Plant Biotechnology Reports

, Volume 11, Issue 1, pp 17–27 | Cite as

Down-regulation of hydroxycinnamoyl CoA: shikimate hydroxycinnamoyl transferase, cinnamoyl CoA reductase, and cinnamyl alcohol dehydrogenase leads to lignin reduction in rice (Oryza sativa L. ssp. japonica cv. Nipponbare)

  • Sathish K. Ponniah
  • Zhenhua Shang
  • M. Aydın Akbudak
  • Vibha Srivastava
  • Muthusamy Manoharan
Original Article

Abstract

Rice straw is one of the largest biomasses in the world that can potentially be exploited for biofuel. Nevertheless, the association of lignin with cellulose and hemicellulose has hindered the efficient utilization of rice straw for cellulosic biofuel. The objective of this study was to down-regulate key genes involved in lignin biosynthesis pathway, such as hydroxycinnamoyl CoA: shikimate hydroxycinnamoyl transferase (HCT), cinnamoyl CoA reductase (CCR), and cinnamyl alcohol dehydrogenase (CAD), through “terminator-less” constructs to reduce lignin in transgenic rice. Real-time qPCR analyses of the selected T1 transgenic rice plants indicated 36–86% transcript reduction in HCT lines, 75–94% in CCR lines, and 10–85% in CAD lines. Of the nine down-regulated lines (three lines from each genes) subjected to lignin analysis, seven showed significant reduction in total lignin content (HCT-4, HCT-7, CAD-1, CAD-7, CCR-3, CCR-7, and CCR-12) with lignin reduction ranging from 4.6 to 10.8%. The results from this study indicated that truncated gene fragments lacking transcription termination sequence can be used for down-regulation of lignin genes in rice, and the rice straw from these transgenic lines could be useful as feedstock for cellulosic biofuel.

Keywords

Biofuel Gene silencing Lignin Rice straw Terminator-less construct 

References

  1. Abbott JC, Barakate A, Pincon G, Legrand M, Lapierre C, Mila I, Schuch W, Halpin C (2002) Simultaneous suppression of multiple genes by single transgenes. Down-regulation of three unrelated lignin biosynthetic genes in tobacco. Plant Physiol 128:844–853CrossRefPubMedPubMedCentralGoogle Scholar
  2. Akbudak MA, Nicholson SJ, Srivastava V (2013) Suppression of Arabidopsis genes by terminator-less transgene constructs. Plant Biotechnol Rep 7:415–424CrossRefGoogle Scholar
  3. Bai Y, Gong W, Liu T, and Zhu Y (2003) Cloning and expression analyses of a cinnamoyl CoA resductase cDNA from rice seeelings. Chin Sci Bull 48:2221–2225CrossRefGoogle Scholar
  4. Barakat A, Yassin NB, Park JS, Choi A, Herr J, Carlson JE (2011) Comparative and phylogenomic analyses of cinnamoyl-CoA reductase and cinnamoyl-CoA-reductase-like gene family in land plants. Plant Sci 181:249–257CrossRefPubMedGoogle Scholar
  5. Baxter HL, Mazarei M, Labbe N, Kline LM, Cheng Q, Windham MT, Mann DGJ, Fu C, Ziebell A, Sykes RW, Rodriguez M Jr, Davis MF, Mielenz JR, Dixon RA, Wang Z-Y, Stewart CN Jr (2014) Two-year field analysis of reduced recalcitrance transgenic switchgrass. Plant Biotechnol J 12:914–924CrossRefPubMedGoogle Scholar
  6. Besseau S, Hoffmann L, Geoffroy P, Lapierre C, Pollet B, Legrand M (2007) Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. Plant Cell 9:148–162CrossRefGoogle Scholar
  7. Binod P, Sindhu R, Singhania R, Vikram S, Devi L, Nagalakashmi S, Kurien N, Sukumaran R, Pandey A (2010) Bioethanol production from rice straw: an overview. Bioresour Technol 101:4767–4774CrossRefPubMedGoogle Scholar
