Engineering secondary cell wall deposition in plants

Plant Biotechnology Journal

Volumn 11, Issue 3, 2013, Pages 325-335

  Yang, Fan ^a   Mitra, Prajakta ^a   Zhang, Ling ^a,b   Prak, Lina ^a   Verhertbruggen, Yves ^a   Kim, Jin Sun ^a   Sun, Lan ^a   Zheng, Kejian ^a   Tang, Kexuan ^b   Auer, Manfred ^a   Scheller, Henrik V ^a   Loqué, Dominique ^a  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

Artificial positive feedback loop; Biofuels; Cell wall; Lignin; Saccharification; Synthetic biology

Indexed keywords

ARABIDOPSIS PROTEIN; BIOFUEL; LIGNIN; NST1 PROTEIN, ARABIDOPSIS; TRANSCRIPTION FACTOR; VND6 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; CELL WALL; FEEDBACK SYSTEM; GENE EXPRESSION REGULATION; GENETIC ENGINEERING; GENETICS; METABOLISM; PROMOTER REGION; VASCULAR BUNDLE (PLANT);

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOFUELS; CELL WALL; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION, PLANT; GENETIC ENGINEERING; LIGNIN; PLANT VASCULAR BUNDLE; PROMOTER REGIONS, GENETIC; TRANSCRIPTION FACTORS;

ANIMALIA; ARABIDOPSIS;

EID: 84875594543     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12016     Document Type: Article

References (70)

