Synergistic Effect of Different Plant Cell Wall–Degrading Enzymes Is Important for Virulence of <i>Fusarium graminearum</i>

Paccanaro, Maria Chiara; Sella, Luca; Castiglioni, Carla; Giacomello, Francesca; Martínez-Rocha, Ana Lilia; D’Ovidio, R.; Schäfer, Wilhelm; Favaron, Francesco

doi:10.1094/mpmi-07-17-0179-r

Cited by 55 publications

(28 citation statements)

References 62 publications

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“…These results suggested that the STK-12-IGO-1 pathway is highly conserved between yeast and filamentous fungi. Like cellulolytic fungi, plant/insect pathogenic fungi also secrete hydrolytic enzymes that degrade components of the host epidermis during the infection process [59]. Thus, further analyses of the functions of STK-12 orthologs in plant/insect pathogenic fungi may aid in the development of novel anti-fungal strategies and more potent strains for insect biocontrol.…”

Section: Discussionmentioning

confidence: 99%

STK-12 acts as a transcriptional brake to control the expression of cellulase-encoding genes in Neurospora crassa

Lin

Wang

et al. 2019

PLoS Genet

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Cellulolytic fungi have evolved a complex regulatory network to maintain the precise balance of nutrients required for growth and hydrolytic enzyme production. When fungi are exposed to cellulose, the transcript levels of cellulase genes rapidly increase and then decline. However, the mechanisms underlying this bell-shaped expression pattern are unclear. We systematically screened a protein kinase deletion set in the filamentous fungus Neurospora crassa to search for mutants exhibiting aberrant expression patterns of cellulase genes. We observed that the loss of stk-12 (NCU07378) caused a dramatic increase in cellulase production and an extended period of high transcript abundance of major cellulase genes. These results suggested that stk-12 plays a critical role as a brake to turn down the transcription of cellulase genes to repress the overexpression of hydrolytic enzymes and prevent energy wastage. Transcriptional profiling analyses revealed that cellulase gene expression levels were maintained at high levels for 56 h in the Δstk-12 mutant, compared to only 8 h in the wild-type (WT) strain. After growth on cellulose for 3 days, the transcript levels of cellulase genes in the Δstk-12 mutant were 3.3-fold over WT, and clr-2 (encoding a transcriptional activator) was up-regulated in Δstk-12 while res-1 and rca-1 (encoding two cellulase repressors) were down-regulated. Consequently, total cellulase production in the Δstk-12 mutant was 7-fold higher than in the WT. These results strongly suggest that stk-12 deletion results in dysregulation of the cellulase expression machinery. Further analyses showed that STK-12 directly targets IGO-1 to regulate cellulase production. The TORC1 pathway promoted cellulase production, at least partly, by inhibiting STK-12 function, and STK-12 and CRE-1 functioned in parallel pathways to repress cellulase gene expression. Our results clarify how cellulase genes are repressed at the transcriptional level during cellulose induction, and highlight a new strategy to improve industrial fungal strains.

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Section: Discussionmentioning

confidence: 99%

STK-12 acts as a transcriptional brake to control the expression of cellulase-encoding genes in Neurospora crassa

Lin

Wang

et al. 2019

PLoS Genet

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“…Wheat plants ( Triticum aestivum cv. Nandu and Amaretto) were grown as reported in Paccanaro et al (2017). Inoculation experiments were performed on wheat spikes at anthesis according to Woriedh et al (2011).…”

Section: Methodsmentioning

confidence: 99%

Different Hydrophobins of Fusarium graminearum Are Involved in Hyphal Growth, Attachment, Water-Air Interface Penetration and Plant Infection

