Identification of the Plant Ribokinase and Discovery of a Role for Arabidopsis Ribokinase in Nucleoside Metabolism
Abstract
Ribose can be used for energy or as a component of several important biomolecules, but for it to be used in either capacity it must first be phosphorylated by ribokinase (RBSK). RBSK proteins are part of the phosphofructokinase-B (pfkB) family of carbohydrate kinases. Sequence comparisons of pfkB proteins from the model plant Arabidopsis thaliana with the human and Escherichia coli RBSK identified a single candidate RBSK, At1g17160 (AtRBSK). AtRBSK is more similar to predicted RBSKs from other plant species and known mammalian and prokaryotic RBSK than to all other PfkB proteins in Arabidopsis. AtRBSK contains a predicted chloroplast transit peptide, and we confirmed plastid localization using AtRBSK fused to YFP. Structure prediction software verified that the AtRBSK sequence mapped onto a known RBSK structure. Kinetic parameters of purified recombinant AtRBSK were determined to be Kmribose = 150 μm ± 17 μm, KmATP = 45 μm ± 5.6 μm, and kcat = 2.0 s₋1. Substrate inhibition was observed for AtRBSK (KiATP = 2.44 mm ± 0.36 mm), as has been demonstrated for other RBSK proteins. Ribose accumulated in Arabidopsis plants lacking AtRBSK. Such plants grew normally unless media was supplemented with ribose, which led to chlorosis and growth inhibition. Both chlorosismore »
- Authors:
- Publication Date:
- Research Org.:
- Univ. of California, Davis, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1769195
- Alternate Identifier(s):
- OSTI ID: 1333861
- Grant/Contract Number:
- FG02–09ER16077; SC0002175
- Resource Type:
- Published Article
- Journal Name:
- Journal of Biological Chemistry
- Additional Journal Information:
- Journal Name: Journal of Biological Chemistry Journal Volume: 291 Journal Issue: 43; Journal ID: ISSN 0021-9258
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 09 BIOMASS FUELS; carbohydrate metabolism; carbohydrate kinase; kinase; ribokinase
Citation Formats
Riggs, John W., Rockwell, Nathan C., Cavales, Philip C., and Callis, Judy. Identification of the Plant Ribokinase and Discovery of a Role for Arabidopsis Ribokinase in Nucleoside Metabolism. United States: N. p., 2016.
Web. doi:10.1074/jbc.M116.754689.
Riggs, John W., Rockwell, Nathan C., Cavales, Philip C., & Callis, Judy. Identification of the Plant Ribokinase and Discovery of a Role for Arabidopsis Ribokinase in Nucleoside Metabolism. United States. https://doi.org/10.1074/jbc.M116.754689
Riggs, John W., Rockwell, Nathan C., Cavales, Philip C., and Callis, Judy. Sat .
"Identification of the Plant Ribokinase and Discovery of a Role for Arabidopsis Ribokinase in Nucleoside Metabolism". United States. https://doi.org/10.1074/jbc.M116.754689.
