scholarly journals Using epidemiological principles to explain fungicide resistance management strategies: why do mixtures outperform alternations?

2017 ◽  
Author(s):  
James A.D. Elderfield ◽  
Francisco J. Lopez-Ruiz ◽  
Frank van den Bosch ◽  
Nik J. Cunniffe
Keyword(s):  
Disease Control ◽  
Fungicide Resistance ◽  
Management Strategies ◽  
Total Yield ◽  
Resistance Management ◽  
Careful Consideration ◽  
List Type ◽  
Septoria Leaf Blotch ◽  
Grapevine Powdery Mildew ◽  
Label Dose

ABSTRACTWhether fungicide resistance management is optimised by spraying chemicals with different modes of action as a mixture (i.e. simultaneously) or in alternation (i.e. sequentially) has been studied by experimenters and modellers for decades, largely inconclusively.We use previously-parameterised and validated mathematical models of wheat septoria leaf blotch and grapevine powdery mildew to test which strategy provides better resistance management, using the total yield before fungicide-resistance causes disease control to become economically-ineffective (“lifetime yield”) to measure effectiveness.Lifetime yield is optimised by spraying as much low-risk fungicide as is permitted, combined with slightly more high-risk fungicide than needed for acceptable initial disease control, applying these fungicides as a mixture. This is invariant to model parameterisation and structure, as well as the pathosystem in question. However if comparison focuses on other metrics, for example lifetime yield at full label dose, either mixtures or alternation can be optimal.Our work shows how epidemiological principles can explain the evolution of fungicide resistance, and highlights a theoretical framework to address the question of whether mixtures or alternation provide better resistance management. Our work also demonstrates that precisely how spray strategies are compared must be given extremely careful consideration.

scholarly journals Using Epidemiological Principles to Explain Fungicide Resistance Management Tactics: Why do Mixtures Outperform Alternations?

2018 ◽  
Vol 108 (7) ◽  
pp. 803-817 ◽  
Author(s):  
James A. D. Elderfield ◽  
Francisco J. Lopez-Ruiz ◽  
Frank van den Bosch ◽  
Nik J. Cunniffe
Keyword(s):  
High Risk ◽  
Disease Control ◽  
Fungicide Resistance ◽  
Total Yield ◽  
Resistance Management ◽  
Careful Consideration ◽  
Low Risk ◽  
Model Parameterization ◽  
Grapevine Powdery Mildew ◽  
Label Dose

Whether fungicide resistance management is optimized by spraying chemicals with different modes of action as a mixture (i.e., simultaneously) or in alternation (i.e., sequentially) has been studied by experimenters and modelers for decades. However, results have been inconclusive. We use previously parameterized and validated mathematical models of wheat Septoria leaf blotch and grapevine powdery mildew to test which tactic provides better resistance management, using the total yield before resistance causes disease control to become economically ineffective (“lifetime yield”) to measure effectiveness. We focus on tactics involving the combination of a low-risk and a high-risk fungicide, and the case in which resistance to the high-risk chemical is complete (i.e., in which there is no partial resistance). Lifetime yield is then optimized by spraying as much low-risk fungicide as is permitted, combined with slightly more high-risk fungicide than needed for acceptable initial disease control, applying these fungicides as a mixture. That mixture rather than alternation gives better performance is invariant to model parameterization and structure, as well as the pathosystem in question. However, if comparison focuses on other metrics, e.g., lifetime yield at full label dose, either mixture or alternation can be optimal. Our work shows how epidemiological principles can explain the evolution of fungicide resistance, and also highlights a theoretical framework to address the question of whether mixture or alternation provides better resistance management. It also demonstrates that precisely how spray tactics are compared must be given careful consideration.[Formula: see text] Copyright © 2018 The Author(s). This is an open access article distributed under the CC BY 4.0 International license .