1. Aden, A., Ruth, M., Ibsen, K., Jechura, J., Neeves, K., Sheehan, J. and Wallace, B. (2002) Lignocellulosic biomass to ethanol process design and economics utilizing co-current dilute acid prehydrolysis and enzymatic hydrolysis for corn stover. In Laboratory Analytical Procedure (Montague, L., Slayton, A. and Lukas, J., eds), pp. 2-89. Golden, CO: National Renewable Energy Laboratory.
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. Blake, A.W., McCartney, L., Flint, J.E., Bolam, D.N., Boraston, A.B., Gilbert, H.J. and Knox, J.P. (2006) Understanding the biological rationale for the diversity of cellulose-directed carbohydrate-binding modules in prokaryotic enzymes. J. Biol. Chem. 281, 29321-29329.
4. Blanch, H.W., Adams, P.D., Andrews-Cramer, K.M., Frommer, W.B., Simmons, B.A. and Keasling, J.D. (2008) Addressing the need for alternative transportation fuels: the Joint BioEnergy Institute. ACS Chem. Biol. 3, 17-20.
5. Blanch, H.W., Simmons, B.A. and Klein-Marcuschamer, D. (2011) Biomass deconstruction to sugars. Biotechnol. J. 6, 1086-1102.
6. Bollhöner, B., Prestele, J. and Tuominen, H. (2012) Xylem cell death: emerging understanding of regulation and function. J. Exp. Bot. 63, 1081-1094.
7. Boyce, C.K., Zwieniecki, M.A., Cody, G.D., Jacobsen, C., Wirick, S., Knoll, A.H. and Holbrook, N.M. (2004) Evolution of xylem lignification and hydrogel transport regulation. Proc. Natl Acad. Sci. USA 101, 17555-17558.
8. Brown, D.M., Zeef, L.A.H., Ellis, J., Goodacre, R. and Turner, S.R. (2005) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17, 2281-2295.
9. Calderini, O., Bovone, T., Scotti, C., Pupilli, F., Piano, E. and Arcioni, S. (2007) Delay of leaf senescence in Medicago sativa transformed with the ipt gene controlled by the senescence-specific promoter SAG12. Plant Cell Rep. 26, 611-615.
10. Cano-Delgado, A., Lee, J.-Y. and Demura, T. (2010) Regulatory mechanisms for specification and patterning of plant vascular tissues. Annu. Rev. Cell Dev. Biol. 26, 605-637.
11. Carroll, A. and Somerville, C. (2009) Cellulosic biofuels. Annu. Rev. Plant Biol. 60, 165-182.
12. Chen, F. and Dixon, R.A. (2007) Lignin modification improves fermentable sugar yields for biofuel production. Nat. Biotechnol. 25, 759-761.
13. Christiansen, M.W., Holm, P.B. and Gregersen, P.L. (2011) Characterization of barley (Hordeum vulgare L.) NAC transcription factors suggests conserved functions compared to both monocots and dicots. BMC Res. Notes 4, 302.
14. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
15. Coleman, H.D., Park, J.-Y., Nair, R., Chapple, C. and Mansfield, S.D. (2008a) RNAi-mediated suppression of p-coumaroyl-CoA 3'-hydroxylase in hybrid poplar impacts lignin deposition and soluble secondary metabolism. Proc. Natl Acad. Sci. USA 105, 4501-4506.
16. Coleman, H.D., Samuels, A.L., Guy, R.D. and Mansfield, S.D. (2008b) Perturbed lignification impacts tree growth in hybrid poplar-a function of sink strength, vascular integrity, and photosynthetic assimilation. Plant Physiol. 148, 1229-1237.
17. Déjardin, A., Laurans, F., Arnaud, D., Breton, C., Pilate, G. and Leplé, J.-C. (2010) Wood formation in angiosperms. C.R. Biol. 333, 325-334.
18. Demura, T. and Ye, Z.-H. (2010) Regulation of plant biomass production. Curr. Opin. Plant Biol. 13, 299-304.
19. Foster, C.E., Martin, T.M. and Pauly, M. (2010) Comprehensive compositional analysis of plant cell walls (Lignocellulosic biomass) part I: lignin. J. Vis. Exp. 37, 1-4.
20. Franke, R., Humphreys, J.M., Hemm, M.R., Denault, J.W., Ruegger, M.O., Cusumano, J.C. and Chapple, C. (2002) The Arabidopsis REF8 gene encodes the 3-hydroxylase of phenylpropanoid metabolism. Plant J. 30, 33-45.
21. Gallego-Giraldo, L., Escamilla-Trevino, L., Jackson, L.A. and Dixon, R.A. (2011a) Salicylic acid mediates the reduced growth of lignin down-regulated plants. Proc. Natl Acad. Sci. USA 108, 20814-20819.
22. Gallego-Giraldo, L., Jikumaru, Y., Kamiya, Y., Tang, Y. and Dixon, R.A. (2011b) Selective lignin downregulation leads to constitutive defense response expression in alfalfa (Medicago sativa L.). New Phytol. 190, 627-639.
23. Gan, S. and Amasino, R.M. (1995) Inhibition of leaf senescence by autoregulated production of cytokinin. Science 270, 1986-1988.
24. Goicoechea, M., Lacombe, E., Legay, S., Mihaljevic, S., Rech, P., Jauneau, A., Lapierre, C., Pollet, B., Verhaegen, D., Chaubet-Gigot, N. and Grima-Pettenati, J. (2005) EgMYB2, a new transcriptional activator from Eucalyptus xylem, regulates secondary cell wall formation and lignin biosynthesis. Plant J. 43, 553-567.
