Action and reaction of host and pathogen during Fusarium head blight disease

New Phytologist

Volumn 185, Issue 1, 2010, Pages 54-66

  Walter, Stephanie ^a   Nicholson, Paul ^b   Doohan, Fiona M ^c  

^a AARHUS UNIVERSITY   (Denmark)

^b JOHN INNES CENTRE   (United Kingdom)

^c UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Deoxynivalenol; Disease resistance; Fusarium head blight (FHB); Necrotroph; Plant pathogen interaction; Trichothecene; Wheat

Indexed keywords

PROTEOME;

COLONIZATION; CROP YIELD; DISEASE CONTROL; DISEASE RESISTANCE; FUNGAL DISEASE; HOST-PATHOGEN INTERACTION; MUTATION; WHEAT;

ADAPTATION; CEREAL; CROP; FUNGAL GENE; FUSARIUM; GENE EXPRESSION; GENETICS; GENOME; HOST PATHOGEN INTERACTION; METABOLOME; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; PLANT GENE; REVIEW; SIGNAL TRANSDUCTION;

ADAPTATION, PHYSIOLOGICAL; CEREALS; CROPS, AGRICULTURAL; FUSARIUM; GENE EXPRESSION; GENES, FUNGAL; GENES, PLANT; GENOME; HOST-PATHOGEN INTERACTIONS; METABOLOME; PLANT DISEASES; PROTEOME; RECEPTOR CROSS-TALK; SIGNAL TRANSDUCTION;

ANIMALIA; FUSARIUM; FUSARIUM CULMORUM; GIBBERELLA ZEAE; TRITICUM AESTIVUM;

EID: 71249158800     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2009.03041.x     Document Type: Review

References (147)

