Skip to main content
SpringerLink
Log in

GWAS scans of cereal cyst nematode (Heterodera avenae) resistance in Indian wheat germplasm

  • Original Article
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Significant yield losses in major cereal-growing regions around the world have been linked to cereal cyst nematodes (Heterodera spp.). Identifying and deploying natural sources of resistance is of utmost importance due to increasing concerns associated with chemical methods over the years. We screened 141 diverse wheat genotypes collected from pan-Indian wheat cultivation states for nematode resistance over two years, alongside two resistant (Raj MR1, W7984 (M6)) and two susceptible (WH147, Opata M85) checks. We performed genome-wide association analysis using four single-locus models (GLM, MLM, CMLM, and ECMLM) and three multi-locus models (Blink, FarmCPU, and MLMM). Single locus models identified nine significant MTAs (−log10 (P) > 3.0) on chromosomes 2A, 3B, and 4B whereas, multi-locus models identified 11 significant MTAs on chromosomes 1B, 2A, 3B, 3D and 4B. Single and multi-locus models identified nine common significant MTAs. Candidate gene analysis identified 33 genes like F-box-like domain superfamily, Cytochrome P450 superfamily, Leucine-rich repeat, cysteine-containing subtype Zinc finger RING/FYVE/PHD-type, etc., having a putative role in disease resistance. Such genetic resources can help to reduce the impact of this disease on wheat production. Additionally, these results can be used to design new strategies for controlling the spread of H. avenae, such as the development of resistant varieties or the use of resistant cultivars. Finally, the obtained results can also be used to identify new sources of resistance to this pathogen and develop novel control methods.

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

Data availability

The plant material and genotyping data used in the current study was obtained from Dr. Sundeep Kumar (Co-author) from NBPGR, New Delhi. The phenotyping datasets generated and analyzed during the current investigation is accessible in the supplemental information. The genotyping data is available, on reasonable request, from Dr. Sundeep Kumar.

References

  • Aditya J, Lewis J, Shirley NJ, Tan HT, Henderson M, Fincher GB, Burton RA, Mather DE, Tucker MR (2015) The dynamics of cereal cyst nematode infection differ between susceptible and resistant barley cultivars and lead to changes in (1, 3; 1, 4)-β-glucan levels and HvCslF gene transcript abundance. New Phytol 207:135–147. https://doi.org/10.1111/nph.1334910.1111/nph.13349

    Article  CAS  PubMed  Google Scholar 

  • Al-Ateeq TK, Al-Doss AA, Al-Hazmi AS, Ghazy AI, Dawabah AM, Motawei MI (2021) Molecular mapping of a novel QTL for resistance to cereal cyst nematode in F4 wheat population. Cereal Res Commun 24:1–7. https://doi.org/10.1007/s42976-021-00159-9

    Article  CAS  Google Scholar 

  • Allard RW (1999) Principles of plant breeding. John Wiley & Sons

    Google Scholar 

  • Allen AM, Winfield MO, Burridge AJ, Downie RC, Benbow HR, Barker GL, Wilkinson PA, Coghill J, Waterfall C, Davassi A, Scopes G (2017) Characterization of a wheat breeders’ array suitable for high-throughput SNP genotyping of global accessions of hexaploid bread wheat (Triticum aestivum). Plant Biotechnol J 15:390–401. https://doi.org/10.1111/pbi.1263510.1111/pbi.12635

    Article  CAS  PubMed  Google Scholar 

  • Alvarado G, López M, Vargas M, Pacheco A, Rodríguez F, Burgueño J, Crossa J (2017) META-R (Multi Environment Trial Analysis with R for Windows) Version 6.01. hdl: 11529/10201. CIMMYT Research Data Software Repository Network

  • Appels R, Eversole K, Feuille C, Keller B, Rogers J, Stein N (2018) The International Wheat Genome Sequencing Consortium (IWGSC). Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361:10–126. https://doi.org/10.1126/science.aar7191