  8. Blee K, Choi JW, O’Connell AP, Jupe SC, Schuch W, Lewis NG, Bolwell GP (2001) Antisense and sense expression of cDNA coding for CYP73A15, a class II cinnamate 4-hydroxylase, leads to a delayed and reduced production of lignin in tobacco. Phytochemistry 57:1159–1166CrossRefPubMedGoogle Scholar
  9. Bouvier d’Yvoire M, Bouchabke-Coussa O, Voorend W, Antelme S, Cezard L, Leg_ee F, Lebris P, Legay S, Whitehead C, McQueen-Mason SJ, Gomez LD, Jouanin L, Lapierre C, Sibout R (2013) Disrupting the cinnamyl alcohol dehydrogenase 1 gene (BdCAD1) leads to altered lignification and improved saccharification in Brachypodium distachyon. Plant J 73:496–508CrossRefPubMedGoogle Scholar
  10. Carpita N, McCann M (2000) The cell wall. In: Buchanan BB, Wilhelm G, Jones RL (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, pp 52–108Google Scholar
  11. Carroll A, Somerville C (2009) Cellulosic biofuels. Annu Rev Plant Biol 60:165–182CrossRefPubMedGoogle Scholar
  12. Chabannes M, Barakate A, Lapierre C, Marita JM, Ralph J, Pean M, Danoun S, Halpin C, Grima-Pettenati J, Boudet AM (2001) Strong decrease in lignin content without significant alteration of plant development is induced by simultaneous down-regulation of cinnamoyl CoA reductase (CCR) and cinnamyl alcohol dehydrogenase (CAD) in tobacco plants. Plant J 28:257–270CrossRefPubMedGoogle Scholar
  13. Chen F, Dixon RA (2007) Lignin modification improves fermentable sugar yields for biofuel production. Nat Biotechnol 25:759–761CrossRefPubMedGoogle Scholar
  14. Chen L, Auh CK, Dowling P, Bell J, Chen F, Hopkins A, Dixon RA, Wang ZY (2003) Improved forage digestibility of tall fescue (Festuca arundinacea) by transgenic down-regulation of cinnamyl alcohol dehydrogenase. Plant Biotech J 1:437–449CrossRefGoogle Scholar
  15. Chen L, Auh C, Dowling P, Bell J, Lehmann D, Wang ZY (2004) Transgenic down regulation of caffeic acid o-methyltransferase (COMT) led to improved digestibility in tall fescue (Festuca arundinacea). Funct Plant Biol 31:235–245CrossRefGoogle Scholar
  16. Dauwe R, Morreel K, Goeminne G, Gielen B, Rohde A, Van Beeumen J, Ralph J, Boudet AM, Kopka J, Rochange SF, Halpin C, Messens E, Boerjan W (2007) Molecular phenotyping of lignin-modified tobacco reveals associated changes in cell-wall metabolism, primary metabolism, stress metabolism and photorespiration. Plant J 52:263–285CrossRefPubMedGoogle Scholar
  17. Dellaporta S, Wood J, Hicks J (1983) Isolation of DNA from higher plants. Plant Mol Biol Rep 1:19–21CrossRefGoogle Scholar
  18. Dien B, Sarath G, Pedersen J, Sattler S, Chen H, Funnell-Harris D, Nichols N, Cotta M (2009) Improved sugar conversion and ethanol yield for forage sorghum (Sorghum bicolor L. Moench) lines with reduced lignin contents. Bioenerg Res 2:153–164CrossRefGoogle Scholar
  19. Doorsselaere J, Baucher M, Chognot E, Chabbert B, Tollier MT, Petit-Conil M, Leplé JC, Pilate G, Cornu D, Monties B (2003) A novel lignin in poplar trees with a reduced caffeic acid/5 hydroxyferulic acid O-methyltransferase activity. Plant J 8:855–864CrossRefGoogle Scholar
  20. Evans RJ, Milne TA (1987) Molecular characterization of the pyrolysis of biomass. Energy Fuels 1:123–137CrossRefGoogle Scholar
  21. Fornalé S, Capellades M, Encina A, Wang K, Irar S, Lapierre C, Ruel K, Joseleau JP, Berenguer, J, Puigdomenech P, Rigau J, Caparros-Ruiz D (2012) Altered lignin biosynthesis improves cellulosic bioethanol production in transgenic maize plants down-regulated for cinnamyl alcohol dehydrogenase. Mol Plant 5:817–830CrossRefPubMedGoogle Scholar
