Genetic structure and genome-wide association study of a genomic panel of two-row, spring barley (Hordeum vulgare L.) with differential reaction to Fusarium head blight (Fusarium graminearum Schwabe) and deoxynivalenol production

References

• Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al. 2000. Gene ontology: tool for the unification of biology. Nat Genet. 25(1):25–29. doi:10.1038/75556.
   PubMed Web of Science ®Google Scholar
• Bai GH, Shaner G. 2004. Management and resistance in wheat and barley to Fusarium head blight. Annu Rev Phytopathol. 42(1):135–161. doi:10.1146/annurev.phyto.42.040803.140340.
   PubMedGoogle Scholar
• Bayer MM, Rapazote-Flores P, Ganal M, Hedley PE, Macaulay M, Plieske J, Ramsay L, Russell J, Shaw PD, Thomas W, et al. 2017. Development and evaluation of a barley 50k iSelect SNP array. Front Plant Sci. 8:1792. doi:10.3389/fpls.2017.01792
   PubMed Web of Science ®Google Scholar
• Bedawy IMA, Dehne HW, Léon J, Naz AA. 2018. Mining the global diversity of barley for Fusarium resistance using leaf and spike inoculations. Euphytica. 214(1):18. doi:10.1007/s10681-017-2103-1.
   Web of Science ®Google Scholar
• Blum M, Chang H, Chuguransky S, Grego T, Kandasaamy S, Mitchell A, Nuka G, Paysan-Lafosse T, Qureshi M, Raj S, et al. 2021. The InterPro protein families and domains database: 20 years on. Nucleic Acids Res. 49(D1):D344–D354. doi:10.1093/nar/gkaa977.
   PubMed Web of Science ®Google Scholar
• Boutigny A-L, Richard-Forget F, Barreau C. 2008. Natural mechanisms for cereal resistance to the accumulation of Fusarium trichothecenes. Eur J Plant Pathol. 121(4):411–423. doi:10.1007/s10658-007-9266-x.
   Web of Science ®Google Scholar
• Buerstmayr H, Legzdina L, Steiner B, Lemmens M. 2004. Variation for resistance to Fusarium head blight in spring barley. Euphytica. 137(3):279–290. doi:10.1023/B:EUPH.0000040440.99352.b9.
   Web of Science ®Google Scholar
• Bush WS, Moore JH. 2012. Chapter 11: genome-wide association studies. PLoS Comput Biol. 8(12):e1002822. doi:10.1371/journal.pcbi.1002822.
   PubMed Web of Science ®Google Scholar
• Chan EK, Rowe HC, Kliebenstein DJ. 2010. Understanding the evolution of defense metabolites in Arabidopsis thaliana using genome-wide association mapping. Genetics. 185(3):991–1007. doi:10.1534/genetics.109.108522.
   PubMed Web of Science ®Google Scholar
• Choo TM, Vigier B, Shen QQ, Martin RA, Ho KM, Savard M. 2004. Barley traits associated with resistance to Fusarium head blight and deoxynivalenol accumulation. Phytopathology. 94(10):1145–1150. doi:10.1094/PHYTO.2004.94.10.1145.
   PubMed Web of Science ®Google Scholar
• Clear RM, Patrick SK, Platford RG, Desjardins M. 1996. Occurrence and distribution of Fusarium species in barley and oat seed from Manitoba in 1993 and 1994. Can J Plant Pathol. 18(4):409–414. doi:10.1080/07060669609500596.
   Web of Science ®Google Scholar
• Close TJ, Bhat PR, Lonardi S, Wu Y, Rostoks N, Ramsay L, Druka A, Stein N, Svensson JT, Wanamaker S, et al. 2009. Development and implementation of high-throughput SNP genotyping in barley. BMC Genomics. 10(1):582. doi:10.1186/1471-2164-10-582.
   PubMed Web of Science ®Google Scholar
• Comadran J, Kilian B, Russell J, Ramsay L, Stein N, Ganal M, Shaw P, Bayer M, Thomas W, Marshall D, et al. 2012. Natural variation in a homolog of Antirrhinum CENTRORADIALIS contributed to spring growth habit and environmental adaptation in cultivated barley. Nat Genet. 44(12):1388–1392. doi:10.1038/ng.2447.
   PubMed Web of Science ®Google Scholar
• Dahleen LS, Agrama HA, Horsley RD, Steffenson BJ, Schwarz PB, Mesfin A, Franckowiak JD. 2003. Identification of QTL associated with Fusarium head blight resistance in Zhedar 2 barley. Theor Appl Genet. 108(1):95–104. doi:10.1007/s00122-003-1409-7.
