Dynamics of biomass partitioning, stem gene expression, cell wall biosynthesis, and sucrose accumulation during development of Sorghum bicolor

Plant Journal

Volumn 88, Issue 4, 2016, Pages 662-680

  McKinley, Brian ^a   Rooney, William ^a   Wilkerson, Curtis ^b   Mullet, John ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

bioenergy; cell wall biology; Sorghum bicolor; stem sucrose; transcriptome analysis; vacuolar invertase

Indexed keywords

BIOCHEMISTRY; BIOMASS; BIOSYNTHESIS; CYTOLOGY; ECOLOGY; ENCODING (SYMBOLS); SIGNAL ENCODING; STEM CELLS; SUGAR (SUCROSE); TRANSCRIPTION;

BIO-ENERGY; CELL WALLS; SORGHUM BICOLOR; TRANSCRIPTOME ANALYSIS; VACUOLAR INVERTASE;

GENE ENCODING;

GLYCOSYLTRANSFERASE; SUCROSE; XYLOGLUCAN - XYLOGLUCOSYLTRANSFERASE;

BIOMASS; CELL WALL; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; PLANT LEAF; PLANT STEM; SORGHUM;

BIOMASS; CELL WALL; GENE EXPRESSION REGULATION, PLANT; GLYCOSYLTRANSFERASES; PLANT LEAVES; PLANT STEMS; SORGHUM; SUCROSE;

EID: 84986543675     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.13269     Document Type: Article

References (103)

