Skip to main content
SpringerLink
Log in

A GWAS to identify the cereal cyst nematode (Heterodera filipjevi) resistance loci in diverse wheat prebreeding lines

  • Plant Genetics • Short Communication
  • Published:
Journal of Applied Genetics Aims and scope Submit manuscript

Abstract

Yield losses because of cereal cyst nematodes could be as high as 92%, causing a bottleneck for wheat production. An integrated approach (application of pesticides, crop rotation, and use of host resistance) is needed to manage this devastating pathogen where resistant cultivars are considered most effective. This necessitates the identification of nematode-resistant sources in the available germplasm. Here, we report on the genetic mapping of nematode resistance in 255 diverse prebreeding lines (PBLs) employing an association mapping strategy. Altogether, seven additive quantitative trait loci (QTL) were identified on chromosomes 1A, 2A, 2B, 2D, 3A, 6B, and 6D explaining a maximum of 9.42% phenotypic variation where at least five QTL (on chromosomes 2A, 2B, 2D, 6B, and 6D) are located on the same chromosomes that harbor the already known nematode resistance genes. Resistant PBLs carried Aegilops squarrosa (436) in their pedigree which could be the possible source of positive alleles. To add to it, better yield performance of the identified nematode-resistant lines under stress conditions indicates that the germplasm can provide both nematode resistance and high-yielding cultivars.

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

References

  • Ali MA, Shahzadi M, Zahoor A, Dababat AA, Toktay H, Bakhsh A, Nawaz MA, Li H (2019) Resistance to cereal cyst nematodes in wheat and barley: an emphasis on classical and modern approaches. Int. J. Mol. Sci. 20:432. https://doi.org/10.3390/ijms20020432

    Article  CAS  PubMed Central  Google Scholar 

  • Akram S, Rehman-Arif MA, Hameed A (2020) A GBS-based GWAS analysis of adaptability and yield traits in bread wheat (Triticum aestivum L.). J Appl Genet:1–15. https://doi.org/10.1007/s13353-020-00593-1

  • Bakker E, Dees R, Bakker J, Goverse A (2006) Mechanisms involved in plant resistance to nematodes. In: Sadik T, Elizabeth B (eds) Multigenic and induced systemic resistance in plants. Springer, pp 314–334

  • 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

  • Brown J, Ellis S (1976) Breeding for resistance to cereal cyst nematode in wheat. Euphytica 25:73–82

    Article  Google Scholar 

  • Cui L, Qiu D, Sun L, Sun Y, Ren Y, Zhang H, Li J, Zou J, Wu P, Hu J (2020) Resistance to Heterodera filipjevi and H. avenae in winter wheat is conferred by different QTL. Phytopathol 110:472–482

    Article  CAS  Google Scholar 

  • Curtis T, Halford N (2014) Food security: the challenge of increasing wheat yield and the importance of not compromising food safety. Ann Appl Biol 164:354–372

    Article  CAS  Google Scholar 

  • Dababat A, Pariyar S, Nicol J, Erginbas-Orakci G, Goll M, Watrin C, Duveiller E, Braun H, Cabrera J, Sikora R (2014) Influence of thiabendazole seed treatment on the integrated control of Heterodera filipjevi on six wheat genotypes with different levels of genetic resistance under controlled conditions. Nematropica 44:25–30

    Google Scholar 

  • Dababat AA, Imren M, Erginbas-Orakci G, Ashrafi S, Yavuzaslanoglu E, Toktay H, Pariyar SR, Elekcioglu HI, Morgounov A, Mekete T (2015) The importance and management strategies of cereal cyst nematodes, Heterodera spp., in Turkey. Euphytica 202:173–188

    Article  Google Scholar 

  • Dababat AA, Fourie H (2018) Nematode parasites of cereals. In: Sikora RA, Coyne D, Hallmann J, Timper P (eds) Plant parasitic nematodes in subtropical and tropical agriculture. CAB International, Wallingford, UK, pp. 163–221

  • 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  Google Scholar 

  • Eastwood R, Lagudah E, 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  CAS  Google Scholar 

  • FAO (2019). Food and Agriculture Organization of the United Nations. Rome, Italy. Available online. http://www.fao.org/worldfoodsituation/csdb/en/. Accessed 21 Sept 2020

