Production of a fungal furocoumarin by a polyketide synthase gene cluster confers the chemo‐resistance of <i>Neurospora crassa</i> to the predation by fungivorous arthropods

Zhao, Yuliang; Ding, Jingjin; Yuan, Weiping; Huang, Jinjin; Huang, Wenxiu; Wang, Yan; Zheng, Wenhua

doi:10.1111/1462-2920.13791

Cited by 20 publications

(19 citation statements)

References 36 publications

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“…Fungi are microorganisms that produce abundant secondary metabolites (SM) (30). These secondary metabolites have been associated with communication (31, 32), development (33–35), the injury response (15, 16), and recently, a chemical response against predators (7, 11, 36–38). Metabolic fingerprinting of T.…”

Section: Discussionmentioning

confidence: 99%

Trichoderma atroviride from Predator to Prey: Role of the Mitogen-Activated Protein Kinase Tmk3 in Fungal Chemical Defense against Fungivory by Drosophila melanogaster Larvae

Atriztán-Hernández

Moreno-Pedraza

Winkler

et al. 2019

Appl Environ Microbiol

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The response to injury represents an important strategy for animals and plants to survive mechanical damage and predation. Plants respond to injury by activating a defense response that includes the production of an important variety of compounds that help them withstand predator attack and recover from mechanical injury (MI). Similarly, the filamentous fungusTrichoderma atrovirideresponds to MI by strongly modifying its transcriptional profile and producing asexual reproduction structures (conidia). Here, we analyzed whether the response to MI inT. atrovirideis related to a possible predator defense mechanism from a metabolic perspective. We found that the production of specific groups of secondary metabolites increases in response to MI but is reduced after fungivory byDrosophila melanogasterlarvae. We further show that fungivory results in repression of the expression of genes putatively involved in the regulation of secondary metabolite production inT. atroviride. Activation of secondary metabolite production appears to depend on the mitogen-activated protein kinase (MAPK) Tmk3. Interestingly,D. melanogasterlarvae preferred to feed on atmk3gene replacement mutant rather than on the wild-type strain. Consumption of the mutant strain, however, resulted in increased larval mortality.IMPORTANCEFungi, like other organisms, have natural predators, including fungivorous nematodes and arthropods that use them as an important food source. Thus, they require mechanisms to detect and respond to injury.Trichoderma atrovirideresponds to mycelial injury by rapidly regenerating its hyphae and developing asexual reproduction structures. Whether this injury response is associated with attack by fungivorous insects is unknown. Therefore, determining the possible conservation of a defense mechanism to predation inT. atrovirideand plants and elucidating the mechanisms involved in the establishment of this response is of major interest. Here, we describe the chemical response ofT. atrovirideto mechanical injury and fungivory and the role of a MAPK pathway in the regulation of this response.

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Section: Discussionmentioning

confidence: 99%

Trichoderma atroviride from Predator to Prey: Role of the Mitogen-Activated Protein Kinase Tmk3 in Fungal Chemical Defense against Fungivory by Drosophila melanogaster Larvae

Atriztán-Hernández

Moreno-Pedraza

Winkler

et al. 2019

Appl Environ Microbiol

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“…In addition to the 1,8-dihydroxynaphthalene (DHN) melanin spore metabolites, several BGCs encode pigments or toxic metabolites that provide protection for fungal sexual structures from environmental extremes or insect predation. Fusarubins are required for pigmentation of the perithecia in Fusarium species 104 , the perithecial toxin furocoumarin (neurosporin A) deters fungivore feeding on Neurospora crassa sexual stage 105 and deletion of a PKS in the fungus Sordaria macrospora inhibits perithecial maturation, whereas its overexpression resulted in malformed fruiting bodies 106 (FIG. 3d).…”

