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Genetic Enhancement of Sorghum for Biomass Utilization

  • Wilfred VermerrisEmail author
  • Ana Saballos
Chapter
Part of the Plant Genetics and Genomics: Crops and Models book series (PGG, volume 11)

Abstract

Biomass produced from sorghum can be utilized as forage and silage to feed ruminant animals and as feedstock for biofuels and bio-based products. The efficiency of biomass utilization is a function of biomass composition and plant architecture. This chapter provides a description of the cell wall polymers that make up the bulk of sorghum biomass, along with information on the genes involved in their biosynthesis. The close evolutionary relationships among the grasses makes it possible to infer gene function across species. Newly developed genomics and bioinformatics resources offer exciting opportunities for the genetic enhancement of sorghum as a biomass crop.

Keywords

Biomass Bioenergy Biofuels Cell wall Forage Near infrared spectroscopy Pyrolysis Silage 

Notes

Acknowledgements

The authors gratefully acknowledge support from the Office of Science (BER), U.S. Department of Energy, grant DE-FG02-07ER64458 for the research on brown midrib genes and NIRS screening of sorghum mutants described in this chapter. We would also like to acknowledge the participation of several colleagues on this project: The sorghum leaf samples were collected by Dr. Ken Lamb (University of Florida) in collaboration with Dr. Zhanguo Xin (USDA-ARS, Lubbock, TX) and his research staff. We thank Drs. Bryan Penning and Nick Carpita (Purdue University) for sharing their most recent data on maize and sorghum CesA genes. The U.S. National Science Foundation Plant Genome Research Program (DBI-0217552) and the University of Florida provided funds to purchase the analytical equipment featured in this chapter.

References

  1. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657PubMedGoogle Scholar
  2. Appenzeller L, Doblin M, Barreiro R, Wang H, Niu X, Kollipara K, Carrigan L, Tomes D, Chapman M, Dhugga KS (2004) Cellulose synthesis in maize: isolation and expression analysis of the cellulose synthase (CesA) gene family. Cellulose 11:287–299Google Scholar
  3. Argillier O, Barrière Y, Hébert Y (1995) Genetic variation and selection criteria for digestibility traits of forage maize. Euphytica 82:175–184Google Scholar
  4. Arioli T, Peng L, Betzner AS, Burn J, Wittke W, Herth W, Camilleri C, Höfte H, Plazinski J, Birch R, Cork A, Glover J, Redmond J, Williamson RE (1998) Molecular analysis of cellulose biosynthesis in Arabidopsis. Science 279:717–720PubMedGoogle Scholar
  5. Ayyangar GNR, Ponnaiya BWX (1941) The occurrence and inheritance of a bloomless sorghum. Curr Sci 10:408–409Google Scholar
  6. Bai L, Singh M, Pitt L, Sweeney M, Brutnell TP (2007) Generating novel allelic variation through Activator insertional mutagenesis in maize. Genetics 175:981–992PubMedGoogle Scholar
  7. Barrière Y, Guillet C, Goffner D, Pichon M (2003) Genetic variation and breeding strategies for improved cell wall digestibility in annual forage crops. A review. Anim Res 52:193–228Google Scholar
  8. Boon JJ (1989) An introduction to pyrolysis mass spectrometry of lignocellulosic material: case studies of barley straw, corn stem and Agropyron. In: Chesson A, Ørskov ER (eds) Physico-chemical characterization of plant residues for industrial and feed use. Elsevier Applied Science, London, pp 25–49Google Scholar
  9. Bout S, Vermerris W (2003) A candidate gene-approach to clone the sorghum Brown midrib gene encoding caffeic acid O-methyltransferase. Mol Genet Genomics 269:205–214PubMedGoogle Scholar
  10. Brinkmann K, Blaschke L, Polle A (2002) Comparison of different methods for lignin determination as a basis for calibration of near-infrared reflectance spectroscopy and implications of lignoproteins. J Chem Ecol 28:2483–2501PubMedGoogle Scholar
