Kinetic variation in grass phosphoenolpyruvate carboxylases provides opportunity to enhance C
C4 photosynthesis
phosphoenolpyruvate carboxylase
plant biochemistry
plant biology
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
03 2021
03 2021
Historique:
revised:
11
12
2020
received:
03
07
2020
accepted:
15
12
2020
pubmed:
22
12
2020
medline:
31
7
2021
entrez:
21
12
2020
Statut:
ppublish
Résumé
The high rates of photosynthesis and the carbon-concentrating mechanism (CCM) in C
Substances chimiques
Plant Proteins
0
Carbon Dioxide
142M471B3J
Phosphoenolpyruvate Carboxylase
EC 4.1.1.31
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
1677-1688Informations de copyright
© 2020 Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Alonso-Cantabrana, H., Cousins, A.B., Danila, F., Ryan, T., Sharwood, R.E., von Caemmerer, S. and Furbank, R.T. (2018) Diffusion of CO2 across the mesophyll-bundle sheath cell interface in a C4 plant with genetically reduced PEP carboxylase activity. Plant Physiol. 178, 72-81.
Ausenhus, S.L. and O’Leary, M.H. (1992) Hydrolysis of phosphoenolpyruvate catalyzed by phosphoenolpyruvate carboxylase from Zea mays. Biochemistry, 31, 6427-6431.
Bar-Even, A., Noor, E., Savir, Y., Liebermeister, W., Davidi, D., Tawfik, D.S. and Milo, R. (2011) The moderately efficient enzyme: evolutionary and physicochemical trends shaping enzyme parameters. Biochemistry, 50, 4402-4410.
Bauwe, H. (1986) An efficient method for the determination of Km values for HCO3− of phosphoenolpyruvate carboxylase. Planta, 169, 356-360.
Bläsing, O.E., Ernst, K., Streubel, M., Westhoff, P. and Svensson, P. (2002) The non-photosynthetic phosphoenolpyruvate carboxylases of the C4 dicot Flaveria trinervia - implications for the evolution of C4 photosynthesis. Planta, 215, 448-456.
Bläsing, O.E., Westhoff, P. and Svensson, P. (2000) Evolution of C4 phosphoenolpyruvate carboxylase in Flaveria, a conserved serine residue in the carboxyl-terminal part of the enzyme is a major determinant for C4-specific characteristics. J. Biol. Chem. 275, 27917-27923.
Boyd, R.A., Gandin, A. and Cousins, A.B. (2015) Temperature responses of C4 photosynthesis: biochemical analysis of rubisco, phosphoenolpyruvate carboxylase, and carbonic anhydrase in Setaria viridis. Plant Physiol. 169, 1850-1861.
Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
Bray, N.L., Pimentel, H., Melsted, P. and Pachter, L. (2016) Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 34, 525-527.
Britto, D.T. and Kronzucker, H.J. (2005) Nitrogen acquisition, PEP carboxylase, and cellular pH homeostasis: new views on old paradigms. Plant Cell Environ. 28, 1396-1409.
Brown, R.H. (1999) Agronomic implications of C4 photosynthesis. In: C4 Plant Biology. Physiological Ecology (Sage, R.F. and Monson, R.K., eds). San Diego: Academic Press, pp. 473-507.
Budde, R.J.A. and Chollet, R. (1986) In vitro phosphorylation of maize leaf phosphoenolpyruvate carboxylase. Plant Physiol. 82, 1107-1114.
Cabido, M., Pons, E., Cantero, J.J., Lewis, J.P. and Anton, A. (2008) Photosynthetic pathway variation among C4 grasses along a precipitation gradient in Argentina. J. Biogeogr. 35, 131-140.
Cano, F.J., Sharwood, R.E., Cousins, A.B. and Ghannoum, O. (2019) The role of leaf width and conductances to CO2 in determining water use efficiency in C4 grasses. New Phytol. 223, 1280-1295.
Chen, Z., Bommareddy, R.R., Frank, D., Rappert, S. and Zeng, A.-P. (2014) Deregulation of feedback inhibition of phosphoenolpyruvate carboxylase for improved lysine production in Corynebacterium glutamicum. Appl. Environ. Microbiol. 80, 1388-1393.
Christin, P.-A., Sage, T.L., Edwards, E.J., Ogburn, R.M., Khoshravesh, R. and Sage, R.F. (2011) Complex evolutionary transitions and the significance of C3-C4 intermediate forms of photosynthesis in Molluginaceae. Evolution, 65, 643-660.
Christin, P.-A., Salamin, N., Savolainen, V., Duvall, M.R. and Besnard, G. (2007) C4 photosynthesis evolved in grasses via parallel adaptive genetic changes. Curr. Biol. 17, 1241-1247.
