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Greater efficiency of photosynthetic carbon fixation due to single amino-acid substitution.

Paulus JK, Schlieper D, Groth G
Nat Commun 4 1518 (2013)
Cited: 44 times
EuropePMC logo PMID: 23443546

Abstract

The C4-photosynthetic carbon cycle is an elaborated addition to the classical C3-photosynthetic pathway, which improves solar conversion efficiency. The key enzyme in this pathway, phosphoenolpyruvate carboxylase, has evolved from an ancestral non-photosynthetic C3 phosphoenolpyruvate carboxylase. During evolution, C4 phosphoenolpyruvate carboxylase has increased its kinetic efficiency and reduced its sensitivity towards the feedback inhibitors malate and aspartate. An open question is the molecular basis of the shift in inhibitor tolerance. Here we show that a single-point mutation is sufficient to account for the drastic differences between the inhibitor tolerances of C3 and C4 phosphoenolpyruvate carboxylases. We solved high-resolution X-ray crystal structures of a C3 phosphoenolpyruvate carboxylase and a closely related C4 phosphoenolpyruvate carboxylase. The comparison of both structures revealed that Arg884 supports tight inhibitor binding in the C3-type enzyme. In the C4 phosphoenolpyruvate carboxylase isoform, this arginine is replaced by glycine. The substitution reduces inhibitor affinity and enables the enzyme to participate in the C4 photosynthesis pathway.

Articles - 3zgb mentioned but not cited (6)

  1. Greater efficiency of photosynthetic carbon fixation due to single amino-acid substitution. Paulus JK, Schlieper D, Groth G. Nat Commun 4 1518 (2013)
  2. Positive selection of Kranz and non-Kranz C4 phosphoenolpyruvate carboxylase amino acids in Suaedoideae (Chenopodiaceae). Rosnow JJ, Edwards GE, Roalson EH. J Exp Bot 65 3595-3607 (2014)
  3. Chalcone-based Selective Inhibitors of a C4 Plant Key Enzyme as Novel Potential Herbicides. Nguyen GT, Erlenkamp G, Jäck O, Küberl A, Bott M, Fiorani F, Gohlke H, Groth G. Sci Rep 6 27333 (2016)
  4. Identification of the allosteric site for neutral amino acids in the maize C4 isozyme of phosphoenolpyruvate carboxylase: The critical role of Ser-100. González-Segura L, Mújica-Jiménez C, Juárez-Díaz JA, Güémez-Toro R, Martinez-Castilla LP, Muñoz-Clares RA. J Biol Chem 293 9945-9957 (2018)
  5. Efficient In Vivo Screening Method for the Identification of C4 Photosynthesis Inhibitors Based on Cell Suspensions of the Single-Cell C4 Plant Bienertia sinuspersici. Minges A, Janßen D, Offermann S, Groth G. Front Plant Sci 10 1350 (2019)
  6. Convergent molecular evolution of phosphoenolpyruvate carboxylase gene family in C4 and crassulacean acid metabolism plants. Shu JP, Yan YH, Wang RJ. PeerJ 10 e12828 (2022)


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  2. Microbial Utilization of Next-Generation Feedstocks for the Biomanufacturing of Value-Added Chemicals and Food Ingredients. Zhang C, Ottenheim C, Weingarten M, Ji L. Front Bioeng Biotechnol 10 874612 (2022)

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  3. Exploiting the Genetic Diversity of Maize Using a Combined Metabolomic, Enzyme Activity Profiling, and Metabolic Modeling Approach to Link Leaf Physiology to Kernel Yield. Cañas RA, Yesbergenova-Cuny Z, Simons M, Chardon F, Armengaud P, Quilleré I, Cukier C, Gibon Y, Limami AM, Nicolas S, Brulé L, Lea PJ, Maranas CD, Hirel B. Plant Cell 29 919-943 (2017)
  4. New evidence for grain specific C4 photosynthesis in wheat. Rangan P, Furtado A, Henry RJ. Sci Rep 6 31721 (2016)
  5. Allosteric Inhibition of Phosphoenolpyruvate Carboxylases is Determined by a Single Amino Acid Residue in Cyanobacteria. Takeya M, Hirai MY, Osanai T. Sci Rep 7 41080 (2017)
  6. Evolution of the Phosphoenolpyruvate Carboxylase Protein Kinase Family in C3 and C4 Flaveria spp. Aldous SH, Weise SE, Sharkey TD, Waldera-Lupa DM, Stühler K, Mallmann J, Groth G, Gowik U, Westhoff P, Arsova B. Plant Physiol 165 1076-1091 (2014)
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  8. Targeted Enrichment of Large Gene Families for Phylogenetic Inference: Phylogeny and Molecular Evolution of Photosynthesis Genes in the Portullugo Clade (Caryophyllales). Moore AJ, Vos JM, Hancock LP, Goolsby E, Edwards EJ. Syst Biol 67 367-383 (2018)
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  14. Recurrent sequence evolution after independent gene duplication. A von der Dunk SH, Snel B. BMC Evol Biol 20 98 (2020)
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  16. The coordination of major events in C4 photosynthesis evolution in the genus Flaveria. Lyu MA, Gowik U, Kelly S, Covshoff S, Hibberd JM, Sage RF, Ludwig M, Wong GK, Westhoff P, Zhu XG. Sci Rep 11 15618 (2021)
  17. Hydrogen peroxide regulated photosynthesis in C4-pepc transgenic rice. Ren CG, Li X, Liu XL, Wei XD, Dai CC. Plant Physiol Biochem 74 218-229 (2014)
  18. Kinetic Modifications of C4 PEPC Are Qualitatively Convergent, but Larger in Panicum Than in Flaveria. Moody NR, Christin PA, Reid JD. Front Plant Sci 11 1014 (2020)
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  20. Anionic Phospholipids Induce Conformational Changes in Phosphoenolpyruvate Carboxylase to Increase Sensitivity to Cathepsin Proteases. Gandullo J, Monreal JA, Álvarez R, Díaz I, García-Mauriño S, Echevarría C. Front Plant Sci 10 582 (2019)
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  24. What Matters for C4 Transporters: Evolutionary Changes of Phosphoenolpyruvate Transporter for C4 Photosynthesis. Lyu MA, Wang Y, Jiang J, Liu X, Chen G, Zhu XG. Front Plant Sci 11 935 (2020)
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  27. Computational Docking Reveals Co-Evolution of C4 Carbon Delivery Enzymes in Diverse Plants. Wu C, Guo D. Int J Mol Sci 23 12688 (2022)
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  31. A Machine Learning Framework Identifies Plastid-Encoded Proteins Harboring C3 and C4 Distinguishing Sequence Information. Yogadasan N, Doxey AC, Chuong SDX. Genome Biol Evol 15 evad129 (2023)
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