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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)

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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.

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References

  • 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 128:844–853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Akbudak MA, Nicholson SJ, Srivastava V (2013) Suppression of Arabidopsis genes by terminator-less transgene constructs. Plant Biotechnol Rep 7:415–424

    Article  Google Scholar 

  • 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 48:2221–2225

    Article  CAS  Google Scholar 

  • 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 181:249–257

    Article  CAS  PubMed  Google Scholar 

  • 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 12:914–924

    Article  PubMed  Google Scholar 

  • 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 9:148–162

    Article  Google Scholar 

  • 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 101:4767–4774

    Article  CAS  PubMed  Google Scholar 

  • 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 57:1159–1166

    Article  CAS  PubMed  Google Scholar 

  • 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 73:496–508

    Article  PubMed  Google Scholar 

  • 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 52–108

    Google Scholar 

  • Carroll A, Somerville C (2009) Cellulosic biofuels. Annu Rev Plant Biol 60:165–182

    Article  CAS  PubMed  Google Scholar 

  • 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 28:257–270

    Article  CAS  PubMed  Google Scholar 

  • Chen F, Dixon RA (2007) Lignin modification improves fermentable sugar yields for biofuel production. Nat Biotechnol 25:759–761

    Article  CAS  PubMed  Google Scholar 

  • 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 1:437–449

    Article  CAS  Google Scholar 

  • 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 31:235–245

    Article  CAS  Google Scholar 

  • 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 52:263–285

    Article  CAS  PubMed  Google Scholar 

  • Dellaporta S, Wood J, Hicks J (1983) Isolation of DNA from higher plants. Plant Mol Biol Rep 1:19–21

    Article  CAS  Google Scholar 

  • 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 2:153–164

    Article  Google Scholar 

  • 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 8:855–864

    Article  Google Scholar 

  • Evans RJ, Milne TA (1987) Molecular characterization of the pyrolysis of biomass. Energy Fuels 1:123–137

    Article  CAS  Google Scholar 

  • 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 5:817–830

    Article  PubMed  Google Scholar 

  • 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 236:272–282

    Article  PubMed  Google Scholar 

  • 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 108:3803–3808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 4:153–164

    Article  Google Scholar 

  • 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 190:627–639

    Article  CAS  PubMed  Google Scholar 

  • Garrote G, Dominguez H, Parajo JC (2002) Autohydrolysis of corncob: study of non-isothermal operation for xylooligosaccharide production. J Food Eng 52:211–218

    Article  Google Scholar 

  • 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 23:503–517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldemberg J (2007) Ethanol for a sustainable energy future. Science 315:808–810

    Article  CAS  PubMed  Google Scholar 

  • 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 14:344

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 217:218–228

    CAS  PubMed  Google Scholar 

  • 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 13:73–88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 31:91–101

    Article  CAS  PubMed  Google Scholar 

  • 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 16:1446–1465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 1:180–192

    Article  Google Scholar 

  • Jones L, Ennos AR, Turner SR (2001) Cloning and characterization of irregular xylem4 (irx4): a severely lignin-deficient mutant of Arabidopsis. Plant J 26:205–216

    Article  CAS  PubMed  Google Scholar 

  • 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. 315–346

    Google Scholar 

  • 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 10:1067–1076

    Article  CAS  PubMed  Google Scholar 

  • 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 11:709–716

    Article  CAS  PubMed  Google Scholar 

  • 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 103:230–235

    Article  CAS  PubMed  Google Scholar 

  • 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 76:25–31

    Article  CAS  PubMed  Google Scholar 

  • 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 119:153–163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 65:313–321

    Article  CAS  PubMed  Google Scholar 

  • 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 19:3669–3691

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu CJ, Cai Y, Zhang X, Gou M, Yang H (2014) Tailoring lignin biosynthesis for efficient and sustainable biofuel production. Plant Biotechnol J 12:1154–1162

    Article  CAS  PubMed  Google Scholar 

  • 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 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Luo Z, Chen Z (2007) Improperly terminated, unpolyadenylated mRNA of sense transgenes is targeted by RDR6-mediated RNA silencing in Arabidopsis. Plant Cell 19:943–958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maiorella BL (1983) Ethanol. In: Young M (ed) Industrial chemicals, biochemicals and Fuels, V.3, comprehensive biotechnology. Pergamon Press, UK, pp 861–914

    Google Scholar 

  • 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 227:943–956

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • 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 179:738–750

