A single serine to alanine substitution decreases bicarbonate affinity of phosphoenolpyruvate carboxylase in C4Flaveria trinervia

DiMario, Robert J.; Cousins, Asaph B.

doi:10.1093/jxb/ery403

Title: A single serine to alanine substitution decreases bicarbonate affinity of phosphoenolpyruvate carboxylase in C₄Flaveria trinervia

Journal Article · Tue Dec 04 00:00:00 EST 2018 · Journal of Experimental Botany

DOI:https://doi.org/10.1093/jxb/ery403· OSTI ID:1610566

DiMario, Robert J. ^[1]; Cousins, Asaph B. ^[1]

Washington State Univ., Pullman, WA (United States)

Phosphoenolpyruvate (PEP) carboxylase (PEPc) catalyzes the first committed step of C₄ photosynthesis generating oxaloacetate from bicarbonate (HCO₃^–) and PEP. It is hypothesized that PEPc affinity for HCO₃^– has undergone selective pressure for a lower K_HCO3 (K_m for HCO₃^–) to increase the carbon flux entering the C₄ cycle, particularly during conditions that limit CO₂ availability. However, the decrease in K_HCO3has been hypothesized to cause an unavoidable increase in K_PEP (K_m for PEP). Therefore, the amino acid residue S774 in the C₄ enzyme, which has been shown to increase K_PEP, should lead to a decrease in K_HCO3. Several studies reported the effect S774 has on K_PEP; however, the influence of this amino acid substitution on K_HCO3 has not been tested. To test these hypotheses, membrane-inlet mass spectrometry (MIMS) was used to measure the K_HCO3 of the photosynthetic PEPc from the C₄Flaveria trinervia and the non-photosynthetic PEPc from the C₃F. pringlei. The cDNAs for these enzymes were overexpressed and purified from the PEPc-less PCR1 Escherichia coli strain. Our work in comparison with previous reports suggests that K_HCO3 and K_PEP are linked by specific amino acids, such as S774; however, these kinetic parameters respond differently to the tested allosteric regulators, malate and glucose-6-phosphate.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Washington State Univ., Pullman, WA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; National Science Foundation (NSF)

Grant/Contract Number:: SC0001685; 0923562

OSTI ID:: 1610566

Journal Information:: Journal of Experimental Botany, Vol. 70, Issue 3; ISSN 0022-0957

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 15 works

Citation information provided by
Web of Science

References (55)