scholarly journals Mixtures as a Fungicide Resistance Management Tactic

2014 ◽  
Vol 104 (12) ◽  
pp. 1264-1273 ◽  
Author(s):  
Frank van den Bosch ◽  
Neil Paveley ◽  
Femke van den Berg ◽  
Peter Hobbelen ◽  
Richard Oliver
Keyword(s):  
At Risk ◽  
Disease Control ◽  
Fungicide Resistance ◽  
Management Strategies ◽  
Resistance Management ◽  
Relative Effect ◽  
Resistance Evolution ◽  
Modes Of Action ◽  
Selection For ◽  
Effective Life

We have reviewed the experimental and modeling evidence on the use of mixtures of fungicides of differing modes of action as a resistance management tactic. The evidence supports the following conclusions. 1. Adding a mixing partner to a fungicide that is at-risk of resistance (without lowering the dose of the at-risk fungicide) reduces the rate of selection for fungicide resistance. This holds for the use of mixing partner fungicides that have either multi-site or single-site modes of action. The resulting predicted increase in the effective life of the at-risk fungicide can be large enough to be of practical relevance. The more effective the mixing partner (due to inherent activity and/or dose), the larger the reduction in selection and the larger the increase in effective life of the at-risk fungicide. 2. Adding a mixing partner while lowering the dose of the at-risk fungicide reduces the selection for fungicide resistance, without compromising effective disease control. The very few studies existing suggest that the reduction in selection is more sensitive to lowering the dose of the at-risk fungicide than to increasing the dose of the mixing partner. 3. Although there are very few studies, the existing evidence suggests that mixing two at-risk fungicides is also a useful resistance management tactic. The aspects that have received too little attention to draw generic conclusions about the effectiveness of fungicide mixtures as resistance management strategies are as follows: (i) the relative effect of the dose of the two mixing partners on selection for fungicide resistance, (ii) the effect of mixing on the effective life of a fungicide (the time from introduction of the fungicide mode of action to the time point where the fungicide can no longer maintain effective disease control), (iii) polygenically determined resistance, (iv) mixtures of two at-risk fungicides, (v) the emergence phase of resistance evolution and the effects of mixtures during this phase, and (vi) monocyclic diseases and nonfoliar diseases. The lack of studies on these aspects of mixture use of fungicides should be a warning against overinterpreting the findings in this review.

scholarly journals Efficacy of Biopesticides and Leaf Removal in Grapevine Powdery Mildew Management

2016 ◽  
Vol 17 (2) ◽  
pp. 84-91
Author(s):  
Michelle M. Moyer ◽  
Jensena M. Newhouse ◽  
Gary G. Grove
Keyword(s):  
Powdery Mildew ◽  
Vitis Vinifera ◽  
Disease Control ◽  
Fungicide Resistance ◽  
Cultural Practices ◽  
Resistance Management ◽  
Leaf Removal ◽  
Control Programs ◽  
Bloom Period ◽  
Grapevine Powdery Mildew

Integrating biological-based fungicides into conventional spray programs may help with fungicide resistance management. However, little is known about how to best integrate these products while still maintaining maximum disease control. Programs with as few as one synthetic fungicide or as many as three synthetic fungicides added to a biopesticide-based rotation during the bloom period of Vitis vinifera had significantly better disease control than a biopesticide-only-based program. When integrated with different timings of fruit-zone leaf removal, specific combinations of biopesticide programs and fruit-zone leaf removal enhanced the efficacy of that program to be on par with disease control seen in a program entirely based on synthetic fungicides. This suggests that when designing a fungicide program using biopesticides as a base, the addition of a synthetic fungicide during the window of ontogenic susceptibility in clusters and the adoption of cultural practices such as leaf removal can significantly improve the efficacy of that program. Accepted for publication 11 April 2016. Published 20 April 2016.

Fungicide Resistance—Lessons for Herbicide Resistance Management?