    Article  CAS  PubMed  Google Scholar 

  • Nicholson SJ, Srivastava V (2009) Transgene constructs lacking transcription termination signal induce efficient silencing of endogenous targets in Arabidopsis. Mol Genet Genom 282:319–328

    Article  CAS  Google Scholar 

  • 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 13:71–83

    Article  CAS  Google Scholar 

  • 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 12:1163–1173

    Article  CAS  PubMed  Google Scholar 

  • 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 30:2215–2231

    Article  CAS  PubMed  Google Scholar 

  • 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 95:12803–12808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 281:8843–8853

    Article  CAS  PubMed  Google Scholar 

  • Ralph J, Akiyama T, Coleman HD, Mansfield SD (2012) Effects on lignin structure of coumarate 3-hydroxylase downregulation in poplar. Bioenergy Res 5:1009–1019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 102:16573–16578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 184:99–113

    Article  CAS  PubMed  Google Scholar 

  • 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:e16416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saha BC (2003) Hemicellulose bioconversion. J Ind Microbiol Biotechnol 30:279–291

    Article  CAS  PubMed  Google Scholar 

  • SAS Institute (2008) Inc. SAS Software version 9.2. SAS Institute, Cary, NC

    Google Scholar 

  • 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 115:41–50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 68:1521–1529

    Article  CAS  PubMed  Google Scholar 

  • Simmons BA, Loque D, Ralph J (2010) Advances in modifying lignin for enhanced biofuel production. Curr Opin Plant Biol 13:313–320

    Article  CAS  PubMed  Google Scholar 

  • Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16:144–158

    CAS  Google Scholar 

  • 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 108:6300–6305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 581:169–183

    Article  CAS  Google Scholar 

  • 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 62:3837–3848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 47:969–976

    Article  CAS  PubMed  Google Scholar 

  • 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 117:101–112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 22:3357–3373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 111:845–850

    Article  PubMed  Google Scholar 

  • 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 57:1399–1411

    Article  PubMed  Google Scholar 

  • Vanholme R, Demedts B, Morreel K, Ralph J, Boerjan W (2010) Lignin biosynthesis and structure. Plant Physiol 153:895–905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 154:874–886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 17:379–392

    Article  PubMed  Google Scholar 

  • 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 104:11856–11861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 81:105–117

    Article  CAS  PubMed  Google Scholar 

  • 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 95:13959–13964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 27:581–590

    Article  CAS  PubMed  Google Scholar 

  • 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 192:611–625

    Article  CAS  PubMed  Google Scholar 

  • 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 5:58

    Article  CAS  Google Scholar 

  • 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 86:88–95

    Article  CAS  PubMed  Google Scholar 

  • Zamora R, Crispin JAS (1995) Production of an acid extract of rice straw. Acta Cient Venez 46:135–139

    CAS  PubMed  Google Scholar 

  • 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 140:972–83

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 52:1856–1871

    Article  CAS  PubMed  Google Scholar 

  • 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 285:38961–38968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by USDA-NIFA Capacity Building Grant # 2010-38821-21540. Authors thank Dr. Parastoo Azadi, Complex Carbohydrate Research Center, University of Georgia, Athens, GA, USA, for lignin analysis. The cDNA clones used in this study were obtained from Rice Genome Resource Center, National Institute of Agrobiological Sciences, Japan.

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Authors and Affiliations

  1. Department of Agriculture, University of Arkansas at Pine Bluff, 144 Woodard Hall, Pine Bluff, AR, 71601, USA

    Sathish K. Ponniah, Zhenhua Shang & Muthusamy Manoharan

  2. Department of Crop, Soil and Environmental Science, University of Arkansas, 115 Plant Science Building, Fayetteville, AR, 72701, USA

    M. Aydın Akbudak & Vibha Srivastava

  3. Department of Agricultural Biotechnology, Akdeniz University, Antalya, 07059, Turkey

    M. Aydın Akbudak

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  1. Sathish K. Ponniah
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  2. Zhenhua Shang
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  3. M. Aydın Akbudak
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  4. Vibha Srivastava
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  5. Muthusamy Manoharan
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Correspondence to Muthusamy Manoharan.

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Ponniah, S.K., Shang, Z., Akbudak, M.A. et al. 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). Plant Biotechnol Rep 11, 17–27 (2017). https://doi.org/10.1007/s11816-017-0426-y

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  • DOI: https://doi.org/10.1007/s11816-017-0426-y

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