  11. Brown L, Torget R (1996) Laboratory Analytical Protocol 009: enzymatic saccharification of lignocellulosic biomass. National Renewable Energy Laboratory, Golden, CO. http://www1.eere.energy.gov/analytical_procedures.html
  12. Burlison AJ, Hodgson J, Illius AW (1991) Sward canopy structure and the bite dimensions and bite weight of grazing sheep. Grass Forage Sci 46:29–38Google Scholar
  13. Burton RA, Wilson SM, Hrmova M, Harvey AJ, Shirley NJ, Medhurst A, Stone BA, Newbigin EJ, Bacic A, Fincher GB (2006) Cellulose synthase-like CslF genes mediate the synthesis of cell wall (1,3;1,4)-β-d-Glucans. Science 311:1940–1942PubMedGoogle Scholar
  14. Busk PK, Møller BL (2002) Dhurrin synthesis in sorghum is regulated at the transcriptional level and induced by nitrogen fertilization in older plants. Plant Physiol 129:1222–1231PubMedGoogle Scholar
  15. Cao P, Jung K-H, Ronald PC (2010) A survey of databases for analysis of plant cell wall-related enzymes. Bioenergy Res 3:108–114Google Scholar
  16. Carpita NC (1996) Structure and biogenesis of the cell walls of grasses. Annu Rev Plant Physiol Plant Mol Biol 47:445–476PubMedGoogle Scholar
  17. Carpita NC, Gibeaut DM (1993) Structural models of the primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the wall during growth. Plant J 3:1–30PubMedGoogle Scholar
  18. Carpita NC, McCann MC (2008) Maize and sorghum: genetic resources for bioenergy grasses. Trends Plant Sci 11:314–320Google Scholar
  19. Casler MD, Carpenter JA (1989) Morphological and chemical responses to selection for in vitro dry matter digestibility in smooth bromegrass. Crop Sci 29:924–928Google Scholar
  20. Chacon EA, Stobbs TH (1976) Influence of progressive defoliation of a grass sward in the eating behaviour of cattle. Aust J Agric Res 27:709–727Google Scholar
  21. Chen F, Dixon RA (2007) Lignin modification improves fermentable sugar yields for biofuel production. Nat Biotechnol 25:759–761PubMedGoogle Scholar
  22. Cherney JH, Cherney DJR, Akin DE, Axtell JD (1991a) Potential of brown-midrib, low-lignin mutants for improving forage quality. Adv Agron 46:157–198Google Scholar
  23. Cherney DJ, Mertens DR, Moore JE (1991b) Fluid and particulate retention times in sheep as influenced by intake level and forage morphological composition. J Anim Sci 69:413–422PubMedGoogle Scholar
  24. Cocuron JC, Lerouxel O, Drakakai G, Alonso AP, Liepman AH, Keegstra K, Raikhel N, Wilkerson CG (2007) A gene from the cellulose synthase-like C family encodes a β-1,4 glucan synthase. Proc Natl Acad Sci U S A 104:8550–8555PubMedGoogle Scholar
  25. Corredor DY, Salazar JM, Hohn KL, Bean S, Bean B, Wang D (2008) Evaluation and characterization of forage sorghum as feedstock for fermentable sugar production. Appl Biochem Biotechnol 158:164–179PubMedGoogle Scholar
  26. Dahlberg JA (2000) Classification and characterization of sorghum. In: Smith CW, Frederiksen RA (eds) Sorghum. Origin, history, technology, and production. Wiley, New York, pp 99–130Google Scholar
  27. Davison BH, Drescher SR, Tuskan GA, Davis MF, Nghiem NP (2006) Variation of S/G ratio and lignin content in a Populus family influences the release of xylose by dilute acid hydrolysis. Appl Biochem Biotechnol 129–132:427–435PubMedGoogle Scholar
  28. De Boever JL, Cottyn BG, Andries JI, Buysse FX, Vanacker JM (1988) The use of cellulase technique to predict digestibility, metabolizable and net energy of forage. Anim Feed Sci Technol 19:247–260Google Scholar
  29. Delmer DP (1999) Cellulose biosynthesis: Exciting times for a difficult field of study. Annu Rev Plant Physiol Plant Mol Biol 50:245–276Google Scholar
  30. Desprez T, Vernhettes S, Fagard M, Refregier G, Desnos T, Aletti E, Py N, Pelletier S, Höfte H (2002) Resistance against herbicide isoxaben and cellulose deficiency caused by distinct mutations in same cellulose synthase isoform CESA6. Plant Physiol 128:482–490PubMedGoogle Scholar
  31. Desprez T, Juraniec M, Crowell EF, Jouy H, Pochylova Z, Parcy F, Höfte H, Gonneau M, Vernhettes S (2007) Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana. Proc Natl Acad Sci U S A 104:15572–15577PubMedGoogle Scholar