et al. 2019

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Hydrophobins (HPs) are small secreted fungal proteins possibly involved in several processes such as formation of fungal aerial structures, attachment to hydrophobic surfaces, interaction with the environment and protection against the host defense system. The genome of the necrotrophic plant pathogen Fusarium graminearum contains five genes encoding for HPs (FgHyd1-5). Single and triple FgHyd mutants were produced and characterized. A reduced growth was observed when the Δ Fghyd2 and the three triple mutants including the deletion of FgHyd2 were grown in complete or minimal medium. Surprisingly, the growth of these mutants was similar to wild-type when grown under ionic, osmotic or oxidative stress conditions. All the mutant strains confirmed the ability to develop conidia and perithecia, suggesting that the FgHyds are not involved in normal development of asexual and sexual structures. A reduction in the ability of hyphae to penetrate through the water-air interface was observed for the single mutants Δ Fghyd2 and Δ Fghyd3 as well as for the triple mutants including the deletion of FgHyd2 and FgHyd3. Besides, Δ Fghyd3 and the triple mutant Δ Fghyd234 were also affected in the attachment to hydrophobic surface. Indeed, wheat infection experiments showed a reduction of symptomatic spikelets for Δ Fghyd2 and Δ Fghyd3 and the triple mutants only when spray inoculation was performed. This result could be ascribed to the affected ability of mutants deleted of FgHyd2 and FgHyd3 to penetrate through the water-air interface and to attach to hydrophobic surfaces such as the spike tissue. This hypothesis is strengthened by a histological analysis, performed by fluorescence microscopy, showing no defects in the morphology of infection structures produced by mutant strains. Interestingly, triple hydrophobin mutants were significantly more inhibited than wild-type by the treatment with a systemic triazole fungicide, while no defects at the cell wall level were observed.

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“…Heterotrophic fungi, for example, usually gain nutrients by secreting extracellular hydrolase. The hydrolases secreted by pathogenic fungi can damage plant cell wall by breaking down polysaccharides, thereby facilitating infection [ 20 ]. Decreased carbohydrate metabolism reduces the production of acetyl-CoA.…”

Section: Discussionmentioning

confidence: 99%

Transcriptome analysis of Valsa mali reveals its response mechanism to the biocontrol actinomycete Saccharothrix yanglingensis Hhs.015

Cong

Fan

et al. 2018

BMC Microbiol

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BackgroundApple canker is a devastating branch disease caused by Valsa mali (Vm). The endophytic actinomycete Saccharothrix yanglingensis Hhs.015 (Sy Hhs.015) can effectively inhibit the growth of Vm. To reveal the mechanism, by which Vm respond to Sy Hhs.015, the transcriptome of Vm was analyzed using RNA-seq technology.ResultsCompared with normal growing Vm in the control group, 1476 genes were significantly differentially expressed in the Sy Hhs.015’s treatment group, of which 851 genes were up-regulated and 625 genes were down-regulated. Combined gene function and pathway analysis of differentially expressed genes (DEGs) revealed that Sy Hhs.015 affected the carbohydrate metabolic pathway, which is utilized by Vm for energy production. Approximately 82% of the glycoside hydrolase genes were down-regulated, including three pectinase genes (PGs), which are key pathogenic factors. The cell wall structure of Vm was disrupted by Sy Hhs.015 and cell wall-related genes were found to be down-regulated. Of the peroxisome associated genes, those encoding catalase (CAT) and superoxide dismutase (SOD) which scavenge reactive oxygen species (ROS), as well as those encoding AMACR and ACAA1 which are related to the β-oxidation of fatty acids, were down-regulated. MS and ICL, key genes in glyoxylate cycle, were also down-regulated. In response to the stress of Sy Hhs.015 exposure, Vm increased amino acid metabolism to synthesize the required nitrogenous compounds, while alpha-keto acids, which involved in the TCA cycle, could be used to produce energy by deamination or transamination. Retinol dehydrogenase, associated with cell wall dextran synthesis, and sterol 24-C-methyltransferase, related to cell membrane ergosterol synthesis, were up-regulated. The genes encoding glutathione S-transferase, (GST), which has antioxidant activity and ABC transporters which have an efflux function, were also up-regulated.ConclusionThese results show that the response of Vm to Sy Hhs.015 exposure is a complicated and highly regulated process, and provide a theoretical basis for both clarifying the biocontrol mechanism of Sy Hhs.015 and the response of Vm to stress.Electronic supplementary materialThe online version of this article (10.1186/s12866-018-1225-5) contains supplementary material, which is available to authorized users.

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Synergistic Effect of Different Plant Cell Wall–Degrading Enzymes Is Important for Virulence of Fusarium graminearum

Cited by 55 publications

References 62 publications

STK-12 acts as a transcriptional brake to control the expression of cellulase-encoding genes in Neurospora crassa

STK-12 acts as a transcriptional brake to control the expression of cellulase-encoding genes in Neurospora crassa

Different Hydrophobins of Fusarium graminearum Are Involved in Hyphal Growth, Attachment, Water-Air Interface Penetration and Plant Infection

Transcriptome analysis of Valsa mali reveals its response mechanism to the biocontrol actinomycete Saccharothrix yanglingensis Hhs.015

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