Section: Functions Of Secondary Metabolitesmentioning

confidence: 99%

Fungal secondary metabolism: regulation, function and drug discovery

2018

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One of the exciting movements in microbial sciences has been a refocusing and revitalization of efforts to mine the fungal secondary metabolome. The magnitude of biosynthetic gene clusters (BGCs) in a single filamentous fungal genome combined with the historic number of sequenced genomes suggests that the secondary metabolite wealth of filamentous fungi is largely untapped. Mining algorithms and scalable expression platforms have greatly expanded access to the chemical repertoire of fungal-derived secondary metabolites. In this Review, I discuss new insights into the transcriptional and epigenetic regulation of BGCs and the ecological roles of fungal secondary metabolites in warfare, defence and development. I also explore avenues for the identification of new fungal metabolites and the challenges in harvesting fungal-derived secondary metabolites. Fungi have a long and intimate connection with humankind, particularly at the chemical level. The realization that fungi were the source of both harmful and beneficial compounds was brought to light by the aflatoxin poisoning event Turkey X disease in the 1960s 1 and the discovery of the first broad-spectrum antibiotic, penicillin, considered the 'wonder drug' of World War II 2. These bioactive molecules, termed secondary metabolites (also known as natural products), are produced by specific fungal taxa, predominately by filamentous fungi that belong to the Pezizomycotina Ascomycete class, and several Basidiomycete classes (for example, Agaricomycetes and Exobasidiomycetes), as well as by unexpected taxa such as Kluyveromyces lactis, in which the pulcherrimin gene cluster was recently discovered 3. Secondary metabolites are derived from central metabolic pathways and primary metabolite pools, with acyl-CoAs being the critical initial building blocks that feed into the synthesis of polyketide (for example, aflatoxin) and terpene (for example, carotene) secondary metabolites and amino acids being used for the synthesis of non-ribosomal peptide secondary metabolites (for example, penicillin) (FIG. 1a). In contrast to genes that are required for the synthesis of a primary metabolite that are dispersed throughout the fungal Competing interests There is no competing interest. Publisher's note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Reviewer information Nature Reviews Microbiology thanks M. Andersen, J. Cary, D. Hoffmeister and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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“…The sexual fruiting body of fungi was constructed by tightly interwoven melanincontained hyphae (Engh et al 2007). Similar to conidia, the unique structure of pseudothecia also confers fungi the capacity to survive in harsh environment (Lambou et al 2008;Zhao et al 2017). Thus, the involvements of melanin in the construction of conidia and pseudothecia endow the resistance of fungi against environmental insults and the effective infection and transmission (Pal et al 2014).…”

Section: Introductionmentioning

confidence: 99%

Regulatory Effects of Nitric Oxide on Reproduction and Melanin Biosynthesis in Onion Pathogenic Fungus Stemphylium Eturmiunum

Zhao

Yuan

Sun

et al. 2020

Preprint

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The formation of propagules (conidia and ascospores) is the critical stage for the transmission of the pathogenic fungus Stemphylium eturmiunum. However, how the development of these propagules is regulated remains to be fully understood. Here, we show that nitric oxide (NO) is necessary for the formation of conidia and pseudothecia in S. eturmiunum. Application of NO scavenger carboxy-CPTIO (cPTIO) or soluble guanylate cyclase (sGC) inhibitor NS2028 abolishes the formation of conidia and pseudothecia. In the culture of S. eturmiunum, supplement of NO-releasing compound sodium nitroprusside (SNP) results in an increased formation of conidia at 0.2 mmol/L, and pseudothecia at 2 mmol/L. SNP supplement also triggered increased biosynthesis of melanin, which can be inhibited partially upon the addition of either arbutin or tricyclazole, the specific inhibitors for 3,4-dihydroxyphenylalanine (DOPA) and dihydroxynaphthalene (DHN) synthetic pathway, respectively. Intriguingly, enhanced melanin biosynthesis triggered an increased formation of propagules; while its inhibition impaired their formation. The SNP-induced increment in the formation of propagules can be also compromised upon supplement of cPTIO or NS-2028. RT-PCR analysis showed that SNP at 0.2 mmol/L promoted transcription of the genes encoding the conidiation co-regulators brlA, abA, and wetA, and inhibited at 2 mmol/L. In contrast, application of SNP at 2 mmol/L increased transcription of the genes encoding mat1, and mat2, the genes related to sexual reproduction, and the transcription of two DNH melanin synthetic genes pks1 and pks2, and the key gene tyr for DOPA melanin biosynthesis. However, the increased transcription of these genes is down-regulated or blocked upon supplement of cPTIO or NS-2028. Thus, NO regulates asexual and sexual development, as well as melanin synthesis in S. eturmiunum possibly through NO-sGC-GMP signaling pathway.

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Production of a fungal furocoumarin by a polyketide synthase gene cluster confers the chemo‐resistance of Neurospora crassa to the predation by fungivorous arthropods

Cited by 20 publications

References 36 publications

Trichoderma atroviride from Predator to Prey: Role of the Mitogen-Activated Protein Kinase Tmk3 in Fungal Chemical Defense against Fungivory by Drosophila melanogaster Larvae

Trichoderma atroviride from Predator to Prey: Role of the Mitogen-Activated Protein Kinase Tmk3 in Fungal Chemical Defense against Fungivory by Drosophila melanogaster Larvae

Fungal secondary metabolism: regulation, function and drug discovery

Regulatory Effects of Nitric Oxide on Reproduction and Melanin Biosynthesis in Onion Pathogenic Fungus Stemphylium Eturmiunum

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