RNA interference suppression of lignin biosynthesis increases fermentable sugar yields for biofuel production from field-grown sugarcane

Plant Biotechnology Journal

Volumn 11, Issue 6, 2013, Pages 709-716

  Jung, Je Hyeong ^a   Vermerris, Wilfred ^a,b   Gallo, Maria ^a,b,c   Fedenko, Jeffrey R ^a   Erickson, John E ^a   Altpeter, Fredy ^a,b  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c UNIVERSITY OF HAWAII AT MANOA   (United States)

Author keywords

Caffeic acid O methyltransferase (COMT); Field performance; Lignocellulosic biofuel; Saccharification efficiency; Saccharum; Sugarcane

Indexed keywords

SACCHARUM;

EID: 84881023585     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12061     Document Type: Article

References (60)

1. Alvira, P., Tomás-Pejó, E., Ballesteros, M. and Negro, M.J. (2010) Pretreatment technologies for an efficient bioethanol production process based on enzymatic hydrolysis: a review. Bioresour. Technol. 101, 4851-4861.
2. Barrière, Y., Ralph, J., Méchin, V., Guillaumie, S., Grabber, J.H., Argillier, O., Chabbert, B. and Lapierre, C. (2004) Genetic and molecular basis of grass cell wall biosynthesis and degradability. II. Lessons from brown-midrib mutants. C. R. Biol. 327, 847-860.
3. Bonawitz, N.D. and Chapple, C. (2010) The genetics of lignin biosynthesis: connecting genotype to phenotype. Annu. Rev. Genet. 44, 337-363.
4. Bout, S. and 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.
5. Bregitzer, P., Dahleen, L.S., Neate, S., Schwarz, P. and Manoharan, M. (2008) A single backcross effectively eliminates agronomic and quality alterations caused by somaclonal variation in transgenic barley. Crop Sci. 48, 471-479.
6. Chen, F. and Dixon, R.A. (2007) Lignin modification improves fermentable sugar yields for biofuel production. Nat. Biotechnol. 25, 759-761.
7. Comstock, J.C., Glynn, N.C. and Davdison, R.W. (2010) Sugarcane rusts in Florida. Proc. Int. Soc. Sugar Cane Technol. 27, 1-9.
8. Crago, C.L., Khanna, M., Barton, J., Giuliani, E. and Amaral, W. (2010) Competitiveness of Brazilian sugarcane ethanol compared to US corn ethanol. Energy Policy, 38, 7404-7415.
9. Dien, B., Sarath, G., Pedersen, J., Sattler, S., Chen, H., Funnell-Harris, D., Nichols, N. and 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. Ehrman, T. (1996) Determination of starch in biomass samples by chemical solubilization and enzymatic digestion. In Laboratory Analytical Procedure (LAP), Procedure #16 Golden, Colorado: National Renewable Energy Laboratory.
11. Fu, C., Mielenz, J.R., Xiao, X., Ge, Y., Hamilton, C.Y., Rodriguez, M. Jr, Chen, F., Foston, M., Ragauskas, A., Bouton, J., Dixon, R.A. and Wang, Z.Y. (2011) Genetic manipulation of lignin reduces recalcitrance and improves ethanol production from switchgrass. Proc. Natl Acad. Sci. USA, 108, 3803-3808.
12. Gallego-Giraldo, L., Escamilla-Trevino, L., Jackson, L.A. and Dixon, R.A. (2011) Salicylic acid mediates the reduced growth of lignin down-regulated plants. Proc. Natl Acad. Sci. USA, 108, 20814-20819.
13. Goldemberg, J. (2007) Ethanol for a sustainable energy future. Science, 315, 808-810.
