Structural studies of cinnamoyl-CoA reductase and cinnamyl-alcohol dehydrogenase, key enzymes of monolignol biosynthesis

Plant Cell

Volumn 26, Issue 9, 2014, Pages 3709-3727

  Wang, Xiaoqiang ^a,e   Zhou, Rui ^a,f   Louie, Gordon V ^b   Mühlemann, Joëlle K ^c   Bomati, Erin K ^b,d   Bowman, Marianne E ^b   Dudareva, Natalia ^c   Dixon, Richard A ^e   Noel, Joseph P ^b,d  

^a PLANT BIOLOGY DIVISION   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c PURDUE UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF NORTH TEXAS   (United States)

^f Conagen ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL DEHYDROGENASE; ALDEHYDE DEHYDROGENASE; CINNAMOYL COA REDUCTASE; CINNAMYL ALCOHOL DEHYDROGENASE; CYSTEINE; DISULFIDE; ESTER; LIGAND; LIGNIN; MUTANT PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; PROPANOL;

BARREL MEDIC; BINDING SITE; BIOCATALYSIS; BIOSYNTHESIS; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; KINETICS; METABOLISM; MOLECULAR CLONING; PETUNIA; STRUCTURAL HOMOLOGY; TEMPERATURE; X RAY CRYSTALLOGRAPHY;

ALCOHOL OXIDOREDUCTASES; ALDEHYDE OXIDOREDUCTASES; BINDING SITES; BIOCATALYSIS; CLONING, MOLECULAR; CRYSTALLOGRAPHY, X-RAY; CYSTEINE; DISULFIDES; ESTERS; KINETICS; LIGANDS; LIGNIN; MEDICAGO TRUNCATULA; MODELS, MOLECULAR; MUTANT PROTEINS; NADP; PETUNIA; PROPANOLS; STRUCTURAL HOMOLOGY, PROTEIN; SUBSTRATE SPECIFICITY; TEMPERATURE;

EID: 84907962767     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.127399     Document Type: Article

References (80)

