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Title: Dose-Duration Reciprocity for G protein activation: Modulation of kinase to substrate ratio alters cell signaling

Abstract

In animal cells, activation of heterotrimeric G protein signaling generally occurs when the system’s cognate signal exceeds a threshold, whereas in plant cells, both the amount and the exposure time of at least one signal, D-glucose, are used toward activation. This unusual signaling property called Dose-Duration Reciprocity, first elucidated in the genetic model Arabidopsis thaliana, is achieved by a complex that is comprised of a 7-transmembrane REGULATOR OF G SIGNALING (RGS) protein (AtRGS1), a Gα subunit that binds and hydrolyzes nucleotide, a Gβγ dimer, and three WITH NO LYSINE (WNK) kinases. D-glucose is one of several signals such as salt and pathogen-derived molecular patterns that operates through this protein complex to activate G protein signaling by WNK kinase transphosphorylation of AtRGS1. Because WNK kinases compete for the same substrate, AtRGS1, we hypothesize that activation is sensitive to the AtRGS1 amount and that modulation of the AtRGS1 pool affects the response to the stimulant. Mathematical simulation revealed that the ratio of AtRGS1 to the kinase affects system sensitivity to D-glucose, and therefore illustrates how modulation of the cellular AtRGS1 level is a means to change signal-induced activation. AtRGS1 levels change under tested conditions that mimic physiological conditions therefore, we propose amore » previously-unknown mechanism by which plants react to changes in their environment.« less

Authors:
 [1];  [2];  [2];  [3];  [4]; ORCiD logo [5]
  1. Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Biology
  2. Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Plant and Microbial Biology
  3. Stevens Inst. of Technology, Hoboken, NJ (United States)
  4. Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Pharmacology
  5. Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Biology, and Dept. of Pharmacology
Publication Date:
Research Org.:
University of North Carolina, Chapel Hill, NC (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1499880
Grant/Contract Number:  
FG02-05ER15671
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 12; Journal Issue: 12; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Liao, Kang-Ling, Melvin, Charles E., Sozzani, Rosangela, Jones, Roger D., Elston, Timothy C., and Jones, Alan M. Dose-Duration Reciprocity for G protein activation: Modulation of kinase to substrate ratio alters cell signaling. United States: N. p., 2017. Web. doi:10.1371/journal.pone.0190000.
Liao, Kang-Ling, Melvin, Charles E., Sozzani, Rosangela, Jones, Roger D., Elston, Timothy C., & Jones, Alan M. Dose-Duration Reciprocity for G protein activation: Modulation of kinase to substrate ratio alters cell signaling. United States. https://doi.org/10.1371/journal.pone.0190000
Liao, Kang-Ling, Melvin, Charles E., Sozzani, Rosangela, Jones, Roger D., Elston, Timothy C., and Jones, Alan M. Fri . "Dose-Duration Reciprocity for G protein activation: Modulation of kinase to substrate ratio alters cell signaling". United States. https://doi.org/10.1371/journal.pone.0190000. https://www.osti.gov/servlets/purl/1499880.
@article{osti_1499880,
title = {Dose-Duration Reciprocity for G protein activation: Modulation of kinase to substrate ratio alters cell signaling},
author = {Liao, Kang-Ling and Melvin, Charles E. and Sozzani, Rosangela and Jones, Roger D. and Elston, Timothy C. and Jones, Alan M.},
abstractNote = {In animal cells, activation of heterotrimeric G protein signaling generally occurs when the system’s cognate signal exceeds a threshold, whereas in plant cells, both the amount and the exposure time of at least one signal, D-glucose, are used toward activation. This unusual signaling property called Dose-Duration Reciprocity, first elucidated in the genetic model Arabidopsis thaliana, is achieved by a complex that is comprised of a 7-transmembrane REGULATOR OF G SIGNALING (RGS) protein (AtRGS1), a Gα subunit that binds and hydrolyzes nucleotide, a Gβγ dimer, and three WITH NO LYSINE (WNK) kinases. D-glucose is one of several signals such as salt and pathogen-derived molecular patterns that operates through this protein complex to activate G protein signaling by WNK kinase transphosphorylation of AtRGS1. Because WNK kinases compete for the same substrate, AtRGS1, we hypothesize that activation is sensitive to the AtRGS1 amount and that modulation of the AtRGS1 pool affects the response to the stimulant. Mathematical simulation revealed that the ratio of AtRGS1 to the kinase affects system sensitivity to D-glucose, and therefore illustrates how modulation of the cellular AtRGS1 level is a means to change signal-induced activation. AtRGS1 levels change under tested conditions that mimic physiological conditions therefore, we propose a previously-unknown mechanism by which plants react to changes in their environment.},
doi = {10.1371/journal.pone.0190000},
journal = {PLoS ONE},
number = 12,
volume = 12,
place = {United States},
year = {Fri Dec 29 00:00:00 EST 2017},
month = {Fri Dec 29 00:00:00 EST 2017}
}

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Works referencing / citing this record:

Long-distance communication in Arabidopsis involving a self-activating G protein
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