Advertisement

Tropical Plant Pathology

, Volume 42, Issue 3, pp 175–183 | Cite as

Deoxynivalenol resistance as a component of FHB resistance

  • L. R. Gunupuru
  • A. Perochon
  • F. M. Doohan
Open Access
Review

Abstract

Fusarium head blight (FHB) is one of the most devastating diseases of wheat (Triticum aestivum), barley (Hordeum vulgare) and other small grain cereals grown in warm and humid regions worldwide. In addition to yield loss, the disease compromises the quality of infected grain as a result of contamination with a range of Fusarium mycotoxins that are harmful to human and animal health. Deoxynivalenol (DON) is the most prevalent trichothecene mycotoxin found in Fusarium-infected grains. DON acts as a virulence factor for Fusarium, facilitating disease spread within wheat heads. Resistance to DON is an innate component of FHB resistance. Here we review FHB as a globally important disease, with a specific focus on the role of DON in disease development, the importance of its’ resistance in plant defence against Fusarium and the current knowledge regarding the genes activated as part of the cereal defence against the toxin.

Keywords

Barley Deoxynivalenol (DON) Fusarium culmorum Fusarium graminearum Fusarium head blight (FHB) Fhb1 Multi-drug resistance (MDR) ABC transporter Plant resistance UDP-glucosyltransferase (UGT) Wheat 

Introduction

Fusarium head blight (FHB) is a devastating disease of small grain cereals caused by Fusarium spp. that reduce the yield and contaminates grain with mycotoxins that are harmful to human and animal health (Desjardins 2006; Osborne and Stein 2007; Mohanty et al. 2013). Many FHB outbreaks have been reported across Europe, America and Asia during the 20 and 21st centuries (Elias et al. 2005; Oliver et al. 2007; McMullen et al. 2012; Giroux et al. 2016). Although many species of Fusarium can cause FHB, the most common causal agents are Fusarium graminearum Schwabe and Fusarium culmorum Saccardo (Schroeder and Christensen 1963; Bai and Shaner 1994, 2004). The fungus infects wheat heads during flowering and thereby interferes with seed development, leading to shrivelled grains that may be light enough to be expelled with chaff during harvesting. The fungus destroys starch granules, storage proteins and cell walls during the invasion of grains (Bechtel et al. 1985). Fusarium spp. that infect cereal crops are able to produce several mycotoxins, but the toxin most associated associated with FHB epidemics is deoxynivalenol (DON), which belongs to a large family of mycotoxigenic sesquiterpene epoxides, namely the trichothecenes and it is commonly found in grain from FHB-diseased cereal heads. This review provides an overview on the deleterious effects of DON, its role in disease development and current knowledge regarding the genes activated as part of the cereal defence against the toxin.

The deleterious effects of DON

Trichothecenes inhibit protein biosynthesis by binding to the 60S subunit of eukaryotic ribosomes and inhibiting either the chain initiation, elongation or termination steps of protein synthesis. Either as a consequence of this, or additional to this, they also cause lipid peroxidation, programmed cell death (apoptosis), ribotoxic stress, inhibition of DNA synthesis, disruption of membrane integrity and inhibition of cell division (Schindler 1974; Carter and Cannon 1977; Azcona-Olivera et al. 1995; Shifrin and Anderson 1999; Kouadio et al. 2005; Arunachalam and Doohan 2013). Numerous studies have demonstrated the negative effects of DON consumption on both human and animal health. DON can cause feed refusal, weight loss and death (Eriksen and Pettersson 2004; Arunachalam and Doohan 2013). In farm animals, the induction of apoptotic lesions in liver and in lymphoid tissues was observed in pigs exposed to DON (Mikami et al. 2010). Depending on cell type and concentration, DON can act as either an immunostimulant or an immunosuppressor (Pestka and Smolinski 2005). Waché et al. (2009) reported the dose-dependent suppression of the cell surface markers CD54, CD14, CD119 and HLA-DP/DQ/DR in human macrophages when cells were treated with DON; these cellular markers play a major role in cell signalling and antigen presentation during the immune response. As a result of their acute toxicity in humans and animals, several countries, including the European Union (http://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32006R1881&from=en) and the United States Food and Drug Administration (U.S. FDA) (http://www.fda.gov/Food/GuidanceRegulation/GuidanceDocumentsRegulatoryInformation/ChemicalContaminantsMetalsNaturalToxinsPesticides/ucm120184.htm) have set the tolerable human and animal daily intake (TDI) levels for DON in cereal and their derivative products.

The role of DON in disease development

F. graminearum is a hemibiotroph, with a short biotrophic phase preceding necrotrophism (Trail 2009). During the biotrophic phase, which is estimated to continue 24 to 32 h after infection (Gottwald et al. 2012), the fungus feeds off living host cells. Fungal conidia and ascospores begin to germinate 6–12 h after the initial contact, and the emergent germ tube gives rise to hyphae that will enter the host through stomata or other susceptible sites; thereafter the fungus grows and extends on the interior surface to form dense mycelial networks (Kang and Buchenauer 2000; Xu and Nicholson 2009). From the point of infection, the hyphae can reach the adjacent florets and spikelets by two routes: either internally via vascular bundles or externally via stomata. When the environmental conditions are optimum for the growth of fungus (high humidity and a warm temperature), the hyphae may penetrate into the rachis and rachilla, and disease will spread up and downwards within the head through the vascular bundles and parenchyma (Kang and Buchenauer 2000; Lewandowski and Bushnell 2001; Bushnell et al. 2003; Goswami and Kistler 2004,). Mycelium may also spread on the surface of glumes from the infected spikelet to healthy ones (Ribichich et al. 2000). The growing fungal mycelium can block the vascular bundle cells in the rachis, preventing the movement of water and nutrients to the head and thus inducing the classic FHB phenotypic symptoms, i.e. the premature bleaching of heads and shrivelling of grains (Xu and Nicholson 2009).

