Deep amplicon sequencing reveals extensive allelic diversity in the erg11/CYP51 promoter and allows multi-population DMI fungicide resistance monitoring in the canola pathogen Leptosphaeria maculans

Scanlan, Jack L.; Mitchell, Adele A.; Marcroft, S. J.; Forsyth, L.; Idnurm, Alexander; Wouw, Angela P. Van de

doi:10.1016/j.fgb.2023.103814

Cited by 3 publications

(2 citation statements)

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“…At present, research on the relationship between fungicides and fungal diversity mainly focuses on the relationship between the resistance of fungicides and the genetic diversity of fungi [1,[4][5][6]52]. The main idea of our research was to investigate the changes in the circadian clock and fruiting body of C. militaris under the influence of fungicides.…”

Section: Discussionmentioning

confidence: 99%

“…The use of fungicides creates a strong selection pressure on the fungus, which reduces the effectiveness of the fungicide. Scanlan et al showed that the DNA insertions into the promoter of the erg11/CYP51 DMI target gene resulted in changes in the canola pathogen Leptosphaeria maculans resistance to demethylation inhibitor (DMI) fungicides [1]. Some fungicides induce a genetic change in Monilinia fructicola in the form of transposon transposition [2].…”

Section: Introductionmentioning

confidence: 99%

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The Stress of Fungicides Changes the Expression of Clock Protein CmFRQ and the Morphology of Fruiting Bodies of Cordyceps militaris

Peng,

Zhang,

Huang

et al. 2024

JoF

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The physiological, biochemical, and morphological changes brought about by fungi in response to fungicides can undoubtedly bring diversity to fungi. Cordyceps militaris strains TN (mating type genes MAT1-1-1, MAT1-1-2, and MAT1-2-1) and CmFRQ-454 (mating type genes MAT1-1-1 and MAT1-1-2) were treated with non-lethal doses of fungicides amphotericin B, L-cysteine, terbinafine, and 5-fluorocytosine. The results showed that the treatment with amphotericin B, terbinafine, and 5-fluorocytosine promoted an increase in the relative content of clock protein CmFRQ (C. militaris FREQUENCY) in the mycelium of strain TN, while the high concentration of L-cysteine inhibited the expression of CmFRQ in strain TN. These four fungicides could reduce the relative contents of CmFRQ in the mycelium of strain CmFRQ454. The relative contents of CmFRQ in the mycelium of strain TN were increased after removing the four fungicides, but the relative contents of CmFRQ in the mycelium of strain CmFRQ454 were decreased after removing the four fungicides. This indicates that the effect of fungicides on CmFRQ on mycelium was still sustained after removing the stress of fungicides, and the operation of the circadian clock was changed. The fruiting bodies of C. militaris strain TN and CmFRQ-454 were still degenerated to varying degrees after removing amphotericin B, L-cysteine, and terbinafine. However, the fruiting bodies of strain TN after removing 5-fluorocytosine did not show significant degeneration; the fruiting bodies of strain CmFRQ-454 after removing 5-fluorocytosine obtained rejuvenation. These results indicate that the stress of fungicides could lead to the degeneration of fruiting bodies as well as the rejuvenation of fruiting bodies, resulting in the morphological diversity of C. militaris. The increase or decrease of the CmFRQ-454, the main component of the circadian clock, caused by the stress of fungicants, might lead to the differential degeneration of different mating-type strains of C. militaris.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The Stress of Fungicides Changes the Expression of Clock Protein CmFRQ and the Morphology of Fruiting Bodies of Cordyceps militaris

Peng,

Zhang,

Huang

et al. 2024

JoF

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Evolution of decreased sensitivity to azole fungicides in western European populations of Plenodomus lingam (Phoma stem canker on oilseed rape)

