The zinc finger protein StMR1 affects the pathogenicity and melanin synthesis of <i>Setosphaeria turcica</i> and directly regulates the expression of DHN melanin synthesis pathway genes

Zhang, Zexue; Jia, Hui; Liu, Ning; Li, Haixiao; Meng, Qingjiang; Wu, Nan; Cao, Zhimian; Dong, Jingao

doi:10.1111/mmi.14786

Cited by 10 publications

(7 citation statements)

References 38 publications

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“…The Zn 2 Cys 6 zinc cluster proteins are a family of transcription factors found exclusively in fungi [ 33 ]. They function as transcriptional regulators and are involved in a wide variety of biological processes, including asexual and sexual development, secondary metabolite biosynthesis, carbon and nitrogen metabolism, stress responses, pleiotropic drug resistance, and fungal pathogenesis [ 34 , 35 , 36 , 37 , 38 ]. However, the functions of Zn 2 Cys 6 TFs in different fungi are diverse.…”

Section: Discussionmentioning

confidence: 99%

Cmcrf1, a Putative Zn2Cys6 Fungal Transcription Factor, Is Involved in Conidiation, Carotenoid Production, and Fruiting Body Development in Cordyceps militaris

Zhang

Lan

et al. 2022

Biology

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Cordyceps militaris is a high-value medicinal and edible fungus that produces many bioactive compounds, including carotenoid, and thus, improving the carotenoid productivity of C. militaris will increase its commercial value. However, little is known about the genetic regulatory mechanism of carotenoid biosynthesis in C. militaris. To further understanding the regulatory mechanism of carotenoid biosynthesis, we performed a large-scale screen of T-DNA insertional mutant library and identified a defective mutant, denoted T111, whose colonies did not change color from white to yellow upon exposure to light. Mutation analysis confirmed that a single T-DNA insertion occurred in the gene encoding a 695-amino-acid putative fungal-specific transcription factor with a predicted Zn2Cys6 binuclear cluster DNA-binding domain found uniquely in fungi. Targeted deletion of this gene, denoted C. militaris carotenogenesis regulatory factor 1 (Cmcrf1), generated the ΔCmcrf1 mutant that exhibited drastically reduced carotenoid biosynthesis and failed to generate fruiting bodies. In addition, the ΔCmcrf1 mutant showed significantly increased conidiation and increased hypersensitivity to cell-wall-perturbing agents compared with the wild-type strain. However, the Cmcrf1 gene did not have an impact on the mycelia growth of C. militaris. These results show that Cmcrf1 is involved in carotenoid biosynthesis and is required for conidiation and fruiting body formation in C. militaris.

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Section: Discussionmentioning

confidence: 99%

Cmcrf1, a Putative Zn2Cys6 Fungal Transcription Factor, Is Involved in Conidiation, Carotenoid Production, and Fruiting Body Development in Cordyceps militaris

Zhang

Lan

et al. 2022

Biology

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“…For the RNAseq analysis, differentially expressed genes (DEGs, in Additional file 1 : Table S4) from three biological replicates of the mutant and WT were identified by Deseq R with a false discovery rate of 1% (fold-change ≥ 2.0, P < 0.01). The DEGs were analyzed using Gene Ontology (GO) analysis in the GO-seq package and Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis [ 96 , 97 ] using the KEGG Orthology (KO)-Based Annotation System (KOBAS) to explore their biological roles based on the classification system including plasma membrane, cell periphery, regulation of cellular process, cellular component organization, regulation of biological process, oxidation-reduction process, oxidoreductase activity, and melanin biosynthesis. The threshold for the significant enrichment of GO terms was P <0.05.…”

Section: Methodsmentioning

confidence: 99%

A polyketide synthase from Verticillium dahliae modulates melanin biosynthesis and hyphal growth to promote virulence

Wang

Zhang

et al. 2022

BMC Biol

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Background During the disease cycle, plant pathogenic fungi exhibit a morphological transition between hyphal growth (the phase of active infection) and the production of long-term survival structures that remain dormant during “overwintering.” Verticillium dahliae is a major plant pathogen that produces heavily melanized microsclerotia (MS) that survive in the soil for 14 or more years. These MS are multicellular structures produced during the necrotrophic phase of the disease cycle. Polyketide synthases (PKSs) are responsible for catalyzing production of many secondary metabolites including melanin. While MS contribute to long-term survival, hyphal growth is key for infection and virulence, but the signaling mechanisms by which the pathogen maintains hyphal growth are unclear. Results We analyzed the VdPKSs that contain at least one conserved domain potentially involved in secondary metabolism (SM), and screened the effect of VdPKS deletions in the virulent strain AT13. Among the five VdPKSs whose deletion affected virulence on cotton, we found that VdPKS9 acted epistatically to the VdPKS1-associated melanin pathway to promote hyphal growth. The decreased hyphal growth in VdPKS9 mutants was accompanied by the up-regulation of melanin biosynthesis and MS formation. Overexpression of VdPKS9 transformed melanized hyphal-type (MH-type) into the albinistic hyaline hyphal-type (AH-type), and VdPKS9 was upregulated in the AH-type population, which also exhibited higher virulence than the MH-type. Conclusions We show that VdPKS9 is a powerful negative regulator of both melanin biosynthesis and MS formation in V. dahliae. These findings provide insight into the mechanism of how plant pathogens promote their virulence by the maintenance of vegetative hyphal growth during infection and colonization of plant hosts, and may provide novel targets for the control of melanin-producing filamentous fungi.

