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Cross-Talk and Multiple Control of Target of Rapamycin (TOR) in Sclerotinia sclerotiorum

Sclerotinia sclerotiorum is a necrotrophic phytopathogenic fungus that cross-talks with its hosts for control of cell-death pathways for colonization. Target of rapamycin (TOR) is a central regulator that controls cell growth, intracellular metabolism, and stress responses in a variety of eukaryotes...

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Autores principales: Jiao, Wenli, Ding, Weichen, Rollins, Jeffrey A., Liu, Jinliang, Zhang, Yanhua, Zhang, Xianghui, Pan, Hongyu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10100786/
https://www.ncbi.nlm.nih.gov/pubmed/36943069
http://dx.doi.org/10.1128/spectrum.00013-23
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author Jiao, Wenli
Ding, Weichen
Rollins, Jeffrey A.
Liu, Jinliang
Zhang, Yanhua
Zhang, Xianghui
Pan, Hongyu
author_facet Jiao, Wenli
Ding, Weichen
Rollins, Jeffrey A.
Liu, Jinliang
Zhang, Yanhua
Zhang, Xianghui
Pan, Hongyu
author_sort Jiao, Wenli
collection PubMed
description Sclerotinia sclerotiorum is a necrotrophic phytopathogenic fungus that cross-talks with its hosts for control of cell-death pathways for colonization. Target of rapamycin (TOR) is a central regulator that controls cell growth, intracellular metabolism, and stress responses in a variety of eukaryotes, but little is known about TOR signaling in S. sclerotiorum. In this study, we identified a conserved TOR signaling pathway and characterized SsTOR as a critical component of this pathway. Hyphal growth of S. sclerotiorum was retarded by silencing SsTOR, moreover, sclerotia and compound appressoria formation were severely disrupted. Notably, pathogenicity assays of strains shows that the virulence of the SsTOR-silenced strains were dramatically decreased. SsTOR was determined to participate in cell wall integrity (CWI) by regulating the phosphorylation level of SsSmk3, a core MAP kinase in the CWI pathway. Importantly, the inactivation of SsTOR induced autophagy in S. sclerotiorum potentially through SsAtg1 and SsAtg13. Taken together, our results suggest that SsTOR is a global regulator controlling cell growth, stress responses, cell wall integrity, autophagy, and virulence of S. sclerotiorum. IMPORTANCE TOR is a conserved protein kinase that regulates cell growth and metabolism in response to growth factors and nutrient abundance. Here, we used gene silencing to characterize SsTOR, which is a critical component of TOR signaling pathway. SsTOR-silenced strains have limited mycelium growth, and the virulence of the SsTOR-silenced strains was decreased. Phosphorylation analysis indicated that SsTOR influenced CWI by regulating the phosphorylation level of SsSmk3. Autophagy is essential to preserve cellular homeostasis in response to cellular and environmental stresses. Inactivation of SsTOR induced autophagy in S. sclerotiorum potentially through SsAtg1 and SsAtg13. These findings further indicated that SsTOR is a global regulator of the growth, development, and pathogenicity of S. sclerotiorum in multiple ways.
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spelling pubmed-101007862023-04-14 Cross-Talk and Multiple Control of Target of Rapamycin (TOR) in Sclerotinia sclerotiorum Jiao, Wenli Ding, Weichen Rollins, Jeffrey A. Liu, Jinliang Zhang, Yanhua Zhang, Xianghui Pan, Hongyu Microbiol Spectr Research Article Sclerotinia sclerotiorum is a necrotrophic phytopathogenic fungus that cross-talks with its hosts for control of cell-death pathways for colonization. Target of rapamycin (TOR) is a central regulator that controls cell growth, intracellular metabolism, and stress responses in a variety of eukaryotes, but little is known about TOR signaling in S. sclerotiorum. In this study, we identified a conserved TOR signaling pathway and characterized SsTOR as a critical component of this pathway. Hyphal growth of S. sclerotiorum was retarded by silencing SsTOR, moreover, sclerotia and compound appressoria formation were severely disrupted. Notably, pathogenicity assays of strains shows that the virulence of the SsTOR-silenced strains were dramatically decreased. SsTOR was determined to participate in cell wall integrity (CWI) by regulating the phosphorylation level of SsSmk3, a core MAP kinase in the CWI pathway. Importantly, the inactivation of SsTOR induced autophagy in S. sclerotiorum potentially through SsAtg1 and SsAtg13. Taken together, our results suggest that SsTOR is a global regulator controlling cell growth, stress responses, cell wall integrity, autophagy, and virulence of S. sclerotiorum. IMPORTANCE TOR is a conserved protein kinase that regulates cell growth and metabolism in response to growth factors and nutrient abundance. Here, we used gene silencing to characterize SsTOR, which is a critical component of TOR signaling pathway. SsTOR-silenced strains have limited mycelium growth, and the virulence of the SsTOR-silenced strains was decreased. Phosphorylation analysis indicated that SsTOR influenced CWI by regulating the phosphorylation level of SsSmk3. Autophagy is essential to preserve cellular homeostasis in response to cellular and environmental stresses. Inactivation of SsTOR induced autophagy in S. sclerotiorum potentially through SsAtg1 and SsAtg13. These findings further indicated that SsTOR is a global regulator of the growth, development, and pathogenicity of S. sclerotiorum in multiple ways. American Society for Microbiology 2023-03-21 /pmc/articles/PMC10100786/ /pubmed/36943069 http://dx.doi.org/10.1128/spectrum.00013-23 Text en Copyright © 2023 Jiao et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Jiao, Wenli
Ding, Weichen
Rollins, Jeffrey A.
Liu, Jinliang
Zhang, Yanhua
Zhang, Xianghui
Pan, Hongyu
Cross-Talk and Multiple Control of Target of Rapamycin (TOR) in Sclerotinia sclerotiorum
title Cross-Talk and Multiple Control of Target of Rapamycin (TOR) in Sclerotinia sclerotiorum
title_full Cross-Talk and Multiple Control of Target of Rapamycin (TOR) in Sclerotinia sclerotiorum
title_fullStr Cross-Talk and Multiple Control of Target of Rapamycin (TOR) in Sclerotinia sclerotiorum
title_full_unstemmed Cross-Talk and Multiple Control of Target of Rapamycin (TOR) in Sclerotinia sclerotiorum
title_short Cross-Talk and Multiple Control of Target of Rapamycin (TOR) in Sclerotinia sclerotiorum
title_sort cross-talk and multiple control of target of rapamycin (tor) in sclerotinia sclerotiorum
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10100786/
https://www.ncbi.nlm.nih.gov/pubmed/36943069
http://dx.doi.org/10.1128/spectrum.00013-23
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