar 

  • Koladia VM, Faris JD, Richards JK, Brueggeman RS, Chao S, Friesen TL (2017) Genetic analysis of net form net blotch resistance in barley lines CIho 5791 and Tifang against a global collection of P. teres f. teres isolates. Theor Appl Genet 130:163–173

    CAS  PubMed  Google Scholar 

  • Lehmensiek A, Platz G, Mace E, Poulsen D, Sutherland M (2008) Mapping of adult plant resistance to net form of net blotch in three Australian barley populations. Crop Pasture Sci 58:1191–1197

    Google Scholar 

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

    PubMed  Google Scholar 

  • Ma Z, Lapitan NL, Steffenson B (2004) QTL mapping of net blotch resistance genes in a doubled-haploid population of six-rowed barley. Euphytica 137:291–296

    CAS  Google Scholar 

  • Manninen O, Kalendar R, Robinson J, Schulman A (2000) Application of BARE-1 retrotransposon markers to the mapping of a major resistance gene for net blotch in barley. Mol Gen Genet 264:325–334

    CAS  PubMed  Google Scholar 

  • Manninen O, 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

    CAS  PubMed  Google Scholar 

  • Martens JW, Seaman WL, Atkinson TG (1988) Disease of field crops in Canada. An illustrated compendium. Can Phytopathol Soc (Revised edition)

  • Mascher M, Muehlbauer GJ, Rokhsar DS, Chapman J, Schmutz J, Barry K, Muñoz-Amatriaín M, Close TJ, Wise RP, Schulman AH, Himmelbach A, Mayer KFX, Scholz U, Poland JA, Stein N, Waugh R (2013) Anchoring and ordering NGS contig assemblies by population sequencing (POPSEQ). Plant J 76:718–727

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mascher M, Gundlach H, Himmelbach A, Beier S, Twardziok SO, Wicker T, Radchuk V, Dockter C, Hedley PE, Russell J, Bayer M (2017) A chromosome conformation capture ordered sequence of the barley genome. Nature 544:427–433

    CAS  PubMed  Google Scholar 

  • Massman J, Cooper B, Horsley R, Neate S, Dill-Macky R, Chao S, Dong Y, Schwarz P, Muehlbauer G, Smith K (2011) Genome-wide association mapping of Fusarium head blight resistance in contemporary barley breeding germplasm. Mol Breed 27:439–454

    Google Scholar 

  • McLean MS, Howlett BJ, Hollaway GJ (2009) Erratum to: epidemiology and control of spot form of net blotch (Pyrenophora teres f. maculata) of barley: a review. Crop Pasture Sci 60:499

    Google Scholar 

  • Mohammadi M, Endelman JB, Nair S, Chao S, Jones SS, Muehlbauer GJ, Ullrich SE, Baik B-K, Wise ML, Smith KP (2014) Association mapping of grain hardness, polyphenol oxidase, total phenolics, amylose content, and β-glucan in US barley breeding germplasm. Mol Breed 34:1229–1243

    CAS  Google Scholar 

  • Mohammadi M, Blake TK, Budde AD, Chao S, Hayes PM, Horsley RD, Obert DE, Ullrich SE, Smith KP (2015) A genome-wide association study of malting quality across eight US barley breeding programs. Theor Appl Genet 128:705–721

    CAS  PubMed  Google Scholar 

  • Muñoz-Amatriaín M, Moscou MJ, Bhat PR, Svensson JT, Bartoš J, Suchánková P, Šimková H, Endo TR, Fenton RD, Lonardi S (2011) An improved consensus linkage map of barley based on flow-sorted chromosomes and single nucleotide polymorphism markers. Plant Genome 4:238–249

    Google Scholar 

  • Novakazi F, Afanasenko O, Anisimova A, Platz GJ, Snowdon R, Kovaleva O, Zubkovich A, Ordon F (2019) Genetic analysis of a worldwide barley collection for resistance to net form of net blotch disease (Pyrenophora teres f. teres). Theor Appl Genet 132:2633–2650

    PubMed  Google Scholar 

  • Pauli D, Muehlbauer GJ, Smith KP, Cooper B, Hole D, Obert DE, Ullrich SE, Blake TK (2014) Association mapping of agronomic QTLs in US spring barley breeding germplasm. Plant Genome 7:3

    Google Scholar 

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

    Google Scholar 

  • R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Rafalski JA (2010) Association genetics in crop improvement. Curr Opin Plant Biol 13:174–180

    CAS  PubMed  Google Scholar 

  • Richards J, Chao S, Friesen T, Brueggeman R (2016) Fine mapping of the barley chromosome 6H net form net blotch susceptibility locus. G3-Genes Genom Genet 6:1809–1818

