scholarly journals Temporal Dynamics and Spatial Variation of Azoxystrobin and Propiconazole Resistance in Zymoseptoria tritici: A Hierarchical Survey of Commercial Winter Wheat Fields in the Willamette Valley, Oregon

2017 ◽  
Vol 107 (3) ◽  
pp. 345-352 ◽  
Author(s):  
Christina H. Hagerty ◽  
Nicole P. Anderson ◽  
Christopher C. Mundt

Fungicide resistance can cause disease control failure in agricultural systems, and is particularly concerning with Zymoseptoria tritici, the causal agent of Septoria tritici blotch of wheat. In North America, the first quinone outside inhibitor resistance in Z. tritici was discovered in the Willamette Valley of Oregon in 2012, which prompted this hierarchical survey of commercial winter wheat fields to monitor azoxystrobin- and propiconazole-resistant Z. tritici. Surveys were conducted in June 2014, January 2015, May 2015, and January 2016. The survey was organized in a hierarchical scheme: regions within the Willamette Valley, fields within the region, transects within the field, and samples within the transect. Overall, frequency of azoxystrobin-resistant isolates increased from 63 to 93% from June 2014 to January 2016. Resistance to azoxystrobin increased over time even within fields receiving no strobilurin applications. Propiconazole sensitivity varied over the course of the study but, overall, did not significantly change. Sensitivity to both fungicides showed no regional aggregation within the Willamette Valley. Greater than 80% of spatial variation in fungicide sensitivity was at the smallest hierarchical scale (within the transect) of the survey for both fungicides, and the resistance phenotypes were randomly distributed within sampled fields. Results suggest a need for a better understanding of the dynamics of fungicide resistance at the landscape level.

Plant Disease ◽  
2021 ◽  
Vol 105 (1) ◽  
pp. 169-174
Author(s):  
Christina H. Hagerty ◽  
Ann M. Klein ◽  
Catherine L. Reardon ◽  
Duncan R. Kroese ◽  
Caroline J. Melle ◽  
...  

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.


2019 ◽  
Vol 58 (1) ◽  
pp. 27-33
Author(s):  
S. Kildea ◽  
D.E. Bucar ◽  
F. Hutton ◽  
S. de la Rosa ◽  
T.E. Welch ◽  
...  

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.


Plant Disease ◽  
2016 ◽  
Vol 100 (2) ◽  
pp. 483-489 ◽  
Author(s):  
Laura E. Hayes ◽  
Kathryn E. Sackett ◽  
Nicole P. Anderson ◽  
Michael D. Flowers ◽  
Christopher C. Mundt

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).


2018 ◽  
Vol 85 (4) ◽  
Author(s):  
Megan C. McDonald ◽  
Melanie Renkin ◽  
Merrin Spackman ◽  
Beverley Orchard ◽  
Daniel Croll ◽  
...  

