Advertisement

Molecular Breeding

, 37:92 | Cite as

SNP discovery from next-generation transcriptome sequencing data and their validation using KASP assay in wheat (Triticum aestivum L.)

  • Saket Chandra
  • Dharmendra Singh
  • Jyoti Pathak
  • Supriya Kumari
  • Manish Kumar
  • Raju Poddar
  • Harindra Singh Balyan
  • Kumble Vinod Prabhu
  • Pushpendra Kumar Gupta
  • Kunal Mukhopadhyay
Article

Abstract

Single nucleotide polymorphisms (SNPs) are becoming the most amenable form of DNA-based molecular markers for genetic analysis. In hexaploid bread wheat (Triticum aestivum L.), it is difficult to discern true polymorphic SNPs due to homoeologous and paralogous genes. Two serial analysis of gene expression (SAGE) libraries were developed utilizing leaves from resistant plants carrying leaf rust resistance gene Lr28; one library was derived from leaves that were mock inoculated and the other was derived from leaves inoculated with the urediniospores of the leaf rust pathogen Puccinia triticina. Next-generation sequencing reads, after quality trimming and removal of fungal sequences, were mapped to wheat reference sequences at Ensembl Plants. CLC Genomics Workbench and Freebayes softwares were employed for SNP calling. A total of 611 SNPs were predicted to be common by both softwares, of which 207 varietal SNPs were identified by ConservedPrimer software. A subset of 100 SNPs was used for validation across 47 wheat genotypes using Kompetitive Allele Specific PCR (KASP) assay; 83 SNPs could be successfully validated. These SNPs were positioned on wheat subgenomes and chromosome arms. When functionally annotated, many sequences harboring SNPs showed homology to resistance and resistance-like genes listed in Plant Resistance Gene database (PRGdb) as well as pathogenesis-related (PR) and stress-responsive genes. The results of the present study involving discovery of SNPs associated with resistance to leaf rust, a major threat to wheat production worldwide, will be valuable for molecular breeding for rust resistance.

Keywords

Single nucleotide polymorphisms Wheat Transcriptome KASP assay Leaf rust 

Notes

Acknowledgements

The authors are thankful to Biotechnology Information System Network Distributed Information Sub Centre (BT/BI/04/065/04) for providing facilities for bioinformatics analyses. This work was supported by Department of Biotechnology, Government of India (Grant No. BT/PR6037/AGR/02/308/05 and BT/PR3925/BID/7/384/2011) and Centre of Excellence, Technical Education Quality Improvement Program-II (Grant No. NPIU/TEQIP II/FIN/31/158).

Authors’ contribution

KM, MK, and PKG designed the experiment and wrote the manuscript; SC, DS, and SK performed SNP genotyping; JP and RP supported the bioinformatics analysis; HSB and KVP revised the manuscript. All the authors read and approved the final manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

11032_2017_696_MOESM1_ESM.docx (33 kb)
Fig. S1 (DOCX 32 kb)
11032_2017_696_MOESM2_ESM.docx (141 kb)
Fig. S2 (DOCX 141 kb)
11032_2017_696_MOESM3_ESM.docx (340 kb)
Fig. S3 (DOCX 339 kb)
11032_2017_696_MOESM4_ESM.docx (60 kb)
Fig. S4 (DOCX 60 kb)
11032_2017_696_MOESM5_ESM.docx (75 kb)
Fig. S5 (DOCX 74 kb)
11032_2017_696_MOESM6_ESM.docx (94 kb)
Fig. S6 (DOCX 93 kb)
11032_2017_696_MOESM7_ESM.docx (146 kb)
Fig. S7 (DOCX 145 kb)
11032_2017_696_MOESM8_ESM.docx (15 kb)
Table S1 (DOCX 15 kb)
11032_2017_696_MOESM9_ESM.docx (36 kb)
Table S2 (DOCX 36 kb)
11032_2017_696_MOESM10_ESM.docx (16 kb)
Table S3 (DOCX 15 kb)
11032_2017_696_MOESM11_ESM.docx (16 kb)
Table S4 (DOCX 15 kb)
11032_2017_696_MOESM12_ESM.docx (15 kb)
Table S5 (DOCX 15 kb)
11032_2017_696_MOESM13_ESM.docx (22 kb)
Table S6 (DOCX 22 kb)
11032_2017_696_MOESM14_ESM.xls (20 kb)
Table S7 (XLS 19 kb)

