Unravelling the biosynthesis of pyriculol in the rice blast fungus Magnaporthe oryzae

Jacob, Stefan; Grötsch, Thomas; Foster, Andrew J.; Schüffler, Anja; Rieger, Patrick H; Sandjo, Louis P.; Liermann, Johannes C.; Opatz, Till; Thines, Eckhard

doi:10.1099/mic.0.000396

Cited by 45 publications

(58 citation statements)

References 42 publications

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“…Furthermore, two di-terpene cyclase-encoding genes (MGG_01949 and MGG_14722) and three dimethylallyl tryptophane synthase (DMATS)-encoding genes (MGG_06540, MGG_10953, and MGG_12480) were upregulated. MGG_10671, encoding a sesquiterpene synthase, was also upregulated (51)(52)(53). With the exception of OXR1 and CYP1, MoLAEA was not found to alter the expression of genes in the ACE1 cluster (54).…”

Section: Resultsmentioning

confidence: 99%

MoLAEA Regulates Secondary Metabolism in Magnaporthe oryzae

Saha

Ghosh

Roy-Barman

2020

mSphere

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Fungi are rich sources of secondary metabolites of pharmaceutical importance, such as antibiotics, antitumor agents, and immunosuppressants, as well as of harmful toxins. Secondary metabolites play important roles in the development and pathogenesis of fungi. LaeA is a global regulator of secondary metabolism and was originally reported in Aspergillus nidulans; however, its role in secondary metabolism in Magnaporthe oryzae has not yet been reported. Here, we investigated the role of a gene homologous to LAEA (loss of AflR expression) of Aspergillus spp. in Magnaporthe oryzae, named M. oryzae LAEA (MoLAEA). Studies on MoLAEA overexpression and knockdown strains have suggested that this gene acts as a negative regulator of sporulation and melanin synthesis. However, it is not involved in the growth and pathogenesis of M. oryzae. Transcriptomic data indicated that MoLAEA regulated genes involved in secondary metabolism. Interestingly, we observed (for the first time, to our knowledge) that this gene is involved in benzylpenicillin (penicillin G) synthesis in M. oryzae. Overexpression of MoLAEA increased penicillin G production, whereas the silenced strain showed a complete absence of penicillin G compared to its presence in the wild type. We also observed that MoLaeA interacted with MoVeA, a velvet family protein involved in fungal development and secondary metabolism, in the nucleus. This study showed that though MoLAEA may not make any contribution in rice blast fungal pathogenesis, it regulates secondary metabolism in M. oryzae and thus can be further studied for identifying other new uncharacterized metabolites in this fungus. IMPORTANCE M. oryzae causes blast disease, the most serious disease of cultivated rice affecting global rice production. The genome of M. oryzae has been shown to have a number of genes involved in secondary metabolism, but most of them are uncharacterized. In fact, compared to studies of other filamentous fungi, hardly any work has been done on secondary metabolism in M. oryzae. It is shown here (for the first time, to our knowledge) that penicillin G is being synthesized in M. oryzae and that MoLAEA is involved in this process. This is the first step in understanding the penicillin G biosynthesis pathway in M. oryzae. This study also unraveled the details of how MoLaeA works by forming a nuclear complex with MoVeA in M. oryzae, thus indicating functional conservation of such a gene across filamentous fungi. All these findings open up avenues for more relevant investigations on the genetic regulation of secondary metabolism in M. oryzae.

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Section: Resultsmentioning

confidence: 99%

MoLAEA Regulates Secondary Metabolism in Magnaporthe oryzae

Saha

Ghosh

Roy-Barman

2020

mSphere

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“…epipyriculol, epidihydropyriculol, pyriculariol and pyricuol), tenuazonic acid and picolinic acid (PA) were produced by P. oryzae on rice leaves (Kim et al , Tsurushima et al ). The tenuazonic acid, PA and pyriculol are of greater importance for blast symptoms development on rice (Umetsu et al , Yoder , Iwahashi et al , Jacob et al ).…”

Section: Introductionmentioning

confidence: 99%

Picolinic acid spray stimulates the antioxidative metabolism and minimizes impairments on photosynthesis on wheat leaves infected by Pyricularia oryzae

