ApWD40a, a Member of the WD40-Repeat Protein Family, Is Crucial for Fungal Development, Toxin Synthesis, and Pathogenicity in the Ginseng Alternaria Leaf Blight Fungus <i>Alternaria panax</i>

<i>Alternaria panax</i>, the primary pathogen that causes ginseng Alternaria leaf blight disease, can lead to a 20–30% reduction in ginseng yield. WD40 repeat-containing proteins are evolutionarily conserved proteins with diverse functions between different organisms. In this study, we c...

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Main Authors: Jinling Lan, Shengjie Mei, Yingxue Du, Meili Chi, Jiayi Yang, Shuliu Guo, Mingliang Chu, Ronglin He, Jie Gao
Format: Article
Language:English
Published: MDPI AG 2025-01-01
Series:Journal of Fungi
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Online Access:https://www.mdpi.com/2309-608X/11/1/59
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author Jinling Lan
Shengjie Mei
Yingxue Du
Meili Chi
Jiayi Yang
Shuliu Guo
Mingliang Chu
Ronglin He
Jie Gao
author_facet Jinling Lan
Shengjie Mei
Yingxue Du
Meili Chi
Jiayi Yang
Shuliu Guo
Mingliang Chu
Ronglin He
Jie Gao
author_sort Jinling Lan
collection DOAJ
description <i>Alternaria panax</i>, the primary pathogen that causes ginseng Alternaria leaf blight disease, can lead to a 20–30% reduction in ginseng yield. WD40 repeat-containing proteins are evolutionarily conserved proteins with diverse functions between different organisms. In this study, we characterized the roles of a WD40 repeat-containing protein in <i>A. panax</i>. The deletion of <i>ApWD40a</i> impaired the mycelial growth, reduced the sporulation, and significantly decreased the efficiency in utilizing various carbon sources. The Δ<i>Apwd40a</i> mutant showed increased sensitivity to osmotic stress and metal ion stress induced by sorbitol, NaCl, and KCl, but decreased the sensitivity to a cell wall stress factor (SDS) and oxidative stress factors (paraquat and H<sub>2</sub>O<sub>2</sub>). Pathogenicity assays performed on detached ginseng leaves and roots revealed that the disruption of <i>ApWD40a</i> significantly decreased the fungal virulence through attenuating melanin and mycotoxin production by <i>A. panax</i>. A comparative transcriptome analysis revealed that <i>ApWD40a</i> was involved in many metabolic and biosynthetic processes, including amino acid metabolism, carbon metabolism, sulfate metabolic pathways, and secondary metabolite pathways. In particular, a significantly upregulated gene that encoded a sulfate permease 2 protein in Δ<i>Apwd40a</i>, named <i>ApSulP2</i>, was deleted in the wild-type strain of <i>A. panax</i>. The deletion of <i>ApSulP2</i> resulted in reduced biomass under sulfate-free conditions, demonstrating that the sulfate transport was impaired. Taken together, our findings highlight that <i>ApWD40a</i> played crucial roles in different biological processes and the pathogenicity of <i>A. panax</i> through modulating the expressions of genes involved in various primary and secondary metabolic processes.