  32. Dhugga KS, Barreiro R, Whitten B, Stecca K, Hazebroek J, Randhawa GS, Dolan M, Kinney AJ, Tomes D, Nichols S, Anderson P (2004) Guar seed β-mannan synthase is a member of the cellulose synthase super gene family. Science 303:363–366PubMedGoogle Scholar
  33. Dien BS, Sarath G, Pedersen JF, Satler SE, Chen H, Funnell-Harris DL, Nichols NN, Cotta MA (2009) Improved sugar conversion and ethanol yield for forage sorghum (Sorghum bicolor (L.) Moench) lines with reduced lignin contents. BioEnergy Res 2:153–164Google Scholar
  34. Ding SY, Himmel ME (2006) The maize primary cell wall microfibril: a new model derived from direct visualization. J Agric Food Chem 54:597–606PubMedGoogle Scholar
  35. Djè Y, Heuertz M, Lefèbvre C, Vekemans X (2000) Assessment of genetic diversity within and among germplasm accessions in cultivated sorghum using microsatellite markers. Theor Appl Genet 100:918–925Google Scholar
  36. Dowe N, McMillan J (2008) SSF Experimental Protocols - Lignocellulosic Biomass Hydrolysis and Fermentation. Laboratory Analytical Procedure (LAP). Technical Report NREL/TP-510-42630. http://www.nrel.gov/biomass/pdfs/42630.pdf Google Scholar
  37. Ehlke NJ, Casler MD (1985) Anatomical characteristics of smooth bromegrass clones selected for in vitro dry matter digestibility. Crop Sci 35:513–517Google Scholar
  38. Evans RJ, Milne TA (1987) Molecular characterization of the pyrolysis of biomass. 1. Fundamentals. Energy Fuel 1:123–137Google Scholar
  39. Ezeji TC, Qureshi N, Blaschek HP (2007) Bioproduction of butanol from biomass: from genes to bioreactors. Curr Opin Biotechnol 18:220–227PubMedGoogle Scholar
  40. Fagard M, Desnos T, Desprez T, Goubet F, Refregier G, Mouille G, McCann M, Rayon C, Vernhettes S, Höfte H (2000) PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis. Plant Cell 12:2409–2423PubMedGoogle Scholar
  41. Faik A (2010) Xylan biosynthesis: news from the grass. Plant Physiol 153:396–402PubMedGoogle Scholar
  42. Fincher GB (2009) Revolutionary times in our understanding of cell wall biosynthesis and remodeling in the grasses. Plant Physiol 149:27–37PubMedGoogle Scholar
  43. Fontaine AS, Bout S, Barrière Y, Vermerris W (2003) Variation in cell wall composition among forage maize (Zea Mays L.) inbred lines and its impact on digestibility. Analysis of neutral detergent fiber composition by pyrolysis-gas chromatography-mass spectrometry. J Agric Food Chem 51:8080–8087PubMedGoogle Scholar
  44. Gerhardt RL, Fritz JO, Moore KJ, Jaster EH (1994) Digestion kinetics and composition of normal and brown midrib sorghum morphological components. Crop Sci 34:1353–1361Google Scholar
  45. Girke T, Lauricha J, Tran H, Keegstra K, Raikhel N (2004) The cell wall navigator database. A systems-based approach to organism-unrestricted mining of protein families involved in cell wall metabolism. Plant Physiol 136:3003–3008PubMedGoogle Scholar
  46. Gorz HJ, Haskins FA, Vogel KP (1986) Inheritance of dhurrin contant in mature sorghum leaves. Crop Sci 26:65–67Google Scholar
  47. Gorz HJ, Haskins FA, Morris R, Johnson BE (1987) Identification of chromosomes that condition dhurrin content in sorghum seedlings. Crop Sci 27:201–203Google Scholar
  48. Grenier C, Bramel-Cox PJ, Hamon P (2001a) Core collection of sorghum. I. Stratification based on eco-geographical data. Crop Sci 41:234–240Google Scholar
  49. Grenier C, Hamon P, Bramel-Cox PJ (2001b) Core collection of sorghum. II. Comparison of three random sampling strategies. Crop Sci 41:241–246Google Scholar
  50. Guillaumie S, San-Clemente H, Deswarte C, Martinez Y, Lapierre C, Murgneux A, Barrière Y, Pichon M, Goffner D (2007) MAIZEWALL. Database and developmental gene expression profiling of cell wall biosynthesis and assembly in maize. Plant Physiol 143:339–363PubMedGoogle Scholar
  51. Hamelinck C, Faaij APC (2006) Production of methanol from biomass. In: Minteer S (ed) Alcoholic fuels. Taylor and Francis, Boca Raton, FL, pp 7–50Google Scholar
