Engineering temporal accumulation of a low recalcitrance polysaccharide leads to increased C6 sugar content in plant cell walls

Plant Biotechnology Journal

Volumn 13, Issue 7, 2015, Pages 903-914

  Vega Sánchez, Miguel E ^a   Loqué, Dominique ^a   Lao, Jeemeng ^a   Catena, Michela ^a   Verhertbruggen, Yves ^a   Herter, Thomas ^a   Yang, Fan ^a,f   Harholt, Jesper ^b   Ebert, Berit ^a,b   Baidoo, Edward E K ^a   Keasling, Jay D ^a,c   Scheller, Henrik V ^a,d   Heazlewood, Joshua L ^a   Ronald, Pamela C ^a,e  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c University of California at Berkeley   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f OHIO STATE UNIVERSITY   (United States)

Author keywords

CslF6; Bioenergy; Cell wall engineering; Gluconic acid; Mixed linkage glucan; Senescence associated promoter

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; HORDEUM; HORDEUM VULGARE; MAGNOLIOPHYTA; POACEAE;

GLUCAN; POLYSACCHARIDE;

AGING; CELL WALL; CHEMISTRY; GENETICS; METABOLISM; PHYSIOLOGY; PLANT CELL; TRANSGENIC PLANT;

AGING; CELL WALL; GLUCANS; PLANT CELLS; PLANTS, GENETICALLY MODIFIED; POLYSACCHARIDES;

EID: 84934914959     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12326     Document Type: Article

References (45)

