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

The Fusarium species Fusarium graminearum and Fusarium culmorum, which are responsible for Fusarium head blight (FHB) disease, reduce world-wide cereal crop yield and, as a consequence of their mycotoxin production in cereal grain, impact on both human and animal health. Their study is greatly promoted by the availability of the genomic sequence of F. graminearum and transcriptomic resources for both F. graminearum and its cereal hosts. Functional genomic, proteomic and metabolomic studies, in combination with targeted mutagenesis or transgenic studies, are unravelling the complex mechanisms involved in Fusarium infection, penetration and colonization of host tissues, and host avoidance thereof. This review illuminates and integrates emerging knowledge regarding the molecular crosstalk between Fusarium and its small-grain cereal hosts. An understanding of the complexity of the host-pathogen interactions will be instrumental in designing new efficient strategies for the control of FHB disease.

[1]  R. Dixon,et al.  Stress-Induced Phenylpropanoid Metabolism. , 1995, The Plant cell.

[2]  B. Gill,et al.  Development of wheat scab symptoms is delayed in transgenic wheat plants that constitutively express a rice thaumatin-like protein gene , 1999, Theoretical and Applied Genetics.

[3]  K. Hammond-Kosack,et al.  NPR1 and EDS11 contribute to host resistance against Fusarium culmorum in Arabidopsis buds and flowers. , 2008, Molecular plant pathology.

[4]  G. Muehlbauer,et al.  Benzothiadiazole-induced gene expression in wheat spikes does not provide resistance to Fusarium head blight , 2001 .

[5]  R. Blanchette.  Delignification by wood-decay fungi , 1991 .

[6]  W. Schäfer,et al.  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 , 2003, Current Genetics.

[7]  G. Chilosi,et al.  Modulation of host pH during the wheat-Fusarium culmorum interaction and its influence on the production and activity of pectolytic enzymes , 2007 .

[8]  W. Schäfer,et al.  The Gpmk1 MAP kinase of Fusarium graminearum regulates the induction of specific secreted enzymes , 2004, Current Genetics.

[9]  B. Keller,et al.  Fusarium graminearum exploits ethylene signalling to colonize dicotyledonous and monocotyledonous plants. , 2009, The New phytologist.

[10]  R. Marchant.  Wall structure and spore germination in Fusarium culmorum. , 1966 .

[11]  Ł. Fornal,et al.  Ferulic Acid and its Position Among the Phenolic Compounds of Wheat , 2006, Critical reviews in food science and nutrition.

[12]  M. Kimura,et al.  A Wheat Xylanase Inhibitor Gene, Xip-I, but Not Taxi-I, Is Significantly Induced by Biotic and Abiotic Signals That Trigger Plant Defense , 2005, Bioscience, biotechnology, and biochemistry.

[13]  D. Somers,et al.  Systemic expression of defense response genes in wheat spikes as a response to Fusarium graminearum infection , 2001 .

[14]  J. Shi,et al.  [Cloning and expression analysis of two salt and Fusarium graminearum stress associated UDP-glucosyltransferases genes in wheat]. , 2009, Yi chuan = Hereditas.

[15]  K. Kuchler,et al.  Detoxification of the Fusarium Mycotoxin Deoxynivalenol by a UDP-glucosyltransferase from Arabidopsis thaliana* , 2003, Journal of Biological Chemistry.

[16]  Jonathan D. G. Jones,et al.  Role of plant hormones in plant defence responses , 2009, Plant Molecular Biology.

[17]  H. Schroeder,et al.  Factors affecting resistance of Wheat to scab caused by Gibberella zeae. , 1963 .

[18]  Christina A. Cuomo,et al.  The Fusarium graminearum Genome Reveals a Link Between Localized Polymorphism and Pathogen Specialization , 2007, Science.

[19]  Magnus Rattray,et al.  Comparative Genome Analysis of Filamentous Fungi Reveals Gene Family Expansions Associated with Fungal Pathogenesis , 2008, PloS one.

[20]  Jin-Rong Xu,et al.  A mitogen-activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. , 2002, Molecular plant-microbe interactions : MPMI.

[21]  Won-Bo Shim,et al.  Functional analyses of heterotrimeric G protein Gα and Gβ subunits in Gibberella zeae , 2008, Microbiology.

[22]  R. Jetter,et al.  Composition of Plant Cuticular Waxes , 2007 .

[23]  A. Laroche,et al.  Differential expression of proteins in response to the interaction between the pathogen Fusarium graminearum and its host, Hordeum vulgare , 2008, Proteomics.