  52. Haney LJ, Coors JG, Lorenz AJ, Raman DR, Anex RP, Scott MP (2008) Development of a fluorescence-based method for monitoring glucose catabolism and its potential use in a biomass hydrolysis assay. Biotechnol Biofuels 1:17PubMedGoogle Scholar
  53. Hatfield R, Ralph J, Grabber JH (2008) A potential role for sinapyl p-coumarate as a radical transfer mechanism in grass lignin formation. Planta 228:919–928PubMedGoogle Scholar
  54. Holland N, Holland D, Helentjaris T, Dhugga KS, Xoconostle-Cazares B, Delmer DP (2000) A comparative analysis of the plant cellulose synthase (CesA) gene family. Plant Physiol 123:1313–1323PubMedGoogle Scholar
  55. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755PubMedGoogle Scholar
  56. Humphreys JM, Chapple C (2002) Rewriting the lignin road map. Curr Opin Plant Biol 5:224–229PubMedGoogle Scholar
  57. 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 U S A 96:10045–10050PubMedGoogle Scholar
  58. Jung HG, Mertens DR, Buxton DR (1998) Forage quality variation among maize inbreds: in vitro fiber digestion kinetics and prediction with NIRS. Crop Sci 38:205–210Google Scholar
  59. Kemsley EK (1998) Discriminant analysis and class modelling of spectroscopic data. Wiley, Chichester, UKGoogle Scholar
  60. Kim S-J, Kim M-R, Bedgar DL, Moinuddin SGA, Cardenas CL, Davin LB, Kang C, Lewis NG (2004) Functional reclassification of the putative cinnamyl alcohol dehydrogenase multigene family in Arabidopsis. Proc Natl Acad Sci U S A 101:1455–1460PubMedGoogle Scholar
  61. Kim J-S, Klein PE, Klein RR, Price HJ, Mullet JE, Stelly DM (2005) Chromosome identification and nomenclature of Sorghum bicolor. Genetics 169:1169–1173PubMedGoogle Scholar
  62. Kim CM, Park SH, Il JB, Park SH, Piao HL, Eun MY, Dolan L, Han CD (2007) OsCSLD1, a cellulose synthase-like D1 gene, is required for root hair morphogenesis in rice. Plant Physiol 143:1220–1230PubMedGoogle Scholar
  63. Knox JP (2008) Revealing the structural and functional diversity of plant cell walls. Curr Opin Plant Biol 11:308–318PubMedGoogle Scholar
  64. Lamb JF, Haskins FA, Gorz HJ, Vogel KP (1987) Inheritance of seedling hydrocyanic acid potential and seed weight in sorghum-sudangrass crosses. Crop Sci 27:522–525Google Scholar
  65. Li B-Z, Balan V, Yuan Y-J, Dale BE (2010) Process optimization to convert forage and sweet sorghum bagasse to ethanol based on ammonia fiber expansion (AFEX) pretreatment. Bioresour Technol 101:1285–1292PubMedGoogle Scholar
  66. Liepman AH, Wilkerson CG, Keegstra K (2005) Expression of cellulose synthase-like (Csl) genes in insect cells reveals that CslA family members encode mannan synthases. Proc Natl Acad Sci U S A 102:2221–2226PubMedGoogle Scholar
  67. Liu L, Ye XP, Womac AR, Sokhansanj S (2010) Variability of biomass chemical composition and rapid analysis using FT-NIR techniques. Carbohydr Polym 81:820–829Google Scholar
  68. Lorenzana RE, Friskop Lewis M, Jung H-HG, Bernardo R (2010) Quantitative trait loci and trait correlations for maize stover cell wall composition and glucose release for cellulosic ethanol. Crop Sci 50:541–555Google Scholar
  69. Lynd LR, van Zyl WH, McBride JE, Laser M (2005) Consolidated bioprocessing of cellulosic biomass: an update. Curr Opin Biotechnol 16:577–583PubMedGoogle Scholar
  70. Mann DGJ, Labbé N, Sykes RW, Gracom K, Kline L, Swamidoss IM, Burris JN, Davis M, Stewart CN (2009) Rapid assessment of lignin content and structure in switchgrass (Panicum virgatum L.) grown under different environmental conditions. Bioenergy Res 2:246–256Google Scholar
  71. Marita J, Vermerris W, Ralph J, Hatfield RD (2003) Variations in the cell wall composition of maize brown midrib mutants. J Agric Food Chem 51:1313–1321PubMedGoogle Scholar
  72. Marsalis MA, Angadi SV, Contreras-Govea FE (2010) Dry matter yield and nutritive value of corn, forage sorghum, and BMR forage sorghum at different plant populations and nitrogen rates. Field Crops Res 116:52–57Google Scholar