1. Bechtold, N. and Pelletier, G. (1998) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol. Biol. 82, 259-266.
2. Burton, R.A., Wilson, S.M., Hrmova, M., Harvey, A.J., Shirley, N.J., Medhurst, A., Stone, B.A., Newbigin, E.J., Bacic, A. and Fincher, G.B. (2006) Cellulose synthase-like CslF genes mediate the synthesis of cell wall (1, 3;1, 4)-beta-D-glucans. Science, 311, 1940-1942.
3. Burton, R.A., Collins, H.M., Kibble, N.A., Smith, J.A., Shirley, N.J., Jobling, S.A., Henderson, M., Singh, R.R., Pettolino, F., Wilson, S.M., Bird, A.R., Topping, D.L., Bacic, A. and Fincher, G.B. (2011) Over-expression of specific HvCslF cellulose synthase-like genes in transgenic barley increases the levels of cell wall (1, 3;1, 4)-beta-d-glucans and alters their fine structure. Plant Biotechnol. J. 9, 117-135.
4. Cannella, D., Hsieh, C.W., Felby, C. and Jorgensen, H. (2012) Production and effect of aldonic acids during enzymatic hydrolysis of lignocellulose at high dry matter content. Biotechnol. Biofuels 5, 26.
5. Carpita, N.C. (1996) Structure and biogenesis of the cell walls of grasses. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 445-476.
6. Carpita, N.C., Defernez, M., Findlay, K., Wells, B., Shoue, D.A., Catchpole, G., Wilson, R.H. and McCann, M.C. (2001) Cell wall architecture of the elongating maize coleoptile. Plant Physiol. 127, 551-565.
7. Chen, F. and Dixon, R.A. (2007) Lignin modification improves fermentable sugar yields for biofuel production. Nat. Biotechnol. 25, 759-761.
8. Chiniquy, D., Sharma, V., Schultink, A., Baidoo, E.E., Rautengarten, C., Cheng, K., Carroll, A., Ulvskov, P., Harholt, J., Keasling, J.D., Pauly, M., Scheller, H.V. and Ronald, P.C. (2012) XAX1 from glycosyltransferase family 61 mediates xylosyltransfer to rice xylan. Proc. Natl Acad. Sci. USA 109, 17117-17122.
9. Chuck, G.S., Tobias, C., Sun, L., Kraemer, F., Li, C., Dibble, D., Arora, R., Bragg, J.N., Vogel, J.P., Singh, S., Simmons, B.A., Pauly, M. and Hake, S. (2011) Overexpression of the maize Corngrass1 microRNA prevents flowering, improves digestibility, and increases starch content of switchgrass. Proc. Natl Acad. Sci. USA 108, 17550-17555.
10. Collins, H.M., Burton, R.A., Topping, D.L., Liao, M.L., Bacic, A. and Fincher, G.B. (2010) Variability in fine structures of noncellulosic cell wall polysaccharides from cereal grains: potential importance in human health and nutrition. Cereal Chem. 87, 272-282.
11. Doblin, M.S., Pettolino, F.A., Wilson, S.M., Campbell, R., Burton, R.A., Fincher, G.B., Newbigin, E. and Bacic, A. (2009) A barley cellulose synthase-like CSLH gene mediates (1, 3;1, 4)-beta-D-glucan synthesis in transgenic Arabidopsis. Proc. Natl Acad. Sci. USA 106, 5996-6001.
12. Doblin, M.S., Johnson, K.L., Humphries, J., Newbigin, E. and Bacic, A. (2014) Are designer plant cell walls a realistic aspiration or will the plasticity of the plant's metabolism win out? Curr. Opin. Biotechnol. 26, 108-114.
13. Earley, K.W., Haag, J.R., Pontes, O., Opper, K., Juehne, T., Song, K. and Pikaard, C.S. (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45, 616-629.
14. Eudes, A., George, A., Mukerjee, P., Kim, J.S., Pollet, B., Benke, P.I., Yang, F., Mitra, P., Sun, L., Cetinkol, O.P., Chabout, S., Mouille, G., Soubigou-Taconnat, L., Balzergue, S., Singh, S., Holmes, B.M., Mukhopadhyay, A., Keasling, J.D., Simmons, B.A., Lapierre, C., Ralph, J. and Loque, D. (2012) Biosynthesis and incorporation of side-chain-truncated lignin monomers to reduce lignin polymerization and enhance saccharification. Plant Biotechnol. J. 10, 609-620.
15. Eudes, A., Liang, Y., Mitra, P. and Loque, D. (2014) Lignin bioengineering. Curr. Opin. Biotechnol. 26C, 189-198.
16. Fahnenstich, H., Saigo, M., Niessen, M., Zanor, M.I., Andreo, C.S., Fernie, A.R., Drincovich, M.F., Flugge, U.I. and Maurino, V.G. (2007) Alteration of organic acid metabolism in Arabidopsis overexpressing the maize C4 NADP-malic enzyme causes accelerated senescence during extended darkness. Plant Physiol. 145, 640-652.
17. Fiehn, O., Kopka, J., Trethewey, R.N. and Willmitzer, L. (2000) Identification of uncommon plant metabolites based on calculation of elemental compositions using gas chromatography and quadrupole mass spectrometry. Anal. Chem. 72, 3573-3580.
18. Fincher, G.B. (2009) Exploring the evolution of (1, 3;1, 4)-beta-D-glucans in plant cell walls: comparative genomics can help!. Curr. Opin. Plant Biol. 12, 140-147.
19. Goubet, F., Barton, C.J., Mortimer, J.C., Yu, X., Zhang, Z., Miles, G.P., Richens, J., Liepman, A.H., Seffen, K. and Dupree, P. (2009) Cell wall glucomannan in Arabidopsis is synthesised by CSLA glycosyltransferases, and influences the progression of embryogenesis. Plant J. 60, 527-538.
20. Grbic, V. (2003) SAG2 and SAG12 protein expression in senescing Arabidopsis plants. Physiol. Plant. 119, 263-269.
21. Himmel, M.E., Ding, S.Y., Johnson, D.K., Adney, W.S., Nimlos, M.R., Brady, J.W. and Foust, T.D. (2007) Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science, 315, 804-807.
