Temporal Changes in Sensitivity of Zymoseptoria tritici Field Populations to Different Fungicidal Modes of Action

Septoria tritici blotch (STB; Zymoseptoria tritici), one of the most important foliar diseases in wheat, is mainly controlled by the intensive use of fungicides during crop growth. Unfortunately, Z. tritici field populations have developed various extents of resistance to different groups of fungicides. Due to the complete resistance to quinone outside inhibitors (QoIs), fungicidal control of STB relies mainly on demethylation inhibitors (DMIs) and succinate dehydrogenase inhibitors (SDHIs) as well as multi-site inhibitors. In this study, temporal changes in the sensitivity of Z. tritici to selected DMIs (tebuconazole, propiconazole, prothioconazole, prochloraz), SDHIs (boscalid, bixafen), and multi-site inhibitors (chlorothalonil, folpet) were determined in microtiter assays using Z. tritici field populations isolated in 1999, 2009, 2014, and 2020 in a high-disease-pressure and high-fungicide-input area in Northern Germany. For the four tested DMI fungicides, a significant shift towards decreasing sensitivity of Z. tritici field populations was observed between 1999 and 2009, whereby concentrations inhibiting fungal growth by 50% (EC50) increased differentially between the four DMIs. Since 2009, EC50 values of tebuconazole, propiconazole, and prochloraz remain stable, whereas for prothioconazole a slightly increased sensitivity shift was found. A shift in sensitivity of Z. tritici was also determined for both tested SDHI fungicides. In contrast to DMIs, EC50 values of boscalid and bixafen increased continuously between 1999 and 2020, but the increasing EC50 values were much smaller compared to those of the four tested DMIs. No changes in sensitivity of Z. tritici were observed for the multi-site inhibitors chlorothalonil and folpet over the last 21 years. The sensitivity adaptation of Z. tritici to both groups of single-site inhibitors (DMIs, SDHIs) mainly used for STB control represents a major challenge for future wheat cultivation.

Download Full-text

Will Triazoles Still Be of Importance in Disease Control of Zymoseptoria tritici in the Future?

Agronomy ◽

10.3390/agronomy11050933 ◽

2021 ◽

Vol 11 (5) ◽

pp. 933

Author(s):

Holger Klink ◽

Joseph-Alexander Verreet ◽

Mario Hasler ◽

Tim Birr

Keyword(s):

Control Strategies ◽

Fungal Growth ◽

Current Control ◽

Septoria Tritici Blotch ◽

Septoria Tritici ◽

Significant Shift ◽

Active Ingredients ◽

Zymoseptoria Tritici ◽

Wheat Diseases

Septoria tritici blotch (STB), caused by Zymoseptoria tritici, is one of the most important foliar wheat diseases worldwide. Current control strategies of STB rely mainly on fungicides, whereby triazoles (demethylation inhibitors; DMIs) have been the backbone in the control of Z. tritici in the last decades. However, in recent years a gradual loss of sensitivity of Z. tritici to several active ingredients of the triazole group has been reported in several European wheat-growing areas. Nevertheless, a new triazole fungicide, namely, mefentrifluconazole, has recently become available in disease management of STB, which belongs to a completely new triazole subclass, the so-called isopropanol triazoles. In this study, the trend in sensitivity development of Z. tritici towards older triazoles (tebuconazole, prothioconazole, and propiconazole) and the new isopropanol triazole mefentrifluconazole was determined in microtiter assays using Z. tritici field populations isolated in 1999, 2009, 2014, and 2020 in a high-disease-pressure and high-fungicide-input area in northern Germany in order to investigate whether the loss of sensitivity of Z. tritici to older triazoles also applies to mefentrifluconazole. For the three triazole fungicides tebuconazole, prothioconazole and propiconazole, a significant shift towards decreasing sensitivity of Z. tritici field populations was observed from 1999 to 2020, whereas the efficacy of mefentrifluconazole in reducing the in vitro fungal growth by 50% (EC50) remained unchanged over the investigated period, demonstrating a stable sensitivity of Z. tritici towards mefentrifluconazole. Although older triazoles are suffering from a loss of sensitivity of Z. tritici field populations due to the selection and spread of less triazole sensitive strains within the Z. tritici population, the efficacy of the new triazole mefentrifluconazole with its unique isopropanol unit was not affected by these changes within the Z. tritici population. Thus, the introduction of such new molecular units could also represent an important contribution for older groups of active ingredients, which previously suffered from a loss of sensitivity.

