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Structural Analysis of the Electron Transfer Complex Between Ferredoxin–Thioredoxin Reductase and Thioredoxin

Juniar, Linda 大阪大学 DOI:10.18910/81887

2020.12.18

概要

Plants have developed regulatory systems to survive through fluctuating light environments. For optimization of metabolic flux in the stroma under such condition, chloroplasts have to tune their metabolic reactions in a light-dependent manner. Thiol-based redox regulation is one of the mechanisms developed to control the enzymatic reactions in chloroplast. In this system, two soluble redox-mediator proteins, known as ferredoxin–thioredoxin reductase (FTR) and thioredoxin (Trx), sequentially transfer the electron from the photosynthetic electron transport chain to the target enzymes such as fructose 1,6 -bisphosphatase, NADP-malate dehydrogenase or 2-Cys peroxiredoxins.

Completion of Arabidopsis thaliana genome sequencing has indicated that 10 Trx isoforms are localized in chloroplasts and classified into five subtypes (two Trx-f, four Trx-m, one Trx-x, two Trx-y, and one Trx-z). On the other hand, the catalytic subunit of FTR is encoded by a unique gene associated with a variable subunit encoded by two genes. FTR acts as an important protein that transfers reducing equivalents from the photosynthetic electron transport chain to Trxs. Several structures of Trxs have been determined by X-ray crystallography. Despite the common Trx-fold, each Trx shows different molecular characteristics, such as the protein surface charge and midpoint redox potential (Em), leading to their differences in target and protein-protein interaction. Based on their FTR-dependent kinetic parameters, A. thaliana Trxs can be clustered into three classes: high, middle, and low efficiency group. The comparative kinetic analysis showed that the electron transfe r efficiency from FTR to Trx is not fully controlled by Em but also by other factors. To date, the three-dimensional structure of Synechocystis FTR and spinach Trx complexes have been reported. The interaction of Trx-m with FTR is similar to that of Trx-f. The conformational difference exists in small rotation angles of Trx molecule to the flat FTR molecule. Since this published FTR:Trx complex consisted of proteins from different organisms, I could not refer those non-physiological complex structures to explain the differences in FTR affinity to three classes of Trx from A. thaliana. Therefore, I focused on the physiological complex between FTR and Trx isoforms from A. thaliana. After extensive screening of crystallization, I have chosen Trx-y1, Trx-f2 and Trx-m2 as a representative for high, middle and low efficiency group, respectively.

In this research, I have successfully determined three structures of FTR:Trx protein complex; FTR:Trx-y1; FTR:Trx-f2; and FTR:Trx-m2, at 1.59 Å, 1.79 Å and 2.4 Å, respectively. FTR:Trx-f2 and FTR:Trx-m2 complexes contained Trx, catalytic and variable subunit of FTR, whereas FTR:Trx-y1 contained Trx and FTR catalytic subunit only. The overall structure of three FTR:Trx complexes was similar with the rmsd values of 0.588 Å based on the Cα atoms of FTR, and the values ranging from 1.2 to 1.5 Å based on those of Trxs. Trx molecules interacted mostly with catalytic subunit of FTR with different rotational angles of 7.9-16.1 degree in polar angle of kappa.

I performed superposition of FTR and Trx in the complex and single form to study the structural changes upon complex formation. I used Synechocystis FTR structure (PDB ID 1DJ7) for comparison with A. thaliana FTR in FTR:Trx complexes, and A. thaliana Trx-m1 (determined at 1.1 Å resolution) and spinach Trx-f (PDB ID 1FAA) for comparison with Trx in the complexes. Since there are no available structures of Trx-y monomer, I could not do the same analysis for Trx-y1. The structural comparison results showed that there were microscopic changes of FTR or Trx upon complex formation. The biggest structural differences were found in the side chain conformations located at the molecular interface.