1. Aleandri MP, Magro P, Chilosi G. 2007. Modulation of host pH during the wheat-Fusarium culmorum interaction and its influence on the production and activity of pectolytic enzymes. Plant Pathology 56 : 517 525.
2. Annis SL, Goodwin PH. 1997. Recent advances in the molecular genetics of plant cell wall-degrading enzymes produced by plant pathogenic fungi. European Journal of Plant Pathology 103 : 1 14.
3. Ansari KI, Walter S, Brennan JM, Lemmens M, Kessans S, McGahern A, Egan D, Doohan FM. 2007. Retrotransposon and gene activation in wheat in response to mycotoxigenic and non-mycotoxigenic-associated Fusarium stress. Theoretical and Applied Genetics 114 : 927 937.
4. Aro N, Pakula T, Penttilä M. 2005. Transcriptional regulation of plant cell wall degradation by filamentous fungi. FEMS Microbiology Reviews 29 : 719 739.
5. Bai G, Shaner G. 1994. Scab of wheat: prospects for control. Plant Disease 78 : 760 766.
6. 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. European Journal of Plant Pathology 117 : 129 140.
7. Bari R, Jones JDG. 2009. Role of plant hormones in plant defence responses. Plant Molecular Biology 69 : 473 488.
8. Beliën T, Van Campenhout S, Van Acker M, Volckaert G. 2005. Cloning and characterization of two endoxylanases from the cereal phytopathogen Fusarium graminearum and their inhibition profile against endoxylanase inhibitors from wheat. Biochemical and Biophysical Research Communications 327 : 407 414.
9. 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. Functional & Integrative Genomics 7 : 69 77.
10. Blanchette RA. 1991. Delignification by wood-decay fungi. Annual Review of Phytopathology 29 : 381 403.
11. Blein J-P, Coutos-Thévenot P, Marion D, Ponchet M. 2002. From elicitins to lipid-transfer proteins: a new insight in cell signalling involved in plant defence mechanisms. Trends in Plant Science 7 : 293 296.
12. Bluhm BH, Zhao X, Flaherty JE, Xu JR, Dunkle LD. 2007. RAS2 regulates growth and pathogenesis in Fusarium graminearum. Molecular Plant-Microbe Interactions 20 : 627 636.
13. Boddu J, Cho S, Kruger WM, Muehlbauer GJ. 2006. Transcriptome analysis of the barley-Fusarium graminearum interaction. Molecular Plant-Microbe Interactions 19 : 407 417.
14. Boddu J, Cho S, Muehlbauer GJ. 2007. Transcriptome analysis of trichothecene-induced gene expression in barley. Molecular Plant-Microbe Interactions 20 : 1364 1375.
15. Boyacloǧlu D, Hettiarachchy NS. 1995. Changes in some biochemical components of wheat grain that was infected with Fusarium graminearum. Journal of Cereal Science 21 : 57 62.
16. Buerstmayr H, Ban T, Anderson JA. 2009. QTL mapping and marker-assisted selection for Fusarium head blight resistance in wheat: a review. Plant Breeding 128 : 1 26.
17. Bushnell WR. 2001. What is known about infection pathways in Fusarium head blight. In : S.M. Canty, J. Lewis, L. Siler, R.W. Ward, eds. National Fusarium head blight forum proceedings. Erlanger, KY, USA : US Wheat & Barley Scab Initiative, 105.
18. Bushnell WR, Hazen BE, Pritsch C. 2003. Histology and physiology of Fusarium head blight. In : Leonard KJ, Bushnell WR, eds. Fusarium head blight of wheat and barley. St Paul, MN, USA : APS Press, 44 83.
19. Bushnell WR, Seeland TM, Perkins-Veazie P, Krueger DE, Collins J, Russo VM. 2004. The effects of deoxynivalenol on barley leaf tissue. In : Tsuyumu S, Leach JE, Shiraishi T, Wolpert T, eds. Genomic and genetic analysis of plant parasitism and defense. The American Phytopathological Society, St Paul, MN, USA : APS Press, 270 281.
20. Carlson A, Skadsen R, Kaeppler H. 2006. Barley hordothionin accumulates in transgenic oat seeds and purified protein retains anti-fungal properties in vitro. In Vitro Cellular & Developmental Biology 42 : 318 323.
21. Carpita NC. 1996. Structure and biogenesis of the cell walls of grasses. Annual Review of Plant Physiology and Plant Molecular Biology 47 : 445 476.