  22. Fornalé S, Rencoret J, Garcia-Calvo L, Capellades M, Encina A, Santiago R, Rigau J, Gutiérrez A, del Río JC, Caparros-Ruiz D (2015) Cell wall modifications triggered by the down-regulation of Coumarate 3-hydroxylase-1 in maize. Plant Sci 236:272–282CrossRefPubMedGoogle Scholar
  23. Fu C, Mielenz JR, Xiao X, Ge Y, Hamilton CY, Rodriguez M Jr, Chen F, Foston M, Ragauskas A, Bouton J, Dixon RA, Wang ZY (2011a) Genetic manipulation of lignin reduces recalcitrance and improves ethanol production from switchgrass. Proc Natl Acad Sci USA 108:3803–3808CrossRefPubMedPubMedCentralGoogle Scholar
  24. Fu C, Xiao X, Xi Y, Ge Y, Chen F, Bouton J, Dixon RA, Wang ZY (2011b) Downregulation of cinnamyl alcohol dehydrogenase (CAD) leads to improved saccharification efficiency in switchgrass. Bioenerg Res 4:153–164CrossRefGoogle Scholar
  25. Gallego-Giraldo L, Jikumaru Y, Kamiya Y, Tang Y, Dixon RA (2011) Selective lignin down-regulation leads to constitutive defense response expression in alfalfa (Medicago sativa L.). New Phytol 190:627–639CrossRefPubMedGoogle Scholar
  26. Garrote G, Dominguez H, Parajo JC (2002) Autohydrolysis of corncob: study of non-isothermal operation for xylooligosaccharide production. J Food Eng 52:211–218CrossRefGoogle Scholar
  27. Giordano A, Liu Z, Panter SN, Dimech AM, Shang Y, Wijesinghe H, Fulgueras K, Ran Y, Mouradov A, Rochfort S, Patron NJ, Spangenberg GC (2014) Reduced lignin content and altered lignin composition in the warm season forage grass Paspalum dilatatum by down-regulation of a Cinnamoyl CoA reductase gene. Transgenic Res 23:503–517CrossRefPubMedPubMedCentralGoogle Scholar
  28. Goldemberg J (2007) Ethanol for a sustainable energy future. Science 315:808–810CrossRefPubMedGoogle Scholar
  29. Gondolf VM, Stoppel R, Ebert B, Rautengarten C, Liwanag AJM, Loqué D, Scheller HV (2014) A gene stacking approach leads to engineered plants with highly increased galactan levels in Arabidopsis. BMC Plant Biol 14:344CrossRefPubMedPubMedCentralGoogle Scholar
  30. Goujon T, Ferret V, Mila I, Pollet B, Ruel K, Burlat V, Joseleau J, Barriere Y, Lapierre C, Jouanin L (2003) Down-regulation of the AtCCR1 gene in Arabidopsis thaliana: effects on phenotype, lignins and cell wall degradability. Planta 217:218–228PubMedGoogle Scholar
  31. Guo D, Chen F, Inoue K, Blount JW, Dixon RA (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 13:73–88CrossRefPubMedPubMedCentralGoogle Scholar
  32. Hirano K, Aya K, Kondo M, Okuno A, Morinaka Y, Matsuoka M (2012) OsCAD2 is the major CAD gene responsible for monolignol biosynthesis in rice culm. Plant Cell Rep 31:91–101CrossRefPubMedGoogle Scholar
  33. Hoffmann L, Besseau S, Geoffroy P, Ritzenthaler C, Meyer D, Lapierre C, Pollet B, Legrand M (2004) Silencing of hydroxycinnamoyl-coenzyme A shikimate/quinate hydroxycinnamoyltransferase affects phenylpropanoid biosynthesis. Plant Cell 16:1446–1465CrossRefPubMedPubMedCentralGoogle Scholar
  34. Jackson L, Shadle G, Zhou R, Nakashima J, Chen F, Dixon R (2008) Improving saccharification efficiency of alfalfa stems through modification of the terminal stages of monolignol biosynthesis. BioEnergy Res 1:180–192CrossRefGoogle Scholar
  35. Jones L, Ennos AR, Turner SR (2001) Cloning and characterization of irregular xylem4 (irx4): a severely lignin-deficient mutant of Arabidopsis. Plant J 26:205–216CrossRefPubMedGoogle Scholar
