Exogenous Abscisic Acid and Gibberellic Acid Elicit Opposing Effects on Fusarium graminearum Infection in Wheat

Although the roles of salicylate (SA) and jasmonic acid (JA) have been well-characterized in Fusarium head blight (FHB)-infected cereals, the roles of other phytohormones remain more ambiguous. Here, the association between an array of phytohormones and FHB pathogenesis in wheat is investigated. Comprehensive profiling of endogenous hormones demonstrated altered cytokinin, gibberellic acid (GA), and JA metabolism in a FHB-resistant cultivar, whereas challenge by Fusarium graminearum increased abscisic acid (ABA), JA, and SA in both FHB-susceptible and -resistant cultivars. Subsequent investigation of ABA or GA coapplication with fungal challenge increased and decreased FHB spread, respectively. These phytohormones-induced effects may be attributed to alteration of the F. graminearum transcriptome because ABA promoted expression of early-infection genes, including hydrolases and cytoskeletal reorganization genes, while GA suppressed nitrogen metabolic gene expression. Neither ABA nor GA elicited significant effects on F. graminearum fungal growth or sporulation in axenic conditions, nor do these phytohormones affect trichothecene gene expression, deoxynivalenol mycotoxin accumulation, or SA/JA biosynthesis in F. graminearum-challenged wheat spikes. Finally, the combined application of GA and paclobutrazol, a Fusarium fungicide, provided additive effects on reducing FHB severity, highlighting the potential for combining fungicidal agents with select phytohormone-related treatments for management of FHB infection in wheat.

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Investigating Useful Properties of Four Streptomyces Strains Active against Fusarium graminearum Growth and Deoxynivalenol Production on Wheat Grains by qPCR

Toxins ◽

10.3390/toxins12090560 ◽

2020 ◽

Vol 12 (9) ◽

pp. 560

Author(s):

Elena Maria Colombo ◽

Andrea Kunova ◽

Claudio Gardana ◽

Cristina Pizzatti ◽

Paolo Simonetti ◽

...

Keyword(s):

Fusarium Graminearum ◽

Plant Pathogens ◽

Fungal Growth ◽

Toxin Production ◽

Fungal Mycelium ◽

Head Blight ◽

Wheat Grains ◽

Streptomyces Spp ◽

Dual Plate

Streptomyces spp. can be exploited as biocontrol agents (BCAs) against plant pathogens such as Fusarium graminearum, the main causal agent of Fusarium head blight (FHB) and against the contamination of grains with deoxynivalenol (DON). In the present research, four Streptomyces strains active against F. graminearum in dual plate assays were characterized for their ability to colonize detached wheat grains in the presence of F. graminearum and to limit DON production. The pathogen and BCA abundance were assessed by a quantitative real-time PCR, while DON production was assessed by HPLC quantification and compared to ergosterol to correlate the toxin production to the amount of fungal mycelium. Fungal growth and mycotoxin production were assessed with both co-inoculation and late inoculation of the BCAs in vitro (three days post-Fusarium inoculation) to test the interaction between the fungus and the bacteria. The level of inhibition of the pathogen and the toxin production were strain-specific. Overall, a higher level of DON inhibition (up to 99%) and a strong reduction in fungal biomass (up to 71%) were achieved when streptomycetes were co-inoculated with the fungus. This research enabled studying the antifungal efficacy of the four Streptomyces strains and monitoring their development in DON-inducing conditions.