   PubMed Web of Science ®Google Scholar
• de la Peña RC, Smith KP, Capettini F, Muehlbauer GJ, Gallo-Meagher M, Dill-Macky R, Somers DA, Rasmusson DC. 1999. Quantitative trait loci associated with resistance to Fusarium head blight and kernel discoloration in barley. Theor Appl Genet. 99(3–4):561–569. doi:10.1007/s001220051269.
   PubMed Web of Science ®Google Scholar
• Earl DA, vonHoldt BM. 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. 4(2):359–361. doi:10.1007/s12686-011-9548-7.
   Google Scholar
• Edgar R. 2002. Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30(1):207–210. doi:10.1093/nar/30.1.207.
   PubMed Web of Science ®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(8):2611–2620. doi:10.1111/j.1365-294X.2005.02553.x.
   PubMed Web of Science ®Google Scholar
• Foroud NA, Ouellet T, Laroche A, Oosterveen B, Jordan MC, Ellis BE, Eudes F. 2012. Differential transcriptome analyses of three wheat genotypes reveal different host response pathways associated with Fusarium head blight and trichothecene resistance. Plant Pathology. 61(2):296–314. doi:10.1111/j.1365-3059.2011.02512.x.
   Web of Science ®Google Scholar
• Foroud NA, Pordel R, Goyal RK, Ryabova D, Chatterton S, Kovalchuk I. 2019. Chemical activation of the ethylene signalling pathway promotes wheat resistance to Fusarium graminearum. Phytopathology. 109(5):796–803. doi:10.1094/PHYTO-08-18-0286-R.
   PubMed Web of Science ®Google Scholar
• Gottwald S, Samans B, Lück S, Friedt W. 2012. Jasmonate and ethylene dependent defence gene expression and suppression of fungal virulence factors: two essential mechanisms of Fusarium head blight resistance in wheat? BMC Genomics. 13(1):369. doi:10.1186/1471-2164-13-369.
   PubMedGoogle Scholar
• Gunupuru LR, Perochon A, Doohan FM. 2017. Deoxynivalenol resistance as a component of FHB resistance. Trop Plant Pathol. 42(3):175–183. doi:10.1007/s40858-017-0147-3.
   Web of Science ®Google Scholar
• He X, Osman M, Capettini F, Helm J, Singh P. 2015. Evaluation of Canadian barley breeding lines for Fusarium head blight resistance. Can J Plant Sci. 95(5):923–925. doi:10.4141/cjps-2015-062.
   Web of Science ®Google Scholar
• Hori K, Kobayashi T, Sato K, Takeda K. 2005. QTL analysis of Fusarium head blight resistance using a high-density linkage map in barley. Theor Appl Genet. 111(8):1661–1672. doi:10.1007/s00122-005-0102-4.
   PubMed Web of Science ®Google Scholar
• Hori K, Sato K, Kobayashi T, Takeda K. 2006. QTL analysis of Fusarium head blight severity in recombinant inbred population derived from a cross between two-rowed barley varieties. Breed Sci. 56(1):25–30. doi:10.1270/jsbbs.56.25.
   Web of Science ®Google Scholar
• Horsley RD, Schmierer D, Maier C, Kudrna D, Urrea CA, Steffenson BJ, Schwarz PB, Franckowiak JD, Green MJ, Zhang B, et al. 2006. Identification of QTLs associated with Fusarium head blight resistance in barley accession CIho 4196. Crop Sci. 46(1):145–156. doi:10.2135/cropsci2005.0247.
   Web of Science ®Google Scholar
• Huang Y, Li L, Smith KP, Muehlbauer GJ. 2016. Differential transcriptomic responses to Fusarium graminearum infection in two barley quantitative trait loci associated with Fusarium head blight resistance. BMC Genomics. 17(1):387. doi:10.1186/s12864-016-2716-0.
   PubMedGoogle Scholar
• Huang Y, Haas M, Heinen S, Steffenson BJ, Smith KP, Muehlbauer GJ. 2018. QTL mapping of Fusarium head blight and correlated agromorphological traits in an elite barley cultivar Rasmusson. Front Plant Sci. 9:1260. doi:10.3389/fpls.2018.01260
   PubMed Web of Science ®Google Scholar
• Hussain RMF, Sheikh AH, Haider I, Quareshy M, Linthorst HJM. 2018. Arabidopsis WRKY50 and TGA transcription factors synergistically activate expression of PR1. Front Plant Sci. 9:930. doi:10.3389/fpls.2018.00930
   PubMed Web of Science ®Google Scholar
• Jia H, Millett BP, Cho S, Bilgic H, Xu WW, Smith KP, Muehlbauer GJ. 2011. Quantitative trait loci conferring resistance to Fusarium head blight in barley respond differentially to Fusarium graminearum infection. Funct Integr Genomics. 11(1):95–102. doi:10.1007/s10142-010-0192-1.
