Posttranslational modification of the RHO of plants protein RACB by phosphorylation and cross-kingdom conserved ubiquitination

Small RHO-type G-proteins act as signaling hubs and master regulators of polarity in eukaryotic cells. Their activity is tightly controlled, as defective RHO signaling leads to aberrant growth and developmental defects. Two major processes regulate G-protein activity: canonical shuttling between dif...

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Veröffentlicht in:PloS one Jg. 17; H. 3; S. e0258924
Hauptverfasser: Weiß, Lukas, Gaelings, Lana, Reiner, Tina, Mergner, Julia, Kuster, Bernhard, Fehér, Attila, Hensel, Götz, Gahrtz, Manfred, Kumlehn, Jochen, Engelhardt, Stefan, Hückelhoven, Ralph
Format: Journal Article
Sprache:Englisch
Veröffentlicht: United States Public Library of Science 25.03.2022
Public Library of Science (PLoS)
Schlagworte:
Amino acids
Analysis
Arabidopsis - genetics
Arabidopsis - metabolism
Arabidopsis thaliana
Barley
Binding proteins
Biology and Life Sciences
Comparative analysis
Conservation
Engineering and Technology
Genetic aspects
Hordeum - genetics
Hordeum - metabolism
Hordeum vulgare
Humans
Kinases
Lipids
Lysine
Mass spectrometry
Mutation
Nucleotides
Nucleotides - metabolism
Oryza - genetics
Oryza - metabolism
Phosphorylation
Physical Sciences
Plant biology
Plant Proteins - genetics
Plant Proteins - metabolism
Point mutation
Polarity
Post-translational modification
Protein Processing, Post-Translational
Proteins
Proteomics
Rac1 protein
Ras genes
Research and Analysis Methods
Residues
rho GTP-Binding Proteins - genetics
rho GTP-Binding Proteins - metabolism
Rho protein
Scientific imaging
Signaling
Success
Ubiquitination
Germany
ISSN:1932-6203, 1932-6203
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Abstract Small RHO-type G-proteins act as signaling hubs and master regulators of polarity in eukaryotic cells. Their activity is tightly controlled, as defective RHO signaling leads to aberrant growth and developmental defects. Two major processes regulate G-protein activity: canonical shuttling between different nucleotide bound states and posttranslational modification (PTM), of which the latter can support or suppress RHO signaling, depending on the individual PTM. In plants, regulation of Rho of plants (ROPs) signaling activity has been shown to act through nucleotide exchange and GTP hydrolysis, as well as through lipid modification, but there is little data available on phosphorylation or ubiquitination of ROPs. Hence, we applied proteomic analyses to identify PTMs of the barley ROP RACB. We observed in vitro phosphorylation by barley ROP binding kinase 1 and in vivo ubiquitination of RACB. Comparative analyses of the newly identified RACB phosphosites and human RHO protein phosphosites revealed conservation of modified amino acid residues, but no overlap of actual phosphorylation patterns. However, the identified RACB ubiquitination site is conserved in all ROPs from Hordeum vulgare , Arabidopsis thaliana and Oryza sativa and in mammalian Rac1 and Rac3. Point mutation of this ubiquitination site leads to stabilization of RACB. Hence, this highly conserved lysine residue may regulate protein stability across different kingdoms.