References

  1. Akhunov E, Nicolet C, Dvorak J (2009) Single nucleotide polymorphism genotyping in polyploid wheat with the Illumina GoldenGate assay. Theor Appl Genet 119:507–517CrossRefPubMedPubMedCentralGoogle Scholar
  2. Allen AM, Barker GL, Berry ST, Coghill JA, Gwilliam R, Kirby S, Robinson P, Brenchley RC, D’Amore R, McKenzie N, Waite D, Hall A, Bevan M, Hall N, Edwards KJ (2011) Transcript-specific, single nucleotide polymorphism discovery and linkage analysis in hexaploid bread wheat (Triticum aestivum L.) Plant Biotechnol J 9:1086–1099CrossRefPubMedGoogle Scholar
  3. Altshuler D, Pollara VJ, Cowles CR, Etten WJV, Baldwin J, Linton L, Lander ES (2000) An SNP map of the human genome generated by reduced representation shotgun sequencing. Nature 407:513–516CrossRefPubMedGoogle Scholar
  4. Babben S, Perovic D, Koch M, Ordon F (2015) An efficient approach for the development of locus specific primers in bread wheat (Triticum aestivum L.) and its application to re-sequencing of genes involved in frost tolerance. PloS ONE 10(11):e0142746CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bajgain P, Rouse MN, Tsilo TJ, Macharia GK, Bhavani S, Jin Y, Anderson JA (2016) Nested association mapping of stem rust resistance in wheat using genotyping by sequencing. PLoS One 11(5):e0155760CrossRefPubMedPubMedCentralGoogle Scholar
  6. Barker GLA, Edwards KJ (2009) A genome-wide analysis of single nucleotide polymorphism diversity in the world’s major cereal crops. Plant Biotechnol J 7:318–325CrossRefPubMedGoogle Scholar
  7. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57:289–300Google Scholar
  8. Bipinraj A, Honrao B, Prashar M, Bhardwaj S, Rao S, Tamhankar S (2011) Validation and identification of molecular markers linked to the leaf rust resistance gene Lr28 in wheat. J Appl Genet 52:171–175CrossRefPubMedGoogle Scholar
  9. Bonman JM, Babiker EM, Cuesta-Marcos A, Esvelt-Klos K, BrownGuedira G, Chao S, See D, Chen J, Akhunov E, Zhang J, Bockelman HE, Gordon TC (2015) Genetic diversity among wheat accessions from the USDA National Small Grains Collection. Crop Sci 55:1243CrossRefGoogle Scholar
  10. Boutet G, Carvalho SA, Falque M, Peterlongo P, Lhuillier E, Bouchez O, Lavaud C, Piley-Nayel M, Riviere N, Baranger A (2016) SNP discovery and genetic mapping using genotyping by sequencing of whole genome genomic DNA from a pea RIL population. BMC Genomics 17:121CrossRefPubMedPubMedCentralGoogle Scholar
  11. Braun HJ, Atlin G, Payne T (2010) Multi-location testing as a tool to identify plant response to global climate change. In: climate change and crop production. Ed: CRP Reynolds, CABI London pp: 115–138Google Scholar
  12. Brockman W, Alvarez P, Young S, Garber M, Giannoukos G, Lee WL, Russ C, Sander ES, Nusbaum C, Jaffe DB (2008) Quality scores and SNP detection in sequencing-by-synthesis systems. Genome Res 18:763–770CrossRefPubMedPubMedCentralGoogle Scholar
  13. Cavanagh CR, Chao S, Wang S, Huang BE, Stephen S, Kiani S, Forrest K, Saintenac C, Brown-Guedira GL, Akhunova A, See D, Bai G, Pumphrey M, Tomar L, Wong D, Kong S, Reynolds M, Da Silva ML, Bockelman H, Talbert L, Anderson JA, Dreisigacker S, Baenziger S, Carter A, Korzun V, Morrell PL, Dubcovsky J, Morell MK, Sorrells ME, Hayden MJ, Akhunov E (2013) Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars. Proc Natl Acad Sci U S A 110:8057–8062CrossRefPubMedPubMedCentralGoogle Scholar
