Determination of the structure and catalytic mechanism of sorghum bicolor caffeic acid O-methyltransferase and the structural impact of three brown midrib12 mutations

Plant Physiology

Volumn 165, Issue 4, 2014, Pages 1440-1456

  Green, Abigail R ^a   Lewis, Kevin M ^a   Barr, John T ^a   Jones, Jeffrey P ^a   Lu, Fachuang ^b   Ralph, John ^b   Vermerris, Wilfred ^c   Sattler, Scott E ^d   Kang, Chulhee ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

^d Grain Forage and Bioenergy Research Unit   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84905233198     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.241729     Document Type: Article

References (62)

1. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, Moriarty NW, Read RJ, Sacchettini JC, Sauter NK, Terwilliger TC (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 58: 1948-1954
2. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402
3. Atanassova R, Favet N, Martz F, Chabbert B, Tollier M, Monties B, Fritig B, Legrand M (1995) Altered lignin composition in transgenic tobacco expressing O-methyltransferase sequences in sense and anti-sense orientation. Plant J 8: 465-477
4. Berlin A, Balakshin M, Gilkes N, Kadla J, Maximenko V, Kubo S, Saddler J (2006) Inhibition of cellulase, xylanase and b-glucosidase activities by softwood lignin preparations. J Biotechnol 125: 198-209
5. Bout S, Vermerris W (2003) A candidate-gene approach to clone the sorghum Brown midrib gene encoding caffeic acid O-methyltransferase. Mol Genet Genomics 269: 205-214
6. Cermak T, Doyle EL, Christian M, Wang L, Zhang Y, Schmidt C, Baller JA, Somia NV, Bogdanove AJ, Voytas DF (2011) Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res 39: e82
7. Chabbert B, Tollier M, Monties B, Barriere Y, Argillier O (1994) Biological variability in lignification of maize: expression of the brown midrib bm3 mutation in three maize cultivars. J Sci Food Agric 64: 349-355
8. Chen F, Dixon RA (2007) Lignin modification improves fermentable sugar yields for biofuel production. Nat Biotechnol 25: 759-761
9. Dien B, Sarath G, Pedersen J, Sattler S, Chen H, Funnel-Harris D, Nichols N, Cotta M (2009) Improved sugar conversion and ethanol yield for forage sorghum (Sorghum bicolor L. Moench) lines with reduced lignin contents. Bioenerg Res 2: 153-164
10. Egawa T, Matsumoto R, Yamamotom D, Takahashi H (2008) Molecular structure of trans-cinnamaldehyde as determined by gas electron diffraction aided by DFT calculations. J Mol Struct 892: 158-162
11. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486-501
12. Frisch M (2004) GaussView, Version 3. Gaussian, Wallingford, CT
13. Frisch M, Trucks G, Schlegel H, Scuseria G, Robb M, Cheeseman J, Scalmani G, Barone V, Mennucci B, Petersson G, et al (2009) Gaussian 09, Revision C.01. Gaussian, Wallingford, CT
14. Fu C, Mielenz JR, Xiao X, Ge Y, Hamilton CY, Rodriguez M Jr, Chen F, Foston M, Ragauskas A, Bouton J, et al (2011) Genetic manipulation of lignin reduces recalcitrance and improves ethanol production from switchgrass. Proc Natl Acad Sci USA 108: 3803-3808
15. Green AR, Hayes RP, Xun L, Kang C (2012) Structural understanding of the glutathione-dependent reduction mechanism of glutathionyl-hydroquinone reductases. J Biol Chem 287: 35838-35848
16. Guo D, Chen F, Inoue K, Blount JW, Dixon RA (2001) Downregulation of caffeic acid 3-O-methyltransferase and caffeoyl CoA 3-O-methyltransferase in transgenic alfalfa: impacts on lignin structure and implications for the bio-synthesis of G and S lignin. Plant Cell 13: 73-88
17. Holm L, Sander C (1993) Protein structure comparison by alignment of distance matrices. J Mol Biol 233: 123-138
18. Humphreys JM, Chapple C (2002) Rewriting the lignin roadmap. Curr Opin Plant Biol 5: 224-229
19. Humphreys JM, Hemm MR, Chapple C (1999) New routes for lignin biosynthesis defined by biochemical characterization of recombinant ferulate 5-hydroxylase, a multifunctional cytochrome P450-dependent monooxygenase. Proc Natl Acad Sci USA 96: 10045-10050
20. Jung JH, Fouad WM, Vermerris W, Gallo M, Altpeter F (2012) RNAi suppression of lignin biosynthesis in sugarcane reduces recalcitrance for biofuel production from lignocellulosic biomass. Plant Biotechnol J 10: 1067-1076
