Parallel evolution of multiple mechanisms for demethylase inhibitor fungicide resistance in the barley pathogen Pyrenophora teres f. sp. maculata

Mair, Wesley J.; Thomas, Geoffrey J.; Dodhia, Kejal N; Hills, Andrea; Jayasena, K. W.; Ellwood, Simon R.; Oliver, Richard P.; Lopez‐Ruiz, Francisco J.

doi:10.1016/j.fgb.2020.103475

Cited by 26 publications

(69 citation statements)

References 76 publications

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“…triticale (Menardo et al, 2016). Although true population frequencies cannot be estimated confidently, it is apparent that among the DMI-resistant WA Ptm isolates found so far, the clonal HR Ptm genotype was clearly predominant (Mair et al, 2020), suggesting the possibility of lineage replacement.…”

Section: Discussionmentioning

confidence: 94%

“…The use of DMI fungicides in barley in Australia begun in 1995 and has increased substantially in subsequent decades (Tucker et al, 2015). It appears likely that the Ptt-Ptm hybridization event took place in the last decade, because the point mutation c1467a in Cyp51A gene is absent in Ptm collections prior to 2017 (Mair et al, 2020), and the same Cyp51A point mutation in Ptt was found only from 2013 onwards (Mair et al, 2016). Analyses of samples from older collections may allow us to more accurately estimate the exact time of hybridisation using a population genomics approach.…”

Section: Discussionmentioning

confidence: 99%

“…A total of 48 HR Ptm isolates were obtained from diseased leaf and stubble samples collected in the 2017 and 2018 cropping seasons from nine locations across the barley growing regions of WA (Table 1). Fungal isolations from infected leaves were conducted as previously described (Mair et al, 2020). For isolation from infected stubble, tissue was washed with sterile water, dried on paper towel, placed in petri dishes on moist paper, and incubated at 15 °C for 5 days.…”

Section: Isolate Collection and Species Identification Using Form-specific Primersmentioning

confidence: 99%

“…Mutation F489L in the DMI fungicide target gene, Cyp51A, was found to be associated with DMI resistance in Ptt isolates since 2013 in Western Australia (WA) (Mair et al, 2016). From 2016 onwards, Ptm isolates resistant to DMI fungicides were found to carry mutation F489L and/or an insertion of a 134 bp fragment of a transposable element in the Cyp51A promoter region (Mair et al, 2020). Cyp51A exists as a single copy in Ptm while two copies have been identified in Ptt (Mair et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

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Species hybridisation and clonal expansion as a new fungicide resistance evolutionary mechanism in Pyrenophora teres spp

Turo

Mair

Martín

et al. 2021

Preprint

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The barley net blotch diseases are caused by two fungal species of the Pyrenophora genus. Specifically, spot form net blotch is caused by P. teres f. sp. maculata (Ptm) whereas net form net blotch is caused by P. teres f. sp. teres (Ptt). Ptt and Ptm show high genetic diversity in the field due to intraspecific sexual recombination and hybridisation of the two species although the latter is considered rare. Here we present occurrence of a natural Ptt/Ptm hybrid with azole fungicides resistance and its implication to barley disease management in Australia. We collected and sequenced a hybrid, 3 Ptm and 10 Ptt isolates and performed recombination analyses in the intergenic and whole genome level. Eleven out of 12 chromosomes showed significant (P < 0.05) recombination events in the intergenic regions while variable recombination rate showed significant recombination across all the chromosomes. Locus specific analyses of Cyp51A1 gene showed at least four recombination breakpoints including a point mutation that alter target protein function. This point mutation did not found in Ptt and Ptm collected prior to 2013 and 2017, respectively. Further genotyping of fourteen Ptt, 48 HR Ptm, fifteen Ptm and two P. teres isolates from barley grass using Diversity Arrays Technology markers showed that all HR Ptm isolates were clonal and not clustered with Ptt or Ptm. The result confirms occurrence of natural recombination between Ptt and Ptm in Western Australia and the HR Ptm is likely acquired azole fungicide resistance through recombination and underwent recent rapid selective sweep likely within the last decade. The use of available fungicide resistance management tactics are essential to minimise and restrict further dissemination of these adaptive HR Ptm isolates.