ABSTRACT Zymoseptoria tritici is a globally distributed fungal pathogen which causes Septoria tritici blotch on wheat. Management of the disease is attempted through the deployment of resistant wheat cultivars and the application of fungicides. However, fungicide resistance is commonly observed in Z. tritici populations, and continuous monitoring is required to detect breakdowns in fungicide efficacy. We recently reported azole-resistant isolates in Australia; however, it remained unknown whether resistance was brought into the continent through gene flow or whether resistance emerged independently. To address this question, we screened 43 isolates across five Australian locations for azole sensitivity and performed whole-genome sequencing on 58 isolates from seven locations to determine the genetic basis of resistance. Population genomic analyses showed extremely strong differentiation between the Australian population recovered after azoles began to be used and both Australian populations recovered before azoles began to be used and populations on different continents. The apparent absence of recent gene flow between Australia and other continents suggests that azole fungicide resistance has evolved de novo and subsequently spread within Tasmania. Despite the isolates being distinct at the whole-genome level, we observed combinations of nonsynonymous substitutions at the CYP51 locus identical to those observed elsewhere in the world. We observed nine previously reported nonsynonymous mutations as well as isolates that carried a combination of the previously reported L50S, S188N, A379G, I381V, Y459DEL, G460DEL, and N513K substitutions. Assays for the 50% effective concentration against a subset of isolates exposed to the tebuconazole and epoxiconazole fungicides showed high levels of azole resistance. The rapid, parallel evolution of a complex CYP51 haplotype that matches a dominant European haplotype demonstrates the enormous potential for de novo resistance emergence in pathogenic fungi. IMPORTANCE Fungicides are essential to control diseases in agriculture because many crops are highly susceptible to pathogens. However, many pathogens rapidly evolve resistance to fungicides. A large body of studies have described specific mutations conferring resistance and have often made inferences about the origins of resistance based on sequencing data from the target gene alone. Here, we show the de novo acquisition of resistance to the ubiquitously used azole fungicides in genetically isolated populations of the wheat pathogen Zymoseptoria tritici in Tasmania, Australia. We confirm evidence for parallel evolution through genome-scale analyses of representative worldwide populations. The emergence of complex resistance haplotypes following a well-documented recent introduction of azoles into Australian farming practices demonstrates how rapidly chemical resistance evolves in agricultural ecosystems.


2021 ◽  
Vol 12 ◽  
Author(s):  
Berit Samils ◽  
Björn Andersson ◽  
Eva Edin ◽  
Malin Elfstrand ◽  
Tilman Rönneburg ◽  
...  

Fungicide resistance has become a challenging problem in management of Septoria tritici blotch (STB), caused by Zymoseptoria tritici, the most destructive disease of winter wheat throughout western and northern Europe. To ensure the continued effectiveness of those fungicides currently used, it is essential to monitor the development and spread of such resistance in field populations of the pathogen. Since resistance to the key families of fungicides used for STB control (demethyalation inhibitors or azoles, succinate dehydrogenase inhibitors or SDHIs and Quinone outside Inhibitors or QoIs) is conferred through target-site mutations, the potential exists to monitor resistance through the molecular detection of alterations in the target site genes. As more efficient fungicides were developed and applied, the pathogen has continuously adapted through accumulating multiple target-site alterations. In order to accurately monitor these changes in field populations, it is therefore becoming increasingly important to completely sequence the targeted genes. Here we report the development of a PacBio assay that facilitates the multiplex amplification and long-read sequencing of the target gene(s) for the azole (CYP51), SDHI (Sdh B, C, and D), and QoI (cytochrome b) fungicides. The assay was developed and optimised using three Irish Z. tritici collections established in spring 2017, which capture the range of fungicide resistance present in modern European populations of Z. tritici. The sequences obtained through the PacBio assay were validated using traditional Sanger sequencing and in vitro sensitivity screenings. To further exploit the long-read and high throughput potential of PacBio sequencing, an additional nine housekeeping genes (act, BTUB, cal, cyp, EF1, GAPDH, hsp80-1, PKC, TFC1) were sequenced and used to provide comprehensive Z. tritici strain genotyping.


2018 ◽  
Vol 132 (4) ◽  
pp. 1121-1135 ◽  
Author(s):  
Cathérine Pauline Herter ◽  
Erhard Ebmeyer ◽  
Sonja Kollers ◽  
Viktor Korzun ◽  
Tobias Würschum ◽  
...  

2017 ◽  
Author(s):  
Graeme J. Kettles ◽  
Carlos Bayon ◽  
Caroline A. Sparks ◽  
Gail Canning ◽  
Kostya Kanyuka ◽  
...  

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.


Author(s):  
Tony Twamley ◽  
Mark Gaffney ◽  
Angela Feechan

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.


2019 ◽  
Author(s):  
Lydie Kerdraon ◽  
Matthieu Barret ◽  
Valérie Laval ◽  
Frédéric Suffert

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.


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