Skip to main content
SpringerLink
Log in

Genome-wide association studies of net form of net blotch resistance at seedling and adult plant stages in spring barley collection

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

Net form of net blotch (NFNB) of barley (Hordeum vulgare L.), caused by Pyrenophora teres f. teres (Ptt) Drechsler (anamorph: Drechslera teres [Sacc.] Shoem.), is considered one of the major constraints of successful barley production in major barley growing regions of the world. Resistance to NFNB was evaluated in a barley collection of 336 genotypes (AM-2014), at seedling stage using isolates LGDPtt.19 and TD10 in the USA, and adult stage in seven hotspot environments in Morocco. The AM-2014 panel was genotyped with 9K SNP markers and genome-wide association studies (GWAS) were carried out using mixed linear model (MLM: Q + K) accounting for population structure (Q) and kinship (K) as covariates. Significant (P < 0.001) marker trait associations were corrected for false discovery rate (FDR) at the q < 0.05. Four genotypes showed an average infection response (IRs ≤ 2) to both isolates, LGDPttt.19 and TD10, at the seedling stage, and 30 genotypes showed resistance in all environments in the field while three genotypes exhibited the highest resistance at both stages. The GWAS of NFNB identified 31 distinct QTLs on all seven barley chromosomes, of which 8 with resistance at seedling stage, 21 were associated with resistance at the adult stage, and two QTLs, QRptt.2H-132.15 and QPtt.6H-54-55, conferred resistance at both stages. Of 31 resistance QTLs reported in this study, 10 QTLs coincided with previously mapped QTL while 21 are novel, thereby validating the GWAS approach used in this study. The resistance sources identified in AM-2014 and QTL mapped in this study are valuable resources for marker-assisted breeding for NFNB resistance in the future.

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

Similar content being viewed by others

References

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

    Article  PubMed  CAS  Google Scholar 

  • Afanasenko O, Mironenko N, Filatova O, Kopahnke D, Kramer I, Ordon F (2007) Genetics of hostpathogen interactions in the Pyrenophora teres f. teres (net form) – barley (Hordeum vulgare) pathosystem. Eur J Plant Pathol 117:267–280. https://doi.org/10.1007/s10658-006-9093-5

  • Amezrou R, Gyawali S, Belqadi L, Chao S, Arbaoui M, Mamidi S, Rehman S, Sreedasyam A, Verma RPS (2017) Molecular and phenotypic diversity of a worldwide ICARDA spring barley collection. Genetic resources and crop evolution. Genet Resour Crop Evol:1–15

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57(1):289–300

    Google Scholar 

  • Box GEP, Cox DR (1964) An analysis of transformations. J R Stat Soc B 26:211–252

    Google Scholar 

  • Bradbury PJ, 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 

  • Brown MP, Steffenson BJ, Webster RK (1993) Host range of Pyrenophora teres f. teres isolates from California. Plant Dis 77:942–974

    Article  Google Scholar 

  • Burlakoti RR, Gyawali S, Chao S, Smith KP, Horsley RD, Cooper B, Muehlbauer GJ, Neate SM (2016) Genome-wide association study of spot form of net blotch resistance in the Upper Midwest barley breeding programs. Phytopathology 107:100–108

    Article  PubMed  Google Scholar 

  • Cakir M, Gupta S, Platz GJ, Ablett GA, Loughman R, Embiri LC, Poulsen D, Li C, 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 

  • Cakir M, Gupta S, Li C, Hayden M, Mather DE, Ablett GA, Platz GJ, Broughton S, Chalmers KJ, Loughman R, Jones MGK, Lance RCM (2011) Genetic mapping and QTL analysis of disease resistance traits in the barley population Baudin x AC Metcalfe. Crop Pasture Sci 62:152–161

    Article  Google Scholar 

  • Caranta C, Lefebvre V, Palloix A (1997) Polygenic resistance of pepper to potyviruses consists of a combination of isolate-specific and broad-spectrum quantitative trait loci. Mol Plant-Microbe Interact 10:872–878

    Article  CAS  Google Scholar 

  • Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4(2):359–361

    Article  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(1):49–56

    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 

  • Eyal Z, Scharen AL, Prescott JM, Van Ginkel M (1987) The Septoria diseases of wheat: concepts and methods of disease management. CIMMYT, Mexico

    Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed  PubMed Central  CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578

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

    Article  CAS  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 CJ, Scoles GJ (2008) Mapping quantitative trait loci associated with barley net blotch resistance. Theor Appl Genet 116:529–539

    Article  PubMed  CAS  Google Scholar 

  • Hickey LT, Lawson W, Platz GJ, Dieters M, Arief VN, German S, Fletcher S, Park RF, Singh D, Pereyra S, Franckowiak J (2011) Mapping Rph20: a gene conferring adult plant resistance to Puccinia hordei in barley. Theor Appl Genet 123:55–68