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spelling doaj-art-989f08bbfc744b51ac687ac293d4749f2025-01-24T13:37:24ZengMDPI AGJournal of Fungi2309-608X2025-01-011115910.3390/jof11010059ApWD40a, a Member of the WD40-Repeat Protein Family, Is Crucial for Fungal Development, Toxin Synthesis, and Pathogenicity in the Ginseng Alternaria Leaf Blight Fungus <i>Alternaria panax</i>Jinling Lan0Shengjie Mei1Yingxue Du2Meili Chi3Jiayi Yang4Shuliu Guo5Mingliang Chu6Ronglin He7Jie Gao8College of Plant Protection, Jilin Agricultural University, Changchun 130118, ChinaCollege of Plant Protection, Jilin Agricultural University, Changchun 130118, ChinaCollege of Plant Protection, Jilin Agricultural University, Changchun 130118, ChinaNational Ginseng Products Quality Inspection Testing Center, Yanji 133000, ChinaCollege of Plant Protection, Jilin Agricultural University, Changchun 130118, ChinaCollege of Plant Protection, Jilin Agricultural University, Changchun 130118, ChinaCollege of Plant Protection, Jilin Agricultural University, Changchun 130118, ChinaCollege of Plant Protection, Jilin Agricultural University, Changchun 130118, ChinaCollege of Plant Protection, Jilin Agricultural University, Changchun 130118, China<i>Alternaria panax</i>, the primary pathogen that causes ginseng Alternaria leaf blight disease, can lead to a 20–30% reduction in ginseng yield. WD40 repeat-containing proteins are evolutionarily conserved proteins with diverse functions between different organisms. In this study, we characterized the roles of a WD40 repeat-containing protein in <i>A. panax</i>. The deletion of <i>ApWD40a</i> impaired the mycelial growth, reduced the sporulation, and significantly decreased the efficiency in utilizing various carbon sources. The Δ<i>Apwd40a</i> mutant showed increased sensitivity to osmotic stress and metal ion stress induced by sorbitol, NaCl, and KCl, but decreased the sensitivity to a cell wall stress factor (SDS) and oxidative stress factors (paraquat and H<sub>2</sub>O<sub>2</sub>). Pathogenicity assays performed on detached ginseng leaves and roots revealed that the disruption of <i>ApWD40a</i> significantly decreased the fungal virulence through attenuating melanin and mycotoxin production by <i>A. panax</i>. A comparative transcriptome analysis revealed that <i>ApWD40a</i> was involved in many metabolic and biosynthetic processes, including amino acid metabolism, carbon metabolism, sulfate metabolic pathways, and secondary metabolite pathways. In particular, a significantly upregulated gene that encoded a sulfate permease 2 protein in Δ<i>Apwd40a</i>, named <i>ApSulP2</i>, was deleted in the wild-type strain of <i>A. panax</i>. The deletion of <i>ApSulP2</i> resulted in reduced biomass under sulfate-free conditions, demonstrating that the sulfate transport was impaired. Taken together, our findings highlight that <i>ApWD40a</i> played crucial roles in different biological processes and the pathogenicity of <i>A. panax</i> through modulating the expressions of genes involved in various primary and secondary metabolic processes.https://www.mdpi.com/2309-608X/11/1/59<i>Alternaria panax</i>WD40 tandemly repeated domainssecondary metabolite productionpathogenicitytranscriptome analysissulfate transport
spellingShingle Jinling Lan
Shengjie Mei
Yingxue Du
Meili Chi
Jiayi Yang
Shuliu Guo
Mingliang Chu
Ronglin He
Jie Gao
ApWD40a, a Member of the WD40-Repeat Protein Family, Is Crucial for Fungal Development, Toxin Synthesis, and Pathogenicity in the Ginseng Alternaria Leaf Blight Fungus <i>Alternaria panax</i>
Journal of Fungi
<i>Alternaria panax</i>
WD40 tandemly repeated domains
secondary metabolite production
pathogenicity
transcriptome analysis
sulfate transport
title ApWD40a, a Member of the WD40-Repeat Protein Family, Is Crucial for Fungal Development, Toxin Synthesis, and Pathogenicity in the Ginseng Alternaria Leaf Blight Fungus <i>Alternaria panax</i>
title_full ApWD40a, a Member of the WD40-Repeat Protein Family, Is Crucial for Fungal Development, Toxin Synthesis, and Pathogenicity in the Ginseng Alternaria Leaf Blight Fungus <i>Alternaria panax</i>
title_fullStr ApWD40a, a Member of the WD40-Repeat Protein Family, Is Crucial for Fungal Development, Toxin Synthesis, and Pathogenicity in the Ginseng Alternaria Leaf Blight Fungus <i>Alternaria panax</i>
title_full_unstemmed ApWD40a, a Member of the WD40-Repeat Protein Family, Is Crucial for Fungal Development, Toxin Synthesis, and Pathogenicity in the Ginseng Alternaria Leaf Blight Fungus <i>Alternaria panax</i>
title_short ApWD40a, a Member of the WD40-Repeat Protein Family, Is Crucial for Fungal Development, Toxin Synthesis, and Pathogenicity in the Ginseng Alternaria Leaf Blight Fungus <i>Alternaria panax</i>
title_sort apwd40a a member of the wd40 repeat protein family is crucial for fungal development toxin synthesis and pathogenicity in the ginseng alternaria leaf blight fungus i alternaria panax i
topic <i>Alternaria panax</i>
WD40 tandemly repeated domains
secondary metabolite production
pathogenicity
transcriptome analysis
sulfate transport
url https://www.mdpi.com/2309-608X/11/1/59
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