The remarkable diversity of plant PEPC (phosphoenolpyruvate carboxylase): recent insights into the physiological functions and post-translational controls of non-photosynthetic PEPCs O'Leary, Brendan; Park, Joonho; Plaxton, William C. Biochemical Journal, Vol. 436, Issue 1 https://doi.org/10.1042/BJ20110078	journal	April 2011
Molecular cloning of the phosphoenolpyruvate carboxylase gene, ppc, of Escherichia coli Sabe, Hisataka; Miwa, Tetsuya; Kodaki, Tsutomu Gene, Vol. 31, Issue 1-3 https://doi.org/10.1016/0378-1119(84)90222-1	journal	November 1984
Simultaneous determination of Rubisco carboxylase and oxygenase kinetic parameters in Triticum aestivum and Zea mays using membrane inlet mass spectrometry Cousins, A. B.; Ghannoum, O.; Von Caemmerer, S. Plant, Cell & Environment, Vol. 33, Issue 3 https://doi.org/10.1111/j.1365-3040.2009.02095.x	journal	March 2010
Nitrogen acquisition, PEP carboxylase, and cellular pH homeostasis: new views on old paradigms Britto, Dev T.; Kronzucker, Herbert J. Plant, Cell and Environment, Vol. 28, Issue 11 https://doi.org/10.1111/j.1365-3040.2005.01372.x	journal	November 2005
The Mechanistic Basis of Internal Conductance: A Theoretical Analysis of Mesophyll Cell Photosynthesis and CO ₂ Diffusion Tholen, Danny; Zhu, Xin-Guang Plant Physiology, Vol. 156, Issue 1 https://doi.org/10.1104/pp.111.172346	journal	March 2011
Maize C4-form phosphoenolpyruvate carboxylase engineered to be functional in C3 plants: mutations for diminished sensitivity to feedback inhibitors and for increased substrate affinity Endo, T.; Mihara, Y.; Furumoto, T. Journal of Experimental Botany, Vol. 59, Issue 7 https://doi.org/10.1093/jxb/ern018	journal	June 2007
Inhibition of Phospho enol pyruvate Carboxylase by Malate Wedding, Randolph T.; Black, M. Kay; Meyer, Christopher R. Plant Physiology, Vol. 92, Issue 2 https://doi.org/10.1104/pp.92.2.456	journal	February 1990
The regulatory role of residues 226–232 in phosphoenolpyruvate carboxylase from maize Yuan, Jiping; Sayegh, Joyce; Mendez, Julian Photosynthesis Research, Vol. 88, Issue 1 https://doi.org/10.1007/s11120-005-9032-x	journal	February 2006
On-line mass spectrometry: membrane inlet sampling Beckmann, Katrin; Messinger, Johannes; Badger, Murray Ronald Photosynthesis Research, Vol. 102, Issue 2-3 https://doi.org/10.1007/s11120-009-9474-7	journal	August 2009
Site-directed mutagenesis of Lys ⁶⁰⁰ in phospho enol pyruvate carboxylase of Flaveria trinervia : its roles in catalytic and regulatory functions Gao, Y.; Woo, K. C. FEBS Letters, Vol. 375, Issue 1-2 https://doi.org/10.1016/0014-5793(95)01189-L	journal	November 1995
Control of Photosynthesis in Amaranthus edulis Mutants with Reduced Amounts of PEP Carboxylase Dever, Louisa V.; Bailey, Karen J.; Leegood, Richard C. Functional Plant Biology, Vol. 24, Issue 4 https://doi.org/10.1071/PP97008	journal	January 1997
Greater efficiency of photosynthetic carbon fixation due to single amino-acid substitution Paulus, Judith Katharina; Schlieper, Daniel; Groth, Georg Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms2504	journal	February 2013
The Role of Phospho enol pyruvate Carboxylase during C ₄ Photosynthetic Isotope Exchange and Stomatal Conductance Cousins, Asaph B.; Baroli, Irene; Badger, Murray R. Plant Physiology, Vol. 145, Issue 3 https://doi.org/10.1104/pp.107.103390	journal	September 2007
Positive selection of Kranz and non-Kranz C4 phosphoenolpyruvate carboxylase amino acids in Suaedoideae (Chenopodiaceae) Rosnow, Josh J.; Edwards, Gerald E.; Roalson, Eric H. Journal of Experimental Botany, Vol. 65, Issue 13 https://doi.org/10.1093/jxb/eru053	journal	March 2014
Light/dark modulation of phosphoenolpyruvate carboxylase in C3 and C4 species Gupta, Sanjay K.; Ku, Maurice S. B.; Lin, Jenq-Horng Photosynthesis Research, Vol. 42, Issue 2 https://doi.org/10.1007/BF02187124	journal	November 1994
Evolution of C4 Phosphoenolpyruvate Carboxylase. Genes and Proteins: a Case Study with the Genus Flaveria Westhoff, P. Annals of Botany, Vol. 93, Issue 1 https://doi.org/10.1093/aob/mch003	journal	January 2004
In Vitro Phosphorylation of Maize Leaf Phosphoenolpyruvate Carboxylase Budde, Raymond J. A.; Chollet, Raymond Plant Physiology, Vol. 82, Issue 4 https://doi.org/10.1104/pp.82.4.1107	journal	December 1986
An efficient method for the determination of K m values for HCO 3 - of phosphoenolpyruvate carboxylase Bauwe, H. Planta, Vol. 169, Issue 3 https://doi.org/10.1007/BF00392131	journal	November 1986
Identification of substrate and effector binding sites of phosphoenolpyruvate carboxylase from Crassula argentea. A possible role of phosphoenolpyruvate as substrate and activator. Rustin, P.; Meyer, C. R.; Wedding, R. T. Journal of Biological Chemistry, Vol. 263, Issue 33 https://doi.org/10.1016/S0021-9258(19)77879-X	journal	November 1988