[24]  M. Giroux,et al.  Wheat puroindolines enhance fungal disease resistance in transgenic rice. , 2001, Molecular plant-microbe interactions : MPMI.

[25]  Hans Goesaert,et al.  Properties of TAXI-type endoxylanase inhibitors. , 2004, Biochimica et biophysica acta.

[26]  J. Manners,et al.  Low pH regulates the production of deoxynivalenol by Fusarium graminearum. , 2009, Microbiology.

[27]  Z. Kang,et al.  Ultrastructural and immunocytochemical investigation of pathogen development and host responses in resistant and susceptible wheat spikes infected by Fusarium culmorum , 2000 .

[28]  M. Kimura,et al.  Involvement of the osmosensor histidine kinase and osmotic stress-activated protein kinases in the regulation of secondary metabolism in Fusarium graminearum. , 2007, Biochemical and biophysical research communications.

[29]  S. Briggs,et al.  CONVERGENT INSIGHTS INTO MECHANISMS DETERMINING DISEASE AND RESISTANCE RESPONSE IN PLANT-FUNGAL INTERACTIONS , 1995 .

[30]  A. Steed,et al.  Characterization of Arabidopsis thaliana-Fusarium graminearum interactions and identification of variation in resistance among ecotypes. , 2006, Molecular plant pathology.

[31]  M. Kimura,et al.  Molecular and Genetic Studies of Fusarium Trichothecene Biosynthesis: Pathways, Genes, and Evolution , 2007, Bioscience, biotechnology, and biochemistry.

[32]  J. Manners,et al.  Nutrient profiling reveals potent inducers of trichothecene biosynthesis in Fusarium graminearum. , 2009, Fungal genetics and biology : FG & B.

[33]  Merja Penttilä,et al.  Transcriptional regulation of plant cell wall degradation by filamentous fungi. , 2005, FEMS microbiology reviews.

[34]  W. Bushnell,et al.  Histology and physiology of Fusarium head blight. , 2003 .

[35]  T. Tohnooka,et al.  Effect of row type, flowering type and several other spike characters on resistance to Fusarium head blight in barley , 2005, Euphytica.

[36]  N. Keller,et al.  Oxylipins as developmental and host-fungal communication signals. , 2007, Trends in microbiology.

[37]  D. Parry,et al.  Fusarium ear blight (scab) in small grain cereals—a review , 1995 .

[38]  Z. Berzsényi,et al.  Effect of various crop production factors on the yield and yield stability of maize in a long-term experiment , 2008 .

[39]  H. Macpherson,et al.  Bread wheat: improvement and production. , 2002 .

[40]  Hans-Werner Mewes,et al.  Development of a Fusarium graminearum Affymetrix GeneChip for profiling fungal gene expression in vitro and in planta. , 2006, Fungal genetics and biology : FG & B.

[41]  G. Volckaert,et al.  Cloning and characterization of two endoxylanases from the cereal phytopathogen Fusarium graminearum and their inhibition profile against endoxylanase inhibitors from wheat. , 2005, Biochemical and biophysical research communications.

[42]  M. Lemmens,et al.  Differential gene expression of related wheat lines with contrasting levels of head blight resistance after Fusarium graminearum inoculation , 2009, Theoretical and Applied Genetics.

[43]  C. Brownlee,et al.  Fungal Membrane Responses Induced by Plant Defensins and Thionins* , 1996, The Journal of Biological Chemistry.

[44]  P. Goodwin,et al.  Recent advances in the molecular genetics of plant cell wall-degrading enzymes produced by plant pathogenic fungi , 1997, European Journal of Plant Pathology.

[45]  A. Laroche,et al.  Identification of differentially regulated proteins in response to a compatible interaction between the pathogen Fusarium graminearum and its host, Triticum aestivum , 2006, Proteomics.

[46]  J. C. Sutton,et al.  Epidemiology of wheat head blight and maize ear rot caused by Fusarium graminearum , 1982 .

[47]  R. Krska,et al.  The ability to detoxify the mycotoxin deoxynivalenol colocalizes with a major quantitative trait locus for Fusarium head blight resistance in wheat. , 2005, Molecular plant-microbe interactions : MPMI.

[48]  J. Rudd,et al.  Host Plant Resistance Genes for Fusarium Head Blight: Sources, Mechanisms, and Utility in Conventional Breeding Systems , 2001 .

[49]  K. Ansari,et al.  Effects of trichothecene mycotoxins on eukaryotic cells: A review , 2005, Food additives and contaminants.

[50]  Guosheng Liu,et al.  The siderophore biosynthetic gene SID1, but not the ferroxidase gene FET3, is required for full Fusarium graminearum virulence. , 2007, Molecular plant pathology.