  36. Jung HG, Deetz DA (1993) Cell wall lignification and degradability. In: Jung HG, Buxton DR, Hatfield RD, Ralph J (eds) Forage cell wall structure and digestibility). ASA-CSSA-SSSA, Madison, pp. 315–346Google Scholar
  37. Jung JH, Fouad WM, Vermerris W, Gallo M, Altpeter F (2012) RNAi suppression of lignin biosynthesis in sugarcane reduces recalcitrance for biofuel production from lignocellulosic biomass. Plant Biotechnol J 10:1067–1076CrossRefPubMedGoogle Scholar
  38. Jung JH, Vermerris W, Gallo M, Fedenko JR, Erickson JE, Altpeter F (2013) RNA interference suppression of lignin biosynthesis increases fermentable sugar yields for biofuel production from field-grown sugarcane. Plant Biotechnol J 11:709–716CrossRefPubMedGoogle Scholar
  39. Kawasaki T, Koita H, Nakatsubo T, Hasegawa K, Wakabayashi K, Takahashi H, Umemura K, Umezawa T, Shimamoto K (2006) Cinnamoyl-CoA reductase, a key enzyme in lignin biosynthesis, is an effector of small GTPase Rac in defense signaling in rice. Proc Natl Acad Sci USA 103:230–235CrossRefPubMedGoogle Scholar
  40. Kim IA, Kim B-G, Kim M, Ahn J-H (2012) Charactrization of hydroxycinnamoyltransferase from rice and its application for biological synthesis of hydroxycinnamoyl glycerols. Phytochemistry 76:25–31CrossRefPubMedGoogle Scholar
  41. Lapierre C, Pollet B, Petit-Conil M, Toval G, Romero J, Pilate G, Leple JC, Boerjan W, Ferret VV, De Nadai V, Jouanin L (1999) Structural alterations of lignins in transgenic poplars with depressed cinnamoyl alcohol dehydrogenase or caffeic acid O-methyltransferase activity have opposite impact on the efficiency of industrial Kraft pulping. Plant Physiol 119:153–163CrossRefPubMedPubMedCentralGoogle Scholar
  42. Lapierre C, Pilate G, Pollet B, Mila I, Leple J-C, Jouanin L, Kim H, Ralph J (2004) Signatures of cinnamyl alcohol dehydrogenase deficiency in poplar lignins. Phytochemistry 65:313–321CrossRefPubMedGoogle Scholar
  43. Leplé J-C, Dauwe R, Morreel K, Storme V, Lapierre C, Pollet B, Naumann A, Kang K-Y, Kim H, Ruel K, Lefebvre A, Joseleau J-P, Grima-Pettenati J, De Rycke R, Andersson-Gunneras S, Erban A, Fehrle I, Petit-Conil M, Kopka J, Polle A, Messens E, Sundberg B, Mansfield SD, Ralph J, Pilate G, Boerjan W (2007) Downregulation of cinnamoyl-Coenzyme A reductase in poplar: multiple-level phenotyping reveals effects on cell wallpolymer metabolism and structure. Plant Cell 19:3669–3691CrossRefPubMedPubMedCentralGoogle Scholar
  44. Liu CJ, Cai Y, Zhang X, Gou M, Yang H (2014) Tailoring lignin biosynthesis for efficient and sustainable biofuel production. Plant Biotechnol J 12:1154–1162CrossRefPubMedGoogle Scholar
  45. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408CrossRefPubMedGoogle Scholar
  46. Luo Z, Chen Z (2007) Improperly terminated, unpolyadenylated mRNA of sense transgenes is targeted by RDR6-mediated RNA silencing in Arabidopsis. Plant Cell 19:943–958CrossRefPubMedPubMedCentralGoogle Scholar
  47. Maiorella BL (1983) Ethanol. In: Young M (ed) Industrial chemicals, biochemicals and Fuels, V.3, comprehensive biotechnology. Pergamon Press, UK, pp 861–914Google Scholar
  48. Mir Derikvand M, Sierra JB, Ruel K, Pollet B, Do CT, Thevenin J, Buffard D, Jouanin L, Lapierre C (2008) Redirection of the phenylpropanoid pathway to feruloyl malate in Arabidopsis mutants deficient for cinnamoyl-CoA reductase 1. Planta 227:943–956CrossRefPubMedGoogle Scholar
  49. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497CrossRefGoogle Scholar