AbstractList Small RHO-type G-proteins act as signaling hubs and master regulators of polarity in eukaryotic cells. Their activity is tightly controlled, as defective RHO signaling leads to aberrant growth and developmental defects. Two major processes regulate G-protein activity: canonical shuttling between different nucleotide bound states and posttranslational modification (PTM), of which the latter can support or suppress RHO signaling, depending on the individual PTM. In plants, regulation of Rho of plants (ROPs) signaling activity has been shown to act through nucleotide exchange and GTP hydrolysis, as well as through lipid modification, but there is little data available on phosphorylation or ubiquitination of ROPs. Hence, we applied proteomic analyses to identify PTMs of the barley ROP RACB. We observed in vitro phosphorylation by barley ROP binding kinase 1 and in vivo ubiquitination of RACB. Comparative analyses of the newly identified RACB phosphosites and human RHO protein phosphosites revealed conservation of modified amino acid residues, but no overlap of actual phosphorylation patterns. However, the identified RACB ubiquitination site is conserved in all ROPs from Hordeum vulgare, Arabidopsis thaliana and Oryza sativa and in mammalian Rac1 and Rac3. Point mutation of this ubiquitination site leads to stabilization of RACB. Hence, this highly conserved lysine residue may regulate protein stability across different kingdoms.Small RHO-type G-proteins act as signaling hubs and master regulators of polarity in eukaryotic cells. Their activity is tightly controlled, as defective RHO signaling leads to aberrant growth and developmental defects. Two major processes regulate G-protein activity: canonical shuttling between different nucleotide bound states and posttranslational modification (PTM), of which the latter can support or suppress RHO signaling, depending on the individual PTM. In plants, regulation of Rho of plants (ROPs) signaling activity has been shown to act through nucleotide exchange and GTP hydrolysis, as well as through lipid modification, but there is little data available on phosphorylation or ubiquitination of ROPs. Hence, we applied proteomic analyses to identify PTMs of the barley ROP RACB. We observed in vitro phosphorylation by barley ROP binding kinase 1 and in vivo ubiquitination of RACB. Comparative analyses of the newly identified RACB phosphosites and human RHO protein phosphosites revealed conservation of modified amino acid residues, but no overlap of actual phosphorylation patterns. However, the identified RACB ubiquitination site is conserved in all ROPs from Hordeum vulgare, Arabidopsis thaliana and Oryza sativa and in mammalian Rac1 and Rac3. Point mutation of this ubiquitination site leads to stabilization of RACB. Hence, this highly conserved lysine residue may regulate protein stability across different kingdoms.
Small RHO-type G-proteins act as signaling hubs and master regulators of polarity in eukaryotic cells. Their activity is tightly controlled, as defective RHO signaling leads to aberrant growth and developmental defects. Two major processes regulate G-protein activity: canonical shuttling between different nucleotide bound states and posttranslational modification (PTM), of which the latter can support or suppress RHO signaling, depending on the individual PTM. In plants, regulation of Rho of plants (ROPs) signaling activity has been shown to act through nucleotide exchange and GTP hydrolysis, as well as through lipid modification, but there is little data available on phosphorylation or ubiquitination of ROPs. Hence, we applied proteomic analyses to identify PTMs of the barley ROP RACB. We observed in vitro phosphorylation by barley ROP binding kinase 1 and in vivo ubiquitination of RACB. Comparative analyses of the newly identified RACB phosphosites and human RHO protein phosphosites revealed conservation of modified amino acid residues, but no overlap of actual phosphorylation patterns. However, the identified RACB ubiquitination site is conserved in all ROPs from Hordeum vulgare, Arabidopsis thaliana and Oryza sativa and in mammalian Rac1 and Rac3. Point mutation of this ubiquitination site leads to stabilization of RACB. Hence, this highly conserved lysine residue may regulate protein stability across different kingdoms.
Small RHO-type G-proteins act as signaling hubs and master regulators of polarity in eukaryotic cells. Their activity is tightly controlled, as defective RHO signaling leads to aberrant growth and developmental defects. Two major processes regulate G-protein activity: canonical shuttling between different nucleotide bound states and posttranslational modification (PTM), of which the latter can support or suppress RHO signaling, depending on the individual PTM. In plants, regulation of Rho of plants (ROPs) signaling activity has been shown to act through nucleotide exchange and GTP hydrolysis, as well as through lipid modification, but there is little data available on phosphorylation or ubiquitination of ROPs. Hence, we applied proteomic analyses to identify PTMs of the barley ROP RACB. We observed in vitro phosphorylation by barley ROP binding kinase 1 and in vivo ubiquitination of RACB. Comparative analyses of the newly identified RACB phosphosites and human RHO protein phosphosites revealed conservation of modified amino acid residues, but no overlap of actual phosphorylation patterns. However, the identified RACB ubiquitination site is conserved in all ROPs from Hordeum vulgare , Arabidopsis thaliana and Oryza sativa and in mammalian Rac1 and Rac3. Point mutation of this ubiquitination site leads to stabilization of RACB. Hence, this highly conserved lysine residue may regulate protein stability across different kingdoms.