1995 ◽  
Vol 9 (4) ◽  
pp. 840-849 ◽  
Author(s):  
Tobin L. Peever ◽  
Michael G. Milgroom
Keyword(s):  
Disease Control ◽  
Fungicide Resistance ◽  
Rapid Development ◽  
Management Strategies ◽  
Experimental Studies ◽  
Resistance Management ◽  
Pathogenic Fungi ◽  
Systemic Fungicides ◽  
Development Of Resistance ◽  
Pathogen Populations

Resistance to agricultural fungicides has increaséd dramatically in the past twenty years, following the introduction of systemic fungicides. Disease control failures associated with fungicide resistance have occurred with many classes of fungicides and in many genera of plant-pathogenic fungi. In some cases, resistance evolved extremely rapidly making the chemicals ineffective for disease control only a few years after they were introduced.The rapid development of resistance to systemic fungicides has led to efforts to develop strategies to avoid or delay the evolution of fungicide resistance in plant pathogen populations. Despite a widespread interest in managing fungicide resistance, very few experimental studies have been performed to elucidate the important factors controlling resistance development. Most fungicide resistance studies have consisted of anecdotal field observations which have rarely been followed up with experimentation. In order to understand what factors affect the evolution of resistance, and to use this information to design effective resistance management strategies, more experimental studies are required.

scholarly journals Fungicide resistance characterised across seven chemical classes in a Botrytis cinerea population isolated from Australian vineyards

2021 ◽  
Author(s):  
Lincoln A. Harper ◽  
Scott Paton ◽  
Barbara Hall ◽  
Suzanne McKay ◽  
Richard P. Oliver ◽  
...  
Keyword(s):  
Adverse Effect ◽  
Botrytis Cinerea ◽  
Fungicide Resistance ◽  
Chemical Control ◽  
Management Strategies ◽  
Resistance Management ◽  
Gray Mold ◽  
Chemical Groups ◽  
Important Disease ◽  
Selection Of

AbstractGray mold, caused by Botrytis cinerea, is an economically important disease of grapes in Australia and across grape growing regions worldwide. Control of this disease relies heavily on canopy management and the application of single site fungicides. Fungicide application can lead to the selection of fungicide resistant B. cinerea populations, which has an adverse effect on the chemical control of the disease. Characterising the distribution and severity of resistant B. cinerea populations is needed to inform resistance management strategies. In this study, 725 isolates were sampled from 75 Australian vineyards during 2013 – 2016 and were screened against seven fungicides with different MOAs. The resistance frequencies for azoxystrobin, boscalid, fenhexamid, fludioxonil, iprodione, pyrimethanil and tebuconazole were 5, 2.8, 2.1, 6.2, 11.6, 7.7 and 2.9% respectively. Nearly half of the resistant isolates (43.7%) were resistant to more than one of the fungicides tested. The frequency of vineyards with at least one isolate simultaneously resistant to 1, 2, 3, 4 or 5 fungicides was 19.5, 7.8, 6.5, 10.4 and 2.6%.Resistance was associated with previously published genotypes in CytB (G143A), SdhB (H272R/Y), Erg27 (F412S), Mrr1 (D354Y), Os1 (I365S, N373S + Q369P, I365S + D757N) and Pos5 (P319A, L412F). Expression analysis was used to characterise fludioxonil resistant isolates exhibiting overexpression (6.3 - 9.6-fold) of the ABC transporter encoded by AtrB (MDR1 phenotype). Novel genotypes were also described in Mrr1 (S611N, D616G) and Cyp51 (P357S). Resistance frequencies were lower when compared to most previously published surveys of both grape and non-grape B. cinerea resistance. Nonetheless, continued monitoring of critical chemical groups used in Australian vineyards is recommended.

scholarly journals Point Mutations in the β-Tubulin of Phytophthora sojae Confer Resistance to Ethaboxam

