Abstract
Fusarium head blight (FHB), or scab, for its devastating nature to wheat production and food security, has stimulated worldwide attention. Multidisciplinary efforts have been made to fight against FHB for a long time, but the great progress has been achieved only in the genomics era of the past 20 years, particularly in the areas of resistance gene/QTL discovery, resistance mechanism elucidation and molecular breeding for better resistance. This review includes the following nine main sections, (1) FHB incidence, epidemic and impact, (2) causal Fusarium species, distribution and virulence, (3) types of host resistance to FHB, (4) germplasm exploitation for FHB resistance, (5) genetic control of FHB resistance, (6) fine mapping of Fhb1, Fhb2, Fhb4 and Fhb5, (7) cloning of Fhb1, (8) omics-based gene discovery and resistance mechanism study and (9) breeding for better FHB resistance. The advancements that have been made are outstanding and exciting; however, judged by the complicated nature of resistance to hemi-biotrophic pathogens like Fusarium species and lack of immune germplasm, it is still a long way to go to overcome FHB.
Similar content being viewed by others
References
Abate ZA, Liu S, McKendry AL (2008) Quantitative trait loci associated with deoxynivalenol content and kernel quality in the soft red winter wheat ‘Ernie’. Crop Sci 48:1408–1418
Alexander NJ (2008) The Tri101 story: engineering wheat and barley to resist fusarium head blight. World Mycotoxin J 1:31–37
Alexander NJ, McCormick SP, Hohn TM (1999) Tri12, a trichothecene efflux pump from Fusarium sporotrichioides: gene isolation and expression in yeast. Mol Gen Genet 261:977–984
Andersen AL (1948) The development of Gibberella zeae head blight of wheat. Phytopathology 38:595–611
Anderson JA (2007) Marker-assisted selection for Fusarium head blight resistance in wheat. Int J Food Microbiol 119:51–53
Anderson JA (2012) Overview of breeding for FHB resistance in wheat—where we’ve come from and where we are. In: Canty S, Clark A, Anderson-Scully A, Van Sanford D (eds) Proceedings of the 2012 National Fusarium head blight forum. Orlando, FL, p 45
Anderson JA, Wiersma JJ, Linkert GL, Kolmer JA, Jin Y, Dill-Macky R, Wiersma JV, Hareland GA (2012) Registration of ‘Sabin’ Wheat. J Plant Reg 6:174–179
Anderson JA, Wiersma JJ, Reynolds SK, Caspers R, Linkert GL, Kolmer JA, Jin Y, Rouse MN, Dill-Macky R, Smith MJ, Dykes L, Ohm JB (2019) Registration of ‘Shelly’ hard red spring wheat. J Plant Reg 12:208–214
Aponyi I, Nagy G, Princzinger G, Kajati I (1998) Fusarium infection of wheat seeds in Hungary between 1970 and 1997. Cereal Res Commun 26:253–258
Arruda MP, Brown PJ, Lipka AE, Krill A, Thurber C, Kolb F (2015) Genomic selection for predicting Fusarium head blight resistance in a wheat breeding program. Plant Genome 8:1–12
Arruda MP, Lipka AE, Brown PJ, Krill AM, Thurber C, Brown-Guedira G, Dong Y, Foresman BJ, Kolb FL (2016) Comparing genomic selection and marker-assisted selection for Fusarium head blight resistance in wheat (Triticum aestivum L.). Mol Breed 36:84
Arthur JC (1891) Wheat scab. Purdue Univ Agric Exp Sta Bull 36:129–132
Atanasoff D (1920) Fusarium blight (scab) of wheat and other cereals. J Agric Res 20:1–32
Badea A, Eudes F, Graf RJ, Laroche A, Gaudet DA, Sadasivaiah RS (2008) Phenotypic and marker-assisted evaluation of spring and winter wheat germplasm for resistance to Fusarium head blight. Euphytica 164:803–819
Bahrini I, Sugisawa M, Kikuchi R, Ogawa T, Kawahigashi H, Ban T, Handa H (2011) Characterization of a wheat transcription factor, TaWRKY45, and its effect on Fusarium head blight resistance in transgenic wheat plants. Breed Sci 61:121–129
Bai GH, Shaner GE (1996) Variation in Fusarium graminearum and cultivar resistance to wheat scab. Plant Dis 80:975–979
Bai G, Xiao Q, Mei J (1989) Studies on the inheritance of scab resistance in six wheat varieties. Acta Agric Shanghai 5:17–23 (in Chinese)
Bai GH, Desjardins AE, Plattner RD (2002) Deoxynivalenol-nonproducing Fusarium graminearum causes initial infection, but does not cause diseasespread in wheat spikes. Mycopathologia 153:91–98
Bai G, Su Z, Cai J (2018) Wheat resistance to Fusarium head blight. Can J Plant Pathol 40:336–346
Bakhsh A, Mengistu N, Baenziger PS, Dweikat I, Wegulo SN, Rose DJ, Bai GH, Eskridge KM (2013) Effect of Fusarium head blight resistance gene Fhb1 on agronomic and end-use quality traits of hard red winter wheat. Crop Sci 53:793–801
Balconi C, Lanzanova C, Conti E, Triulzi T, Forlani F, Cattaneo M, Lupotto E (2007) Fusarium head blight evaluation in wheat transgenic plants expressing the maize b-32 antifungal gene. Eur J Plant Pathol 117:129–140
Ban T (1997) Evaluation of resistance to Fusarium head blight in indigenous Japanese species of Agropyron (Elymus). Euphytica 97:39–44
Ban T (2003) Comparative genetic analysis of FHB-resistant germplasm for wheat improvement. In: Canty SM, Lewis J, Ward RW (eds) Proceedings of the 2003 National Fusarium head blight forum. Bloomington, MN, pp 215–217
Ban T, Suenaga K (2000) Genetic analysis of resistance to Fusarium head blight caused by Fusarium graminearum in Chinese wheat cultivar Sumai 3 and the Japanese cultivar Saikai 165. Euphytica 113:87–99
Ban T, Kawad N, Yanagisawag A, Takezaki A (2008) Progress and future prospects of resistance breeding to Fusarium head blight in Japan. Cereal Res Commun 36:23–29
Bernardo A, Bai G, Guo P, Xiao K, Guenzi AC, Ayoubi P (2007) Fusarium graminearum-induced changes in gene expression between Fusarium head blight-resistant and susceptible wheat cultivars. Funct Integr Genom 7:69–77
Bernardo A, Bai G, Yu J, Kolb F, Bockus W, Dong Y (2014) Registration of near-isogenic winter wheat germplasm contrasting in for Fusarium head blight resistance. J Plant Reg 8:106–108
Berrocal-Lobo M, Molina A (2014) Ethylene response factor 1 mediates Arabidopsis resistance to the soilborne fungus Fusarium oxysporum. Mol Plant Microbe Interact 17:763–770
Berzonsky WA, Gebhard BL, Gamotin E, Leach GD, Ali S (2007) A reciprocal backcross monosomic analysis of the scab resistant spring wheat (Triticum aestivum L.) cultivar, ‘Frontana’. Plant Breed 126:234–239
Beyer M, Pogoda F, Pallez M, Lazic J, Hoffmann L, Pasquali M (2014) Evidence for a reversible drought induced shift in the species composition of mycotoxin producing Fusarium head blight pathogens isolated from symptomatic wheat heads. Int J Food Microbiol 182–183:51–56
Bilska K, Jurczak S, Kulik T, Ropelewska E, Olszewski J, Żelechowski M, Zapotoczny P (2018) Species composition and trichothecene genotype profiling of Fusarium field isolates recovered from wheat in Poland. Toxins 10:325
Biselli C, Bagnaresi P, Faccioli P, Hu X, Balcerzak M, Mattera MG, Yan Z, Ouellet T, Cattivelli L, Valè G (2018) Comparative transcriptome profiles of near-isogenic hexaploid wheat lines differing for effective alleles at the 2DL FHB resistance QTL. Front Plant Sci 9:37
Boddu J, Cho S, Kruger WM, Muehlbauer GJ (2006) Transcriptome analysis of the barley-Fusarium graminearum interaction. Mol Plant Microbe Interact 19:407–417
Boddu J, Cho S, Muehlbauer GJ (2007) Transcriptome analysis of trichothecene-induced gene expression in barley. Mol Plant Microbe Interact 20:1364–1375
Bollina V, Kumaraswamy KG, Kushalappa AC, Choo TM, Dion Y, Rioux S, Faubert D, Hamzehzarghani H (2010) Mass spectrometry based metabolomics application to identify quantitative resistance related metabolites in barley against Fusarium head blight. Mol Plant Pathol 11:769–782
Bollina V, Kushalappa AC, Choo TM, Dion Y, Rioux S (2011) Identification of metabolites related to mechanisms of resistance in barley against Fusarium graminearum, based on mass spectrometry. Plant Mol Biol 77:355–370
Bonin CM, Kolb FL (2009) Resistance to Fusarium head blight and kernel damage in a winter wheat recombinant inbred line population. Crop Sci 49:1304–1312
Bönnighausen J, Schauer N, Schäfer W, Bormann J (2019) Metabolic profiling of wheat rachis node infection by Fusarium graminearum–decoding deoxynivalenol-dependent susceptibility. New Phytol 221:459–469
Bottalico A, Perrone G (2002) Toxigenic Fusarium species and mycotoxins associated with head blight in small-grain cereals in Europe. Eur J Plant Pathol 108:611–624
Boudsocq M, Willmann MR, McCormack M, Lee H, Shan L, He P, Bush J, Cheng SH, Sheen J (2010) Differential innate immune signaling via Ca2+ sensor protein kinases. Nature 464:418–422
Boutigny A, Ward TJ, Van Coller GJ, Flett B, Lamprecht SC, O’Donnell K, Viljoen A (2011) Analysis of the Fusarium graminearum species complex from wheat, barley and maize in South Africa provides evidence of species-specific differences in host preference. Fungal Genet Biol 48:914–920
Brar GS, Brûlé-Babel A, Ruan YF, Henriquez MA, Pozniak CJ, Kutcher HR, Huci PJ (2019a) Genetic factors affecting Fusarium head blight resistance improvement from introgression of exotic Sumai 3 alleles (including Fhb1, Fhb2, and Fhb5) in hard red spring wheat. BMC Plant Biol 19:179
Brar GS, Karunakaran C, Bond T, Stobbs J, Liu N, Hucl PJ, Kutcher HR (2019b) Showcasing the application of synchrotron-based X-ray computed tomography in host–pathogen interactions: the role of wheat rachilla and rachis nodes in Type-II resistance to Fusarium graminearum. Plant Cell Environ 42:509–526
Brar GS, Pozniak CJ, Kutcher HR, Hucl PJ (2019c) Evaluation of Fusarium head blight resistance genes Fhb1, Fhb2, and Fhb5 introgressed into elite Canadian hard red spring wheats: effect on agronomic and end-use quality traits and implications for breeding. Mol Breed 39:44
Brown NA, Urban M, van de Meene AML, Hammond-Kosack KE (2010) The infection biology of Fusarium graminearum: defining the pathways of spikelet to spikelet colonisation in wheat ears. Fungal Biol 114:555–571
Brown-Guedira G, Griffey C, Kolb F, Mckendry A, Murphy P, van Sanford D (2008) Breeding FHB-resistant soft winter wheat: progress and prospects. Cereal Res Commun 36(Supplement 6):31–35
Buechley G, Shaner GE (1999) Resistance in wheat cultivar Chokwang to Fusarium gramimearum. In: Wagester J, Ward R, Hart OP, Hazen SP, Lewis J, Borden H (eds) 1999 National Fusarium head blight forum proceedings. Sioux Falls, South Dakota, pp 123–126
