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Title: Phosphorylation of Ribosomal Protein RPS6 Integrates Light Signals and Circadian Clock Signals

Abstract

The translation of mRNA into protein is tightly regulated by the light environment as well as by the circadian clock. Although changes in translational efficiency have been well documented at the level of mRNA-ribosome loading, the underlying mechanisms are unclear. The reversible phosphorylation of RIBOSOMAL PROTEIN OF THE SMALL SUBUNIT 6 (RPS6) has been known for 40 years, but the biochemical significance of this event remains unclear to this day. Here, we confirm using a clock-deficient strain of Arabidopsis thaliana that RPS6 phosphorylation (RPS6-P) is controlled by the diel light-dark cycle with a peak during the day. Strikingly, when wild-type, clock-enabled, seedlings that have been entrained to a light-dark cycle are placed under free-running conditions, the circadian clock drives a cycle of RPS6-P with an opposite phase, peaking during the subjective night. We show that in wild-type seedlings under a light-dark cycle, the incoherent light and clock signals are integrated by the plant to cause an oscillation in RPS6-P with a reduced amplitude with a peak during the day. Sucrose can stimulate RPS6-P, as seen when sucrose in the medium masks the light response of etiolated seedlings. However, the diel cycles of RPS6-P are observed in the presence of 1%more » sucrose and in its absence. Sucrose at a high concentration of 3% appears to interfere with the robust integration of light and clock signals at the level of RPS6-P. Finally, we addressed whether RPS6-P occurs uniformly in polysomes, non-polysomal ribosomes and their subunits, and non-ribosomal protein. It is the polysomal RPS6 whose phosphorylation is most highly stimulated by light and repressed by darkness. These data exemplify a striking case of contrasting biochemical regulation between clock signals and light signals. Although the physiological significance of RPS6-P remains unknown, our data provide a mechanistic basis for the future understanding of this enigmatic event.« less

Authors:
 [1];  [1];  [1];  [2];  [1];  [1];  [3];  [4];  [5]
+ Show Author Affiliations
  1. Univ. of Tennessee, Knoxville, TN (United States). Dept. of Biochemistry, Cellular and Molecular Biology
  2. Univ. of Tennessee, Knoxville, TN (United States). Graduate School of Genome Science and Technology
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical Sciences Division
  4. Univ. of Tennessee, Knoxville, TN (United States). Graduate School of Genome Science and Technology; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical Sciences Division
  5. Univ. of Tennessee, Knoxville, TN (United States). Dept. of Biochemistry, Cellular and Molecular Biology. Graduate School of Genome Science and Technology
Publication Date:
Research Org.:
Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE; National Science Foundation (NSF); Univ. of Tennessee (United States)
OSTI Identifier:
1432165
Grant/Contract Number:  
AC05-00OR22725; IOS-1456988
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 8; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; translation; circadian clock; RPS6; phosphorylation; diurnal; Arabidopsis; eS6