@article{osti_1769195,
title = {Identification of the Plant Ribokinase and Discovery of a Role for Arabidopsis Ribokinase in Nucleoside Metabolism},
author = {Riggs, John W. and Rockwell, Nathan C. and Cavales, Philip C. and Callis, Judy},
abstractNote = {Ribose can be used for energy or as a component of several important biomolecules, but for it to be used in either capacity it must first be phosphorylated by ribokinase (RBSK). RBSK proteins are part of the phosphofructokinase-B (pfkB) family of carbohydrate kinases. Sequence comparisons of pfkB proteins from the model plant Arabidopsis thaliana with the human and Escherichia coli RBSK identified a single candidate RBSK, At1g17160 (AtRBSK). AtRBSK is more similar to predicted RBSKs from other plant species and known mammalian and prokaryotic RBSK than to all other PfkB proteins in Arabidopsis. AtRBSK contains a predicted chloroplast transit peptide, and we confirmed plastid localization using AtRBSK fused to YFP. Structure prediction software verified that the AtRBSK sequence mapped onto a known RBSK structure. Kinetic parameters of purified recombinant AtRBSK were determined to be Kmribose = 150 μm ± 17 μm, KmATP = 45 μm ± 5.6 μm, and kcat = 2.0 s₋1. Substrate inhibition was observed for AtRBSK (KiATP = 2.44 mm ± 0.36 mm), as has been demonstrated for other RBSK proteins. Ribose accumulated in Arabidopsis plants lacking AtRBSK. Such plants grew normally unless media was supplemented with ribose, which led to chlorosis and growth inhibition. Both chlorosis and ribose accumulation were abolished upon the introduction of a transgene expressing AtRBSK-MYC, demonstrating that the loss of protein is responsible for ribose hypersensitivity. Lastly, ribose accumulation in plants lacking AtRBSK was reduced in plants also deficient in the nucleoside ribohydrolase NSH1, linking AtRBSK activity to nucleoside metabolism.},
doi = {10.1074/jbc.M116.754689},
journal = {Journal of Biological Chemistry},
number = 43,
volume = 291,
place = {United States},
year = {Sat Oct 01 00:00:00 EDT 2016},
month = {Sat Oct 01 00:00:00 EDT 2016}
}
https://doi.org/10.1074/jbc.M116.754689
Web of Science
Works referenced in this record:
Flexible mapping of homology onto structure with Homolmapper
journal, April 2007
- Rockwell, Nathan C.; Lagarias, J. Clark
- BMC Bioinformatics, Vol. 8, Issue 1
Role of monovalent and divalent metal cations in human ribokinase catalysis and regulation
journal, March 2015
- Quiroga-Roger, Diego; Babul, Jorge; Guixé, Victoria
- BioMetals, Vol. 28, Issue 2
Identification and characterization of human ribokinase and comparison of its properties with E. coli ribokinase and human adenosine kinase
journal, June 2007
- Park, Jae; van Koeverden, Paul; Singh, Bhag
- FEBS Letters, Vol. 581, Issue 17
Pentavalent Ions Dependency Is a Conserved Property of Adenosine Kinase from Diverse Sources: Identification of a Novel Motif Implicated in Phosphate and Magnesium Ion Binding and Substrate Inhibition †
journal, March 2002
- Maj, Mary C.; Singh, Bhag; Gupta, Radhey S.
- Biochemistry, Vol. 41, Issue 12
Multiple local maxima for likelihoods of phylogenetic trees: a simulation study
journal, August 1999
- Rogers, J. S.; Swofford, D. L.
- Molecular Biology and Evolution, Vol. 16, Issue 8
ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites
journal, January 1999
- Emanuelsson, Olof; Nielsen, Henrik; Heijne, Gunnar Von
- Protein Science, Vol. 8, Issue 5
Activation of ribokinase by monovalent cations
journal, January 2002
- Andersson, C. Evalena; Mowbray, Sherry L.
- Journal of Molecular Biology, Vol. 315, Issue 3
Arabidopsis thaliana nucleosidase mutants provide new insights into nucleoside degradation
journal, May 2011
- Riegler, Heike; Geserick, Claudia; Zrenner, Rita
- New Phytologist, Vol. 191, Issue 2
Adenosine kinase and ribokinase – the RK family of proteins
journal, June 2008
- Park, J.; Gupta, R. S.
- Cellular and Molecular Life Sciences, Vol. 65, Issue 18
Sorting Signals, N-Terminal Modifications and Abundance of the Chloroplast Proteome
journal, April 2008
- Zybailov, Boris; Rutschow, Heidi; Friso, Giulia
- PLoS ONE, Vol. 3, Issue 4
Glucose Transport into Spinach Chloroplasts
journal, August 1977
- Schäfer, Gisela; Heber, Ulrich; Heldt, Hans W.
- Plant Physiology, Vol. 60, Issue 2
Basic local alignment search tool
journal, October 1990
- Altschul, Stephen F.; Gish, Warren; Miller, Webb
- Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
MUSCLE: a multiple sequence alignment method with reduced time and space complexity
journal, August 2004
- Edgar, Robert C.