Since the resolution of the complex structures were quite good, I comparatively studied the interaction between FTR and Trxs. The Trx molecules interact with FTR mainly through hydrophobic interactions which can be clustered into two types, common interaction for all Trx isoforms and isoform-specific peripheral interaction. The FTR:Trx-y1 complex had more isoform-specific interactions, followed by FTR:Trx-f2 and FTR:Trx-m2, which was supported by the total buried surface area of FTR:Trx-y1 around 1622 Å2 whereas Trx-f2 and Trx-m2 were 1470 Å2, and 1509 Å2, respectively. S0.5 of Trx-y1 was 10-fold smaller than that of Trx-f2, while S0.5 of Trx-m2 was not so different from that of Trx-f2. The electrostatic potential of each Trx may drive the differences in isoform-specific interaction leading to different affinity of FTR toward Trx.

Based on my determined three X-ray structures of FTR:Trxs, I have concluded that there were small but significant structural changes of FTR and Trx upon complex formation, and the number of isoform -specific interaction located peripherally is the key for the three classes of enzymatic efficiency, which may be facilitated by the differential charged surface of Trx isoforms.

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参考文献

[1] M.P. Johnson, Photosynthesis, Essays Biochem. 60 (2016) 255–273. https://doi.org/10.1042/EBC20160016.

[2] L. Michelet, M. Zaffagnini, S. Morisse, F. Sparla, M.E. Pérez-Pérez, F. Francia, A. Danon, C.H. Marchand, S. Fermani, P. Trost, S.D. Lemaire, Redox regulation of the Calvin-Benson cycle: Something old, something new, Front. Plant Sci. 4 (2013) 1–21. https://doi.org/10.3389/fpls.2013.00470.

[3] C. Spetea, E. Rintamäki, B. Schoefs, Changing the light environment: Chloroplast signalling and response mechanisms, Philos. Trans. R. Soc. B Biol. Sci. 369 (2014) 1–3. https://doi.org/10.1098/rstb.2013.0220.

[4] R.M. Larkin, Influence of plastids on light signalling and development, Philos. Trans. R. Soc. B Biol. Sci. 369 (2014). https://doi.org/10.1098/rstb.2013.0232.

[5] B.C. Tripathy, R. Oelmüller, Reactive oxygen species generation and signaling in plants, Plant Signal. Behav. 7 (2012) 1621–1633. https://doi.org/10.4161/psb.22455.

[6] H. Kirchhoff, Chloroplast ultrastructure in plants, New Phytol. 223 (2019) 565–574. https://doi.org/10.1111/nph.15730.

[7] L. Vogelsang, K.J. Dietz, Regulatory thiol oxidation in chloroplast metabolism, oxidative stress response and environmental signaling in plants, Biochem. J. 477 (2020) 1865–1878. https://doi.org/10.1042/BCJ20190124.

[8] G. Noctor, J.P. Reichheld, C.H. Foyer, ROS-related redox regulation and signaling in plants, Semin. Cell Dev. Biol. 80 (2018) 3–12. https://doi.org/10.1016/j.semcdb.2017.07.013.

[9] K.J. Dietz, Redox signal integration: From stimulus to networks and genes, Physiol. Plant. 133 (2008) 459–468. https://doi.org/10.1111/j.1399-3054.2008.01120.x.

[10] P. Schürmann, R.A. Wolosiuk, Studies on the regulatory properties of chloroplast fructose-1,6-bisphosphatase, Biochim. Biophys. Acta. 522 (1978) 130–138.

[11] C. Queiroz-Claret, J.C. Meunier, Light Activation of Sedoheptulose-1,7- Bisphosphatase by aReconstituted Thylakoid System Compared with DTT Activation. Evidence for Protein-Enzyme Interactions, J. Plant Physiol. 145 (1995) 45–49. https://doi.org/10.1016/S0176-1617(11)81844-4.

[12] B.B. Buchanan, Role of Light in the Regulation of Chloroplast Enzymes, Annu. Rev. Plant Physiol. 31 (1980) 341–374. https://doi.org/10.1146/annurev.pp.31.060180.002013.

