Multiple mutations across the succinate dehydrogenase gene complex are associated with boscalid resistance in Didymella tanaceti in pyrethrum

Pearce, T; Wilson, C. R.; Gent, David H.; Scott, Jason B.

doi:10.1371/journal.pone.0218569

Cited by 19 publications

(5 citation statements)

References 72 publications

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“…The G143A mutation of cytochrome b also emerged at least twice independently in European populations of Plasmopara viticola (Chen et al 2007). Multiple independent origins by parallel evolution were also inferred for mutations in the Sdh complex genes in Australian populations of Didymella tanaceti (Pearce et al 2019), and for several mutations conferring resistance to different modes of action in North American populations of Botrytis cinerea (Fernández-Ortuño et al 2015). As far as we are aware, the current study represents the only description of independent origins of the same amino acid substitution in the fungicide target site deriving from multiple distinct nucleotide substitutions.…”

Section: Discussionmentioning

confidence: 63%

Parallel evolution of multiple mechanisms for demethylase inhibitor fungicide resistance in the barley pathogenPyrenophora teresf. sp.maculata

Mair

Thomas

Dodhia

et al. 2019

Preprint

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The demethylase inhibitor (DMI) or group 3 fungicides are the most important class of compounds for the control both of plant and human fungal pathogens. The necrotrophic fungal pathogen Pyrenophora teres f. sp. maculata (Ptm), responsible for spot form of net blotch (SFNB), is currently the most significant disease of barley in Australia, and a disease of increasing concern worldwide. The main basis for management of SFNB is by fungicide application, and in Australia the DMIs predominate. Although reduced sensitivity to DMI fungicides has recently been described in the closely related pathogen P. teres f. sp. teres (Ptt), the mechanisms of DMI resistance have not thus far been described for Ptm. In this study, several different levels of sensitivity to DMI fungicides were identified in Western Australian strains of Ptm from 2016 onwards, and reduced sensitivity phenotypes were correlated with a number of distinct mutations in both the promoter region and coding sequence of the DMI target gene encoding cytochrome P450 sterol 14α-demethylase (Cyp51A). Five insertions elements of 134-base pairs in length were found at different positions within the upstream regulatory region of Cyp51A in both highly DMI-resistant (HR) and select moderately DMI-resistant (MR1) Ptm isolates. The five insertion elements had at least 95% sequence identity and were determined to be Solo-LTR (Long Terminal Repeat) elements, all deriving from Ty1/Copia-family LTR Retrotransposons. The 134-bp elements contained a predicted promoter sequence and several predicted transcription factor binding sites, and the presence of an insertion element was correlated with constitutive overexpression of Cyp51A. The substitution of phenylalanine by leucine at position 489 of the predicted amino acid sequence of CYP51A was found in both HR and select moderately DMI-resistant (MR2) Ptm isolates. The same F489L amino acid substitution has been previously reported in Western Australian strains of Ptt, where it has also been associated with reduced sensitivity to DMI fungicides. In Ptm, the F489L amino acid change was associated with either of three different single nucleotide polymorphisms in codon 489. This suggests that, in contrast to Ptt, in Ptm the F489L mutation has emerged as a result of three distinct mutational events. Moderately DMI-resistant isolates had one or the other of the F489L substitution or a promoter insertion mutation, whereas highly DMI-resistant isolates were found to have combinations of both mechanisms together. Therefore, multiple mechanisms acting both alone and in concert were found to contribute to the observed phenomena of DMI fungicide resistance in Ptm. Moreover, these mutations have apparently emerged repeatedly and independently in Western Australian Ptm populations, by a process of convergent or parallel evolution.

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Section: Discussionmentioning

confidence: 63%

Parallel evolution of multiple mechanisms for demethylase inhibitor fungicide resistance in the barley pathogenPyrenophora teresf. sp.maculata

Mair

Thomas

Dodhia

et al. 2019

Preprint

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“…Members of the family Didymellaceae (possibly Allophoma , Didymella , and Phoma and allied genera) also formed part of the microflora of P. unifilis eggs. These taxa comprise plant pathogenic, saprobic and endophytic species associated with a wide range of hosts, including crops [ 97 , 98 , 99 , 100 ]. More interestingly, the species Phoma multirostrata has been isolated from eggs of C. mydas [ 64 ], and several congenerics synthetize antifungal compounds with broad-spectrum activity [ 101 , 102 ].…”