  50. Nakashima J, Chen F, Jackson, L, Shadle G, Dixon RA (2008) Multisite genetic modification of monolignol biosynthesis in alfalfa (Medicago sativa): effects on lignin composition in specific cell types. New Phytol 179:738–750CrossRefPubMedGoogle Scholar
  51. Nicholson SJ, Srivastava V (2009) Transgene constructs lacking transcription termination signal induce efficient silencing of endogenous targets in Arabidopsis. Mol Genet Genom 282:319–328CrossRefGoogle Scholar
  52. Piquemal J, Lapierre C, Myton K, O’Connell A, Schuch W, Grima-Pettenati J, Boudet AM (1998) Down-regulation of cinnamoyl-CoA reductase induces significant changes of lignin profiles in transgenic tobacco plants. Plant J 13:71–83CrossRefGoogle Scholar
  53. Poovaiah CR, Nageswara-Rao M, Soneji JR, Baxter HL, Stewart CN Jr (2014) Altered lignin biosynthesis using biotechnology to improve lignocellulosic biofuel feedstocks. Plant Biotechnol J 12:1163–1173CrossRefPubMedGoogle Scholar
  54. Prashant S, Srilakshmi Sunita M, Pramod S, Ranadheer K, Gupta K, Anil Kumar S, Rao Karumanchi S, Rawal SK, Kavi Kishor PS (2011) Downregulation of Leucaena leucocephala cinnamoyl CoA reductase (LiCCR) gene induces significant changes in phenotype, soluble phenolic pools and lignin in transgenic tobacco. Plant Cell Rep 30:2215–2231CrossRefPubMedGoogle Scholar
  55. Ralph J, Hatfield RD, Piquemal J, Yahiaoui N, Pean M (1998) NMR characterization of altered lignins extracted from tobacco plants downregulated for lignification enzymes cinnamylalcohol dehydrogenase and cinnamoyl-CoA reductase. Proc Natl Acad Sci USA 95:12803–12808CrossRefPubMedPubMedCentralGoogle Scholar
  56. Ralph J, Akiyama T, Kim H, Lu FC, Schatz PF, Marita JM, Ralph SA, Reddy MSS, Chen FDixon RA (2006) Effects of coumarate 3-hydroxylase down-regulation on lignin structure. J Biol Chem 281:8843–8853CrossRefPubMedGoogle Scholar
  57. Ralph J, Akiyama T, Coleman HD, Mansfield SD (2012) Effects on lignin structure of coumarate 3-hydroxylase downregulation in poplar. Bioenergy Res 5:1009–1019CrossRefPubMedPubMedCentralGoogle Scholar
  58. Reddy MS, Chen F, Shadle G, Jackson L, Aljoe H, Dixon RA (2005) Targeted down-regulation of cytochrome P450 enzymes for forage quality improvement in alfalfa (Medicago sativa L.). Proc Natl Acad Sci USA 102:16573–16578CrossRefPubMedPubMedCentralGoogle Scholar
  59. Ruel K, Berrio-Sierra J, Mir Derikvand M, Pollet B, Thévenin J, Lapierre C, Jouanin L, Joseleau J-P (2009) Impact of CCR1 silencing on the assembly of lignified secondary walls in Arabidopsis thaliana. New Phytol 184:99–113CrossRefPubMedGoogle Scholar
  60. Saathoff AJ, Sarath G, Chow EK, Dien BS, Tobias CM (2011) Downregulation of cinnamyl-alcohol dehydrogenase in switchgrass by RNA silencing results in enhanced glucose release after cellulase treatment. PLoS One 6:e16416CrossRefPubMedPubMedCentralGoogle Scholar
  61. Saha BC (2003) Hemicellulose bioconversion. J Ind Microbiol Biotechnol 30:279–291CrossRefPubMedGoogle Scholar
  62. SAS Institute (2008) Inc. SAS Software version 9.2. SAS Institute, Cary, NCGoogle Scholar
  63. Sewalt V, Ni W, Blount JW, Jung HG, Masoud SA, Howles PA, Lamb C, Dixon RA (1997) Reduced lignin content and altered lignin composition in transgenic tobacco down-regulated in expression of l-phenylalanine ammonia-lyase or Cinnamate 4-hydroxylase. Plant Physiol 115:41–50CrossRefPubMedPubMedCentralGoogle Scholar