    Article  CAS  Google Scholar 

  • Barker KR, Pederson GA, Windham GL (1998) Plant and nematode interactions. Agronomy Monograph 36. American Society of Agronomy, Madison

  • Bar-Or C, Kapulnik Y, Koltai H (2005) A broad characterization of the transcriptional profile of the compatible tomato response to the plant parasitic root knot nematode Meloidogyne javanica. Eur J Plant Pathol 111(2):181–192

    Article  CAS  Google Scholar 

  • Borrill P, Ramirez-Gonzalez R, Uauy C (2016) expVIP: a customizable RNA-seq data analysis and visualization platform. Plant Physiol 170:2172–2186. https://doi.org/10.1104/pp.15.01667

    Article  CAS  PubMed  PubMed Central  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. Bioinfo 23:2633–2635

    Article  CAS  Google Scholar 

  • Breseghello F, Sorrells ME (2006) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172:1165–1177. https://doi.org/10.1534/genetics.105.044586

    Article  PubMed  PubMed Central  Google Scholar 

  • Brown JAM, Ellis SE (1976) Breeding for resistance to cereal cyst nematode in wheat. Euphytica 25:73–82. https://doi.org/10.1007/BF00041530

    Article  Google Scholar 

  • Chen J, Zhang F, Zhao C, Lv G, Sun C, Pan Y, Guo X, Chen F (2019) Genome-wide association study of six quality traits reveals the association of the TaRPP13L1 gene with flour colour in Chinese bread wheat. Plant Biotechnol J 17:2106–2122. https://doi.org/10.1111/pbi.13126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cobb NA (1918) Estimating the nema population of soil, with special references to the sugarbeet and root-gall nemas, Heterodera schachtii Schmidt and Heterodera radicicola (Greef) Muller, and with a description of Tylencholaimus aequalis n. sp. Agric Tech Circular 1:48

    Google Scholar 

  • Comstock RE, Robinson HF (1952) Estimation of average dominance of genes. Heterosis 2:494–516

    Google Scholar 

  • Cui L, Qiu D, Sun L, Sun Y, Ren Y, Zhang H, Li J, Zou J, Wu P, Hu J, Xie J, Liu H, Yang L, Zhou Y, Wang Y, Lv Y, Liu Z, Murray TD, Li H (2020) Resistance to Heterodera filipjevi and H. avenae in winter wheat is conferred by different QTL. Phytopathology 110:472–482. https://doi.org/10.1094/PHYTO-04-19-0135-R

    Article  CAS  PubMed  Google Scholar 

  • Dababat AA, Ferney GBH, Erginbas-Orakci G, Dreisigacker S, Imren M, Toktay H, Elekcioglu HI, Mekete T, Nicol JM, Ansari O, Ogbonnaya F (2016) Association analysis of resistance to cereal cyst nematodes (Heterodera avenae) and root lesion nematodes (Pratylenchus neglectus and P. thornei) in CIMMYT advanced spring wheat lines for semi-arid conditions. Breed Sci. https://doi.org/10.1270/jsbbs.15158

    Article  PubMed  PubMed Central  Google Scholar 

  • Dababat A, Arif MAR, Toktay H, Atiya O, Shokat S, Gul E, Imren M, Singh S (2021) A GWAS to identify the cereal cyst nematode (Heterodera filipjevi) resistance loci in diverse wheat prebreeding lines. J Appl Genet 62:93–98. https://doi.org/10.1007/s13353-020-00607-y

    Article  CAS  PubMed  Google Scholar 

  • Dutta TK, Khan MR, Phani V (2019) Plant-parasitic nematode management via biofumigation using brassica and non-brassica plants: current status and future prospects. Curr Plant Biol 17:17–32