Buerstmayr H, Lemmens M, Grausgruber H, Ruckenbauer P (1996) Scab resistance of international wheat germplasm. Cereal Res Commun 24:195–202
Buerstmayr H, Lemmens M, Fedak G, Ruckenbauer P (1999) Back-cross reciprocal monosomic analysis of Fusarium head blight resistance in wheat (Triticum aestivum L.). Theor Appl Genet 98:76–85
Buerstmayr H, Stierschneider M, Steiner B, Lemmens M, Griesser M, Nevo E, Fahima T (2003) Variation for resistance to head blight caused by Fusarium graminearum in wild emmer (Triticum dicoccoides) originating from Israel. Euphytica 130:17–23
Buerstmayr H, Ban T, Anderson J (2009) QTL mapping and marker-assisted selection for Fusarium head blight resistance in wheat: a review. Plant Breed 128:1–26
Buerstmayr M, Huber K, Heckmann J, Steiner B, Nelson JC, Buerstmayr H (2012) Mapping of QTL for Fusarium head blight resistance and morphological and developmental traits in three backcross populations derived from Triticum dicoccum × Triticum durum. Theor Appl Genet 125:1751–1765
Buerstmayr M, Alimari A, Steiner B, Buerstmayr H (2013) Genetic mapping of QTL for resistance to Fusarium head blight spread (type 2 resistance) in a Triticum dicoccoides × Triticum durum backcross-derived population. Theor Appl Genet 126:2825–2834
Buerstmayr H, Buerstmayr M, Schweiger W, Steiner B (2014) Breeding for resistance to head blight caused by Fusarium spp. in wheat. CAB Rev 9:007
Buerstmayr M, Steiner B, Wagner C, Schwarz P, Brugger K, Barabaschi D, Volante A, Valè G, Cattivelli L, Buerstmayr H (2018) High-resolution mapping of the pericentromeric region on wheat chromosome arm 5AS harbouring the Fusarium head blight resistance QTL Qfhs.ifa-5A. Plant Biotechnol J 16:1046–1056
Buhrow LM, Cram D, Tulpan D, Foroud NA, Loewen MC (2016) Exogenous abscisic acid and gibberellic acid elicit opposing effects on Fusarium graminearum infection in wheat. Phytopathology 106:986–996
Cai X, Chen PD, Xu SS, Oliver RE, Chen X (2005) Utilization of alien genes to enhance Fusarium head blight resistance in wheat: a review. Euphytica 142:309–318
Cainong JC, Bockus WW, Feng Y, Chen P, Qi L, Sehgal SK, Danilova TV, Koo D-H, Friebe B, Gill BS (2015) Chromosome engineering, mapping, and transferring of resistance to Fusarium head blight disease from Elymus tsukushiensis into wheat. Theor Appl Genet 128:1019–1027
Cativelli M, Lewis S, Appendino ML (2013) A Fusarium head blight resistance quantitative trait locus on chromosome 7D of the spring wheat cultivar Catbird. Crop Sci 53:1464–1471
CCRWS (1984a) Evaluation of wheat varietal germplasm for scab resistance. Zuowu Pinzhong Ziyuan 4:2–7 (in Chinese)
CCRWS (1984b) Studies on Fusarium species infecting wheat spikes in China. J Shanghai Norm Univ (Nat Sci) 3:69–82 (in Chinese)
Chelkowski J (1998) Distribution of Fusarium species and their mycotoxins in cereal grains. In: Sinha KK, Bhatnagar D (eds) Mycotoxins in agriculture and food safety. Marcel Dekker Inc, New York, pp 63–82
Chen P, Liu D (2000) Transfer scab resistance from Leymus racemosus, Roegneria ciliaris, and Roegneria kamoji into common wheat. In: Raupp WJ, Ma Z, Chen P, Liu D (eds) International symposium on wheat improvement for scab resistance. KSU Printing Service, Suzhou, pp 62–67
Chen P, Wang Z, Wang S, Huang L, Wang Y, Liu D (1995) Transfer of useful germplasm from Leymus racemosus Lam. to common wheat. III. Development of addition lines with wheat scab resistance. Acta Genet Sin 22:206–210 (in Chinese)
Chen LF, Bai GH, Desjardins AE (2000a) Recent advances in wheat head scab research in China. An abridged version of a paper prepared for National Agricultural Library, USDA, USA. In: Raupp WJ, Ma Z, Chen P, Liu D (eds) International symposium on wheat improvement for scab resistance. KSU Printing Service, Suzhou, pp 258–273
Chen J, Griffey CA, Pridgen T, Chappell M, Shaw J (2000b) Assessment and rational utilization of scab resistance sources in the Virginia Wheat Breeding Program. In: Raupp WJ, Ma Z, Chen P, Liu D (eds) International symposium on wheat improvement for scab resistance. KSU Printing Service, Suzhou, pp 10–17
Chen X, Steed A, Travella S, Keller B, Nicholson P (2009) Fusarium graminearum exploits ethylene signalling to colonize dicotyledonous and monocotyledonous plants. New Phytol 182:975–983
Chen J, Griffey CA, Liu S, Saghai Maroof MA, Paul Murphy J, Navarro RA, Sneller CH, Brown-Guedira G, Souza EJ (2012a) Registration of Fusarium head blight–resistant soft red winter wheat germplasm VA04W-433 and VA04W-474. J Plant Reg 6:111
Chen S, Huang Z, Zhang Y, Ge J, Zhu X, Gao Y, Chen J (2012b) Chromosomal location of the genes associated with FHB resistance of Lophopyrum elongatum in Chinese Spring background. J Triticeae Crops 32:839–845 (in Chinese)
Chen W, Kastner C, Nowara D, Oliveira-Garcia E, Rutten T, Zhao Y, Deising HB, Kumlehn J, Schweizer P (2016) Host-induced silencing of Fusarium culmorum genes protects wheat from infection. J Exp Bot 67:4979–4991
Cheng H, Lu J (1962) Conditions for perithecial production of wheat Fusarium graminearum. J Plant Prot 1:440–441 (in Chinese)
Cheng W, Li H, Zhang J, Du H, Wei Q, Huang T, Yang P, Kong X, Liao Y (2015a) Tissue-specific and pathogen-inducible expression of a fusion protein containing a Fusarium-specific antibody and a fungal chitinase protects wheat against Fusarium pathogens and mycotoxins. Plant Biotechnol J 13:664–674
Cheng W, Song XS, Li HP, Cao LH, Sun K, Qiu XL, Xu YB, Yang P, Huang T, Zhang JB, Qu B, Liao YC (2015b) Host-induced gene silencing of an essential chitin synthase gene confers durable resistance to Fusarium head blight and seedling blight in wheat. Plant Biotechnol J 13:1335–1345
Chester FD (1890) The scab of the wheat. Del Agric Exp Sta Rep 3:89–90
Chou Y (1952) Wheat scab. Zhonghua Book Company, Shanghai
Christensen JJ, Stakman EC (1927) Susceptibility of wheat varieties and hybrids to wheat scab in Minnesota. Phytopathology 17:40–41
Chrpová J, Šíp V, Štočková L, Milec Z, Bobkova L (2010) Resistance of winter wheat varieties registered in the Czech Republic to Fusarium head blight in relation to the presence of specific Rht alleles. Czech J Genet Plant 46:122–134
Chrpová J, Šíp V, Štočková L, Dumalasová V (2012) Evaluation of Fusarium head blight resistance in wheat under high infection pressure in field conditions. Cereal Res Commun 40:396–404
Chu VM (1937) Diseases of wheat, barley and oats: how to control them. J Agric Assoc China 156:1–46 (in Chinese)
Comeau A, Langevin F, Caetano VR, Haber S, Savard ME, Voldeng H, Fedak G, Dion Y, Rioux S, Gilbert J, Martin RA, Eudes F, Scheeren PL (2011) A different path to the summit of Fusarium head blight resistance in wheat: developing germplasm with a systemic approach. Plant Breed Seed Sci 63:39–48
Costa JM, Bockelman HE, Brown-Guedira G, Cambron SE, Chen X, Cooper A, Cowger C, Dong Y, Grybauskas A, Jin Y, Kolmer J, Paul Murphy J, Sneller C, Souza E (2015) Registration of the soft red winter wheat germplasm MD01W233-06-1 resistant to Fusarium head blight. J Plant Reg 4:255–260
Cuperlovic-Culf M, Wang L, Forseille L, Boyle K, Merkley N, Burton I, Fobert PR (2016) Metabolic biomarker panels of response to Fusarium head blight infection in different wheat varieties. PLoS ONE 11:e0153642
Cuthbert PA, Somers DJ, Thomas J, Cloutier S, Brulé-Babel A (2006) Fine mapping Fhb1, a major gene controlling fusarium head blight resistance in bread wheat (Triticum aestivum L.). Theor Appl Genet 112:1465–1472
Cuthbert PA, Somers DJ, Brulé-Babel A (2007) Mapping of Fhb2 on chromosome 6BS: a gene controlling Fusarium head blight field resistance in bread wheat (Triticum aestivum L.). Theor Appl Genet 114:429–437
Cuzick A, Lee S, Gezan S, Hammond-Kosack KE (2008) NPR1 and EDS11 contribute to host resistance against Fusarium culmorum in Arabidopsis buds and flowers. Mol Plant Pathol 9:697–704
Dai SE (1941) Problems related to breeding for scab resistance of wheat varieties. Agric Rep 6:616–625 (in Chinese)
de Jong CF, Laxalt AM, Bargmann BO, de Wit PJ, Joosten MH, Munnik T (2004) Phosphatidic acid accumulation is an early response in the Cf-4/Avr4 interaction. Plant J 39:1–12
Dhokane D, Karre S, Kushalappa AC, McCartney C (2016) Integrated metabolo-transcriptomics reveals Fusarium head blight resistance genes in wheat QTL-Fhb2. PLoS ONE 11:e0155851
Di R, Blechl A, Dill-Macky R, Tortora A, Tumer NE (2010) Expression of a truncated form of yeast ribosomal protein L3 in transgenic wheat improves resistance to Fusarium head blight. Plant Sci 178:374–380
Dickson JG (1942) Scab of wheat and barley and its control. USDA Farmer Bull 1599:1–22
Dickson JG, Johann H, Wineland G (1921) Second progress report on the Fusarium blight (scab) of wheat. Phytopathology 11:35
Dill-Macky R, Jones RK (2000) The effect of previous crop residues and tillage on Fusarium head blight of wheat. Plant Dis 84:71–76
Ding L, Xu H, Yi H, Yang L, Kong Z, Zhang L, Xue S, Jia H, Ma Z (2011) Resistance to hemi-biotrophic F. graminearum infection is associated with coordinated and ordered expression of diverse defense signaling pathways. PLoS ONE 6:e19008
Dixon RA, Achnine L, Kota C, Liu C, Redy MSS, Wang L (2002) The phenylpropanoid pathway and plant defense—a genomics perspective. Mol Plant Pathol 3:371–390
Dong H, Wang R, Yuan Y, Anderson J, Pumphrey M, Zhang Z, Chen J (2018) Evaluation of the potential for genomic selection to improve spring wheat resistance to Fusarium head blight in the Pacific Northwest. Front Plant Sci 9:911
Draeger R, Gosman N, Steed A, Chandler E, Thomsett M, Srinivasachary Schondelmaier J, Buerstmayr H, Lemmens M, Schmolke M, Mesterhazy A, Nicholson P (2007) Identification of QTLs for resistance to Fusarium head blight, DON accumulation and associated traits in the winter wheat variety Arina. Theor Appl Genet 115:617–625
Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209
Eldakak M, Das A, Zhuang Y, Rohila JS, Glover K, Yen Y (2018) A quantitative proteomics view on the function of Qfhb1, a major QTL for Fusarium head blight resistance in wheat. Pathogens 7:58