25. Gomez, L.D., Steele-King, C.G. and McQueen-Mason, S.J. (2008) Sustainable liquid biofuels from biomass: the writing's on the walls. New Phytol. 178, 473-485.
26. Handakumbura, P.P. and Hazen, S.P. (2012) Transcriptional regulation of grass secondary cell wall biosynthesis: playing catch-up with Arabidopsis thaliana. Front. Plant Sci. 3, 74.
27. Jorgensen, H., Kristensen, J.B. and Felby, C. (2007) Enzymatic conversion of lignocellulose into fermentable sugars: challenges and opportunities. Biofuel Bioprod. Bior. 1, 119-134.
28. Kitin, P., Voelker, S.L., Meinzer, F.C., Beeckman, H., Strauss, S.H. and Lachenbruch, B. (2010) Tyloses and phenolic deposits in xylem vessels impede water transport in low-lignin transgenic poplars: a study by cryo-fluorescence microscopy. Plant Physiol. 154, 887-898.
29. Klein-Marcuschamer, D., Oleskowicz-Popiel, P., Simmons, B.A. and Blanch, H.W. (2010) Technoeconomic analysis of biofuels: a wiki-based platform for lignocellulosic biorefineries. Biomass Bioenergy 34, 1914-1921.
30. Ko, J.-H., Kim, H.-T., Hwang, I. and Han, K.-H. (2012) Tissue-type-specific transcriptome analysis identifies developing xylem-specific promoters in poplar. Plant Biotechnol. J. 10, 587-596.
31. Kubo, M., Udagawa, M., Nishikubo, N., Horiguchi, G., Yamaguchi, M., Ito, J., Mimura, T., Fukuda, H. and Demura, T. (2005) Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev. 19, 1855-1860.
32. Kumar, A., Cameron, J.B. and Flynn, P.C. (2005) Pipeline transport and simultaneous saccharification of corn stover. Bioresour. Technol. 96, 819-829.
33. Lalonde, S., Sero, A., Pratelli, R., Pilot, G., Chen, J., Sardi, M.I., Parsa, S.A., Kim, D.-Y., Acharya, B.R., Stein, E.V., Hu, H.-C., Villiers, F., Takeda, K., Yang, Y., Han, Y.S., Schwacke, R., Chiang, W., Kato, N., Loque, D., Assmann, S.M., Kwak, J.M., Schroeder, J., Rhee, S.Y. and Frommer, W.B. (2010) Frontiers: a membrane protein/signaling protein interaction network for Arabidopsis version AMPv2. Front. Plant Sci. 1, 24.
34. Li, X. and Chapple, C. (2010) Understanding lignification: challenges beyond monolignol biosynthesis. Plant Physiol. 154, 449-452.
35. McCabe, M., Garratt, L., Schepers, F., Jordi, W., Stoopen, G., Davelaar, E., van Rhijn, J., Power, J. and Davey, M. (2001) Effects of pSAG12-IPT gene expression on development and senescence in transgenic lettuce. Plant Physiol. 127, 505-516.
36. McCartney, L., Gilbert, H.J., Bolam, D.N., Boraston, A.B. and Knox, J.P. (2004) Glycoside hydrolase carbohydrate-binding modules as molecular probes for the analysis of plant cell wall polymers. Anal. Biochem. 326, 49-54.
37. McCartney, L., Marcus, S.E. and Knox, J.P. (2005) Monoclonal antibodies to plant cell wall xylans and arabinoxylans. J. Histochem. Cytochem. 53, 543-546.
38. Meyer, K., Shirley, A.M., Cusumano, J.C., Bell-Lelong, D.A. and 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.
39. Miller, G. (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal. Chem. 31, 426-428.
40. Mitsuda, N. and Ohme-Takagi, M. (2009) Functional analysis of transcription factors in Arabidopsis. Plant Cell Physiol. 50, 1232-1248.
41. Mitsuda, N., Seki, M., Shinozaki, K. and Ohme-Takagi, M. (2005) The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence. Plant Cell 17, 2993-3006.
42. Nakano, J., Meshitsuka, G., lin, S. and Dence, C. (eds) (1992) The Detection of Lignin Methods in Lignin Chemistry. Berlin: Springer-Verlag.
43. Ohtani, M., Nishikubo, N., Xu, B., Yamaguchi, M., Mitsuda, N., Goué, N., Shi, F., Ohme-Takagi, M. and Demura, T. (2011) A NAC domain protein family contributing to the regulation of wood formation in poplar. Plant J. 67, 499-512.
44. Robson, P., Donnison, I., Wang, K., Frame, B., Pegg, S., Thomas, A. and Thomas, H. (2004) Leaf senescence is delayed in maize expressing the Agrobacterium IPT gene under the control of a novel maize senescence-enhanced promoter. Plant Biotechnol. J. 2, 101-112.
45. Ruegger, M. and Chapple, C. (2001) Mutations that reduce sinapoylmalate accumulation in Arabidopsis thaliana define loci with diverse roles in phenylpropanoid metabolism. Genetics 159, 1741-1749.
46. Ruprecht, C., Mutwil, M., Saxe, F., Eder, M., Nikoloski, Z. and Persson, S. (2011) Large-scale co-expression approach to dissect secondary cell wall formation across plant species. Front. Plant Sci. 2, 23.