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Novel Genes of Fusarium graminearum That Negatively Regulate Deoxynivalenol Production and Virulence

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-22-12-1588 ◽

2009 ◽

Vol 22 (12) ◽

pp. 1588-1600 ◽

Cited By ~ 76

Author(s):

Donald M. Gardiner ◽

Kemal Kazan ◽

John M. Manners

Keyword(s):

Gene Expression ◽

Fusarium Graminearum ◽

Global Analysis ◽

Gene Clusters ◽

Head Blight ◽

Knock Out ◽

Serious Disease ◽

Amine Compounds ◽

Fungal Genes ◽

Fungal Gene Expression

Fusarium head blight of wheat, caused by Fusarium graminearum, is a serious disease resulting in both reduced yields and contamination of grain with trichothecene toxins, with severe consequences for mammalian health. Recently, we have identified several related amine compounds such as agmatine and putrescine that promote the production of high levels of trichothecene toxins, such as deoxynivalenol (DON), in culture by F. graminearum and F. sporotrichioides. Here, a global analysis of fungal gene expression using the Affymetrix Fusarium GeneChip during culture under DON-inducing conditions compared with noninducing conditions is reported. Agmatine differentially regulated a large number of fungal genes, including both known and previously uncharacterized putative secondary metabolite biosynthetic gene clusters. In silico prediction of binding sites for the transcriptional regulator (TRI6) controlling TRI gene expression and gene expression analysis in a TRI6 mutant of F. graminearum showed that three of the differentially regulated genes were under the control of TRI6. Gene knock-out mutations of two of these genes resulted in mutants with massively increased production of DON and increased aggressiveness toward wheat. Our results not only identify a novel mechanism of negative regulation of DON production and virulence in F. graminearum but also point out the potential of this pathogen to evolve with an ability to produce massively increased amounts of toxins and increased virulence.

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Wheat transcriptome profiling reveals abscisic and gibberellic acid treatments regulate early-stage phytohormone defense signaling, cell wall fortification, and metabolic switches following Fusarium graminearum-challenge

10.1101/2020.09.17.302737 ◽

2020 ◽

Author(s):

Leann M. Buhrow ◽

Ziying Liu ◽

Dustin Cram ◽

Tanya Sharma ◽

Nora A. Foroud ◽

...

Keyword(s):

Cell Wall ◽

Gibberellic Acid ◽

Secondary Metabolism ◽

Fusarium Graminearum ◽

Stress Responses ◽

Early Stage ◽

Molecular Transport ◽

Defense Responses ◽

Head Blight ◽

Primary And Secondary Metabolism

ABSTRACTBackgroundApplication of the wheat phytohormones abscisic acid (ABA) or gibberellic acid (GA) affect Fusarium head blight (FHB) disease severity; however, the molecular underpinnings of the elicited phenotypes remain unclear. Herein, the transcriptomic responses of an FHB-susceptible wheat cultivar ‘Fielder’ were characterized upon treatment with ABA, an ABA receptor antagonist (AS6), or GA in the presence or absence of Fusarium graminearum (Fg) challenge.ResultsA total of 30,876 differentially expressed genes (DEGs) where identified in ‘Fielder’ (26,004) and Fg (4,872). Fg challenge alone resulted in the most substantial wheat DEGs contributing to 57.2% of the total transcriptomic variation. Using a combination of topology overlap and correlation analyses, 9,689 Fg-related wheat DEGs were defined. Further enrichment analysis of the top 1% networked wheat DEGs identified critical expression changes within defense responses, cell structural metabolism, molecular transport, and membrane/lipid metabolism. Fg-challenged conditions also included the expression of a putative Fg ABA-biosynthetic cytochrome P450 and repression of wheat FUS3 for dysregulating ABA and GA crosstalk. ABA treatment alone elicited 4536 (32%) wheat DEGs common to those of the Fg-challenge, and Fg+ABA further enhanced 888 (12.5%) of them. These ABA elicited DEGs are involved in defense through both classical and non-classical phytohormone signaling and regulating cell wall structures including polyphenolic metabolism. Conversely, Fg+GA opposed 2239 (33%) Fg-elicited wheat DEGs, including modulating primary and secondary metabolism, defense responses, and flowering genes. ABA and jointly ABA⍰Fg⍰[Fg+ABA] treatments repressed, while Fg+GA induced an over-representation of wheat DEGs mapping to chromosome 6BL. Finally, compared to Fg+ABA, co-application of Fg+AS6 did not antagonize ABA biosynthesis or signal but rather elicited antagonistic Fg (557) and wheat (11) DEGs responses directly tied to stress responses, phytohormone transport, and FHB.ConclusionsComparative transcriptomics highlight the effects of wheat phytohormones on individual pathway and global metabolism simultaneously. Application of ABA may reduce FHB severity through misregulating defense mechanisms and cell wall fortification pathways. GA application may alter primary and secondary metabolism, creating a metabolic shift to ultimately reduce FHB severity. By comparing these findings to those previously reported for four additional plant genotypes, an additive model of the wheat-Fg interaction is proposed.