  73. McCarty DR, Settles AM, Suzuki M, Tan BC, Latshaw S, Porch T, Robin K, Baier J, Avigne W, Lai J (2005) Steady-state transposon mutagenesis in inbred maize. Plant J 44:52–61PubMedGoogle Scholar
  74. Menz MA, Klein RR, Unruh N, Rooney WL, Klein PE, Mullet JE (2004) Genetic diversity of public inbreeds of sorghum determined by mapped AFLP and SSR markers. Crop sci 44:1236–1244Google Scholar
  75. Miller GL (1959) Use of dinitrosalisylic acid reagent for determination of reducing sugars. Anal Chem 31:426–428Google Scholar
  76. Miron J, Zuckerman E, Adin G, Solomon R, Shoshani E, Nikbachat M, Yosef E, Zenou A, Gershon Weinberg Z, Chen Y, Halachmi I, Ben-Ghedalia D (2007) Comparison of two forage sorghum varieties with corn and the effect of feeding their silages on eating behavior and lactation performance of dairy cows. Anim Feed Sci Technol 139:23–39Google Scholar
  77. Mitchell RAC, Dupree P, Shewry PR (2007) A novel bioinformatics approach identifies candidate genes fo the synthesis and feruoylation of arabinoxylan. Plant Physiol 144:43–53PubMedGoogle Scholar
  78. Mohanraj K, Gopalan A, Shanmuganathan M (2006) Genetic parameters for hydrocyanic acid content in forage sorghum. J Agric Sci 6:59–62Google Scholar
  79. Mosier N, Wyman C, Dale B, Elander R, Lee YY, Holtzapple M, Ladisch M (2005) Features of promising technologies for pretreatment of lignocellulosic biomass. Biores Technol 96:673–686Google Scholar
  80. Mueller SC, Brown Jr RM (1980) Evidence for an intramembrane component associated with a cellulose microfibril synthesizing complex in higher plants. J Cell Biol 84:315–326Google Scholar
  81. Murray SC, Sharma A, Rooney WL, Klein PE, Mullet JE, Mitchell SE, Kresovich S (2008) Genetic improvement of sorghum as a biofuel feedstock II: quantitative loci for stem and leaf structural carbohydrates. Crop Sci 48:2180–2193Google Scholar
  82. Myton KE, Fry SC (1994) Intraprotoplasmic feruoylation of arabinoxylans in Festuca arundinacea cell cultures. Planta 193:326–330Google Scholar
  83. Nemeth C, Freeman J, Jones HD, Sparks C, Pellny MD, Wilkinson MD, Dunwell J, Andersson AAM, Åman P, Guillon F, Saulnier L, Mitchell RAC, Shewry PR (2010) Down-regulation of the CSLF6 gene results in decreased (1,3;1,4)-β-d-glucan in endosperm of wheat. Plant Physiol 152:1209–1218PubMedGoogle Scholar
  84. Oliver AL, Grant RJ, Pedersen JF, O’Rear J (2004) Comparison of brown midrib-6 and -18 forage sorghum with conventional sorghum and corn silage in diets of lactating dairy cows. J Dairy Sci 87:637–644PubMedGoogle Scholar
  85. Oliver AL, Klopfenstein TJ, Grant RJ, Pedersen JF (2005a) Comparative effects of the sorghum bmr-6 and bmr-12 genes. I. Forage sorghum yield and quality. Crop Sci 45:2234–2239Google Scholar
  86. Oliver AL, Klopfenstein TJ, Jose HD, Pedersen JF, Grant RJ (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 45:2240–2245Google Scholar
  87. Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87PubMedGoogle Scholar
  88. Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K et al (2003) Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res 10:239–247PubMedGoogle Scholar
  89. 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 229:115–127PubMedGoogle Scholar
  90. Palonen H, Tjerneld F, Zacchi G, Tenkanen M (2004) Adsorption of Trichoderma reesei CBH I and EG II and their catalytic domains on steam pretreated softwood and isolated lignin. J Biotechnol 107:65–72PubMedGoogle Scholar
  91. Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556PubMedGoogle Scholar
  92. Pear JR, Kawagoe Y, Schreckengost WE, Delmer DP, Stalker DM (1996) Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit oif cellulose synthase. Proc Natl Acad Sci U S A 93:12637–12642PubMedGoogle Scholar
  93. Pedersen JF, Fritz JO (2000) Forages and fodder. In: Smith CW, Frederiksen RA (eds) Sorghum: origin, history, technology, and production. Wiley, New York, pp 797–810Google Scholar
  94. Pedersen JF, Funell DL, Toy JJ, Oliver AL, Grant RJ (2006) Registration of seven forage sorghum genetic stocks near-isogenic for the brown midrib genes bmr-6 and bmr-12. Crop Sci 46:490Google Scholar