21. Jung JH, Vermerris W, Gallo M, Fedenko JR, Erickson JE, Altpeter F (2013) RNA interference suppression of lignin biosynthesis increases fermentable sugar yields for biofuel production from field-grown sugarcane. Plant Biotechnol J 11: 709-716
22. Kempf JG, Jung JY, Ragain C, Sampson NS, Loria JP (2007) Dynamic requirements for a functional protein hinge. J Mol Biol 368: 131-149
23. Lapierre C, Tollier M, Monties B (1988) Mise en évidence d'un nouveau type d'unité constitutive dans les lignines d'un mutant de maïs bm3. CR Acad Sci Paris Ser III 307: 723-728
24. Louie GV, Bowman ME, Tu Y, Mouradov A, Spangenberg G, Noel JP (2010) Structure-function analyses of a caffeic acid O-methyltransferase from perennial ryegrass reveal the molecular basis for substrate preference. Plant Cell 22: 4114-4127
25. Maia J, Urquiza Carvalho G, Mangueira C, Santana S, Cabral L, Rocha G (2012) GPU linear algebra libraries and GPGPU programming for accelerating MOPAC semiempirical quantum chemistry calculations. J Chem Theory Comput 8: 3072-3081
26. Marita JM, Vermerris W, Ralph J, Hatfield RD (2003) Variations in the cell wall composition of maize brown midrib mutants. J Agric Food Chem 51: 1313-1321
27. Martz F, Maury S, Pinçon G, Legrand M (1998) cDNA cloning, substrate specificity and expression study of tobacco caffeoyl-CoA 3-O-methyl-transferase, a lignin biosynthetic enzyme. Plant Mol Biol 36: 427-437
28. Meng H, Campbell WH (1998) Substrate profiles and expression of caffeoyl coenzyme A and caffeic acid O-methyltransferases in secondary xylem of aspen during seasonal development. Plant Mol Biol 38: 513-520
29. Meyer K, Cusumano JC, Somerville C, Chapple CC (1996) Ferulate-5-hydroxylase from Arabidopsis thaliana defines a new family of cytochrome P450-dependent monooxygenases. Proc Natl Acad Sci USA 93: 6869-6874
30. Meyer K, Shirley AM, Cusumano JC, Bell-Lelong DA, Chapple C (1998) Lignin monomer composition is determined by the expression of a cytochrome P450-dependent monooxygenase in Arabidopsis. Proc Natl Acad Sci USA 95: 6619-6623
31. Morreel K, Ralph J, Lu F, Goeminne G, Busson R, Herdewijn P, Goeman JL, Van der Eycken J, Boerjan W, Messens E (2004) Phenolic profiling of caffeic acid O-methyltransferase-deficient poplar reveals novel benzodioxane oligolignols. Plant Physiol 136: 4023-4036
32. Osakabe K, Tsao CC, Li L, Popko JL, Umezawa T, Carraway DT, Smeltzer RH, Joshi CP, Chiang VL (1999) Coniferyl aldehyde 5-hydroxylation and methylation direct syringyl lignin biosynthesis in angiosperms. Proc Natl Acad Sci USA 96: 8955-8960
33. Otwinowski Z, Minor W (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326
34. Palmer NA, Sattler SE, Saathoff AJ, Funnell D, Pedersen JF, Sarath G (2008) Genetic background impacts soluble and cell wall-bound aromatics in brown midrib mutants of sorghum. Planta 229: 115-127
35. Parvathi K, Chen F, Guo D, Blount JW, Dixon RA (2001) Substrate preferences of O-methyltransferases in alfalfa suggest new pathways for 3-O-methylation of monolignols. Plant J 25: 193-202
36. Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457: 551-556
37. Pedersen J, Toy J, Funnell D, Sattler S, Oliver A, Grant R (2008) Registration of BN611, AN612, BN612, and RN613 Sorghum genetic stocks with stacked bmr-6 and bmr-12 genes. Journal of Plant Registrations 2: 258-262
38. Peterson K, Dunning T (2002) Accurate correlation consistent basis sets for molecular core-valence correlation effects: the second row atoms Al-Ar, and the first row atoms B-Ne revisited. J Chem Phys 117: 10548-10560
39. Propheter J, Staggenborg S (2010) Performance of annual and perennial biofuel crops: nutrient removal during the first two years. Agron J 102: 798-805
40. Ralph J, Lapierre C, Marita JM, Kim H, Lu F, Hatfield RD, Ralph S, Chapple C, Franke R, Hemm MR, et al (2001) Elucidation of new structures in lignins of CAD-and COMT-deficient plants by NMR. Phytochemistry 57: 993-1003
41. Ralph J, Lundquist K, Brunow G, Lu F, Kim H, Schatz P, Marita J, Hatfield R, Ralph S, Christensen J, et al (2004) Lignins: natural polymers from oxidative coupling of 4-hydroxyphenylpropanoids. Phytochem Rev 3: 29-60