  14. Chandra S, Singh D, Pathak J, Kumari S, Kumar M, Poddar R, Balyan HS, Gupta PK, Prabhu KV, Mukhopadhyay K (2016) De novo assembled wheat transcriptomes delineate differentially expressed host genes in response to leaf rust infection. PLoS One 11:e0148453CrossRefPubMedPubMedCentralGoogle Scholar
  15. Chapman JA, Mascher M, Bulu A, Barry K, Georganas E, Session A, Strnadova V, Jenkins J, Sehgal S, Oliker L, Schmutz J, Yelick KA, Scholz U, Waugh R, Poland JA, Muehlbauer GJ, Stein N, Rokhsar DS (2015) A whole-genome shotgun approach for assembling and anchoring the hexaploid bread wheat genome. Genome Biol 16:26CrossRefPubMedPubMedCentralGoogle Scholar
  16. Charpe A, Koul S, Gupta SK, Singh A, Pallavi JK, Prabhu KV (2012) Marker assisted gene pyramiding of leaf rust resistance genes Lr9, Lr24 and Lr 28 in a bread wheat cultivar HD2329. J Wheat Res 4:20–28Google Scholar
  17. Chopra R, Burow G, Hayes C, Emendack Y, Xin Z, Burke J (2015) Transcriptome profiling and validation of gene based single nucleotide polymorphisms (SNPs) in sorghum genotypes with contrasting responses to cold stress. BMC Genomics 16:1040CrossRefPubMedPubMedCentralGoogle Scholar
  18. Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, Land SJ, Lu X, Ruden DM (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6:80–92CrossRefPubMedPubMedCentralGoogle Scholar
  19. Conesa A, Götz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676CrossRefPubMedGoogle Scholar
  20. Dean R, Van-Kan JAL, Pretorius ZA, Hammond-Kosack KE, Pietro AD, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430CrossRefPubMedGoogle Scholar
  21. Dvorak J, Dubcovsky J (2007) Genome plasticity a key factor in the success of polyploid wheat under domestication. Science 316:1862–1866CrossRefPubMedPubMedCentralGoogle Scholar
  22. Edwards D, Wilcox S, Barrero RA, Fleury D, Cavanagh CR, Forrest KL, Hayden MJ, Moolhuijzen P, Keeble-Gagnère G, Bellgard MI, Lorenc MT, Shang CA, Baumann U, Taylor JM, Morell MK, Langridge P, Appels R, Fitzgerald A (2012) Bread matters: a national initiative to profile the genetic diversity of Australian wheat. Plant Biotechnol J 10:703–708CrossRefPubMedGoogle Scholar
  23. Eversole K, Feuillet C, Mayer KF, Rogers J (2014) Slicing the wheat genome. Science 345:285–287CrossRefPubMedGoogle Scholar
  24. Feschotte C, Jiang N, Wessler SR (2002) Plant transposable elements: where genetics meets genomics. Nat Rev Genet 3:329–341CrossRefPubMedGoogle Scholar
  25. Ganal MW, Altmann T, Roder MS (2009) SNP identification in crop plants. Curr Opin in Plant Biol 12:211–217CrossRefGoogle Scholar
  26. Gao L, Turner MK, Chao S, Kolmer J, Anderson JA (2016) Genome wide association study of seedling and adult plant leaf rust resistance in elite spring wheat breeding lines. PLoS One 11:e0148671CrossRefPubMedPubMedCentralGoogle Scholar
  27. Garrison E, Marth G (2012) Haplotype-based variant detection from short-read sequencing. arXiv preprint arXiv. 1207: 3907Google Scholar
  28. Goutam U, Kukreja S, Yadav R, Salaria N, Thakur K, Goyal AK (2015) Recent trends and perspectives of molecular markers against fungal diseases in wheat. Front Microbiol 6:861CrossRefPubMedPubMedCentralGoogle Scholar
  29. Guo B, Beavis WD (2011) In silico genotyping of the maize nested association mapping population. Mol Breed 27:107–113CrossRefPubMedGoogle Scholar
  30. Gupta PK, Langridge P, Mir RR (2010) Marker-assisted wheat breeding: present status and future possibilities. Mol Breed 26:145–161CrossRefGoogle Scholar