2019 ◽  
Vol 109 (12) ◽  
pp. 2096-2106 ◽  
Author(s):  
Qin Peng ◽  
Zhiwen Wang ◽  
Yuan Fang ◽  
Weizhen Wang ◽  
Xingkai Cheng ◽  
...  
Keyword(s):  
Fungicide Resistance ◽  
Germination Rate ◽  
Management Strategies ◽  
Resistance Management ◽  
Point Mutations ◽  
Phytophthora Sojae ◽  
Cross Resistance ◽  
Baseline Sensitivity ◽  
Resistant Mutants ◽  
Β Tubulin

Ethaboxam is a β-tubulin inhibitor registered for the control of oomycete pathogens. The current study was established to determine the ethaboxam sensitivity of the plant pathogen Phytophthora sojae and investigate the potential for the emergence of fungicide resistance. The effective concentration for 50% inhibition (EC50) of 112 Phytophthora sojae isolates exhibited a unimodal distribution with a mean EC50 for ethaboxam of 0.033 µg/ml. Establishing this baseline sensitivity provided critical data for monitoring changes in ethaboxam-sensitivity in field populations. The potential for fungicide resistance was investigated using adaptation on ethaboxam-amended V8 agar, which resulted in the isolation of 20 resistant mutants. An assessment of the biological characteristics of the mutants including mycelial growth, sporulation, germination rate and pathogenicity indicated that the resistance risk in Phytophthora sojae was low to medium with no cross-resistance between ethaboxam and cymoxanil, metalaxyl, flumorph, and oxathiapiprolin being detected. However, positive cross-resistance was found between ethaboxam and zoxamide for Q8L and I258V but negative cross-resistance for C165Y. Further investigation revealed that the ethaboxam-resistant mutants had point mutations at amino acids Q8L, C165Y, or I258V of their β-tubulin protein sequences. CRISPR/Cas9-mediated transformation experiments confirmed that the Q8L, C165Y, or I258V mutations could confer ethaboxam resistance in Phytophthora sojae and that the C165Y mutation induces high levels of resistance. Taken together, the results of the study provide essential data for monitoring the emergence of resistance and resistance management strategies for ethaboxam, as well as for improving the design of novel β-tubulin inhibitors for future development.

Fitness Penalties in the Evolution of Fungicide Resistance

2018 ◽  
Vol 56 (1) ◽  
pp. 339-360 ◽  
Author(s):  
N.J. Hawkins ◽  
B.A. Fraaije
Keyword(s):  
Fungicide Resistance ◽  
Management Strategies ◽  
Crop Protection ◽  
Resistance Management ◽  
Nutrient Status ◽  
Selective Advantage ◽  
Life Cycle Stage ◽  
Epistatic Interactions ◽  
Resistance Risk ◽  
Evolution Of Resistance

The evolution of resistance poses an ongoing threat to crop protection. Fungicide resistance provides a selective advantage under fungicide selection, but resistance-conferring mutations may also result in fitness penalties, resulting in an evolutionary trade-off. These penalties may result from the functional constraints of an evolving target site or from the resource allocation costs of overexpression or active transport. The extent to which such fitness penalties are present has important implications for resistance management strategies, determining whether resistance persists or declines between treatments, and for resistance risk assessments for new modes of action. Experimental results have proven variable, depending on factors such as temperature, nutrient status, osmotic or oxidative stress, and pathogen life-cycle stage. Functional genetics tools allow pathogen genetic background to be controlled, but this in turn raises the question of epistatic interactions. Combining fitness penalties under various conditions into a field-realistic scenario poses an important future challenge.

scholarly journals Whole genome sequencing elucidates the species-wide diversity and evolution of fungicide resistance in the early blight pathogen Alternaria solani

2021 ◽  
Author(s):  
Severin Einspanier ◽  
Tamara Susanto ◽  
Nicole Metz ◽  
Pieter J. Wolters ◽  
Vivianne G.A.A. Vleeshouwers ◽  
...  
Keyword(s):  
Genetic Diversity ◽  
Whole Genome Sequencing ◽  
Genome Sequencing ◽  
Fungicide Resistance ◽  
Early Blight ◽  
Management Strategies ◽  
Resistance Management ◽  
Alternaria Solani ◽  
Whole Genome ◽  
A Genome