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

    Article  CAS  PubMed  Google Scholar 

  • Fu L, Wu J, Yang S, Jin Y, Liu J, Yang M, Rasheed A, Zhang Y, Xia X, Jing R, He Z (2020) Genome-wide association analysis of stem water-soluble carbohydrate content in bread wheat. Theor Appl Genet 133:2897–2914. https://doi.org/10.1007/s00122-020-03640-x

    Article  CAS  PubMed  Google Scholar 

  • Fu T, Han JH, Shin JH, Song H, Ko J, Lee YH, Kim KT, Kim KS (2021) Homeobox transcription factors are required for fungal development and the suppression of host defense mechanisms in the Colletotrichum scovillei-pepper pathosystem. Mbio 12:01620–01621. https://doi.org/10.1128/mBio.01620-21

    Article  Google Scholar 

  • GRDC (2017) Rotations and resistant varieties vital for controlling cereal cyst nematode (CCN). Tips and Tactics: Cereal Cyst Nematode. https://grdc.com.au/TT-cereal-cyst-nematode

  • Guerra FP, Yáñez A, Matus I, Del Pozo A (2021) Genome-wide association of stem carbohydrate accumulation and remobilization during grain growth in bread wheat (Triticum aestivum L.) in Mediterranean environments. Plants 10:539. https://doi.org/10.3390/plants10030539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta SK, Rai AK, Kanwar SS, Sharma TR (2012) Comparative analysis of zinc finger proteins involved in plant disease resistance. PLoS ONE 7:42578. https://doi.org/10.1371/journal.pone.0042578

    Article  CAS  Google Scholar 

  • He Y, Ahmad D, Zhang X, Zhang Y, Wu L, Jiang P, Ma H (2018) Genome-wide analysis of family-1 UDP glycosyltransferases (UGT) and identification of UGT genes for FHB resistance in wheat (Triticum aestivum L.). BMC Plant Biol 18:1–20. https://doi.org/10.1186/s12870-018-1286-5

    Article  CAS  Google Scholar 

  • İmren M, YILDIZ Ş, Çiftçi V, Dababat A (2020) Effect of cereal cyst nematode Heterodera filipjevi on wheat yields in Turkey. Turk J Agric For 1:39-45

  • Jahier J, Tanguy AM, Abelard P, Rivoal R (1996) Utilization of deletions to localize a gene for resistance to the cereal cyst nematode, Heterodera avenue, on an Aegilops ventricosa chromosome. Plant Breed 115:282–284. https://doi.org/10.1111/j.1439-0523.1996.tb00919.x

    Article  Google Scholar 

  • Jahier J, Abelard P, Tanguy M, Dedryver F, Rivoal R, Khatkar S, Bariana HS, 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. https://doi.org/10.1046/j.1439-0523.2001.00585.x

    Article  CAS  Google Scholar 

  • Jamil M, Ali A, Gul A, Ghafoor A, Napar AA, Ibrahim AM, Naveed NH, Yasin NA, Mujeeb-Kazi A (2019) Genome-wide association studies of seven agronomic traits under two sowing conditions in bread wheat. BMC Plant Biol 19:1–8. https://doi.org/10.1186/s12870-019-1754-6

    Article  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 35:1–2

    Article  CAS  Google Scholar 

  • Kanwar RS, Nandal SN, Paruthi IJ, Bajaj HK (2011) Status of Heterodera avenae Woll. and losses caused by it in wheat in Haryana state of India. HAU J Agric Res 41:21–23

  • 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 5:299–304

  • Kidane YG, Gesesse CA, Hailemariam BN, Desta EA, Mengistu DK, Fadda C, Pè ME, Dell’Acqua M (2019) A large nested association mapping population for breeding and quantitative trait locus mapping in Ethiopian durum wheat. Plant Biotechnol J 17:1380–1393. https://doi.org/10.1111/pbi.13062

    Article  PubMed  PubMed Central  Google Scholar 

  • Kumar D, Sharma S, Sharma R, Pundir S, Singh VK, Chaturvedi D, Singh B, Kumar S, Sharma S (2021) Genome-wide association study in hexaploid wheat identifies novel genomic regions associated with resistance to root lesion nematode (Pratylenchus thornei). Sci Rep 11:1–4. https://doi.org/10.1038/s41598-021-80996-0