  31. Gurung S, Mamidi S, Bonman JM, Xiong M, Brown-Guedira G, Adhikari TB (2014) Genome-wide association study reveals novel quantitative trait loci associated with resistance to multiple leaf spot diseases of spring wheat. PLoS One 9:e108179CrossRefPubMedPubMedCentralGoogle Scholar
  32. Jordan KW, Wang S, Lun Y, Gardiner LJ, MacLachlan R, Hucl P, Wiebe K, Wong D, Forrest KL, IWGSC, Sharpe AG, CHD S, Hall N, Toomajian C, Close T, Dubcovsky J, Akhunova A, Talbert L, Bansal UK, Bariana HS, Hayden MJ, Pozniak C, Jeddeloh JA, Hall A, Akhunova E (2015) A haplotype map of allohexaploid wheat reveals distinct patterns of selection on homoeologous genomes. Genome Biol 16:48CrossRefPubMedPubMedCentralGoogle Scholar
  33. Juliana P, Rutkoski JE, Poland JA, Singh RP, Murugasamy S, Natesan S, Barbier H, Sorrells ME (2015) Genome-wide association mapping for leaf tip necrosis and pseudo-black chaff in relation to durable rust resistance in wheat. Plant Genome 8:2CrossRefGoogle Scholar
  34. Kal AJ, van Zonneveld AJ, Benes V, den Berg MV, Koerkamp MG, Albermann K, Strack N, Ruijter JM, Richter A, Dujon B, Ansorge W, Tabak HF (1999) Dynamics of gene expression revealed by comparison of serial analysis of gene expression transcript profiles from yeast grown on two different carbon sources. Mol Biol Cell 10:1859–1872CrossRefPubMedPubMedCentralGoogle Scholar
  35. Kanehisa M, Sato Y, Morishima K (2016) BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 428:726–731CrossRefPubMedGoogle Scholar
  36. Kassa MT, You FM, Hiebert CW, Pozniak CJ, Fobert PR, Sharpe AG, Menzies JG, Humphreys DG, Rezac HN, Fellers JP, McCallum BD, McCartney CA (2017) Highly predictive SNP markers for efficient selection of the wheat leaf rust resistance gene Lr16. BMC Plant Biol 17:45CrossRefPubMedPubMedCentralGoogle Scholar
  37. Kertho A, Mamidi S, Bonman JM, McClean PE, Acevedo M (2015) Genome-wide association mapping for resistance to leaf and stripe rust in winter-habit hexaploid wheat landraces. PLoS One 10:e0129580CrossRefPubMedPubMedCentralGoogle Scholar
  38. Koboldt DC, Steinberg KM, Larson DE, Wilson RK, Mardis E (2013) The next-generation sequencing revolution and its impact on genomics. Cell 155:27–38CrossRefPubMedPubMedCentralGoogle Scholar
  39. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645CrossRefPubMedPubMedCentralGoogle Scholar
  40. Lai K, Lorenc MT, Lee HC, Berkman PJ, Bayer PE, Visendi P, Ruperao P, Fitzgerald TL, Zander M, Chan CK, Manoli S, Stiller J, Batley J, Edwards D (2015) Identification and characterization of more than 4 million intervarietal SNPs across the group 7 chromosomes of bread wheat. Plant Biotechnol J 13:97–104CrossRefPubMedGoogle Scholar
  41. Li G, Xu X, Bai G, Carver BF, Hunger R, Bonman JM, Kolmer J, Dong H (2016) Genome-wide association mapping reveals novel QTL for seedling leaf rust resistance in a worldwide collection of winter wheat. Plant Genome 9:3Google Scholar
  42. Maccaferri M, Zhang J, Bulli P, Abate Z, Chao S, Cantu D, Bossolini E, Chen X, Pumphrey M, Dubcovsky J (2015) A genome-wide association study of resistance to stripe rust (Puccinia striiformis f. sp. tritici) in a worldwide collection of hexaploid spring wheat (Triticum aestivum L.) G3 5:449–465CrossRefPubMedPubMedCentralGoogle Scholar