[51]  D. Somers,et al.  Fungal development and induction of defense response genes during early infection of wheat spikes by Fusarium graminearum. , 2000, Molecular plant-microbe interactions : MPMI.

[52]  Z. Kang,et al.  Cytology and ultrastructure of the infection of wheat spikes by Fusarium culmorum , 2000 .

[53]  J. Gilbert,et al.  Microarray analysis of Fusarium graminearum-induced wheat genes: identification of organ-specific and differentially expressed genes. , 2007, Plant biotechnology journal.

[54]  Markus Riederer,et al.  Biology of the plant cuticle , 2006 .

[55]  E. Conti,et al.  Fusarium head blight evaluation in wheat transgenic plants expressing the maize b-32 antifungal gene , 2007, European Journal of Plant Pathology.

[56]  A. Haikara,et al.  Fungal Hydrophobins in the Barley-to-Beer Chain , 2007 .

[57]  M. Kimura,et al.  New TAXI-type xylanase inhibitor genes are inducible by pathogens and wounding in hexaploid wheat. , 2004, Plant & cell physiology.

[58]  V. Buonocore,et al.  Structural and antifungal properties of a pathogenesis-related protein from wheat kernel , 1996, Journal of protein chemistry.

[59]  K. F. Ribichich,et al.  Histopathological Spikelet Changes Produced by Fusarium graminearum in Susceptible and Resistant Wheat Cultivars. , 2000, Plant disease.

[60]  I. Fomsgaard,et al.  Benzoxazinoid concentrations show correlation with Fusarium Head Blight resistance in Danish wheat varieties , 2008 .

[61]  K. K. Thomsen,et al.  The role of the barley testa layer and its flavonoid content in resistance to Fusarium infections , 2004 .

[62]  R. Clark,et al.  Health Effects of Mycotoxins: A Toxicological Overview , 2004, Journal of toxicology. Clinical toxicology.

[63]  Sarah A Kessans,et al.  Retrotransposon and gene activation in wheat in response to mycotoxigenic and non-mycotoxigenic-associated Fusarium stress , 2007, Theoretical and Applied Genetics.

[64]  H. Buchenauer,et al.  Importance of Cell Wall Degrading Enzymes Produced by Fusarium graminearum during Infection of Wheat Heads , 2002, European Journal of Plant Pathology.

[65]  M. Mohammadi,et al.  Changes in peroxidase and polyphenol oxidase activities in susceptible and resistant wheat heads inoculated with Fusarium graminearum and induced resistance , 2002 .

[66]  Xinhua Zhao,et al.  Two mitogen‐activated protein kinase signalling cascades mediate basal resistance to antifungal plant defensins in Fusarium graminearum , 2007, Cellular microbiology.

[67]  J. Anderson,et al.  QTL mapping and marker-assisted selection for Fusarium head blight resistance in wheat: A review , 2009 .

[68]  D. Shah,et al.  Glucosylceramide synthase is essential for alfalfa defensin‐mediated growth inhibition but not for pathogenicity of Fusarium graminearum , 2007, Molecular microbiology.

[69]  J. Sweigard,et al.  Magnaporthe grisea Pth11p Is a Novel Plasma Membrane Protein That Mediates Appressorium Differentiation in Response to Inductive Substrate Cues , 1999, Plant Cell.

[70]  J. Chełkowski,et al.  Influence of deoxynivalenol on elektrolyte leakage in cereal seedling leaves , 1995 .

[71]  S. Harris,et al.  Characterization of Fusarium graminearum Mes1 reveals roles in cell-surface organization and virulence. , 2008, Fungal genetics and biology : FG & B.

[72]  J. Wagacha,et al.  Fusarium culmorum: Infection process, mechanisms of mycotoxin production and their role in pathogenesis in wheat , 2007 .

[73]  A. Kushalappa,et al.  Resistance-related metabolites in wheat against Fusarium graminearum and the virulence factor deoxynivalenol (DON) , 2008 .

[74]  F. Leistritz,et al.  ECONOMIC IMPACTS OF FUSARIUM HEAD BLIGHT IN WHEAT AND BARLEY: 1993-2001 , 2001 .

[75]  E. Weiler,et al.  Oligogalacturonides and chitosan activate plant defensive genes through the octadecanoid pathway. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[76]  J. Shah.  Lipids, lipases, and lipid-modifying enzymes in plant disease resistance. , 2005, Annual review of phytopathology.

[77]  Guihua Bai,et al.  Fusarium graminearum-induced changes in gene expression between Fusarium head blight-resistant and susceptible wheat cultivars , 2006, Functional & Integrative Genomics.