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Phases of Infection and Gene Expression of Fusarium graminearum During Crown Rot Disease of Wheat

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-21-12-1571 ◽

2008 ◽

Vol 21 (12) ◽

pp. 1571-1581 ◽

Cited By ~ 77

Author(s):

Amber E. Stephens ◽

Donald M. Gardiner ◽

Rosemary G. White ◽

Alan L. Munn ◽

John M. Manners

Keyword(s):

Gene Expression ◽

Fusarium Graminearum ◽

Quantitative Polymerase Chain Reaction ◽

Crown Rot ◽

Fungal Colonization ◽

Published Data ◽

In Planta ◽

Head Blight ◽

Fungal Gene Expression ◽

Fungal Gene

Fusarium graminearum causes head blight (FHB) and crown rot (CR) diseases in wheat. Compared with FHB, CR symptom development occurs slowly, usually taking 4 to 8 weeks to become visible. To characterize CR development, we used histological and real-time quantitative polymerase chain reaction analyses to assess fungal colonization during a timecourse of infection. Three distinct phases of infection were identified: i) initial spore germination with formation of a superficial hyphal mat at the inoculation point, ii) colonization of the adaxial epidermis of the outer leaf sheath and mycelial growth from the inoculation point to the crown, concomitant with a drop in fungal biomass, and iii) extensive colonization of the internal crown tissue. Fungal gene expression was examined during each phase using Affymetrix GeneChips. In total, 1,839 F. graminearum genes were significantly upregulated, including some known FHB virulence genes (e.g., TRI5 and TRI14), and 2,649 genes were significantly downregulated in planta compared with axenically cultured mycelia. Global comparisons of fungal gene expression with published data for FHB showed significant similarities between early stages of FHB and CR. These results indicate that CR disease development involves distinct phases of colonization, each of which is associated with a different fungal gene expression program.

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Jasmonic acid and abscisic acid play important roles in host–pathogen interaction between Fusarium graminearum and wheat during the early stages of fusarium head blight

Physiological and Molecular Plant Pathology ◽

10.1016/j.pmpp.2015.12.004 ◽

2016 ◽

Vol 93 ◽

pp. 39-48 ◽

Cited By ~ 43

Author(s):

Peng-Fei Qi ◽

Margaret Balcerzak ◽

Hélène Rocheleau ◽

Winnie Leung ◽

Yu-Ming Wei ◽

...

Keyword(s):

Abscisic Acid ◽

Jasmonic Acid ◽

Fusarium Head Blight ◽

Fusarium Graminearum ◽

Head Blight ◽

Host Pathogen Interaction ◽

Early Stages ◽

Host Pathogen

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Synergistic antimicrobial effect of chitosan polymers and oligomers

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-07-20-0185-r ◽

2021 ◽

Author(s):

Maha Attjioui ◽

Dominique Gillet ◽

Nour Eddine El Gueddari ◽

Bruno Maria Moerschbacher

Keyword(s):