Audience Academic
Author Fehér, Attila
Gahrtz, Manfred
Weiß, Lukas
Engelhardt, Stefan
Hensel, Götz
Reiner, Tina
Mergner, Julia
Gaelings, Lana
Kumlehn, Jochen
Hückelhoven, Ralph
Kuster, Bernhard
AuthorAffiliation 4 Chair of Plant Biology, University of Szeged, and Institute of Plant Biology, Biological Research Centre, Szeged, Hungary
2 Chair of Proteomics and Bioanalytics, Technical University of Munich (TUM), Freising, Germany
3 Bavarian Biomolecular Mass Spectrometry Center (BayBioMS), TUM, Freising, Germany
Iwate University, JAPAN
1 Chair of Phytopathology, Technical University of Munich (TUM), Freising, Germany
5 Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben, Germany
AuthorAffiliation_xml – name: Iwate University, JAPAN
– name: 2 Chair of Proteomics and Bioanalytics, Technical University of Munich (TUM), Freising, Germany
– name: 1 Chair of Phytopathology, Technical University of Munich (TUM), Freising, Germany
– name: 4 Chair of Plant Biology, University of Szeged, and Institute of Plant Biology, Biological Research Centre, Szeged, Hungary
– name: 3 Bavarian Biomolecular Mass Spectrometry Center (BayBioMS), TUM, Freising, Germany
– name: 5 Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben, Germany
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  surname: Hückelhoven
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/35333858$$D View this record in MEDLINE/PubMed
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2022 Weiß et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2022 Weiß et al 2022 Weiß et al
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– notice: 2022 Weiß et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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DocumentTitleAlternate Posttranslational modification of the RHO of plants protein RACB by phosphorylation and ubiquitination
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Current address: Chair of Brewing and Beverage Technology, Technical University of Munich (TUM), Freising, Germany
Competing Interests: The authors have declared that no competing interests exist.
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Snippet Small RHO-type G-proteins act as signaling hubs and master regulators of polarity in eukaryotic cells. Their activity is tightly controlled, as defective RHO...
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StartPage e0258924
SubjectTerms Amino acids
Analysis
Arabidopsis - genetics
Arabidopsis - metabolism
Arabidopsis thaliana
Barley
Binding proteins
Biology and Life Sciences
Comparative analysis
Conservation
Engineering and Technology
Genetic aspects
Hordeum - genetics
Hordeum - metabolism
Hordeum vulgare
Humans
Kinases
Lipids
Lysine
Mass spectrometry
Mutation
Nucleotides
Nucleotides - metabolism
Oryza - genetics
Oryza - metabolism
Phosphorylation
Physical Sciences
Plant biology
Plant Proteins - genetics
Plant Proteins - metabolism
Point mutation
Polarity
Post-translational modification
Protein Processing, Post-Translational
Proteins
Proteomics
Rac1 protein
Ras genes
Research and Analysis Methods
Residues
rho GTP-Binding Proteins - genetics
rho GTP-Binding Proteins - metabolism
Rho protein
Scientific imaging
Signaling
Success
Ubiquitination
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Title Posttranslational modification of the RHO of plants protein RACB by phosphorylation and cross-kingdom conserved ubiquitination
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http://dx.doi.org/10.1371/journal.pone.0258924
Volume 17
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