  43. Manickavelu A, Kawaura K, Oishi K, Shin T, Kohara Y, Yahiaoui N, Keller B, Abe R, Suzuki A, Nagayama T, Yano K, Ogihara Y (2012) Comprehensive functional analyses of expressed sequence tags in common wheat (Triticum aestivum). DNA Res 19:165–177CrossRefPubMedPubMedCentralGoogle Scholar
  44. Marcel TC, Aghnoum R, Durand J, Varshney RK, Niks RE (2007) Dissection of the barley 2L1.0 region carrying the ‘Laevigatum’ quantitative resistance gene to leaf rust using near-isogenic lines (NIL) and sub NIL. Mol Plant-Microbe Interact 20:1604–1615CrossRefPubMedGoogle Scholar
  45. McIntosh RA, Pretorius ZA (2011) Borlaug Global Rust Initiative provides momentum for wheat rust research. Euphytica 179:1–2CrossRefGoogle Scholar
  46. McNally KL, Childs KL, Bohnert R, Davidson RM, Zhao K, Ulat VJ, Zeller G, Clark RM, Hoen DR, Bureau TE, Stokowski R, Ballinger DG, Frazer KA, Cox DR, Padhukasahasram B, Bustamante CD, Weigel D, Mackill DJ, Bruskiewich RM, Ratsch G, Buell CR, Leung H, Leach JE (2009) Genome-wide SNP variation reveals relationships among landraces and modern varieties of rice. Proc Natl Acad Sci U S A 106:12273–12278CrossRefPubMedPubMedCentralGoogle Scholar
  47. Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth and death process. Genome Res 8:1113–1130CrossRefPubMedGoogle Scholar
  48. Ming R, Wai CM (2015) Assembling allopolyploid genomes: no longer formidable. Genome Biol 16:27CrossRefPubMedPubMedCentralGoogle Scholar
  49. Neelam K, Brown-Guedira G, Huang L (2013) Development and validation of a breeder friendly KASPar marker for wheat leaf rust resistance locus Lr21. Mol Breed 31:233–237CrossRefGoogle Scholar
  50. Pingault L, Choulet F, Alberti A, Glover N, Wincker P, Feuillet C, Paux E (2015) Deep transcriptome sequencing provides new insights into the structural and functional organization of the wheat genome. Genome Biol 16:29CrossRefPubMedPubMedCentralGoogle Scholar
  51. Prabhu KV, Gupta SK, Charpe A, Koul S, Cherukuri DP, Dhaliwal HS, Vikal Y, Chhuneja P, Haq QMR (2003) Molecular markers detect redundancy and miss-identity in genetic stocks with alien leaf rust resistance genes Lr32 and Lr28 in bread wheat. J Plant Biochem Biot 12:123–129CrossRefGoogle Scholar
  52. Rasheed A, Wen W, Gao F, Zhai S, Jin H, Liu J, Guo Q, Zhang Y, Dreisigacker S, Xia X, He Z (2016) Development and validation of KASP assays for genes underpinning key economic traits in bread wheat. Theor Appl Genet 129(10):1843–1860CrossRefPubMedGoogle Scholar
  53. Sanseverino W, Hermoso A, D'Alessandro R, Vlasova A, Andolfo G, Frusciante L, Lowy E, Roma G, Ercolano MR (2013) PRGdb 2.0: towards a community-based database model for the analysis of R-genes in plants. Nucleic Acids Res Database Issue 41:D1167–D1171CrossRefGoogle Scholar
  54. Semagn K, Babu R, Hearne S, Olsen M (2014) Single nucleotide polymorphism genotyping using Kompetitive Allele Specific PCR (KASP): overview of the technology and its application in crop improvement. Mol Breed 33:1–14CrossRefGoogle Scholar
  55. Shen J, Araki H, Chen L, Chen JQ, Tian D (2006) Unique evolutionary mechanism in R-genes under the presence/absence polymorphism in Arabidopsis thaliana. Genetics 172:1243–1250CrossRefPubMedPubMedCentralGoogle Scholar
  56. Singh D, Bhaganagare G, Bandopadhyay R, Prabhu KV, Gupta PK, Mukhopadhyay K (2012) Targeted spatio-temporal expression based characterization of state of infection and time-point of maximum defense in wheat NILs during leaf rust infection. Mol Biol Rep 39:9373–9382CrossRefPubMedGoogle Scholar