47. Schilmiller, A.L., Stout, J., Weng, J.-K., Humphreys, J., Ruegger, M.O. and Chapple, C. (2009) Mutations in the cinnamate 4-hydroxylase gene impact metabolism, growth and development in Arabidopsis. Plant J. 60, 771-782.
48. Schwab, R., Ossowski, S., Riester, M., Warthmann, N. and Weigel, D. (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18, 1121-1133.
49. Searcy, E., Flynn, P., Ghafoori, E. and Kumar, A. (2007) The relative cost of biomass energy transport. Appl. Biochem. Biotechnol. 137-140, 639-652.
50. 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.
51. 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.
52. Simmons, B.A., Loque, D. and Blanch, H.W. (2008) Next-generation biomass feedstocks for biofuel production. Genome Biol. 9, 242.
53. Somerville, C., Youngs, H., Taylor, C., Davis, S.C. and Long, S.P. (2010) Feedstocks for lignocellulosic biofuels. Science 329, 790-792.
54. Sun, L., Simmons, B.A. and Singh, S. (2011) Understanding tissue specific compositions of bioenergy feedstocks through hyperspectral Raman imaging. Biotechnol. Bioeng. 108, 286-295.
55. Vera-Sirera, F., Minguet, E.G., Singh, S.K., Ljung, K., Tuominen, H., Blázquez, M.A. and Carbonell, J. (2010) Role of polyamines in plant vascular development. Plant Physiol. Biochem. 48, 534-539.
56. Verhertbruggen, Y., Marcus, S.E., Haeger, A., Verhoef, R., Schols, H.A., McCleary, B.V., McKee, L., Gilbert, H.J. and Knox, J.P. (2009) Developmental complexity of arabinan polysaccharides and their processing in plant cell walls. Plant J. 59, 413-425.
57. Vinzant, T., Ehrman, C., Adney, W., Thomas, S. and Himmel, M. (1997) Simultaneous saccharification and fermentation of pretreated hardwoods-effect of native lignin content. Appl. Biochem. Biotechnol. 62, 99-104.
58. Voelker, S.L., Lachenbruch, B., Meinzer, F.C., Jourdes, M., Ki, C., Patten, A.M., Davin, L.B., Lewis, N.G., Tuskan, G.A., Gunter, L., Decker, S.R., Selig, M.J., Sykes, R., Himmel, M.E., Kitin, P., Shevchenko, O. and Strauss, S.H. (2010) Antisense down-regulation of 4CL expression alters lignification, tree growth, and saccharification potential of field-grown poplar. Plant Physiol. 154, 874-886.
59. Voinnet, O., Vain, P., Angell, S. and Baulcombe, D.C. (1998) Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell 95, 177-187.
60. Wang, H.-Z. and Dixon, R.A. (2011) On-off switches for secondary cell wall biosynthesis. Mol. Plant, 5, 297-303.
61. Wang, H., Zhao, Q., Chen, F., Wang, M. and Dixon, R.A. (2011) NAC domain function and transcriptional control of a secondary cell wall master switch. Plant J., 68, 1104-1114.
62. Weng, J.-K., Akiyama, T., Bonawitz, N.D., Li, X., Ralph, J. and Chapple, C. (2010) Convergent evolution of syringyl lignin biosynthesis via distinct pathways in the lycophyte Selaginella and flowering plants. Plant Cell 22, 1033-1045.
63. Yamaguchi, M., Kubo, M., Fukuda, H. and Demura, T. (2008) Vascular-related NAC-DOMAIN7 is involved in the differentiation of all types of xylem vessels in Arabidopsis roots and shoots. Plant J. 55, 652-664.
64. Yamaguchi, M., Ohtani, M., Mitsuda, N., Kubo, M., Ohme-Takagi, M., Fukuda, H. and Demura, T. (2010) VND-INTERACTING2, a NAC domain transcription factor, negatively regulates xylem vessel formation in Arabidopsis. Plant Cell 22, 1249-1263.
65. Yin, L., Verhertbruggen, Y., Oikawa, A., Manisseri, C., Knierim, B., Prak, L., Jensen, J.K., Knox, J.P., Auer, M., Willats, W.G.T. and Scheller, H.V. (2011) The cooperative activities of CSLD2, CSLD3, and CSLD5 are required for normal Arabidopsis development. Mol. Plant, 4, 1024-1037.
66. Zhong, R. and Ye, Z.-H. (2010) The poplar PtrWNDs are transcriptional activators of secondary cell wall biosynthesis. Plant Signal. Behav. 5, 469-472.
67. Zhong, R., Lee, C., Zhou, J., McCarthy, R.L. and Ye, Z.-H. (2008) A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell 20, 2763-2782.
68. Zhong, R., Lee, C. and Ye, Z.-H. (2010) Functional characterization of poplar wood-associated NAC domain transcription factors. Plant Physiol. 152, 1044-1055.
69. Zhong, R., Lee, C., McCarthy, R.L., Reeves, C.K., Jones, E.G. and Ye, Z.-H. (2011a) Transcriptional activation of secondary wall biosynthesis by rice and maize NAC and MYB transcription factors. Plant Cell Physiol. 52, 1856-1871.
70. Zhong, R., McCarthy, R.L., Lee, C. and Ye, Z.-H. (2011b) Dissection of the transcriptional program regulating secondary wall biosynthesis during wood formation in poplar. Plant Physiol. 157, 1452-1468.