A bacterial type III effector hijacks plant ubiquitin proteases to evade degradation
Gram-negative bacterial pathogens inject effector proteins inside plant cells using a type III secretion system. These effectors manipulate plant cellular functions and suppress the plant immune system in order to promote bacterial proliferation. Despite the fact that bacterial effectors are exogeno...
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Published in | PLoS pathogens Vol. 21; no. 1; p. e1012882 |
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Main Authors | , , , , , , , |
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Language | English |
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22.01.2025
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Abstract | Gram-negative bacterial pathogens inject effector proteins inside plant cells using a type III secretion system. These effectors manipulate plant cellular functions and suppress the plant immune system in order to promote bacterial proliferation. Despite the fact that bacterial effectors are exogenous threatening proteins potentially exposed to the protein degradation systems inside plant cells, effectors are relative stable and able to perform their virulence functions. In this work, we found that RipE1, an effector protein secreted by the bacterial wilt pathogen,
Ralstonia solanacearum
, undergoes phosphorylation of specific residues inside plant cells, and this promotes its stability. Moreover, RipE1 associates with plant ubiquitin proteases, which contribute to RipE1 deubiquitination and stabilization. The absence of those specific phosphorylation sites or specific host ubiquitin proteases leads to a substantial decrease in RipE1 protein accumulation, indicating that RipE1 hijacks plant post-translational modification regulators in order to promote its own stability. These results suggest that effector stability or degradation in plant cells constitute another molecular event subject to co-evolution between plants and pathogens. |
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AbstractList | Gram-negative bacterial pathogens inject effector proteins inside plant cells using a type III secretion system. These effectors manipulate plant cellular functions and suppress the plant immune system in order to promote bacterial proliferation. Despite the fact that bacterial effectors are exogenous threatening proteins potentially exposed to the protein degradation systems inside plant cells, effectors are relative stable and able to perform their virulence functions. In this work, we found that RipE1, an effector protein secreted by the bacterial wilt pathogen, Ralstonia solanacearum, undergoes phosphorylation of specific residues inside plant cells, and this promotes its stability. Moreover, RipE1 associates with plant ubiquitin proteases, which contribute to RipE1 deubiquitination and stabilization. The absence of those specific phosphorylation sites or specific host ubiquitin proteases leads to a substantial decrease in RipE1 protein accumulation, indicating that RipE1 hijacks plant post-translational modification regulators in order to promote its own stability. These results suggest that effector stability or degradation in plant cells constitute another molecular event subject to co-evolution between plants and pathogens.Gram-negative bacterial pathogens inject effector proteins inside plant cells using a type III secretion system. These effectors manipulate plant cellular functions and suppress the plant immune system in order to promote bacterial proliferation. Despite the fact that bacterial effectors are exogenous threatening proteins potentially exposed to the protein degradation systems inside plant cells, effectors are relative stable and able to perform their virulence functions. In this work, we found that RipE1, an effector protein secreted by the bacterial wilt pathogen, Ralstonia solanacearum, undergoes phosphorylation of specific residues inside plant cells, and this promotes its stability. Moreover, RipE1 associates with plant ubiquitin proteases, which contribute to RipE1 deubiquitination and stabilization. The absence of those specific phosphorylation sites or specific host ubiquitin proteases leads to a substantial decrease in RipE1 protein accumulation, indicating that RipE1 hijacks plant post-translational modification regulators in order to promote its own stability. These results suggest that effector stability or degradation in plant cells constitute another molecular event subject to co-evolution between plants and pathogens. Gram-negative bacterial pathogens inject effector proteins inside plant cells using a type III secretion system. These effectors manipulate plant cellular functions and suppress the plant immune system in order to promote bacterial proliferation. Despite the fact that bacterial effectors are exogenous threatening proteins potentially exposed to the protein degradation systems inside plant cells, effectors are relative stable and able to perform their virulence functions. In this work, we found that RipE1, an effector protein secreted by the bacterial wilt pathogen, Ralstonia solanacearum , undergoes phosphorylation of specific residues inside plant cells, and this promotes its stability. Moreover, RipE1 associates with plant ubiquitin proteases, which contribute to RipE1 deubiquitination and stabilization. The absence of those specific phosphorylation sites or specific host ubiquitin proteases leads to a substantial decrease in RipE1 protein accumulation, indicating that RipE1 hijacks plant post-translational modification regulators in order to promote its own stability. These results suggest that effector stability or degradation in plant cells constitute another molecular event subject to co-evolution between plants and pathogens. Most bacterial plant pathogens inject effector proteins inside host cells to suppress immune responses and manipulate other plant functions in order to cause disease. Even though these effector proteins could be targeted by the protein degradation systems in plant cells, they are able to perform their virulence functions, which suggests that they are relatively stable, even though the mechanisms leading to this stability remain poorly understood. In this work, we found that RipE1, an effector protein secreted by the bacterial wilt pathogen, Ralstonia solanacearum , has the potential to be ubiquitinated and degraded in plant cells. However, RipE1 