    Article  CAS  Google Scholar 

  • Letunic I, Bork P (2007) Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 1:127–128. https://doi.org/10.1093/bioinformatics/btl529

    Article  CAS  Google Scholar 

  • Li F, Wen W, Liu J, Zhang Y, Cao S, He Z, Rasheed A, Jin H, Zhang C, Yan J, Zhang P (2019) Genetic architecture of grain yield in bread wheat based on genome-wide association studies. BMC Plant Biol 19:1–9. https://doi.org/10.1186/s12870-019-1781-3

    Article  Google Scholar 

  • Linsell KJ, Rahman MS, Taylor JD, Davey RS, Gogel BJ, Wallwork H, Forrest KL, Hayden MJ, Taylor SP, Oldach KH (2014) QTL for resistance to root lesion nematode (Pratylenchus thornei) from a synthetic hexaploid wheat source. Theor Appl Genet 127:1409–1421. https://doi.org/10.1007/s00122-014-2308-9

    Article  CAS  PubMed  Google Scholar 

  • Lipka AE, Tian F, Wang Q, Peiffer J, Li M, Bradbury PJ, Gore MA, Buckler ES, Zhang Z (2012) GAPIT: genome association and prediction integrated tool. Bioinformatics 28:2397–2399. https://doi.org/10.1093/bioinformatics/bts444

    Article  CAS  PubMed  Google Scholar 

  • Luján Basile SM, Ramírez IA, Crescente JM, Conde MB, Demichelis M, Abbate P, Rogers WJ, Pontaroli AC, Helguera M, Vanzetti LS (2019) Haplotype block analysis of an Argentinean hexaploid wheat collection and GWAS for yield components and adaptation. BMC Plant Biol 19:1–6. https://doi.org/10.1186/s12870-019-2015-4

    Article  CAS  Google Scholar 

  • McDonald AH, Nicol JM (2005) Nematode parasites of cereals. In: Luc M, Sikora RA, Bridge J (eds) Plant parasitic nematodes in subtropical and tropical agriculture, vol 2. CABI, England, pp 131–191. https://doi.org/10.1079/9780851997278.0131

    Chapter  Google Scholar 

  • Meagher JW, Brown RH, Rovira AD (1978) The effects of cereal cyst nematode (Heterodera avenae) and Rhizoctonia solani on the growth and yield of wheat. Aust J Agric Res 29:1127–1137. https://doi.org/10.1071/AR9781127

    Article  CAS  Google Scholar 

  • Moustafa KA, Al-Doss AA, Motawei MI, Al-Otayk S, Dawabah AA, Abdel-Mawgood AL, Al-Rehiayani SM, Al-Hazmi AS (2015) Selection of spring bread wheat genotypes for resistance to cereal cyst nematode (‘Heterodera avenae’ Woll.) based on field performance and molecular markers. Plant Omics 8:392–397. https://doi.org/10.3316/informit.514851759251055

    Article  CAS  Google Scholar 

  • Mulki MA, Jighly A, Ye G, Emebiri LC, Moody D, Ansari O, Ogbonnaya FC (2013) Association mapping for soilborne pathogen resistance in synthetic hexaploid wheat. Mol Breed 31:299–311. https://doi.org/10.1007/s11032-012-9790-z

    Article  CAS  Google Scholar 

  • N’Diaye A, Haile JK, Cory AT, Clarke FR, Clarke JM, Knox RE, Pozniak CJ (2017) Single marker and haplotype-based association analysis of semolina and pasta colour in elite durum wheat breeding lines using a high-density consensus map. PLoS ONE 12:0170941

    Google Scholar 

  • Nicol JM (2002) Important nematode pests. In: Bread wheat: improvement and production. FAO plant production and protection series, Rome, pp 345–366