King,

Barr,

Bousquet

et al. 2024

Plant Pathology

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Plenodomus lingam (Leptosphaeria maculans) and P. biglobosus (L. biglobosa) are fungi causing Phoma leaf spot/stem canker, an international damaging disease of oilseed rape (Brassica napus) and other brassicas. In Europe, fungicides used for disease management are mainly sterol 14α‐demethylase (CYP51) inhibitors (DMIs/azoles); quinone‐outside inhibitors (QoIs) and succinate dehydrogenase inhibitors (SDHIs) are also used. Decreased DMI sensitivity has emerged in Australian and eastern European P. lingam populations and is mediated by CYP51 promoter inserts resulting in target site overexpression. In this study using in vitro sensitivity testing, we report decreased DMI (prothioconazole‐desthio, mefentrifluconazole) sensitivity in modern western European P. lingam isolates (collected 2022–2023) compared to older baseline (1992–2005) isolates. Around 85% of modern western European P. lingam isolates collected, for which the CYP51 promoter region was sequenced, carried a promoter insert, but target site alterations were not detected. Six different CYP51 promoter inserts were identified, most commonly a 237 bp fragment of the Sahana transposable element. Inserts were associated with an approximately 3‐ to 10‐fold decrease in sensitivity to the DMIs tested. In contrast to P. lingam, PCR screening revealed CYP51 promoter inserts were absent in modern western European P. biglobosus isolates (2021–2023). Combined data indicate P. lingam isolates lacking an insert were similarly (or slightly more) sensitive to the DMIs tested for P. biglobosus, whereas those carrying an insert were slightly less sensitive than P. biglobosus. No evidence for substantive sensitivity shifts to the QoI (pyraclostrobin) or SDHI (boscalid) fungicides tested was obtained for either Plenodomus species.

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Genome‐wide mapping in an international isolate collection identifies a transcontinental erg11/CYP51 promoter insertion associated with fungicide resistance in Leptosphaeria maculans

Scanlan,

Idnurm,

Van de Wouw

2024

Plant Pathology

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Fungicide resistance is often conferred through the mutation of genes encoding fungicide targets or proteins that remove fungicides from cells, but mechanisms can vary widely between taxa. Discovering the specific resistance alleles present in pathogen populations is essential for monitoring the evolution and movement of resistant genotypes. In this study, we explored the genomic basis of demethylase inhibitor (DMI) resistance in Leptosphaeria maculans, the main pathogen of the canola crop Brassica napus. Using an international collection of over 200 genome‐sequenced isolates, we assayed in vitro sensitivity to the DMI tebuconazole and conducted a genome‐wide association study on a variant set including single‐nucleotide polymorphisms (SNPs), small indels and structural variants. The main resistance allele identified was a 237 bp remnant transposable element insertion in the promoter of the erg11/CYP51 DMI target gene in a large proportion of isolates from Europe, an allele known to confer DMI resistance in Australia. Several associated loci were identified, none of which are commonly linked to DMI resistance in other phytopathogens. We also found little to no relationship between DMI tolerance and baseline growth rate, suggesting minimal fitness effects of fungicide resistance in these isolates. This study indicates common DMI resistance alleles in L. maculans are shared across continents and erg11/CYP51 coding mutations, which are near‐ubiquitous in other fungal pathogens, may not underpin DMI resistance in this species. Furthermore, that resistance occurs frequently in numerous canola‐growing regions suggests management is essential for growers.

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Deep amplicon sequencing reveals extensive allelic diversity in the erg11/CYP51 promoter and allows multi-population DMI fungicide resistance monitoring in the canola pathogen Leptosphaeria maculans

Cited by 3 publications

References 68 publications

The Stress of Fungicides Changes the Expression of Clock Protein CmFRQ and the Morphology of Fruiting Bodies of Cordyceps militaris

The Stress of Fungicides Changes the Expression of Clock Protein CmFRQ and the Morphology of Fruiting Bodies of Cordyceps militaris

Evolution of decreased sensitivity to azole fungicides in western European populations of Plenodomus lingam (Phoma stem canker on oilseed rape)

Genome‐wide mapping in an international isolate collection identifies a transcontinental erg11/CYP51 promoter insertion associated with fungicide resistance in Leptosphaeria maculans

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