Cousins, A.B., Baroli, I., Badger, M.R., Ivakov, A., Lea, P.J., Leegood, R.C. and von Caemmerer, S. (2007) The role of phosphoenolpyruvate carboxylase during C4 photosynthetic isotope exchange and stomatal conductance. Plant Physiol. 145, 1006-1017.
Davies, D.D. (1986) The fine control of cytosolic pH. Physiol. Plant. 67, 702-706.
DiMario, R.J. and Cousins, A.B. (2019) A single serine to alanine substitution decreases bicarbonate affinity of phosphoenolpyruvate carboxylase in C4 Flaveria trinervia. J. Exp. Bot. 70, 995-1004.
Edwards, E.J. and Smith, S.A. (2010) Phylogenetic analyses reveal the shady history of C4 grasses. Proc. Natl Acad. Sci. USA, 107, 2532-2537.
Ehleringer, J.R., Cerling, T.E. and Helliker, B.R. (1997) C4 photosynthesis, atmospheric CO2, and climate. Oecologia, 112, 285-299.
Ehleringer, J.R. and Monson, R.K. (1993) Evolutionary and ecological aspects of photosynthetic pathway variation. Annu. Rev. Ecol. Evol. Syst. 24, 411-439.
Ellis, R.P., Vogel, J.C. and Fuls, A. (1980) Photosynthetic pathways and the geographical distribution of grasses in South West Africa/Namibia. S. Afr. J. Sci. 61, 307-314.
Engelmann, S., Bläsing, O.E., Westhoff, P. and Svensson, P. (2002) Serine 774 and amino acids 296 to 437 comprise the major C4 determinants of the C4 phosphoenolpyruvate carboxylase of Flaveria trinervia. FEBS Lett. 524, 11-14.
Fox, J. and Weisberg, S. (2019) An R Companion to Applied Regression, 3rd edn. Thousand Oaks CA: Sage [Accessed April 28, 2020].
Gao, Y. and Woo, K.C. (1996) Site-directed mutagenesis of Flaveria trinervia phosphoenolpyruvate carboxylase: Arg450 and Arg767 are essential for catalytic activity and Lys829 affects substrate binding. FEBS Lett. 392, 285-288.
Gao, Y. and Woo, K.C. (1995) Site-directed mutagenesis of Lys600 in phosphoenolpyruvate carboxylase of Flaveria trinervia: its roles in catalytic and regulatory functions. FEBS Lett. 375, 95-98.
GBIF.org. (2019) GBIF Home Page. Available from: https://www.gbif.org [Accessed October 21, 2019].
Gibson, D.G., Young, L., Chuang, R.-Y., Venter, J.C., Hutchison, C.A. and Smith, H.O. (2009) Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods, 6, 343-345.
González-Segura, L., Mújica-Jiménez, C., Juárez-Díaz, J.A., Güémez-Toro, R., Martinez-Castilla, L.P. and Muñoz-Clares, R.A. (2018) Identification of the allosteric site for neutral amino acids in the maize C4 isozyme of phosphoenolpyruvate carboxylase: the critical role of Ser-100. J. Biol. Chem. 293, 9945-9957.
Goodstein, D.M., Shu, S., Howson, R. et al. (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 40, D1178-D1186.
Gowik, U., Burscheidt, J., Akyildiz, M., Schlue, U., Koczor, M., Streubel, M. and Westhoff, P. (2004) cis-Regulatory elements for mesophyll-specific gene expression in the C4 plant Flaveria trinervia, the promoter of the C4 phosphoenolpyruvate carboxylase gene. Plant Cell, 16, 1077-1090.
Gowik, U., Engelmann, S., Bläsing, O.E., Raghavendra, A.S. and Westhoff, P. (2006) 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. Planta, 223, 359-368.
Gowik, U. and Westhoff, P. (2011) The Path from C3 to C4 Photosynthesis. Plant Physiol. 155, 56-63.
Grabherr, M.G., Haas, B.J., Yassour, M. et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644-652.
Grass Phylogeny Working Group II. (2012) New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins. New Phytol. 193, 304-312.
Harris, R.S. (2007) Improved pairwise alignment of genomic DNA. Available from: https://etda.libraries.psu.edu/catalog/7971 [Accessed May 18, 2020].
Hatch, M.D. (1987) C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochim. Biophys. Acta. Rev. Bioenerget. 895, 81-106.
Hermans, J. and Westhoff, P. (1992) Homologous genes for the C4 isoform of phosphoenolpyruvate carboxylase in a C3 and a C4 Flaveria species. Molec. Gen. Genet. 234, 275-284.
Hijmans, R.J. and van Etten, J. (2012) Geographic analysis and modeling with raster data. R Package Version 2, 1-25.