  95. Pedersen JF, Toy JJ, Funnell DL, Sattler SE, Oliver AL, Grant RA (2008) Registration of BN611, AN612, BN612 and BN613 sorghum genetic stocks with stacked bmr-6 and bmr-12 genes. J Plant Registr 2:258–262Google Scholar
  96. Penning B, Tayengwa R, Hunter CT III, Eveland A, Vermerris W, Olek A, Koch KE, McCarty DR, Davis M, Thomas SR, McCann M, Carpita N (2009) Genetic resources for functional genomics of maize cell wall biology. Plant Physiol 153:1703–1728Google Scholar
  97. Pillonel C, Mulder MM, Boon JJ, Forster B, Binder A (1991) Involvement of cinnamyl-alcohol dehydrogenase in the control of lignin formation in Sorghum bicolor (L.) Moench. Planta 185:538–544Google Scholar
  98. Porter KS, Axtell JD, Lechtenberg VL, Colenbrander VF (1978) Phenotype, fiber composition, and in vitro dry matter disappearance of chemically induced brown midrib (bmr) mutants of sorghum. Crop Sci 18:205–209Google Scholar
  99. Ragauskas AJ, Williams CK, Davison BH, Britovsek G, Cairney J, Eckert CA, Frederick WJ Jr, Hallett JP, Leak DJ, Liotta CL, Mielenz JR, Murphy R, Templer R, Tschaplinski T (2006) The path forward for biofuels and biomaterials. Science 311:484–489PubMedGoogle Scholar
  100. Ralph J, Grabber JG, Hatfield RD (1995) Lignin-ferulate cross-links in grasses: active incorporation of ferulate polysaccharide esters into ryegrass lignins. Carbohydr Res 275:167–178Google Scholar
  101. Ralph J, Bunzel M, Marita JM, Hatfield RD, Lu F, Kim H, Schatz PF, Grabber JH, Steinhart H (2004a) Peroxidase-dependent cross-linking reactions of p-hydroxycinnamates in plant cell walls. Phytochem Rev 3:79–96Google Scholar
  102. Ralph J, Guillaumie S, Grabber JH, Lapierre C, Barrière Y (2004b) Genetic and molecular basis of grass cell wall biosynthesis and degradability. III. Towards a forage grass idiotype. C R Biol 327:467–479PubMedGoogle Scholar
  103. Ralph J, Hatfield RD (1991) Pyrolysis-GC-MS analysis of forage materials. J Agric Food Chem 39:1426-1437PubMedGoogle Scholar
  104. Ralph J, Lundquist K, Brunow G, Lu F, Kim H, Schatz PF, Marita JM, Hatfield RD, Ralph SA, Christensen JH, Boerjan W (2004c) Lignins: natural polymers from oxidative coupling of 4-hydroxyphenylpropanoids. Phytochem Rev 3:29–60Google Scholar
  105. Riboulet C, Fabre F, Dénoue D, Martinant JP, Lefèvre B, Barrière Y (2008) QTL mapping and candidate gene research for lignin content and cell digestibility in a top-cross of a flint maize recombinant inbreed line progeny harvested at silage stage. Maydica 53:1–9Google Scholar
  106. Robinson AR, Mansfield SD (2009) Rapid analysis of poplar lignin monomer composition by a streamlined thioacidolysis procedure and near-infrared reflectance-based prediction modeling. Plant J 58:706–714PubMedGoogle Scholar
  107. Ronquist F, Huelsenbeck JP, VanDerMark P (2005) MrBayes 3.1 Manual. http://mrbayes.csit.fsu.edu/manual.php
  108. Rooney WL, Blumenthal J, Bean B, Mullet JE (2007) Designing sorghum as a dedicated bioenergy feedstock. Biofuels Bioprod Bioref 1:147–157Google Scholar
  109. Rose JK, Braam J, Fry SC, Nishitani K (2002) The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature. Plant Cell Physiol 43:1421–1435PubMedGoogle Scholar
  110. 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). Bioenergy Res 1:3–4Google Scholar
  111. Saballos A, Ejeta G, Kang CH, Vermerris W (2009) A genomewide analysis of the cinnamyl alcohol dehydrogenase family in sorghum [Sorghum bicolor (L.) Moench] identifies SbCAD2 as the Brown midrib6 gene. Genetics 181:783–795PubMedGoogle Scholar
  112. Samson D, Legeau F, Karsenty E, Reboux S, Veyrieras J-B, Just J, Barillot E (2003) GenoPlante-Info (GPI): a collection of databases and bioinformatics resources for plant genomics. Nucleic Acids Res 31:179–182PubMedGoogle Scholar
  113. Sattler SE, Saathoff AJ, Haas EJ, Palmer NA, Funnell-Harris DL, Sarath G, Pedersen JF (2009) A nonsense mutation in a cinnamyl alcohol dehydrogenase gene is responsible for the sorghum brown midrib6 phenotype. Plant Physiol 150:584–595PubMedGoogle Scholar