Early blight of potato is caused by the fungal pathogen Alternaria solani and is an increasing problem worldwide. The primary strategy to control the disease is applying fungicides such as succinate dehydrogenase inhibitors (SDHI). SDHI-resistant strains, showing reduced sensitivity to treatments, appeared in Germany in 2013, five years after introduction of SDHIs. Two primary mutations in the Sdh complex (SdhB-H278Y and SdhC-H134R) have been frequently found throughout Europe. How these resistances arose and spread, and whether they are linked to other genomic features, remains unknown. We performed whole-genome sequencing for A. solani isolates from potato fields across Europe (Germany, Sweden, Belgium, and Serbia) to better understand the pathogen's genetic diversity in general and understand the development and spread of the genetic mutations that lead to SDHI resistance. We used ancestry analysis and phylogenetics to determine the genetic background of 48 isolates. The isolates can be grouped into 7 genotypes. These genotypes do not show a geographical pattern but appear spread throughout Europe. The Sdh mutations appear in different genetic backgrounds, suggesting they arose independently, and the observed admixtures might indicate a higher adaptive potential in the fungus than previously thought. Our research gives insights into the genetic diversity of A. solani on a genome level. The mixed occurrence of different genotypes and apparent admixture in the populations indicate higher genomic complexity than anticipated. The conclusion that SDHI tolerance arose multiple times independently has important implications for future fungicide resistance management strategies. These should not solely focus on preventing the spread of isolates between locations but also on limiting population size and the selective pressure posed by fungicides in a given field to avoid the rise of new mutations in other genetic backgrounds.

scholarly journals First Report of Resistance to Cyflufenamid in Podosphaera xanthii, Causal Agent of Powdery Mildew, from Melon and Zucchini Fields in Italy

Plant Disease ◽  
2014 ◽  
Vol 98 (11) ◽  
pp. 1581-1581 ◽  
Author(s):  
A. Pirondi ◽  
I. M. Nanni ◽  
A. Brunelli ◽  
M. Collina
Keyword(s):  
Powdery Mildew ◽  
Fungicide Resistance ◽  
Management Strategies ◽  
Resistance Management ◽  
Personal Communication ◽  
Causal Agent ◽  
Infected Leaf ◽  
Podosphaera Xanthii ◽  
Growing Seasons ◽  
Action Committee