  • Nicol JM, Rivoal R (2008) Global knowledge and its application for the integrated control and management of nematodes on wheat. In: Ciancio A, Mukerji KG (eds) Integrated management and biocontrol of vegetable and grain crops nematodes. Springer, Dordrecht, pp 251–294. https://doi.org/10.1007/978-1-4020-6063-2_13

    Chapter  Google Scholar 

  • Nicol JM, Turner SJ, Coyne DL, Nijs LD, Hockland S, Maafi ZT (2011) Current nematode threats to world agriculture. In: Jones J, Gheysen G, Fenoll C (eds) Genomics and molecular genetics of plant–nematode interactions. Springer, Dordrecht, pp 21–43. https://doi.org/10.1007/978-94-007-0434-3_2

    Chapter  Google Scholar 

  • Ogbonnaya FC, Seah S, Delibes A, Jahier J, Lopez-Brana I, Eastwood RF, Lagudah ES (2001) Molecular-genetic characterisation of a new nematode resistance gene in wheat. Theor Appl Genet 102:623–629. https://doi.org/10.1007/s001220051689

    Article  CAS  Google Scholar 

  • Ogbonnaya FC, Rasheed A, Okechukwu EC, Jighly A, Makdis F, Wuletaw T, Hagras A, Uguru MI, Agbo CU (2017) Genome-wide association study for agronomic and physiological traits in spring wheat evaluated in a range of heat prone environments. Theor Appl Genet 130:1819–1835. https://doi.org/10.1007/s00122-017-2927-z

    Article  PubMed  Google Scholar 

  • Pang Y, Liu C, Wang D, Amand PS, Bernardo A, Li W, He F, Li L, Wang L, Yuan X, Dong L (2020) High-resolution genome-wide association study identifies genomic regions and candidate genes for important agronomic traits in wheat. Mol Plant 13:1311–1327. https://doi.org/10.1016/j.molp.2020.07.008

    Article  CAS  PubMed  Google Scholar 

  • Pariyar SR, Dababat AA, Sannemann W, Erginbas-Orakci G, Elashry A, Siddique S, Morgounov A, Leon J, Grundler FM (2016) Genome-wide association study in wheat identifies resistance to the cereal cyst nematode Heterodera filipjevi. Phytopathology 106:1128–1138. https://doi.org/10.1094/PHYTO-02-16-0054-FI

    Article  CAS  PubMed  Google Scholar 

  • Priyadharshini B, Vignesh M, Prakash M, Anandan R (2019) Comparison of methods for genomic deoxyribonucleic acid (DNA) extraction suitable for whole-genome genotyping in traditional varieties of rice. Agric Sci Digest A Res J 39:228–231. https://doi.org/10.18805/ag.D-4768

    Article  Google Scholar 

  • Pundir S, Sharma R, Kumar D, Singh VK, Chaturvedi D, Kanwar RS, Röder MS, Börner A, Ganal MW, Gupta PK, Sharma S (2022a) QTL mapping for resistance against cereal cyst nematode (Heterodera avenae Woll.) in wheat (Triticum aestivum L.). Sci Rep 12:1–14. https://doi.org/10.1038/s41598-022-12988-7

    Article  CAS  Google Scholar 

  • Pundir S, Singh VK, Kumar S, Chaturvedi D, Kumar D, Kanwar RS, Kumar A, Börner A, Sharma S, Sharma S (2022b) Validation of resistance to cereal cyst nematode (Heterodera avenae) and yield performance study in doubled haploid lines of wheat (Triticum aestivum L.). Genet Resour Crop Evol 14:1–7

    Google Scholar 

  • Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, De Bakker PI, Daly MJ, Sham PC (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559–575. https://doi.org/10.1086/519795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qian L, Hickey LT, Stahl A, Werner CR, Hayes B, Snowdon RJ, Voss-Fels KP (2017) Exploring and harnessing haplotype diversity to improve yield stability in crops. Front Plant Sci 8:1534