hijacks plant kinases and undergoes phosphorylation of specific residues inside plant cells, and this counteracts its ubiquitination and promotes its stability. Moreover, RipE1 associates with plant ubiquitin proteases, which contribute to RipE1 deubiquitination and stabilization. Our study suggests that effector stability or degradation in plant cells constitute another molecular event subject to co-evolution between plants and pathogens, and that pathogen effectors hijack plant post-translational modification regulators in order to promote their own stability. Gram-negative bacterial pathogens inject effector proteins inside plant cells using a type III secretion system. These effectors manipulate plant cellular functions and suppress the plant immune system in order to promote bacterial proliferation. Despite the fact that bacterial effectors are exogenous threatening proteins potentially exposed to the protein degradation systems inside plant cells, effectors are relative stable and able to perform their virulence functions. In this work, we found that RipE1, an effector protein secreted by the bacterial wilt pathogen, Ralstonia solanacearum , undergoes phosphorylation of specific residues inside plant cells, and this promotes its stability. Moreover, RipE1 associates with plant ubiquitin proteases, which contribute to RipE1 deubiquitination and stabilization. The absence of those specific phosphorylation sites or specific host ubiquitin proteases leads to a substantial decrease in RipE1 protein accumulation, indicating that RipE1 hijacks plant post-translational modification regulators in order to promote its own stability. These results suggest that effector stability or degradation in plant cells constitute another molecular event subject to co-evolution between plants and pathogens. Gram-negative bacterial pathogens inject effector proteins inside plant cells using a type III secretion system. These effectors manipulate plant cellular functions and suppress the plant immune system in order to promote bacterial proliferation. Despite the fact that bacterial effectors are exogenous threatening proteins potentially exposed to the protein degradation systems inside plant cells, effectors are relative stable and able to perform their virulence functions. In this work, we found that RipE1, an effector protein secreted by the bacterial wilt pathogen, Ralstonia solanacearum, undergoes phosphorylation of specific residues inside plant cells, and this promotes its stability. Moreover, RipE1 associates with plant ubiquitin proteases, which contribute to RipE1 deubiquitination and stabilization. The absence of those specific phosphorylation sites or specific host ubiquitin proteases leads to a substantial decrease in RipE1 protein accumulation, indicating that RipE1 hijacks plant post-translational modification regulators in order to promote its own stability. These results suggest that effector stability or degradation in plant cells constitute another molecular event subject to co-evolution between plants and pathogens. |
Audience | Academic |
Author | Yu, Wenjia Luo, Jiamin Macho, Alberto P. Li, Meng Wang, Wenjun Sang, Yuying Zhuang, Haiyan Segonzac, Cecile |
AuthorAffiliation | 3 Department of Agriculture, Forestry and Bioresources, Seoul National University, Seoul, Republic of Korea 2 University of the Chinese Academy of Sciences, Beijing, China Leibniz Institute of Plant Biochemistry: Leibniz-Institut fur Pflanzenbiochemie, GERMANY 1 Shanghai Center for Plant Stress Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, China |
AuthorAffiliation_xml | – name: 3 Department of Agriculture, Forestry and Bioresources, Seoul National University, Seoul, Republic of Korea – name: 2 University of the Chinese Academy of Sciences, Beijing, China – name: Leibniz Institute of Plant Biochemistry: Leibniz-Institut fur Pflanzenbiochemie, GERMANY – name: 1 Shanghai Center for Plant Stress Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, China |
Author_xml | – sequence: 1 givenname: Wenjia surname: Yu fullname: Yu, Wenjia – sequence: 2 givenname: Meng surname: Li fullname: Li, Meng – sequence: 3 givenname: Wenjun surname: Wang fullname: Wang, Wenjun – sequence: 4 givenname: Haiyan surname: Zhuang fullname: Zhuang, Haiyan – sequence: 5 givenname: Jiamin surname: Luo fullname: Luo, Jiamin – sequence: 6 givenname: Yuying surname: Sang fullname: Sang, Yuying – sequence: 7 givenname: Cecile surname: Segonzac fullname: Segonzac, Cecile – sequence: 8 givenname: Alberto P. orcidid: 0000-0001-9935-8026 surname: Macho fullname: Macho, Alberto P. |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/39841799$$D View this record in MEDLINE/PubMed |
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Cites_doi | 10.1074/jbc.REV120.010852 10.7717/peerj.7346 10.1038/nplants.2016.126 10.1111/j.1469-8137.2011.03672.x 10.1111/nph.13605 10.1146/annurev-phyto-021622-123232 10.1111/mpp.13360 10.3389/fpls.2017.01899 10.1094/MPMI-03-18-0062-R 10.3390/cells11050851 10.1111/nph.15601 10.1016/S0092-8674(03)00849-3 10.15252/embj.2021110352 10.1111/j.1469-8137.2007.02293.x 10.1105/tpc.17.00216 10.3390/cells9102219 10.1016/j.pbi.2023.102396 10.1074/jbc.M115.678953 10.1126/science.1067554 10.1038/s41579-022-00710-3 10.1094/MPMI-23-3-0251 10.1016/j.molp.2022.11.008 10.1371/journal.ppat.1008933 10.1016/j.xplc.2020.100025 10.1146/annurev-phyto-021622-110443 10.15252/embj.2020107257 10.1146/annurev-biochem-061516-044908 10.1073/pnas.1715556115 10.1111/mpp.12504 10.1038/s41467-020-17573-y 10.1105/tpc.17.00579 10.1093/jxb/erad246 10.1016/j.tibs.2009.12.005 10.1111/nph.18533 10.1111/mpp.13363 10.1146/annurev-phyto-080615-100204 10.1128/MMBR.68.4.771-795.2004 |
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SubjectTerms | Bacterial diseases of plants Bacterial proteins Bacterial Proteins - genetics Bacterial Proteins - metabolism Biology and Life Sciences Host-Pathogen Interactions Microbiological research Physiological aspects Plant Diseases - microbiology Plant Immunity Plant Proteins - metabolism Proteolysis Ralstonia solanacearum - metabolism Ralstonia solanacearum - pathogenicity Research and Analysis Methods Type III Secretion Systems - metabolism Ubiquitin-proteasome system Ubiquitin-Specific Proteases - metabolism |
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Title | A bacterial type III effector hijacks plant ubiquitin proteases to evade degradation |
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