PdSlt2 Penicillium digitatum mitogen-activated-protein kinase controls sporulation and virulence during citrus fruit infection

Ramón-Carbonell, Marta de; Sánchez-Torres, Paloma

doi:10.1016/j.funbio.2017.09.004

Cited by 17 publications

(17 citation statements)

References 53 publications

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“…Disruption of slt2 led to increased sensitivity to DMI-fungicide imazalil in wheat pathogen M. graminicola [93], also suggesting Slt2-MAPK function in fungal DMIresistance. However, slt2-deleted P. digitatum exhibited no obvious change in DMI-resistance [73], indicating that Slt2-MAPK might be irrelevant to the fungal anti-DMI strategy. Actually, according to prochloraz-resistant P. digitatum transcriptomes [11], the orthologs of PiSlt2-MAPK genes were not included in up-regulated DEGs (Additional file 13: Table S9).…”

Section: Discussionmentioning

confidence: 97%

“…These results suggested different strategies in ERGs response of the two Penicillium species to develop DMIresistance. Fungal multidrug resistance has been linked with MAPK signaling pathways including Slt2-MAPK [73,[90][91][92]. The Slt2-MAPK middle-stream components, two MAPKK-encoding genes ScMkk1 and ScMkk2, have been characterized in the model yeast S. cerevisiae to function in CWI signaling-mediated fungicide resistance [90,91].…”

Section: Discussionmentioning

confidence: 99%

“…The mitogen-activated protein (MAP) kinase signaling pathways, ubiquitously found in eukaryotes (from yeasts to various pathogenic fungi), comprise a set of cascaded protein kinases, MAP kinase kinase kinase (MAPKKK), MAP kinase kinase (MAPKK) and MAP kinase (MAPK), acting in series to modulate target protein activities [63,64]. Three major MAPK signaling pathways, Fus3/Kss1, Hog1, and Slt2, have been revealed in model yeasts [65][66][67] and filamentous fungi, including the citrus pathogens Alternaria alternata [68][69][70][71] and P. digitatum [72,73], regulating pheromone/invasion processes, high osmolarity glycerol anabolism, and stress-induced cell wall remodeling, respectively. Hog1-MAPK (PdOs2)-mediated CWI signaling are involved in P. digitatum resistance to the fungicides iprodione and fludioxonil [72].…”

Section: (Continued From Previous Page)mentioning

confidence: 99%

“…FgOs2 also participated in Fusarium graminearum resistance to fludioxonil [76]. The latest evidence has suggested an essential role of PdSlt2 MAPK in regulating gene expression to develop azole-fungicide resistance [73]. Ca 2+ signaling via Ca 2+ /calmodulin (CaM)dependent kinases (CaMKs), usually linked with particular MAPK pathway(s), extensively participates in fungal responses to environmental stresses.…”

Section: (Continued From Previous Page)mentioning

confidence: 99%

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Transcriptome analysis of fungicide-responsive gene expression profiles in two Penicillium italicum strains with different response to the sterol demethylation inhibitor (DMI) fungicide prochloraz

Zhang

Cao

et al. 2020

BMC Genomics

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Background: Penicillium italicum (blue mold) is one of citrus pathogens causing undesirable citrus fruit decay even at strictly-controlled low temperatures (< 10°C) during shipping and storage. P. italicum isolates with considerably high resistance to sterol demethylation inhibitor (DMI) fungicides have emerged; however, mechanism(s) underlying such DMI-resistance remains unclear. In contrast to available elucidation on anti-DMI mechanism for P. digitatum (green mold), how P. italicum DMI-resistance develops has not yet been clarified.Results: The present study prepared RNA-sequencing (RNA-seq) libraries for two P. italicum strains (highly resistant (Pi-R) versus highly sensitive (Pi-S) to DMI fungicides), with and without prochloraz treatment, to identify prochlorazresponsive genes facilitating DMI-resistance. After 6 h prochloraz-treatment, comparative transcriptome profiling showed more differentially expressed genes (DEGs) in Pi-R than Pi-S. Functional enrichments identified 15 DEGs in the prochloraz-induced Pi-R transcriptome, simultaneously up-regulated in P. italicum resistance. These included ATP-binding cassette (ABC) transporter-encoding genes, major facilitator superfamily (MFS) transporter-encoding genes, ergosterol (ERG) anabolism component genes ERG2, ERG6 and EGR11 (CYP51A), mitogen-activated protein kinase (MAPK) signaling-inducer genes Mkk1 and Hog1, and Ca 2+ /calmodulin-dependent kinase (CaMK) signalinginducer genes CaMK1 and CaMK2. Fragments Per Kilobase per Million mapped reads (FPKM) analysis of Pi-R transcrtiptome showed that prochloraz induced mRNA increase of additional 4 unigenes, including the other two ERG11 isoforms CYP51B and CYP51C and the remaining kinase-encoding genes (i.e., Bck1 and Slt2) required for Slt2-MAPK signaling. The expression patterns of all the 19 prochloraz-responsive genes, obtained in our RNA-seq data sets, have been validated by quantitative real-time PCR (qRT-PCR). These lines of evidence in together draw a general portrait of anti-DMI mechanisms for P. italicum species. Intriguingly, some strategies adopted by the present Pi-R were not observed in the previously documented prochloraz-resistant P. digitatum transcrtiptomes. These included simultaneous induction of all major EGR11 isoforms (CYP51A/B/C), over-expression of ERG2 and ERG6 to modulate ergosterol anabolism, and concurrent mobilization of Slt2-MAPK and CaMK signaling processes to overcome fungicide-induced stresses.