Section: Discussionmentioning

confidence: 99%

Beyond Sea Turtles: Fusarium keratoplasticum in Eggshells of Podocnemis unifilis, a Threatened Amazonian Freshwater Turtle

García-Martín

Sarmiento-Ramírez

Diéguez-Uribeondo

2021

JoF

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The endangered yellow-spotted river turtle (Podocnemis unifilis) has experienced a dramatic population decline in the Ecuadorian Amazonia, mainly due to overexploitation of its eggs. To reverse this trend, the Wildlife Conservation Society has developed a head-start program in Yasuní National Park since 2008, but the potential risk that microbes associated with its eggs might represent for hatching success has not been evaluated yet. Members of the Fusarium solani species complex (FSSC) are involved in egg failure in sea turtles under natural and hatchery conditions, but their role in infecting the eggs of P. unifilis is unknown. In this study, we collected eggshells of P. unifilis and obtained 50 fungal and bacterial isolates. Some potentially pathogenic fungi of the genera Fusarium, Penicillium and Rhizopus were identified based on molecular data. Most importantly, the sea turtle pathogenic species F. keratoplasticum not only was present, but it was the most frequently found. Conversely, we have also isolated other microorganisms, such as Pseudomonas or Phoma-like species, producing a wide spectrum of antifungal compounds that may have a protective role against fungal diseases. Our survey provides useful information on potential pathogens found in P. unifilis eggshells, upon which the success of conservation programs may depend.

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“…Resistance development can compromise the effectiveness of boscalid, rendering it ineffective in controlling early blight. One of the primary boscalid targets within fungal cells is the succinate dehydrogenase (SDH) multi-subunit enzyme complex including SdhB, SdhC, and SdhD subunits (Pearce et al, 2019). Mutations in these SDH genes were identi ed as a key mechanism of resistance to boscalid in various fungal pathogens (Pearce et al, 2019, Campbell et al, 2020.…”

Section: Introductionmentioning

confidence: 99%

“…One of the primary boscalid targets within fungal cells is the succinate dehydrogenase (SDH) multi-subunit enzyme complex including SdhB, SdhC, and SdhD subunits (Pearce et al, 2019). Mutations in these SDH genes were identi ed as a key mechanism of resistance to boscalid in various fungal pathogens (Pearce et al, 2019, Campbell et al, 2020. These mutations change the amino acid composition of SDH subunits, disrupting the boscalid binding site and ultimately rendering the fungicide ineffective (Mostafanezhad et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

Assessing boscalid efficacy and resistance of large-spored Alternaria pathogens of potato and tomato crops

Kokaeva,

Berezov,

Pobedinskaya

et al. 2024

Preprint

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Large-spored Alternaria species of the section Porri were evaluated for resistance to boscalid through laboratory assays. Most isolates had EC50 values above 100 µg/mL, indicating widespread fungicide resistance. Only isolates of A. solani demonstrated sensitivity with EC50 values below 7 µg/mL. Isolates of A. linariae, A. protenta and A. alternariacida were resistant. A moderate level of resistance to the fungicide was found in A. grandis (mean EC50 = 76,8 µg/mL). Even though the resistance levels varied among strains, sampling location did not appear to be a significant factor. One of the primary targets of boscalid within fungal cells is the succinate dehydrogenase (SDH) enzyme complex, which consists of several subunits. Mutations in these genes have been identified to be a key mechanism of boscalid resistance in various fungal pathogens. Our study revealed the absence of H134R and H278Y mutations within the SdhB gene among the Alternaria isolates. We further analyzed the sequences from Sdh gene subunits B, C, and D in the isolates originating from potato, including A. alternariacida, A. grandis, A. linariae, A. protenta, and A. solani. This analysis identified several single nucleotide polymorphisms (SNPs) that effectively distinguished these isolates from the tomato-derived A. linariae ones.

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Multiple mutations across the succinate dehydrogenase gene complex are associated with boscalid resistance in Didymella tanaceti in pyrethrum

Cited by 19 publications

References 72 publications

Parallel evolution of multiple mechanisms for demethylase inhibitor fungicide resistance in the barley pathogenPyrenophora teresf. sp.maculata

Parallel evolution of multiple mechanisms for demethylase inhibitor fungicide resistance in the barley pathogenPyrenophora teresf. sp.maculata

Beyond Sea Turtles: Fusarium keratoplasticum in Eggshells of Podocnemis unifilis, a Threatened Amazonian Freshwater Turtle

Assessing boscalid efficacy and resistance of large-spored Alternaria pathogens of potato and tomato crops

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