Plant Protection ◽

Synergistic Effects ◽

Fungal Growth ◽

Antimicrobial Effect ◽

Time Lapse ◽

Inhibitory Effect ◽

Degree Of Polymerization ◽

Head Blight ◽

Conidia Germination ◽

Combined Application

This study evaluated the efficacy of the combined application of well-characterized chitosan polymer (degree of acetylation DA = 10%, degree of polymerization DPn = 90, dispersity ÐDP = 2.8) and oligomers (paCOS) (DP = 2-17) on conidia germination and mycelial growth of Fusarium graminearum, the major causal agent of Fusarium Head Blight in wheat. The polymer alone showed a higher inhibitory effect than the paCOS mixture alone, with half-maximal inhibitory concentrations (IC50) of less than 50 µg mL⁻¹ and more than 100 µg mL⁻¹, respectively. Using time-lapse microscopy, we also showed that paCOS did not affect conidia germination at 50 μg mL⁻¹, while chitosan polymer at the same concentration led to a delay in germination and in elongation of germ tubes. Scanning electron microscopy was used to observe the chitosan-induced changes in hyphal morphology. Surprisingly, the combination of chitosan polymer and paCOS led to strong synergistic effects in inhibiting conidia germination and fungal growth, as quantified by both the Abbot and Wadley equation. To our knowledge, this is the first report on a synergistic effect of a combination of chitosan polymers and oligomers, also highlighting for the first time the importance of ÐDP when studying structure-function relationships of functional biopolymers such as chitosan. The consequences of this finding for the improvement of chitosan-based antimicrobial or plant protective products are discussed. Given the economic importance of F. graminearum, this study suggests that the combination of chitosan polymer and oligomers can be used to support an efficient, sustainable plant protection strategy.

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Early detection of toxigenic Fusarium graminearum in wheat

World Mycotoxin Journal ◽

10.3920/wmj2011.1348 ◽

2012 ◽

Vol 5 (2) ◽

pp. 143-152 ◽

Cited By ~ 7

Author(s):

J.R. Girotti ◽

I. Malbrán ◽

G.A. Lori ◽

M.P. Juárez

Keyword(s):

Fusarium Graminearum ◽

Solid Phase Microextraction ◽

Solid Phase ◽

Time Lag ◽

Fungal Growth ◽

Agricultural Crops ◽

Wheat Cultivars ◽

Head Blight ◽

Trichothecene Mycotoxin ◽

Mycotoxin Contamination

Fusarium graminearum (Schwabe) contaminates agricultural crops and commodities with trichothecenes, mostly deoxynivalenol and its acetyl-derivatives. Current techniques available to detect final mycotoxin contamination products usually require an extended time lag between sampling and the corresponding report, and include different clean-up steps and eventually derivatisation. This study was aimed to develop a methodology to detect toxigenic F. graminearum prior to mycotoxin production. Headspace solid-phase microextraction coupled to capillary gas chromatography is shown to be useful to predict the potential of trichothecene mycotoxin formation by detecting the presence of F. graminearum at early stages of fungal growth in wheat cultivars, based on the detection of trichodiene (TRI), the volatile intermediate of trichothecenes. We showed that TRI is a useful marker to detect toxigenic Fusarium in wheat spikes from live plants, regardless of the actual development of Fusarium head blight (FHB). This is the first predictive methodology for FHB and trichothecene occurrence in field-collected samples. It might be a useful tool to help to prevent the risk of mycotoxin contamination.

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Effect of Carbendazim Resistance on Trichothecene Production and Aggressiveness of Fusarium graminearum

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-22-9-1143 ◽

2009 ◽

Vol 22 (9) ◽

pp. 1143-1150 ◽

Cited By ~ 55

Author(s):

Yan-Jun Zhang ◽

Jun-Jie Yu ◽

Yan-Nan Zhang ◽

Xiao Zhang ◽

Chang-Jun Cheng ◽

...