  114. Sattler SE, Funnell-Harris DL, Pedersen JF (2010) Brown midrib mutations and their importance to the utilization of maize, sorghum, and pearl millet lignocellulosic tissues. Plant Sci 178:229–238Google Scholar
  115. Saxena IM, Brown RM (2005) Cellulose biosynthesis: current views and evolving concepts. Ann Bot 96:9–21PubMedGoogle Scholar
  116. Scheible W-R, Eshed R, Richmond T, Delmer D, Somerville C (2001) Modifications of cellulose synthase confer resistance to isoxaben and thiazolidinone herbicides in Arabidopsis Ixr1 mutants. Proc Natl Acad Sci U S A 98:10079–10084PubMedGoogle Scholar
  117. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115PubMedGoogle Scholar
  118. Schwarz AK, Godsey CM, Luebbe MK, Erickson GE, Klopfenstein TL, Mitchell RB, Pedersen JF (2008) Forage quality and grazing performance of beef cattle grazing brown mid-rib grain sorghum residue. 2008 Nebraska Beef Reports. Lincoln, University of NebraskaGoogle Scholar
  119. Sedlak M, Ho NWY (2004) Production of ethanol from cellulosic biomass hydrolyzates using genetically engineered Saccharomyces yeast capable of cofermenting glucose and xylose. Appl Biochem Biotechnol 113:403–416PubMedGoogle Scholar
  120. Sendich E, Laser M, Kim S, Alizadeh H, Laureano-Perez L, Dale B, Lynd L (2008) Recent process improvement for the ammonia fiber expansion (AFEX) process and resulting reductions in minimum ethanol selling price. Bioresour Technol 99:8429–8434PubMedGoogle Scholar
  121. Sewell MM, Davis MF, Tuskan GA, Wheeler NC, Elam CC, Bassoni DL, Neale DB (2002) Identification of QTLs influencing wood property traits in loblolly pine (Pinus taeda L.). Theor Appl Genet 104:214–222PubMedGoogle Scholar
  122. Shen H, Yin Y, Chen F, Xu Y, Dixon R (2009) A bioinformatic analysis of NAC genes for plant cell wall development in relation to lignocellulosic bioenergy production. Bioenergy Res 2:217–232Google Scholar
  123. Sibout R, Eudes A, Mouille G, Pollet B, Lapierre C, Jouanin L, Seguin A (2005) Cinnamyl alcohol dehydrogenase-C and -D are the primary genes involved in lignin biosynthesis in the floral stem of Arabidopsis. Plant Cell 17:2059–2076PubMedGoogle Scholar
  124. Siesler HW, Ozaki Y, Kawata S, Heise HM (2002) Near-infrared spectroscopy: principles, instruments, applications. Wiley, WeinheimGoogle Scholar
  125. Smith CW, Frederiksen RA (2000) Sorghum: origin, history, technology and production. Wiley, New YorkGoogle Scholar
  126. Somerville C (2006) Cellulose synthesis in higher plants. Annu Rev Cell Dev Biol 22:53–78PubMedGoogle Scholar
  127. Studer MH, DeMartini JD, Brethauer S, McKenzie HL, Wyman CE (2010) Engineering of a high-throughput screening system to identify cellulosic biomass, pretreatments, and enzyme formulations that enhance sugar release. Biotechnol Bioeng 105:231–238PubMedGoogle Scholar
  128. Taylor NG, Scheible WR, Cutler S, Somerville CR, Turner SR (1999) The irregular xylem3 locus of Arabidopsis encodes a cellulose synthase required for secondary cell wall synthesis. Plant Cell 11:769–779PubMedGoogle Scholar
  129. Taylor NG, Laurie S, Turner SR (2000) Multiple cellulose synthase catalytic subunits are required for cellulose synthesis in Arabidopsis. Plant Cell 12:2529–2539PubMedGoogle Scholar
  130. Taylor NG, Howells RM, Huttly AK, Vickers K, Turner SR (2003) Interactions among three distinct CesA proteins essential for cellulose synthesis. Proc Natl Acad Sci U S A 100:1450–1455PubMedGoogle Scholar
  131. Tew TL, Cobill RM, Richard JEP (2008) Evaluation of sweet sorghum and sorghum  ×  sudangrass hybrids as feedstocks for ethanol production. Bioenergy Res 1:147–152Google Scholar
  132. Theander O, Åman P, Westerlund E, Andersson R, Pettersson D (1995) Total dietary fiber determined as neutral sugar residues, uronic acid residues, and Klason lignin (the Uppsala method): ­collaborative study. J AOAC Int 78:1030–1044PubMedGoogle Scholar