Izui, K., Matsumura, H., Furumoto, T. and Kai, Y. (2004) PHOSPHOENOLPYRUVATE CARBOXYLASE: a new era of structural biology. Annu. Rev. Plant Biol. 55, 69-84.
Jacobs, B., Engelmann, S., Westhoff, P. and Gowik, U. (2008) Evolution of C4 phosphoenolpyruvate carboxylase in Flaveria: determinants for high tolerance towards the inhibitor L-malate. Plant Cell Environ. 31, 793-803.
Kai, Y., Matsumura, H., Inoue, T., Terada, K., Nagara, Y., Yoshinaga, T., Kihara, A., Tsumura, K. and Izui, K. (1999) Three-dimensional structure of phosphoenolpyruvate carboxylase: a proposed mechanism for allosteric inhibition. Proc. Natl Acad. Sci. USA, 96, 823-828.
Kai, Y., Matsumura, H. and Izui, K. (2003) Phosphoenolpyruvate carboxylase: three-dimensional structure and molecular mechanisms. Arch. Biochem. Biophys. 414, 170-179.
Laforest, M., Soufiane, B., Simard, M.-J., Obeid, K., Page, E. and Nurse, R.E. (2017) Acetyl-CoA carboxylase overexpression in herbicide-resistant large crabgrass (Digitaria sanguinalis). Pest Manag. Sci. 73, 2227-2235.
Lara, M.V., Chuong, S.D.X., Akhani, H., Andreo, C.S. and Edwards, G.E. (2006) Species having C4 single-cell-type photosynthesis in the Chenopodiaceae family evolved a photosynthetic phosphoenolpyruvate carboxylase like that of Kranz-type C4 species. Plant Physiol. 142, 673-684.
Leegood, R.C. and von Caemmerer, S. (1989) Some relationships between contents of photosynthetic intermediates and the rate of photosynthetic carbon assimilation in leaves of Zea mays L. Planta, 178, 258-266.
Leegood, R.C. and von Caemmerer, S. (1988) The relationship between contents of photosynthetic metabolites and the rate of photosynthetic carbon assimilation in leaves of Amaranthus edulis L. Planta, 174, 253-262.
Moody, N.R., Christin, P.-A. and Reid, J.D. (2020) Kinetic Modifications of C4 PEPC Are Qualitatively Convergent, but Larger in Panicum Than in Flaveria. Front. Plant Sci. 11, 1-11.
Ogle, D.H., Wheeler, P. and Dinno, A. (2020) FSA: Fisheries Stock Analysis. Available from: https://github.com/droglenc/FSA [Accessed April 28, 2020].
O’Leary, B., Park, J. and Plaxton, W.C. (2011) The remarkable diversity of plant PEPC (phosphoenolpyruvate carboxylase): recent insights into the physiological functions and post-translational controls of non-photosynthetic PEPCs. Biochem. J. 436, 15-34.
Osborne, C.P. and Freckleton, R.P. (2009) Ecological selection pressures for C4 photosynthesis in the grasses. P. Roy. Soc. B-Biol. Sci. 276, 1753-1760.
Parvathi, K., Bhagwat, A.S., Ueno, Y., Izui, K. and Raghavendra, A.S. (2000) Illumination increases the affinity of phosphoenolpyruvate carboxylase to bicarbonate in leaves of a C4 Plant, Amaranthus hypochondriacus. Plant Cell Physiol. 41, 905-910.
Parvathi, K. and Raghavendra, A.S. (1997) Both rubisco and phosphoenolpyruvate carboxylase are beneficial for stomatal function in epidermal strips of Commelina benghalensis. Plant Sci. 124, 153-157.
Pathare, V.S., Koteyeva, N. and Cousins, A.B. (2019) Increased adaxial stomatal density is associated with greater mesophyll surface area exposed to intercellular air spaces and mesophyll conductance in diverse C4 grasses. New Phytol. 225, 169-182.
Phansopa, C., Dunning, L.T., Reid, J.D. and Christin, P.-A. (2020) Lateral gene transfer acts as an evolutionary shortcut to efficient C4 biochemistry. Mol. Biol. Evol. 37, 3094-3104.
Plaxton, W.C. and Podestá, F.E. (2006) The functional organization and control of plant respiration. Crit. Rev. Plant Sci. 25, 159-198.
Rademacher, T., Häusler, R.E., Hirsch, H.-J., Zhang, L., Lipka, V., Weier, D., Kreuzaler, F. and Peterhänsel, C. (2002) An engineered phosphoenolpyruvate carboxylase redirects carbon and nitrogen flow in transgenic potato plants. Plant J. 32, 25-39.