The fungicide cyflufenamid (phenyl-acetamide, Fungicide Resistance Action Committee [FRAC] code U6) was approved for use in Italy in 2011 as Takumi (Certis Europe, Utrecht, The Netherlands) to control Podosphaera xanthii (Castagne) U. Braun. & N. Shishkoff, the main causal agent of cucurbit powdery mildew. Considering that strains of this pathogen have developed resistance to strobilurin (5) and demethylation inhibitor (DMI) (4) fungicides, cyflufenamid represented a viable alternative to control this disease. However, this fungicide is also prone to resistance development as illustrated by resistance of P. xanthii in Japan (3). In the 2012 and 2013 growing seasons, significant declines in cyflufenamid efficacy were observed in two experimental fields in the Apulia (AP) and Emilia-Romagna (ER) regions of Italy on Cucumis melo and Cucurbita pepo, respectively. Takumi had been applied four times at the recommended field rate of 0.15 liter/ha (15 μg/ml of active ingredient [a.i.]) each growing season since 2010 in each field. Powdery mildew-infected leaf samples were collected in 2012 from both fields (25 isolates from AP and 19 from ER), and from five gardens (one isolate per garden); while in 2013, samples were collected only from the ER field (two polyconidial isolates). Isolates were maintained on detached zucchini cotyledons (1). Sensitivity of the isolates to cyflufenamid was determined by leaf disk bioassays (4) using Takumi at 0.01, 0.1, 1, 10, 20, and 50 μg a.i./ml. The 50% effective concentration (EC50) and the minimum inhibitory concentration (MIC) values were calculated (2). Isolates collected in ER and the gardens in 2012 all had an EC50< 0.01 μg/ml, and the MIC ranged from <0.01 to <1 μg/ml. Isolates from AP in 2012 had elevated EC50 values, from 0.230 to >50 μg/ml, and MIC values from <10 to >50 μg/ml; by 2013, the EC50 values of ER isolates ranged from 3.35 to >50 μg/ml. Based on the mean EC50 value of 0.0019 μg/ml for sensitive isolates of P. xanthii in Japan (2), isolates from both the ER field and gardens in 2012 were considered sensitive to cyflufenamid. Additionally, EC50 values of AP isolates from 2012 and ER isolates from 2013 were greater than those of sensitive isolates, indicating a shift in sensitivity toward resistance to cyflufenamid (resistance factor >100 [2]). Consequently, poor control of powdery mildew with cyflufenamid applications in the AP and ER trials was most likely a result of fungicide resistance. Isolates from these fields were exposed to selection pressure for fungicide resistance because cyflufenamid was applied more times than permitted in the label instructions. However, control of powdery mildew in 2013 was not as effective as in previous years in commercial fields in AP (C. Dongiovanni, personal communication). This observation, combined with proof of reduced sensitivity of some P. xanthii strains in Italy to cyflufenamid, highlights the need for implementing resistance management strategies to minimize the risk of fungicide resistant strains developing in cucurbit fields. References: (1) B. Álvarez and J. A. Torés. Bol. San. Veg. Plagas 23:283, 1997. (2) M. Haramoto et al. J. Pest. Sci. 31:397, 2006. (3) H. Hosokawa et al. Jpn. J. Phytopathol. 72:260, 2006. (4) M. T. McGrath et al. Plant Dis. 80:697, 1996. (5) M. T. McGrath and N. Shishkoff. Plant. Dis. 87:1007, 2003.

scholarly journals Optimal Fungicide Application Timings for Disease Control Are Also an Effective Anti-Resistance Strategy: A Case Study for Zymoseptoria tritici (Mycosphaerella graminicola) on Wheat

2013 ◽  
Vol 103 (12) ◽  
pp. 1209-1219 ◽  
Author(s):  
F. van den Berg ◽  
F. van den Bosch ◽  
N. D. Paveley
Keyword(s):  
Disease Control ◽  
Fungicide Resistance ◽  
Flag Leaf ◽  
Resistance Management ◽  
Equation Model ◽  
Effective Control ◽  
Zymoseptoria Tritici ◽  
Fungicide Application ◽  
T1 And T2 ◽  
Effective Life

Strategies to slow fungicide resistance evolution often advocate early “prophylactic” fungicide application and avoidance of “curative” treatments where possible. There is little evidence to support such guidance. Fungicide applications are usually timed to maximize the efficiency of disease control during the yield-forming period. This article reports mathematical modeling to explore whether earlier timings might be more beneficial for fungicide resistance management compared with the timings that are optimal for efficacy. There are two key timings for fungicide treatment of winter wheat in the United Kingdom: full emergence of leaf three (counting down the canopy) and full emergence of the flag leaf (leaf 1). These timings (referred to as T1 and T2, respectively) maximize disease control on the upper leaves of the crop canopy that are crucial to yield. A differential equation model was developed to track the dynamics of leaf emergence and senescence, epidemic growth, fungicide efficacy, and selection for a resistant strain. The model represented Zymoseptoria tritici on wheat treated twice at varying spray timings. At all fungicide doses tested, moving one or both of the two sprays earlier than the normal T1 and T2 timings reduced selection but also reduced efficacy. Despite these opposing effects, at a fungicide dose just sufficient to obtain effective control, the T1 and T2 timings optimized fungicide effective life (the number of years that effective control can be maintained). At a higher dose, earlier spray timings maximized effective life but caused some reduction in efficacy, whereas the T1 and T2 timings maximized efficacy but resulted in an effective life 1 year shorter than the maximum achievable.

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