1. Adams, P. D., et al. (2010). PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66: 213-221.
2. Anterola, A. M., and Lewis, N. G. (2002). Trends in lignin modification: a comprehensive analysis of the effects of genetic manipulations/mutations on lignification and vascular integrity. Phytochemistry 61: 221-294.
3. Baltas, M., Lapeyre, C., Bedos-Belval, F., Maturano, M., Saint-Aguet, P., Roussel, L., Duran, H., and Grima-Pettenati, J. (2005). Kinetic and inhibition studies of cinnamoyl-CoA reductase 1 from Arabidopsis thaliana. Plant Physiol. Biochem. 43: 746-753.
4. Barakat, A., Yassin, N. B., Park, J. S., Choi, A., Herr, J., and Carlson, J. E. (2011). Comparative and phylogenomic analyses of cinnamoyl-CoA reductase and cinnamoyl-CoA-reductase-like gene family in land plants. Plant Sci. 181: 249-257.
5. Barakat, A., Bagniewska-Zadworna, A., Choi, A., Plakkat, U., DiLoreto, D. S., Yellanki, P., and Carlson, J. E. (2009). The cinnamyl alcohol dehydrogenase gene family in Populus: phylogeny, organization, and expression. BMC Plant Biol. 9: 26.
6. Battye, T. G., Kontogiannis, L., Johnson, O., Powell, H. R., and Leslie, A. G. (2011). iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr. D Biol. Crystallogr. 67: 271-281.
7. Baucher, M., Halpin, C., Petit-Conil, M., and Boerjan, W. (2003). Lignin: genetic engineering and impact on pulping. Crit. Rev. Biochem. Mol. Biol. 38: 305-350.
8. Boatright, J., Negre, F., Chen, X., Kish, C. M., Wood, B., Peel, G., Orlova, I., Gang, D., Rhodes, D., and Dudareva, N. (2004). Understanding in vivo benzenoid metabolism in petunia petal tissue. Plant Physiol. 135: 1993-2011.
9. Boerjan, W., Ralph, J., and Baucher, M. (2003). Lignin biosynthesis. Annu. Rev. Plant Biol. 54: 519-546.
10. Bomati, E. K., and Noel, J. P. (2005). Structural and kinetic basis for substrate selectivity in Populus tremuloides sinapyl alcohol dehydrogenase. Plant Cell 17: 1598-1611.
11. Boudet, A. M., Lapierre, C., and Grima-Pettenati, J. (1995). Tansley review No. 80. Biochemistry and molecular biology of lignification. New Phytol. 129: 203-236.
12. Breton, R., Housset, D., Mazza, C., and Fontecilla-Camps, J. C. (1996). The structure of a complex of human 17beta-hydroxysteroid dehydrogenase with estradiol and NADP+ identifies two principal targets for the design of inhibitors. Structure 4: 905-915.
13. Brünger, A. T., et al. (1998). Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54: 905-921.
14. Campbell, M. M., and Sederoff, R. R. (1996). Variation in lignin content and composition. Mechanisms of control and implications for the genetic improvement of plants. Plant Physiol. 110: 3-13.
15. Carugo, O., and Argos, P. (1997). NADP-dependent enzymes. I: Conserved stereochemistry of cofactor binding. Proteins 28: 10-28.
16. Chen, F., and Dixon, R. A. (2007). Lignin modification improves fermentable sugar yields for biofuel production. Nat. Biotechnol. 25: 759-761.
17. Chen, V. B., Arendall, W. B., III., Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010). MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66: 12-21.
18. Clermont, S., Corbier, C., Mely, Y., Gerard, D., Wonacott, A., and Branlant, G. (1993). Determinants of coenzyme specificity in glyceraldehyde-3-phosphate dehydrogenase: role of the acidic residue in the fingerprint region of the nucleotide binding fold. Biochemistry 32: 10178-10184.
19. Costa, M. A., Collins, R. E., Anterola, A. M., Cochrane, F. C., Davin, L. B., and Lewis, N. G. (2003). An in silico assessment of gene function and organization of the phenylpropanoid pathway metabolic networks in Arabidopsis thaliana and limitations thereof. Phytochemistry 64: 1097-1112.
20. Damiani, I., Morreel, K., Danoun, S., Goeminne, G., Yahiaoui, N., Marque, C., Kopka, J., Messens, E., Goffner, D., Boerjan, W., Boudet, A. M., and Rochange, S. (2005). Metabolite profiling reveals a role for atypical cinnamyl alcohol dehydrogenase CAD1 in the synthesis of coniferyl alcohol in tobacco xylem. Plant Mol. Biol. 59: 753-769.
