Field strains of Stemphylium vesicarium with a resistance to dicarboximide fungicides correlated with changes in a two-component histidine kinase

Alberoni, Giulia; Lanen, Catherine; Leroux, Pierre; Brunelli, A.

doi:10.1007/s10658-010-9642-9

Cited by 12 publications

(7 citation statements)

References 24 publications

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“…This suggests similar molecular mechanisms for resistance. Resistance to the dicarboximide iprodione and/or to the phenylpyrrole fludioxonil is conferred in many fungi by mutations of the osmosensing histidine kinase, which is orthologous to Bos1 in B. cinerea (reviewed in [52] ). We therefore sequenced the bos1 gene in the G20P and G20I induced mutants and compared it to that of the parental G0 strains.…”

Section: Resultsmentioning

confidence: 99%

“…Although their precise mode of action remains unclear, Pillonel and Meyer [30] showed differences in protein kinase inhibition profiles between phenylpyrrole and dicarboximide fungicides. In many plant pathogenic fungi, isolates cross-resistant to both fungicides harbour mutations in the osmo-sensing histidine kinase gene (reviewed in [52] ). In this study we compared the selection exerted by the dicarboximide iprodione to that exerted by pyrrolnitrin, a natural and structural analogue of phenylpyrroles, on the function and structure of the histidine-kinase Bos1 of B. cinerea .…”

Section: Discussionmentioning

confidence: 99%

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Functional and Structural Comparison of Pyrrolnitrin- and Iprodione-Induced Modifications in the Class III Histidine-Kinase Bos1 of Botrytis cinerea

Fillinger

Ajouz²,

Nicot³

et al. 2012

PLoS ONE

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Dicarboximides and phenylpyrroles are commonly used fungicides against plant pathogenic ascomycetes. Although their effect on fungal osmosensing systems has been shown in many studies, their modes-of-action still remain unclear. Laboratory- or field-mutants of fungi resistant to either or both fungicide categories generally harbour point mutations in the sensor histidine kinase of the osmotic signal transduction cascade.In the present study we compared the mechanisms of resistance to the dicarboximide iprodione and to pyrrolnitrin, a structural analogue of phenylpyrrole fungicides, in Botrytis cinerea. Pyrrolnitrin-induced mutants and iprodione-induced mutants of B. cinerea were produced in vitro. For the pyrrolnitrin-induced mutants, a high level of resistance to pyrrolnitrin was associated with a high level of resistance to iprodione. For the iprodione-induced mutants, the high level of resistance to iprodione generated variable levels of resistance to pyrrolnitrin and phenylpyrroles. All selected mutants showed hypersensitivity to high osmolarity and regardless of their resistance levels to phenylpyrroles, they showed strongly reduced fitness parameters (sporulation, mycelial growth, aggressiveness on plants) compared to the parental phenotypes. Most of the mutants presented modifications in the osmosensing class III histidine kinase affecting the HAMP domains. Site directed mutagenesis of the bos1 gene was applied to validate eight of the identified mutations. Structure modelling of the HAMP domains revealed that the replacements of hydrophobic residues within the HAMP domains generally affected their helical structure, probably abolishing signal transduction. Comparing mutant phenotypes to the HAMP structures, our study suggests that mutations perturbing helical structures of HAMP2-4 abolish signal-transduction leading to loss-of-function phenotype. The mutation of residues E529, M427, and T581, without consequences on HAMP structure, highlighted their involvement in signal transduction. E529 and M427 seem to be principally involved in osmotic signal transduction.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Functional and Structural Comparison of Pyrrolnitrin- and Iprodione-Induced Modifications in the Class III Histidine-Kinase Bos1 of Botrytis cinerea

Fillinger

Ajouz²,

Nicot³

et al. 2012

PLoS ONE

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“…The HHKs involved in fludioxonil sensing are principally those belonging to class III (Ochiai et al, 2001; Avenot et al, 2005; Motoyama et al, 2005; Viaud et al, 2006; Dongo et al, 2009; Alberoni et al, 2010; Furukawa et al, 2012), but some data indicate a possible role in phenylpyrrole sensing of other HHKs. In Candida lusitaniae Chk1, the HHK of class VI, homologous to the osmosensing HHK Sln1 of S. cerevisiae , interferes with phenylpyrrole sensitivity (Chapeland-Leclerc et al, 2007).…”

Section: Fungal Histidine Kinases Linked To Phenylpyrrole Resistancementioning

confidence: 99%

“…They localize within or between the HAMP domains of the HHKs (Oshima et al, 2002; Alberoni et al, 2010; Fillinger et al, 2012; Firoz et al, 2015), while others are frameshift or non-sense mutations (Ochiai et al, 2001; Iacomi-Vasilescu et al, 2004; Duan et al, 2014; Ren et al, 2016). Altogether these results are in agreement with the hypothesis that in most cases loss-of-function mutations are responsible for fludioxonil resistance in plant pathogenic fungi (mainly laboratory mutants; reviewed in Defosse et al, 2015), but mutations leading to modified function or even constitutively active HHK may exist as well, probably at very low frequencies.…”

Section: Fungal Histidine Kinases Linked To Phenylpyrrole Resistancementioning

confidence: 99%

Phenylpyrroles: 30 Years, Two Molecules and (Nearly) No Resistance

Kilani¹,

Fillinger²

2016

Front. Microbiol.