22. Caruso C, Caporale C, Chilosi G, Vacca F, Bertini L, Magro P, Poerio E, Buonocore V. 1996. Structural and antifungal properties of a pathogenesis-related protein from wheat kernel. Journal of Protein Chemistry 15 : 35 44.
23. Caruso C, Chilosi G, Caporale C, Leonardi L, Bertini L, Magro P, Buonocore V. 1999. Induction of pathogenesis-related proteins in germinating wheat seeds infected with Fusarium culmorum. Plant Science 140 : 87 97.
24. Chen WP, Chen PD, Liu Z, Kynast R, Friebe B, Velazhahan R, Muthukrishnan S, Gill BS. 1999. Development of wheat scab symptoms is delayed in transgenic wheat plants that constitutively express a rice thaumatin-like protein gene. Theoretical and Applied Genetics 99 : 755 760.
25. Chen X, Steed A, Harden C, Nicholson P. 2006. Characterization of Arabidopsis thaliana-Fusarium graminearum interactions and identification of variation in resistance among ecotypes. Molecular Plant Pathology 7 : 391 403.
26. Chen X, Steed A, Travella S, Keller B, Nicholson P. 2009. Fusarium graminearum exploits ethylene signalling to colonize dicotyledonous and monocotyledonous plants. New Phytologist 182 : 975 983.
27. Colhoun J, Taylor GS, Tomlinson R. 1968. Fusarium diseases of cereals II. Infection of seedlings by F. culmorum and F. avenaceum in relation to environmental factors. Transactions of the British Mycological Society 51 : 397 404.
28. Cuomo CA, Güldener U, Xu JR, Trail F, Turgeon BG, Di Pietro A, Walton JD, Ma LJ, Baker SE, Rep M et al. 2007. The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317 : 1400 1402.
29. Cuthbert P, Somers D, 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.). Theoretical and Applied Genetics 112 : 1465 1472.
30. 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. Molecular Plant Pathology 9 : 697 704.
31. De Gara L, de Pinto MC, Tommasi F. 2003. The antioxidant systems vis-à-vis reactive oxygen species during plant-pathogen interaction. Plant Physiology and Biochemistry 41 : 863 870.
32. Desmond OJ, CI E, Manners JM, MacLean DJ, Schenk PM, Kazan K. 2006. Methyl jasmonate induced gene expression in wheat delays symptom development by the crown rot pathogen Fusarium pseudograminearum. Physiological and Molecular Plant Pathology 67 : 171 179.
33. Desmond OJ, Manners JM, Stephens AE, MacLean DJ, Schenk PM, Gardiner DM, Munn AL, Kazan K. 2008. The Fusarium mycotoxin deoxynivalenol elicits hydrogen peroxide production, programmed cell death and defence responses in wheat. Molecular Plant Pathology 9 : 435 445.
34. DeZwaan TM, Carroll AM, Valent B, Sweigard JA. 1999. Magnaporthe grisea Pth11p is a novel plasma membrane protein that mediates sppressorium fifferentiation in response to inductive dubstrate vues. Plant Cell 11 : 2013 2030.
35. Dickson JG, Johann H, Wineland G. 1921. Second progress report on the Fusarium head blight (scab) on wheat. Phytopathology 11 : 35.
36. Ding S, Mehrabi R, Koten C, Kang Z, Wei Y, Seong K, Kistler HC, Xu J-R. 2009. Transducin beta-like gene FTL1 is essential for pathogenesis in Fusarium graminearum. Eukaryotic Cell 8 : 867 876.
37. Divon HH, Fluhr R. 2007. Nutrition acquisition strategies during fungal infection of plants. FEMS Microbiology Letters 266 : 65 74.
38. Dixon RA, Paiva NL. 1995. Stress-induced phenylpropanoid metabolism. Plant Cell 7 : 1085 1097.
39. Doares SH, Syrovets T, Weiler EW, Ryan CA. 1995. Oligogalacturonides and chitosan activate plant defensive genes through the octadecanoid pathway. Proceedings of the National Academy of Sciences, USA 92 : 4095 4098.
40. El-Gendy W, Brownleader MD, Ismail H, Clarke PJ, Gilbert J, El-Bordiny F, Trevan M, Hopkins J, Naldrett M, Jackson P. 2001. Rapid deposition of wheat cell wall structural proteins in response to Fusarium-derived elicitors. Journal of Experimental Botany 54 : 85 90.
41. Friebe A, Vilich V, Hennig L, Kluge M, Sicker D. 1998. Detoxification of benzoxazolinone allelochemicals from wheat by Gaeumannomyces graminis var. tritici, G. graminis var. graminis, G. graminis var. avenae, and Fusarium culmorum. Applied Environmental Microbiology 64 : 2386 2391.