DON is a fungal virulence factor that facilitates disease spread within wheat heads (Bai et al. 2002). Production of DON is typically observed 24 h post-inoculation (Chen et al. 1995), with a significant increase in levels by 96 h (Savard et al. 2000). The switch to necrotrophy is associated with an increase in DON production (Boddu et al. 2006; Walter et al. 2010). DON can be transported through vascular elements, upwards and downwards, to the neighbouring healthy spikelets (Kang and Buchenauer 1999). Varying concentrations of DON (1–100 ppm) elicited a wide range of defence responses in wheat leaves, including hydrogen peroxide accumulation and programmed cell death (PCD) (Desmond et al. 2008). Interestingly, Diamond et al. (2013) showed that both 10 ppm DON and a DON-producing strain of F. graminearum prevented heat-induced PCD in Arabidopsis cell cultures. They speculated that the suppression of PCD by low levels of DON might facilitate pathogen establishment in the initial biotrophic phase of Fusarium infection whereas higher level of DON may support the necrotrophic phase of the disease that ultimately leads to the appearance of the FHB disease symptoms. These symptoms typically manifest as premature bleaching of wheat spikelets but can also include the appearance of water-soaked brown, dark purple to black coloured necrotic lesions on the exterior surface of the florets. Like FHB, DON has also been shown to cause premature bleaching of plant tissue: it causes premature bleaching of both wheat heads and barley leaf tissues (Bushnell et al. 2003, 2010; Lemmens et al. 2005; Schweiger et al. 2010; Diamond et al. 2013). Application of DON to the central spikelets of wheat heads led to the premature bleaching of florets in both the antipetal and basipetal direction (Lemmens et al. 2005; Ansari et al. 2007).

Host resistance to FHB

Wheat cultivars differ in their response to FHB; some are more resistant, some are highly susceptible, but no genotype is immune. Resistance is horizontal, i.e. it is not considered Fusarium species-specific (Van Eeuwijk et al. 1995), but it is quantitative, polygenic and can be affected by the environment (Bai and Shaner 2004). Several components or ‘types’ of FHB resistance have been described, but types I and II are most widely accepted. Type I is defined as resistance to initial infection and type II as resistance to pathogen spread within the spike (Schroeder and Christensen 1963; Mesterhazy 1995). Other types of FHB resistance include resistance to kernel infection (type III), tolerance to FHB and DON (type IV) and resistance to DON accumulation (type V) (Boutigny et al. 2008). Type V resistance has also been divided into two subclasses to delineate processes that chemically modify trichothecenes (class 1) from processes that reduce the accumulation of trichothecenes (class 2) (Boutigny et al. 2008). Many people consider Type V as a subcomponent of type II resistance because it reduces the spread of disease.

Genetic loci linked to DON detoxification

Many quantitative trait loci (QTL) have been identified that contribute to different types of FHB resistance in wheat (Prat et al. 2014). Many FHB resistance QTL have also been associated with low DON accumulation (Somers et al. 2003; Ma et al. 2006). But few have been tested for their ability to either detoxify DON or enhance resistance to the toxin. Somers et al. (2003) mapped QTL controlling FHB resistance and DON accumulation in a double haploid population derived from a cross between cultivars Wuhan-1 and Nyubai. They reported QTL on chromosomes 2DS and 5AS that control the accumulation of DON, and they showed that this association was independent of FHB resistance. QTL Fhb1 was the first major QTL discovered for type II resistance and it was identified on chromosome 3B of cv. Sumai-3 (Bai et al. 1999; Anderson et al. 2001; Zhou et al. 2002; Cuthbert et al. 2006). The first functional characteristic to be linked to Fhb1 QTL was reported by Lemmens et al. (2005), whereby plants carrying Fhb1 were more resistant to DON-induced bleaching and were able to convert DON into a less toxic derivate, DON-3-O-glucoside (D3G). As will be discussed below, UDP-glycosyltransferases (UGTs) can convert DON to D3G (Poppenberger et al. 2003). Based on the sequenced cv. Chinese Spring genome, several UGTs have been annotated in a contig that contains the QTL Fhb1 region of cv. Sumai-3 (Choulet et al. 2010). But the first Fhb1-encoded gene conclusively linked to FHB resistance does not encode a UGT. Recently, using a combination of mutation analysis, gene silencing and transgenic overexpression, a gene within Fhb1 was shown to confer FHB resistance (Rawat et al. 2016). It encodes a pore-forming toxin-like protein (PFT) with a chimeric lectin and an ETX/MTX2 toxin domain. Surprisingly, they showed that PFT does not play a role in DON detoxification and suggested that the DON detoxification locus is near the same genetic block. Thus, it may be that the association between QTL Fhb1 and DON detoxification is due to either genetic linkage or the manifestation of downstream regulatory effects of the locus. This warrants further investigation.

Genes that directly effects DON resistance and/or DON detoxification

Table 1 outlines examples of genes directly involved in DON resistance and/or DON detoxification. As stated above, UGTs have been shown to convert DON to less toxic DON-3-G (Poppenberger et al. 2003). Overexpression of the UGT gene DOGT1 in Arabidopsis enhanced the conversion of DON to less toxic DON-3-G (Poppenberger et al. 2003). This discovery was a major breakthrough with regard to advancing DON detoxification strategies and it stimulated the search for cereal UGTs that had the same biochemical potential. A wheat UGT similar to DOGT1, TaUGT3, could enhance DON tolerance when expressed in Arabidopsis (Lulin et al. 2010). Wheat UGT gene TaUGT12887 provided weak DON tolerance when expressed in a toxin sensitive yeast strain (Schweiger et al. 2013b). Transgenic Arabidopsis lines expressing a barley UGT (HvUGT13248) showed enhanced tolerance to DON toxicity (Shin et al. 2012). Li et al. (2015) went on to demonstrate that the expression of this barley gene in transgenic wheat rapidly and efficiently conjugated DON to D3G and generally reduced the severity of FHB under field conditions. The model cereal Brachypodium distachyon encodes two homologs of HvUGT13248, and the encoded proteins were shown to convert DON to D3G when expressed in yeast (Schweiger et al. 2013a). Overexpression of Brachypodium UGT Bradi5g03300 reduced the toxicity of DON towards root tissue and enhanced spikelet resistance to FHB disease (Pasquet et al. 2016).
Table 1