Rosnow, J.J., Edwards, G.E. and Roalson, E.H. (2014) Positive selection of Kranz and non-Kranz C4 phosphoenolpyruvate carboxylase amino acids in Suaedoideae (Chenopodiaceae). J. Exp. Bot. 65, 3595-3607.
Rosnow, J.J., Evans, M.A., Kapralov, M.V., Cousins, A.B., Edwards, G.E. and Roalson, E.H. (2015) Kranz and single-cell forms of C4 plants in the subfamily Suaedoideae show kinetic C4 convergence for PEPC and Rubisco with divergent amino acid substitutions. J. Exp. Bot. 66, 7347-7358.
RStudio Team. (2016) RStudio: integrated development for R. Boston, MA: RStudio, Inc. Available from: http://www.rstudio.com/ [Accessed September 25, 2018].
Sabe, H., Miwa, T., Kodaki, T., Izui, K., Hiraga, S. and Katsuki, H. (1984) Molecular cloning of the phosphoenolpyruvate carboxylase gene, ppc, of Escherichia coli. Gene, 31, 279-283.
Sage, R.F., Christin, P.-A. and Edwards, E.J. (2011) The C4 plant lineages of planet Earth. J. Exp. Bot. 62, 3155-3169.
Sage, R.F., Wedin, D.A. and Li, M. (1999) 10 - The biogeography of C4 photosynthesis: patterns and controlling factors. In: C4 Plant Biology. Physiological Ecology (Sage, R.F. and Monson, R.K., eds). San Diego: Academic Press, pp. 313-373.
Sangwan, R.S., Singh, N. and Plaxton, W.C. (1992) Phosphoenolpyruvate carboxylase activity and concentration in the endosperm of developing and germinating castor oil seeds. Plant Physiol. 99, 445-449.
Sievers, F., Wilm, A., Dineen, D. et al. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539.
Svensson, P., Biasing, O.E. and Westhoff, P. (1997) Evolution of the enzymatic characteristics of C4 phosphoenolpyruvate carboxylase. Eur. J. Biochem. 246, 452-460.
Taub, D.R. (2000) Climate and the U.S. distribution of C4 grass subfamilies and decarboxylation variants of C4 photosynthesis. Am. J. Bot. 87, 1211-1215.
Tholen, D. and Zhu, X.-G. (2011) The mechanistic basis of internal conductance: a theoretical analysis of mesophyll cell photosynthesis and CO2 diffusion. Plant Physiol. 156, 90-105.
Ubierna, N., Sun, W., Kramer, D.M. and Cousins, A.B. (2013) The efficiency of C4 photosynthesis under low light conditions in Zea mays, Miscanthus × giganteus and Flaveria bidentis. Plant Cell Environ. 36, 365-381.
von Caemmerer, S., Evans, J.R., Hudson, G.S. and Andrews, T.J. (1994) The kinetics of ribulose-1,5-bisphosphate carboxylase/oxygenase in vivo inferred from measurements of photosynthesis in leaves of transgenic tobacco. Planta, 195, 88-97.
von Caemmerer, S. and Furbank, R.T. (2003) The C4 pathway: an efficient CO2 pump. Photosynth. Res. 77, 191.
von Caemmerer, S. (2000) Biochemical Models of Leaf Photosynthesis. Collingwood: Csiro Publishing.
Washburn, J.D., Schnable, J.C., Conant, G.C., Brutnell, T.P., Shao, Y., Zhang, Y., Ludwig, M., Davidse, G. and Pires, J.C. (2017) Genome-guided phylo-transcriptomic methods and the nuclear phylogenetic tree of the Paniceae grasses. Sci. Rep. 7, 13528.
Westhoff, P. and Gowik, U. (2004) Evolution of C4 phosphoenolpyruvate carboxylase. Genes and proteins: a case study with the genus Flaveria. Ann. Bot. 93, 13-23.
Westhoff, P., Svensson, P., Ernst, K., Bläsing, O., Burscheidt, J. and Stockhaus, J. (1997) Molecular evolution of C4 phosphoenolpyruvate carboxylase in the genus Flaveria. Funct. Plant Biol. 24, 429-436.
Williams, B.P., Aubry, S. and Hibberd, J.M. (2012) Molecular evolution of genes recruited into C4 photosynthesis. Trends Plant Sci. 17, 213-220.
WorldClim Global Climate Data. Free climate data for ecological modeling and GIS. Available from: http://www.worldclim.org/ [Accessed October 17, 2019].
Yuan, J., Sayegh, J., Mendez, J., Sward, L., Sanchez, N., Sanchez, S., Waldrop, G. and Grover, S. (2006) The regulatory role of residues 226-232 in phosphoenolpyruvate carboxylase from maize. Photosynth. Res. 88, 73-81.