Elias EM, Manthey FA, Stack RW, Kianian SF (2005) Breeding efforts to develop Fusarium head blight resistant durum wheat in North Dakota. In: Canty SM, Boring T, Wardwell J, Siler L, Ward RW (eds) Proceedings of the 2005 National Fusarium Head Blight Forum. Milwaukee, Wisconsin, pp 25–26
Erayman M, Turktas M, Akdogan G, Gurkok T, Inal B, Ishakoglu E, Ilhan E, Unver T (2015) Transcriptome analysis of wheat inoculated with Fusarium graminearum. Front Plant Sci 6:867
Fedak G (2000) Sources of resistance to Fusarium head blight. In: Raupp WJ, Ma Z, Chen P, Liu D (eds) International symposium on wheat improvement for scab resistance. KSU Printing Service, Suzhou, p 4
Ferrari S, Plotnikova JM, De Lorenzo G, Ausubel FM (2003) Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. Plant J 35:193–205
Ferrari S, Sella L, Janni M, De Lorenzo G, Favaron F, D’Ovidio R (2012) Transgenic expression of polygalacturonase-inhibiting proteins in Arabidopsis and wheat increases resistance to the flower pathogen Fusarium graminearum. Plant Biol 14:31–38
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 Pathol 61:296–314
Frohberg RC, Stack RW, Olson T, Miller JD, Megoum M (2006) Registration of ‘Alsen’ wheat. Crop Sci 46:2311–2312
Fu S, Lv Z, Qi B, Guo X, Li J, Liu B, Han F (2012) Molecular cytogenetic characterization of wheat–Thinopyrum elongatum addition, substitution and translocation lines with a novel source of resistance to wheat Fusarium head blight. J Genet Genomics 39:103–110
Gagkaeva TY (2003) Importance of Fusarium head blight in Russia and the search for new sources of genetic resistance in wheat and barley. In: Canty SM, Lewis J, Ward RW (eds) Proceeding of the National Fusarium head blight forum. Bloomington, MN, pp 219–222
Gagkaeva T, Gavrilova OP, Yli-Mattila T, Loskutov IG (2013) Sources of resistance to Fusarium head blight in VIR oat collection. Euphytica 191(3):355–364
Gatti M, Cambon F, Tassy C, Macadre C, Guerard F, Langin T, Dufresne M (2019) The Brachypodium distachyon UGT Bradi5gUGT03300 confers type II Fusarium head blight resistance in wheat. Plant Pathol 68:334–343
Ghavami F, Elias EM, Mamidi S, Ansari O, Sargolzaei M, Adhikari T, Mergoum M, Kianian SF (2011) Mixed model association mapping for Fusarium head blight resistance in Tunisian-derived durum wheat populations. G3(1):209–218
Gilbert J, Tekauz A (2000) Review: recent developments in research on Fusarium head blight of wheat in Canada. Canadian J Plant Pathol 22:1–8
Gilchrist L, Rajaram S, Mujeeb-Kazi A, Van Ginkel M, Vivar H, Pfeiffer W (1997) Fusarium scab screening program at CIMMYT. In: Dubin HJ, Gilchrist L, Reeves J, McNab A (eds) Fusarium head scab: global status and future prospects. CIMMYT, Mexico, pp 7–12
Gilchrist L, Velazquez C, Mujeeb-Kazi A (1999) Resistance to Fusarium head blight in synthetic hexaploidy wheats (2n = 6x = 42, AABBDD). In: Wagester JA, Ward R, Hart LP, Hazen SP, Lewis J, Borden H (eds) Proceedings of the National Fusarium head blight forum. Sioux Falls, SD, pp 162–164
Gladysz C, Lemmens M, Steiner B, Buerstmayr H (2007) Evaluation and genetic mapping of resistance to Fusarium head blight in Triticum dicoccoides. Isr J Plant Sci 55:263–266
Glover KD, Rudd JC, Devkota RN, Hall RG, Jin Y, Osborne LE, Ingemansen JA, Rickertsen JR, Baltensperger DD, Hareland GA (2010) Registration of ‘brick’ wheat. J Plant Reg 4:22–27
Gocho H (1985) Wheat breeding for scab resistance. Wheat Inf Serv 60:41
Golkari S, Gilbert J, Prashar S, Procunier JD (2007) Microarray analysis of Fusarium graminearum-induced wheat genes: identification of organ-specific and differentially expressed genes. Plant Biotechnol J 5:38–49
Golkari S, Gilbert J, Ban T, Procunier DJ (2009) QTL-specific microarray gene expression analysis of wheat resistance to Fusarium head blight in Sumai-3 and two susceptible NILs. Genome 52:409–418
Gooding RW, Lafever HN, Campbell KG, Herald LD (1997) Registration of ‘Freedom’ wheat. Crop Sci 37:1007
Gordon CS, Rajagopalan N, Risseeuw EP, Surpin M, Ball FJ, Barber CJ, Buhrow LM, Clark SM, Page JE, Todd CD, Abrams SR, Loewen MC (2016) Characterization of Triticum aestivum abscisic acid receptors and a possible role for these in mediating Fusairum head blight susceptibility in wheat. PLoS ONE 11:e0164996
Goswami RS, Kistler HC (2004) Heading for disaster: Fusarium graminearum on cereal crops. Mol Plant Pathol 5(6):515–525
Gottwald S, Samans B, Lueck 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 Genom 13:369
Gräfenhan T, Johnston PR, Vaughan MM, McCormick SP, Proctor RH, Busman M, Ward TJ, O’Donnell K (2016) Fusarium praegraminearum sp. nov., a novel nivalenol mycotoxin-producing pathogen from New Zealand can induce head blight on wheat. Mycologia 108:1229–1239
Grausgruber H, Lemmens M, Bürstmayr H, Ruckenbauer P (1998) Chromosomal location of Fusarium head blight resistance and in vitro toxin tolerance in wheat using the Hobbit ‘sib’ (Triticum macha) chromosome substitution lines. J Genet Breed 7(2):73–80
Griffey CA, Starling TM, Price AM, Sisson WL, Das MK, Pridgen TH, Vaughn ME, Rohrer WL, Brann DE (2001) Registration of ‘Roane’ wheat registration by CSSA. Crop Sci 41:1359–1360
Gu J (1983) A study on the genetics of resistance to wheat scab. Sci Agric Sin 6:61–64
Gunnaiah R, Kushalappa AC (2014) Metabolomics deciphers the host resistance mechanisms in wheat cultivar Sumai-3, against trichothecene producing and non-producing isolates of Fusarium graminearum. Plant Physiol Biochem 83:40–50
Gunnaiah R, Kushalappa AC, Duggavathi R, Fox S, Somers DJ (2012) Integrated metabolo-proteomic approach to decipher the mechanisms by which wheat QTL (Fhb1) contributes to resistance against Fusarium graminearum. PLoS ONE 7:e40695
Guo J, Zhang X, Hou Y, Cai J, Shen X, Zhou T, Xu H, Ohm HW, Wang H, Li A, Han F, Wang H, Kong L (2015) High-density mapping of the major FHB resistance gene Fhb7 derived from Thinopyrum ponticum and its pyramiding with Fhb1 by marker-assisted selection. Theor Appl Genet 128:2301–2316
Hamzehzarghani H, Kushalappa AC, Dion Y, Rioux S, Comeau A, Yaylayan V, Marshall WD, Mather DE (2005) Metabolic profiling and factor analysis to discriminate quantitative resistance in wheat cultivars against fusarium head blight. Physiol Mol Plant Pathol 66:119–133
Hamzehzarghani H, Paranidharan V, Abu-Nada Y, Kushalappa AC, Dion Y, Rioux S, Comeau A, Yaylayan V, Marshall WD (2008a) Metabolite profiling coupled with statistical analyses for potential high-throughput screening of quantitative resistance to Fusarium head blight in wheat. Can J Plant Path 30:24–36
Hamzehzarghani H, Paranidharan V, Abu-Nada Y, Kushalappa AC, Mamer O, Somers D (2008b) Metabolic profiling to discriminate wheat near isogenic lines, with quantitative trait loci at chromosome 2DL, varying in resistance to Fusarium head blight. Can J Plant Sci 88:789–797
Han J, Lakshman DK, Galvez LC, Mitra S, Baenziger PS, Mitra A (2012) Transgenic expression of lactoferrin imparts enhanced resistance to head blight of wheat caused by Fusarium graminearum. BMC Plant Biol 12:33
Hanson EW, Ausemus ER, Stakman EC (1950) Varietal resistance of spring wheats to Fusarium head blight. Phytopathology 40:902–914
Hao Q, Wang W, Han X, Wu J, Lyu B, Chen F, Caplan A, Li C, Wu J, Wang W, Xu Q, Fu D (2018) Isochorismate-based salicylic acid biosynthesis confers basal resistance to Fusarium graminearum in barley. Mol Plant Pathol 19:1995–2010
Hayes HK (1923) Inheritance of kernel and spike characters in crosses between varieties of Triticum vulgare. Univ Minn Stud Biol Sci 4:163–183
He ZH, van Ginkel M, Gilchrist L, Rajaram S (2000) Progress of China/CIMMYT shuttle breeding and germplasm exchange aimed at combining high yield potential with scab resistance. In: Proceedings of the National Fusarium head blight forum, Cincinnati, USA, pp 264–268
He X, Singh PK, Duveiller E, Schlang N, Dreisigacker S, Singh RP (2013a) Identification and characterization of international Fusarium head blight screening nurseries of wheat at CIMMYT, Mexico. Eur J Plant Pathol 136:123–134
He X, Singh PK, Duveiller E, Dreisigacker S, Singh RP (2013b) Development and characterization of International Maize and Wheat Improvement Center (CIMMYT) germplasm for Fusarium head blight resistance. In: Alconada Magliano T, Chulze S (eds) Fusarium head blight in Latin America. Springer, Dordrecht, pp 241–262
He F, Pasam R, Shi F, Kant S, Keeble-Gagnere G, Kay P, Forrest K, Fritz A, Hucl P, Wiebe K, Knox R, Cuthbert R, Pozniak C, Akhunova A, Morrell PL, Davies JP, Webb SR, Spangenberg G, Hayes B, Daetwyler H, Tibbits J, Hayden M, Akhunov E (2019) Exome sequencing highlights the role of wild-relative introgression in shaping the adaptive landscape of the wheat genome. Nat Genet 51:896–904
Hoffer GN, Johnson AG, Atanasoff D (1918) Corn root rot and wheat scab. J Agric Res 14:611–612
Hoffstetter A, Cabrera A, Huang M, Sneller C (2016) Optimizing training population data and validation of genomic selection for economic traits in soft winter wheat. G3 6:2919–2928
Hofstad AN, Nussbaumer T, Akhunov E, Shin S, Kugler KG, Kistler HC, Mayer KF, Muehlbauer GJ (2016) Examining the transcriptional response in wheat Fhb1 near-isogenic lines to infection and deoxynivalenol treatment. Plant Genome. https://doi.org/10.3835/plantgenome2015.05.0032
Hou W, Mu J, Li A, Wang H, Kong L (2015) Identification of a wheat polygalacturonase-inhibiting protein involved in Fusarium head blight resistance. Eur J Plant Pathol 141:731–745
Hsia YT, Hsiao CP, Gao CX (1956) The development of Gibberella zeae head blight of wheat, I. Relations of development and dissemination of spores and amount of rainfall to epiphytotics. Acta Phytopathol Sin 2:187–202
Huang C, Jiang YY, Wu JW, Qu K, Yang YJ (2019) Occurrence characteristics and reason analysis of wheat head blight in 2018 in China. Plant Prot 45:160–163 (in Chinese)
Huhn MR, Elias EM, Ghavami F, Kianian SF, Chao S, Zhong S, Alamri MS, Yahyaoui A, Mergoum M (2012) Tetraploid Tunisian wheat germplasm as a new source of Fusarium head blight resistance. Crop Sci 52:136–145
Igawa T, Ochiai-Fukuda T, Takahashi-Ando N, Ohsato S, Shibata T, Yamaguchi I, Kimura M (2004) New TAXI-type xylanase inhibitor genes are inducible by pathogens and wounding in hexaploid wheat. Plant Cell Physiol 45:1347–1360