Genes that contribute to DON resistance and/or DON detoxification

Gene annotation

Gene

Reference

Cytochrome P450

Ddna

Ito et al. 2013

Ethylene Insensitive 2

EIN2

Chen et al. 2009

Gibberellic acid sensitive DELLA protein

TaRht-B1b and TaRht-D1b

Saville et al. 2012

Methionyl-tRNA synthetase

TaMetRS

Zuo et al. 2016

Multi-drug resistance ABC transporter

ScPDR5

Mitterbauer and Adam 2002

TaABCC3.1

Walter et al. 2015

UDP-glucosyltransferase

DOGT1

Poppenberger et al. 2003

TaUGT3

Lulin et al. 2010

HvUGT13248

Shin et al. 2012; Li et al. 2015

Bradi5g02780; Bradi5g03300

Schweiger et al. 2013a; Pasquet et al. 2016

TaUGT12887

Schweiger et al. 2013b

Unknown function

TaFROG

Perochon et al. 2015

Several other microbial and plant genes, including cereal genes, have been shown to directly affect DON resistance. These include genes encoding detoxification enzymes, transporters, tRNA synthesis, regulators of hormones signalling and proteins of unknown function (Table 1). Multidrug resistance (MDR) ABC transporters genes encoding yeast pleiotropic drug transporter 5 (PDR5) and the wheat ABCC transporter protein TaABCC3.1 were shown to contribute to DON tolerance. Deletion of a yeast PDR5 gene increased sensitivity to growth inhibition caused by DON and expression of the yeast gene in tobacco increased DON resistance (Mitterbauer and Adam 2002). TaABCC3.1 was shown to contribute to DON tolerance in wheat, as determined via enhanced DON bleaching of spikelets in plants in which the gene was silenced (Fig. 1; Walter et al. 2015). While PDR5 is likely to act as a molecular efflux pump, removing toxic substances, the function of TaABCC3.1 is unknown.
Fig. 1

Virus Induced Gene Silencing (VIGS) of the multi-drug resistance (MDR) ABC transporter TaABCC3.1 in wheat heads resulted in more DON-induced bleaching of spikelets (Walter et al. 2015). Treatments: FES (buffer control), BSMV:00 (empty virus vector), BSMV:ABCC3V1 (silencing construct 1), BSMV:ABCC3V2 (silencing construct 2), T20 (Tween-20), DON (deoxynivalenol)

Enzymes involved in diverse processes have been shown to enhance DON resistance. Expression of a wheat DON-activated methionyl-tRNA synthetase gene (TaMetRS) in Arabidopsis enhanced seedling resistance towards DON and floret resistance towards Fusarium (Zuo et al. 2016). The bacterial cytochrome P450 Ddna was showed to convert DON to 16-hydroxy-DON (16-HDON) (Ito et al. 2013). When the hydroxylated 16-HDON product was tested on wheat seedlings the seedlings did not show any reduction in shoot length and fresh weight, indicating the hydroxylated product is a non-toxic DON metabolite (Ito et al. 2013). Phytohormones play a major role in plant defence against biotrophic and necrotrophic pathogens. Doohan et al. (2008) speculated that maintenance of hormone homeostasis plays an important role in DON tolerance. Chen et al. (2009) demonstrated the role of ethylene signalling in DON-induced PCD. Silencing of a gene encoding Ethylene Insensitive 2 (EIN2) in wheat resulted in FHB resistance and reduced DON-induced PCD in leaves. Moreover the gain of function (GoF) of gibberellic acid sensitive (GA) DELLA NIL lines Rht-B1b and Rht-B1c showed more resistance to Fusarium infected spikes and DON associated bleaching compare to taller counter parts rht-tall NIL lines. Both the NIL lines Rht-B1b and Rht-B1c also showed reduced lesion lengths and DON induced cell death than rht-tall lines (Saville et al. 2012).

There is increasing evidence that organisms have evolved taxonomically restricted ‘orphan’ genes to help them overcome environmental stress (Arendsee et al. 2014; Perochon et al. 2015). DON resistance research has contributed to our understanding of cereal evolution in that a Pooideae-restricted gene was discovered based on its responsiveness to the toxin. Perochon et al. (2015) characterised TaFROG, which is the wheat homolog of a Pooideae-specific gene, and demonstrated that overexpression of this gene enhanced DON and FHB resistance in wheat. Additionally, gene silencing of TaFROG resulted in more DON associated bleaching of wheat spikelets in the DON resistant wheat cv. CM82036 (Perochon et al. 2015). Ongoing studies are trying to delineate other orphan genes involved in wheat resistance to disease, including FHB disease.