  133. Theodorou MK, William BA, Dhanoa MS, McAllan AB, France J (1994) A simple gas production method using a pressure transducer to determine the fermentation kinetics of ruminant feeds. Anim Feed Sci Technol 48:185–197Google Scholar
  134. Thompson JE, Fry SK (2001) Restructuring of wall-bound xyloglucan by transglycosylation in living plant cells. Plant J 26:23–34PubMedGoogle Scholar
  135. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedGoogle Scholar
  136. Tilley JMA, Terry RA (1963) A two-stage technique for the in vitro digestion of forage crops. J Br Grassl Soc 18:104–111Google Scholar
  137. Van Soest PJ (1967) Development of a comprehensive system of feed analyses and its application to forages. J Anim Sci 26:119–128Google Scholar
  138. Vandenbrink JP, Delgado MP, Frederick JR, Feltus FA (2010) A sorghum diversity panel biofuel feedstock screen for genotypes with high hydrolysis yield potential. Ind Crops Prod 31:444–448Google Scholar
  139. Vanholme R, Morreel K, Ralph J, Boerjan W (2008) Lignin engineering. Curr Opin Plant Biol 11:278–285PubMedGoogle Scholar
  140. Venuto B, Kindiger B (2008) Forage and biomass feedstock production from hybrid forage sorghum and sorghum-sudangrass hybrids. Grassland Sci 54:189–196Google Scholar
  141. Vermerris W (2009) Cell wall biosynthetic genes of maize and their potential for bioenergy production. In: Bennetzen J, Hake S (eds) Handbook of maize: genetics and genomics. Springer, New York, pp 741–767Google Scholar
  142. Vermerris W, Nicholson R (2006) Phenolic compound biochemistry. Springer, DordrechtGoogle Scholar
  143. Vermerris W, Saballos A, Ejeta G, Mosier NS, Ladisch MR, Carpita NC (2007) Molecular breeding to enhance ethanol production from corn and sorghum Stover. Crop Sci 47:S145–S153Google Scholar
  144. Weimer PJ, Dien BS, Springer TL, Vogel KP (2005) In vitro gas production as a surrogate measure of the fermentability of cellulosic biomass to ethanol. Appl Microbiol Biotechnol 67:52–58PubMedGoogle Scholar
  145. Wheeler JL, Mulcahy C (1989) Consequences for animal production of cyanogenesis in sorghum forage and hay: a review. Tropical Grasslands 23:193–202Google Scholar
  146. Wilson WA, Harrington SE, Woodman WL, Lee M, Sorrells ME, McCouch SR (1999) Inferences on the genome structure of progenitor maize through comparative analysis of rice, maize and the domesticated Panicoids. Genetics 153:453–473PubMedGoogle Scholar
  147. Xin Z, Wang ML, Barkley NA, Burow G, Franks C, Pederson G, Burke J (2008) Applying genotyping (TILLING) and phenotyping analyses to elucidate gene function in a chemically induced sorghum mutant population. BMC Plant Biol 8:108–140Google Scholar
  148. Xin Z, Wang ML, Burow G, Burke J (2009) An induced sorghum mutant population suitable for bioenergy research. Bioenergy Res 2:10–16Google Scholar
  149. Xu Z, Zhang D, Hu J, Zhou X, Ye X, Reichel KL, Stewart NR, Syrenne RD, Yang X, Gao P et al (2009) Comparative genome analysis of lignin biosynthesis gene families across the plant kingdom. BMC Bioinformatics 10(Suppl 11):S3PubMedGoogle Scholar
  150. Yong W, Link B, O’Malley R, Tewari J, Hunter CT, Lu CA, Li X, Bleecker AB, Koch KE, McCann MC, McCarty DR, Staiger C, Thomas SR, Vermerris W, Carpita NC (2005) Genomics of plant cell wall biogenesis. Planta 221:747–751PubMedGoogle Scholar
  151. Zhao Q, Gallego-Giraldo L, Wang H, Zeng Y, Ding SY, Chen F, Dixon R (2010) A NAC transcription factor orchestrates multiple features of cell wall development in Medicago truncatula. Plant J. 63:100–114Google Scholar
  152. Zugenmaier P (2001) Conformation and packing of various crystalline cellulose fibers. Prog Polym Sci 26:1341–1417Google Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Genetics Institute and Agronomy DepartmentUniversity of FloridaGainesvilleUSA
  2. 2.Department of Agricultural & Biological Engineering and Laboratory of Renewable Resources EngineeringPurdue UniversityWest LafayetteUSA

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