  64. Shadle G, Chen F, Srinivasa Reddy MS, Jackson L, Nakashima J, Dixon RA (2007) Down-regulation of hydroxycinnamoyl CoA: shikimate hydroxycinnamoyl transferase in transgenic alfalfa affects lignification, development and forage quality. Phytochemistry 68:1521–1529CrossRefPubMedGoogle Scholar
  65. Simmons BA, Loque D, Ralph J (2010) Advances in modifying lignin for enhanced biofuel production. Curr Opin Plant Biol 13:313–320CrossRefPubMedGoogle Scholar
  66. Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16:144–158Google Scholar
  67. Studer M, DeMartini J, Davis M, Sykes R, Davison B, Keller M, Tuskan G, Wyman C (2011) Lignin content in natural Populus variants affects sugar release. Proc Natl Acad Sci USA 108:6300–6305CrossRefPubMedPubMedCentralGoogle Scholar
  68. Sykes R, Yung M, Novaes E, Kirst M, Peter G, Davis M (2009) High-throughput screening of plant cell-wall composition using pyrolysis molecular beam mass spectroscopy. Biofuels: Methods Protoc Methods Mol Bio 581:169–183CrossRefGoogle Scholar
  69. Tamasloukht B, Wong Quai Lam MS, Martinez Y, Tozo K, Barbier O, Jourda C, Jauneau A, Borderies G, Balzergue S, Renou JP, Huguet S, Martinant JP, Tatout C, Lapierre C, Barriere Y, Goffner D, Pichon M (2011) Characterization of a cinnamoyl-CoA reductase 1 (CCR1) mutant in maize: effects on lignification, fibre development, and global gene expression. J Exp Bot 62:3837–3848CrossRefPubMedPubMedCentralGoogle Scholar
  70. Toki S, Hara N, Ono K, Onodera H, Tagiri A, Oka S, Tanaka H (2006) Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. Plant J 47:969–976CrossRefPubMedGoogle Scholar
  71. Tsai CJ, Popko JL, Mielke MR, Hu WJ, Podila GK, Chiang VL (1998) Suppression of O-methyltransferase gene by homologous sense transgene in quaking aspen causes red-brown wood phenotypes. Plant Physiol 117:101–112CrossRefPubMedPubMedCentralGoogle Scholar
  72. Tu Y, Rochfort S, Liu Z, Ran Y, Griffith M, Badenhorst P, Louie GV, Bowman ME, Smith KF, Noel JP, Mouradov A, Spangenberg G (2010) Functional analyses of caffeic acid O-methyltransferase and cinnamoyl-CoA-reductase genes from perennial ryegrass (Lolium perenne). Plant Cell 22:3357–3373CrossRefPubMedPubMedCentralGoogle Scholar
  73. Van Acker R, Leplé J-C, Aerts D, Storme V, Goeminne G, Ivens B, Légée F, Lapierre C, Piens K, Van Montagu MCE, Santoro N, Foster CE, Ralph J, Soetaert W, Pilate G, Boerjan W (2014) Improved saccharification and ethanol yield from field-grown transgenic poplar deficient in cinnamoyl-CoA reductase. Proc Natl Acad Sci USA 111:845–850CrossRefPubMedGoogle Scholar
  74. Van der Rest B, Danoun S, Boudet AM, Rochange SF (2006) Downregulation of cinnamoyl-CoA reductase in tomato (Solanum lycopersicum L.) induces dramatic changes in soluble phenolic pools. J Exp Bot 57:1399–1411CrossRefPubMedGoogle Scholar
  75. Vanholme R, Demedts B, Morreel K, Ralph J, Boerjan W (2010) Lignin biosynthesis and structure. Plant Physiol 153:895–905CrossRefPubMedPubMedCentralGoogle Scholar
  76. Voelker SL, Lachenbruch B, Meinzer FC, Jourdes M, Ki C, Patten AM, Davin LB, Lewis NG, Tuskan GA, Gunter L, Decker SR, Selig MJ, Sykes R, Himmel ME, Kitin P, Shevchenko O, Strauss SH (2010) Antisense down-regulation of 4CL expression alters lignification, tree growth, and saccharification potential of field-grown poplar. Plant Physiol 154:874–886CrossRefPubMedPubMedCentralGoogle Scholar
  77. Wadenbäck J, von Arnold S, Egertsdotter U, Walter MH, Grima-Pettenati J, Goffner D, Gellerstedt G, Gullion T, Clapham D (2008) Lignin biosynthesis in transgenic Norway spruce plants harboring an antisense construct for cinnamoyl CoA reductase (CCR). Transgenic Res 17:379–392CrossRefPubMedGoogle Scholar