103

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Phenylpyrroles are chemical analogs of the natural antifungal compound pyrrolnitrin. Fenpiclonil, but mainly fludioxonil are registered against multiple fungal crop diseases since over 25 years for seed or foliar treatment. They have severe physiological impacts on the pathogen, including membrane hyperpolarization, changes in carbon metabolism and the accumulation of metabolites leading to hyphal swelling and burst. The selection and characterization of mutants resistant to phenylpyrroles have revealed that these fungicides activate the fungal osmotic signal transduction pathway through their perception by a typical fungal hybrid histidine kinase (HHK). The HHK is prone to point mutations that confer fungicide resistance and affect its sensor domain, composed of tandem repeats of HAMP motifs. Fludioxonil resistant mutants have been selected in many fungal species under laboratory conditions. Generally they present severe impacts on fitness parameters. Since only few cases of field resistance specific to phenylpyrroles have been reported one may suspect that the fitness penalty of phenylpyrrole resistance is the reason for the lack of field resistance.

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“…(Dry et al 2004;Avenot et al 2005;Luo et al 2008Luo et al , 2012, Sclerotinia spp. (Ma et al 2009;Kuang et al 2011;Duan et al 2013), B. cinerea (Fraile et al 1986;Oshima et al 2002;Cui et al 2004;Grabke et al 2014), Magnaporthe grisea (Motoyama et al 2005), Stemphylium vesicarium (Alberoni et al 2010), Neurospora crassa (Fujimura et al 2000;Miller et al 2002;Ochiai et al 2010) and Cochliobolus heterostrophus (Yoshimi et al 2003(Yoshimi et al , 2004. The molecular mechanisms of DCFresistance include amino acid substitution in group III HK proteins, deletion or insertion mutations in their coding regions (Cui et al 2004;Dry et al 2004;Luo et al 2008).…”

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confidence: 99%

Biochemical and molecular characterization of Alternaria alternata isolates highly resistant to procymidone from broccoli and cabbage

et al. 2021

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Alternaria alternata, a causal agent of leaf blights and spots on a wide range of hosts, has a high risk of developing resistance to fungicides. Procymidone, a dicarboximide fungicide (DCF), has been widely used in controlling Alternaria leaf blights in China for decades. However, the resistance of A. alternata against DCFs has rarely been reported from crucifer plants. A total of 198 A. alternata isolates were collected from commercial fields of broccoli and cabbage during 2018–2019, and their sensitivities to procymidone were determined. Biochemical and molecular characteristics were subsequently compared between the high-level procymidone-resistant (ProHR) and procymidone-sensitive (ProS) isolates, and also between ProHR isolates from broccoli and cabbage. Compared with ProS isolates, the mycelial growth rate, sporulation capacity and virulence of most ProHR isolates were reduced; ProHR isolates displayed an increased sensitivity to osmotic stresses and a reduced sensitivity to sodium dodecyl sulfate (SDS); all ProHR isolates showed a reduced sensitivity to hydrogen peroxide (H2O2) except for the isolate B102. Correlation analysis revealed a positive cross-resistance between procymidone and iprodione, or fludioxonil. When treated with 10 μg/mL of procymidone, both mycelial intracellular glycerol accumulations (MIGAs) and relative expression of AaHK1 in ProS isolates were higher than those in ProHR isolates. Sequence alignment of AaHK1 from ten ProHR isolates demonstrated that five of them possessed a single-point mutation (P94A, V612L, E708K or Q924STOP), and four isolates had an insertion or a deletion in their coding regions. No significant difference in biochemical characteristics was observed among ProHR isolates from two different hosts, though mutations in AaHK1 of the cabbage-originated ProHR isolates were distinct from those of the broccoli-originated ProHR isolates.

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Field strains of Stemphylium vesicarium with a resistance to dicarboximide fungicides correlated with changes in a two-component histidine kinase

Cited by 12 publications

References 24 publications

Functional and Structural Comparison of Pyrrolnitrin- and Iprodione-Induced Modifications in the Class III Histidine-Kinase Bos1 of Botrytis cinerea

Functional and Structural Comparison of Pyrrolnitrin- and Iprodione-Induced Modifications in the Class III Histidine-Kinase Bos1 of Botrytis cinerea

Phenylpyrroles: 30 Years, Two Molecules and (Nearly) No Resistance

Biochemical and molecular characterization of Alternaria alternata isolates highly resistant to procymidone from broccoli and cabbage

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