    Article  PubMed  PubMed Central  Google Scholar 

  • Rahman MS, Linsell KJ, Taylor JD, Hayden MJ, Collins NC, Oldach KH (2020) Fine mapping of root lesion nematode (Pratylenchus thornei) resistance loci on chromosomes 6D and 2B of wheat. Theor Appl Genet 133:635–652. https://doi.org/10.1007/s00122-019-03495-x

    Article  CAS  PubMed  Google Scholar 

  • Ramírez-González RH, Borrill P, Lang D, Harrington SA, Brinton J, Venturini L, Davey M, Jacobs J, Van Ex F, Pasha A, Khedikar Y (2018) The transcriptional landscape of polyploid wheat. Science 6403:6089. https://doi.org/10.1126/science.aar6089

    Article  CAS  Google Scholar 

  • Rivoal R, Dosba F, Jahier J, Pierre JS, Penard P, Tanguy AM, Abelard P, Querrien MT (1986) The wheat-Aegilops ventricosa Tausch addition lines. VI.—Study of the chromosomal localization of resistance to Heterodera avenae Woll. Agronomy 6:143–148

    Article  Google Scholar 

  • Robinson HF, Comstock RE, Harvey PH (1949) Estimate of heritability and degree of dominance in corn. Agron J 41:353–359. https://doi.org/10.2134/agronj1949.00021962004100080005x

    Article  Google Scholar 

  • Schaff JE, Nielsen DM, Smith CP, Scholl EH, Bird DM (2007) Comprehensive transcriptome profiling in tomato reveals a role for glycosyltransferase in Mi-mediated nematode resistance. Plant Physiol 144:1079–1092. https://doi.org/10.1104/pp.106.090241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma GL, Sharma SN (2000) Evaluation of cereal cyst nematode (Heterodera avenae) resistant wheat variety in Rajasthan, India. Wheat Info Serv 90:49–51

    Google Scholar 

  • Simbolo M, Gottardi M, Corbo V, Fassan M, Mafficini A, Malpeli G, Lawlor RT, Scarpa A (2013) DNA qualification workflow for next generation sequencing of histopathological samples. PLoS ONE 8:62692

    Article  Google Scholar 

  • Singh K, Chhuneja P, Singh I, Sharma SK, Garg T, Garg M, Keller B, Dhaliwal HS (2010) Molecular mapping of cereal cyst nematode resistance in Triticum monococcum L. and its transfer to the genetic background of cultivated wheat. Euphytica 176:213–222

    Article  CAS  Google Scholar 

  • Slootmaker LA, Lange W, Jochemsen G, Schepers J (1974) Monosomic analysis in bread wheat of resistance to cereal root eelworm. Euphytica 23:497–503. https://doi.org/10.1007/BF00022470

    Article  Google Scholar 

  • Smiley RW, Marshall JM (2016) Detection of dual Heterodera avenae resistance plus tolerance traits in spring wheat. Plant Dis 100:1677–1685. https://doi.org/10.1094/PDIS-09-15-1055-RE

    Article  PubMed  Google Scholar 

  • Team RC (2016) R: a language and environment for statistical computing [Computer software manual]. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Thompson JP, Brennan PS, Clewett TG, Sheedy JG, Seymour NP (1999) Progress in breeding wheat for tolerance and resistance to root-lesion nematode (Pratylenchus thornei). Australas Plant Pathol 28:45–52. https://doi.org/10.1071/AP99006

    Article  Google Scholar 

  • Toumi F, Waeyenberge L, Viaene N, Dababat AA, Nicol JM, Ogbonnaya F, Moens M (2018) Cereal cyst nematodes: importance, distribution, identification, quantification, and control. Eur J Plant Pathol 150:1–20. https://doi.org/10.1007/s10658-017-1263-0