1. Anders, N., Wilkinson, M.D., Lovegrove, A. et al. (2012) Glycosyl transferases in family 61 mediate arabinofuranosyl transfer onto xylan in grasses. Proc. Natl Acad. Sci. USA, 109, 989–993.
2. Arundale, R.A., Bauer, S., Haffner, F.B., Mitchell, V.D., Voigt, T.B. and Long, S.P. (2015) Environment has little effect on biomass biochemical composition of Miscanthus× giganteus across soil types, nitrogen fertilization, and times of harvest. Bioenergy Res. 8, 1636–1646.
3. Bartley, L.E., Peck, M.L., Kim, S.R. et al. (2013) Overexpression of a BAHD acyltransferase, OsAt10, alters rice cell wall hydroxycinnamic acid content and saccharification. Plant Physiol. 161, 1615–1633.
4. Berthet, S., Demont-Caulet, N., Pollet, B. et al. (2011) Disruption of LACCASE4 and 17 results in tissue-specific alterations to lignification of Arabidopsis thaliana stems. Plant Cell, 23, 1124–1137.
5. Biswal, A.K., Hao, Z.Y., Pattathil, S. et al. (2015) Downregulation of GAUT12 in Populus deltoides by RNA silencing results in reduced recalcitrance, increased growth and reduced xylan and pectin in a woody biofuel feedstock. Biotechnol. Biofuels, 8, 41.
6. Boyle, M.G., Boyer, J.S. and Morgan, P.W. (1991) Stem infusion of liquid culture medium prevents reproductive failure of maize at low water potential. Crop Sci. 31, 1246–1252.
7. Bromley, J.R., Busse-Wicher, M., Tryfona, T., Mortimer, J.C., Zhang, Z., Brown, D.M. and Dupree, P. (2013) GUX1 and GUX2 glucuronyltransferases decorate distinct domains of glucuronoxylan with different substitution patterns. Plant J. 74, 423–434.
8. Burton, R.A. and Fincher, G.B. (2012) Current challenges in cell wall biology in the cereals and grasses. Front. Plant Sci. 3, 130.
9. 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.
10. Byrt, C.S., Grof, C.P.L. and Furbank, R.T. (2011) C-4 plants as biofuel feedstocks: optimising biomass production and feedstock quality from a lignocellulosic perspectivefree access. J. Integr. Plant Biol. 53, 120–135.
11. Calvino, M., Bruggmann, R. and Messing, J. (2008) Screen of genes linked to high-sugar content in stems by comparative genomics. Rice, 1, 166–176.
12. Calvino, M., Bruggmann, R. and Messing, J. (2011) Characterization of the small RNA component of the transcriptome from grain and sweet sorghum stems. BMC Genom., 12, 356.
13. Carpita, N.C. (1996) Structure and biogenesis of the cell walls of grasses. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 445–476.
14. Chen, X.Y. and Kim, J.Y. (2009) Callose synthesis in higher plants. Plant Signal. Behav. 4, 489–492.
15. Chiniquy, D., Sharma, V., Schultink, A. et al. (2012) XAX1 from glycosyltransferase family 61 mediates xylosyltransfer to rice xylan. Proc. Natl Acad. Sci. USA, 109, 17117–17122.
16. Dien, B.S., Sarath, G., Pedersen, J.F., Sattler, S.E., Chen, H., Funnell-Harris, D.L., Nichols, N.N. and Cotta, M.A. (2009) Improved sugar conversion and ethanol yield for forage Sorghum (Sorghum bicolor L. Moench) lines with reduced lignin contents. Bioenergy Res. 2, 153–164.
17. Dionex. (2003) The determination of sugars in molasses by high-performance anion exchange with pulsed amperometric detection, Application Note 92. Available at: http://www.dionex.com/en-us/webdocs/4666-AN92_LPN0565.pdf.
18. Duncan, R.R., Bockholt, A.J. and Miller, F.R. (1981) Descriptive comparison of senescent and non-senescent sorghum genotypes. Agron. J. 73, 849–853.
19. Ebert, B., Rautengarten, C., Guo, X.Y. et al. (2015) Identification and characterization of a golgi-localized UDP-xylose transporter family from Arabidopsis. Plant Cell, 27, 1218–1227.
20. Ermawar, R.A., Collins, H.M., Byrt, C.S., Betts, N.S., Henderson, M., Shirley, N.J., Schwerdt, J., Lahnstein, J., Fincher, G.B. and Burton, R.A. (2015) Distribution, structure and biosynthetic gene families of (1,3;1,4)-beta-glucan in Sorghum bicolor. J. Integr. Plant Biol. 57, 429–445.