42. Fung F, Clark RF. 2004. Health effects of mycotoxins: a toxicological overview. Journal of Toxicology: Clinical Toxicology 42 : 217 234.
43. Gardiner DM, Kazan K, Manners JM. 2009a. Nutrient profiling reveals potent inducers of trichothecene biosynthesis in Fusarium graminearum. Fungal Genetics and Biology 46 : 604 613.
44. Gardiner DM, Osborne S, Kazan K, Manners JM. 2009b. Low pH regulates the production of deoxynivalenol by Fusarium graminearum. Microbiology 155 : 3149 3156.
45. Gebruers K, Brijs K, Courtin CM, Fierens K, Goesaert H, Rabijns A, Raedschelders G, Robben J, Sansen S, Sørensen JF et al. 2004. Properties of TAXI-type endoxylanase inhibitors. Biochimica et Biophysica Acta 1696 : 213 221.
46. Geddes J, Eudes F, Laroche A, Selinger LB. 2008. Differential expression of proteins in response to the interaction between the pathogen Fusarium graminearum and its host, Hordeum vulgare. Proteomics 8 : 545 554.
47. 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 Biotechnology Journal 5 : 38 49.
48. Grant M, Lamb C. 2006. Systemic immunity. Current Opinion in Plant Biology 9 : 414 420.
49. Greenshields DL, Liu G, Feng J, Selvaraj G, Wei Y. 2007. The siderophore biosynthetic gene SID1, but not the ferroxidase gene FET3, is required for full Fusarium graminearum virulence. Molecular Plant Pathology 8 : 411 421.
50. Güldener U, Seong K-Y, Boddu J, Cho S, Trail F, Xu J-R, Adam G, Mewes H-W, Muehlbauer GJ, Kistler HC. 2006. Development of a Fusarium graminearum Affymetrix GeneChip for profiling fungal gene expression in vitro and in planta. Fungal Genetics and Biology 43 : 316 325.
51. Guo X-m, Chen Y-f, Li C-l, Ren H-l. 2007. Effects of Fusarium graminearum crude toxin on MDA contents and SOD and PAL activities in the seedlings of different wheat varieties. Xibei Zhiwu Xuebao 27 (1 68 73.
52. 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. Physiological and Molecular Plant Pathology 66 : 119 133.
53. Hill-Ambroz K, Webb CA, Matthews AR, Li WL, Gill BS, Fellers JP. 2006. Expression Analysis and Physical Mapping of a cDNA Library of Fusarium Head Blight Infected Wheat Spikes. Crop Science 46 (S1 S15 S26.
54. Hou Z, Xue C, Peng Y, Katan T, Kistler HC, Xu JR. 2002. A mitogen-activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Molecular Plant-Microbe Interactions 15 : 1119 1127.
55. 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 Physiology 45 : 1347 1360.
56. Igawa T, Tokai T, Kudo T, Yamaguchi I, Kimura M. 2005. A wheat xylanase inhibitor gene, Xip-I, but not Taxi-I, is significantly induced by biotic and abiotic signals that trigger plant defense. Bioscience, Biotechnology, and Biochemistry 69 : 1058 1063.
57. Jackson SL, Heath IB. 1993. Roles of calcium ions in hyphal tip growth. Microbiology and Molecular Biology Reviews 57 : 367 382.
58. Jansen C, von Wettstein D, Schäfer W, Kogel K-H, Felk A, Maier FJ. 2005. Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum. Proceedings of the National Academy of Sciences, USA 102 : 16892 16897.
59. Jenczmionka NJ, Schäfer W. 2005. The Gpmk1 MAP kinase of Fusarium graminearum regulates the induction of specific secreted enzymes. Current Genetics 47 : 29 36.
60. Jenczmionka NJ, Maier FJ, Lösch AP, Schäfer W. 2003. Mating, conidiation and pathogenicity of Fusarium graminearum, the main causal agent of the head-blight disease of wheat, are regulated by the MAP kinase gpmk1. Current Genetics 43 : 87 95.
61. Jetter R, Kunst L, Samuels AL. 2006. Composition of Plant Cuticular Waxes. In : Riederer M, Müller C, eds. Biology of the plant cuticle. Oxford, UK : Blackwell, 145 181.
62. Johal GS, Gray J, Gruis D, Briggs SP. 1995. Convergent insights into mechanisms determining disease and resistance response in plant-fungal interactions. Canadian Journal of Botany 1 : 468 474.
63. Kang Z, Buchenauer H. 2000a. Cytology and ultrastructure of the infection of wheat spikes by Fusarium culmorum. Mycological Research 104 : 1083 1093.