[78]  R. Dixon,et al.  THE OXIDATIVE BURST IN PLANT DISEASE RESISTANCE. , 1997, Annual review of plant physiology and plant molecular biology.

[79]  McKeehen Jd,et al.  Evaluation of wheat (Triticum aestivum L.) phenolic acids during grain development and their contribution to Fusarium resistance. , 1999 .

[80]  Z. Kang,et al.  Ultrastructural and Cytochemical Studies on Cellulose, Xylan and Pectin Degradation in Wheat Spikes Infected by Fusarium culmorum , 2000 .

[81]  Xiang-ming Xu,et al.  Community ecology of fungal pathogens causing wheat head blight. , 2009, Annual review of phytopathology.

[82]  H. Giese,et al.  Role of a Fusarium culmorum ABC transporter (FcABC1) during infection of wheat and barley , 2004 .

[83]  J. Miller,et al.  Toxic effects of deoxynivalenol on ribosomes and tissues of the spring wheat cultivars Frontana and Casavant. , 1997, Natural toxins.

[84]  Xinhua Zhao,et al.  RAS2 regulates growth and pathogenesis in Fusarium graminearum. , 2007, Molecular plant-microbe interactions : MPMI.

[85]  G. Bai,et al.  Scab of wheat: prospects for control. , 1994 .

[86]  D. Marion,et al.  From elicitins to lipid-transfer proteins: a new insight in cell signalling involved in plant defence mechanisms. , 2002, Trends in plant science.

[87]  G. Adam,et al.  Saccharomyces cerevisae and Arabidopsis thaliana: Useful model systems for the identification of molecular mechanisms involved in resistance of plants to toxins , 2002 .

[88]  R. Cook,et al.  Effect of water potential on reproduction and spore germination by Fusarium roseum 'Graminearum,' 'Culmorum,' and 'Avenaceum'. , 1981 .

[89]  Jin-Rong Xu,et al.  Transducin Beta-Like Gene FTL1 Is Essential for Pathogenesis in Fusarium graminearum , 2009, Eukaryotic Cell.

[90]  R. Proctor,et al.  Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene. , 1995, Molecular plant-microbe interactions : MPMI.

[91]  A. Comeau,et al.  Metabolic profiling and factor analysis to discriminate quantitative resistance in wheat cultivars against fusarium head blight , 2005 .

[92]  J. Leach,et al.  Genomic And Genetic Analysis Of Plant Parasitism And Defense , 2003 .

[93]  G. Muehlbauer,et al.  Transcriptome analysis of trichothecene-induced gene expression in barley. , 2007, Molecular plant-microbe interactions : MPMI.

[94]  Jonathan D. G. Jones,et al.  Pathological hormone imbalances. , 2007, Current opinion in plant biology.

[95]  C. K. Evans,et al.  Distribution of Mycelial Colonies and Lesions in Field-Grown Barley Inoculated with Fusarium graminearum. , 2006, Phytopathology.

[96]  Z. Kang,et al.  Immunocytochemical Localization of Cell Wall-Bound Thionins and Hydroxyproline-Rich Glycoproteins in Fusarium culmorum-Infected Wheat Spikes , 2003 .

[97]  F. Trognitz,et al.  Components of the gene network associated with genotype-dependent response of wheat to the Fusarium mycotoxin deoxynivalenol , 2008, Functional & Integrative Genomics.

[98]  L. Gara,et al.  The antioxidant systems vis-à-vis reactive oxygen species during plant–pathogen interaction , 2003 .

[99]  M. Lemmens,et al.  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. , 2006, Molecular plant pathology.

[100]  Christina A. Cuomo,et al.  Comparative proteomics of extracellular proteins in vitro and in planta from the pathogenic fungus Fusarium graminearum , 2007, Proteomics.

[101]  J. Manners,et al.  The Fusarium mycotoxin deoxynivalenol elicits hydrogen peroxide production, programmed cell death and defence responses in wheat. , 2008, Molecular plant pathology.

[102]  P. Angers,et al.  Chitosan treatment of wheat seeds induces resistance to Fusarium graminearum and improves seed quality. , 1999, Journal of agricultural and food chemistry.

[103]  P. J. Clarke,et al.  Rapid deposition of wheat cell wall structural proteins in response to Fusarium-derived elicitors. , 2001, Journal of experimental botany.

[104]  M. Anderson,et al.  Defensins--components of the innate immune system in plants. , 2005, Current protein & peptide science.