21. Gill, J.R., Burks, P.S., Staggenborg, S.A., Odvody, G.N., Heiniger, R.W., Macoon, B., Moore, K.J., Barrett, M. and Rooney, W.L. (2014) Yield results and stability analysis from the sorghum regional biomass feedstock trial. Bioenergy Res. 7, 1026–1034.
22. Gille, S., de Souza, A., Xiong, G., Benz, M., Cheng, K., Schultink, A., Reca, I.B. and Pauly, M. (2011) O-acetylation of Arabidopsis hemicellulose xyloglucan requires AXY4 or AXY4L, proteins with a TBL and DUF231 domain. Plant Cell, 23, 4041–4053.
23. Gnansounou, E. and Dauriat, A. (2010) Techno-economic analysis of lignocellulosic ethanol: a review. Bioresour. Technol. 101, 4980–4991.
24. 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.
25. Gutjahr, S., Clement-Vidal, A., Soutiras, A., Sonderegger, N., Braconnier, S., Dingkuhn, M. and Luquet, D. (2013) Grain, sugar and biomass accumulation in photoperiod-sensitive sorghums. II. Biochemical processes at internode level and interaction with phenology. Funct. Plant Biol. 40, 355–368.
26. Harrison, R.L. and Miller, F.R. (1993) Registration of della sweet Sorghum. Crop Sci. 33, 1416–1416.
27. 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 Agr. 79, 891–899.
28. Hirano, K., Aya, K., Morinaka, Y., Nagamatsu, S., Sato, Y., Antonio, B.A., Namiki, N., Nagamura, Y. and Matsuoka, M. (2013) Survey of genes involved in rice secondary cell wall formation through a co-expression network. Plant Cell Physiol. 54, 1803–1821.
29. HoffmannThoma, G., Hinkel, K., Nicolay, P. and Willenbrink, J. (1996) Sucrose accumulation in sweet sorghum stem internodes in relation to growth. Physiol. Plant. 97, 277–284.
30. Hrmova, M. and Fincher, G.B. (2001) Structure-function relationships of beta-D-glucan endo- and exohydrolases from higher plants. Plant Mol. Biol. 47, 73–91.
31. Jackson, D.R., Arthur, M.F., Davis, M., Kresovich, S., Lawhon, W.T., Lipinsky, E.S., Price, M. and Rudolph, A. (1980) Research Report on Development of Sweet Sorghum as an Energy Crop Volume I: Agricultural Task. Battele, Columbus: USDOE, U.S. Department of Commerce.
32. Jiang, S.Y., Ma, Z., Vanitha, J. and Ramachandran, S. (2013) Genetic variation and expression diversity between grain and sweet sorghum lines. BMC Genom., 14, 18.
33. Jung, H.G. and Phillips, R.L. (2010) Putative Seedling Ferulate Ester (sfe) Maize mutant: morphology, biomass yield, and stover cell wall composition and rumen degradability. Crop Sci. 50, 403–418.
34. Jung, H.J.G., Samac, D.A. and Sarath, G. (2012) Modifying crops to increase cell wall digestibility. Plant Sci. 185, 65–77.
35. Kebrom, T.H. and Mullet, J.E. (2016) Transcriptome profiling of tiller buds provides new insights into PhyB regulation of tillering and indeterminate growth in Sorghum. Plant Physiol. 170, 2232–2250.
36. Knoller, A.S., Blakeslee, J.J., Richards, E.L., Peer, W.A. and Murphy, A.S. (2010) Brachytic2/ZmABCB1 functions in IAA export from intercalary meristems. J. Exp. Bot. 61, 3689–3696.
37. Lee, C., Teng, Q., Zhong, R. and Ye, Z.H. (2011) The four Arabidopsis reduced wall acetylation genes are expressed in secondary wall-containing cells and required for the acetylation of xylan. Plant Cell Physiol. 52, 1289–1301.
38. Li, X., Weng, J.K. and Chapple, C. (2008) Improvement of biomass through lignin modification. Plant J. 54, 569–581.
39. Li, M., Xiong, G., Li, R., Cui, J., Tang, D., Zhang, B., Pauly, M., Cheng, Z. and Zhou, Y. (2009) Rice cellulose synthase-like D4 is essential for normal cell-wall biosynthesis and plant growth. Plant J. 60, 1055–1069.
40. Liepman, A.H. and Cavalier, D.M. (2012) The CELLULOSE SYNTHASE-LIKE A and CELLULOSE SYNTHASE-LIKE C families: recent advances and future perspectives. Front. Plant Sci. 3, 109.
41. Lingle, S.E. (1987) Sucrose metabolism in the primary culm of sweet Sorghum during development. Crop Sci. 27, 1214–1219.
42. Lingle, S.E. (1989) Evidence for the uptake of sucrose intact into sugarcane internodes. Plant Physiol. 90, 6–8.