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Section: Discussionmentioning

confidence: 94%

Section: Discussionmentioning

confidence: 99%

Section: Isolate Collection and Species Identification Using Form-specific Primersmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Species hybridisation and clonal expansion as a new fungicide resistance evolutionary mechanism in Pyrenophora teres spp

Turo

Mair

Martín

et al. 2021

Preprint

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“…For CYP51, multiple origins were inferred for I381 V but not for other CYP51 mutations when studied in 2004-2005 European populations of Z. tritici (Brunner et al, 2008), nine CYP51 mutations previously reported in Z. tritici in Europe have evolved independently in Australia (McDonald et al, 2019), and the F489L substitution has arisen multiple times as three different synonymous codons in Australian populations of Pyrenophora teres f. sp. teres (Mair et al, 2020). However, there are not enough studies where the number of intraspecific origins has been inferred to make comparisons between fungicide classes.…”

Section: Cases Of Fungicide Resistance Listed By the Fungicide Resistancementioning

confidence: 99%

Contrasting levels of genetic predictability in the evolution of resistance to major classes of fungicides

Hawkins

Fraaije

2021

Molecular Ecology

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The extent to which evolution is predictable, both phenotypically and at a genetic level (Stern & Orgogozo, 2009), has wide-ranging implications in evolutionary biology, especially in systems such as pathogens and cancers, where predicting future evolution would enable the design of more durable treatments (Lässig et al., 2017). The emergence of resistance to drugs and pesticides is an example of rapid, contemporary evolution. It has important practical implications for human health and wellbeing, both directly through clinical drug resistance (Hughes & Andersson, 2015) and through impacts on food production (Fisher et al., 2018). It can also provide useful case studies of repeated evolution under a defined novel selective pressure, which could address wider evolutionary questions, including questions concerning the repeatability of evolution. Resistance has evolved repeatedly across pest and pathogen taxa, including antibiotic resistance in clinical (Baker et al., 2018) and plant pathogens (Sundin & Wang, 2018), insecticide and herbicide resistance in agricultural pests and weeds (Gould et al., 2018), and

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Detection of Ramularia collo‐cygni from barley in Australia using triplex quantitative and droplet digital PCR

Knight

Moslemi

Begum

et al. 2021

Pest Management Science

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BACKGROUND: Ramularia leaf spot (RLS), caused by Ramularia collo-cygni, is an emerging threat to barley (Hordeum vulgare L.) production. RLS has been reported in Australia, however only minimal information is available regarding its detection and distribution. Due to initial asymptomatic growth in planta, slow growth in vitro and symptomatic similarities to net blotch and physiological leaf spots, detection of this pathogen can be challenging. Quantitative polymerase chain reaction (PCR)-based methods for R. collo-cygni-specific identification and detection have been described, however these assays have been demonstrated to lack specificity. False-positive detections may have serious implications, thus we aimed to design a robust R. collocygni-specific PCR method.RESULTS: Using the phylogenetically informative RNA polymerase II second largest subunit (rpb2) and translation elongation factor 1-alpha (tef1-⊍) genes, along with the tef1-⊍ gene of H. vulgare, a triplex assay was developed for both quantitative and droplet digital PCR. The triplex assay detected R. collo-cygni DNA in barley leaves from New South Wales, South Australia, Tasmania, Victoria and Western Australia. No R. collo-cygni DNA was detected in barley seed grown in Western Australia.CONCLUSION: The presence of R. collo-cygni DNA has been confirmed in Australian barley crops, suggesting a distribution ranging across the southern barley growing regions of Australia. The R. collo-cygni-specific assay will be a valuable tool to assist with monitoring the distribution and impact of R. collo-cygni in Australia and other regions.

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Parallel evolution of multiple mechanisms for demethylase inhibitor fungicide resistance in the barley pathogen Pyrenophora teres f. sp. maculata

Cited by 26 publications

References 76 publications

Species hybridisation and clonal expansion as a new fungicide resistance evolutionary mechanism in Pyrenophora teres spp

Species hybridisation and clonal expansion as a new fungicide resistance evolutionary mechanism in Pyrenophora teres spp

Contrasting levels of genetic predictability in the evolution of resistance to major classes of fungicides

Detection of Ramularia collo‐cygni from barley in Australia using triplex quantitative and droplet digital PCR

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