Download Full-text

Prevalence of QoI resistance and mtDNA diversity in the Irish Zymoseptoria tritici population

Irish Journal of Agricultural and Food Research ◽

10.2478/ijafr-2019-0004 ◽

2019 ◽

Vol 58 (1) ◽

pp. 27-33

Author(s):

S. Kildea ◽

D.E. Bucar ◽

F. Hutton ◽

S. de la Rosa ◽

T.E. Welch ◽

...

Keyword(s):

Septoria Tritici Blotch ◽

Septoria Tritici ◽

Entire Group ◽

Zymoseptoria Tritici ◽

Qoi Fungicides ◽

Quinone Outside Inhibitor ◽

Strain Collection ◽

Increased Sensitivity ◽

Mtdna Diversity

Abstract The emergence and spread of Quinone outside Inhibitor (QoI) fungicide resistance in the Irish Zymoseptoria tritici population in the early 2000s had immediate impacts on the efficacy of the entire group of fungicides for the control of septoria tritici blotch. As a result, a dramatic reduction in the quantities applied to winter wheat occurred in the following seasons. Even in the absence of these fungicides, the frequency of the resistance allele, G143A in the pathogens mtDNA has remained exceptionally high (>97%), and as such, it can be anticipated that continued poor efficacy of current QoI fungicides will be observed. Amongst the isolates with G143A, differences in sensitivity to the QoI pyraclostrobin were observed in vitro. The addition of the alternative oxidase (AOX) inhibitor salicylhydroxamic acid increased sensitivity in these isolates, suggesting some continued impairment of respiration by the QoI fungicides, albeit weak. Interestingly, amongst those tested, the strains from a site with a high frequency of inserts in the MFS1 transporter gene known to enhance QoI efflux did not exhibit this increase in sensitivity. A total of 19 mtDNA haplotypes were detected amongst the 2017 strain collection. Phylogenetic analysis confirmed the suggestion of a common ancestry of all the haplotypes, even though three of the haplotypes contained at least one sensitive strain.

Download Full-text

Baseline and Temporal Changes in Sensitivity of Zymoseptoria tritici Isolates to Benzovindiflupyr in Oregon, U.S.A., and Cross-Sensitivity to Other SDHI Fungicides

Plant Disease ◽

10.1094/pdis-10-19-2125-re ◽

2021 ◽

Vol 105 (1) ◽

pp. 169-174

Author(s):

Christina H. Hagerty ◽

Ann M. Klein ◽

Catherine L. Reardon ◽

Duncan R. Kroese ◽

Caroline J. Melle ◽

...

Keyword(s):

Fungicide Resistance ◽

Fungal Growth ◽

Careful Consideration ◽

Septoria Tritici Blotch ◽

Septoria Tritici ◽

Willamette Valley ◽

Active Ingredients ◽

Effective Population ◽

Zymoseptoria Tritici ◽

Cross Sensitivity

Zymoseptoria tritici is the causal agent of Septoria tritici blotch (STB), a disease of wheat (Triticum aestivum) that results in significant yield loss worldwide. Z. tritici’s life cycle, reproductive system, effective population size, and gene flow put it at high likelihood of developing fungicide resistance. Succinate dehydrogenase inhibitor (SDHI) fungicides (FRAC code 7) were not widely used to control STB in the Willamette Valley until 2016. Field isolates of Z. tritici collected in the Willamette Valley at dates spanning the introduction of SDHI (2015 to 2017) were screened for sensitivity to four SDHI active ingredients: benzovindiflupyr, penthiopyrad, fluxapyroxad, and fluindapyr. Fungicide sensitivity changes were determined by the fungicide concentration at which fungal growth is decreased by 50% (EC50) values. The benzovindiflupyr EC50 values increased significantly, indicating a reduction in sensitivity, following the adoption of SDHI fungicides in Oregon (P < 0.0001). Additionally, significant reduction in cross-sensitivity among SDHI active ingredients was also observed with a moderate and significant relationship between penthiopyrad and benzovindiflupyr (P = 0.0002) and a weak relationship between penthiopyrad and fluxapyroxad (P = 0.0482). No change in cross-sensitivity was observed with fluindapyr, which has not yet been labeled in the region. The results document a decrease in SDHI sensitivity in Z. tritici isolates following the introduction of the active ingredients to the Willamette Valley. The reduction in cross-sensitivity observed between SDHI active ingredients highlights the notion that careful consideration is required to manage fungicide resistance and suggests that within-group rotation is insufficient for resistance management.