43. Lionetti, V., Francocci, F., Ferrari, S., Volpi, C., Bellincampi, D., Galletti, R., D'Ovidio, R., De Lorenzo, G. and Cervone, F. (2010) Engineering the cell wall by reducing de-methyl-esterified homogalacturonan improves saccharification of plant tissues for bioconversion. Proc. Natl Acad. Sci. USA, 107, 616–621.
44. Martin, A.P., Palmer, W.M., Byrt, C.S., Furbank, R.T. and Grof, C.P.L. (2013) A holistic high-throughput screening framework for biofuel feedstock assessment that characterises variations in soluble sugars and cell wall composition in Sorghum bicolor. Biotechnol. Biofuels, 6, 186.
45. Mcbee, G.G. and Miller, F.R. (1982) Carbohydrates in Sorghum culms as influenced by cultivars, spacing, and maturity over a diurnal period. Crop Sci. 22, 381–385.
46. McCann, M.C. and Carpita, N.C. (2015) Biomass recalcitrance: a multi-scale, multi-factor, and conversion-specific property. J. Exp. Bot. 66, 4109–4118.
47. McQueen-Mason, S.J. and Cosgrove, D.J. (1995) Expansin mode of action on cell walls. Analysis of wall hydrolysis, stress relaxation, and binding. Plant Physiol. 107, 87–100.
48. Mitchell, R.A., Dupree, P. and Shewry, P.R. (2007) A novel bioinformatics approach identifies candidate genes for the synthesis and feruloylation of arabinoxylan. Plant Physiol. 144, 43–53.
49. Monk, R.L., Miller, F.R. and Mcbee, G.G. (1984) Sorghum improvement for energy-production. Biomass, 6, 145–153.
50. Moore, P.H. (1995) Temporal and spatial regulation of sucrose accumulation in the sugarcane stem. Aust. J. Plant Physiol. 22, 661–679.
51. Mullet, J., Morishige, D., McCormick, R., Truong, S., Hilley, J., McKinley, B., Anderson, R., Olson, S. and Rooney, W. (2014) Energy Sorghum—a genetic model for the design of C4 grass bioenergy crops. J. Exp. Bot. 65, 3479–3489.
52. Murphy, R.L., Klein, R.R., Morishige, D.T., Brady, J.A., Rooney, W.L., Miller, F.R., Dugas, D.V., Klein, P.E. and Mullet, J.E. (2011) Coincident light and clock regulation of pseudoresponse regulator protein 37 (PRR37) controls photoperiodic flowering in sorghum. Proc. Natl Acad. Sci. USA, 108, 16469–16474.
53. Murphy, R.L., Morishige, D.T., Brady, J.A., Rooney, W.L., Yang, S., Klein, P.E. and Mullet, J.E. (2014) Represses Sorghum flowering in long days: alleles enhance biomass accumulation and grain production. Plant Genome, 7, 1–10.
54. Murray, S.C., Sharma, A., Rooney, W.L., Klein, P.E., Mullet, J.E., Mitchell, S.E. and Kresovich, S. (2008) Genetic improvement of Sorghum as a biofuel feedstock: I. QTL for stem sugar and grain nonstructural carbohydrates. Crop Sci. 48, 2165–2179.
55. Murray, S.C., Rooney, W.L., Hamblin, M.T., Mitchell, S.E. and Kresovich, S. (2009) Sweet Sorghum genetic diversity and association mapping for brix and height. Plant Genome, 2, 48–62.
56. Olson, S.N., Ritter, K., Rooney, W., Kemanian, A., McCarl, B.A., Zhang, Y., Hall, S., Packer, D. and Mullet, J. (2012) High biomass yield energy sorghum: developing a genetic model for C4 grass bioenergy crops. Biofuels, Bioprod. Biorefin. 6, 640–655.
57. Olson, S.N., Ritter, K., Medley, J., Wilson, T., Rooney, W.L. and Mullet, J.E. (2013) Energy sorghum hybrids: functional dynamics of high nitrogen use efficiency. Biomass Bioenergy, 56, 307–316.
58. Park, Y.B. and Cosgrove, D.J. (2015) Xyloglucan and its interactions with other components of the growing cell wall. Plant Cell Physiol. 56, 180–194.
59. Paterson, A.H., Bowers, J.E., Bruggmann, R. et al. (2009) The Sorghum bicolor genome and the diversification of grasses. Nature, 457, 551–556.
60. Pauly, M. and Keegstra, K. (2008) Cell-wall carbohydrates and their modification as a resource for biofuels. Plant J. 54, 559–568.
61. Penning, B.W., Hunter, C.T. 3rd, Tayengwa, R. et al. (2009) Genetic resources for maize cell wall biology. Plant Physiol. 151, 1703–1728.
62. Perlack, R.D., Eaton, L.M., Turhollow, A.F. Jr et al. (2011) US billion-ton update: biomass supply for a bioenergy and bioproducts industry. Digital Repository at Iowa State University, pp. 1–195.