Genes associated with DON resistance and the DON response

Table 2 outlines examples of the wheat genes that have been associated with DON resistance and DON production by F. graminearum. Comparative transcript analysis studies using near isogenic or double haploid lines that segregated for Fhb1 identified several genes associated, at the transcriptional level, with either Fusarium or DON resistance conferred by QTL Fhb1 (Buerstmayr et al. 2003; Ansari et al. 2007; Walter et al. 2008, 2015; Jia et al. 2009; Schweiger et al. 2013b, 2016). The genes linked to Fhb1 are involved in numerous defence responses in plants, including pathogenesis-related (PR) proteins, the synthesis of antimicrobial compounds, antioxidative stress responses, DON detoxification, cell morphogenesis and cell wall fortification (Walter and Doohan 2011; Foroud et al. 2012; Schweiger et al. 2016). Walter et al. (2008) investigated the transcriptomic response to DON of a double haploid population that segregated for both QTL Fhb1 and the toxin resistance phenotype (DON induced bleaching). Based on this analysis, they identified genes associated with the DON resistance phenotype at the transcriptional level, including those encoding the aforementioned TaABCC3.1 ABC transporter, and those coding for cytochrome P450 enzyme homologs (CYP450s), an AAA+ family ATPase, a zinc binding alcohol dehydrogenase-1, a mitochondrial phosphate transporter and an uridine diphosphate-glucosyltransferase (UGT). Li et al. (2010) reported that a CYP450 was more highly induced by DON in the FHB and DON resistant wheat cv. Sumai3 than in the susceptible cv. Annong 8455. In a study conducted by Schweiger et al. (2013b), DON induced the transcription of genes encoding UGT and glutathione-S-transferases (GSTs) in wheat carrying both Fhb1 and a FHB resistance QTL on chromosome 5A (DON independent). In a recent RNAseq study conducted by Hofstad et al. (2016) on wheat near isogenic lines carrying QTL Fhb1, DON induced genes included those encoding CYP450s, GSTs, UGTs, an ABC transporter and an O-methyltransferase.
Table 2

Wheat genes associated with DON resistance and the DON response

Gene annotation

Stimulanta

Wheat cultivarb

Reference

Cellular metabolism

 AAA+ ATPase

DON vs Tween-20

‘CM82036’ (R) vs ‘Remus’ (S), DH lines

Walter et al. 2008

 Zinc binding alcohol dehydrogenase

 O-methyltransferase

DON vs Water;

RI 63 (R) vs MN97448 (S), NIL lines

Hofstad et al. 2016

 Tetratricopeptide repeat protein

F. g (WT) vs Water

Detoxification

 Glutathione S-transferase

DON vs Water;

GS-1-EM0040 and GS-1-EM0168 (R) vs ‘Superb’ (MS)

Foroud et al. 2012

F. g (WT) vs Water

RI 63 (R) vs MN97448 (S), NIL lines

Hofstad et al. 2016

 UDP-glycosyltransferase

DON vs Tween-20

‘CM82036’ (R) vs ‘Remus’ (S), DH lines

Walter et al. 2008

DON vs Water;

RI 63 (R) vs MN97448 (S), NIL lines

Hofstad et al. 2016

F. g (WT) vs Water

Kinases

 CDPK-related protein kinase

DON vs Water;

GS-1-EM0040 and GS-1-EM0168 (R) vs ‘Superb’ (MS)

Foroud et al. 2012

 Nucleoside diphosphate kinase III

F. g (WT) vs Water

 Phytosulfokine LRR receptor kinase

 

 Protein kinase 1

 

 Putative MAPKKK

 

 Serine ⁄ threonine protein kinase

 

 Serine/threonine kinase receptor-associated protein

 

 Receptor-like protein kinase

 

RI 63 (R) vs MN97448 (S) NIL lines

Hofstad et al. 2016

Oxidoreductases

 Alternative oxidase

DON vs Tween-20

‘CM82036’ (R) vs ‘Remus’ (S), DH lines

Walter et al. 2008

 Cytochrome P450s

DON vs Tween-20

‘CM82036’ (R) vs ‘Remus’ (S), DH lines

Walter et al. 2008

DON vs Water

‘Sumai3’ (R) vs ‘Annong8455’ (S)

Li et al. 2010

F. g (WT) vs Water

RI 63 (R) vs MN97448 (S), NIL lines

Hofstad et al. 2016

 Peroxidase

DON vs Tween-20

‘CM82036’ (R) vs ‘Remus’ (S), DH lines

Ansari et al. 2007

Programmed Cell Death

 Bax Inhibitor-1

DON vs Water

Rht-tall, Rht-B1b, Rht-B1c. NIL lines

Saville et al. 2012

 Radical Induced Cell Death 1

Retrotransposons

 Long terminal repeat of an Erika retrotransposon

DON vs Tween-20

‘CM82036’ (R) vs ‘Remus’ (S), DH lines

Ansari et al. 2007

 Poly protein of a Romani retrotransposon

Transporter proteins

 Mitochondrial phosphate transporter

DON vs Tween-20

‘CM82036’ (R) vs ‘Remus’ (S), DH lines

Walter et al. 2008

 Multi-drug resistance ABC transporter

DON vs Tween-20

‘CM82036’ (R) vs ‘Remus’ (S), DH lines

Walter et al. 2015

DON vs Water;

RI 63 (R) vs MN97448 (S), NIL lines

Hofstad et al. 2016

F. g (WT) vs Water

Unknown function

 Orphan gene (TaFROG)

DON vs Tween-20;

‘CM82036’ (R)

Perochon et al. 2015

F. g (WT) vs F. g (Mu)

a F. g (WT) F. graminearum wild type, F. g (Mu) F. graminearum DON-minus mutant, DH double haploid lines, NIL near isogenic lines

b R resistant cultivar, S susceptible cultivar, MS moderately susceptible cultivar