[13] K. Yoshida, Y. Yokochi, T. Hisabori, New Light on Chloroplast Redox Regulation: Molecular Mechanism of Protein Thiol Oxidation, Front. Plant Sci. 10 (2019) 1–6. https://doi.org/10.3389/fpls.2019.01534.

[14] K.J. Dietz, R. Hell, Thiol switches in redox regulation of chloroplasts: Balancing redox state, metabolism and oxidative stress, Biol. Chem. 396 (2015) 483–494. https://doi.org/10.1515/hsz-2014-0281.

[15] K. Yoshida, T. Hisabori, Two distinct redox cascades cooperatively regulate chloroplast functions and sustain plant viability, Proc. Natl. Acad. Sci. U. S. A. 113 (2016) E3967–E3976. https://doi.org/10.1073/pnas.1604101113.

[16] S. Dai, C. Schwendtmayer, P. Schürmann, S. Ramaswamy, H. Eklund, Redox signaling in chloroplasts: Cleavage of disulfides by an iron- sulfur cluster, Science (80-. ). 287 (2000) 655–658. https://doi.org/10.1126/science.287.5453.655.

[17] E. Keryer, V. Collin, D. Lavergne, S. Lemaire, E. Issakidis-Bourguet, Characterization of Arabidopsis mutants for the variable subunit of ferredoxin:thioredoxin reductase, Photosynth. Res. 79 (2004) 265–274. https://doi.org/10.1023/B:PRES.0000017173.46185.3e.

[18] E. Gelhaye, N. Rouhier, N. Navrot, J.P. Jacquot, The plant thioredoxin system, Cell. Mol. Life Sci. 62 (2005) 24–35. https://doi.org/10.1007/s00018-004-4296-4.

[19] F.J. Cejudo, A.J. Meyer, J.P. Reichheld, N. Rouhier, J.A. Traverso, Thiol-based redox homeostasis and signaling, Front. Plant Sci. 5 (2014) 2013–2015. https://doi.org/10.3389/fpls.2014.00266.

[20] Y. Meyer, J.P. Reichheld, F. Vignols, Thioredoxins in Arabidopsis and other plants, Photosynth. Res. 86 (2005) 419–433. https://doi.org/10.1007/s11120-005-5220-y.

[21] G. Capitani, Z. Marković-Housley, G. DelVal, M. Morris, J.N. Jansonius, P. Schürmann, Crystal structures of two functionally different thioredoxins in spinach chloroplasts, J. Mol. Biol. 302 (2000) 135–154. https://doi.org/10.1006/jmbi.2000.4006.

[22] J.L. Martin, Thioredoxin -a fold for all reasons, Structure. 3 (1995) 245–250. https://doi.org/10.1016/S0969-2126(01)00154-X.

[23] S. Dai, R. Friemann, D.A. Glauser, F. Bourquin, W. Manieri, P. Schürmann, H. Eklund, Structural snapshots along the reaction pathway of ferredoxin-thioredoxin reductase, Nature. 448 (2007) 92–96. https://doi.org/10.1038/nature05937.

[24] The Arabidopsis Genome Initiative, Analysis of the genome sequence of the flowering plant Arabidopsis thaliana, Nature. 408 (2000) 796–815. https://doi.org/10.1038/35048692.

[25] K. Yoshida, T. Hisabori, Distinct electron transfer from ferredoxin-thioredoxin reductase to multiple thioredoxin isoforms in chloroplasts, Biochem. J. 474 (2017) 1347–1360. https://doi.org/10.1042/BCJ20161089.

[26] K. Chibani, L. Tarrago, P. Schürmann, J.P. Jacquot, N. Rouhier, Biochemical properties of poplar thioredoxin z, FEBS Lett. 585 (2011) 1077–1081. https://doi.org/10.1016/j.febslet.2011.03.006.

[27] Y. Meyer, F. Vignols, J.P. Reichheld, Classification of plant thioredoxins by sequence similarity and intron position, Methods Enzymol. 347 (2002) 394–402. https://doi.org/10.1016/S0076-6879(02)47039-5.