Imathiu SM, Edwards SG, Ray RV, Back M (2014) Artificial inoculum and inoculation techniques commonly used in the investigation of Fusarium head blight in cereals. Acta Phytopathol Entomol Hung 49:129–139
Ittu M, Ittu G, Săulescu NN (1996) Screening for Fusarium scab resistance in triticale. In: Guedes-Pinto H, Darvey N, Carnide VP (eds) Triticale: today and tomorrow. Springer, Dordrecht, pp 527–533
Ittu M, Saulescu NN, Ittu G (1997) Breeding wheat for resistance to Fusarium head blight in Romania. In: Altay F, Kronstad WE, Beniwal SPS, Mcnab A, Braun HJ (eds) Wheat: prospects for global improvement. Springer, Dordrecht, pp 87–92
IWGSC (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361:eaar7191
Jansen C, von Wettstein D, Schäfer W, Kogel KH, Felk A, Maier FJ (2005) Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum. Proc Natl Acad Sci USA 102:16892–16897
Jennings P, Coates ME, Walsh K, Turner JA, Nicholson P (2004) Determination of deoxynivalenol- and nivalenol-producing chemotypes of Fusarium graminearum isolated from wheat crops in England and Wales. Plant Pathol 53:643–652
Jia H, Cho S, Muehlbauer GJ (2009) Transcriptome analysis of a wheat near-isogenic line pair carrying Fusarium head blight-resistant and -susceptible alleles. Mol Plant Microbe Interact 22:1366–1378
Jia HY, Zhou JY, Xue SL, Li GQ, Yan HS, Ran CF, Zhang YD, Shi JX, Jia L, Wang X, Luo J, Ma ZQ (2018) A journey to understand wheat Fusarium head blight resistance in the Chinese wheat Wangshuibai. Crop J 6:48–59
Jia LJ, Tang HY, Wang WQ, Yuan TL, Wei WQ, Pang B, Gong XM, Wang SF, Li YJ, Zhang D, Liu W, Tang WH (2019) A linear nonribosomal octapeptide from Fusarium graminearum facilitates cell-to-cell invasion of wheat. Nat Commun 10:922
Jiang GL, Dong Y, Shi J, Ward RW (2007) QTL analysis of resistance to Fusarium head blight in the novel wheat germplasm CJ 9306. II. Resistance to deoxynivalenol accumulation and grain yield loss. Theor Appl Genet 115:1043–1052
Jiang Y, Zhao Y, Rodemann B, Plieske J, Kollers S, Korzun V, Ebmeyer E, Argillier O, Hinze M, Ling J, Roder MS, Ganal MW, Mette MF, Reif JC (2015) Potential and limits to unravel the genetic architecture and predict the variation of Fusarium head blight resistance in European winter wheat (Triticum aestivum L.). Heredity 114:318–326
Jiang C, Cao S, Wang Z, Xu H, Liang J, Liu H, Wang G, Ding M, Wang Q, Gong C, Feng C, Hao C, Xu JR (2019) An expanded subfamily of G-protein-coupled receptor genes in Fusarium graminearum required for wheat infection. Nat Microbiol 4:1582–1591
Jin F, Zhang D, Bockus W, Baenziger PS, Carver B, Bai G (2013) Fusarium head blight resistance in US winter wheat cultivars and elite breeding lines. Crop Sci 53:2006–2013
Jin F, Bai G, Zhang D, Dong Y, Ma L, Bockus W, Dowell F (2014) Fusarium-damaged kernels and deoxynivalenol in Fusarium-infected US winter wheat. Phytopathology 104:472–478
Kage U, Karre S, Kushalappa AC, McCartney C (2017a) Identification and characterization of a Fusarium head blight resistance gene TaACT in wheat QTL-2DL. Plant Biotechnol J 15(4):447–457
Kage U, Yogendra KN, Kushalappa AC (2017b) TaWRKY70 transcription factor in wheat QTL-2DL regulates downstream metabolite biosynthetic genes to resist Fusarium graminearum infection spread within spike. Sci Rep 7:42596
Karasov TL, Chae E, Herman JJ, Bergelson J (2017) Mechanisms to mitigate the trade-off between growth and defense. Plant Cell 29:666–680
Karre S, Kumar A, Dhokane D, Kushalappa AC (2017) Metabolo-transcriptome profiling of barley reveals induction of chitin elicitor receptor kinase gene (HvCERK1) conferring resistance against Fusarium graminearum. Plant Mol Biol 93:247–267
Kazan K, Gardiner DM (2018) Transcriptomics of cereal-Fusarium graminearum interactions: what we have learned so far. Mol Plant Pathol 19:764–778
Kheiri A, Moosawi Jorf SA, Malihipour A (2019) Infection process and wheat response to Fusarium head blight caused by Fusarium graminearum. Eur J Plant Pathol 153:489–502
Kinkema M, Fan W, Dong X (2000) Nuclear localization of NPR1 is required for activation of PR gene expression. Plant Cell 12:2339–2350
Koch A, Kumar N, Weber L, Keller H, Imani J, Kogel KH (2013) Host-induced gene silencing of cytochrome P450 lanosterol C14α-demethylase-encoding genes confers strong resistance to Fusarium species. Proc Natl Acad Sci USA 10:19324–19329
Kohli MM, de Ackermann MD (2013) Resistance to Fusarium head blight in South American wheat germplasm. In: Alconada Magliano TM, Chulze SN (eds) Fusarium head blight in Latin America. Springer, Dordrecht, pp 263–297
Kolb FL, Bai GH, Muehlbauer GJ, Anderson JA, Smith KP, Fedak G (2001) Host plant resistance genes for Fusarium head blight: mapping and manipulation with molecular markers. Crop Sci 41:611–619
Kollers S, Rodemann B, Ling J, Korzun V, Ebmeyer E, Argillier O, Hinze M, Plieske J, Kulosa D, Ganal MW, Röder MS (2013) Whole genome association mapping of Fusarium head blight resistance in European winter wheat (Triticum aestivum L.). PLoS ONE 8:e57500
Kong L, Anderson JM, Ohm HW (2005) Induction of wheat defense and stress-related genes in response to Fusarium graminearum. Genome 48:29–40
Kong L, Ohm HW, Anderson JM (2007) Expression analysis of defense related genes in wheat in response to infection by Fusarium graminearum. Genome 50:1038–1048
Kopahnke D, Miedaner T, Brunsbach G, Lind V, Schliephake E, Ordon F (2008) Screening of Triticum monococcum and T. dicoccum for resistance to Fusarium culmorum. Cereal Res Commun 36:109–111
Kosaka A, Manickavelu A, Kajihara D, Nakagawa H, Ban T (2015) Altered gene expression profiles of wheat genotypes against Fusarium head blight. Toxins 7:604–620
Kosova K, Chrpova J, Sip V (2009) Cereal resistance to Fusarium head blight and possibilities of its improvement through breeding. Czech J Genet Plant 45:87–105
Kruger WM, Pritsch C, Chao S, Muehlbauer GJ (2002) Functional and comparative bioinformatic analysis of expressed genes from wheat spikes infected with Fusarium graminearum. Mol Plant Microbe Interact 15:445–455
Kubo K, Kawada N, Nakajima T, Hirayae K, Fujita M (2014) Field evaluation of resistance to kernel infection and mycotoxin accumulation caused by Fusarium head blight in western Japanese wheat (Triticum aestivum L.) cultivars. Euphytica 200:81–93
Kugler KG, Siegwart G, Nussbaumer T, Ametz C, Spannagl M, Steiner B, Lemmens M, Mayer KF, Buerstmayr H, Schweiger W (2013) Quantitative trait loci-dependent analysis of a gene co-expression network associated with Fusarium head blight resistance in bread wheat (Triticum aestivum L.). BMC Genom 14:728
Kumar S, Stack RW, Friesen TL, Faris JD (2007) Identification of a novel Fusarium head blight resistance quantitative trait locus on chromosome 7A in tetraploid wheat. Phytopathology 97:592–597
Kumaraswamy KG, Kushalappa AC, Choo TM, Dion Y, Rioux S (2011) Mass spectrometry based metabolomics to identify potential biomarkers for resistance in barley against Fusarium head blight (Fusarium graminearum). J Chem Ecol 37:846–856
Leon-Reyes A, Du Y, Koornneef A, Proietti S, Körbes AP, Memelink J, Pieterse CM, Ritsema T (2010) Ethylene signaling renders the jasmonate response of Arabidopsis insensitive to future suppression by salicylic acid. Mol Plant Microbe Interact 23:187–197
Li QX, Wang ZM (1982) Identification of pathogenicity of Fusarium graminearum Schw. Acta Phytopathol Sin 9:163–168 (in Chinese)
Li G, Yen Y (2008) Jasmonate and ethylene signaling pathway may mediate Fusarium head blight resistance in wheat. Crop Sci 48:1888–1896
Li Y, Yu Y (1988) Monosomic analysis for scab resistance index in wheat cultivar “WZHHS”. J Huazhong Agric Univ 7:327–331 (in Chinese)
Li WL, Faris JD, Muthukrishnan S, Liu DJ, Chen PD, Gill BS (2001) Isolation and characterization of novel cDNA clones of acidic chitinases and β-1,3-glucanases from wheat spikes infected by Fusarium graminearum. Theor Appl Genet 102:353–362
Li J, Brader G, Palva ET (2004) The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 16:319–331
Li HP, Zhang JB, Shi RP, Huang T, Fischer R, Liao YC (2008a) Engineering Fusarium head blight resistance in wheat by expression of a fusion protein containing a Fusarium-specific antibody and an antifungal peptide. Mol Plant Microbe Interact 21:1242–1248
Li CJ, Zhu HL, Zhang CQ, Lin F, Xue SL, Cao Y, Zhang ZZ, Zhang LX, Ma ZQ (2008b) Mapping QTLs associated with Fusarium-damaged kernels in the Nanda 2419 × Wangshuibai population. Euphytica 163:185–191
Li T, Bai G, Wu S, Gu S (2011a) Quantitative trait loci for resistance to Fusarium head blight in a Chinese wheat landrace Haiyanzhong. Theor Appl Genet 122:1497–1502
Li Z, Zhou M, Zhang Z, Ren L, Du L, Zhang B, Xu H, Xin Z (2011b) Expression of a radish defensin in transgenic wheat confers increased resistance to Fusarium graminearum and Rhizoctonia cerealis. Funct Integr Genom 11:63–70
Li X, Shin S, Heinen S, Dill-Macky R, Berthiller F, Nersesian N, Clemente T, McCormick S, Muehlbauer GJ (2015) Transgenic wheat expressing a barley UDP-glucosyltransferase detoxifies deoxynivalenol and provides high levels of resistance to Fusarium graminearum. Mol Plant Microbe Interact 28:1237–1246
Li X, Michlmayr H, Schweiger W, Malachova A, Shin S, Huang Y, Dong Y, Wiesenberger G, McCormick S, Lemmens M, Fruhmann P, Hametner C, Berthiller F, Adam G, Muehlbauer GJ (2017) A barley UDP-glucosyltransferase inactivates nivalenol and provides Fusarium head blight resistance in transgenic wheat. J Exp Bot 68:2187–2197
Li GQ, Jia L, Zhou JY, Fan JC, Yan HS, Shi JX, Wang X, Fan M, Xue SL, Cao SY, Tian SS, Jia HY, Ma ZQ (2019a) Evaluation and precise mapping of QFhb.nau-2B conferring resistance against Fusarium infection and spread within spikes in wheat (Triticum aestivum L.). Mol Breed 39:62
Li GQ, Zhou JY, Jia HY, Gao ZX, Fan M, Luo YJ, Zhao PT, Xue SL, Li N, Yuan Y, Ma SW, Kong ZX, Jia L, An X, Jiang G, Liu WX, Cao WJ, Zhang RR, Fan JC, Xu XW, Liu YF, Kong QQ, Zheng SH, Wang Y, Qin B, Cao SY, Ding YX, Shi JX, Yan HS, Wang X, Ran CF, Ma ZQ (2019b) Mutation of a histidine-rich calcium-binding protein gene in wheat confers resistance to Fusarium head blight. Nat Genet 51:1106–1112