64. Kang Z, Buchenauer H. 2000b. Ultrastructural and cytochemical studies on cellulose, xylan and pectin degradation in wheat spikes infected by Fusarium culmorum. Journal of Phytopathology 148 : 263 275.
65. Kang Z, Buchenauer H. 2000c. Ultrastructural and immunocytchemical investigation of pathogen development and host responses in resistant and susceptible wheat spikes infected by Fusarium culmorum. Physiological and Molecular Plant Pathology 57 : 255 268.
66. Kang Z, Buchenauer H. 2003. Immunocytochemical localization of cell wall-bound thionins and hydroxyproline-rich glycoproteins in Fusarium culmorum-infected wheat spikes. Journal of Phytopathology 151 : 120 129.
67. Kimura M, Tokai T, Takahashi-Ando N, Ohsato S, Fujimura M. 2007. Molecular and genetic studies of Fusarium trichothecene biosynthesis: pathways, genes, and evolution. Bioscience Biotechnology, and Biochemistry 71 : 2105 2123.
68. Kirby EJM. 2002. Botany of the wheat plant. In : Curtis BC, Rajaram S, Gómez Macpherson H, eds. Bread wheat: improvement and production. Rome, Italy : Food and Agriculture organization of the United Nations, 19 38.
69. Klepacka J, Fornal ł. 2006. Ferulic acid and its position among the phenolic compounds of wheat. Critical Reviews in Food Science and Nutrition 46 : 639 647.
70. Krishnamurthy K, Balconi C, Sherwood JE, Giroux MJ. 2001. Wheat puroindolines enhance fungal disease resistance in transgenic rice. Molecular Plant-Microbe Interactions 14 : 1255 1260.
71. Lamb C, Dixon RA. 1997. The oxidative burst in plant disease resistance. Annual Review of Plant Physiology and Plant Molecular Biology 48 : 251 275.
72. Lay FT, Anderson MA. 2005. Defensins - components of the innate immune system in plants. Current Protein & Peptide Science 6 : 85 101.
73. Lemmens M, Scholz U, Berthiller F, Dall Asta C, Koutnik A, Schuhmacher R, Adam G, Buerstmayr H, Mesterházy Á, Krska R et al. 2005. The ability to detoxify the mycotoxin deoxynivalenol colocalizes with a major quantitative trait locus for Fusarium head blight resistance in wheat. Molecular Plant-Microbe Interactions 18 : 1318 1324.
74. Lewandowski SM, Bushnell WR, Evans CK. 2006. Distribution of mycelial colonies and lesions in field-grown barley inoculated with Fusarium graminearum. Phytopathology 96 : 567 581.
75. Li G, Yen Y. 2008. Jasmonate and ethylene signaling pathway may mediate Fusarium head blight resistance in wheat. Crop Science 48 : 1888 1896.
76. 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. Theoretical and Applied Genetics 102 : 353 362.
77. Lifeng C, Yuli S, Yonggao X, Li N, Langlai X. 1997. Comparison for activities of superoxide dismutase and catalase between Scab-resistant and susceptible wheat varieties. Acta Phytopathologica Sinica 27 : 209 213.
78. Lin FY, Lu QX, Xu JH, Shi JR. 2008. Cloning and expression analysis of two salt and Fusarium graminearum stress associated UDP-glucosyltransferases genes in wheat. (Article in Chinese.) Yi Chuan 30 : 1608 1614.
79. van Loon LC, Rep M, Pieterse CMJ. 2006. Significance of inducible defense-related proteins in infected plants. Annual Review of Phytopathology 44 : 135 162.
80. Maier FJ, Miedaner T, Hadeler B, Felk A, Salomon S, Lemmens M, Kassner H, Schäfer W. 2006. Involvement of trichothecenes in fusarioses of wheat, barley and maize evaluated by gene disruption of the trichodiene synthase (Tri5) gene in three field isolates of different chemotype and virulence. Molecular Plant Pathology 7 : 449 461.
81. 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. Molecular Plant-Microbe Interactions 19 : 123 129.
82. Marchant R. 1966. Wall structure and spore germination in Fusarium culmorum. Annals of Botany 30 : 821 830.
83. Marchant R, White MF. 1966. Spore swelling and germination in Fusarium culmorum. Journal of General Microbiology 42 : 237 245.
84. McKeehen JD, Busch RH, Fulcher RG. 1999. Evaluation of wheat (Triticum aestivum L.) phenolic acids during grain development and their contribution to Fusarium resistance. Journal of Agricultural and Food Chemistry 47 : 1476 1482.