Foroud et al. (2012) analysed the effect of DON, wild type F. graminearum and its’ DON-minus mutant derivative on the transcriptome of an FHB susceptible wheat genotype and two double haploid lines with moderate FHB resistance derived from the susceptible genotype and resistant parents. The pattern of gene expression in response to DON suggested that the toxin delayed the plant defence response in a susceptible genotype, but was less effective in doing so in the resistant genotypes. DON also up-regulated genes encoding ribosomal components in the resistant wheat lines, but not in the susceptible genotype. The resistant double haploid lines were chosen for the study based on their ability to tolerate DON in an in vitro screen and, as the authors stated, this screen may have selected lines that overproduce ribosome or DON-sensitive ribosome components. Differential expression of phenylalanine ammonia-lyase (PAL) genes was expressed upon DON treatment suggesting the role of phenylpropanoid pathway metabolites in DON response. In the resistant cultivars, the genes coding for PAL are up-regulated and in susceptible cultivars they are down-regulated. Early up-regulation of genes coding for peroxidases and elicitor response PR genes were mainly observed in the resistant lines upon application of DON, suggesting that the resistant lines activate their defence response much earlier than the susceptible lines. Genes encoding terpene synthase, GST, CYP450, GDSL lipase acyl hydrolase and lipoxygenase were activated by the wild type but not by the DON-minus mutant fungus, suggesting they played a role in the response to the toxin.

A study conducted by Boddu et al. (2007) analysed the transcriptional response of barley head tissue to wild type F. graminearum and its trichothecene-minus mutant derivative. Although this study was conducted on the FHB susceptible cv. Morex, the comparison of the results obtained for the wild type with those obtained for the DON-minus fungal strain gave insights into the processes activated during barley defence against DON. They found that Contig20755 was responsive to DON production and this is the barley homolog of the wheat DON resistance orphan gene TaFROG characterised by Perochon et al. (2015). Other barley genes up-regulated in response to DON production by the fungus encoded UGTs, CYP450s, transporters and proteins involved in ubiquitination and PCD. A subsequent transcriptome study of this barley cv. Morex confirmed that genes encoding ABC transporters, UGTs, CYP450s and GSTs were responsive to pure DON (Gardiner et al. 2010) and that overexpression of cystathionine β-synthase, a key enzyme for glutathione production, enhanced the conversion of DON to the less toxic derivative DON-glutathione in yeast.

Conclusions

Elucidating the host resistance mechanisms that confer resistance to DON and enhance DON detoxification mechanisms will help us to develop tools and strategies to prevent mycotoxin contamination of grain and reduce yield loss due to FHB disease. The information derived from various functional genomics studies gave much insight into the paths to follow in order to enhance DON and thus FHB resistance. Many of the genes identified are expression markers in that they were delineated on the basis of enhanced expression being associated with a toxin resistance phenotype. CYPs, ABC transporters and UGTs are among the most common gene families involved in the cereal response to DON. For some, gene overexpression or gene silencing has confirmed their role in DON resistance; for others, their effect on DON resistance remains to be determined. From a breeding perspective the identification of gene promoter polymorphisms linked to differential gene expression will provide valuable markers for breeders to track specific alleles of interest within their breeding programmes. Genes proven to enhance DON resistance will serve both breeders and the GM industry as tools to develop transgenic, cisgenic or gene-edited crops with enhanced Fusarium resistance.

Notes

Acknowledgements

We acknowledge Science Foundation Ireland for providing funding (project nos. 10/IN.1/B3028 and 14/1A/2508).