Liao Y, Yu Y (1985) Genetic analysis of scab resistance in the local wheat variety Wangshuibai. J Huazhong Agric Coll 4:6–14 (in Chinese)
Lin YB, Yang ZP, Wu ZS (1992) Genetic analysis of resistance to scab in wheat varieties from different regions. Acta Agric Shanghai 8:31–36 (in Chinese)
Lin F, Kong ZX, Zhu HL, Xue SL, Wu JZ, Tian DG, Wei JB, Zhang CQ, Ma ZQ (2004) Mapping QTL associated with resistance to Fusarium head blight in the Nanda2419 × Wangshuibai population. I. Type II resistance. Theor Appl Genet 109:1504–1511
Lin F, Xue SL, Zhang ZZ, Zhang CQ, Kong ZX, Yao GQ, Tian DG, Zhu HL, Li CJ, Cao Y, Wei JB, Luo QY, Ma ZQ (2006) Mapping QTL associated with resistance to Fusarium head blight in the Nanda2419 × Wangshuibai population. II: Type I resistance. Theor Appl Genet 112:528–535
Lionetti V, Giancaspro A, Fabri E, Giove SL, Reem N, Zabotina OA, Blanco A, Gadaleta A, Bellincampi D (2015) Cell wall traits as potential resources to improve resistance of durum wheat against Fusarium graminearum. BMC Plant Biol 15:6
Liu Z, Wang Z, Zhao W (1985) A study on scab resistance of wheat germplasm resources. Acta Agric Shanghai 1:75–84 (in Chinese)
Liu Z, Wang Z, Zhao W, Huang D, Huang X, Sun X (1992) Sources of scab resistance in improved wheat varieties and problems in attaining improved scab resistance in China. Sci Agr Sin 25:47–52 (in Chinese)
Liu S, Wu S, Li S, Fang Y, Xu W (1998) Studies on the breeding for transgressive resistance to scab in wheat. Sci Agric Sin 1:40–45 (in Chinese)
Liu S, Zhang X, Pumphrey MO, Stack RW, Gill BS, Anderson JA (2006) Complex microcolinearity among wheat, rice, and barley revealed by fine mapping of the genomic region harboring a major QTL for resistance to Fusarium head blight in wheat. Funct Integr Genom 6:83–89
Liu S, Pumphrey MO, Gill BS, Trick HN, Zhang JX, Dolezel J, Chalhoub B, Anderson JA (2008) Toward positional cloning of Fhb1, a major QTL for Fusarium head blight resistance in wheat. Cereal Res Commun 36:195–201
Liu W, Liu Z, Huang C, Lu M, Liu J, Yang Q (2016) Statistics and analysis of crop yield losses caused by main diseases and insect pests in recent 10 years. Plant Prot 42:1–9 (in Chinese)
Liu YY, Sun HY, Li W, Xia YL, Deng YY, Zhang AX, Chen HG (2017) Fitness of three chemotypes of Fusarium graminearum species complex in major winter wheat-producing areas of China. PLoS ONE 12:e0174040
Long X, Balcerzak M, Gulden S, Cao W, Fedak G, Wei Y, Zheng Y, Somers D, Ouellet T (2015) Expression profiling identifies differentially expressed genes associated with the Fusarium head blight resistance QTL 2DL from the wheat variety Wuhan-1. Physiol Mol Plant Pathol 90:1–11
Lorenzo O, Piqueras R, Sánchez-Serrano JJ, Solano R (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15:165–178
Lu W, Cheng S, Wang Y (2001) Studies of wheat scab. China Science Publishing and Media Ltd., Beijing (in Chinese)
Luo S, Yang T (1982) A discussion of wheat breeding for FHB resistance improvement. Zhejiang Agric Sci 6:291–294 (in Chinese)
Ma LJ, Geiser DM, Proctor RH, Rooney AP, O’Donnell K, Trail F, Gardiner DM, Manners JM, Kazan K (2013) Fusarium pathogenomics. Annu Rev Microbiol 67:399–416
Ma X, Du X, Liu G, Yang Z, Hou W, Wang H, Feng D, Li A, Kong L (2015) Cloning and characterization of a novel UDP-glycosyltransferase gene induced by DON from wheat. J Integr Agric 14:830–838
Machado AK, Brown NA, Urban M, Kanyuka K, Hammond-Kosack KE (2018) RNAi as an emerging approach to control Fusarium head blight disease and mycotoxin contamination in cereals. Pest Manag Sci 74:790–799
MacInnes J, Fogelman R (1923) Wheat scab in Minnesota. Univ Minn Agric Exp Sta Tech Bull 18:1–43
Mackintosh CA, Lewis J, Radmer LE, Shin S, Heinen SJ, Smith LA, Wyckoff MN, Dill-Macky R, Evans CK, Kravchenko S, Baldridge GD, Zeyen RJ, Muehlbauer GJ (2007) Overexpression of defense response genes in transgenic wheat enhances resistance to Fusarium head blight. Plant Cell Rep 26:479–488
Maiorano A, Blandino M, Reyneri A, Vanara F (2008) Effects of maize residues on the Fusarium spp. infection and deoxynivalenol (DON) contamination of wheat grain. Crop Prot 27:182–188
Makandar R, Essig JS, Schapaugh MA, Trick HN, Shah J (2006) Genetically engineered resistance to Fusarium head blight in wheat by expression of Arabidopsis NPR1. Mol Plant Microbe Interact 19:123–129
Makandar R, Nalam V, Chaturvedi R, Jeannotte R, Sparks AA, Shah J (2010) Involvement of salicylate and jasmonate signaling pathways in Arabidopsis interaction with Fusarium graminearum. Mol Plant Microbe Interact 23:861–870
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 Plant Microbe Interact 25:431–439
Maldonado-Ramirez SL, Schmale DG III, Shields EJ, Bergstrom GC (2005) The relative abundance of viable spores of Gibberella zeae in the planetary boundary layer suggest the role of long-distance transport in regional epidemics of Fusarium head blight. Agric For Meteorol 132:20–27
Martinez de Ilarduya O, Xie Q, Kaloshian I (2003) Aphid-induced defense responses in Mi-1-mediated compatible and incompatible tomato interactions. Mol Plant Microbe Interact 16:699–708
McCartney CA, Brûlé-Babel AL, Fedak G, Martin RA, McCallum BD, Gilbert J, Hiebert CW, Pozniak CJ (2016) Fusarium head blight resistance QTL in the spring wheat cross Kenyon/86ISMN 2137. Front Microbiol 7:1542
McKendry AL, Berg JE, Tague DN, Kephart KD (1995) Registration of ‘Ernie’ wheat. Crop Sci 35:1513
McKendry AL, Tague DN, Wright RL, Tremain JA, Conley SP (2005) Registration of ‘Truman’ wheat. Crop Sci 45:421–423
Mentewab AR, Zanoor H, Gosman NW, Rland A, Nicholson P (2000) Chromosomal location of Fusarium head blight resistance genes and analysis of the relationship between resistance to head blight and brown foot rot. Plant Breed 119:15–20
Mergoum M, Frohberg RC, Stack RW (2007) Breeding hard red spring wheat for Fusarium head blight resistance, successes and challenges. In: Buck HT, Nisi JE, Salomón N (eds) Wheat production in Stressed Environments. Springer, Dordrecht, pp 161–167
Mesterházy A (1995) Types and components of resistance to Fusarium head blight of wheat. Plant Breed 114:377–386
Mesterházy Á (2014) Chemical control of Fusarium head blight of wheat. In: Leslie J, Logrieco A (eds) Mycotoxin reduction in grain chains. Wiley, Manhattan, pp 232–247
Mesterházy Á, Bartók T, Mirocha CG, Komoróczy R (1999) Nature of wheat resistance to Fusarium head blight and the role of deoxynivalenol for breeding. Plant Breed 118:97–110
Mesterházy A, Lehoczki-Krsjak S, Varga M, Szabó-Hevér Á, Tóth B, Lemmens M (2015) Breeding for FHB resistance via Fusarium damaged kernels and deoxynivalenol accumulation as well as inoculation methods in winter wheat. Agric Sci 6:970–1002
Meuwissen TH, Hayes BJ, Goddard ME (2001) Prediction of total genetic value using genome-wide dense marker maps. Genetics 157:1819–1829
Miedaner T, Wilde F, Steiner B, Buerstmayr H, Korzun V, Ebmeyer E (2006) Stacking quantitative trait loci (QTL) for Fusarium head blight resistance from non–adapted sources in a European elite spring wheat background and assessing their effects on deoxynivalenol (DON) content and disease severity. Theor Appl Genet 112:562–569
Miller JD, Arnison PG (1986) Degradation of deoxynivalenol by suspension cultures of the Fusarium head blight resistant wheat cultivar Frontana. Can J Plant Pathol 8:147–150
Miller JD, Young JC, Sampson DR (1985) Deoxynivalenol and Fusarium head blight resistance in spring cereals. J Phytopathol 113:359–367
Mirdita V, He S, Zhao Y, Korzun V, Bothe R, Ebmeyer E, Reif JC, Jiang Y (2015) Potential and limits of whole genome prediction of resistance to Fusarium head blight and Septoria tritici blotch in a vast central European elite winter wheat population. Theor Appl Genet 128:2471–2481
Moore JW, Herrera-Foessel S, Lan C, Schnippenkoetter W, Ayliffe M, Huerta-Espino J, Lillemo M, Viccars L, Milne R, Periyannan S, Kong X, Spielmeyer W, Talbot M, Bariana H, Patrick JW, Dodds P, Singh R, Lagudah E (2015) A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat. Nat Genet 47:1494–1498
Moscetti I, Tundo S, Janni M, Sella L, Gazzetti K, Tauzin A, Giardina T, Masci S, Favaron F, D’Ovidio R (2013) Constitutive expression of the xylanase inhibitor TAXI-III delays Fusarium head blight symptoms in durum wheat transgenic plants. Mol Plant Microbe Interact 26:1464–1472
Muhovski Y, Batoko H, Jacquemin JM (2012) Identification, characterization and mapping of differentially expressed genes in a winter wheat cultivar (Centenaire) resistant to Fusarium graminearum infection. Mol Biol Rep 39:9583–9600
Mujeeb-Kazi A, Rodriguez R (1981) An intergeneric hybrid of Triticum aestivum L. × Elymus giganteus. J Hered 72:253–256
Mujeeb-Kazi A, Delgado R, Cano S, Rosas V, Cortés A (2000) Alien genetic diversity for wheat improvement: focus on scab resistance. In: Proceedings of the National Fusarium head blight forum. Erlanger, KY, pp 220–224
Nakagawa M (1955) Studies on ear-scab resistance of wheat varieties. 3. Relation of the “variety-testing” and the “seed reaction” of fusarial head blight in winter wheat varieties. Jpn J Breed 5:100–106
Nielsen LK, Jensen JD, Nielsen GC, Jensen JE, Spliid NH, Thomsen IK, Justesen AF, Collinge DB, Jorgensen LN (2011) Fusarium head blight of cereals in Denmark: species complex and related mycotoxins. Phytopathology 101:960–969
Nishio Z, Takata K, Tabiki T, Ito M, Takenaka S, Kuwabara T, Iriki N, Ban T (2004) Diversity of resistance to Fusarium head blight in Japanese winter wheat. Breed Sci 54:79–84
Nisikado Y (1959) Studies on the wheat scab, caused by Gibberella zeae (Schw.) Petch, and its control. Report of the Ohara Institute for Agricultural Biology, Okayama University, pp 141–165
Niwa S, Kazama Y, Abe T, Ban T (2018) Tracking haplotype for QTLs associated with Fusarium head blight resistance in Japanese wheat (Triticum aestivum L.) lineage. Agric Food Secur 7:4