14. Goujon, T., Ferret, V., Mila, I., Pollet, B., Ruel, K., Burlat, V., Joseleau, J.-P., Barrière, Y., Lapierre, C. and Jouanin, L. (2003) Down-regulation of the AtCCR1 gene in Arabidopsis thaliana: effects on phenotype, lignins and cell wall degradability. Planta, 217, 218-228.
15. Grabber, J.H. (2005) How do lignin composition, structure, and cross-linking affect degradability? A review of cell wall model studies. Crop Sci. 45, 820-831.
16. Grabber, J.H., Quideau, S. and Ralph, J. (1996) p-Coumaroylated syringyl units in maize lignin: Implications for β-ether cleavage by thioacidolysis. Phytochemistry, 43, 1189-1194.
17. Grabber, J.H., Ralph, J. and Hatfield, R.D. (1998) Ferulate cross-links limit the enzymatic degradation of synthetically lignified primary walls of maize. J. Agric. Food Chem. 46, 2609-2614.
18. Guo, D., Chen, F., Inoue, K., Blount, J.W. and Dixon, R.A. (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 biosynthesis of G and S lignin. Plant Cell, 13, 73-88.
19. Hatfield, R.D., Wilson, J.R. and Mertens, D.R. (1999) Composition of cell walls isolated from cell types of grain sorghum stems. J. Sci. Food Agric. 79, 891-899.
20. Hatfield, R., Ralph, J. and Grabber, J. (2008) A potential role for sinapyl p-coumarate as a radical transfer mechanism in grass lignin formation. Planta, 228, 919-928.
21. Hu, W.-J., Harding, S.A., Lung, J., Popko, J.L., Ralph, J., Stokke, D.D., Tsai, C.-J. and Chiang, V.L. (1999) Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees. Nat. Biotech. 17, 808-812.
22. Humphreys, J.M., Hemm, M.R. and 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.
23. Jørgensen, H., Kristensen, J.B. and Felby, C. (2007) Enzymatic conversion of lignocellulose into fermentable sugars: challenges and opportunities. Biofuels, Bioprod. Biorefin. 1, 119-134.
24. Jung, J.H., Fouad, W.M., Vermerris, W., Gallo, M. and Altpeter, F. (2012) RNAi suppression of lignin biosynthesis in sugarcane reduces recalcitrance for biofuel production from lignocellulosic biomass. Plant Biotechnol. J. 10, 1067-1076.
25. Lee, M.H. and Brewbaker, J.L. (1984) Effects of brown midrib-3 on yields and yield components of maize. Crop Sci. 24, 105-108.
26. Leite, R.C.C., Leal, M.R.L.V., Cortez, L.A.B., Griffin, W.M. and Scandiffio, M.I.G. (2009) Can Brazil replace 5% of the 2025 gasoline world demand with ethanol? Energy, 34, 655-661.
27. Louie, G.V., Bowman, M.E., Tu, Y., Mouradov, A., Spangenberg, G. and Noel, J.P. (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.
28. Mansfield, S.D., Mooney, C. and Saddler, J.N. (1999) Substrate and enzyme characteristics that limit cellulose hydrolysis. Biotechnol. Prog. 15, 804-816.
29. Marita, J.M., Vermerris, W., Ralph, J. and Hatfield, R.D. (2003) Variations in the cell wall composition of maize brown midrib mutants. J. Agric. Food Chem. 51, 1313-1321.
30. Miller, J.E., Geadelmann, J.L. and Marten, G.C. (1983) Effect of the brown midrib-allele on maize silage quality and yield. Crop Sci. 23, 493-496.
31. Oliver, A.L., Pedersen, J.F., Grant, R.J. and Klopfenstein, T.J. (2005a) Comparative effects of the sorghum bmr-6 and bmr-12 genes: I. Forage sorghum yield and quality. Crop Sci. 45, 2234-2239.