    Article  PubMed  CAS  Google Scholar 

  • Hickey LT, Lawson W, Platz GJ, Fowler RA, Arief V, Dieters M, German S, Fletcher S, Park RF, Singh D, Pereyra S, Franckowiak J (2012) Mapping quantitative trait loci for partial resistance to powdery mildew in an Australian barley population. Crop Sci 52:1021–1032

    Article  Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332

    Article  PubMed  PubMed Central  Google Scholar 

  • Jalli M, Robinson J (1999) 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 

  • Jordan VW, Allen E (1984) Barley net blotch: influence of straw disposal and cultivation methods on inoculum potential, and on incidence and severity of autumn disease. Plant Pathol 33:547–559

    Article  Google Scholar 

  • Koladia VM, Faris JD, Richards JK, Brueggeman RS, Chao S, Friesen TL (2016) 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(1):163–173

    Article  PubMed  CAS  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 Breeding 32:641–650. https://doi.org/10.1007/s11032-013-9897-x

    Article  CAS  Google Scholar 

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

  • Li ZK, Arif M, Zhong DB, Fu BY, Xu JL, Domingo-Rey J, Ali J, Vijayakumar CHM, Yu SB, Khush GS (2006) Complex genetic networks underlying the defensive system of rice (Oryza sativa L.) to Xanthomonas oryzae pv. oryzae. Proc Natl Acad Sci 103:7994–7999

    Article  PubMed  PubMed Central  CAS  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):1–19

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  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  PubMed  CAS  Google Scholar 

  • Marcel TC, Gorguet B, Ta MT, Kohutova Z, Vels A, Niks RE (2008) Isolate specificity of quantitative trait loci for partial resistance of barley to Puccinia hordei conformed in mapping populations of near-isogenic lines. New Phytol 177:743–755

    Article  PubMed  Google Scholar 

  • Mascher M, Muehlbauer GJ, Rokhsar DS, Chapman J, Schmutz J, Barry K, Marıa M-A, 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. https://doi.org/10.1111/tpj.12319

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mathre DE (1997) Compendium of barley diseases, 2nd edn. The American Phytopathological Society. APS Press, St. Paul

    Google Scholar 

  • McLean MS, Howlett BJ, Turkington TK, Platz GJ, Hollaway GJ (2012) Spot form of net blotch resistance in a diverse set of barley lines in Australia and Canada. Plant Dis 96:569–576

    Article  Google Scholar 

  • McLean MS, Weppler R, Howlett BJ, Hollaway GJ (2016) Spot form of net blotch suppression and yield of barley in response to fungicide application in the Wimmera region of Victoria, Australia. Australas Plant Pathol 45(1):37–43

    Article  CAS  Google Scholar 

  • Munoz-Amatriain M, Cuesta-Marcos A, Endelman JB, Comadran J, Bonman JM et al (2014) The USDA barley core collection: genetic diversity, population structure, and potential for genome-wide association studies. PLoS One 9(4):e94688. https://doi.org/10.1371/journal.pone.0094688

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Myles S, Peiffer J, Brown PJ, Ersoz ES, Zhang Z, Costish DE, Buckler ES (2009) Association mapping: critical consideration shift from genotyping to experimental design. Plant Cell 21:2194–2202

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Patterson N, Price AL, Reich D (2006) Population structure and eigenanalysis. PLoS Genet 2:e190

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    PubMed  PubMed Central  CAS  Google Scholar 

  • Payne RW (2013) The Guide to the GenStat ® Command Language (Release 16). Part 2: statistics. Lawes Agricultural Trust, Rothamsted Experimental Station, Harpenden

    Google Scholar 

  • Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ (2008) Shades of gray: the world of quantitative disease resistance. Trends Plant Sci 14:21–29

    Article  PubMed  CAS  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 

  • Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt WR, Doebley J, Kresovich S, Goodman MM, Buckler ES (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. PNAS 98(20):1479–11484

    Article  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(5):915–927

    Article  PubMed  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(8):1225–1234

    Article  CAS  Google Scholar 

  • Robinson J, Jalli M (1996) Diversity among Finnish net blotch isolates and resistance in barley. Euphytica 92:81–87

    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  PubMed Central  Google Scholar 

  • Saari EE, Prescott JM (1975) A scale for appraising the foliar intensity of wheat disease. Plant Dis Reporter 59:377–380

    Google Scholar 

  • Sharma RC, Duveiller E (2006) Spot blotch continues to cause substantial grain yield reductions under resource-limited farming conditions. J Phytopathol 154:482–488

  • Shipton WA, Khan TN, Boyd WJR (1973) Net blotch of barley. Rev Plant Pathol 52:269–290

    Google Scholar 

  • Slotta TAB, Brady L, Chao S (2008) High throughput tissue preparation for large-scale genotyping experiments. Mol Ecol Resour 8:83–87. https://doi.org/10.1111/j.1471-8286.2007.01907.x

