Cargando…
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...
Autores principales: | , , , , , , |
---|---|
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 |
_version_ | 1785025356536741888 |
---|---|
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. |
format | Online Article Text |
id | pubmed-10100786 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
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 |
work_keys_str_mv | AT jiaowenli crosstalkandmultiplecontroloftargetofrapamycintorinsclerotiniasclerotiorum AT dingweichen crosstalkandmultiplecontroloftargetofrapamycintorinsclerotiniasclerotiorum AT rollinsjeffreya crosstalkandmultiplecontroloftargetofrapamycintorinsclerotiniasclerotiorum AT liujinliang crosstalkandmultiplecontroloftargetofrapamycintorinsclerotiniasclerotiorum AT zhangyanhua crosstalkandmultiplecontroloftargetofrapamycintorinsclerotiniasclerotiorum AT zhangxianghui crosstalkandmultiplecontroloftargetofrapamycintorinsclerotiniasclerotiorum AT panhongyu crosstalkandmultiplecontroloftargetofrapamycintorinsclerotiniasclerotiorum |