Download Full-text

The effect of fungicide dose rate and mixtures on Zymoseptoria tritici in two cultivars of autumn sown wheat

New Zealand Plant Protection ◽

10.30843/nzpp.2015.68.5822 ◽

2015 ◽

Vol 68 ◽

pp. 420-427

Author(s):

J.B. Drummond ◽

R.A. Craigie ◽

M. Braithwaite ◽

A.T. Gillum ◽

B.L. McCloy

Keyword(s):

Fungal Pathogen ◽

Growth Stage ◽

Flag Leaf ◽

Septoria Tritici Blotch ◽

Septoria Tritici ◽

Zymoseptoria Tritici ◽

Fixed Rate ◽

Disease Pressure ◽

Succinate Dehydrogenase Inhibitor ◽

Demethylation Inhibitor

In the 201213 and 201314 seasons septoria tritici blotch (STB) caused by the fungal pathogen Zymoseptoria tritici was poorly controlled in autumn sown wheat in Canterbury In 201415 a low disease pressure season three trials were conducted to define the protectant and curative properties of two applications of triazole demethylation inhibitor inhibitor (DMI) and succinate dehydrogenase inhibitor (SDHI) fungicides for the control of STB at growth stage 31 and 39 on two cultivars of autumn sown wheat The protectant activity of triazole and SDHI fungicides was more effective on the flag leaf than the curative activity on leaf two The addition of an SDHI to a 75 fixed rate of triazole was more effective at controlling STB infection than triazoles alone The addition of SDHI fungicides also significantly increased yield The highest mean yields were achieved with the addition of a third application at GS65

Download Full-text

Characterisation of an antimicrobial and phytotoxic ribonuclease secreted by the fungal wheat pathogen Zymoseptoria tritici

10.1101/130393 ◽

2017 ◽

Cited By ~ 1

Author(s):

Graeme J. Kettles ◽

Carlos Bayon ◽

Caroline A. Sparks ◽

Gail Canning ◽

Kostya Kanyuka ◽

...

Keyword(s):

Expression Pattern ◽

Effector Proteins ◽

Yeast Cells ◽

Septoria Tritici Blotch ◽

Septoria Tritici ◽

List Type ◽

Expression Systems ◽

Zymoseptoria Tritici ◽

Loop Region

Abstract-The fungus Zymoseptoria tritici is the causal agent of Septoria Tritici Blotch (STB) disease of wheat leaves. Z. tritici secretes many functionally uncharacterised effector proteins during infection. Here we characterised a secreted ribonuclease (Zt6) with an unusual biphasic expression pattern.-Transient expression systems were used to characterise Zt6, and mutants thereof, in both host and non-host plants. Cell-free protein expression systems monitored impact of Zt6 protein on functional ribosomes, and in vitro assays of cells treated with recombinant Zt6 determined toxicity against bacteria, yeasts and filamentous fungi.-We demonstrated that Zt6 is a functional ribonuclease and that phytotoxicity is dependent on both the presence of a 22-amino acid N-terminal “loop” region and its catalytic activity. Zt6 selectively cleaves both plant and animal rRNA species, and is toxic to wheat, tobacco, bacterial and yeast cells but not to Z. tritici itself.-Zt6 is the first Z. tritici effector demonstrated to have a likely dual functionality. The expression pattern of Zt6 and potent toxicity towards microorganisms suggests that whilst it may contribute to the execution of wheat cell death, it is also likely to have an important secondary function in antimicrobial competition and niche protection.