  • Imren M, Yildiz Ş, Kasapoğlu E, Toktay H, Kütük H, Dababat, AA (2015) The plant-parasitic nematodes associated with cereal crops in Bolu, Turkey. In: Proceedings of the Fifth International Cereal Nematode Initiative Workshop, 12–15 September, 2015, Ankara, Turkey, pp. 131–141

  • Jahier J, Abelard P, Tanguy M, Dedryver F, Rivoal R, Khatkar S, Bariana H, Koebner R (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 

  • Jayatilake DV, Tucker EJ, Brueggemann J, Lewis J, Garcia M, Dreisigacker S, Hayden MJ, Chalmers K, Mather DE (2015) Genetic mapping of the Cre8 locus for resistance against cereal cyst nematode (Heterodera avenae Woll.) in wheat. Mol Breed 35:66–78

    Article  Google Scholar 

  • Karimipour Fard H, Pourjam E, Tanha Maafi Z, Safaie N (2018) Assessment of yield loss of wheat cultivars caused by Heterodera filipjevi under field conditions. J Phytopathol 166:299–304

    Article  CAS  Google Scholar 

  • Kimber, G, Feldman, M. (1987) Wild wheat. An introduction. pp. 1–142. Special Report 353, College of Agriculture, Univ. of Missouri, Columbia, USA

  • Kyndt T, Goverse A, Haegeman A, Warmerdam S, Wanjau C, Jahani M, Engler G, de Almeida EJ, Gheysen G (2016) Redirection of auxin flow in Arabidopsis thaliana roots after infection by root-knot nematodes. J. Exp. Bot. 67:4559–4570

    Article  CAS  Google Scholar 

  • Nicol JM, Rivoal R, Trethowan RM, Van Ginkel M, Mergoum M, Singh RP (2001) CIMMYT’s approach to identify and use resistance to nematodes and soil-borne fungi, in developing superior wheat germplasm. In: Bedo Z, Lang L (eds) Wheat in a global environment. Kluwer Academic Publishers the Netherlands, Dordrecht, pp 381–389

    Chapter  Google Scholar 

  • Ogbonnaya F, Seah S, Delibes A, Jahier J, Lopez-Brana I, Eastwood R, Lagudah E (2001) Molecular-genetic characterisation of a new nematode resistance gene in wheat. Theor. Appl. Genet. 102:623–629

    Article  CAS  Google Scholar 

  • Pariyar SR, Dababat AA, Sannemann W, Erginbas-Orakci G, Elashry A, Siddique S, Morgounov A, Leon J, Grundler FM (2016a) Genome-wide association study in wheat identifies resistance to the cereal cyst nematode Heterodera filipjevi. Phytopathol 106:1128–1138

    Article  CAS  Google Scholar 

  • Pariyar SR, Dababat AA, Siddique S, Erginbas-Orakci G, Elashry A, Morgounov A, Grundler FM (2016b) Identification and characterisation of resistance to the cereal cyst nematode Heterodera filipjevi in winter wheat. Nematol 18:377–402

    Article  Google Scholar 

  • Ray DK, Mueller ND, West PC, Foley JA (2013) Yield trends are insufficient to double global crop production by 2050. PLoS One 8(6):e66428. https://doi.org/10.1371/journal.pone.0066428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rehman-Arif MA, Börner A (2020) An SNP based GWAS analysis of seed longevity in wheat. Cereal Res Commun 48:149–156

    Article  Google Scholar 

  • Riley IT, McKay AC (2009) Cereal cyst nematode in Australia: biography of a biological invader. In: Riley IT, Nicol JM, Dababat AA (eds) Cereal cyst nematodes: status, research and outlook. CIMMYT, Ankara, pp 23–28

    Google Scholar 

  • Safari E, Gororo N, Eastwood R, Lewis J, Eagles H, Ogbonnaya F (2005) Impact of Cre1, Cre8 and Cre3 genes on cereal cyst nematode resistance in wheat. Theor. Appl. Genet. 110:567–572

    Article  CAS  Google Scholar 

  • Sasser JN, Freckman DW (1987) A world perspective on nematology: the role of the society. Vistas on Nematology. (Veech JA, Dickson DW eds), pp 7-14. Society of Nematologists

  • Shiferaw B, Smale M, Braun HJ, Duveiller E, Reynolds M, Muricho G (2013) Crops that feed the world 10. Past successes and future challenges to the role played by wheat in global food security. Food Sec 5:291–317

    Article  Google Scholar 

  • Singh S et al (2018) Harnessing genetic potential of wheat germplasm banks through impact-oriented-prebreeding for future food and nutritional security. Sci. Rep. 8:12527