32. Oliver, A.L., Pedersen, J.F., Grant, R.J., Klopfenstein, T.J. and Jose, H.D. (2005b) Comparative effects of the sorghum bmr-6 and bmr-12 genes: II. Grain yield, stover yield, and stover quality in grain sorghum. Crop Sci. 45, 2240-2245.
33. Osakabe, K., Tsao, C.C., Li, L., Popko, J.L., Umezawa, T., Carraway, D.T., Smeltzer, R.H., Joshi, C.P. and Chiang, V.L. (1999) Coniferyl aldehyde 5-hydroxylation and methylation direct syringyl lignin biosynthesis in angiosperms. Proc. Natl Acad. Sci. USA, 96, 8955-8960.
34. Palmer, N., Sattler, S., Saathoff, A., Funnell, D., Pedersen, J. and Sarath, G. (2008) Genetic background impacts soluble and cell wall-bound aromatics in brown midrib mutants of sorghum. Planta, 229, 115-127.
35. Pedersen, J.F., Vogel, K.P. and Funnell, D.L. (2005) Impact of reduced lignin on plant fitness. Crop Sci. 45, 812-819.
36. Pilate, G., Guiney, E., Holt, K., Petit-Conil, M., Lapierre, C., Leple, J.-C., Pollet, B., Mila, I., Webster, E.A., Marstorp, H.G., Hopkins, D.W., Jouanin, L., Boerjan, W., Schuch, W., Cornu, D. and Halpin, C. (2002) Field and pulping performances of transgenic trees with altered lignification. Nat. Biotechnol. 20, 607-612.
37. Pinçon, G., Maury, S., Hoffmann, L., Geoffroy, P., Lapierre, C., Pollet, B. and Legrand, M. (2001) Repression of O-methyltransferase genes in transgenic tobacco affects lignin synthesis and plant growth. Phytochemistry, 57, 1167-1176.
38. Piquemal, J., Lapierre, C., Myton, K., O'Connell, A., Schuch, W., Grima-pettenati, J. and Boudet, A.-M. (1998) Down-regulation of cinnamoyl-CoA reductase induces significant changes of lignin profiles in transgenic tobacco plants. Plant J, 13, 71-83.
39. Piquemal, J., Chamayou, S., Nadaud, I., Beckert, M., Barrière, Y., Mila, I., Lapierre, C., Rigau, J., Puigdomenech, P., Jauneau, A., Digonnet, C., Boudet, A.-M., Goffner, D. and Pichon, M. (2002) Down-regulation of caffeic acid O-methyltransferase in maize revisited using a transgenic approach. Plant Physiol. 130, 1675-1685.
40. Ralph, J. (2010) Hydroxycinnamates in lignification. Phytochem. Rev. 9, 65-83.
41. Ralph, J., Hatfield, R.D., Quideau, S., Helm, R.F., Grabber, J.H. and Jung, H.-J.G. (1994) Pathway of p-coumaric acid incorporation into maize lignin as revealed by NMR. J. Am. Chem. Soc. 116, 9448-9456.
42. Ralph, J., Akiyama, T., Kim, H., Lu, F., Schatz, P.F., Marita, J.M., Ralph, S.A., Srinivasa Reddy, M.S., Chen, F. and Dixon, R.A. (2006) Effects of coumarate 3-hydroxylase down-regulation on lignin structure. J. Biol. Chem. 281, 8843-8853.
43. Robinson, A.R. and Mansfield, S.D. (2009) Rapid analysis of poplar lignin monomer composition by a streamlined thioacidolysis procedure and near-infrared reflectance-based prediction modeling. Plant J, 58, 706-714.
44. Saathoff, A.J., Sarath, G., Chow, E.K., Dien, B.S. and Tobias, C.M. (2011) Downregulation of cinnamyl-alcohol dehydrogenase in switchgrass by RNA silencing results in enhanced glucose release after cellulase treatment. PLoS ONE, 6, e16416.
45. Saballos, A., Vermerris, W., Rivera, L. and 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.
46. Sattler, S.E., Funnell-Harris, D.L. and Pedersen, J.F. (2010) Brown midrib mutations and their importance to the utilization of maize, sorghum, and pearl millet lignocellulosic tissues. Plant Sci. 178, 229-238.