Download Full-text

A Microbial Fermentation Mixture Reduces Fusarium Head Blight and Promotes Grain Weight but does not impact Septoria tritici blotch

European Journal of Plant Pathology ◽

10.1007/s10658-021-02396-4 ◽

2021 ◽

Author(s):

Tony Twamley ◽

Mark Gaffney ◽

Angela Feechan

Keyword(s):

Fusarium Head Blight ◽

Fungal Pathogens ◽

Septoria Tritici Blotch ◽

Septoria Tritici ◽

Microbial Fermentation ◽

In Planta ◽

Head Blight ◽

Zymoseptoria Tritici ◽

The Impact

AbstractFusarium graminearum and Zymoseptoria tritici cause economically important diseases of wheat. F. graminearum is one of the primary causal agents of Fusarium head blight (FHB) and Z. tritici is the causal agent of Septoria tritici blotch (STB). Alternative control methods are required in the face of fungicide resistance and EU legislation which seek to cut pesticide use by 2030. Both fungal pathogens have been described as either hemibiotrophs or necrotrophs. A microbial fermentation-based product (MFP) was previously demonstrated to control the biotrophic pathogen powdery mildew, on wheat. Here we investigated if MFP would be effective against the non-biotrophic fungal pathogens of wheat, F. graminearum and Z. tritici. We assessed the impact of MFP on fungal growth, disease control and also evaluated the individual constituent parts of MFP. Antifungal activity towards both pathogens was found in vitro but MFP only significantly decreased disease symptoms of FHB in planta. In addition, MFP was found to improve the grain number and weight, of uninfected and F. graminearum infected wheat heads.

Download Full-text

Differential dynamics of microbial community networks help identify microorganisms interacting with residue-borne pathogens: the case of Zymoseptoria tritici in wheat

10.1101/587667 ◽

2019 ◽

Author(s):

Lydie Kerdraon ◽

Matthieu Barret ◽

Valérie Laval ◽

Frédéric Suffert

Keyword(s):

Microbial Community ◽

Microbial Communities ◽

Fungal Pathogen ◽

Crop Residues ◽

Septoria Tritici Blotch ◽

Septoria Tritici ◽

Zymoseptoria Tritici ◽

Essential Information ◽

Linear Discriminant ◽

Network Analyses

AbstractBackgroundWheat residues are a crucial determinant of the epidemiology of Septoria tritici blotch, as they support the sexual reproduction of the causal agent Zymoseptoria tritici. We aimed to characterize the effect of infection with this fungal pathogen on the microbial communities present on wheat residues, and to identify microorganisms interacting with it. We used metabarcoding to characterize the microbiome associated with wheat residues placed outdoors, with and without preliminary Z. tritici inoculation, comparing a first set of residues in contact with the soil and a second set without contact with the soil, on four sampling dates in two consecutive years.ResultsThe diversity of the tested conditions, leading to the establishment of different microbial communities according to the origins of the constitutive taxa (plant only, or plant and soil), highlighted the effect of Z. tritici on the wheat residue microbiome. Several microorganisms were affected by Z. tritici infection, even after the disappearance of the pathogen. Linear discriminant analyses and ecological network analyses were combined to describe the communities affected by infection. The number of fungi and bacteria promoted or inhibited by inoculation with Z. tritici decreased over time, and was smaller for residues in contact with the soil. The interactions between the pathogen and other microorganisms appeared to be mostly indirect, despite the strong position of the pathogen as a keystone taxon in networks. Direct interactions with other members of the communities mostly involved fungi, including other wheat pathogens. Our results provide essential information about the alterations to the microbial community in wheat residues induced by the mere presence of a fungal pathogen, and vice versa. Species already described as beneficial or biocontrol agents were found to be affected by pathogen inoculation.ConclusionsThe strategy developed here can be viewed as a proof-of-concept focusing on crop residues as a particularly rich ecological compartment, with a high diversity of fungal and bacterial taxa originating from both the plant and soil compartments, and for Z. tritici-wheat as a model pathosystem. By revealing putative antagonistic interactions, this study paves the way for improving the biological control of residue-borne diseases.

Download Full-text

Advances in breeding techniques for durable Septoria tritici blotch (STB) resistance in cereals

10.19103/as.2021.0092.12 ◽

2021 ◽

pp. 303-356

Author(s):

Harsh Raman ◽

Keyword(s):

Quantitative Resistance ◽

Durable Resistance ◽

Genetic Resistance ◽

Septoria Tritici Blotch ◽

Septoria Tritici ◽

Zymoseptoria Tritici ◽

Winter Cereal ◽

Cereal Breeding ◽

Qualitative Resistance ◽

Breeding Techniques

Septoria tritici blotch (STB), caused by the hemibiotrophic fungus Zymoseptoria tritici, is one of the most important foliar diseases of winter cereal crops. Recent advances are helping to understand the genetic basis and architecture of resistance to STB. To date, at least 22 genes for qualitative resistance and over 200 quantitative trait loci (QTL) for quantitative resistance have been identified in cereals. This knowledge is enabling cereal breeding programs to develop varieties with more durable resistance to STB. This chapter reviews recent research on genetic resistance loci and breeding strategies based on both conventional and biotechnology-based breeding approaches (molecular marker/genomic-assisted breeding, genetic transformation, and gene-editing) to achieve achieving durable resistance to STB infection and minimise grain yield losses.