   PubMed Web of Science ®Google Scholar
• Jones JDG, Dangl JL. 2006. The plant immune system. Nature. 444(7117):323–329. doi:10.1038/nature05286.
   PubMed Web of Science ®Google Scholar
• Juskiw P, Oatway L, Oro MP, Nyachiro JM, Anbessa Y, Xi K, Turkington TK, Lohr S, Bowness J, Capettini F. 2019. Registration of ‘Lowe’, a two-rowed malting barley with enhanced resistance to Fusarium head blight. J Plant Regist. 13(3):301–310. doi:10.3198/jpr2018.11.0075crc.
   Web of Science ®Google Scholar
• Karre S, Kumar A, Yogendra K, Kage U, Kushalappa A, Charron JB. 2019. HvWRKY23 regulates flavonoid glycoside and hydroxycinnamic acid amide biosynthetic genes in barley to combat Fusarium head blight. Plant Mol Biol. 100(6):591–605. doi:10.1007/s11103-019-00882-2.
   PubMed Web of Science ®Google Scholar
• Koppolu R, Anwar N, Sakuma S, Tagiri A, Lundqvist U, Pourkheirandish M, Rutten T, Seiler C, Himmelbach A, Ariyadasa R, et al.$3$2 2013. Six-Rowed spike4 (Vrs4) controls spikelet determinacy and row-type in barley. Proc Natl Acad Sci U S a. 110(32):13198–13203. doi:10.1073/pnas.1221950110
   PubMed Web of Science ®Google Scholar
• Kumar A, Yogendra KN, Karre S, Kushalappa AC, Dion Y, Choo TM. 2016. WAX INDUCER1 (HvWIN1) transcription factor regulates free fatty acid biosynthetic genes to reinforce cuticle to resist Fusarium head blight in barley spikelets. J Exp Bot. 67(14):4127–4139. doi:10.1093/jxb/erw187.
   PubMed Web of Science ®Google Scholar
• Kushalappa AC, Yogendra KN, Karre S. 2016. Plant innate immune response: qualitative and quantitative resistance. Crit Rev Plant Sci. 35(1):38–55. doi:10.1080/07352689.2016.1148980.
   Web of Science ®Google Scholar
• Laitila A. 2015. Toxigenic fungi and mycotoxins in the barley-to-beer chain. In: Hill A, editor. Brewing microbiology: managing microbes, ensuring quality and valorising waste, woodhead publishing series in food science, technology and nutrition. Oxford (UK,): Woodland Publishing; p. 107–139. doi:10.1016/B978-1-78242-331-7.00006-X
   Google Scholar
• Lancova K, Hajslova J, Poustka J, Krplova A, Zachariasova M, Dostalek P, Sachambula L. 2008. Transfer of Fusarium mycotoxins and ‘masked’ deoxynivalenol (deoxynivalenol-3-glucoside) from field barley through malt to beer. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 25(6):732–744. doi:10.1080/02652030701779625.
   PubMed Web of Science ®Google Scholar
• Legge WG, Therrien MC, Tucker JR, Banik M, Tekauz A, Somers D, Savard ME, Rossnagel BG, Lefol E, Voth D, et al. 2004. Progress in breeding for resistance to fusarium head blight in barley. Can J Plant Pathol. 26(4):436–442. doi:10.1080/07060660409507163.
   Web of Science ®Google Scholar
• Legge WG, Badea A, Tucker JR, Fetch TG, Haber S, Menzies JG, Tekauz A, Turkington TK, Martin RA, Choo TM, et al. 2017. AAC Connect barley. Can J Plant Sci. 97:539–548. doi:10.1139/cjps-2016-0312
   Web of Science ®Google Scholar
• Legge WG, Badea A, Tucker JR, Fetch TG, Banik M, Haber S, Menzies JG, Tekauz A, Turkington TK, Martin RA, et al. 2018. AAC Goldman barley. Can J Plant Sci. 98(5):1203–1211. doi:10.1139/cjps-2017-0361.
