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

Journal Article · · Frontiers in Plant Science
 [1];  [1];  [1];  [2];  [1];  [1];  [3];  [4];  [5]
  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
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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.

Research Organization:
Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
USDOE; National Science Foundation (NSF); Univ. of Tennessee (United States)
Grant/Contract Number:
AC05-00OR22725; IOS-1456988
OSTI ID:
1432165
Journal Information:
Frontiers in Plant Science, Vol. 8; ISSN 1664-462X
Publisher:
Frontiers Research FoundationCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 36 works
Citation information provided by
Web of Science

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Cited By (7)

The nucleolus, an ally, and an enemy of cancer cells journal August 2018
TOR and RPS6 transmit light signals to enhance protein translation in deetiolating Arabidopsis seedlings journal November 2018
Integration of nutrient, energy, light, and hormone signalling via TOR in plants journal February 2019
Target of Rapamycin kinase: central regulatory hub for plant growth and metabolism journal April 2019
Thermal imaging as a noninvasive technique for analyzing circadian rhythms in plants journal September 2019
Recent advances in understanding regulation of the Arabidopsis circadian clock by local cellular environment journal January 2020
Recent advances in understanding regulation of the Arabidopsis circadian clock by local cellular environment. text January 2020

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
translation
circadian clock
RPS6
phosphorylation
diurnal
Arabidopsis
eS6