Keyword(s):

Gene Expression ◽

Fusarium Graminearum ◽

Gibberella Zeae ◽

Shake Culture ◽

Wild Type ◽

Head Blight ◽

Exponential Relationship ◽

Sensitive Site ◽

Resistant Strains ◽

Type Strains

Fusarium graminearum (teleomorph, Gibberella zeae) causes head blight of cereals and contaminates grains with trichothecene mycotoxins that are harmful to humans and domesticated animals. Control of Fusarium head blight relies on carbendazim (MBC) in China, but resistance to MBC in F. graminearum is now widespread. Sixty-seven strains were evaluated for trichothecene production in shake culture or in the field. The strains included 60 wild-type strains (30 MBC-resistant and 30 MBC-sensitive), three MBC-resistant site-directed mutants at codon 167 in β2-tubulin, three MBC-sensitive site-directed mutants at codon 240 in β2-tubulin, and their MBC-sensitive wild-type progenitor strain ZF21. The incidence of infected spikelets and the amount of F. graminearum DNA in field grain (AFgDNA) also were evaluated for all strains. MBC resistance increased trichothecene production in shake culture or in the field. Although MBC resistance did not change the incidence of infected spikelets, it did increase AFgDNA. Tri5 gene expression increased in MBC-resistant strains grown in shake culture. We found a significant exponential relationship between trichothecene production and Tri5 gene expression in shake culture and a linear relationship between the incidence of infected spikelets or AFgDNA and trichothecene production in field grain.

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Wheat transcriptome profiling reveals abscisic and gibberellic acid treatments regulate early-stage phytohormone defense signaling, cell wall fortification, and metabolic switches following Fusarium graminearum-challenge

BMC Genomics ◽

10.1186/s12864-021-08069-0 ◽

2021 ◽

Vol 22 (1) ◽

Author(s):

Leann M. Buhrow ◽

Ziying Liu ◽

Dustin Cram ◽

Tanya Sharma ◽

Nora A. Foroud ◽

...

Keyword(s):

Cell Wall ◽

Gibberellic Acid ◽

Secondary Metabolism ◽

Fusarium Graminearum ◽

Molecular Mechanisms ◽

Early Stage ◽

Molecular Transport ◽

Defense Responses ◽

Head Blight ◽

Primary And Secondary Metabolism

Abstract Background Treatment of wheat with the phytohormones abscisic acid (ABA) and gibberellic acid (GA) has been shown to affect Fusarium head blight (FHB) disease severity. However, the molecular mechanisms underlying the elicited phenotypes remain unclear. Toward addressing this gap in our knowledge, global transcriptomic profiling was applied to the FHB-susceptible wheat cultivar ‘Fielder’ to map the regulatory responses effected upon treatment with ABA, an ABA receptor antagonist (AS6), or GA in the presence or absence of Fusarium graminearum (Fg) challenge. Results Spike treatments resulted in a total of 30,876 differentially expressed genes (DEGs) identified in ‘Fielder’ (26,004) and the Fg (4872) pathogen. Topology overlap and correlation analyses defined 9689 wheat DEGs as Fg-related across the treatments. Further enrichment analyses demonstrated that these included expression changes within ‘Fielder’ defense responses, cell structural metabolism, molecular transport, and membrane/lipid metabolism. Dysregulation of ABA and GA crosstalk arising from repression of ‘Fielder’ FUS3 was noted. As well, expression of a putative Fg ABA-biosynthetic cytochrome P450 was detected. The co-applied condition of Fg + ABA elicited further up-regulation of phytohormone biosynthesis, as well as SA and ET signaling pathways and cell wall/polyphenolic metabolism. In contrast, co-applied Fg + GA mainly suppressed phytohormone biosynthesis and signaling, while modulating primary and secondary metabolism and flowering. Unexpectedly, co-applied Fg + AS6 did not affect ABA biosynthesis or signaling, but rather elicited antagonistic responses tied to stress, phytohormone transport, and FHB disease-related genes. Conclusions Observed exacerbation (misregulation) of classical defense mechanisms and cell wall fortifications upon ABA treatment are consistent with its ability to promote FHB severity and its proposed role as a fungal effector. In contrast, GA was found to modulate primary and secondary metabolism, suggesting a general metabolic shift underlying its reduction in FHB severity. While AS6 did not antagonize traditional ABA pathways, its impact on host defense and Fg responses imply potential for future investigation. Overall, by comparing these findings to those previously reported for four additional plant genotypes, an additive model of the wheat-Fg interaction is proposed in the context of phytohormone responses.

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