[105]  Jyoti Shah,et al.  Genetically engineered resistance to Fusarium head blight in wheat by expression of Arabidopsis NPR1. , 2006, Molecular plant-microbe interactions : MPMI.

[106]  D. Somers,et al.  Fine mapping Fhb1, a major gene controlling fusarium head blight resistance in bread wheat (Triticum aestivum L.) , 2006, Theoretical and Applied Genetics.

[107]  C. Wasternack,et al.  Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. , 2007, Annals of botany.

[108]  U. Stahl,et al.  Antifungal proteins: targets, mechanisms and prospective applications , 2004, Cellular and Molecular Life Sciences CMLS.

[109]  B. Gill,et al.  Expression Analysis and Physical Mapping of a cDNA Library of Fusarium Head Blight Infected Wheat Spikes , 2006 .

[110]  F. Stirpe,et al.  Ribosome-inactivating proteins: progress and problems , 2006, Cellular and Molecular Life Sciences CMLS.

[111]  Karl-Heinz Kogel,et al.  Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[112]  D. Boyacioğlu,et al.  Changes in some biochemical components of wheat grain that was infected with Fusarium graminearum , 1995 .

[113]  D. Kudrna,et al.  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 , 1999, Theoretical and Applied Genetics.

[114]  Y. Yen,et al.  Jasmonate and Ethylene Signaling Pathway May Mediate Fusarium Head Blight Resistance in Wheat , 2008 .

[115]  I. Heath,et al.  Roles of calcium ions in hyphal tip growth. , 1993, Microbiological reviews.

[116]  R. Verpoorte,et al.  Elicitor signal transduction leading to production of plant secondary metabolites. , 2005, Biotechnology advances.

[117]  G. Muehlbauer,et al.  Transcriptome analysis of the barley-Fusarium graminearum interaction. , 2006, Molecular plant-microbe interactions : MPMI.

[118]  M. Kluge,et al.  Detoxification of Benzoxazolinone Allelochemicals from Wheat byGaeumannomyces graminis var. tritici, G. graminis var. graminis, G. graminis var.avenae, and Fusarium culmorum , 1998, Applied and Environmental Microbiology.

[119]  N. Carpita.  STRUCTURE AND BIOGENESIS OF THE CELL WALLS OF GRASSES. , 1996, Annual review of plant physiology and plant molecular biology.

[120]  H. Smith,et al.  The isolation and identification of choline and betaine as the two major components in anthers and wheat germ that stimulate Fusarium graminearum in vitro , 1974 .

[121]  R. Marchant,et al.  Spore swelling and germination in Fusarium culmorum. , 1966, Journal of general microbiology.

[122]  V. Buonocore,et al.  Induction of pathogenesis-related proteins in germinating wheat seeds infected with Fusarium culmorum☆ , 1999 .

[123]  C. Pieterse,et al.  NPR1: the spider in the web of induced resistance signaling pathways. , 2004, Current opinion in plant biology.

[124]  B. Rožej,et al.  Interaction of abscisic acid and ethylene in relation to disease development in wheat seedlings infected by Fusarium culmorum (W. G. Sm.) Sacc. , 1990 .

[125]  H. Kaeppler,et al.  Barley hordothionin accumulates in transgenic oat seeds and purified protein retains anti-fungal properties in vitro , 2006, In Vitro Cellular & Developmental Biology - Plant.

[126]  J. Manners,et al.  Methyl jasmonate induced gene expression in wheat delays symptom development by the crown rot pathogen Fusarium pseudograminearum , 2005 .

[127]  R. Tomlinson,et al.  Fusarium diseases of cereals: II. Infection of seedlings by F. Culmorum and F. Avenaceum in relation to environmental factors , 1968 .

[128]  C. Pieterse,et al.  Significance of inducible defense-related proteins in infected plants. , 2006, Annual review of phytopathology.

[129]  Z. Kang,et al.  Studies on Symptom Development, Phenolic Compounds and Morphological Defence Responses in Wheat Cultivars Differing in Resistance to Fusarium Head Blight , 2002 .

[130]  C. Voigt,et al.  A secreted lipase of Fusarium graminearum is a virulence factor required for infection of cereals. , 2005, The Plant journal : for cell and molecular biology.

[131]  B. Gill,et al.  Isolation and characterization of novel cDNA clones of acidic chitinases and β-1,3-glucanases from wheat spikes infected by Fusarium graminearum , 2001, Theoretical and Applied Genetics.

[132]  Associations between anther extrusion and Fusarium Head Blight in European wheat , 2008 .

[133]  U. Güldener,et al.  Conidial germination in the filamentous fungus Fusarium graminearum. , 2008, Fungal genetics and biology : FG & B.