The complex genomic basis of rapid convergent adaptation to pesticides across continents in a fungal plant pathogen

Hartmann, Fanny E.; Vonlanthen, Tiziana; Singh, Navreet; McDonald, Megan C.; Milgate, Andrew; Croll, Daniel

doi:10.1111/mec.15737

Cited by 20 publications

(15 citation statements)

References 80 publications

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“…Further studies on larger population are needed to verify the consistency of this finding. Understanding the evolutionary pressure of environmental fungicides also on clinical isolates may allow to better decipher the mechanisms leading to fungicide adaptation [41]. This can lead to set the most appropriate clinical and agricultural fungicide treatments under the "One health" framework applied to Fusarium pathogen control strategies [2].…”

Section: Discussionmentioning

confidence: 99%

Fusarium musae from Diseased Bananas and Human Patients: Susceptibility to Fungicides Used in Clinical and Agricultural Settings

Tava

Prigitano

Esposto

et al. 2021

JoF

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Fusarium musae belongs to the Fusarium fujikuroi species complex. It causes crown rot disease in banana but also keratitis and skin infections as well as systemic infections in immunocompromised patients. Antifungal treatments in clinical and agricultural settings rely mostly on molecules belonging to the azole class. Given the potential risk of pathogen spread from food to clinical settings, the goal of the work was to define the level of susceptibility to different azoles of a worldwide population of F. musae. Eight fungicides used in agriculture and five antifungals used in clinical settings (4 azoles and amphotericin B) were tested using the CLSI (Clinical and Laboratory Standards Institute) protocol methodology on 19 F. musae strains collected from both infected patients and bananas. The level of susceptibility to the different active molecules was not dependent on the source of isolation with the exception of fenbuconazole and difenoconazole which had a higher efficiency on banana-isolated strains. Minimal inhibitory concentrations (MICs) of the different molecules ranged from 0.12–0.25 mg/L for prochloraz to more than 16 mg/L for tetraconazole and fenbuconazole. Compared to the F. verticillioides, F. musae MICs were higher suggesting the importance of monitoring the potential future spread of this species also in clinical settings.

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Section: Discussionmentioning

confidence: 99%

Fusarium musae from Diseased Bananas and Human Patients: Susceptibility to Fungicides Used in Clinical and Agricultural Settings

Tava

Prigitano

Esposto

et al. 2021

JoF

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“…As a consequence, the pathogen showed rapid responses across all major wheat-producing areas to overcome host resistance and gain tolerance to fungicides in less than a decade 10 . Population genomic analyses showed that rapid adaptation of the pathogen was facilitated by parallel evolution across geographic regions 14 , 15 . However, a comprehensive picture of pathogen dispersal and adaptation across the global distribution range is lacking.…”

Section: Introductionmentioning

confidence: 99%

A thousand-genome panel retraces the global spread and adaptation of a major fungal crop pathogen

et al. 2023

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Human activity impacts the evolutionary trajectories of many species worldwide. Global trade of agricultural goods contributes to the dispersal of pathogens reshaping their genetic makeup and providing opportunities for virulence gains. Understanding how pathogens surmount control strategies and cope with new climates is crucial to predicting the future impact of crop pathogens. Here, we address this by assembling a global thousand-genome panel of Zymoseptoria tritici, a major fungal pathogen of wheat reported in all production areas worldwide. We identify the global invasion routes and ongoing genetic exchange of the pathogen among wheat-growing regions. We find that the global expansion was accompanied by increased activity of transposable elements and weakened genomic defenses. Finally, we find significant standing variation for adaptation to new climates encountered during the global spread. Our work shows how large population genomic panels enable deep insights into the evolutionary trajectory of a major crop pathogen.

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“…Although loci may be linked for genes which are close together on the same chromosome, resistance of Septoria to some high-risk fungicide classes is conferred by mutations to genes on different chromosomes, leading to independent assortment. For example, resistance to methyl benzimidazoles are caused by mutations to chromosome 1 whereas resistance to succinate dehydrogenase inhibitors can be caused by mutations to chromosome 4, 7 or 8 (Hartmann et al, 2020). The proportion of sexual reproduction between seasons is assumed to be constant, despite evidence that sexual reproduction is influenced by density of infection (Suffert et al, 2018;Eriksen et al, 2001).…”

mentioning

confidence: 99%

Optimal Resistance Management for Mixtures of High-Risk Fungicides: Robustness to the Initial Frequency of Resistance and Pathogen Sexual Reproduction

Taylor

Cunniffe

2023

Phytopathology®

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There is a strong consensus that selection for fungicide resistant pathogen strains can be most effectively limited by using applications of mixtures of fungicides designed to balance disease control against selection. However, how to do this in practice is not entirely characterised. Previous work indicates optimal mixtures of pairs of fungicides which are both at a high risk of resistance can be constructed using pairs of doses which select equally for both single resistant strains in the first year of application. What has not been addressed thus far is the important real-world case in which the initial levels of resistance to each fungicide differ, for example because the chemicals have been available for different lengths of time. We show how recommendations based on equal selection in the first year can be sub-optimal in this case. We introduce a simple alternative approach, based on equalising the frequencies of single resistant strains in the year that achieving acceptable levels of control is predicted to become impossible. We show that this strategy is robust to changes in parameters controlling pathogen epidemiology and fungicide efficacy. We develop our recommendation using a pre-existing, parameterised model of Zymoseptoria tritici (the pathogen causing Septoria leaf blotch on wheat), which exemplifies the range of plant pathogens which predominantly spread clonally, but for which sexual reproduction forms an important component of the life cycle. We show that pathogen sexual reproduction can influence the rate at which fungicide resistance develops, but does not qualitatively affect our optimal resistance management recommendation.

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The complex genomic basis of rapid convergent adaptation to pesticides across continents in a fungal plant pathogen

Cited by 20 publications

References 80 publications

Fusarium musae from Diseased Bananas and Human Patients: Susceptibility to Fungicides Used in Clinical and Agricultural Settings

Fusarium musae from Diseased Bananas and Human Patients: Susceptibility to Fungicides Used in Clinical and Agricultural Settings

A thousand-genome panel retraces the global spread and adaptation of a major fungal crop pathogen

Optimal Resistance Management for Mixtures of High-Risk Fungicides: Robustness to the Initial Frequency of Resistance and Pathogen Sexual Reproduction

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