Citation Formats

Enganti, Ramya, Cho, Sung Ki, Toperzer, Jody D., Urquidi-Camacho, Ricardo A., Cakir, Ozkan S., Ray, Alexandria P., Abraham, Paul E., Hettich, Robert L., and von Arnim, Albrecht G. Phosphorylation of Ribosomal Protein RPS6 Integrates Light Signals and Circadian Clock Signals. United States: N. p., 2018. Web. doi:10.3389/fpls.2017.02210.
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Enganti, Ramya, Cho, Sung Ki, Toperzer, Jody D., Urquidi-Camacho, Ricardo A., Cakir, Ozkan S., Ray, Alexandria P., Abraham, Paul E., Hettich, Robert L., & von Arnim, Albrecht G. Phosphorylation of Ribosomal Protein RPS6 Integrates Light Signals and Circadian Clock Signals. United States. https://doi.org/10.3389/fpls.2017.02210
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Enganti, Ramya, Cho, Sung Ki, Toperzer, Jody D., Urquidi-Camacho, Ricardo A., Cakir, Ozkan S., Ray, Alexandria P., Abraham, Paul E., Hettich, Robert L., and von Arnim, Albrecht G. Fri . "Phosphorylation of Ribosomal Protein RPS6 Integrates Light Signals and Circadian Clock Signals". United States. https://doi.org/10.3389/fpls.2017.02210. https://www.osti.gov/servlets/purl/1432165.
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@article{osti_1432165,
title = {Phosphorylation of Ribosomal Protein RPS6 Integrates Light Signals and Circadian Clock Signals},
author = {Enganti, Ramya and Cho, Sung Ki and Toperzer, Jody D. and Urquidi-Camacho, Ricardo A. and Cakir, Ozkan S. and Ray, Alexandria P. and Abraham, Paul E. and Hettich, Robert L. and von Arnim, Albrecht G.},
abstractNote = {The translation of mRNA into protein is tightly regulated by the light environment as well as by the circadian clock. Although changes in translational efficiency have been well documented at the level of mRNA-ribosome loading, the underlying mechanisms are unclear. The reversible phosphorylation of RIBOSOMAL PROTEIN OF THE SMALL SUBUNIT 6 (RPS6) has been known for 40 years, but the biochemical significance of this event remains unclear to this day. Here, we confirm using a clock-deficient strain of Arabidopsis thaliana that RPS6 phosphorylation (RPS6-P) is controlled by the diel light-dark cycle with a peak during the day. Strikingly, when wild-type, clock-enabled, seedlings that have been entrained to a light-dark cycle are placed under free-running conditions, the circadian clock drives a cycle of RPS6-P with an opposite phase, peaking during the subjective night. We show that in wild-type seedlings under a light-dark cycle, the incoherent light and clock signals are integrated by the plant to cause an oscillation in RPS6-P with a reduced amplitude with a peak during the day. Sucrose can stimulate RPS6-P, as seen when sucrose in the medium masks the light response of etiolated seedlings. However, the diel cycles of RPS6-P are observed in the presence of 1% sucrose and in its absence. Sucrose at a high concentration of 3% appears to interfere with the robust integration of light and clock signals at the level of RPS6-P. Finally, we addressed whether RPS6-P occurs uniformly in polysomes, non-polysomal ribosomes and their subunits, and non-ribosomal protein. It is the polysomal RPS6 whose phosphorylation is most highly stimulated by light and repressed by darkness. These data exemplify a striking case of contrasting biochemical regulation between clock signals and light signals. Although the physiological significance of RPS6-P remains unknown, our data provide a mechanistic basis for the future understanding of this enigmatic event.},
doi = {10.3389/fpls.2017.02210},
journal = {Frontiers in Plant Science},
number = ,
volume = 8,
place = {United States},
year = {Fri Jan 19 00:00:00 EST 2018},
month = {Fri Jan 19 00:00:00 EST 2018}
}
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https://doi.org/10.3389/fpls.2017.02210
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PhosPhAt: the Arabidopsis thaliana phosphorylation site database. An update
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Circadian Waves of Expression of the APRR1/TOC1 Family of Pseudo-Response Regulators in Arabidopsis thaliana : Insight into the Plant Circadian Clock
journal, September 2000

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journal, January 2002

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The Diurnal Project: Diurnal and Circadian Expression Profiling, Model-based Pattern Matching, and Promoter Analysis
journal, January 2007

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Light Control of Nuclear Gene mRNA Abundance and Translation in Tobacco
journal, December 2003

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Phytohormones Participate in an S6 Kinase Signal Transduction Pathway in Arabidopsis
journal, April 2004

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  • Plant Physiology, Vol. 134, Issue 4
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The Role of Target of Rapamycin Signaling Networks in Plant Growth and Metabolism
journal, January 2014

Overexpression of Arabidopsis Phytochrome B Inhibits Phytochrome A Function in the Presence of Sucrose
journal, April 1999

Translational Landscape of Photomorphogenic Arabidopsis
journal, October 2013

The Circadian Clock Modulates Global Daily Cycles of mRNA Ribosome Loading
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Protein Degradation Rate in Arabidopsis thaliana Leaf Growth and Development
journal, January 2017

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Sucrose control of phytochrome A signaling in Arabidopsis.
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Differential Phosphorylation of Ribosomal Proteins in Arabidopsis thaliana Plants during Day and Night
journal, December 2011

Photosynthetic Control of Arabidopsis Leaf Cytoplasmic Translation Initiation by Protein Phosphorylation
journal, July 2013

Dynamic Light Regulation of Translation Status in Arabidopsis thaliana
journal, January 2012

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    • Ryabova, Lyubov A.; Robaglia, Christophe; Meyer, Christian
    • Journal of Experimental Botany, Vol. 70, Issue 8
    • DOI: 10.1093/jxb/erz108
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