    Article  Google Scholar 

  • Singh S, Sehgal D, Kumar S, Rehman-Arif MA, Vikram P, Sansaloni C, Fuentes-Dávila G, Ortiz C (2020) GWAS revealed a novel resistance locus on chromosome 4D for the quarantine disease Karnal bunt in diverse wheat pre-breeding germplasm. Sci. Rep. 10:1–11

    Article  CAS  Google Scholar 

  • Smiley RW, Nicol JM (2009) Nematodes which challenge global wheat production. In: Carver BF (ed) Wheat science and trade. Wiley-Blackwell, Ames, pp 171–187

    Chapter  Google Scholar 

  • Smiley RW, Dababat AA, Iqbal S, Jones MG, Maafi ZT, Peng D et al (2017) Cereal cyst nematodes: a complex and destructive group of Heterodera species. Plant Dis 101:1692–1720. https://doi.org/10.1094/PDIS-03-17-0355-FE

    Article  CAS  PubMed  Google Scholar 

  • Taylor C, Shepherd K, Langridge P (1998) A molecular genetic map of the long arm of chromosome 6R of rye incorporating the cereal cyst nematode resistance gene, CreR. Theor. Appl. Genet. 97:1000–1012

    Article  CAS  Google Scholar 

  • 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

  • Wilson R, Hollamby G, Bayraktar A (1983) Selecting for high yield potential in wheat with tolerance to cereal cyst nematode. Aust Field Crops Newsl 18:21–25

    Google Scholar 

  • Zhai X, Zhao T, Liu Y, Long H, Deng G, Pan Z, Yu M (2008) Characterization and expression profiling of a novel cereal cyst nematode resistance gene analog in wheat. Mol. Biol. 42:960–965

    Article  CAS  Google Scholar 

  • Zhang R, Feng Y, Li H, Yuan H, Dai J, Cao A, Xing L, Li H (2016) Cereal cyst nematode resistance gene CreV effective against Heterodera filipjevi transferred from chromosome 6VL of Dasypyrum villosum to bread wheat. Mol Breed 36:122–133

    Article  Google Scholar 

Download references

Author information

Author notes

  1. Abdelfattah Dababat and Mian Abdur Rehman Arif contributed equally to this work.

Authors and Affiliations

  1. International Maize and Wheat Improvement Centre, Turkey Office P.K. 39 Emek, 06511, Ankara, Turkey

    Abdelfattah Dababat & Gul E-Orakci

  2. Nuclear Institute for Agriculture and Biology, Faisalabad, 38000, Pakistan

    Mian Abdur Rehman Arif & Sajid Shokat

  3. Faculty of Agricultural Sciences and Technologies, Niğde Ömer Halisdemir University, Niğde, Turkey

    Halil Toktay & Osameh Atiya

  4. Faculty of Agriculture, Bolu Abant Izzet Baysal University, Bolu, Turkey

    Mustafa Imren

  5. Geneshifters, 222 Mary Jena Lane, Pullman, WA, 99163, USA

    Sukhwinder Singh

Authors
  1. Abdelfattah Dababat
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mian Abdur Rehman Arif
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Halil Toktay
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Osameh Atiya
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sajid Shokat
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gul E-Orakci
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mustafa Imren
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sukhwinder Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Abdelfattah Dababat and Sukhwinder Singh conceived the idea and designed the study. Halil Toktay, Osameh Atiya, Gul E-Orakci, and Mustafa Imren performed the experiments. Mian Abdur Rehman Arif and Sajid Shokat performed the analysis. Mian Abdur Rehman Arif wrote the manuscript. Abdelfattah Dababat reviewed the manuscript.

Corresponding author

Correspondence to Sukhwinder Singh.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with animals or humans performed by any of the authors.

Additional information

Communicated by: Izabela Pawłowicz

Publisher’s note

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

Supplementary information

ESM 1

(DOCX 124 kb)

Table S1

(DOCX 45 kb)

Table S2

(DOCX 16 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dababat, A., Arif, M.A.R., Toktay, H. et al. A GWAS to identify the cereal cyst nematode (Heterodera filipjevi) resistance loci in diverse wheat prebreeding lines. J Appl Genetics 62, 93–98 (2021). https://doi.org/10.1007/s13353-020-00607-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13353-020-00607-y

Keywords

Search

Navigation