Species Having C ₄ Single-Cell-Type Photosynthesis in the Chenopodiaceae Family Evolved a Photosynthetic Phospho enol pyruvate Carboxylase Like That of Kranz-Type C ₄ Species Lara, María Valeria; Chuong, Simon D. X.; Akhani, Hossein Plant Physiology, Vol. 142, Issue 2 https://doi.org/10.1104/pp.106.085829	journal	August 2006
Illumination Increases the Affinity of Phosphoenolpyruvate Carboxylase to Bicarbonate in Leaves of a C4 Plant, Amaranthus hypochondriacus Parvathi, K.; Bhagwat, A. S.; Ueno, Y. Plant and Cell Physiology, Vol. 41, Issue 8 https://doi.org/10.1093/pcp/pcd012	journal	August 2000
C4 photosynthesis: a unique elend of modified biochemistry, anatomy and ultrastructure Hatch, Marshall D. Biochimica et Biophysica Acta (BBA) - Reviews on Bioenergetics, Vol. 895, Issue 2 https://doi.org/10.1016/S0304-4173(87)80009-5	journal	January 1987
Site-directed mutagenesis of Flaveria trinervia phospho enol pyruvate carboxylase: Arg ⁴⁵⁰ and Arg ⁷⁶⁷ are essential for catalytic activity and Lys ⁸²⁹ affects substrate binding Gao, Y.; Woo, K. C. FEBS Letters, Vol. 392, Issue 3 https://doi.org/10.1016/0014-5793(96)00832-0	journal	September 1996
Kranz and single-cell forms of C ₄ plants in the subfamily Suaedoideae show kinetic C ₄ convergence for PEPC and Rubisco with divergent amino acid substitutions Rosnow, Josh J.; Evans, Marc A.; Kapralov, Maxim V. Journal of Experimental Botany, Vol. 66, Issue 22 https://doi.org/10.1093/jxb/erv431	journal	September 2015
Evolution of C ₄ phosphoenolpyruvate carboxylase in Flaveria: determinants for high tolerance towards the inhibitor L-malate Jacobs, Bianca; Engelmann, Sascha; Westhoff, Peter Plant, Cell & Environment, Vol. 31, Issue 6 https://doi.org/10.1111/j.1365-3040.2008.01796.x	journal	June 2008
The efficiency of C ₄ photosynthesis under low light conditions in Zea mays , Miscanthus x giganteus and Flaveria bidentis : Efficiency of light-limited C Ubierna, Nerea; Sun, Wei; Kramer, David M. Plant, Cell & Environment, Vol. 36, Issue 2 https://doi.org/10.1111/j.1365-3040.2012.02579.x	journal	August 2012
The fine control of cytosolic pH Davies, D. D. Physiologia Plantarum, Vol. 67, Issue 4 https://doi.org/10.1111/j.1399-3054.1986.tb05081.x	journal	August 1986
Cloning, Expression, and Characterization of a Root-Form Phosphoenolpyruvate Carboxylase from Zea mays: Comparison with the C4-Form Enzyme Dong, L. -Y.; Masuda, T.; Kawamura, T. Plant and Cell Physiology, Vol. 39, Issue 8 https://doi.org/10.1093/oxfordjournals.pcp.a029446	journal	August 1998
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Bradford, Marion M. Analytical Biochemistry, Vol. 72, Issue 1-2 https://doi.org/10.1016/0003-2697(76)90527-3	journal	May 1976
The Functional Organization and Control of Plant Respiration Plaxton, William C.; Podestá, Florencio E. Critical Reviews in Plant Sciences, Vol. 25, Issue 2 https://doi.org/10.1080/07352680600563876	journal	May 2006
Two independent C ₄ origins in Aristidoideae (Poaceae) revealed by the recruitment of distinct phosphoenolpyruvate carboxylase genes Christin, Pascal-Antoine; Besnard, Guillaume American Journal of Botany, Vol. 96, Issue 12 https://doi.org/10.3732/ajb.0900111	journal	December 2009
Control of C4 photosynthesis: effects of reduced activities of phosphoenolpyruvate carboxylase on CO2 assimilation in Amaranthus edulis L. Bailey, Karen J.; Battistelli, Alberto; Dever, Louisa V. Journal of Experimental Botany, Vol. 51, Issue suppl_1 https://doi.org/10.1093/jexbot/51.suppl_1.339	journal	February 2000
The non-photosynthetic phosphoenolpyruvate carboxylases of the C4 dicot Flaveria trinervia - implications for the evolution of C4 photosynthesis Bläsing, Oliver; Ernst, Karin; Streubel, Monika Planta, Vol. 215, Issue 3 https://doi.org/10.1007/s00425-002-0757-x	journal	July 2002
Biochemical Models of Leaf Photosynthesis von Caemmerer, S. https://doi.org/10.1071/9780643103405	book	January 2000
Evolution of the Enzymatic Characteristics of C4Phosphoenol Pyruvate Carboxylase. A Comparison of the Orthologous Ppca Phosphoenol Pyruvate Carboxylases of Flaveria Trinervia (C4) and Flaveria Pringlei (C3) Svensson, Per; Biasing, Oliver Ernst; Westhoff, Peter European Journal of Biochemistry, Vol. 246, Issue 2 https://doi.org/10.1111/j.1432-1033.1997.t01-1-00452.x	journal	June 1997
The kinetics of ribulose-1,5-bisphosphate carboxylase/oxygenase in vivo inferred from measurements of photosynthesis in leaves of transgenic tobacco von Caemmerer, Susanne; Evans, John R.; Hudson, Graham S. Planta, Vol. 195, Issue 1 https://doi.org/10.1007/BF00206296	journal	November 1994
Resolving the Activation Site of Positive Regulators in Plant Phosphoenolpyruvate Carboxylase Schlieper, Daniel; Förster, Kerstin; Paulus, Judith K. Molecular Plant, Vol. 7, Issue 2 https://doi.org/10.1093/mp/sst130	journal	February 2014
