The TOR Signaling Pathway Governs Fungal Development, Virulence and Ustiloxin Biosynthesis in <i>Ustilaginoidea virens</i>

<i>Ustilaginoidea virens</i> is an economically important plant pathogen that causes rice false smut, which causes yield reduction and produces mycotoxins in infected grains that pose a serious threat to human and animal health. The target of rapamycin (TOR) signaling pathway acts as a m...

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Main Authors: Yuejiao Li, Shuqin Sun, Guangsheng Li, Zezhong Yang, Yuqi Xing, Ruixiang Wang, Yuanhu Xuan, Xiurong Yang
Format: Article
Language:English
Published: MDPI AG 2025-03-01
Series:Journal of Fungi
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Online Access:https://www.mdpi.com/2309-608X/11/4/239
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author Yuejiao Li
Shuqin Sun
Guangsheng Li
Zezhong Yang
Yuqi Xing
Ruixiang Wang
Yuanhu Xuan
Xiurong Yang
author_facet Yuejiao Li
Shuqin Sun
Guangsheng Li
Zezhong Yang
Yuqi Xing
Ruixiang Wang
Yuanhu Xuan
Xiurong Yang
author_sort Yuejiao Li
collection DOAJ
description <i>Ustilaginoidea virens</i> is an economically important plant pathogen that causes rice false smut, which causes yield reduction and produces mycotoxins in infected grains that pose a serious threat to human and animal health. The target of rapamycin (TOR) signaling pathway acts as a master regular in regulating cell growth and secondary metabolism in fungi. However, little is known about the function of the TOR pathway in regulating fungal development, pathogenicity and mycotoxin biosynthesis in <i>U. virens</i>. Here, we demonstrate that the TOR signaling pathway positively regulates the cell growth, conidiation and pathogenicity in <i>U. virens</i> through the biochemical inhibition of TOR kinases. The inhibition of TOR in <i>U. virens</i> (<i>UvTOR</i>) by rapamycin significantly induces the expression of genes related to mycotoxin biosynthesis, especially that of ustiloxins. Transcriptome analysis under TOR inhibition revealed that the TOR signaling pathway is a regulatory hub that governs <i>U. virens</i> growth and metabolism. A total of 275 differentially expressed genes (DEGs), consisting of 109 up-regulated DEGs and 166 down-regulated DEGs, were identified after rapamycin treatment. The up-regulated DEGs were enriched in amino acid- and acetyl-CoA-related metabolism pathways and the down-regulated DEGs were enriched in carbohydrate- and fatty acid-related metabolism pathways. Collectively, our results provide the first in-depth insight into the TOR signaling pathway in regulating vegetable growth, virulence and mycotoxin biosynthesis in <i>U. virens</i>.
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spelling doaj-art-199c6c8d74a74c0b821ea554106ea7682025-08-20T02:18:14ZengMDPI AGJournal of Fungi2309-608X2025-03-0111423910.3390/jof11040239The TOR Signaling Pathway Governs Fungal Development, Virulence and Ustiloxin Biosynthesis in <i>Ustilaginoidea virens</i>Yuejiao Li0Shuqin Sun1Guangsheng Li2Zezhong Yang3Yuqi Xing4Ruixiang Wang5Yuanhu Xuan6Xiurong Yang7Institute of Plant Protection, Tianjin Academy of Agricultural Sciences, Tianjin 300381, ChinaInstitute of Plant Protection, Tianjin Academy of Agricultural Sciences, Tianjin 300381, ChinaInstitute of Plant Protection, Tianjin Academy of Agricultural Sciences, Tianjin 300381, ChinaInstitute of Plant Protection, Tianjin Academy of Agricultural Sciences, Tianjin 300381, ChinaInstitute of Plant Protection, Tianjin Academy of Agricultural Sciences, Tianjin 300381, ChinaInstitute of Plant Protection, Tianjin Academy of Agricultural Sciences, Tianjin 300381, ChinaState Key Laboratory of Elemento-Organic Chemistry and Department of Plant Protection, National Pesticide Engineering Research Center (Tianjin), Nankai University, Tianjin 300071, ChinaInstitute of Plant Protection, Tianjin Academy of Agricultural Sciences, Tianjin 300381, China<i>Ustilaginoidea virens</i> is an economically important plant pathogen that causes rice false smut, which causes yield reduction and produces mycotoxins in infected grains that pose a serious threat to human and animal health. The target of rapamycin (TOR) signaling pathway acts as a master regular in regulating cell growth and secondary metabolism in fungi. However, little is known about the function of the TOR pathway in regulating fungal development, pathogenicity and mycotoxin biosynthesis in <i>U. virens</i>. Here, we demonstrate that the TOR signaling pathway positively regulates the cell growth, conidiation and pathogenicity in <i>U. virens</i> through the biochemical inhibition of TOR kinases. The inhibition of TOR in <i>U. virens</i> (<i>UvTOR</i>) by rapamycin significantly induces the expression of genes related to mycotoxin biosynthesis, especially that of ustiloxins. Transcriptome analysis under TOR inhibition revealed that the TOR signaling pathway is a regulatory hub that governs <i>U. virens</i> growth and metabolism. A total of 275 differentially expressed genes (DEGs), consisting of 109 up-regulated DEGs and 166 down-regulated DEGs, were identified after rapamycin treatment. The up-regulated DEGs were enriched in amino acid- and acetyl-CoA-related metabolism pathways and the down-regulated DEGs were enriched in carbohydrate- and fatty acid-related metabolism pathways. Collectively, our results provide the first in-depth insight into the TOR signaling pathway in regulating vegetable growth, virulence and mycotoxin biosynthesis in <i>U. virens</i>.https://www.mdpi.com/2309-608X/11/4/239<i>Ustilaginoidea virens</i>target of rapamycin (TOR) pathwaymycelial growthpathogenicitymycotoxins
spellingShingle Yuejiao Li
Shuqin Sun
Guangsheng Li
Zezhong Yang
Yuqi Xing
Ruixiang Wang
Yuanhu Xuan
Xiurong Yang
The TOR Signaling Pathway Governs Fungal Development, Virulence and Ustiloxin Biosynthesis in <i>Ustilaginoidea virens</i>
Journal of Fungi
<i>Ustilaginoidea virens</i>
target of rapamycin (TOR) pathway
mycelial growth
pathogenicity
mycotoxins
title The TOR Signaling Pathway Governs Fungal Development, Virulence and Ustiloxin Biosynthesis in <i>Ustilaginoidea virens</i>
title_full The TOR Signaling Pathway Governs Fungal Development, Virulence and Ustiloxin Biosynthesis in <i>Ustilaginoidea virens</i>
title_fullStr The TOR Signaling Pathway Governs Fungal Development, Virulence and Ustiloxin Biosynthesis in <i>Ustilaginoidea virens</i>
title_full_unstemmed The TOR Signaling Pathway Governs Fungal Development, Virulence and Ustiloxin Biosynthesis in <i>Ustilaginoidea virens</i>
title_short The TOR Signaling Pathway Governs Fungal Development, Virulence and Ustiloxin Biosynthesis in <i>Ustilaginoidea virens</i>
title_sort tor signaling pathway governs fungal development virulence and ustiloxin biosynthesis in i ustilaginoidea virens i
topic <i>Ustilaginoidea virens</i>
target of rapamycin (TOR) pathway
mycelial growth
pathogenicity
mycotoxins
url https://www.mdpi.com/2309-608X/11/4/239
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