   Web of Science ®Google Scholar
• Linkmeyer A, Götz M, Hu L, Asam S, Rychlik M, Hausladen H, Hess M, Hückelhoven R. 2013. Assessment and introduction of quantitative resistance to Fusarium head blight in elite spring barley. Phytopathology. 103(12):1252–1259. doi:10.1094/PHYTO-02-13-0056-R.
   PubMed Web of Science ®Google Scholar
• Liu J, Osbourn A, Ma P. 2015. MYB Transcription factors as Regulators of phenylpropanoid metabolism in plants. Mol Plant. 8(5):689–708. doi:10.1016/j.molp.2015.03.012.
   PubMed Web of Science ®Google Scholar
• Ma Z, Steffenson BJ, Prom LK, Lapitan NL. 2000. Mapping of quantitative trait loci for Fusarium head blight resistance in barley. Phytopathology. 90(10):1079–1088. doi:10.1094/PHYTO.2000.90.10.1079.
   PubMed Web of Science ®Google Scholar
• Makandar R, Nalam VJ, Lee H, Trick HN, Dong Y, Shah J. 2012. Salicylic acid regulates basal resistance to Fusarium head blight in wheat. Mol PlantMicrobe Interact. 25:431–439. doi:10.1094/MPMI-09-11-0232
   PubMed Web of Science ®Google Scholar
• Mamo BE, Steffenson BJ. 2015. Genome-wide association mapping of Fusarium head blight resistance and agromorphological traits in barley landraces from Ethiopia and Eritrea. Crop Sci. 55(4):1494–1512. doi:10.2135/cropsci2014.06.0428.
   Web of Science ®Google Scholar
• Mascher M, Wicker T, Jenkins J, Plott C, Lux T, Koh CS, Ens J, Gundlach H, Boston LB, Tulpová Z, et al. 2021. Long-read sequence assembly: a technical evaluation in barley. Plant Cell. 33(6):1888–1906. doi:10.1093/plcell/koab077.
   PubMed Web of Science ®Google Scholar
• Massman J, Cooper B, Horsley R, Neate S, Dill-Macky R, Chao S, Dong Y, Schwarz P, Muehlbauer GJ, Smith KP. 2011. Genome-wide association mapping of Fusarium head blight resistance in contemporary barley breeding germplasm. Mol Breed. 27(4):439–454. doi:10.1007/s11032-010-9442-0.
   Web of Science ®Google Scholar
• McLaughlin JE, Darwish NI, Garcia-Sanchez J, Tyagi N, Trick HN, McCormick S, Dill-Macky R, Tumer NE. 2021. A lipid transfer protein has antifungal and antioxidant activity and suppresses Fusarium head blight disease and DON accumulation in transgenic wheat. Phytopathology. 111(4):671–683. doi:10.1094/PHYTO-04-20-0153-R.
   PubMed Web of Science ®Google Scholar
• Mesfin A, Smith KP, Dill-Macky R, Evans CK, Waugh R, Gustus CD, Muehlbauer GJ. 2003. Quantitative trait loci for Fusarium head blight resistance in barley detected in a two-rowed by six-rowed population. Crop Sci. 43(1):307–318. doi:10.2135/cropsci2003.3070.
   Web of Science ®Google Scholar
• Meuwissen TH, Hayes BJ, Goddard ME. 2001. Prediction of total genetic value using genome-wide dense marker maps. Genetics. 157(4):1819–1829. doi:10.1093/genetics/157.4.1819.
   PubMed Web of Science ®Google Scholar
• Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar GA, Sonnhammer ELL, Tosatto SCE, Paladin L, Raj S, Richardson LJ, et al. 2020. Pfam: the protein families database in 2021. Nucleic Acids Res. 49(D1):D412–D419. doi:10.1093/nar/gkaa913.
   Web of Science ®Google Scholar
• Ogrodowicz P, Kuczyńska A, Mikołajczak K, Adamski T, Surma M, Krajewski P, Ćwiek-Kupczyńska H, Kempa M, Rokicki M, Jasińska D, et al. 2020. Mapping of quantitative trait loci for traits linked to fusarium head blight in barley. PLoS One. 15(2):e0222375. doi:10.1371/journal.pone.0222375.
   PubMed Web of Science ®Google Scholar
• Pritchard JK, Stephens M, Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics. 155(2):945–959. doi:10.1093/genetics/155.2.945.