Nussbaumer T, Warth B, Sharma S, Ametz C, Bueschl C, Parich A, Pfeifer M, Siegwart G, Steiner B, Lemmens M, Schuhmacher R, Buerstmayr H, Mayer KF, Kugler KG, Schweiger W (2015) Joint transcriptomic and metabolomic analyses reveal changes in the primary metabolism and imbalances in the subgenome orchestration in the bread wheat molecular response to Fusarium graminearum. G3 5:2579–2592
O’Donnell K, Ward TJ, Aberra D, Kistler HC, Aoki T, Orwig N, Kimura M, Bjørnstad Å, Klemsdal SS (2008) Multilocus genotyping and molecular phylogenetics resolve a novel head blight pathogen within the Fusarium graminearum species complex from Ethiopia. Fungal Genet Biol 45:1514–1522
O’Donnell K, Kistler HC, Tacke BK, Casper HH (2000) Gene genealogies reveal global phylogeographic structure and reproductive isolation among lineages of Fusarium graminearum, the fungus causing wheat scab. Proc Natl Acad Sci USA 97:7905–7910
Okubara PA, Blechl AE, McCormick SP, Alexander NJ, Dill MR, Hohn TM (2002) Engineering deoxynivalenol metabolism in wheat through the expression of a fungal trichothecene acetyltransferase gene. Theor Appl Genet 106:74–83
Oliver RE, Cai X, Xu SS, Chen X, Stack RW (2005) Wheat-alien species derivatives: a novel source of resistance to Fusarium head blight in wheat. Crop Sci 45:1353–1360
Oliver RE, Stack RW, Miller JD, Cai X (2007) Reaction of wild emmer wheat accessions to Fusarium head blight. Crop Sci 47:893–897
Oliver RE, Cai X, Friesen TL, Halley S, Stack RW, Xu SS (2008) Evaluation of Fusarium head blight resistance in tetraploid wheat (Triticum turgidum L.). Crop Sci 48:213–222
Olson PD, Varner JE (1993) Hydrogen peroxide and lignification. Plant Cell 4:887–892
Osborne LE, Stein JM (2007) Epidemiology of Fusarium head blight on small-grain cereals. Int J Food Microbiol 119:103–108
Otto CD, Kianian SF, Elias EM, Stack RW, Joppa LR (2002) Genetic dissection of a major Fusarium head blight QTL in tetraploid wheat. Plant Mol Biol 48:625–632
Pan Y, Liu Z, Rocheleau H, Fauteux F, Wang Y, McCartney C, Ouellet T (2018) Transcriptome dynamics associated with resistance and susceptibility against Fusarium head blight in four wheat genotypes. BMC Genom 19:642
Paranidharan V, Abu-Nada Y, Hamzehzarghani H, Kushalappa AC, Dion Y, Rioux S, Comeau A, Choiniere L (2008) Resistance related metabolites in wheat against Fusarium graminearum and the virulence factor deoxynivalenol (DON). Botany 86:1168–1179
Parry DW, Jenkinson P, McLeod L (1995) Fusarium ear blight (scab) in small grain cereals—a review. Plant Pathol 44:207–238
Penninckx IA, Thomma BP, Buchala A, Metraux JP, Broekaert WF (1998) Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10:2103–2113
Pereyra S, Lori GA (2013) Crop residues and their management in the epidemiology of Fusarium head blight. In: Alconada Magliano T, Chulze S (eds) Fusarium head blight in Latin America. Springer, Dordrecht, pp 143–156
Perlikowski D, Wiśniewska H, Góral T, Kwiatek M, Majka M, Kosmala A (2014) Identification of kernel proteins associated with the resistance to Fusarium head blight in winter wheat (Triticum aestivum L.). PLoS One 9:e110822
Perlikowski D, Wiśniewska H, Kaczmarek J, Góral T, Ochodzki P, Kwiatek M, Majka M, Augustyniak A, Kosmala A (2016) Alterations in kernel proteome after infection with Fusarium culmorum in two triticale cultivars with contrasting resistance to Fusarium head blight. Front Plant Sci 7:1217
Perochon A, Jianguang J, Kahla A, Arunachalam C, Scofield SR, Bowden S, Wallington E, Doohan FM (2015) TaFROG encodes a Pooideae orphan protein that interacts with SnRK1 and enhances resistance to the mycotoxigenic fungus Fusarium graminearum. Plant Physiol 169:2895–2906
Perochon A, Kahla A, Vranic M, Jia J, Malla KB, Craze M, Wallington E, Doohan FM (2019) A wheat NAC interacts with an orphan protein and enhances resistance to Fusarium head blight disease. Plant Biotechnol J 17:1892–1904
Peschen D, Li HP, Fischer R, Kreuzaler F, Liao YC (2004) Fusion proteins comprising a Fusarium-specific antibody linked to antifungal peptides protect plants against a fungal pathogen. Nat Biotechnol 22:732–738
Pirgozliev SR, Edwards SG, Hare MC, Jenkinson P (2003) Strategies for the control of Fusarium head blight in cereals. Eur J Plant Pathol 109:731–742
Pont C, Leroy T, Seidel M, Tondelli A, Duchemin W, Armisen D, Lang D, Bustos-Korts D, Goué N, Balfourier F, Molnár-Láng M, Lage J, Kilian B, Özkan H, Waite D, Dyer S, Letellier T, Alaux M, Russell J, Keller B, van Eeuwijk F, Spannagl M, Mayer KFX, Waugh R, Stein N, Cattivelli L, Haberer G, Charmet G, Salse J, Wheat and Barley Legacy for Breeding Improvement (WHEALBI) Consortium (2019) Tracing the ancestry of modern bread wheats. Nat Genet 51:905–911
Poppenberger B, Berthiller F, Lucyshyn D, Sieberer T, Schuhmacher R, Krska R, Kuchler K, Glössl J, Luschnig C, Adam G (2003) Detoxification of the Fusarium mycotoxin deoxynivalenol by a UDP-glucosyltransferase from Arabidopsis thaliana. J Biol Chem 278:47905–47914
Pré M, Atallah M, Champion A, De Vos M, Pieterse CM, Memelink J (2008) The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. Plant Physiol 147:1347–1357
Pritsch C, Muehlbauer GJ, Bushnell WR, Somers DA, Vance CP (2000) Fungal development and induction of defense response genes during early infection of wheat spikes by Fusarium graminearum. Mol Plant Microbe Interact 13:159–169
Pritsch C, Vance CP, Bushnell WR, Somers DA, Hohn TM, Muehlbauer GJ (2001) Systemic expression of defense response genes in wheat spikes as a response to Fusarium graminearum infection. Physiol Mol Plant Pathol 58:1–12
Proctor RH, Hohn TM, Mccormick SP (1995) Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene. Mol Plant Microbe Interact 8:593–601
Pugh GW, Johann H, Dickson JG (1933) Factors affecting infection of wheat heads by Gibberella saubinetii. J Agric Res 46:771–797
Pumphrey MO, Bernardo R, Anderson JA (2007) Validating the QTL for Fusarium head blight resistance in near-isogenic wheat lines developed from breeding populations. Crop Sci 47:200–206
Qi LL, Pumphrey MO, Friebe B, Chen PD, Gill BS (2008) Molecular cytogenetic characterization of alien introgressions with gene Fhb3 for resistance to Fusarium head blight disease of wheat. Theor Appl Genet 117:1155–1166
Qi P, Balcerzak M, Rocheleau H, Leung W, Wei Y, Zheng Y, Ouellet T (2016) Jasmonic acid and abscisic acid play important roles in host–pathogen interaction between Fusarium graminearum and wheat during the early stages of Fusarium head blight. Physiol Mol Plant Pathol 93:39–48
Qiu J, Xu J, Shi J (2019) Fusarium toxins in Chinese wheat since the 1980s. Toxins 11:248
Quraishi UM, Pont C, Ain QU, Flores R, Burlot L, Alaux M, Quesneville H, Salse J (2017) Combined genomic and genetic data integration of major agronomical traits in bread wheat (Triticum aestivum L.). Front Plant Sci 8:1843
Rajtilak M, Kanniah R, Cary JW (2017) RNA interference (RNAi) as a potential tool for control of mycotoxin contamination in crop plants: concepts and Considerations. Front Plant Sci 8:200
Ravensdale M, Rocheleau H, Wang L, Nasmith C, Ouellet T, Subramaniam R (2014) Components of priming-induced resistance to Fusarium head blight in wheat revealed by two distinct mutants of Fusarium graminearum. Mol Plant Pathol 15:948–956
Rawat N, Pumphrey MO, Liu S, Zhang X, Tiwari VK, Ando K, Trick HN, Bockus WW, Akhunov E, Anderson JA, Gill BS (2016) Wheat Fhb1 encodes a chimeric lectin with agglutinin domains and a pore-forming toxin-like domain conferring resistance to Fusarium head blight. Nat Genet 48:1576–1580
Ren JD, Wang Z, Du ZY, Che MZ, Zhang YB, Quan W, Wang YJ, Jiang X, Zhang ZJ (2019) Detection and validation of a novel major QTL for resistance to Fusarium head blight from Triticum aestivum in the terminal region of chromosome 7DL. Theor Appl Genet 132:241–255
Rossi V, Ravanetti A, Pattori E, Giosuè S (2001) Influence of temperature and humidity on the infection of wheat spikes by some fungi causing Fusarium head blight. J Plant Pathol 83:189–198
Roux M, Schwessinger B, Albrecht C, Chinchilla D, Jones A, Holton N, Malinovsky FG, Tör M, de Vries S, Zipfel C (2011) The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell 23:2440–2455
Ruan Y, Comeau A, Langevin F, Hucl P, Clarke JM, Brule-Babel A, Pozniak CJ (2012) Identification of novel QTL for resistance to Fusarium head blight in a tetraploid wheat population. Genome 55:853–864
Ruckenbauer P, Buerstmayr H, Lemmens M (2007) Strategies of the European initiative for resistance breeding against Fusarium head blight. In: Buck HT, Nisi JE, Salomón N (eds) Wheat production in stressed environments. Springer, Dordrecht, pp 103–107
Rutkoski J, Benson J, Jia Y, Brown-Guedira G, Jannink JL, Sorrells M (2012) Evaluation of genomic prediction methods for Fusarium head blight resistance in wheat. Plant Genome 5:51–61
Sakalauskas S, Stumbriene K, Suproniene S, Svegzda P (2014) Changes in Fusarium link species composition from Lithuanian wheat grain in years 2005–2007 to 2011–2013. Proc Latvia Univ Agric 32:45–50
Salameh A, Buerstmayr M, Steiner B, Neumayer A, Lemmens M, Buerstmayr H (2011) Effects of introgression of two QTL for Fusarium head blight resistance from Asian spring wheat by marker-assisted backcrossing into European winter wheat on Fusarium head blight resistance, yield and quality traits. Mol Breed 28:485–494
Sarver BAJ, Ward TJ, Gale LR, Broz K, Corby Kistler H, Aoki T, Nicholson P, Carter J, O’Donnell K (2011) Novel Fusarium head blight pathogens from Nepal and Louisiana revealed by multilocus genealogical concordance. Fungal Genet Biol 48:1096–1107
Sasaki K, Kuwabara C, Umeki N, Fujioka M, Saburi W, Matsui H, Abe F, Imai R (2016) The cold-induced defensin TAD1 confers resistance against snow mold and Fusarium head blight in transgenic wheat. J Biotechnol 228:3–7
Sattler SE, Funnell-Harris DL (2013) Modifying lignin to improve bioenergy feedstocks: strengthening the barrier against pathogens? Front Plant Sci 4:70
Saur L (1991) Sources of resistance to head blight caused by Fusarium culmorum in bread wheat and related species. Agronomie 11:535–541
Schroeder HW, Christensen JJ (1963) Factors affecting resistance of wheat to scab caused by Gibberella zeae. Phytopathology 53:831–838