References

  1. Anderson JA, Stack R, Liu S, Waldron B, Fjeld A, Coyne C, Moreno SB, Fetch JM, Song Q, Cregan P (2001) DNA markers for Fusarium head blight resistance in two wheat populations. Theor Appl Genet 102:1164–1168CrossRefGoogle Scholar
  2. 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. Theor Appl Genet 114:927–937CrossRefPubMedGoogle Scholar
  3. Arendsee ZW, Li L, Wurtele ES (2014) Coming of age: orphan genes in plants. Trends Plant Sci 19:698–708CrossRefPubMedGoogle Scholar
  4. Arunachalam C, Doohan FM (2013) Trichothecene toxicity in eukaryotes: cellular and molecular mechanisms in plants and animals. Toxicol Lett 217:149–158CrossRefPubMedGoogle Scholar
  5. Azcona-Olivera J, Ouyang YL, Warner R, Linz J, Pestka J (1995) Effects of vomitoxin (deoxynivalenol) and cycloheximide on IL-2, 4, 5 and 6 secretion and mRNA levels in murine CD4+ cells. Food Chem Toxicol 33:433–441CrossRefPubMedGoogle Scholar
  6. Bai G, Shaner G (1994) Scab of wheat: prospects for control. Plant Dis 78:760–766CrossRefGoogle Scholar
  7. Bai G, Shaner G (2004) Management and resistance in wheat and barley to Fusarium head blight. Annu Rev Phytopathol 42:135–161Google Scholar
  8. Bai G, Kolb FL, Shaner G, Domier LL (1999) Amplified fragment length polymorphism markers linked to a major quantitative trait locus controlling scab resistance in wheat. Phytopathology 89:343–348CrossRefPubMedGoogle Scholar
  9. Bai GH, Desjardins AE, Plattner R (2002) Deoxynivalenol-nonproducing Fusarium graminearum causes initial infection, but does not cause disease spread in wheat spikes. Mycopathologia 153:91–98CrossRefPubMedGoogle Scholar
  10. Bechtel D, Kaleikau L, Gaines R, Seitz L (1985) The effects of Fusarium graminearum infection on wheat kernels. Cereal Chem 62:191–197Google Scholar
  11. Boddu J, Cho S, Muehlbauer GJ (2007) Transcriptome analysis of trichothecene-induced gene expression in barley. Mol Plant-Microbe Interact 20:1364–1375Google Scholar
  12. Boddu J, Cho S, Kruger WM, Muehlbauer GJ (2006) Transcriptome analysis of the barley Fusarium graminearum interaction. Mol Plant-Microbe Interact 19:407–417CrossRefPubMedGoogle Scholar
  13. Boutigny AL, Richard Forget F, Barreau C (2008) Natural mechanisms for cereal resistance to the accumulation of Fusarium trichothecenes. Eur J Plant Pathol 121:411–423CrossRefGoogle Scholar
  14. Buerstmayr H, Steiner B, Hartl L, Griesser M, Angerer N, Lengauer D, Miedaner T, Schneider B, Lemmens M (2003) Molecular mapping of QTLs for Fusarium head blight resistance in spring wheat. II. Resistance to fungal penetration and spread. Theor Appl Genet 107:503–508CrossRefPubMedGoogle Scholar
  15. Bushnell WR, Hazen BE, Pritsch C, Leonard K (2003) Histology and physiology of Fusarium head blight. In: Leonard KJ, Bushnell WR (eds) Fusarium Head Blight of Wheat and Barley. St. Paul, MN APS Press, p 44–83Google Scholar
  16. Bushnell W, Perkins VP, Russo V, Collins J, Seeland T (2010) Effects of deoxynivalenol on content of chloroplast pigments in barley leaf tissues. Phytopathology 100:33–41CrossRefPubMedGoogle Scholar
  17. Carter CJ, Cannon M (1977) Structural requirements for the inhibitory action of 12, 13-epoxytrichothecenes on protein synthesis in eukaryotes. Biochem J 166:399–409CrossRefPubMedPubMedCentralGoogle Scholar
  18. Chen L, Song Y, Xu Y (1995) Variation in the concentrations of deoxynivalenol in the spikes of winter wheat infected by Fusarium graminearum Schw. Acta Phys Sin 26:25–28Google Scholar
  19. Chen X, Steed A, Travella S, Keller B, Nicholson P (2009) Fusarium graminearum exploits ethylene signalling to colonize dicotyledonous and monocotyledonous plants. New Phytol 182:975–983CrossRefPubMedGoogle Scholar
  20. Choulet F, Wicker T, Rustenholz C, Paux E, Salse J, Leroy P, Schlub S, Le Paslier MC, Magdelenat G, Gonthier C, Couloux A (2010) Megabase level sequencing reveals contrasted organization and evolution patterns of the wheat gene and transposable element spaces. Plant Cell 22:686-701Google Scholar
  21. Cuthbert PA, Somers DJ, Thomas J, Cloutier S, Brulé BA (2006) Fine mapping Fhb1, a major gene controlling Fusarium head blight resistance in bread wheat (Triticum aestivum L.) Theor Appl Genet 112:1465–1472CrossRefPubMedGoogle Scholar
  22. Desjardins AE (2006) Fusarium mycotoxins: chemistry, genetics, and biology. American Phytopathological Society (APS Press)Google Scholar
  23. 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. Mol Plant Pathol 9:435–445CrossRefPubMedGoogle Scholar
  24. Diamond M, Reape TJ, Rocha O, Doyle SM, Kacprzyk J, Doohan FM, Mccabe PF (2013) The Fusarium mycotoxin deoxynivalenol can inhibit plant apoptosis-like programmed cell death. PLoS One 8:e69542CrossRefPubMedPubMedCentralGoogle Scholar
  25. Doohan F, Arunachalam C, Jiang S, Khan M, Egan D, Erard G, Walter S (2008) The wheat response to deoxynivalenol: does maintenance of hormone homeostasis and alleviation of oxidative stress play an important role in toxin tolerance? Cereal Res Commun 36:233–237CrossRefGoogle Scholar
  26. Elias EM, Manthey FA, Stack RW, Kianian SF (2005) Breeding efforts to develop Fusarium head blight resistant durum wheat in North Dakota. Proceedings of the 2005 national head blight forum p 25–26Google Scholar
  27. Eriksen GS, Pettersson H (2004) Toxicological evaluation of trichothecenes in animal feed. Anim Feed Sci Technol 114:205–239CrossRefGoogle Scholar
  28. Foroud N, Ouellet T, Laroche A, Oosterveen B, Jordan M, Ellis B, 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 61:296–314CrossRefGoogle Scholar