22. Iwase, A., Hideno, A., Watanabe, K., Mitsuda, N. and Ohme-Takagi, M. (2009) A chimeric NST repressor has the potential to improve glucose productivity from plant cell walls. J. Biotechnol. 142, 279-284.
23. Juminaga, D., Baidoo, E.E., Redding-Johanson, A.M., Batth, T.S., Burd, H., Mukhopadhyay, A., Petzold, C.J. and Keasling, J.D. (2012) Modular engineering of L-tyrosine production in Escherichia coli. Appl. Environ. Microbiol. 78, 89-98.
24. Lim, P.O., Kim, H.J. and Nam, H.G. (2007) Leaf senescence. Annu. Rev. Plant Biol. 58, 115-136.
25. Liwanag, A.J., Ebert, B., Verhertbruggen, Y., Rennie, E.A., Rautengarten, C., Oikawa, A., Andersen, M.C., Clausen, M.H. and Scheller, H.V. (2012) Pectin biosynthesis: GALS1 in Arabidopsis thaliana is a beta-1, 4-galactan beta-1, 4-galactosyltransferase. Plant Cell, 24, 5024-5036.
26. Lohman, K.N., Gan, S.S., John, M.C. and Amasino, R.M. (1994) Molecular analysis of natural leaf senescence in Arabidopsis thaliana. Physiol. Plant. 92, 322-328.
27. Meikle, P.J., Hoogenraad, N.J., Bonig, I., Clarke, A.E. and Stone, B.A. (1994) A (1->3, 1->4)-beta-glucan-specific monoclonal antibody and its use in the quantitation and immunocytochemical location of (1->3, 1->4)-beta-glucans. Plant J. 5, 1-9.
28. 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.
29. Noh, Y.S. and Amasino, R.M. (1999) Identification of a promoter region responsible for the senescence-specific expression of SAG12. Plant Mol. Biol. 41, 181-194.
30. Pauly, M. and Keegstra, K. (2010) Plant cell wall polymers as precursors for biofuels. Curr. Opin. Plant Biol. 13, 305-312.
31. Petersen, P.D., Lau, J., Ebert, B., Yang, F., Verhertbruggen, Y., Kim, J.S., Varanasi, P., Suttangkakul, A., Auer, M., Loque, D. and Scheller, H.V. (2012) Engineering of plants with improved properties as biofuels feedstocks by vessel-specific complementation of xylan biosynthesis mutants. Biotechnol. Biofuels 5, 84.
32. Ramachandran, S., Fontanille, P., Pandey, A. and Larroche, C. (2006) Gluconic acid: properties, applications and microbial production. Food Technol. Biotechnol. 44, 185-195.
33. Sanchez, D.H., Siahpoosh, M.R., Roessner, U., Udvardi, M. and Kopka, J. (2008) Plant metabolomics reveals conserved and divergent metabolic responses to salinity. Physiol. Plant. 132, 209-219.
34. Scheller, H.V. and Ulvskov, P. (2010) Hemicelluloses. Annu. Rev. Plant Biol. 61, 263-289.
35. Sorensen, I., Pettolino, F.A., Wilson, S.M., Doblin, M.S., Johansen, B., Bacic, A. and Willats, W.G. (2008) Mixed-linkage (1->3), (1->4)-beta-D-glucan is not unique to the Poales and is an abundant component of Equisetum arvense cell walls. Plant J. 54, 510-521.
36. Taketa, S., Yuo, T., Tonooka, T., Tsumuraya, Y., Inagaki, Y., Haruyama, N., Larroque, O. and Jobling, S.A. (2012) Functional characterization of barley betaglucanless mutants demonstrates a unique role for CslF6 in (1, 3;1, 4)-beta-D-glucan biosynthesis. J. Exp. Bot. 63, 381-392.
37. Taylor, N.G., Howells, R.M., Huttly, A.K., Vickers, K. and Turner, S.R. (2003) Interactions among three distinct CesA proteins essential for cellulose synthesis. Proc. Natl Acad. Sci. USA 100, 1450-1455.
38. Vega-Sanchez, M.E. and Ronald, P.C. (2010) Genetic and biotechnological approaches for biofuel crop improvement. Curr. Opin. Biotechnol. 21, 218-224.
39. Vega-Sanchez, M.E., Verhertbruggen, Y., Christensen, U., Chen, X., Sharma, V., Varanasi, P., Jobling, S.A., Talbot, M., White, R.G., Joo, M., Singh, S., Auer, M., Scheller, H.V. and Ronald, P.C. (2012) Loss of Cellulose synthase-like F6 function affects mixed-linkage glucan deposition, cell wall mechanical properties, and defense responses in vegetative tissues of rice. Plant Physiol. 159, 56-69.
40. Vega-Sanchez, M.E., Verhertbruggen, Y., Scheller, H.V. and Ronald, P.C. (2013) Abundance of mixed linkage glucan in mature tissues and secondary cell walls of grasses. Plant Signal. Behav. 8, e23143.
41. Weise, S.E., Aung, K., Jarou, Z.J., Mehrshahi, P., Li, Z., Hardy, A.C., Carr, D.J. and Sharkey, T.D. (2012) Engineering starch accumulation by manipulation of phosphate metabolism of starch. Plant Biotechnol. J. 10, 545-554.
42. Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G.V. and Provart, N.J. (2007) An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS ONE, 2, e718.
43. Xue, L.J., Guo, W., Yuan, Y., Anino, E.O., Nyamdari, B., Wilson, M.C., Frost, C.J., Chen, H.Y., Babst, B.A., Harding, S.A. and Tsai, C.J. (2013) Constitutively elevated salicylic acid levels alter photosynthesis and oxidative state but not growth in transgenic populus. Plant Cell, 25, 2714-2730.
44. Yang, F., Mitra, P., Zhang, L., Prak, L., Verhertbruggen, Y., Kim, J.S., Sun, L., Zheng, K., Tang, K., Auer, M., Scheller, H.V. and Loque, D. (2013) Engineering secondary cell wall deposition in plants. Plant Biotechnol. J. 11, 325-335.
45. Young, E., Lee, S.M. and Alper, H. (2010) Optimizing pentose utilization in yeast: the need for novel tools and approaches. Biotechnol. Biofuels 3, 24.