- BMC Bioinformatics, Vol. 5, Issue 1, p. 113
Visualization of Plastid Nucleoids In situ Using the PEND–GFP Fusion Protein
journal, April 2005
- Terasawa, Kimihiro; Sato, Naoki
- Plant and Cell Physiology, Vol. 46, Issue 4
Process for the integrated extraction, identification and quantification of metabolites, proteins and RNA to reveal their co-regulation in biochemical networks
journal, January 2004
- Weckwerth, Wolfram; Wenzel, Kathrin; Fiehn, Oliver
- PROTEOMICS, Vol. 4, Issue 1
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega
journal, January 2011
- Sievers, Fabian; Wilm, Andreas; Dineen, David
- Molecular Systems Biology, Vol. 7, Issue 1
Uridine-Ribohydrolase Is a Key Regulator in the Uridine Degradation Pathway of Arabidopsis
journal, March 2009
- Jung, Benjamin; Flörchinger, Martin; Kunz, Hans-Henning
- The Plant Cell, Vol. 21, Issue 3
Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation
journal, July 2007
- Nakagawa, Tsuyoshi; Kurose, Takayuki; Hino, Takeshi
- Journal of Bioscience and Bioengineering, Vol. 104, Issue 1
Pyrimidine and Purine Biosynthesis and Degradation in Plants
journal, June 2006
- Zrenner, Rita; Stitt, Mark; Sonnewald, Uwe
- Annual Review of Plant Biology, Vol. 57, Issue 1
Gateway-compatible vectors for plant functional genomics and proteomics
journal, February 2006
- Earley, Keith W.; Haag, Jeremy R.; Pontes, Olga
- The Plant Journal, Vol. 45, Issue 4
Ribokinase family evolution and the role of conserved residues at the active site of the PfkB subfamily representative, Pfk-2 from Escherichia coli
journal, October 2010
- Cabrera, Ricardo; Babul, Jorge; Guixé, Victoria
- Archives of Biochemistry and Biophysics, Vol. 502, Issue 1
Phosphofructokinases from Escherichia coli. Purification and characterization of the nonallosteric isozyme.
journal, June 1978
- Babul, J.
- Journal of Biological Chemistry, Vol. 253, Issue 12
Evidence for a Catalytic Mg 2+ Ion and Effect of Phosphate on the Activity of Escherichia coli Phosphofructokinase-2: Regulatory Properties of a Ribokinase Family Member †
journal, August 2006
- Parducci, Rafael E.; Cabrera, Ricardo; Baez, Mauricio
- Biochemistry, Vol. 45, Issue 30
Ribokinase from E. coli: Expression, purification, and substrate specificity
journal, September 2006
- Chuvikovsky, D.; Esipov, R.; Skoblov, Y.
- Bioorganic & Medicinal Chemistry, Vol. 14, Issue 18
Arabidopsis nucleoside hydrolases involved in intracellular and extracellular degradation of purines: Arabidopsis nucleoside hydrolase family
journal, January 2011
- Jung, Benjamin; Hoffmann, Christiane; Möhlmann, Torsten
- The Plant Journal, Vol. 65, Issue 5
Ribokinase from Escherichia coli K12. Nucleotide sequence and overexpression of the rbsK gene and purification of ribokinase.
journal, June 1986
- Hope, J. N.; Bell, A. W.; Hermodson, M. A.
- Journal of Biological Chemistry, Vol. 261, Issue 17
VMD: Visual molecular dynamics
journal, February 1996
- Humphrey, William; Dalke, Andrew; Schulten, Klaus
- Journal of Molecular Graphics, Vol. 14, Issue 1
Metabolism of pyrimidine bases and nucleosides by pyrimidine-nucleoside phosphorylases in cultured human lymphoid cells
journal, April 1987
- Pérignon, Jean-Louis; Bories, Dominique M.; Houllier, Anne-Marie
- Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 928, Issue 2
Development of a fluorescent nanosensor for ribose
journal, September 2003
- Lager, Ida; Fehr, Marcus; Frommer, Wolf B.
- FEBS Letters, Vol. 553, Issue 1-2
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Metatranscriptomic and metabolite profiling reveals vertical heterogeneity within a Zygnema green algal mat from Svalbard (High Arctic)
journal, September 2019
- Rippin, Martin; Pichrtová, Martina; Arc, Erwann
- Environmental Microbiology, Vol. 21, Issue 11