  78. Wagner A, Ralph J, Akiyama T, Flint H, Phillips L, Torr K, Nanayakkara B, Te Kiri L (2007) Exploring lignification in conifers by silencing hydroxycinnamoyl-CoA: shikimate hydroxycinnamoyltransferase in Pinus radiata. Proc Natl Acad Sci USA 104:11856–11861CrossRefPubMedPubMedCentralGoogle Scholar
  79. Wagner A, Tobimatsu Y, Goeminne G, Phillips L, Flint H, Steward D, Torr K, Donaldson L, Boerjan W, Ralph J (2013) Suppression of CCR impacts metabolite profile and cell wall composition in Pinus radiate tracheary elements. Plant Mol Biol 81:105–117CrossRefPubMedGoogle Scholar
  80. Waterhouse PM, Graham HW, Wang MB (1998) Virus resistance and gene silencing in plants can be induced by simultaneous expression of sense and antisense RNA. Proc Natl Acad Sci USA 95:13959–13964CrossRefPubMedPubMedCentralGoogle Scholar
  81. Wesley SV, Helliwell CA, Smith NA, Wang MB, Rouse DT, Liu Q, Gooding PS, Singh SP, Abbott D, Stoutjesdijk PA, Robinson SP, Gleave AP, Green AG, Waterhouse PM (2001) Construct design for efficient, effective and high throughput gene silencing in plants. Plant J 27:581–590CrossRefPubMedGoogle Scholar
  82. Xu B, Escamilla-Trevino LL, Sathitsuksanoh N, Shen Z, Shen H, Zhang YHP, Dixon RA, 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 192:611–625CrossRefPubMedGoogle Scholar
  83. Xu N, Zhang W, Ren S, Liu F, Zhao C, Liao H, Xu Z, Huang J, Li Q, Tu Y, Bin Yu, Wang Y, Jiang J, Qin J, Peng L (2012) Hemicelluloses negatively affect lignocellulose crystallinity for high biomass digestibility under NaOH and H2SO4 pretreatments in Miscanthus. Biotech Biofuel 5:58CrossRefGoogle Scholar
  84. Yang B, Wyman CE (2004) Effect of xylan and lignin removal by batch and flowthrough pretreatment on the enzymatic digestibility of corn stover cellulose. Biotechnol Bioeng 86:88–95CrossRefPubMedGoogle Scholar
  85. Zamora R, Crispin JAS (1995) Production of an acid extract of rice straw. Acta Cient Venez 46:135–139PubMedGoogle Scholar
  86. Zhang K, Qian Q, Huang Z, Wang Y, Li M, Hong L, Zeng D, Gu M, Chu C, Cheng Z (2006) GOLD HULL AND INTERNODE2 encodes a primarily multifunctional cinnamyl-alcohol dehydrogenase in rice. Plant Physiol 140:972–83CrossRefPubMedPubMedCentralGoogle Scholar
  87. Zhong R, Lee C, McCarthy RL, Reeves CK, Jones EG, Ye ZH (2011) Transcriptional activation of secondary wall biosynthesis by rice maize NAC and MYB transcription factors. Plant Cell Physiol 52:1856–1871CrossRefPubMedGoogle Scholar
  88. Ziebell A, Gracom K, Katahira R, Chen F, Pu YQ, Ragauskas A, Dixon RA, Davis M (2010) Increase in 4-coumaryl alcohol units during lignification in alfalfa (Medicago sativa) alters the extractability and molecular weight of lignin. J Biol Chem 285:38961–38968CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Korean Society for Plant Biotechnology and Springer Japan 2017

Authors and Affiliations

  • Sathish K. Ponniah
    • 1
  • Zhenhua Shang
    • 1
  • M. Aydın Akbudak
    • 2
    • 3
  • Vibha Srivastava
    • 2
  • Muthusamy Manoharan
    • 1
  1. 1.Department of AgricultureUniversity of Arkansas at Pine BluffPine BluffUSA
  2. 2.Department of Crop, Soil and Environmental ScienceUniversity of ArkansasFayettevilleUSA
  3. 3.Department of Agricultural BiotechnologyAkdeniz UniversityAntalyaTurkey

Personalised recommendations