[28] V. Collin, P. Lamkemeyer, M. Miginiac-Maslow, M. Hirasawa, D.B. Knaff, K.J. Dietz, E. Issakidis-Bourguet, Characterization of plastidial thioredoxins from arabidopsis belonging to the new y-type, Plant Physiol. 136 (2004) 4088–4095. https://doi.org/10.1104/pp.104.052233.

[29] L. Nikkanen, E. Rintamäki, Thioredoxin-dependent regulatory networks in chloroplasts under fluctuating light conditions, Philos. Trans. R. Soc. B Biol. Sci. 369 (2014) 1–7. https://doi.org/10.1098/rstb.2013.0224.

[30] W. Kabsch, XDS, Acta Crystallogr. Sect. D Biol. Crystallogr. 66 (2010) 125–132. https://doi.org/10.1107/S0907444909047337.

[31] A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, R.J. Read, Phaser crystallographic software, J. Appl. Crystallogr. 40 (2007) 658–674. https://doi.org/10.1107/S0021889807021206.

[32] D. Liebschner, P. V. Afonine, M.L. Baker, G. Bunkoczi, V.B. Chen, T.I. Croll, B. Hintze, L.W. Hung, S. Jain, A.J. McCoy, N.W. Moriarty, R.D. Oeffner, B.K. Poon, M.G. Prisant, R.J. Read, J.S. Richardson, D.C. Richardson, M.D. Sammito, O. V. Sobolev, D.H. Stockwell, T.C. Terwilliger, A.G. Urzhumtsev, L.L. Videau, C.J. Williams, P.D. Adams, Macromolecular structure determination using X-rays, neutrons and electrons: Recent developments in Phenix, Acta Crystallogr. Sect. D Struct. Biol. 75 (2019) 861–877. https://doi.org/10.1107/S2059798319011471.

[33] R.A. Laskowski, M.B. Swindells, LigPlot+: multiple ligand-protein interaction diagrams for drug discovery, J. Chem. Inf. Model. 51 (2011) 2778–2786.

[34] B.W. Matthews, Solvent content of protein crystals, J. Mol. Biol. 33 (1968) 491–497. https://doi.org/10.1016/0022-2836(68)90205-2.

[35] A.J. McCoy, Acknowledging errors: Advanced molecular replacement with phaser, Methods Mol. Biol. 1607 (2017) 421–453. https://doi.org/10.1007/978-1-4939- 7000-1_18.

[36] P. Emsley, B. Lohkamp, W.G. Scott, K. Cowtan, Features and development of Coot, Acta Crystallogr. Sect. D Biol. Crystallogr. 66 (2010) 486–501. https://doi.org/10.1107/S0907444910007493.

[37] P. V. Afonine, R.W. Grosse-Kunstleve, N. Echols, J.J. Headd, N.W. Moriarty, M. Mustyakimov, T.C. Terwilliger, A. Urzhumtsev, P.H. Zwart, P.D. Adams, Towards automated crystallographic structure refinement with phenix.refine, Acta Crystallogr. Sect. D Biol. Crystallogr. 68 (2012) 352–367. https://doi.org/10.1107/S0907444912001308.

[38] S. Dai, C. Schwendtmayer, K. Johansson, S. Ramaswamy, P. Schürmann, H. Eklund, How does light regulate chloroplast enzymes? Structure-function studies of the ferredoxin/thioredoxin system, Q. Rev. Biophys. 33 (2000) 67–108. https://doi.org/10.1017/S0033583500003607.

[39] K. Yoshida, S. Hara, T. Hisabori, Thioredoxin selectivity for thiol-based redox regulation of target Proteins in Chloroplasts, J. Biol. Chem. 290 (2015) 14278– 14288. https://doi.org/10.1074/jbc.M115.647545.

[40] E. Gaymard, L. Franchini, W. Manieri, E. Stutz, P. Schürmann, A dicistronic construct for the expression of functional spinach chloroplast ferredoxin: Thioredoxin reductase in Escherichia coli, Plant Sci. 158 (2000) 107–113. https://doi.org/10.1016/S0168-9452(00)00310-1.