85. McLaughlin CS, Vaughan MH, Campbell IM, Wei CM, Stafford ME, Hansen BS. 1977. Inhibition of protein synthesis by trichothecenes. In : Rodricks JV, Hesseltine CW, Mehlman MA, eds. Mycotoxins in human and animal health (Proceedings of a conference on mycotoxins in human and animal health). Illinois, IL, USA : Pathotox Publishers, 263 273.
86. Michniewicz M, Czerwinska E, Rozej B, Bobkiewicz W. 1983. Control of growth and development of isolates of Fusarium culmorum (W.G.Sm.) Sacc. of different pathogenicity to wheat seedlings by plant growth regulators. II. ethylene. Acta Physiologiae Plantarum 5 : 189 198.
87. Michniewicz M, Czerwinska E, Rozej B. 1990. Interaction of abscisic acid and ethylene in relation to disease development in wheat seedlings infected by Fusarium culmorum (W.G.Sm.) Sacc. Acta Physiologiae Plantarum 12 : 41 48.
88. Miller JD, Ewen MA. 1997. Toxic effects of deoxynivalenol on ribosomes and tissues of the spring wheat cultivars Frontana and Casavant. Natural Toxins 5 : 234 237.
89. Mitterbauer R, Adam G. 2002. Saccharomyces cerevisae and Arabidopsis thaliana: useful model systems for the identification of molecular mechanisms involved in resistance of plants to toxins. European Journal of Plant Pathology 108 : 699 703.
90. Mohammadi M, Kazemi H. 2002. Changes in peroxidase and polyphenol oxidase activities in susceptible and resistant wheat heads inoculated with Fusarium graminearum and induced resistance. Plant Science 162 : 491 498.
91. Nganje WE, Kaitibie S, Wilson WW, Leistritz FL, Bangsund DA. 2004. Economic impacts of Fusarium head blight in wheat and barley: 1993-2001. In : Department of Agribusiness and Applied Economics, Agricultural Experiment Station, ed. Agribusiness and applied economics report. Fargo, ND, USA : North Dakota State University, 62.
92. Ochiai N, Tokai T, Nishiuchi T., Takahashi-Ando N, Fujimura M, Kimura M. 2007. Involvement of the osmosensor histidine kinase and osmotic stress-activated protein kinases in the regulation of secondary metabolism in Fusarium graminearum. Biochemical and Biophysical Research Communications 363 : 639 644.
93. Paper JM, Scott-Craig JS, Adhikari ND, Cuomo CA, Walton JD. 2007. Comparative proteomics of extracellular proteins in vitro and in planta from the pathogenic fungus Fusarium graminearum. Proteomics 7 : 3171 3183.
94. Paranidharan V, Abu-Nada Y, Hamzehzarghani H, Kushalappa AC, Mamer O, Dion Y, Rioux S, Comeau A, Choiniere L. 2008. Resistance-related metabolites in wheat against Fusarium graminearum and the virulence factor deoxynivalenol (DON). Botany-Botanique 86 : 1168 1179.
95. Parry DW, Jenkinson P, McLeod L. 1995. Fusarium ear blight (scab) in small grain cereals - a review. Plant Pathology 44 : 207 238.
96. Pieterse CMJ, van Loon LC. 2004. NPR1: the spider in the web of induced resistance signaling pathways. Current Opinion in Plant Biology 7 : 456 464.
97. 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. Journal of Biological Chemistry 278 : 47905 47914.
98. 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. Molecular Plant-Microbe Interactions 13 : 159 169.
99. 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. Physiological and Molecular Plant Pathology 58 : 1 12.
100. Proctor R, Hohn T, McCormick S. 1995. Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene. Molecular Plant-Microbe Interactions 8 : 593 601.
101. Pugh GW, Johann H, Dickson JG. 1933. Factors affecting infection of wheat heads by Gibberella saubinetii. Journal of Agricultural Research 46 : 771 779.
102. Ramamoorthy V, Cahoon EB, Li J, Thokala M, Minto RE, Shah DM. 2007a. Glucosylceramide synthase is essential for alfalfa defensin-mediated growth inhibition but not for pathogenicity of Fusarium graminearum. Molecular Microbiology 66 : 771 786.
103. Ramamoorthy V, Zhao X, Snyder AK, Xu JR, Shah DM. 2007b. Two mitogen-activated protein kinase signalling cascades mediate basal resistance to antifungal plant defensins in Fusarium graminearum. Cellular Microbiology 9 : 1491 1506.
