G Protein Activation without a GEF in the Plant Kingdom
Identifieur interne : 001092 ( Pmc/Curation ); précédent : 001091; suivant : 001093G Protein Activation without a GEF in the Plant Kingdom
Auteurs : Daisuke Urano [États-Unis] ; Janice C. Jones [États-Unis] ; Hao Wang [États-Unis] ; Melissa Matthews [États-Unis] ; William Bradford [États-Unis] ; Jeffrey L. Bennetzen [États-Unis] ; Alan M. Jones [États-Unis]Source :
- PLoS Genetics [ 1553-7390 ] ; 2012.
Abstract
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
Url:
DOI: 10.1371/journal.pgen.1002756
PubMed: 22761582
PubMed Central: 3386157
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PMC:3386157Le document en format XML
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<front><div type="abstract" xml:lang="en"><p>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 <italic>Arabidopsis thaliana</italic>
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 <italic>in vitro</italic>
. 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.</p>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS Genet</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS Genet</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plosgen</journal-id>
<journal-title-group><journal-title>PLoS Genetics</journal-title>
</journal-title-group>
<issn pub-type="ppub">1553-7390</issn>
<issn pub-type="epub">1553-7404</issn>
<publisher><publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">22761582</article-id>
<article-id pub-id-type="pmc">3386157</article-id>
<article-id pub-id-type="publisher-id">PGENETICS-D-12-00464</article-id>
<article-id pub-id-type="doi">10.1371/journal.pgen.1002756</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline-v2"><subject>Biology</subject>
<subj-group><subject>Evolutionary Biology</subject>
</subj-group>
<subj-group><subject>Molecular Cell Biology</subject>
<subj-group><subject>Signal Transduction</subject>
</subj-group>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>G Protein Activation without a GEF in the Plant Kingdom</article-title>
<alt-title alt-title-type="running-head">G Protein Activation without a GEF</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author" equal-contrib="yes"><name><surname>Urano</surname>
<given-names>Daisuke</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author" equal-contrib="yes"><name><surname>Jones</surname>
<given-names>Janice C.</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wang</surname>
<given-names>Hao</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Matthews</surname>
<given-names>Melissa</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Bradford</surname>
<given-names>William</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Bennetzen</surname>
<given-names>Jeffrey L.</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Jones</surname>
<given-names>Alan M.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>*</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>1</label>
<addr-line>Department of Biology, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America</addr-line>
</aff>
<aff id="aff2"><label>2</label>
<addr-line>Department of Biochemistry and Biophysics, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America</addr-line>
</aff>
<aff id="aff3"><label>3</label>
<addr-line>Department of Genetics, University of Georgia, Athens, Georgia, United States of America</addr-line>
</aff>
<aff id="aff4"><label>4</label>
<addr-line>Department of Pharmacology, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Malik</surname>
<given-names>Harmit S.</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1">Fred Hutchinson Cancer Research Center, United States of America</aff>
<author-notes><corresp id="cor1">* E-mail: <email>alan_jones@unc.edu</email>
</corresp>
<fn fn-type="con"><p>Conceived and designed the experiments: DU JCJ HW MM WB JLB AMJ. Performed the experiments: DU JCJ HW MM WB. Analyzed the data: DU JCJ HW MM WB JB JLB AMJ. Contributed reagents/materials/analysis tools: AMJ JLB. Wrote the paper: DU JCJ JLB AMJ.</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><month>6</month>
<year>2012</year>
</pub-date>
<pub-date pub-type="epub"><day>28</day>
<month>6</month>
<year>2012</year>
</pub-date>
<volume>8</volume>
<issue>6</issue>
<elocation-id>e1002756</elocation-id>
<history><date date-type="received"><day>21</day>
<month>2</month>
<year>2012</year>
</date>
<date date-type="accepted"><day>25</day>
<month>4</month>
<year>2012</year>
</date>
</history>
<permissions><copyright-statement>Urano et al.</copyright-statement>
<copyright-year>2012</copyright-year>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>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.</license-p>
</license>
</permissions>
<abstract><p>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 <italic>Arabidopsis thaliana</italic>
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 <italic>in vitro</italic>
. 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.</p>
</abstract>
<abstract abstract-type="summary"><title>Author Summary</title>
<p>Extracellular signals activate intracellular changes that lead to cell behaviors. This spatial coupling is mediated by cell-surface receptor activation of the heterotrimeric G protein complex located on the cytoplasmic side of the plasma membrane. Unlike the case for metazoans, plant G proteins are constitutively active. Plants use multiple mechanisms to keep the G protein complex in its resting state, and activation occurs by inhibition of this property. One mechanism involves a cell surface receptor that accelerates the return to the resting state through direct interaction with the G protein at a specific protein interface. This unique protein, AtRGS1, has both an animal like receptor domain and a domain (RGS box) responsible for accelerating deactivation. One group of plants (cereals) lost this protein through, first, a mutation in the protein interface that reduces the affinity for the RGS box to the G protein, followed by gene loss.</p>
</abstract>
<counts><page-count count="13"></page-count>
</counts>
</article-meta>
</front>
</pmc>
</record>
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