Schweiger W, Boddu J, Shin S, Poppenberger B, Berthiller F, Lemmens M, Muehlbauer GJ, Adam G (2010) Validation of a candidate deoxynivalenol-inactivating UDP-glucosyltransferase from barley by heterologous expression in yeast. Mol Plant Microbe Interact 23:977–986
Schweiger W, Steiner B, Ametz C, Siegwart G, Wiesenberger G, Berthiller F, Lemmens M, Jia HY, Adam G, Muehlbauer GJ, Kreil DP, Buerstmayr H (2013) Transcriptomic characterization of two major Fusarium resistance quantitative trait loci (QTLs), Fhb1 and Qfhs.ifa-5A, identifies novel candidate genes. Mol Plant Pathol 14:772–785
Schweiger W, Steiner B, Vautrin S, Nussbaumer T, Siegwart G, Zamini M, Jungreithmeier F, Gratl V, Lemmens M, Mayer KFX, Bérgès H, Adam G, Buerstmayr H (2016) Suppressed recombination and unique candidate genes in the divergent haplotype encoding Fhb1, a major Fusarium head blight resistance locus in wheat. Theor Appl Genet 129:1607–1623
Scott IT (1927) Varietal resistance and susceptibility to wheat scab. Univ Mo Agric Exp Sta Res Bull 111:3–14
Sears ER (1954) The aneuploids of common wheat. Mo Agric Exp Stn Res Bull 572:1–58
Selby AD, Manns TF (1909) Studies in diseases of cereals and grasses. Bull Ohio Agric Exp Sta 203:187–236
Shakoor N, Lee S, Mockler TC (2017) High throughput phenotyping to accelerate crop breeding and monitoring of diseases in the field. Curr Opin Plant Biol 38:184–192
Shan L, He P, Li J, Heese A, Peck SC, Nürnberger T, Martin GB, Sheen J (2008) Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4:17–27
Shen X, Ohm H (2007) Molecular mapping of Thinopyrum-derived Fusarium head blight resistance in common wheat. Mol Breed 20:131–140
Shen X, Kong L, Ohm H (2004) Fusarium head blight resistance in hexaploid wheat (Triticum aestivum)-Lophopyrum genetic lines and tagging of the alien chromatin by PCR markers. Theor Appl Genet 108:808–813
Shin S, Mackintosh CA, Lewis J, Heinen SJ, Radmer L, Dill-Macky R, Baldridge GD, Zeyen RJ, Muehlbauer GJ (2008) Transgenic wheat expressing a barley class II chitinase gene has enhanced resistance against Fusarium graminearum. J Exp Bot 59:2371–2378
Singh RP, van Ginkel M (1997) Breeding strategies for introgressing diverse scab resistances into adapted wheats. In: Dubin HJ, Gilchrist L, Reeves J, McNab A (eds) Fusarium head scab: global status and future prospects. CIMMYT, Mexico, pp 86–92
Singh RP, Ma H, Rajaram S (1995) Genetic-analysis of resistance to scab in spring wheat cultivar Frontana. Plant Dis 79:238–240
Smith WG (1884) Diseases of field and garden crops. MacMillan and Co., London
Snijders CHA (1990) Genetic variation for resistance to Fusarium head blight in bread wheat. Euphytica 50:171–179
Somers DJ, Fedak G, Clarke J, Cao W (2006) Mapping of FHB resistance QTLs in tetraploid wheat. Genome 49:1586–1593
Song M, Xu WQ, Xiang Y, Jia HY, Zhang LX, Ma ZQ (2013) Association of jacalin-related lectins with wheat responses to stresses revealed by transcriptional profiling. Plant Mol Biol 84:95–110
Spoel SH, Koornneef A, Claessens SM, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala AJ, Métraux JP, Brown R, Kazan K, Van Loon LC, Dong X, Pieterse CM (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760–770
Stack RW, Elias EM, Fetch JM, Miller JD, Joppa LR (2002) Fusarium head blight reaction of Langdon durum-Triticum dicoccoides chromosome substitution lines. Crop Sci 42:637–642
Steed A, Chandler E, Thomsett M, Gosman N, Faure S, Nicholson P (2005) Identification of type I resistance to Fusarium head blight controlled by a major gene located on chromosome 4A of Triticum macha. Theor Appl Genet 111:521–529
Steiner B, Kurz H, Lemmens M, Buerstmayr H (2009) Differential gene expression of related wheat lines with contrasting levels of head blight resistance after Fusarium graminearum inoculation. Theor Appl Genet 118:753–764
Steiner B, Buerstmayr M, Michel S, Schweiger W, Lemmens M, Buerstmayr H (2017) Breeding strategies and advances in line selection for Fusarium head blight resistance in wheat. Trop Plant Pathol 42:165–174
Steiner B, Buerstmayr M, Wagner C, Danler A, Eshonkulov B, Ehn M, Buerstmayr H (2019a) Fine-mapping of the Fusarium head blight resistance QTL Qfhs.ifa-5A identifies two resistance QTL associated with anther extrusion. Theor Appl Genet 132:2039–2053
Steiner B, Michel S, Maccaferri M, Lemmens M, Tuberosa R, Buerstmayr H (2019b) Exploring and exploiting the genetic variation of Fusarium head blight resistance for genomic-assisted breeding in the elite durum wheat gene pool. Theor Appl Genet 132(4):969–988
Su Z, Jin S, Zhang D, Bai G (2018) Development and validation of diagnostic markers for Fhb1 region, a major QTL for Fusarium head blight resistance in wheat. Theor Appl Genet 131:2371–2380
Su Z, Bernardo A, Tian B, Chen H, Wang S, Ma H, Cai S, Liu D, Zhang D, Li T, Trick H, Amand P, Yu J, Zhang Z, Bai G (2019) A deletion mutation in TaHRC confers Fhb1 resistance to Fusarium head blight in wheat. Nat Genet 51:1099–1105
Sun JY, Gaudet DA, Lu ZX, Frick M, Puchalski B, Laroche A (2008) Characterization and antifungal properties of wheat nonspecific lipid transfer proteins. Mol Plant Microbe Interact 21:346–360
Szabó-Hevér Á, Lehoczki-Krsjak S, Tóth B, Purnhauser L, Buerstmayr H, Steiner B, Mesterházy Á (2012) Identification and validation of Fusarium head blight and Fusarium-damaged kernel QTL in a Frontana/Remus DH mapping population. Can J Plant Pathol 34:224–238
Szabó-Hevér Á, Lehoczki-Krsjak S, Varga M, Purnhauser L, Pauk J, Lantos C, Mesterházy Á (2014) Differential influence of QTL linked to Fusarium head blight, Fusarium-damaged kernel, deoxynivalenol contents and associated morphological traits in a Frontana-derived wheat population. Euphytica 200:9–26
Szabó-Hevér Á, Zhang Q, Friesen TL, Zhong S, Elias EM, Cai X, Jin Y, Faris JD, Chao S, Xu SS (2018) Genetic diversity and resistance to Fusarium head blight in synthetic hexaploid wheat derived from Aegilops tauschii and diverse Triticum turgidum subspecies. Front Plant Sci 9:1829
Taheri P (2018) Cereal diseases caused by Fusarium graminearum: from biology of the pathogen to oxidative burst-related host defense responses. Eur J Plant Pathol 152:1–20
Talas F, Longin F, Miedaner T (2011) Sources of resistance to Fusarium head blight within Syrian durum wheat landraces. Plant Breed 130:398–400
Tekauz A (2018) History of FHB research in (western) Canada. In: Gräfenhan T, Fetch T (eds) 9th Canadian workshop on fusarium head blight, Winnipeg, p 30
Teli B, Chattopadhyay A, Meena SC, Gangwar GP, Pandey SK (2016) Present status of Fusarium head blight of wheat and barley in India. In: Vaish SS (ed) Diseases of wheat and their management. Astral International (P) Ltd., New Delhi, pp 79–92
Thapa G, Gunupuru LR, Hehir JG, Kahla A, Mullins E, Doohan FM (2018) A pathogen-responsive leucine rich receptor like kinase contributes to Fusarium resistance in cereals. Front Plant Sci 9:867
Tundo S, Kalunke R, Janni M, Volpi C, Lionetti V, Bellincampi D, Favaron F, D’Ovidio R (2016) Pyramiding PvPGIP2 and TAXI-III but not PvPGIP2 and PMEI enhances resistance against Fusarium graminearum. Mol Plant Microbe Interact 29:629–639
Van der Does D, Leon-Reyes A, Koornneef A, Van Verk MC, Rodenburg N, Pauwels L, Goossens A, Körbes AP, Memelink J, Ritsema T, Van Wees SC, Pieterse CM (2013) Salicylic acid suppresses jasmonic acid signaling downstream of SCFCOI1-JAZ by targeting GCC promoter motifs via transcription factor ORA59. Plant Cell 25(2):744–761
van der Lee T, Zhang H, van Diepeningen A, Waalwijk C (2015) Biogeography of Fusarium graminearum species complex and chemotypes: a review. Food Addit Contam A 32:453–460
van Ginkel M, Van Der Schaar W, Yang Z, Rajaram S (1996) Inheritance of resistance to scab in two wheat cultivars from Brazil and China. Plant Dis 80:863–867
Vaughan M, Backhouse D, Ponte ED (2016) Climate change impacts on the ecology of Fusarium graminearum species complex and susceptibility of wheat to Fusarium head blight: a review. World Mycotoxin J 9:685–700
Venske E, dos Santos RS, Farias DdR, Rother V, da Maia LC, Pegoraro C, Costa de Oliveira A (2019) Meta-analysis of the QTLome of Fusarium head blight resistance in bread wheat: refining the current puzzle. Front Plant Sci 10:727
Veronese P, Nakagami H, Bluhm B, Abuqamar S, Chen X, Salmeron J, Dietrich RA, Hirt H, Mengiste T (2006) The membrane-anchored BOTRYTIS-INDUCED KINASE1 plays distinct roles in Arabidopsis resistance to necrotrophic and biotrophic pathogens. Plant Cell 18:257–273
Volpi C, Janni M, Lionetti V, Bellincampi D, Favaron F, D’Ovidio R (2011) The ectopic expression of a pectin methyl esterase inhibitor increases pectin methyl esterification and limits fungal diseases in wheat. Mol Plant Microbe Interact 24:1012–1019
Von Der Ohe C, Ebmeyer E, Korzun V, Miedaner T (2010) Agronomic and quality performance of winter wheat backcross populations carrying non-adapted Fusarium head blight resistance QTL. Crop Sci 50:2283–2290
Waalwijk C, Kastelein P, de Vries I, Kerényi Z, van der Lee T, Hesselink T, Köhl J, Kema G (2003) Major changes in Fusarium spp. in wheat in the Netherlands. Eur J Plant Pathol 109:743–754
Walter S, Kahla A, Arunachalam C, Perochon A, Khan MR, Scofield SR, Doohan FM (2015) A wheat ABC transporter contributes to both grain formation and mycotoxin tolerance. J Exp Bot 66:2583–2593
Wan Y, Yen C, Yang J, Liu D (1997a) The diversity of resources resistant to scab in Triticeae (Poaceae). Wheat Inf Serv 84:7–12
Wan YF, Yen C, Yang JL, Liu FQ (1997b) Evaluation of Roegneria for resistance to head scab caused by Fusarium graminearum Schwabe. Genet Resour Crop Evol 44:211–215 (in Chinese)
Wang Y, Yang X, Xiao C (1982) The improvement of identification technique of scab (Gibberella zeae Petch) resistance of wheat and the development of resistant sources. Sci Agric Sin 5:67–77 (in Chinese)
Wang Y, Chen P, Liu D (1986) Transfer of useful germplasm from Elymus giganteus L. to common wheat. I. Production of (T. aestivum L. cv. Chinese Spring × Elymus giganteus) F1. J Nanjing Agric Univ 1:10–14 (in Chinese)
Wang Y, Wang J, Liu Y (1992) Genetical studies on the resistance to scab spread in wheat varieties. Acta Agron Sin 5:373–379 (in Chinese)