    CAS  Google Scholar 

  • Richards JK, Friesen TL, Brueggeman RS (2017) Association mapping utilizing diverse barley lines reveals net form net blotch seedling resistance/susceptibility loci. Theor Appl Genet 130:915–927

    CAS  PubMed  Google Scholar 

  • Rozanova IV, Lashina NM, Mustafin ZS, Gorobets SA, Efimov VM, Afanasenko OS, Khlestkina EK (2019) SNPs associated with barley resistance to isolates of Pyrenophora teres f. teres. BMC Genomics 20(3):292

    PubMed  PubMed Central  Google Scholar 

  • Serenius M, Mironenko N, Manninen O (2005) Genetic variation, occurrence of mating types and different forms of Pyrenophora teres causing net blotch of barley in Finland. Mycol Res 109:809–817

    CAS  PubMed  Google Scholar 

  • Sneller C, Mather D, Crepieux S (2009) Analytical approaches and population types for finding and utilizing QTL in complex plant populations. Crop Sci 49:363–380

    Google Scholar 

  • Steffenson B (1997) Compendium of barley diseases

  • Steffenson BJ, Smith KP (2006) Breeding barley for multiple disease resistance in the Upper Midwest region of the USA. Czech J Genet Plant Breed 42:79

    Google Scholar 

  • Steffenson B, Hayes P, 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 92:552–558

    CAS  PubMed  Google Scholar 

  • Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci 100:9440–9445

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Wonneberger R, Ficke A, Lillemo M (2017) Identification of quantitative trait loci associated with resistance to net form net blotch in a collection of Nordic barley germplasm. Theor Appl Genet 130:2025–2043

    CAS  PubMed  Google Scholar 

  • Triticeae Coordinated Agricultural Project. https://triticeaecap.org/

  • Triticeae Coordinated Agricultural Project, T3 Barley Toolbox database. https://triticeaetoolbox.org/barley/

  • Yu J, Buckler ES (2006) Genetic association mapping and genome organization of maize. Curr Opin Biotechnol 17:155–160

    CAS  PubMed  Google Scholar 

  • Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208

    CAS  PubMed  Google Scholar 

  • Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14:415–421

    Google Scholar 

  • Zhou H, Steffenson B (2013a) Genome-wide association mapping reveals genetic architecture of durable spot blotch resistance in US barley breeding germplasm. Mol Breed 32:139–154

    Google Scholar 

  • Zhou H, Steffenson BJ (2013b) Association mapping of septoria speckled leaf blotch resistance in US barley breeding germplasm. Phytopathology 103:600–609

    PubMed  Google Scholar 

  • Zhou H, Steffenson B, Muehlbauer G, Wanyera R, Njau P, Ndeda S (2014) Association mapping of stem rust race TTKSK resistance in US barley breeding germplasm. Theor Appl Genet 127:1293–1304

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu C, Gore M, Buckler ES, Yu J (2008) Status and prospects of association mapping in plants. Plant Genome 1:5–20

    CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge the funding from American Malting Barley Association. The authors would also like to acknowledge help from Amar Elakkad, and Beheshteh Zargaran during phenotyping and Dr. Ahmad Sallam and Dr. Austin Case during data analysis.

Author information

Author notes

  1. Anil Adhikari

    Present address: Soil and Crop Science Department, Texas A&M University, College Station, TX, 77845, USA

Authors and Affiliations

  1. Department of Plant Pathology, University of Minnesota, Saint Paul, MN, 55108, USA

    Anil Adhikari, Brian J. Steffenson, Madeleine Smith & Ruth Dill-Macky

  2. Department of Agronomy and Plant Genetics, University of Minnesota, Saint Paul, MN, 55108, USA

    Kevin P. Smith

Authors
  1. Anil Adhikari
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Brian J. Steffenson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kevin P. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Madeleine Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ruth Dill-Macky
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

RDM, KPS and BJS planned the experiments. RDM conducted the phenotyping. AA conducted the analysis and drafted the manuscript. KPS and RDM guided the analysis and manuscript writing. All authors reviewed the manuscript.

Corresponding authors

Correspondence to Anil Adhikari or Ruth Dill-Macky.

Ethics declarations

Conflict of interests

The authors declare no conflict of interests.

Additional information

Communicated by Albrecht E. Melchinger.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 4088 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Adhikari, A., Steffenson, B.J., Smith, K.P. et al. Identification of quantitative trait loci for net form net blotch resistance in contemporary barley breeding germplasm from the USA using genome-wide association mapping. Theor Appl Genet 133, 1019–1037 (2020). https://doi.org/10.1007/s00122-019-03528-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-019-03528-5

Search

Navigation