21. Danehy, J. P., Doherty, B. T., and Egan, C. P. (1971). The oxidation of organic divalent sulfur by iodine. 11. The equilibrating thiol-iodinedisulfide-hydrogen iodide system in acetic acid and evidence for sulfenyl iodide intermediates. J. Org. Chem. 36: 2525-2530.
22. Davin, L. B., and Lewis, N. G. (1992). Phenylpropanoid metabolism: biosynthesis of monolignols, lignans and neolignans, lignins and suberins. Recent Adv. Phytochem. 26: 325-375.
23. Deacon, A. M., Ni, Y. S., and Coleman, W. G., Jr., andEalick, S. E. (2000). The crystal structure of ADP-L-glycero-D-mannoheptose 6-epimerase: catalysis with a twist. Structure 8: 453-462.
24. Dixon, R. A., Chen, F., Guo, D., and Parvathi, K. (2001). The biosynthesis of monolignols: a "metabolic grid", or independent pathways to guaiacyl and syringyl units? Phytochemistry 57: 1069-1084.
25. Donaldson, L. A. (2001). Lignification and lignin topochemistry-an ultrastructural view. Phytochemistry 57: 859-873.
26. Doublié, S. (1997). Preparation of selenomethionyl proteins for phase determination. Methods Enzymol. 276: 523-530.
27. Ebel, J., and Grisebach, H. (1973). Reduction of cinnamic acids to cinnamyl alcohols with an enzyme preparation from cell suspension cultures of soybean (Glycine max). FEBS Lett. 30: 141-143.
28. Emsley, P., and Cowtan, K. (2004). Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60: 2126-2132.
29. Escamilla-Treviño, L. L., Shen, H., Uppalapati, S. R., Ray, T., Tang, Y., Hernandez, T., Yin, Y., Xu, Y., and Dixon, R. A. (2010). Switchgrass (Panicum virgatum) possesses a divergent family of cinnamoyl CoA reductases with distinct biochemical properties. New Phytol. 185: 143-155.
30. Evans, P. (2006). Scaling and assessment of data quality. Acta Crystallogr. D Biol. Crystallogr. 62: 72-82.
31. Filling, C., Berndt, K. D., Benach, J., Knapp, S., Prozorovski, T., Nordling, E., Ladenstein, R., Jörnvall, H., and Oppermann, U. (2002). Critical residues for structure and catalysis in short-chain dehydrogenases/reductases. J. Biol. Chem. 277: 25677-25684.
32. Gargouri, M., Manigand, C., Maugé, C., Granier, T., Langlois d'Estaintot, B., Cala, O., Pianet, I., Bathany, K., Chaudière, J., and Gallois, B. (2009). Structure and epimerase activity of anthocyanidin reductase from Vitis vinifera. Acta Crystallogr. D Biol. Crystallogr. 65: 989-1000.
33. Goffner, D., Van Doorsselaere, J., Yahiaoui, N., Samaj, J., Grima-Pettenati, J., and Boudet, A. M. (1998). A novel aromatic alcohol dehydrogenase in higher plants: molecular cloning and expression. Plant Mol. Biol. 36: 755-765.
34. Gourley, D. G., Shrive, A. K., Polikarpov, I., Krell, T., Coggins, J. R., Hawkins, A. R., Isaacs, N. W., and Sawyer, L. (1999). The two types of 3-dehydroquinase have distinct structures but catalyze the same overall reaction. Nat. Struct. Biol. 6: 521-525.
35. Jez, J. M., Bowman, M. E., Dixon, R. A., and Noel, J. P. (2000). Structure and mechanism of the evolutionarily unique plant enzyme chalcone isomerase. Nat. Struct. Biol. 7: 786-791.
36. Jones, G., Willett, P., Glen, R. C., Leach, A. R., and Taylor, R. (1997). Development and validation of a genetic algorithm for flexible docking. J. Mol. Biol. 267: 727-748.
37. Jones, T. A., Zou, J.-Y., Cowan, S. W., and Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47: 110-119.
38. Jörnvall, H., Persson, M., and Jeffery, J. (1981). Alcohol and polyol dehydrogenases are both divided into two protein types, and structural properties cross-relate the different enzyme activities within each type. Proc. Natl. Acad. Sci. USA 78: 4226-4230.
39. Jörnvall, H., Hedlund, J., Bergman, T., Oppermann, U., and Persson, B. (2010). Superfamilies SDR and MDR: from early ancestry to present forms. Emergence of three lines, a Zn-metalloenzyme, and distinct variabilities. Biochem. Biophys. Res. Commun. 396: 125-130.
40. Jörnvall, H., Persson, B., Krook, M., Atrian, S., Gonzàlez-Duarte, R., Jeffery, J., and Ghosh, D. (1995). Short-chain dehydrogenases/reductases (SDR). Biochemistry 34: 6003-6013.