  57. Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Holsten T, Gardner J, Wang B, Zhai WX, Zhu LH (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804–1806CrossRefPubMedGoogle Scholar
  58. Sukumaran S, Dreisigacker S, Lopes M, Chavez P, Reynolds MP (2015) Genome-wide association study for grain yield and related traits in an elite spring wheat population grown in temperate irrigated environments. Theor Appl Genet 128:353–363CrossRefPubMedGoogle Scholar
  59. Vij S, Giri J, Dansana PK, Kapoor S, Tyagi AK (2008) The receptor-like cytoplasmic kinase (OsRLCK) gene family in rice: organization, phylogenetic relationship, and expression during development and stress. Mol Plant 1:732–750CrossRefPubMedGoogle Scholar
  60. Wang S, Wong D, Forrest K, Allen A, Chao S, Huang BE, Maccaferri M, Salvi S, Milner SG, Cattivelli L, Mastrangelo AM, Whan AM, Stephe S, Barker G, Wieseke R, Plieske J, International Wheat Genome Sequencing Consortium, Lillemo M, Mather D, Appels R, Dolferus R, Brown-Guedira G, Korol A, Akhunova AR, Feuillet C, Salse J, MorganteM PC, Luo M-C, Dvorak J, Morell M, Dubcovsky J, Ganal M, Tuberosa R, Lawley C, Mikoulitch I, Cavanagh C, Edwards KJ, Hayden M, Akhunov E (2014) Characterization of polyploid wheat genomic diversity using a high-density 90,000 single nucleotide polymorphism array. Plant Biotech J 12:787–796CrossRefGoogle Scholar
  61. Wicker T, Mayer KFX, Gundlach H, Martis M, Steuernage B, Scholz U, Simková H, Kubaláková M, Choulet F, Taudien S, Platzer M, Feuillet C, Fahima T, Budak H, Dolezel J, Keller B, Stein N (2011) Frequent gene movement and pseudogene evolution is common to the large and complex genomes of wheat, barley, and their relatives. Plant Cell 23:1706–1719CrossRefPubMedPubMedCentralGoogle Scholar
  62. You FM, Huo N, Gu YQ, Lazo GR, Dvorak J, Anderson OD (2009) ConservedPrimers 2.0: a high-throughput pipeline for comparative genome referenced intron-flanking PCR primer design and its application in wheat SNP discovery. BMC Bioinformatics. 13: 331Google Scholar
  63. You FM, Huo N, Deal KR, Gu YQ, Luo M, McGuire PE, Dvorak J, Anderson OD (2011) Annotation-based genome-wide SNP discovery in the large and complex Aegilops tauschii genome using next-generation sequencing without a reference genome sequence. BMC Genomics 12:59CrossRefPubMedPubMedCentralGoogle Scholar
  64. Zegeye H, Rasheed A, Makdis F, Badebo A, Ogbonnaya FC (2014) Genome-wide association mapping for seedling and adult plant resistance to stripe rust in synthetic hexaploid wheat. PLoS One 9:e105593CrossRefPubMedPubMedCentralGoogle Scholar
  65. Zhang D, Bai G, Hunger RM, Bockus WW, Yu J, Carver BF, Brown-Guedira G (2011) Association study of resistance to soil borne wheat mosaic virus in U.S. winter wheat. Phytopathology 101:1322–1329CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  • Saket Chandra
    • 1
  • Dharmendra Singh
    • 1
    • 2
  • Jyoti Pathak
    • 1
  • Supriya Kumari
    • 3
  • Manish Kumar
    • 1
  • Raju Poddar
    • 1
  • Harindra Singh Balyan
    • 3
  • Kumble Vinod Prabhu
    • 4
  • Pushpendra Kumar Gupta
    • 3
  • Kunal Mukhopadhyay
    • 1
  1. 1.Department of Bio-EngineeringBirla Institute of TechnologyRanchiIndia
  2. 2.QAAF1, Centre of Plant ScienceThe University of QueenslandBrisbaneAustralia
  3. 3.Department of Genetics and Plant BreedingChaudhary Charan Singh UniversityMeerutIndia
  4. 4.Department of GeneticsIndian Agricultural Research InstituteNew DelhiIndia

Personalised recommendations