47. Selig, M., Weiss, N. and Ji, Y. (2008) Enzymatic saccharification of lignocellulosic biomass. In Laboratory Analytical Procedure (LAP), Technical Report NREL/TP-510-42629. Golden, CO: National Renewable Energy Laboratory.
48. Shadle, G., Chen, F., Srinivasa Reddy, M.S., Jackson, L., Nakashima, J. and Dixon, R.A. (2007) Down-regulation of hydroxycinnamoyl CoA: shikimate hydroxycinnamoyl transferase in transgenic alfalfa affects lignification, development and forage quality. Phytochemistry, 68, 1521-1529.
49. Sluiter, A., Hames, B., Ruiz, R., Scarlata, C., Sluiter, J., Templeton, D. and Crocker, D. (2008) Determination of structural carbohydrates and lignin in biomass In Laboratory Analytical Procedure (LAP), Technical Report NREL/TP-510-42618). Golden, Colorado: National Renewable Energy Laboratory.
50. Somerville, C., Youngs, H., Taylor, C., Davis, S.C. and Long, S.P. (2010) Feedstocks for lignocellulosic biofuels. Science, 329, 790-792.
51. Srinivasa Reddy, M.S., Chen, F., Shadle, G., Jackson, L., Aljoe, H. and Dixon, R.A. (2005) Targeted down-regulation of cytochrome P450 enzymes for forage quality improvement in alfalfa (Medicago sativa L.). Proc. Natl Acad. Sci. USA, 102, 16573-16578.
52. Taparia, Y., Fouad, W., Gallo, M. and Altpeter, F. (2012a) Rapid production of transgenic sugarcane with the introduction of simple loci following biolistic transfer of a minimal expression cassette and direct embryogenesis. In Vitro Cell Dev. Biol. Plant 48, 15-22.
53. Taparia, Y., Gallo, M. and Altpeter, F. (2012b) Comparison of direct and indirect embryogenesis protocols, biolistic gene transfer and selection parameters for efficient genetic transformation of sugarcane. Plant Cell Tiss. Org. Cult. 111, 131-141.
54. Tew, T.L. and Cobill, R.M. (2008) Genetic improvement of sugarcane (Saccharum spp.) as an energy crop. In Genetic Improvement of Bioenergy Crops, (Vermerris, W. ed), pp. 273-294. New York, NY: Springer.
55. Vanholme, R., Storme, V., Vanholme, B., Sundin, L., Christensen, J.H., Goeminne, G., Halpin, C., Rohde, A., Morreel, K. and Boerjan, W. (2012) A Systems biology view of responses to lignin biosynthesis perturbations in Arabidopsis. Plant Cell, 24, 3506-3529.
56. Vermerris, W. (2011) Survey of genomics approaches to improve bioenergy traits in maize, sorghum and sugarcane. J. Integr. Plant Biol. 53, 105-119.
57. Waclawovsky, A.J., Sato, P.M., Lembke, C.G., Moore, P.H. and Souza, G.M. (2010) Sugarcane for bioenergy production: an assessment of yield and regulation of sucrose content. Plant Biotechnol. J., 8, 263-276.
58. Xu, B., Escamilla-Treviño, L.L., Sathitsuksanoh, N., Shen, Z., Shen, H., Percival Zhang, Y.H., Dixon, R.A. and Zhao, B. (2011) Silencing of 4-coumarate:coenzyme A ligase in switchgrass leads to reduced lignin content and improved fermentable sugar yields for biofuel production. New Phytol. 192, 611-625.
59. Yang, B. and Wyman, C.E. (2008) Pretreatment: the key to unlocking low-cost cellulosic ethanol. Biofuels, Bioprod. Biorefin. 2, 26-40.
60. Yue, F., Lu, F., Sun, R.-C. and Ralph, J. (2012) Syntheses of lignin-derived thioacidolysis monomers and their uses as quantitation standards. J. Agric. Food Chem. 60, 922-928.