Phosphoenolpyruvate carboxylase: three-dimensional structure and molecular mechanisms Kai, Yasushi; Matsumura, Hiroyoshi; Izui, Katsura Archives of Biochemistry and Biophysics, Vol. 414, Issue 2 https://doi.org/10.1016/S0003-9861(03)00170-X	journal	June 2003
Evolution of C4 phosphoenolpyruvate carboxylase in Flaveria-a conserved serine residue in the carboxyterminal part of the enzyme is a major determinant for C4-specific characteristics Blasing, O. E. Journal of Biological Chemistry https://doi.org/10.1074/jbc.M909832199	journal	June 2000
Evolution of C4 phosphoenolpyruvate carboxylase in the genus Alternanthera: gene families and the enzymatic characteristics of the C4 isozyme and its orthologues in C3 and C3/C4 Alternantheras Gowik, U.; Engelmann, S.; Bläsing, O. E. Planta, Vol. 223, Issue 2 https://doi.org/10.1007/s00425-005-0085-z	journal	September 2005
C4 Photosynthesis Evolved in Grasses via Parallel Adaptive Genetic Changes Christin, Pascal-Antoine; Salamin, Nicolas; Savolainen, Vincent Current Biology, Vol. 17, Issue 14 https://doi.org/10.1016/j.cub.2007.06.036	journal	July 2007
Inhibition of phosphoenolpyruvate carboxylase from C ₄ plants by malate and aspartate Huber, S. C.; Edwards, G. E. Canadian Journal of Botany, Vol. 53, Issue 17 https://doi.org/10.1139/b75-216	journal	September 1975
cis -Regulatory Elements for Mesophyll-Specific Gene Expression in the C ₄ Plant Flaveria trinervia , the Promoter of the C ₄ Phosphoenolpyruvate Carboxylase Gene Gowik, Udo; Burscheidt, Janet; Akyildiz, Meryem The Plant Cell, Vol. 16, Issue 5 https://doi.org/10.1105/tpc.019729	journal	April 2004
A kinetic investigation of phosphoenolpyruvate carboxylase from Zea mays Janc, James W.; O'Leary, Marion H.; Cleland, W. W. Biochemistry, Vol. 31, Issue 28 https://doi.org/10.1021/bi00143a009	journal	July 1992
Phospho enol pyruvate Carboxylase Activity and Concentration in the Endosperm of Developing and Germinating Castor Oil Seeds Sangwan, Rajender S.; Singh, Neelam; Plaxton, William C. Plant Physiology, Vol. 99, Issue 2 https://doi.org/10.1104/pp.99.2.445	journal	June 1992
An engineered phosphoenolpyruvate carboxylase redirects carbon and nitrogen flow in transgenic potato plants Rademacher, Thomas; Häusler, Rainer E.; Hirsch, Heinz-Josef The Plant Journal, Vol. 32, Issue 1 https://doi.org/10.1046/j.1365-313X.2002.01397.x	journal	October 2002
Regulation of photosynthetic carbon assimilation in leaves of C3–C4 intermediate species of Moricandia and Flaveria Leegood, Richard C.; von Caemmerer, Susanne Planta, Vol. 192, Issue 2 https://doi.org/10.1007/bf00194457	journal	January 1994
Homologous genes for the C4 isoform of phosphoenolpyruvate carboxylase in a C3 and a C4 Flaveria species Hermans, Jürgen; Westhoff, Peter Molecular and General Genetics MGG, Vol. 234, Issue 2 https://doi.org/10.1007/bf00283848	journal	August 1992
Kinetic evidence of the existence of a regulatory phosphoenolpyruvate binding site in maize leaf phosphoenolpyruvate carboxylase Rodríguez-Sotres, Rogelio; Muñoz-Clares, Rosario A. Archives of Biochemistry and Biophysics, Vol. 276, Issue 1 https://doi.org/10.1016/0003-9861(90)90025-t	journal	January 1990
C4 Photosynthesis: Convergence upon Convergence upon… Roalson, Eric H. Current Biology, Vol. 17, Issue 17 https://doi.org/10.1016/j.cub.2007.07.004	journal	September 2007
Serine 774 and amino acids 296 to 437 comprise the major C4 determinants of the C4 phospho enol pyruvate carboxylase of Flaveria trinervia Engelmann, Sascha; Bläsing, Oliver E.; Westhoff, Peter FEBS Letters, Vol. 524, Issue 1-3 https://doi.org/10.1016/s0014-5793(02)02975-7	journal	July 2002
Studies of the allosteric properties of maize leaf phosphoenolpyruvate carboxylase with the phosphoenolpyruvate analog phosphomycin as activator Mújica-Jiménez, Carlos; Castellanos-Martı́nez, A.; Muñoz-Clares, R. A. Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, Vol. 1386, Issue 1 https://doi.org/10.1016/s0167-4838(98)00093-4	journal	July 1998
Both rubisco and phosphoenolpyruvate carboxylase are beneficial for stomatal function in epidermal strips of Commelina benghalensis Parvathi, K.; Raghavendra, A. S. Plant Science, Vol. 124, Issue 2 https://doi.org/10.1016/s0168-9452(97)04601-3	journal	May 1997
Molecular Evolution of C4 Phosphoenolpyruvate Carboxylase in the Genus Flaveria Westhoff, Peter; Svensson, Per; Ernst, Karin Functional Plant Biology, Vol. 24, Issue 4 https://doi.org/10.1071/pp97006	journal	January 1997
Maize C4 photosynthesis involves differential regulation of phosphoenolpyruvate carboxylase genes Schaffner, Anton R.; Sheen, Jen The Plant Journal, Vol. 2, Issue 2 https://doi.org/10.1111/j.1365-313x.1992.00221.x	journal	March 1992