104. Reddy MVB, Arul J, Angers P, Couture L. 1999. Chitosan treatment of wheat seeds induces resistance to Fusarium graminearum and improves seed quality. Journal of Agricultural and Food Chemistry 47 : 1208 1216.
105. Ribichich KF, Lopez SE, Vegetti AC. 2000. Histopathological spikelet changes produced by Fusarium graminearum in susceptible and resistant wheat cultivars. Plant Disease 84 : 794 802.
106. Roberti S, Janni M, Pontiggia D, Gerunzi M, Favaron F, Cervone F, De Lorenzo G, D'Ovidio R. 2003. Gene characterization and chromosomal localization of polygalacturonase inhibiting proteins (PGIPs) in wheat. In : N.E. Pogna, M. Romanò, E.A. Pogna, G. Galterio, eds. Tenth international wheat genetics symposium. Paestum, Italy. 1041 1043.
107. Robert-Seilaniantz A, Navarro L, Bari R, Jones JDG. 2007. Pathological hormone imbalances. Current Opinion in Plant Biology 10 : 372 379.
108. Rocha O, Ansari K, Doohan FM. 2005. Effects of trichothecene mycotoxins on eukaryotic cells: a review. Food Additives and Contaminants 22 : 369 378.
109. Rittenour WR, Harris SD. 2008. Characterization of Fusarium graminearum Mes1 reveals roles in cell-surface organization and virulence. Fungal Genetics and Biology 45 (6 933 946.
110. Rudd JC, Horsley RD, McKendry AL, Elias EM. 2001. Host plant resistance genes for Fusarium head blight: sources, mechanisms, and utility in conventional breeding systems. Crop Science 41 : 620 627.
111. Sarlin T, Kivioja T, Linder M, Nakari-Setälä T. 2006. Identification and characterisation of hydrophobins from Fusarium graminearum. In : C. Waalwijk, ed. 9th European Fusarium seminar. Wageningen, The Netherlands, 168.
112. Sarlin T, Vilpola A, Kotaviita E, Olkku J, Haikara A. 2007. Fungal hydrophobins in the barley-to-beer chain. Journal of the Institute of Brewing 113 : 147 153.
113. Schroeder HW, Christensen JJ. 1963. Factors affecting resistance of wheat to scab caused by Gibberella zeae. Phytopathology 53 : 831 838.
114. Seong K-Y, Zhao X, Xu J-R, Güldener U, Kistler HC. 2008. Conidial germination in the filamentous fungus Fusarium graminearum. Fungal Genetics and Biology 45 : 389 399.
115. Shah J. 2005. Lipids, lipases, and lipid-modifying enzymes in plant disease resistance. Annual Review of Phytopathology 43 : 229.
116. Siranidou E, Kang Z, Buchenauer H. 2002. Studies on symptom development, phenolic compounds and morphological defence responses in wheat cultivars differing in resistance to Fusarium head blight. Journal of Phytopathology 150 : 200 208.
117. Skadhauge B, Thomsen KK, Wettstein D. 1997. The role of the barley testa layer and its flavonoid content in resistance to Fusarium infections. Hereditas 126 : 147 160.
118. Skinnes H, Tarkegne Y, Dieseth J, Bjørnstad Å. 2008. Associations between anther extrusion and Fusarium head blight in European wheat. Cereal research communications 36 : 223 231.
119. Skov J, Lemmens M, Giese H. 2004. Role of a Fusarium culmorum ABC transporter (FcABC1) during infection of wheat and barley. Physiological and Molecular Plant Pathology 64 : 245 254.
120. Slikova S, Havrlentova M, Sudyova V, Mihalik D, Gregova E. 2008. Cell wall beta-D-glucan during disease progress (Fusarium head blight) in wheat spikes. Cereal Research Communications 36 : 167 169.
121. Soanes DM, Alam I, Cornell M, Wong HM, Hedeler C, Paton NW, Rattray M, Hubbard SJ, Oliver SG, Talbot NJ. 2008. Comparative genome analysis of filamentous fungi reveals gene family expansions associated with fungal pathogenesis. PLoS One 3 : e2300.
122. Søltoft M, Jørgensen LN, Svensmark B, Fomsgaard IS. 2008. Benzoxazinoid concentrations show correlation with Fusarium head blight resistance in Danish wheat varieties. Biochemical Systematics and Ecology 36 : 245 259.
123. 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. Theoretical and Applied Genetics 118 (4 753 764.