41. Kamitori, S., Iguchi, A., Ohtaki, A., Yamada, M., and Kita, K. (2005). X-ray structures of NADPH-dependent carbonyl reductase from Sporobolomyces salmonicolor provide insights into stereoselective reductions of carbonyl compounds. J. Mol. Biol. 352: 551-558.
42. Kim, S. J., Kim, M. R., Bedgar, D. L., Moinuddin, S. G., Cardenas, C. L., Davin, L. B., Kang, C., and Lewis, N. G. (2004). Functional reclassification of the putative cinnamyl alcohol dehydrogenase multigene family in Arabidopsis. Proc. Natl. Acad. Sci. USA 101: 1455-1460.
43. Klempien, A., et al. (2012). Contribution of CoA ligases to benzenoid biosynthesis in petunia flowers. Plant Cell 24: 2015-2030.
44. Kraulis, P. J. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24: 946-950.
45. Lamzin, V. S., Perrakis, A., andWilson, K. S. (2001). The ARP/WARP suite for automated construction and refinement of protein models. In Int. Tables for Crystallography: Crystallography of Biological Macromolecules, M. G. Rossmann and E. Arnold, eds (Dordrecht/Boston/London: Kluwer Academic Publishers), pp. 720-722.
46. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993). PROCHECK-a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26: 283-291.
47. Lauvergeat, V., Lacomme, C., Lacombe, E., Lasserre, E., Roby, D., and Grima-Pettenati, J. (2001). Two cinnamoyl-CoA reductase (CCR) genes from Arabidopsis thaliana are differentially expressed during development and in response to infection with pathogenic bacteria. Phytochemistry 57: 1187-1195.
48. Lee, Y., Chen, F., Gallego-Giraldo, L., Dixon, R. A., and Voit, E. O. (2011). Integrative analysis of transgenic alfalfa (Medicago sativa L.) suggests new metabolic control mechanisms for monolignol biosynthesis. PLOS Comput. Biol. 7: e1002047.
49. Lewis, N. G., and Yamamoto, E. (1990). Lignin: occurrence, biogenesis and biodegradation. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41: 455-496.
50. Li, L., Cheng, X., Lu, S., Nakatsubo, T., Umezawa, T., and Chiang, V. L. (2005). Clarification of cinnamoyl co-enzyme A reductase catalysis in monolignol biosynthesis of aspen. Plant Cell Physiol. 46: 1073-1082.
51. Lüderitz, T., and Grisebach, H. (1981). Enzymic synthesis of lignin precursors. Comparison of cinnamoyl-CoA reductase and cinnamyl alcohol: NADP+ dehydrogenase from spruce (Picea abies L.) and soybean (Glycine max L.). Eur. J. Biochem. 119: 115-124.
52. Mansell, R. L., Gross, G. G., Stöckigt, J., Franke, H., and Zenk, M. H. (1974). Purification and properties of cinnamyl alcohol dehydrogenase from higher plants involved in lignin biosynthesis. Phytochemistry 13: 2427-2435.
53. Martí-Renom, M. A., Stuart, A. C., Fiser, A., Sánchez, R., Melo, F., and Sali, A. (2000). Comparative protein structure modeling of genes and genomes. Annu. Rev. Biophys. Biomol. Struct. 29: 291-325.
54. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007). Phaser crystallographic software. J. Appl. Cryst. 40: 658-674.
55. McKinley-McKee, J. S., Winberg, J. O., and Pettersson, G. (1991). Mechanism of action of Drosophila melanogaster alcohol dehydrogenase. Biochem. Int. 25: 879-885.
56. McRee, D. E. (1999). XtalView/Xfit-A versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol. 125: 156-165.
57. Mellerowicz, E. J., Baucher, M., Sundberg, B., and Boerjan, W. (2001). Unravelling cell wall formation in the woody dicot stem. Plant Mol. Biol. 47: 239-274.
58. Moummou, H., Kallberg, Y., Tonfack, L. B., Persson, B., and van der Rest, B. (2012). The plant short-chain dehydrogenase (SDR) superfamily: genome-wide inventory and diversification patterns. BMC Plant Biol. 12: 219.
59. Niesen, F. H., Berglund, H., and Vedadi, M. (2007). The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability. Nat. Protoc. 2: 2212-2221.
60. Otwinowski, Z., and Minor, W. (1997). Processing of x-ray diffraction data collected in oscillation mode. In Methods in Enzymology, C. W. Carter and R. M. Sweet, eds (New York: Academic Press), pp. 307-326.
