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G Protein Activation without a GEF in the Plant Kingdom

Animal heterotrimeric G proteins are activated by guanine nucleotide exchange factors (GEF), typically seven transmembrane receptors that trigger GDP release and subsequent GTP binding. In contrast, the Arabidopsis thaliana G protein (AtGPA1) rapidly activates itself without a GEF and is instead reg...

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Autores principales: Urano, Daisuke, Jones, Janice C., Wang, Hao, Matthews, Melissa, Bradford, William, Bennetzen, Jeffrey L., Jones, Alan M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3386157/
https://www.ncbi.nlm.nih.gov/pubmed/22761582
http://dx.doi.org/10.1371/journal.pgen.1002756
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author Urano, Daisuke
Jones, Janice C.
Wang, Hao
Matthews, Melissa
Bradford, William
Bennetzen, Jeffrey L.
Jones, Alan M.
author_facet Urano, Daisuke
Jones, Janice C.
Wang, Hao
Matthews, Melissa
Bradford, William
Bennetzen, Jeffrey L.
Jones, Alan M.
author_sort Urano, Daisuke
collection PubMed
description Animal heterotrimeric G proteins are activated by guanine nucleotide exchange factors (GEF), typically seven transmembrane receptors that trigger GDP release and subsequent GTP binding. In contrast, the Arabidopsis thaliana G protein (AtGPA1) rapidly activates itself without a GEF and is instead regulated by a seven transmembrane Regulator of G protein Signaling (7TM-RGS) protein that promotes GTP hydrolysis to reset the inactive (GDP-bound) state. It is not known if this unusual activation is a major and constraining part of the evolutionary history of G signaling in eukaryotes. In particular, it is not known if this is an ancestral form or if this mechanism is maintained, and therefore constrained, within the plant kingdom. To determine if this mode of signal regulation is conserved throughout the plant kingdom, we analyzed available plant genomes for G protein signaling components, and we purified individually the plant components encoded in an informative set of plant genomes in order to determine their activation properties in vitro. While the subunits of the heterotrimeric G protein complex are encoded in vascular plant genomes, the 7TM-RGS genes were lost in all investigated grasses. Despite the absence of a Gα-inactivating protein in grasses, all vascular plant Gα proteins examined rapidly released GDP without a receptor and slowly hydrolyzed GTP, indicating that these Gα are self-activating. We showed further that a single amino acid substitution found naturally in grass Gα proteins reduced the Gα-RGS interaction, and this amino acid substitution occurred before the loss of the RGS gene in the grass lineage. Like grasses, non-vascular plants also appear to lack RGS proteins. However, unlike grasses, one representative non-vascular plant Gα showed rapid GTP hydrolysis, likely compensating for the loss of the RGS gene. Our findings, the loss of a regulatory gene and the retention of the “self-activating” trait, indicate the existence of divergent Gα regulatory mechanisms in the plant kingdom. In the grasses, purifying selection on the regulatory gene was lost after the physical decoupling of the RGS protein and its cognate Gα partner. More broadly these findings show extreme divergence in Gα activation and regulation that played a critical role in the evolution of G protein signaling pathways.
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spelling pubmed-33861572012-07-03 G Protein Activation without a GEF in the Plant Kingdom Urano, Daisuke Jones, Janice C. Wang, Hao Matthews, Melissa Bradford, William Bennetzen, Jeffrey L. Jones, Alan M. PLoS Genet Research Article Animal heterotrimeric G proteins are activated by guanine nucleotide exchange factors (GEF), typically seven transmembrane receptors that trigger GDP release and subsequent GTP binding. In contrast, the Arabidopsis thaliana G protein (AtGPA1) rapidly activates itself without a GEF and is instead regulated by a seven transmembrane Regulator of G protein Signaling (7TM-RGS) protein that promotes GTP hydrolysis to reset the inactive (GDP-bound) state. It is not known if this unusual activation is a major and constraining part of the evolutionary history of G signaling in eukaryotes. In particular, it is not known if this is an ancestral form or if this mechanism is maintained, and therefore constrained, within the plant kingdom. To determine if this mode of signal regulation is conserved throughout the plant kingdom, we analyzed available plant genomes for G protein signaling components, and we purified individually the plant components encoded in an informative set of plant genomes in order to determine their activation properties in vitro. While the subunits of the heterotrimeric G protein complex are encoded in vascular plant genomes, the 7TM-RGS genes were lost in all investigated grasses. Despite the absence of a Gα-inactivating protein in grasses, all vascular plant Gα proteins examined rapidly released GDP without a receptor and slowly hydrolyzed GTP, indicating that these Gα are self-activating. We showed further that a single amino acid substitution found naturally in grass Gα proteins reduced the Gα-RGS interaction, and this amino acid substitution occurred before the loss of the RGS gene in the grass lineage. Like grasses, non-vascular plants also appear to lack RGS proteins. However, unlike grasses, one representative non-vascular plant Gα showed rapid GTP hydrolysis, likely compensating for the loss of the RGS gene. Our findings, the loss of a regulatory gene and the retention of the “self-activating” trait, indicate the existence of divergent Gα regulatory mechanisms in the plant kingdom. In the grasses, purifying selection on the regulatory gene was lost after the physical decoupling of the RGS protein and its cognate Gα partner. More broadly these findings show extreme divergence in Gα activation and regulation that played a critical role in the evolution of G protein signaling pathways. Public Library of Science 2012-06-28 /pmc/articles/PMC3386157/ /pubmed/22761582 http://dx.doi.org/10.1371/journal.pgen.1002756 Text en Urano et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Urano, Daisuke
Jones, Janice C.
Wang, Hao
Matthews, Melissa
Bradford, William
Bennetzen, Jeffrey L.
Jones, Alan M.
G Protein Activation without a GEF in the Plant Kingdom
title G Protein Activation without a GEF in the Plant Kingdom
title_full G Protein Activation without a GEF in the Plant Kingdom
title_fullStr G Protein Activation without a GEF in the Plant Kingdom
title_full_unstemmed G Protein Activation without a GEF in the Plant Kingdom
title_short G Protein Activation without a GEF in the Plant Kingdom
title_sort g protein activation without a gef in the plant kingdom
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3386157/
https://www.ncbi.nlm.nih.gov/pubmed/22761582
http://dx.doi.org/10.1371/journal.pgen.1002756
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