63. Persson, S., Paredez, A., Carroll, A., Palsdottir, H., Doblin, M., Poindexter, P., Khitrov, N., Auer, M. and Somerville, C.R. (2007) Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proc. Natl Acad. Sci. USA, 104, 15566–15571.
64. Qazi, H.A., Paranjpe, S. and Bhargava, S. (2012) Stem sugar accumulation in sweet sorghum - activity and expression of sucrose metabolizing enzymes and sucrose transporters. J. Plant Physiol. 169, 605–613.
65. Quinby, J.R. (1974) Sorghum improvement and the genetics of growth. College Station, TX: Texas Agricultural Experiment Station, pp. 1–122.
66. Rennie, E.A. and Scheller, H.V. (2014) Xylan biosynthesis. Curr. Opin. Biotechnol. 26, 100–107.
67. Rennie, E.A., Hansen, S.F., Baidoo, E.E., Hadi, M.Z., Keasling, J.D. and Scheller, H.V. (2012) Three members of the Arabidopsis glycosyltransferase family 8 are xylan glucuronosyltransferases. Plant Physiol. 159, 1408–1417.
68. Ritter, K.B., Jordan, D.R., Chapman, S.C., Godwin, I.D., Mace, E.S. and McIntyre, C.L. (2008) Identification of QTL for sugar-related traits in a sweet x grain sorghum (Sorghum bicolor L. Moench) recombinant inbred population. Mol. Breeding, 22, 367–384.
69. Robinson, M.D., McCarthy, D.J. and Smyth, G.K. (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26, 139–140.
70. Rooney, W.L., Blumenthal, J., Bean, B. and Mullet, J.E. (2007) Designing sorghum as a dedicated bioenergy feedstock. Biofuel Bioprod. Bior. 1, 147–157.
71. Roudier, F., Fernandez, A.G., Fujita, M. et al. (2005) COBRA, an Arabidopsis extracellular glycosyl-phosphatidyl inositol-anchored protein, specifically controls highly anisotropic expansion through its involvement in cellulose microfibril orientation. Plant Cell, 17, 1749–1763.
72. Ruan, Y.L., Jin, Y., Yang, Y.J., Li, G.J. and Boyer, J.S. (2010) Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat. Mol. Plant, 3, 942–955.
73. Saballos, A., Sattler, S.E., Sanchez, E., Foster, T.P., Xin, Z.G., Kang, C., Pedersen, J.F. and Vermerris, W. (2012) Brown midrib2 (Bmr2) encodes the major 4-coumarate:coenzyme A ligase involved in lignin biosynthesis in sorghum (Sorghum bicolor (L.) Moench). Plant J. 70, 818–830.
74. Sage, R.F. and Zhu, X.G. (2011) Exploiting the engine of C(4) photosynthesis. J. Exp. Bot. 62, 2989–3000.
75. Sattler, S.E., Saathoff, A.J., Haas, E.J., Palmer, N.A., Funnell-Harris, D.L., Sarath, G. and Pedersen, J.F. (2009) A nonsense mutation in a cinnamyl alcohol dehydrogenase gene is responsible for the sorghum brown midrib6 phenotype. Plant Physiol. 150, 584–595.
76. Sattler, S.E., Palmer, N.A., Saballos, A., Greene, A.M., Xin, Z.G., Sarath, G., Vermerris, W. and Pedersen, J.F. (2012) Identification and characterization of four missense mutations in Brown midrib 12 (Bmr12), the Caffeic O-Methyltranferase (COMT) of Sorghum. Bioenergy Res. 5, 855–865.
77. Shen, H., Mazarei, M., Hisano, H., Escamilla-Trevino, L., Fu, C., Pu, Y., Rudis, M.R., Tang, Y., Xiao, X. and Jackson, L. (2013) A genomics approach to deciphering lignin biosynthesis in switchgrass. Plant Cell, 25, 4342–4361.
78. Shiringani, A.L. and Friedt, W. (2011) QTL for fibre-related traits in grain× sweet sorghum as a tool for the enhancement of sorghum as a biomass crop. Theor. Appl. Genet. 123, 999–1011.
79. Slewinski, T.L. (2012) Non-structural carbohydrate partitioning in grass stems: a target to increase yield stability, stress tolerance, and biofuel production. J. Exp. Bot. 63, 4647–4670.
80. Sluiter, A. and Sluiter, J. (2005) Determination of starch in solid biomass samples by HPLC. NREL Laboratory Analytical Procedure. http://devafdc.nrel.gov/pdfs/9360.pdf.
81. Stefaniak, T.R., Dahlberg, J.A., Bean, B.W., Dighe, N., Wolfrum, E.J. and Rooney, W.L. (2012) Variation in biomass composition components among forage, biomass, sorghum-sudangrass, and sweet sorghum types. Crop Sci. 52, 1949–1954.