  29. Gardiner SA, Boddu J, Berthiller F, Hametner C, Stupar RM, Adam G, Muehlbauer GJ (2010) Transcriptome analysis of the barley-deoxynivalenol interaction: evidence for a role of glutathione in deoxynivalenol detoxification. Mol Plant-Microbe Interact 23:962–976CrossRefPubMedGoogle Scholar
  30. Giroux ME, Bourgeois G, Dion Y, Rioux S, Pageau D, Zoghlami S, Parent C, Vachon E, Vanasse A (2016) Evaluation of forecasting models for Fusarium head blight of wheat under growing conditions of Quebec, Canada. Plant Dis 100:1192–1201CrossRefGoogle Scholar
  31. Goswami RS, Kistler HC (2004) Heading for disaster: Fusarium graminearum on cereal crops. Mol Plant Pathol 5:515–525CrossRefPubMedGoogle Scholar
  32. Gottwald S, Samans B, Lück S, Friedt W (2012) Jasmonate and ethylene dependent defence gene expression and suppression of fungal virulence factors: two essential mechanisms of Fusarium head blight resistance in wheat? BMC Genomics 13:369CrossRefPubMedPubMedCentralGoogle Scholar
  33. Hofstad AN, Nussbaumer T, Akhunov E, Shin S, Kugler KG, Kistler HC, Mayer KF Muehlbauer GJ (2016) Examining the transcriptional response in wheat near-isogenic lines to infection and deoxynivalenol treatment. The Plant Genome 9. doi:  10.3835/plantgenome2015.05.0032
  34. Ito M, Sato I, Ishizaka M, Yoshida SI, Koitabashi M, Yoshida S, Tsushima S (2013) Bacterial cytochrome P450 system catabolizing the Fusarium toxin deoxynivalenol. Appl Environ Microbiol 79:1619–1628CrossRefPubMedPubMedCentralGoogle Scholar
  35. 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 22:1366–1378CrossRefPubMedGoogle Scholar
  36. Kang Z, Buchenauer H (1999) Immunocytochemical localization of Fusarium toxins in infected wheat spikes by Fusarium culmorum. Physiol Mol Plant Pathol 55:275–288CrossRefGoogle Scholar
  37. Kang Z, Buchenauer H (2000) Cytology and ultrastructure of the infection of wheat spikes by Fusarium culmorum. Mycol Res 104:1083–1093CrossRefGoogle Scholar
  38. Kouadio JH, Mobio TA, Baudrimont I, Moukha S, Dano SD, Creppy EE (2005) Comparative study of cytotoxicity and oxidative stress induced by deoxynivalenol, zearalenone or fumonisin B1 in human intestinal cell line Caco-2. Toxicology 213:56–65CrossRefPubMedGoogle Scholar
  39. Lemmens M, Scholz U, Berthiller F, Dall'asta C, Koutnik A, Schuhmacher R, Adam G, Buerstmayr H, Mesterházy Á, Krska R (2005) The ability to detoxify the mycotoxin deoxynivalenol colocalizes with a major quantitative trait locus for Fusarium head blight resistance in wheat. Mol Plant-Microbe Interact 18:1318–1324CrossRefPubMedGoogle Scholar
  40. Lewandowski S, Bushnell W (2001) Development of Fusarium graminearum on floret surfaces of field-grown barley. National Fusarium Head Blight Forum Proceedings 2001, p 128Google Scholar
  41. Li X, Zhang J, Song B, Li H, Xu H, Qu B, Dang F, Liao Y (2010) Resistance to Fusarium head blight and seedling blight in wheat is associated with activation of a cytochrome P450 gene. Phytopathology 100:183–191CrossRefPubMedGoogle Scholar
  42. 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 28:1237–1246CrossRefPubMedGoogle Scholar
  43. Lulin M, Yi S, Aizhong C, Zengjun Q, Liping X, Peidu C, Dajun L, Xiu EW (2010) Molecular cloning and characterization of an up-regulated UDP-glucosyltransferase gene induced by DON from Triticum aestivum L. cv. Wangshuibai. Mol Biol Rep 37:785–795CrossRefPubMedGoogle Scholar
  44. Ma H, Zhang K, Gao L, Bai G, Chen H, Cai Z, Lu W (2006) Quantitative trait loci for resistance to Fusarium head blight and deoxynivalenol accumulation in Wangshuibai wheat under field conditions. Plant Pathol 55:739–745CrossRefGoogle Scholar
  45. Mcmullen M, Bergstrom G, De Wolf E, Dill Macky R, Hershman D, Shaner G, Van Sanford D (2012) A unified effort to fight an enemy of wheat and barley: Fusarium head blight. Plant Dis 96:1712–1728CrossRefGoogle Scholar
  46. Mesterhazy A (1995) Types and components of resistance to Fusarium head blight of wheat. Plant Breed 114:377–386CrossRefGoogle Scholar
  47. Mikami O, Yamaguchi H, Murata H, Nakajima Y, Miyazaki S (2010) Induction of apoptotic lesions in liver and lymphoid tissues and modulation of cytokine mRNA expression by acute exposure to deoxynivalenol in piglets. J Vet Sci 11:107–113CrossRefPubMedPubMedCentralGoogle Scholar
  48. 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. Mycotoxins in plant disease. Eur J Plant Pathol 108(7):699–703CrossRefGoogle Scholar
  49. Mohanty I, Gangasagar P, Rath S (2013) Amplification and molecular characterization of DREB1A transcription factor fragment from finger millet [(Eleusine coracana (L.) Gaertn]. J Agric Sci 5:37–49Google Scholar
  50. Oliver R, Stack R, Miller J, Cai X (2007) Reaction of wild emmer wheat accessions to Fusarium head blight. Crop Sci 47:893–897CrossRefGoogle Scholar
  51. Osborne LE, Stein JM (2007) Epidemiology of Fusarium head blight on small-grain cereals. Int J Food Microbiol 119:103–108CrossRefPubMedGoogle Scholar
  52. Pasquet JC, Changenet V, Macadré C, Boex Fontvieille E, Soulhat C, Bouchabké CO, Dalmais M, Atanasova Pénichon V, Bendahmane A, Saindrenan P (2016) A Brachypodium UDP-glycosytransferase confers root tolerance to deoxynivalenol and resistance to Fusarium infection. Plant Physiol 172:559–74Google Scholar
  53. 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 169:2895–2906PubMedPubMedCentralGoogle Scholar
  54. Pestka JJ, Smolinski AT (2005) Deoxynivalenol: toxicology and potential effects on humans. J Toxicol Environ Health 8:39–69CrossRefGoogle Scholar
  55. 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 278:47905–47914CrossRefPubMedGoogle Scholar
  56. Prat N, Buerstmayr M, Steiner B, Robert O, Buerstmayr H (2014) Current knowledge on resistance to Fusarium head blight in tetraploid wheat. Mol Breed 34:1689–1699CrossRefGoogle Scholar
