Comparative functional analysis of a new CDR1-like ABC transporter gene in multidrug resistance and virulence between Magnaporthe oryzae and Trichophyton mentagrophytes

Abstract Fungi are notorious for causing diseases in plants and domestic animals. ABC transporters play pivotal roles in multidrug resistance in fungi, with some ABC proteins indispensable for the pathogenicity of plant fungal pathogens. However, the roles of ABC proteins in animal pathogenic fungi,...

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Main Authors: Jing Wang, Chenwen Xiao, Shuang Liang, Muhammad Noman, Yingying Cai, Zhen Zhang, Xueming Zhu, Rongyao Chai, Haiping Qiu, Zhongna Hao, Yanli Wang, Jiaoyu Wang, Guolian Bao, Guochang Sun, Fucheng Lin
Format: Article
Language:English
Published: BMC 2025-02-01
Series:Cell Communication and Signaling
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Online Access:https://doi.org/10.1186/s12964-024-02022-w
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author Jing Wang
Chenwen Xiao
Shuang Liang
Muhammad Noman
Yingying Cai
Zhen Zhang
Xueming Zhu
Rongyao Chai
Haiping Qiu
Zhongna Hao
Yanli Wang
Jiaoyu Wang
Guolian Bao
Guochang Sun
Fucheng Lin
author_facet Jing Wang
Chenwen Xiao
Shuang Liang
Muhammad Noman
Yingying Cai
Zhen Zhang
Xueming Zhu
Rongyao Chai
Haiping Qiu
Zhongna Hao
Yanli Wang
Jiaoyu Wang
Guolian Bao
Guochang Sun
Fucheng Lin
author_sort Jing Wang
collection DOAJ
description Abstract Fungi are notorious for causing diseases in plants and domestic animals. ABC transporters play pivotal roles in multidrug resistance in fungi, with some ABC proteins indispensable for the pathogenicity of plant fungal pathogens. However, the roles of ABC proteins in animal pathogenic fungi, and the functional connections between ABC homologues in plant and animal pathogenic fungi are largely obscure. Here, we identified a new ABCG-1 gene, MoCDR1, in rice-blast fungus Magnaporthe oryzae. MoCDR1 disruption caused hypersensitivity to multidrugs, and impaired conidiation, appressorium formation, and pathogenicity. Subsequently, we systematically retrieved ABC proteins in animal pathogenic fungus Trichophyton mentagrophytes and identified TmCdr1, a homologue to MoCdr1. TmCDR1 effectively rescued the drug sensitivity and virulence of ΔMocdr1 and mediated the drug resistance and animal skin infection in T. mentagrophytes. Moreover, MoCDR1 also rescued the defects in drug sensitivity and virulence of ΔTmcdr1. MoCdr1 and TmCdr1 are conserved in structures and functions, and both involved in drug resistance and pathogenicity by analogously regulating gene expression levels related to transporter activity, MAPK signaling pathway, and metabolic processes. Altogether, our results represent the first comprehensive characterization of ABC genes in T. mentagrophytes, establishing a functional correlation between homologous ABC genes in plant and animal pathogenic fungi.
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spelling doaj-art-7e68db33b00b41ba99ba1e68b55e5eca2025-02-09T12:47:18ZengBMCCell Communication and Signaling1478-811X2025-02-0123112210.1186/s12964-024-02022-wComparative functional analysis of a new CDR1-like ABC transporter gene in multidrug resistance and virulence between Magnaporthe oryzae and Trichophyton mentagrophytesJing Wang0Chenwen Xiao1Shuang Liang2Muhammad Noman3Yingying Cai4Zhen Zhang5Xueming Zhu6Rongyao Chai7Haiping Qiu8Zhongna Hao9Yanli Wang10Jiaoyu Wang11Guolian Bao12Guochang Sun13Fucheng Lin14State Key Laboratory for Quality and Safety of Agro-Products Key Laboratory of Agricultural Microbiome of Zhejiang Province, Key Laboratory of Biotechnology in Plant Protection of MARA, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural SciencesState Key Laboratory for Quality and Safety of Agro-Products Key Laboratory of Agricultural Microbiome of Zhejiang Province, Key Laboratory of Biotechnology in Plant Protection of MARA, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural SciencesState Key Laboratory for Quality and Safety of Agro-Products Key Laboratory of Agricultural Microbiome of Zhejiang Province, Key Laboratory of Biotechnology in Plant Protection of MARA, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural SciencesState Key Laboratory for Quality and Safety of Agro-Products Key Laboratory of Agricultural Microbiome of Zhejiang Province, Key Laboratory of Biotechnology in Plant Protection of MARA, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural SciencesState Key Laboratory for Quality and Safety of Agro-Products Key Laboratory of Agricultural Microbiome of Zhejiang Province, Key Laboratory of Biotechnology in Plant Protection of MARA, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural SciencesState Key Laboratory for Quality and Safety of Agro-Products Key Laboratory of Agricultural Microbiome of Zhejiang Province, Key Laboratory of Biotechnology in Plant Protection of MARA, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural SciencesState Key Laboratory for Quality and Safety of Agro-Products Key Laboratory of Agricultural Microbiome of Zhejiang Province, Key Laboratory of Biotechnology in Plant Protection of MARA, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural SciencesState Key Laboratory for Quality and Safety of Agro-Products Key Laboratory of Agricultural Microbiome of Zhejiang Province, Key Laboratory of Biotechnology in Plant Protection of MARA, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural SciencesState Key Laboratory for Quality and Safety of Agro-Products Key Laboratory of Agricultural Microbiome of Zhejiang Province, Key Laboratory of Biotechnology in Plant Protection of MARA, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural SciencesState Key Laboratory for Quality and Safety of Agro-Products Key Laboratory of Agricultural Microbiome of Zhejiang Province, Key Laboratory of Biotechnology in Plant Protection of MARA, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural SciencesState Key Laboratory for Quality and Safety of Agro-Products Key Laboratory of Agricultural Microbiome of Zhejiang Province, Key Laboratory of Biotechnology in Plant Protection of MARA, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural SciencesState Key Laboratory for Quality and Safety of Agro-Products Key Laboratory of Agricultural Microbiome of Zhejiang Province, Key Laboratory of Biotechnology in Plant Protection of MARA, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural SciencesInstitute of Animal Husbandry and Veterinary Science, Zhejiang Academy of Agricultural SciencesState Key Laboratory for Quality and Safety of Agro-Products Key Laboratory of Agricultural Microbiome of Zhejiang Province, Key Laboratory of Biotechnology in Plant Protection of MARA, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural SciencesState Key Laboratory for Quality and Safety of Agro-Products Key Laboratory of Agricultural Microbiome of Zhejiang Province, Key Laboratory of Biotechnology in Plant Protection of MARA, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural SciencesAbstract Fungi are notorious for causing diseases in plants and domestic animals. ABC transporters play pivotal roles in multidrug resistance in fungi, with some ABC proteins indispensable for the pathogenicity of plant fungal pathogens. However, the roles of ABC proteins in animal pathogenic fungi, and the functional connections between ABC homologues in plant and animal pathogenic fungi are largely obscure. Here, we identified a new ABCG-1 gene, MoCDR1, in rice-blast fungus Magnaporthe oryzae. MoCDR1 disruption caused hypersensitivity to multidrugs, and impaired conidiation, appressorium formation, and pathogenicity. Subsequently, we systematically retrieved ABC proteins in animal pathogenic fungus Trichophyton mentagrophytes and identified TmCdr1, a homologue to MoCdr1. TmCDR1 effectively rescued the drug sensitivity and virulence of ΔMocdr1 and mediated the drug resistance and animal skin infection in T. mentagrophytes. Moreover, MoCDR1 also rescued the defects in drug sensitivity and virulence of ΔTmcdr1. MoCdr1 and TmCdr1 are conserved in structures and functions, and both involved in drug resistance and pathogenicity by analogously regulating gene expression levels related to transporter activity, MAPK signaling pathway, and metabolic processes. Altogether, our results represent the first comprehensive characterization of ABC genes in T. mentagrophytes, establishing a functional correlation between homologous ABC genes in plant and animal pathogenic fungi.https://doi.org/10.1186/s12964-024-02022-wMoCDR1TmCDR1ABC transportersMagnaporthe oryzaeTrichophyton mentagrophytes
spellingShingle Jing Wang
Chenwen Xiao
Shuang Liang
Muhammad Noman
Yingying Cai
Zhen Zhang
Xueming Zhu
Rongyao Chai
Haiping Qiu
Zhongna Hao
Yanli Wang
Jiaoyu Wang
Guolian Bao
Guochang Sun
Fucheng Lin
Comparative functional analysis of a new CDR1-like ABC transporter gene in multidrug resistance and virulence between Magnaporthe oryzae and Trichophyton mentagrophytes
Cell Communication and Signaling
MoCDR1
TmCDR1
ABC transporters
Magnaporthe oryzae
Trichophyton mentagrophytes
title Comparative functional analysis of a new CDR1-like ABC transporter gene in multidrug resistance and virulence between Magnaporthe oryzae and Trichophyton mentagrophytes
title_full Comparative functional analysis of a new CDR1-like ABC transporter gene in multidrug resistance and virulence between Magnaporthe oryzae and Trichophyton mentagrophytes
title_fullStr Comparative functional analysis of a new CDR1-like ABC transporter gene in multidrug resistance and virulence between Magnaporthe oryzae and Trichophyton mentagrophytes
title_full_unstemmed Comparative functional analysis of a new CDR1-like ABC transporter gene in multidrug resistance and virulence between Magnaporthe oryzae and Trichophyton mentagrophytes
title_short Comparative functional analysis of a new CDR1-like ABC transporter gene in multidrug resistance and virulence between Magnaporthe oryzae and Trichophyton mentagrophytes
title_sort comparative functional analysis of a new cdr1 like abc transporter gene in multidrug resistance and virulence between magnaporthe oryzae and trichophyton mentagrophytes
topic MoCDR1
TmCDR1
ABC transporters
Magnaporthe oryzae
Trichophyton mentagrophytes
url https://doi.org/10.1186/s12964-024-02022-w
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