124. Stirpe F, Battelli MG. 2006. Ribosome-inactivating proteins: progress and problems. Cellular and Molecular Life Sciences 63 : 1850 1866.
125. Strange RN, Majer JR, Smith H. 1974. The isolation and identification of choline and betaine as the two major components in anthers and wheat germ that stimulate Fusarium graminearum in vitro. Physiological and Molecular Plant Pathology 4 : 277 290.
126. Sung JM, Cook RJ. 1981. Effect of water potential on reproduction and spore germination by Fusarium roseum;'Graminearum', 'Culmorum', and 'Avenaceum'. Phytopathology 71 : 499 504.
127. Sutton JC. 1982. Epidemiology of wheat head blight and maize ear rot caused by Fusarium graminearum. The Canadian Journal of Plant Pathology 4 : 195 209.
128. Theis T, Stahl U. 2004. Antifungal proteins: targets, mechanisms and prospective applications. Cellular and Molecular Life Sciences 61 : 437 455.
129. Thevissen K, Ghazi A, De Samblanx GW, Brownlee C, Osborn RW, Broekaert WF. 1996. Fungal membrane responses induced by plant defensins and thionins. Journal of Biological Chemistry 271 : 15018 15025.
130. Tsitsigiannis DI, Keller NP. 2007. Oxylipins as developmental and host-fungal communication signals. Trends in Microbiology 15 : 109 118.
131. Voigt CA, Schäfer W, Salomon S. 2005. A secreted lipase of Fusarium graminearum is a virulence factor required for infection of cereals. Plant Journal 42 : 364 375.
132. Wagacha JM, Muthomi JW. 2007. Fusarium culmorum: infection process, mechanisms of mycotoxin production and their role in pathogenesis in wheat. Crop Protection 26 : 877 885.
133. Walter S, Brennan J, Arunachalam C, Ansari K, Hu X, Khan MR, Trognitz F, Trognitz B, Leonard G, Egan D et al. 2008. Components of the gene network associated with genotype-dependent response of wheat to the Fusarium mycotoxin deoxynivalenol. Functional & Integrative Genomics 8 : 421 427.
134. Wang Y-P, Liu Y-Q, Shi L, Pai N-S, Chen Z-L. 1993. SOD activity of wheat varieties with different resistance to scab. Acta Phytophysiologica Sinica 19 : 353 358.
135. Wanjiru WM, Kang Z, Buchenauer H. 2002. Importance of cell wall degrading enzymes produced by Fusarium graminearum during infection of wheat heads. European Journal of Plant Pathology 108 : 803 810.
136. Wasternack C. 2007. Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Annals of Botany 100 : 681 697.
137. Whetten R, Sederoff R. 1995. Lignin biosynthesis. Plant Cell 7 : 1001 1013.
138. Wojciechowski S, Chelkowski J, Kostecki M. 1995. Influence of deoxynivalenol on electrolyte leakage in cereal seedling leaves. Acta Physiologiae Plantarum 17 : 357 360.
139. Xu X, Nicholson P. 2009. Community ecology of fungal pathogens causing wheat head blight. Annual Review of Phytopathology 47 : 83 103.
140. Yoshida M, Kawada N, Tohnooka T. 2005. Effect of row type, flowering type and several other spike characters on resistance to Fusarium head blight in barley. Euphytica 141 : 217 227.
141. Yu G-Y, Muehlbauer GJ. 2001. Benzothiadiazole-induced gene expression inwheat spikes does not provide resistance to Fusarium head blight. Physiological and Molecular Plant Pathology 59 : 129 136.
142. Yu Q-L, Liu T-R, Liu Y-X, Jia G-X. 1996. Pathological anatomy of the rachis in wheat varieties with resistance against scab. Journal of the Heilongjiang August First Land Reclamation University 8 : 42 45.
143. Yu H-Y, Seo J-A, Kim J-E, Han K-H, Shim W-B, Yun S-H, Lee Y-W. 2008. Functional analyses of heterotrimeric G protein Gα and Gβ subunits in Gibberella zeae. Microbiology 154 : 392 401.
144. Zhang Y-H, Ye H-Z. 1993. A study of histology of resistance of wheat to head scab (Fusarium graminearum). Journal of Sichuan Agricultural University 11 : 444 450.
145. Zhao J, Davis LC, Verpoorte R. 2005. Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnology Advances 23 : 283 333.
146. 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.
147. 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. Theoretical and Applied Genetics 99 : 1221 1232.