    Article  Google Scholar 

  • Vanderplank JE (1966) Horizontal (polygenic) and vertical (oligogenic) resistance against blight. Am Potato J 43:43–52

    Article  Google Scholar 

  • Williams AM, Ward P, Chapman C (2003) Training perceptual skill in field hockey: is there transfer from the laboratory to the field? Res Q Exerc Sport 74:98–103. https://doi.org/10.1080/02701367.2003.10609068

    Article  PubMed  Google Scholar 

  • Williams KJ, Willsmore KL, Olson S, Matic M, Kuchel H (2006) Mapping of a novel QTL for resistance to cereal cyst nematode in wheat. Theor Appl Genet 112:1480–1486. https://doi.org/10.1007/s00122-006-0251-0

    Article  CAS  PubMed  Google Scholar 

  • Ye J, Zhang Y, Cui H, Liu J, Wu Y, Cheng Y, Xu H, Huang X, Li S, Zhou A, Zhang X (2018) WEGO 2.0: a web tool for analyzing and plotting GO annotations, 2018 update. Nucleic Acids Res 46:W71–W75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeb M, Shah MK, Faryal R (2013) Development of putative molecular markers to trace durable rust resistance genes in wheat breeding stocks. Pak J Bot 45:359–366

    CAS  Google Scholar 

  • Zwart RS, Thompson JP, Sheedy JG, Nelson JC (2006) Mapping quantitative trait loci for resistance to Pratylenchus thornei from synthetic hexaploid wheat in the International Triticeae Mapping Initiative (ITMI) population. Aust J Agric Res 57:525–530. https://doi.org/10.1071/AR05177

    Article  Google Scholar 

Download references

Acknowledgements

Thanks are due to the Department of Biotechnology (DBT), Govt. of India, for providing funds in the form of Ramalingaswami Re-entry fellowship project (BT/RLF/Re-entry/34/2015; award BT/HRD/35/02/2006) to Shailendra Sharma to carry out this research work. Authors also acknowledge the Department of Science and Technology (DST) Govt. of India for providing funds in the form of DST-INSPIRE to Vikas Kumar Singh to carry out his research work. The authors are also thankful to Chaudhary Charan Singh University, Meerut, for providing necessary research facilities.

Author information

Authors and Affiliations

  1. Department of Genetics and Plant Breeding, Chaudhary Charan Singh University (CCSU), Meerut, 250 004, Uttar Pradesh, India

    Vikas Kumar Singh, Deepti Chaturvedi, Saksham Pundir, Deepak Kumar, Shiveta Sharma & Shailendra Sharma

  2. Department of Botany, Chaudhary Charan Singh University (CCSU), Meerut, 250 004, Uttar Pradesh, India

    Saksham Pundir & Deepak Kumar

  3. Scotland’s Rural College (SRUC), Peter Wilson Building, West Mains Road, Edinburgh, EH9 3JG, UK

    Rajiv Sharma

  4. Division of Genomic Resources, National Bureau of Plant Genetic Resources (NBPGR), Pusa Campus, New Delhi, 110 012, India

    Sundeep Kumar

Authors
  1. Vikas Kumar Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Deepti Chaturvedi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Saksham Pundir
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Deepak Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rajiv Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sundeep Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shiveta Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shailendra Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SS conceived the research idea. VKS, and RS performed the analysis part. VKS, SSh, DC, SP and DK performed experiments. All authors including SK contributed to the writing of the manuscript. The manuscript was read and revised by all authors and finalized by SS.

Corresponding author

Correspondence to Shailendra Sharma.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare.

Additional information

Communicated by Bing Yang.

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 1833 KB)

Supplementary file2 (XLSX 62 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Singh, V.K., Chaturvedi, D., Pundir, S. et al. GWAS scans of cereal cyst nematode (Heterodera avenae) resistance in Indian wheat germplasm. Mol Genet Genomics 298, 579–601 (2023). https://doi.org/10.1007/s00438-023-01996-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-023-01996-5

Keywords

Search

Navigation