    Article  PubMed  CAS  Google Scholar 

  • St. Clair DA (2010) Quantitative disease resistance and quantitative trait loci in breeding. Annu Rev Phytopathol 48:247–268

    Article  PubMed  CAS  Google Scholar 

  • St Pierre S, 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(1):80–84

    Article  PubMed  CAS  Google Scholar 

  • Steffenson BJ, Hayes HM, 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

    Article  PubMed  CAS  Google Scholar 

  • Steffenson B, Pederson J, Pederson V (1999) Common barley diseases in North Dakota. Extension Bulletin, NDSU Ext. Service

  • Tamang P, Neupane A, Mamidi S, Friesen T, Brueggeman R (2015) Association mapping of seedling resistance to spot form of net blotch in a worldwide collection of barley. Phytopathology 105:500–508

    Article  PubMed  CAS  Google Scholar 

  • Tekauz A (1985) A numerical scale to classify reactions of barley to Pyrenophora teres. Can J Plant Pathol 7(2):181–183

    Article  Google Scholar 

  • Wang X, Mace ES, Platz GJ, Hunt CH, Hickey LT, Franckowiak JD, Jordan DR (2014) Spot form of net blotch resistance in barley is under complex genetic control. Theor Appl Genet 128:489–499

    Article  CAS  Google Scholar 

  • Weir BS (1979) Inferences about linkage disequilibrium. Biometrics 35:235–254

    Article  PubMed  CAS  Google Scholar 

  • Wonneberger R, Ficke A, Lillemo M (2017a) Identification of quantitative trait loci associated with resistance to net form net blotch in a collection of Nordic barley germplasm. Theor Appl Genet:1–19

  • Wonneberger R, Ficke A, Lillemo M (2017b) Mapping of quantitative trait loci associated with resistance to net form net blotch (Pyrenophora teres f. teres) in a doubled haploid Norwegian barley population. PLoS ONE 12(4):e0175773 https://doi.org/10.1371

  • Young ND (1996) QTL mapping and quantitative disease resistance in plants. Annu Rev Phytopathol 34:479–501

    Article  PubMed  CAS  Google Scholar 

  • Youcef-Benkada M, Bendahmane BS, Sy AA, Barrault G, Albertini L (1994) Effects of inoculation of barley inflorescences with Drechslera teres upon location of seed-borne inoculum and its transmission of seedlings as modified by temperature and soil moisture. Plant Pathol 43:350–355

    Article  Google Scholar 

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

  • Yun SJ, Gyenis L, Hayes PM, Matus I, Smith KP, Steffenson BJ, Muehlbauer GJ (2005) Quantitative trait loci for multiple disease resistance in wild barley. Crop Sci 45(6):2563–2572

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Zhao HH, Fernando RL, Dkeers JCM (2007) Power and precision of alternate methods for linkage disequilibrium mapping of quantitative trait loci. Genetics 175:1975–1986

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ziems L, Hickey L, Hunt C, Mace E, Platz GJ, Franckowiak J, Jordan D (2014) Association mapping of resistance to Puccinia hordei in Australia barley breeding germplasm. Theor Appl Genet 127:1199–1212

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This study was undertaken as part of the CGIAR Research Program on Dryland Cereals (CRP-DC). The financial supports from CRP-DC and USAID-CGIAR Linkage program are highly acknowledged.

Author information

Authors and Affiliations

  1. BIGM Program, International Center for Agricultural Research in the Dry Areas (ICARDA), Rabat, Morocco

    Reda Amezrou, Ramesh Pal Singh Verma, Sajid Rehman & Sanjaya Gyawali

  2. USDA-ARS, Fargo, ND, USA

    Shiaoman Chao

  3. Dept. Plant Pathology, North Dakota State University, Fargo, ND, USA

    Robert S. Brueggeman

  4. Dept. Plant Breeding and Genetics, IAV Hassan II, Rabat, Morocco

    Loubna Belqadi & Mustapha Arbaoui

  5. University of Manitoba, 222-Agriculture Building, Dafoe Road, Winnipeg, MB, Canada

    Sanjaya Gyawali

Authors
  1. Reda Amezrou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ramesh Pal Singh Verma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shiaoman Chao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Robert S. Brueggeman
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Loubna Belqadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mustapha Arbaoui
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sajid Rehman
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sanjaya Gyawali
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sanjaya Gyawali.

Electronic supplementary material

ESM 1

(XLSX 55 kb)

ESM 2

(DOCX 214 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Amezrou, R., Verma, R.P.S., Chao, S. et al. Genome-wide association studies of net form of net blotch resistance at seedling and adult plant stages in spring barley collection. Mol Breeding 38, 58 (2018). https://doi.org/10.1007/s11032-018-0813-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11032-018-0813-2

Keywords

Search

Navigation