Download Full-text

Evidence of Selection for Fungicide Resistance in Zymoseptoria tritici Populations on Wheat in Western Oregon

Plant Disease ◽

10.1094/pdis-02-15-0214-re ◽

2016 ◽

Vol 100 (2) ◽

pp. 483-489 ◽

Cited By ~ 22

Author(s):

Laura E. Hayes ◽

Kathryn E. Sackett ◽

Nicole P. Anderson ◽

Michael D. Flowers ◽

Christopher C. Mundt

Keyword(s):

Fungicide Resistance ◽

Fungal Pathogen ◽

Plant Pathogens ◽

Septoria Tritici Blotch ◽

Septoria Tritici ◽

Zymoseptoria Tritici ◽

Resistance Evolution ◽

Regional Control ◽

Selection For ◽

Moderately Resistant

Plant pathogens pose a major challenge to maintaining food security in many parts of the world. Where major plant pathogens are fungal, fungicide resistance can often thwart regional control efforts. Zymoseptoria tritici, causal agent of Septoria tritici blotch, is a major fungal pathogen of wheat that has evolved resistance to chemical control products in four fungicide classes in Europe. Compared with Europe, however, fungicide use has been less and studies of fungicide resistance have been infrequent in North American Z. tritici populations. Here, we confirm first reports of Z. tritici fungicide resistance evolution in western Oregon through analysis of the effects of spray applications of propiconazole and an azoxystrobin + propiconazole mixture during a single growing season. Frequencies of strobilurin-resistant isolates, quantified as proportions of G143A mutants, were significantly higher in azoxystrobin-sprayed plots compared with plots with no azoxystrobin treatment at two different locations and were significantly higher in plots of a moderately resistant cultivar than in plots of a susceptible cultivar. Thus, it appears that western Oregon Z. tritici populations have the potential to evolve levels of strobilurin resistance similar to those observed in Europe. Although the concentration of propiconazole required to reduce pathogen growth by 50% values were numerically greater for isolates collected from plots receiving propiconazole than in control plots, this effect was not significant (P > 0.05).

Download Full-text

Presence of ice-nucleating Pseudomonas on wheat leaves promotes Septoria tritici blotch disease (Zymoseptoria tritici) via a mutually beneficial interaction

Scientific Reports ◽

10.1038/s41598-020-74615-7 ◽

2020 ◽

Vol 10 (1) ◽

Author(s):

Helen N. Fones

Keyword(s):

Frost Damage ◽

Ice Nucleation ◽

Septoria Tritici Blotch ◽

Septoria Tritici ◽

Zymoseptoria Tritici ◽

Bacterial Populations ◽

Wheat Leaf ◽

Ina Bacteria ◽

Wheat Leaves ◽

Important Disease

Abstract Zymoseptoria tritici causes Septoria tritici blotch (STB) of wheat, an economically important disease causing yield losses of up to 10% despite the use of fungicides and resistant cultivars. Z. tritici infection is symptomless for around 10 days, during which time the fungus grows randomly across the leaf surface prior to entry through stomata. Wounded leaves show faster, more extensive STB, suggesting that wounds facilitate fungal entry. Wheat leaves also host epiphytic bacteria; these include ice-nucleating (INA+) bacteria, which induce frost damage at warmer temperatures than it otherwise occurs. Here, STB is shown to be more rapid and severe when wheat is exposed to both INA+ bacteria and sub-zero temperatures. This suggests that ice-nucleation-induced wounding of the wheat leaf provides additional openings for fungal entry. INA+ bacterial populations are shown to benefit from the presence of Z. tritici, indicating that this microbial interaction is mutualistic. Finally, control of INA+ bacteria is shown to reduce STB.

Download Full-text