  57. Rawat N, Pumphrey MO, Liu S, Zhang X, Tiwari VK, Ando K, Trick HN, Bockus WW, Akhunov E, Anderson JA (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 48:1576–1580Google Scholar
  58. Ribichich KF, Lopez SE, Vegetti AC (2000) Histopathological spikelet changes produced by Fusarium graminearum in susceptible and resistant wheat cultivars. Plant Dis 84:794–802CrossRefGoogle Scholar
  59. Savard ME, Sinha RC, Lloyd Seaman W, Fedak G (2000) Sequential distribution of the mycotoxin deoxynivalenol in wheat spikes after inoculation with Fusarium graminearum. Can J Plant Pathol 22:280–285CrossRefGoogle Scholar
  60. Saville R, Gosman N, Burt C, Makepeace J, Steed A, Corbitt M, Chandler E, Brown J, Boulton M, Nicholson P (2012) The ‘Green Revolution’dwarfing genes play a role in disease resistance in Triticum aestivum and Hordeum vulgare. J Exp Bot 63:1271–1283CrossRefPubMedGoogle Scholar
  61. Schindler D (1974) Two classes of inhibitors of peptidyl transferase activity in eukaryotes. Nature 249:38–41CrossRefPubMedGoogle Scholar
  62. Schroeder H, Christensen J (1963) Factors affecting resistance of wheat to scab caused by Gibberella zeae. Phytopathology 53:831–838Google Scholar
  63. 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 23:977–986CrossRefPubMedGoogle Scholar
  64. Schweiger W, Pasquet JC, Nussbaumer T, Paris MPK, Wiesenberger G, Macadré C, Ametz C, Berthiller F, Lemmens M, Saindrenan P (2013a) Functional characterization of two clusters of Brachypodium distachyon UDP-glycosyltransferases encoding putative deoxynivalenol detoxification genes. Mol Plant-Microbe Interact 26:781–792CrossRefPubMedGoogle Scholar
  65. Schweiger W, Steiner B, Ametz C, Siegwart G, Wiesenberger G, Berthiller F, Lemmens M, Jia H, Adam G, Muehlbauer GJ (2013b) Transcriptomic characterization of two major Fusarium resistance quantitative trait loci (QTLs), Fhb1 and Qfhs. Ifa-5A, identifies novel candidate genes. Mol Plant Pathol 14:772–785CrossRefPubMedPubMedCentralGoogle Scholar
  66. Schweiger W, Steiner B, Vautrin S, Nussbaumer T, Siegwart G, Zamini M, Jungreithmeier F, Gratl V, Lemmens M, Mayer KF, Berges H (2016) Suppressed recombination and unique candidate genes in the divergent haplotype encoding Fhb1. Theor Appl Genet 129:1607–1623Google Scholar
  67. Shifrin VI, Anderson P (1999) Trichothecene mycotoxins trigger a ribotoxic stress response that activates c-Jun N-terminal kinase and p38 mitogen-activated protein kinase and induces apoptosis. J Biol Chem 274:13985–13992CrossRefPubMedGoogle Scholar
  68. Shin S, Torres AJA, Heinen SJ, Mccormick S, Lemmens M, Paris MPK, Berthiller F, Adam G, Muehlbauer GJ (2012) Transgenic Arabidopsis thaliana expressing a barley UDP-glucosyltransferase exhibit resistance to the mycotoxin deoxynivalenol. J Exp Bot 63:4731–4740CrossRefPubMedPubMedCentralGoogle Scholar
  69. Somers DJ, Fedak G, Savard M (2003) Molecular mapping of novel genes controlling Fusarium head blight resistance and deoxynivalenol accumulation in spring wheat. Genome 46:555–564CrossRefPubMedGoogle Scholar
  70. Trail F (2009) For blighted waves of grain: Fusarium graminearum in the postgenomics era. Plant Physiol 149:103–110CrossRefPubMedPubMedCentralGoogle Scholar
  71. Van Eeuwijk F, Mesterhazy A, Kling CI, Ruckenbauer P, Saur L, Buerstmayr H, Lemmens M, Keizer L, Maurin N, Snijders C (1995) Assessing non-specificity of resistance in wheat to head blight caused by inoculation with European strains of Fusarium culmorum, F. graminearum and F. nivale using a multiplicative model for interaction. Theor Appl Genet 90:221–228CrossRefPubMedGoogle Scholar
  72. Waché YJ, Hbabi HL, Guzylack PL, Belkhelfa H, Roques C, Oswald IP (2009) The mycotoxin deoxynivalenol inhibits the cell surface expression of activation markers in human macrophages. Toxicology 262:239–244CrossRefPubMedGoogle Scholar
  73. Walter S, Doohan F (2011) Transcript profiling of the phytotoxic response of wheat to the Fusarium mycotoxin deoxynivalenol. Mycotoxin Res 27:221–230CrossRefPubMedGoogle Scholar
  74. Walter S, Brennan JM, Arunachalam C, Ansari KI, Hu X, Khan MR, Trognitz F, Trognitz B, Leonard G, Egan D (2008) Components of the gene network associated with genotype-dependent response of wheat to the Fusarium mycotoxin deoxynivalenol. Funct Integr Genomics 8:421–427CrossRefPubMedGoogle Scholar
  75. Walter S, Nicholson P, Doohan FM (2010) Action and reaction of host and pathogen during Fusarium head blight disease. New Phytol 185:54–66CrossRefPubMedGoogle Scholar
  76. 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(9):2583–93Google Scholar
  77. Xu X, Nicholson P (2009) Community ecology of fungal pathogens causing wheat head blight. Annu Rev Phytopathol 47:83–103CrossRefPubMedGoogle Scholar
  78. Zhou WC, Kolb F, Bai GH, Domier L, Yao JB (2002) Effect of individual Sumai 3 chromosomes on resistance to scab spread within spikes and deoxynivalenol accumulation within kernels in wheat. Hereditas 137:81–89CrossRefPubMedGoogle Scholar
  79. Zuo DY, Yi SY, Liu RJ, Qu B, Huang T, He WJ, Li C, Li HP, Liao YC (2016) A deoxynivalenol-activated methionyl-tRNA synthetase gene from wheat encodes a nuclear localized protein and protects plants against Fusarium pathogens and mycotoxins. Phytopathology 106:614–623CrossRefPubMedGoogle Scholar

Copyright information

© The Author(s) 2017

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  1. 1.Molecular Plant-Microbe Interactions Laboratory, UCD School of Biology and Environmental Science and UCD Earth InstituteUniversity College DublinDublinIreland

Personalised recommendations