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Section: Discussionmentioning

confidence: 97%

Section: Discussionmentioning

confidence: 99%

Section: (Continued From Previous Page)mentioning

confidence: 99%

Section: (Continued From Previous Page)mentioning

confidence: 99%

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Transcriptome analysis of fungicide-responsive gene expression profiles in two Penicillium italicum strains with different response to the sterol demethylation inhibitor (DMI) fungicide prochloraz

Zhang

Cao

et al. 2020

BMC Genomics

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“…Besides, most MFS transporters that affect virulence act as a toxin efflux pumps that contributes to the self-preservation of different toxins, and disruption of these genes drastically reduces pathogenicity [10,37]. However, among the several virulence genes described in P. digitatum that included a protein kinase [38], a chitin synthase [39], a o-mannosyl transferase [40], proteases [21], polygalacturonases [41], transcription factors [18,[42][43][44], and MAP kinases [45,46], no toxin has been reported for P. digitatum to be involved in virulence processes. In that sense, the role of PdMFS1 in fungal virulence might be related to the elimination of host defense compounds.…”

Section: Discussionmentioning

confidence: 99%

PdMFS1 Transporter Contributes to Penicilliun digitatum Fungicide Resistance and Fungal Virulence during Citrus Fruit Infection

Ramón-Carbonell

López‐Pérez

González-Candelas

et al. 2019

JoF

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A new Penicillium digitatum major facilitator superfamily (MFS) transporter (PdMFS1) was identified and functionally characterized in order to shed more light on the mechanisms underlying fungicide resistance. PdMFS1 can play an important role in the intensification of resistance to fungicides normally used in P. digitatum postharvest treatments. In the PdMFS1 disrupted mutants, a slight effect in response to chemical fungicides was observed, but fungicide sensitivity was highly affected in the overexpression mutants which became resistant to wide range of chemical fungicides. Moreover, P. digitatum knock-out mutants exhibited a lower rate of fungal virulence when infected oranges were stored at 20 °C. Disease symptoms were higher in the PdMFS1 overexpression mutants coming from the low-virulent P. digitatum parental strain. In addition, the gene expression analysis showed an induction of PdMFS1 transcription in all overexpression mutants regardless from which progenitor came from, and four-time intensification of the parental wild type strain during citrus infection reinforcing PdMFS1 role in fungal virulence. The P. digitatum MFS transporter PdMFS1 contributes not only to the acquisition of wide range of fungicide resistance but also in fungal virulence during citrus infection.

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Differential roles, crosstalk and response to the Antifungal Protein AfpB in the three Mitogen-Activated Protein Kinases (MAPK) pathways of the citrus postharvest pathogen Penicillium digitatum

Gandía

Garrigues

Hernanz-Koers

et al. 2019

Fungal Genetics and Biology

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PdSlt2 Penicillium digitatum mitogen-activated-protein kinase controls sporulation and virulence during citrus fruit infection

Cited by 17 publications

References 53 publications

Transcriptome analysis of fungicide-responsive gene expression profiles in two Penicillium italicum strains with different response to the sterol demethylation inhibitor (DMI) fungicide prochloraz

Transcriptome analysis of fungicide-responsive gene expression profiles in two Penicillium italicum strains with different response to the sterol demethylation inhibitor (DMI) fungicide prochloraz

PdMFS1 Transporter Contributes to Penicilliun digitatum Fungicide Resistance and Fungal Virulence during Citrus Fruit Infection

Differential roles, crosstalk and response to the Antifungal Protein AfpB in the three Mitogen-Activated Protein Kinases (MAPK) pathways of the citrus postharvest pathogen Penicillium digitatum

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