Wang X, Wu L, Chen P, Liu D (1995) Preliminary report on breeding and identification of Triticum aestivum and Roegneria kamoji alien addition lines. Acta Bot Sin 37:878–884 (in Chinese)
Wang X, Chen P, Liu D (1997) Development of euplasmic T. aestivum-R. ciliaris disomic addition line D and ditelosomic addition line tBL. Chinese J Genet 24:127–131 (in Chinese)
Wang Y, Yang L, Xu H, Li Q, Ma Z, Chu C (2005) Differential proteomic analysis of proteins in wheat spikes induced by Fusarium graminearum. Proteomics 5:4496–4503
Wang G, Hou W, Zhang L, Wu H, Zhao L, Du X, Ma X, Li A, Wang H, Kong L (2016) Functional analysis of a wheat pleiotropic drug resistance gene involved in Fusarium head blight resistance. J Integr Agric 15:2215–2227
Wang L, Li Q, Liu Z, Surendra A, Pan Y, Li Y, Zaharia LI, Ouellet T, Fobert PR (2018) Integrated transcriptome and hormone profiling highlight the role of multiple phytohormone pathways in wheat resistance against Fusarium head blight. PLoS ONE 13:e0207036
Ward TJ, Clear RM, Rooney AP, O’Donnell K, Gaba D, Patrick S, Starkey DE, Gilbert J, Geiser DM, Nowicki TW (2008) An adaptive evolutionary shift in Fusarium head blight pathogen populations is driving the rapid spread of more toxigenic Fusarium graminearum in North America. Fungal Genet Biol 45:473–484
Warth B, Parich A, Bueschl C, Schoefbeck D, Neumann NKN, Kluger B, Schuster K, Krska R, Adam G, Lemmens M, Schuhmacher R (2015) GC–MS based targeted metabolic profiling identifies changes in the wheat metabolome following deoxynivalenol treatment. Metabolomics 11:722–738
Watson A, Ghosh S, Williams MJ, Cuddy WS, Simmonds J, Rey MD, Asyraf Md Hatta M, Hinchliffe A, Steed A, Reynolds D, Adamski NM, Breakspear A, Korolev A, Rayner T, Dixon LE, Riaz A, Martin W, Ryan M, Edwards D, Batley J, Raman H, Carter J, Rogers C, Domoney C, Moore G, Harwood W, Nicholson P, Dieters MJ, DeLacy IH, Zhou J, Uauy C, Boden SA, Park RF, Wulff BBH, Hickey LT (2018) Speed breeding is a powerful tool to accelerate crop research and breeding. Nat Plants 4:23–29
Wegulo SN (2012) Factors influencing deoxynivalenol accumulation in small grain cereals. Toxins 4:1157–1180
Weng Y, Liu D (1989) Morphology, scab resistance and cytogenetics of intergeneric hybrids of Triticum aestivum L. with Roegneria C. Koch (Agropyron) species. Sci Agric Sin 22:1–7 (in Chinese)
West JS, Holdgate S, Townsend JA, Edwards SG, Jennings P, Fitt BDL (2012) Impacts of changing climate and agronomic factors on Fusarium ear blight of wheat in the UK. Fungal Ecol 5:53–61
Wilson WW, McKee G, Nganje W, Dahl B, Bangsund D (2017) Economic impact of USWBSI’s Scab Initiative to reduce FHB. Agribus Appl Econ 774
Wiśniewska H, Surma M, Krystkowiak K, Adamski T, Kuczyńska A, Ogrodowicz P, Mikolajczak K, Belter J, Majka M, Kaczmarek Z, Krajewski P, Sawikowska A, Lenc L, Baturo-Cieśniewska A, Łukanowski A, Góral T, Sadowski C (2016) Simultaneous selection for yield-related traits and susceptibility to Fusarium head blight in spring wheat RIL population. Breed Sci 66:281–292
Wood M, Comis D, Harden D, McGraw L, Stelljes KB (1999) Fighting Fusarium. Agric Res 47:18–21
Wu YS (1939) Wheat scab. The Nung Ling Sin Pao 32–36:20–32 (in Chinese)
Wu ZS, Shen JQ, Lu WZ (1984) Development of a gene pool with improved resistance to scab in wheat. Acta Agron Sin 10:73–80 (in Chinese)
Xiang Y, Song M, Wei Z, Tong J, Zhang L, Xiao L, Ma ZQ, Wang Y (2011) A jacalin-related lectin-like gene in wheat is a component of the plant defence system. J Exp Bot 62:5471–5483
Xiao J, Jin X, Jia X, Wang H, Cao A, Zhao W, Pei H, Xue Z, He L, Chen Q, Wang X (2013) Transcriptome-based discovery of pathways and genes related to resistance against Fusarium head blight in wheat landrace Wangshuibai. BMC Genom 14:197
Xu X, Nicholson P (2009) Community ecology of fungal pathogens causing wheat head blight. Annu Rev Phytopathol 47:83–103
Xu XM, Parry DW, Nicholson P, Thomsett MA, Simpson D, Edwards SG, Cooke BM, Doohan FM, Brennan JM, Moretti A, Tocco G, Mule G, Hornok L, Giczey G, Tatnell J (2005) Predominance and association of pathogenic species causing Fusarium ear blight in wheat. Eur J Plant Path 112:143–154
Xu F, Li W, Yan S, Zhang C, Zheng J, Du J, Zhang Z, Shi X (2017) Analysis of pyramiding effect of major QTLs for resistance to scab in wheat. J Triticeae Crop 37:585–593 (in Chinese)
Xue S, Zhang Z, Lin F, Kong Z, Cao Y, Li C, Yi H, Mei M, Zhu H, Wu J, Xu H, Zhao D, Tian D, Zhang C, Ma Z (2008) A high-density intervarietal map of the wheat genome enriched with markers derived from expressed sequence tags. Theor Appl Genet 117(2):181–189
Xue SL, Li GQ, Jia HY, Lin F, Cao Y, Xu F, Tang MZ, Wang Y, Wu XY, Zhang ZZ, Zhang LX, Kong ZX, Ma ZQ (2010a) Marker-assisted development and evaluation of near-isogenic lines for scab resistance QTLs of wheat. Mol Breed 25:397–405
Xue S, Li G, Jia H, Xu F, Lin F, Tang M, Wang Y, An X, Xu H, Zhang L, Kong Z, Ma Z (2010b) Fine mapping Fhb4, a major QTL conditioning resistance to Fusarium infection in bread wheat (Triticum aestivum L.). Theor Appl Genet 121:147–156
Xue S, Xu F, Tang M, Zhou Y, Li G, An X, Lin F, Xu H, Jia H, Zhang L, Kong Z, Ma Z (2011) Precise mapping Fhb5, a major QTL conditioning resistance to Fusarium infection in bread wheat (Triticum aestivum L.). Theor Appl Genet 123:1055–1063
Yang Z, Gilbert J, Fedak G, Somers DJ (2005) Genetic characterization of QTL associated with resistance to Fusarium head blight in a doubled-haploid spring wheat population. Genome 48:187–196
Yang Z, Gilbert J, Procunier JD (2006) Genetic diversity of resistance genes controlling Fusarium head blight with simple sequence repeat markers in thirty-six wheat accessions from east Asian origin. Euphytica 148:345–352
Yao J, Ge Y, Wang S, Yao G, Zhou Z, Qian Y (1997) Chromosomal location of genes for scab resistance in wheat cultivar Sumai 3. Acta Agron Sin 4:450–453 (in Chinese)
Yu Y (1982) Monosomic analyses of wheat scab resistance and yield components in the variety Sumai 3. J Huazhong Agric Coll 2:70–72 (in Chinese)
Yu Y (1991) Genetic analysis for scab resistance in five wheat varieties, PHJZM, HHDTB, CYHM, YGFZ and WN2. Acta Agron Sin 4:248–254 (in Chinese)
Yu JB, Bai GH, Cai SB, Dong YH, Ban T (2008) New Fusarium head blight-resistant sources from Asian wheat germplasm. Crop Sci 48:1090–1097
Yu G, Zhang X, Yao J, Zhou M, Ma H (2017) Resistance against Fusarium head blight in transgenic wheat plants expressing the ScNPR1 gene. J Phytopathol 165:223–231
Zantinge J, Kumar K, Xi K, Johns M, Murray A, Jones T, Helm JH, Juskiw P (2010) Comparison of barley seed proteomic profiles associated with Fusarium head blight reaction. Can J Plant Pathol 32:496–512
Zhang L, Pan X (1982) A study on resistance to colonization of Gibberela zeae in wheat varieties. J South China Agric Coll 3:21–29
Zhang LQ, Pan XP, Chen HY (1993) Studies on recurrent selection of wheat resistance to Gibberella zeae (Schw.) Petch (resistance to spread). J South China Agric Univ 14:55–60 (in Chinese)
Zhang H, Van der Lee T, Waalwijk C, Chen W, Xu J, Xu J, Zhang Y, Feng J (2012) Population analysis of the Fusarium graminearum species complex from wheat in China show a shift to more aggressive isolates. PLoS ONE 7:e31722
Zhang X, Halder J, White RP, Hughes DJ, Ye Z, Wang C, Xu R, Gan B, Fitt BDL (2014) Climate change increases risk of Fusarium ear blight on wheat in central China. Ann Appl Biol 164:384–395
Zhang WT, Francis T, Gao P, Boyle K, Jiang FY, Eudes F, Cuthbert R, Sharpe A, Fobert PR (2018) Genetic characterization of type II Fusarium head blight resistance derived from transgressive segregation in a cross between eastern and western Canadian spring wheat. Mol Breed 38:13
Zhou CF, Xia SH, Qian CM, Yao GC, Shen JX (1987) On the problem of wheat breeding for scab resistance. Sci Agric Sin 20:19–25 (in Chinese)
Zhou W, Kolb FL, Riechers DE (2005) Identification of proteins induced or upregulated by Fusarium head blight infection in the spikes of hexaploid wheat (Triticum aestivum). Genome 48:770–780
Zhou W, Eudes F, Laroche A (2006) Identification of differentially regulated proteins in response to a compatible interaction between the pathogen Fusarium graminearum and its host, Triticum aestivum. Proteomics 6:4599–4609
Zhu X, Li Z, Xu H, Zhou M, Du L, Zhang Z (2012) Overexpression of wheat lipid transfer protein gene TaLTP5 increases resistances to Cochliobolus sativus and Fusarium graminearum in transgenic wheat. Funct Integr Genom 12:481–488
Zhu X, Zhong S, Chao S, Gu YQ, Kianian SF, Elias E, Cai XW (2016) Toward a better understanding of the genomic region harboring Fusarium head blight resistance QTL Qfhs.ndsu-3AS in durum wheat. Theor Appl Genet 129:31–43
Zhu Z, Xu D, Cheng S, Gao C, Xia X, Hao Y, He Z (2018) Characterization of Fusarium head blight resistance gene Fhb1 and its putative ancestor in Chinese wheat germplasm. Acta Agron Sin 44:473–482
Zhuang ZY, Liang SC, Li MF (1995) Application of dominant nucleus sterile gene Ta1 in breeding E-Mai 11. Hubei Agric Sci 34:18–20 (in Chinese)
Acknowledgements
This research was partially supported by grants from National Natural Science Foundation of China (31930081, 30025030, 30430440, 30721140555, 31030054, 30671295 and 31501306), the Ministry of Science and Technology of China (2016YFD0101004, 2016YFD0101802, 2009ZX08009-049B, 2002AA224161), and Jiangsu collaborative innovation initiative for modern crop production. We have tried hard to summarize all the excellent researches in the related field, but omission still exists due to the scope.
Author information
Authors and Affiliations
Contributions
ZQM made the concept, edited and approved the manuscript, GQL, QX and JYZ prepared the draft, HYJ, ZXK, NL, and YY reviewed the paper.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Additional information
Communicated by Xianchun Xia.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ma, Z., Xie, Q., Li, G. et al. Germplasms, genetics and genomics for better control of disastrous wheat Fusarium head blight. Theor Appl Genet 133, 1541–1568 (2020). https://doi.org/10.1007/s00122-019-03525-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-019-03525-8