   PubMed Web of Science ®Google Scholar
• R Core Team. 2021. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. [ accessed 2022 Apr 13]. https://www.R-project.org/
   Google Scholar
• Ramasamy RK, Ramasamy S, Bindroo BB, Naik VG. 2014. STRUCTURE PLOT: a program for drawing elegant STRUCTURE bar plots in user friendly interface. Springerplus. 3(1):431. doi:10.1186/2193-1801-3-431.
   PubMedGoogle Scholar
• Rossnagel BG, Zatorski T, Voth WD, Scoles GJ, Legge WG, Tucker JR, Tekauz A, Savard M. 2008. Registration of ‘CDC Mindon’ barley. J Plant Reg. 2(2):79–84. doi:10.3198/jpr2007.10.0568crc.
   Google Scholar
• Sallam AH, Endelman JB, Jannink J-L, Smith KP. 2015. Assessing genomic selection prediction accuracy in a dynamic barley breeding population. Plant Genome. 8:lantgenome2014.05.0020. doi:10.3835/plantgenome2014.05.0020
   PubMed Web of Science ®Google Scholar
• SAS Institute Inc. 2019. SAS JMP Genomics version 9.1. Cary, NC, USA: SAS Institute Inc.
   Google Scholar
• Tang D, Wang G, Zhou J-M. 2017. Receptor kinases in plant-pathogen interactions: more than pattern recognition. Plant Cell. 29(4):618–637. doi:10.1105/tpc.16.00891.
   PubMed Web of Science ®Google Scholar
• Tekauz A, McCallum B, Gilbert J. 2000. Review: fusarium head blight of barley in western Canada. Can J Plant Pathol. 22(1):9–16. doi:10.1080/07060660009501156.
   Web of Science ®Google Scholar
• Tsuda K, Somssich IE. 2015. Transcriptional networks in plant immunity. New Phytol. 206(3):932–947. doi:10.1111/nph.1328.
   PubMed Web of Science ®Google Scholar
• Tucker JR, Badea A, Blagden R, Pleskach K, Tittlemier SA, Fernando WGD. 2019. Deoxynivalenol-3-Glucoside content is highly associated with deoxynivalenol levels in two-Row barley genotypes of importance to Canadian barley breeding programs. Toxins. 11(6):319. doi:10.3390/toxins11060319.
   Web of Science ®Google Scholar
• Tucker JR, Legge WG, Maiti S, Hiebert CW, Simsek S, Yao Z, Xu W, Badea A, Fernando WGD. 2021. Transcriptome alterations of an in vitro-selected, moderately resistant, two-row malting barley in response to 3ADON, 15ADON, and NIV Chemotypes of Fusarium graminearum. Front Plant Sci. 12:701969. doi:10.3389/fpls.2021.701969
   PubMed Web of Science ®Google Scholar
• Turner A, Beales J, Faure S, Dunford RP, Laurie DA. 2005. The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science. 310(5750):1031–1034. doi:10.1126/science.1117619.
   PubMed Web of Science ®Google Scholar
• Uluhan E, Keleş EN, Tufan F. 2019. Analysis of WRKY transcription factors in barley cultivars infected with Fusarium culmorum. Int J Life Sci and Biotechnol. 2(3):165–174. doi:10.38001/ijlsb.588730.
   Google Scholar
• Waugh R, Jannink J-L, Muehlbauer G, Ramsay L. 2009. The emergence of whole genome association scans in barley. Curr Opin Plant Bio. 12(2):218–222. doi:10.1016/j.pbi.2008.12.007.
   PubMed Web of Science ®Google Scholar
• Yu GT, Franckowiak JD, Neate SM, Zhang B, Horsley RD. 2010. A native QTL for Fusarium head blight resistance in North American barley (Hordeum vulgare L.) independent of height, maturity, and spike type loci. Genome. 53(2):111–118. doi:10.1139/G09-091.
   PubMed Web of Science ®Google Scholar
• Zadoks JC, Chang TT, Konzak CF. 1974. A decimal code for the growth stages of cereals. Weed Res. 14(6):415–421. doi:10.1111/j.1365-3180.1974.tb01084.x.
   Web of Science ®Google Scholar
• Zhu H, Gilchrist L, Hayes P, Kleinhofs A, Kudrna D, Liu Z, Prom L, Steffenson B, Toojinda T, Vivar H. 1999. Does function follow form? Principal QTLs for Fusarium head blight (FHB) resistance are coincident with QTLs for inflorescence traits and plant height in a doubled-haploid population of barley. Theor Appl Genet. 99(6):1221–1232. doi:10.1007/s001220051328.
   Google Scholar