Aucique‐Pérez

Resende

Neto

et al. 2019

Physiologia Plantarum

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Fungal pathogens produce toxins that are important for their pathogenesis and/or aggressiveness towards their hosts. Picolinic acid (PA), a non-host selective toxin, causes lesions on rice leaves resembling those originated from Pyricularia oryzae infection. Considering that non-host selective toxins can be useful for plant diseases control, this study investigated whether the foliar spray with PA on wheat (Triticum aestivum L.) plants, in a non-phytotoxic concentration, could increase their resistance to blast, stimulate the anti-oxidative metabolism, and minimize alterations in photosynthesis. The PA spray at concentrations greater than 0.1 mg ml −1 caused foliar lesions, compromised the photosynthesis and was linked with greater accumulation of hydrogen peroxide (H 2 O 2 ) and superoxide anion radical (O 2 •− ). Fungal mycelial growth, conidia production and germination decreased by PA at 0.3 mg ml −1 . Blast severity was significantly reduced by 59 and 23%, respectively, at 72 and 96 h after inoculation for plants sprayed with PA (0.1 mg ml −1 ) at 24 h before fungal inoculation compared to non-sprayed plants. Reduction on blast symptoms was linked with increases on ascorbate peroxidase (EC 1.superoxide dismutase (EC 1.15.1.1) activities, lower H 2 O 2 and O 2•− accumulation, reduced malondialdehyde production as well as less impairments to the photosynthetic apparatus. A more efficient antioxidative metabolism that rapidly scavenges the reactive oxygen species generated during P. oryzae infection, without dramatically decreasing the photosynthetic performance, was a remarkable effect obtained with PA spray.Abbreviations -A, net CO 2 assimilation rate; APX, ascorbate peroxidase; BS, blast severity; CAT, catalase; C i , internal CO 2 concentration; E, transpiration rate; F m , maximum fluorescence image; F v /F m , variable-to-maximum chlorophyll fluorescence ratio; GPX, glutathione peroxidase; g s , stomatal conductance to water vapor; GST, glutathione-S-transferase; hai, hours after inoculation; H 2 O 2 , hydrogen peroxide; MDA, malondialdehyde; O 2 •− , superoxide anion radical; PA, picolinic acid; POX, peroxidase; q P , coefficient for photochemical quenching; SOD, superoxide dismutase; Y(II), effective photosystem II quantum yield; Y(NO), quantum yield of non-regulated energy dissipation; Y(NPQ), quantum yield of regulated energy dissipation.

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“…The antimelanogenic effect of compound C-9-H was also analyzed against other melanized fungus viz., Magnaporthe oryzae, Aspergillus terreus, and Aspergillus flavus ( Figure 2). The results revealed that only M. oryzae which produces melanin through DHN polyketide pathway, 25 developed white demelanized colonies at 2.34 mM C-9-H concentration, whereas no demelanization was observed in A. terreus and A. flavus ( Figure 2). A. terreus lacks pksP homolog in melanin biosynthesis pathway, 26 whereas A. flavus produces melanin through non-DHN pathway.…”

Section: Resultsmentioning

confidence: 99%

cis-9-Hexadecenal, a Natural Compound Targeting Cell Wall Organization, Critical Growth Factor, and Virulence of Aspergillus fumigatus

et al. 2020

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Aspergillus fumigatus causes several nosocomial pulmonary infections and accounts for high morbidity and mortality rate globally. Among various virulence factors, 1,8-dihydroxynaphthalene-melanin plays an important role in the survival during unfavorable conditions both in vivo and in vitro, masks various molecular patterns associated with A. fumigatus, and protects it from the host immune system. In the present study, we aim to understand the potential of cis-9-hexadecenal as an antimelanogenic compound and its role in modulating other associated virulence factors in A. fumigatus. cis-9-Hexadecenal is a bioactive compound that belongs to C 16 mono-unsaturated fatty-aldehyde groups. Minimum effective concentration of cis-9-hexadecenal affecting A. fumigatus melanin biosynthesis was determined using broth microdilution method. The spectrophotometric analysis revealed reduced melanin content (91%) and hydrophobicity (59%) at 0.293 mM of cis-9-hexadecenal. Cell surface organizational changes using electron microscopy showed altered demelanized smooth A. fumigatus conidial surface without any protrusions after cis-9-hexadecenal treatment. The transcript analysis of polyketide synthase (PKS) pksP/alb1 gene was quantified through qRT-PCR which revealed an upregulated expression. Total proteome profiling conducted through LC-MS-MS showed upregulated PKS enzyme but other downstream proteins involved in the 1,8-dihydroxynaphthalene-melanin biosynthesis pathway were absent. The homology modeling of PKS using Expasy's web server predicted that PKS is stable at varied conditions and is hydrophilic in nature. The Ramachandran plot by PROCHECK confirmed the 3-D structure of PKS to be reliable. Docking analysis using AutoDock-4.2.6 predicted the binding of cis-9-hexadecenal and PKS at Thr-264 and Ser-171 residue via hydrogen bonding at a low binding energy of −4.95 kcal/mol.

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Unravelling the biosynthesis of pyriculol in the rice blast fungus Magnaporthe oryzae

Cited by 45 publications

References 42 publications

MoLAEA Regulates Secondary Metabolism in Magnaporthe oryzae

MoLAEA Regulates Secondary Metabolism in Magnaporthe oryzae

Picolinic acid spray stimulates the antioxidative metabolism and minimizes impairments on photosynthesis on wheat leaves infected by Pyricularia oryzae

cis-9-Hexadecenal, a Natural Compound Targeting Cell Wall Organization, Critical Growth Factor, and Virulence of Aspergillus fumigatus

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