82. Tanaka, K., Murata, K., Yamazaki, M., Onosato, K., Miyao, A. and Hirochika, H. (2003) Three distinct rice cellulose synthase catalytic subunit genes required for cellulose synthesis in the secondary wall. Plant Physiol. 133, 73–83.
83. Tarpley, L. and Vietor, D.M. (2007) Compartmentation of sucrose during radial transfer in mature sorghum culm. BMC Plant Biol. 7, 33.
84. Tarpley, L., Lingle, S.E., Vietor, D.M., Andrews, D.L. and Miller, F.R. (1994a) Enzymatic control of nonstructural carbohydrate concentrations in stems and panicles of sorghum. Crop Sci. 34, 446–452.
85. Tarpley, L., Vietor, D.M. and Miller, F.R. (1994b) Internodal compartmentation of stem-infused [C-14] sucrose in sweet and grain-sorghum. Crop Sci. 34, 1116–1120.
86. Taylor-Teeples, M., Lin, L., de Lucas, M. et al. (2015) An Arabidopsis gene regulatory network for secondary cell wall synthesis. Nature, 517, 571–575.
87. Vain, T., Crowell, E.F., Timpano, H. et al. (2014) The cellulase KORRIGAN is part of the cellulose synthase complex. Plant Physiol. 165, 1521–1532.
88. Vanderlip, R.L. and Reeves, H.E. (1972) Growth stages of sorghum [Sorghum bicolor,(L.) Moench.]. Agron. J. 64, 13–16.
89. Vanholme, R., Demedts, B., Morreel, K., Ralph, J. and Boerjan, W. (2010) Lignin biosynthesis and structure. Plant Physiol. 153, 895–905.
90. 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.
91. Vega-Sanchez, M.E., Loque, D., Lao, J.M. et al. (2015) Engineering temporal accumulation of a low recalcitrance polysaccharide leads to increased C6 sugar content in plant cell walls. Plant Biotechnol. J. 13, 903–914.
92. Vega-Sánchez, M.E., Verhertbruggen, Y., Christensen, U., Chen, X., Sharma, V., Varanasi, P., Jobling, S.A., Talbot, M., White, R.G. and Joo, M. (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.
93. Verhertbruggen, Y., Yin, L., Oikawa, A. and Scheller, H.V. (2011) Mannan synthase activity in the CSLD family. Plant Signal. Behav. 6, 1620–1623.
94. Vermerris, W., Thompson, K.J. and McIntyre, L.M. (2002) The maize Brown midrib1 locus affects cell wall composition and plant development in a dose-dependent manner. Heredity (Edinb), 88, 450–457.
95. 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.
96. Wang, M.L., Zhu, C.S., Barkley, N.A., Chen, Z.B., Erpelding, J.E., Murray, S.C., Tuinstra, M.R., Tesso, T., Pederson, G.A. and Yu, J.M. (2009) Genetic diversity and population structure analysis of accessions in the US historic sweet sorghum collection. Theor. Appl. Genet. 120, 13–23.
97. van der Weijde, T., Kamei, C.L.A., Torres, A.F., Vermerris, W., Dolstra, O., Visser, R.G.F. and Trindade, L.M. (2013) The potential of C4 grasses for cellulosic biofuel production. Front.Plant Sci. 4, 1–18.
98. Wilkerson, C.G., Mansfield, S.D., Lu, F. et al. (2014) Monolignol ferulate transferase introduces chemically labile linkages into the lignin backbone. Science, 344, 90–93.
99. Withers, S., Lu, F., Kim, H., Zhu, Y., Ralph, J. and Wilkerson, C.G. (2012) Identification of grass-specific enzyme that acylates monolignols with p-coumarate. J. Biol. Chem. 287, 8347–8355.
100. Wolfrum, E., Payne, C., Stefaniak, T., Rooney, W., Dighe, N., Bean, B. and Dahlberg, J. (2013) Multivariate calibration models for sorghum composition using near-infrared spectroscopy. Contract, 303, 1–8.
101. Wu, X.R., Staggenborg, S., Propheter, J.L., Rooney, W.L., Yu, J.M. and Wang, D.H. (2010) Features of sweet sorghum juice and their performance in ethanol fermentation. Ind. Crop Prod. 31, 164–170.
102. Zhang, B., Zhao, T., Yu, W., Kuang, B., Yao, Y., Liu, T., Chen, X., Zhang, W. and Wu, A.M. (2014) Functional conservation of the glycosyltransferase gene GT47A in the monocot rice. J. Plant. Res. 127, 423–432.
103. Zhu, Y.J., Komor, E. and Moore, P.H. (1997) Sucrose accumulation in the sugarcane stem is regulated by the difference between the activities of soluble acid invertase and sucrose phosphate synthase. Plant Physiol. 115, 609–616.