42. Saballos A, Vermerris W, Rivera L, Ejeta G (2008) Allelic association, chemical characterization and saccharification properties of brown midrib mutants of sorghum (Sorghum bicolor (L.) Moench). Bioenerg Res 1: 193-204
43. Sarath G, Mitchell RB, Sattler SE, Funnell D, Pedersen JF, Graybosch RA, Vogel KP (2008) Opportunities and roadblocks in utilizing forages and small grains for liquid fuels. J Ind Microbiol Biotechnol 35: 343-354
44. Sattler S, Funnell-Harris D, Pedersen J (2010) Brown midrib mutations and their importance to the utilization of maize, sorghum, and pearl millet lignocellulosic tissues. Plant Sci 178: 229-238
45. Sattler S, Palmer N, Saballos A, Greene A, Xin Z, Sarath G, Vermerris W, Pedersen J (2012) Identification and characterization of four missense 1456 mutations in Brown midrib12 (Bmr12), the caffeic acid O-methyltransferase (COMT) of sorghum. Bioenerg Res 5: 855-865
46. Shadle G, Chen F, Srinivasa Reddy MS, Jackson L, Nakashima J, Dixon RA (2007) Down-regulation of hydroxycinnamoyl CoA: Shikimate hydroxy-cinnamoyl transferase in transgenic alfalfa affects lignification, development and forage quality. Phytochem 68: 1521-1529
47. Stewart JJ (2007) Optimization of parameters for semiempirical methods. V. Modification of NDDO approximations and application to 70 elements. J Mol Model 13: 1173-1213
48. Stewart JJ (2009) Application of the PM6 method to modeling proteins. J Mol Model 15: 765-805
49. Stewart J (2012) MOPAC2012. Stewart Computational Chemistry, Colorado Springs, CO
50. Stewart JJ (2013) Optimization of parameters for semiempirical methods. VI. More modifications to the NDDO approximations and re-optimization of parameters. J Mol Model 19: 1-32
51. Tu Y, Rochfort S, Liu Z, Ran Y, Griffith M, Badenhorst P, Louie GV, Bowman ME, Smith KF, Noel JP, et al (2010) Functional analyses of caffeic acid O-methyltransferase and cinnamoyl-CoA-reductase genes from perennial ryegrass (Lolium perenne). Plant Cell 22: 3357-3373
52. Van Doorsselaere J, Baucher M, Chognot E, Chabbert B, Tollier M, Petit-Conil M, Leplé J, Pilate G, Cornu D, Monties B, et al (1995) A novel lignin in poplar trees with a reduced caffeic acid/5-hydroxyferulic acid O-methyltransferase activity. Plant J 8: 855-864
53. Vanholme R, Demedts B, Morreel K, Ralph J, Boerjan W (2010) Lignin biosynthesis and structure. Plant Physiol 153: 895-905
54. Vanholme R, Morreel K, Ralph J, Boerjan W (2008) Lignin engineering. Curr Opin Plant Biol 11: 278-285
55. Vermerris W, Saballos A (2012) Genetic enhancement of sorghum for biomass utilization. In A Paterson, ed, Genetics and Genomics of the Saccharinae. Springer, New York, pp 391-428
56. Vermerris W, Saballos A, Ejeta G, Mosier N, Ladisch M, Carpita N (2007) Molecular breeding to enhance ethanol production from corn and sorghum stover. Crop Sci 47: S142-S153
57. Vermerris W, Sherman DM, McIntyre LM (2010) Phenotypic plasticity in cell walls of maize brown midrib mutants is limited by lignin composition. J Exp Bot 61: 2479-2490
58. Wagner A, Tobimatsu Y, Phillips L, Flint H, Torr K, Donaldson L, Pears L, Ralph J (2011) CCoAOMT suppression modifies lignin composition in Pinus radiata. Plant J 67: 119-129
59. Walker A, Hayes R, Youn B, Vermerris W, Sattler S, Kang C (2013) Elucidation of the structure and reaction mechanism of sorghum hydroxycinnamoyltransferase and its structural relationship to other coenzyme A-dependent transferases and synthases. Plant Physiol 162: 640-651
60. Wortmann CS, Regassa T (2011) Sweet sorghum as a bioenergy crop for the US Great Plains. In M Aurelio Dos Santos Bernardes, ed, Economic Effects of Biofuel Production, InTech, pp 225-240 http://www.intechopen.com/books/economic-effects-of-biofuelproduction/sweet-soghum-as-a-bioenergy-crop-for-the-us-great-plains
61. Ximenes E, Kim Y, Mosier N, Dien B, Ladisch M (2010) Inhibition of cellulases by phenols. Enzyme Microb Technol 46: 170-176
62. Zubieta C, Kota P, Ferrer JL, Dixon RA, Noel JP (2002) Structural basis for the modulation of lignin monomer methylation by caffeic acid/ 5-hydroxyferulic acid 3/5-O-methyltransferase. Plant Cell 14: 1265-1277