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“…Cmr1 is characterized by the presence of two types of DNA binding motifs, two Cys 2 His 2 zinc finger motifs and one GAL4-like Zn(II) 2 Cys 6 binuclear cluster DNA-binding motif. Until now, Cmr1 homologs that have been identified and confirmed their roles as the regulators in the DHN-melanin biosynthesis pathway of several plant fungal pathogens, include Pig1 in Magnaporthe grisea (Tsuji et al 2000 ), Cmr1 in Cochliobolus heterostrophus (Eliahu et al 2007 ), Bmr1 in Bipolaris oryzae (Kihara et al 2008 ), Amr1 in Alternaria brassicicola (Cho et al 2012 ), CmrA in Alternaria alternata (Fetzner et al 2014 ), BcSMR1 in Botrytis cinerea (Zhou et al 2017 ), Zmr1 in Zymoseptoria tritici (Krishnan et al 2018 ), CgCmr1 in Colletotrichum gloeosporioides (Wang et al 2021a , b ), and StMR1 in Setosphaeria turcica (Zhang et al 2022 ). Apart from a role in controlling DHN-melanin biosynthesis, Cmr1 homologs also affect the morphology and pathogenicity of some phytopathogenic fungi, suggesting the functional diversification of Cmr1 homologs.…”

Section: Introductionmentioning

confidence: 99%

“…Currently, two Cmr1 homologs including Amr1 in A. brassicicola (Cho et al 2012 ) and CmrA in A. alternata (Fetzner et al 2014 ) have been identified and characterized in Alternaria . The function of Cmr1 homologs in regulating the DHN-melanin biosynthesis is highly conserved in A. brassicicola , A. alternata , and other fungi described above (Tsuji et al 2000 ; Eliahu et al 2007 ; Kihara et al 2008 ; Cho et al 2012 ; Fetzner et al 2014 ; Zhou et al 2017 ; Krishnan et al 2018 ; Wang et al 2021a , b ; Zhang et al 2022 ). Interestingly, based on the amino acid sequence comparison between Amr1 and CmrA, there was one amino acid insertion at site 934 in Amr1 and 31 polymorphic sites (data not shown), suggesting that the amino acid sequences have diverged in Amr1 and CmrA.…”

Section: Introductionmentioning

confidence: 99%

Positive selection and functional diversification of transcription factor Cmr1 homologs in Alternaria

Qiu,

Liu

2024

Appl Microbiol Biotechnol

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Transcription factor Cmr1 (Colletotrichum melanin regulation 1) and its homologs in several plant fungal pathogens are the regulators of the 1,8-dihydroxynaphthalene (DHN)-melanin biosynthesis pathway and have evolved functional diversification in morphology and pathogenicity. The fungal genus Alternaria comprises the group of “black fungi” that are rich in DHN-melanin in the primary cell wall and septa of the conidia. Some Alternaria species cause many economically important plant diseases worldwide. However, the evolution and function of Cmr1 homologs in Alternaria remain poorly understood. Here, we identified a total of forty-two Cmr1 homologs from forty-two Alternaria spp. and all contained one additional diverse fungal specific transcription factor motif. Phylogenetic analysis indicated the division of these homologs into five major clades and three branches. Dated phylogeny showed the A and D clades diverged latest and earliest, respectively. Molecular evolutionary analyses revealed that three amino acid sites of Cmr1 homologs in Alternaria were the targets of positive selection. Asmr1, the homolog of Cmr1 in the potato early blight pathogen, Alternaria solani was amplified and displayed the sequence conservation at the amino acid level in different A. solani isolates. Asmr1 was further confirmed to have the transcriptional activation activity and was upregulated during the early stage of potato infection. Deletion of asmr1 led to the decreased melanin content and pathogenicity, deformed conidial morphology, and responses to cell wall and fungicide stresses in A. solani. These results suggest positive selection and functional divergence have played a role in the evolution of Cmr1 homologs in Alternaria. Key points • Cmr1 homologs were under positive selection in Alternaria species • Asmr1 is a functional transcription factor, involved in spore development, melanin biosynthesis, pathogenicity, and responses to cell wall and fungicide stresses in A. solani • Cmr1 might be used as a potential taxonomic marker of the genus Alternaria

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The zinc finger protein StMR1 affects the pathogenicity and melanin synthesis of Setosphaeria turcica and directly regulates the expression of DHN melanin synthesis pathway genes

Cited by 10 publications

References 38 publications

Cmcrf1, a Putative Zn2Cys6 Fungal Transcription Factor, Is Involved in Conidiation, Carotenoid Production, and Fruiting Body Development in Cordyceps militaris

Cmcrf1, a Putative Zn2Cys6 Fungal Transcription Factor, Is Involved in Conidiation, Carotenoid Production, and Fruiting Body Development in Cordyceps militaris

A polyketide synthase from Verticillium dahliae modulates melanin biosynthesis and hyphal growth to promote virulence

Positive selection and functional diversification of transcription factor Cmr1 homologs in Alternaria

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