61. Perrakis, A., Morris, R., and Lamzin, V. S. (1999). Automated protein model building combined with iterative structure refinement. Nat. Struct. Biol. 6: 458-463.
62. Petit, P., Granier, T., d'Estaintot, B. L., Manigand, C., Bathany, K., Schmitter, J. M., Lauvergeat, V., Hamdi, S., and Gallois, B. (2007). Crystal structure of grape dihydroflavonol 4-reductase, a key enzyme in flavonoid biosynthesis. J. Mol. Biol. 368: 1345-1357.
63. Ravilious, G. E., Nguyen, A., Francois, J. A., and Jez, J. M. (2012). Structural basis and evolution of redox regulation in plant adenosine-59-phosphosulfate kinase. Proc. Natl. Acad. Sci. USA 109: 309-314.
64. Rossmann, M. G., Liljas, A., Branden, C.-I., and Bansazak, L. J. (1975). Evolutionary and Structural Relationships among Dehydrogenases. (New York: Academic Press).
65. Ryu, S. E. (2012). Structural mechanism of disulphide bond-mediated redox switches. J. Biochem. 151: 579-588.
66. Sali, A., and Blundell, T. L. (1993). Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234: 779-815.
67. Shao, H., Dixon, R. A., and Wang, X. (2007). Crystal structure of vestitone reductase from alfalfa (Medicago sativa L.). J. Mol. Biol. 369: 265-276.
68. Sibout, R., Eudes, A., Mouille, G., Pollet, B., Lapierre, C., Jouanin, L., and Séguin, A. (2005). CINNAMYL ALCOHOL DEHYDROGENASE-C and-D are the primary genes involved in lignin biosynthesis in the floral stem of Arabidopsis. Plant Cell 17: 2059-2076.
69. Sonawane, P., Vishwakarma, R. K., and Khan, B. M. (2013). Biochemical characterization of recombinant cinnamoyl CoA reductase 1 (Ll-CCRH1) from Leucaena leucocephala. Int. J. Biol. Macromol. 58: 154-159.
70. Tanaka, N., Nonaka, T., Nakamura, K. T., and Hara, A. (2001). SDR: structure, mechanism of action, and substrate recognition. Curr. Org. Chem. 5: 89-111.
71. Tu, Y., Rochfort, S., Liu, Z., Ran, Y., Griffith, M., Badenhorst, P., Louie, G. V., Bowman, M. E., Smith, K. F., Noel, J. P., Mouradov, A., and Spangenberg, G. (2010). Functional analyses of caffeic acid O-methyltransferase and Cinnamoyl-CoA-reductase genes from perennial ryegrass (Lolium perenne). Plant Cell 22: 3357-3373.
72. Vagin, A., and Teplyakov, A. (2010). Molecular replacement with MOLREP. Acta Crystallogr. D Biol. Crystallogr. 66: 22-25.
73. Valencia, E., Larroy, C., Ochoa, W. F., Parés, X., Fita, I., and Biosca, J. A. (2004). Apo and Holo structures of an NADPH-dependent cinnamyl alcohol dehydrogenase from Saccharomyces cerevisiae. J. Mol. Biol. 341: 1049-1062.
74. Vanholme, R., et al. (2013). Caffeoyl shikimate esterase (CSE) is an enzyme in the lignin biosynthetic pathway in Arabidopsis. Science 341: 1103-1106.
75. Wagner, A., Tobimatsu, Y., Goeminne, G., Phillips, L., Flint, H., Steward, D., Torr, K., Donaldson, L., Boerjan, W., and Ralph, J. (2013). Suppression of CCR impacts metabolite profile and cell wall composition in Pinus radiata tracheary elements. Plant Mol. Biol. 81: 105-117.
76. Wengenmayer, H., Ebel, J., and Grisebach, H. (1976). Enzymic synthesis of lignin precursors. Purification and properties of a cinnamoyl-CoA: NADPH reductase from cell suspension cultures of soybean (Glycine max). Eur. J. Biochem. 65: 529-536.
77. Whetten, R., and Sederoff, R. (1995). Lignin biosynthesis. Plant Cell 7: 1001-1013.
78. Youn, B., Camacho, R., Moinuddin, S. G., Lee, C., Davin, L. B., Lewis, N. G., and Kang, C. (2006). Crystal structures and catalytic mechanism of the Arabidopsis cinnamyl alcohol dehydrogenases AtCAD5 and AtCAD4. Org. Biomol. Chem. 4: 1687-1697.
79. Zhao, Q., et al. (2013). Loss of function of cinnamyl alcohol dehydrogenase 1 leads to unconventional lignin and temperaturesensitive growth reduction in Medicago truncatula. Proc. Natl. Acad. Sci. USA 110: 13660-13665.
80. Zhou, R., Jackson, L., Shadle, G., Nakashima, J., Temple, S., Chen, F., and Dixon, R. A. (2010). Distinct cinnamoyl CoA reductases involved in parallel routes to lignin in Medicago truncatula. Proc. Natl. Acad. Sci. USA 107: 17803-17808.