Similar Records

Environmental effects on photorespiration of C sub 3 -C sub 4 species. I. Influence of CO sub 2 and O sub 2 during growth on photorespiratory characteristics and leaf anatomy. [Flaveria pringlei; Flaveria flroidana; Flaveria trinervia; Panicum milloides; Panicum laxum]

Journal Article · Sat Jul 01 00:00:00 EDT 1989 · Plant Physiology; (USA) · OSTI ID:1610566

Byrd, G T; Brown, R H

Photosynthetic induction in a C/sub 4/ dicot, Flaveria trinervia. II. Metabolism of products of /sup 14/CO/sub 2/ fixation after different illumination times

Journal Article · Sun Jun 01 00:00:00 EDT 1986 · Plant Physiol.; (United States) · OSTI ID:1610566

Moore, B D; Edwards, G E

Photosynthetic metabolism of malate and aspartate in Flaveria trinervia a C/sub 4/ dicot

Thesis/Dissertation · Wed Jan 01 00:00:00 EST 1986 · OSTI ID:1610566

Moore, B A

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
plant sciences
bicarbonate kinetics
C4 photosynthesis
membrane-inlet mass spectrometry
phosphoenolpyruvate carboxylase

Title: A single serine to alanine substitution decreases bicarbonate affinity of phosphoenolpyruvate carboxylase in C4Flaveria trinervia

Citation Formats

References (55)

Similar Records

Related Subjects

Title: A single serine to alanine substitution decreases bicarbonate affinity of phosphoenolpyruvate carboxylase in C₄Flaveria trinervia