[41] W. Manieri, L. Franchini, L. Raeber, S. Dai, A.L. Stritt-Etter, P. Schürmann, N- terminal truncation of the variable subunit stabilizes spinach ferredoxin:Thioredoxin reductase, FEBS Lett. 549 (2003) 167–170. https://doi.org/10.1016/S0014-5793(03)00811-1.

[42] P. Wang, J. Liu, B. Liu, D. Feng, Q. Da, P. Wang, S. Shu, J. Su, Y. Zhang, J. Wang, H. Bin Wang, Evidence for a role of chloroplastic m-type thioredoxins in the biogenesis of photosystem II in arabidopsis, Plant Physiol. 163 (2013) 1710–1728. https://doi.org/10.1104/pp.113.228353.

[43] Z. Kang, T. Qin, Z. Zhao, Thioredoxins and thioredoxin reductase in chloroplasts: A review, Gene. 706 (2019) 32–42. https://doi.org/10.1016/j.gene.2019.04.041.

[44] M.D. Winn, C.C. Ballard, K.D. Cowtan, E.J. Dodson, P. Emsley, P.R. Evans, R.M. Keegan, E.B. Krissinel, A.G.W. Leslie, A. McCoy, S.J. McNicholas, G.N. Murshudov, N.S. Pannu, E.A. Potterton, H.R. Powell, R.J. Read, A. Vagin, K.S. Wilson, Overview of the CCP4 suite and current developments, Acta Crystallogr. Sect. D Biol. Crystallogr. 67 (2011) 235–242. https://doi.org/10.1107/S0907444910045749.

[45] G.M. Sheldrick, Crystal structure refinement with SHELXL, Acta Crystallogr. Sect. C Struct. Chem. 71 (2015) 3–8. https://doi.org/10.1107/S2053229614024218.

[46] E. Krissinel, K. Henrick, Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions, Acta Crystallogr. Sect. D Biol. Crystallogr. 60 (2004) 2256–2268. https://doi.org/10.1107/S0907444904026460.

[47] B. Lee, F.M. Richards, The interpretation of protein structures: Estimation of static accessibility, J. Mol. Biol. 55 (1971). https://doi.org/10.1016/0022-2836(71)90324- X.

[48] B.B. Buchanan, R.A. Wolosiuk, P. Schürmann, Thioredoxin and enzyme regulation, Trends Biochem. Sci. 4 (1979) 93–96. https://doi.org/10.1016/0968-0004(79)90191-9.

[49] Z. Kang, T. Qin, Z. Zhao, Thioredoxins and thioredoxin reductase in chloroplasts: A review, Gene. 706 (2019) 32–42. https://doi.org/10.1016/j.gene.2019.04.041.

[50] S.K. Katti, D.M. LeMaster, H. Eklund, Crystal structure of thioredoxin from Escherichia coli at 1.68 Å resolution, J. Mol. Biol. 212 (1990) 167–184. https://doi.org/10.1016/0022-2836(90)90313-B.

[51] A. Weichsel, J.R. Gasdaska, G. Powis, W.R. Montfort, Crystal structures of reduced, oxidized, and mutated human thioredoxins: Evidence for a regulatory homodimer, Structure. 4 (1996) 735–751. https://doi.org/10.1016/S0969-2126(96)00079-2.

[52] S.D. Lemaire, M. Miginiac-Maslow, The thioredoxin superfamily in Chlamydomonas reinhardtii, Photosynth. Res. 82 (2004) 203–220. https://doi.org/10.1007/s11120-004-1091-x.

[53] S.D. Lemaire, D. Tedesco, P. Crozet, L. Michelet, S. Fermani, M. Zaffagnini, J. Henri, Crystal structure of chloroplastic thioredoxin f2 from Chlamydomonas reinhardtii reveals distinct surface properties, Antioxidants. 7 (2018). https://doi.org/10.3390/antiox7120171.

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