Acta Physiologiae Plantarum

, 38:269 | Cite as

Building the wall: recent advances in understanding lignin metabolism in grasses

  • Igor CesarinoEmail author
  • Marcella Siqueira Simões
  • Michael dos Santos Brito
  • Amanda Fanelli
  • Tatiane da Franca Silva
  • Elisson Romanel


Secondary cell walls account for the majority of total plant biomass and, as mostly composed of polysaccharides, constitute a promising source of fermentable sugars for the production of biofuels and biomaterials. However, the presence of the aromatic polymer lignin largely precludes the release of monosaccharides during enzymatic hydrolysis of cell wall polysaccharides in the biorefinery. Therefore, it is essential to unraveling the molecular mechanisms underlying lignin metabolism in order to better exploit the potential of lignocellulosic biomass. In the context of the bioeconomy, grasses emerge as a prominent lignocellulosic feedstock due to their high yield potential for biomass production. Still, many aspects of lignin metabolism in grasses, including transcriptional regulation, biosynthesis and polymerization, remain poorly understood, in contrast to eudicots species. Moreover, grasses differ considerably from eudicots in vascular patterning and cell wall composition, suggesting the presence of many grass-specific molecular and biochemical mechanisms that are not found in eudicots and whose knowledge cannot be extrapolated from data obtained with eudicot model plants. Here, we summarize the most recent advances on structural features of grass lignin and on functional characterization of genes directly involved in diverse aspects of lignin metabolism in grasses.


Grasses Secondary cell wall Lignin Transcriptional regulation Bioengineering 



Marvin was used for drawing the chemical structures shown in Fig. 1, Marvin 15.3.30 (version number), 2015, ChemAxon ( Igor Cesarino acknowledges the Foundation for Research of the State of São Paulo (FAPESP) for the BIOEN Young Investigators Awards research fellowship (Grant 2015/02527-1). Marcella Siqueira Simões is indebted to FAPESP for a master fellowship (Grant 2015/18361-5). Michael dos Santos Brito thanks FAPESP for the financial support (Grant 2014/08468-4) and Young Investigators Awards research fellowship (Grant 2014/23017-9). Elisson Romanel acknowledges FAPESP for the financial support (Grants 2014/17486-6 and 2014/06923-6) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the financial support (Grant 444912/2014-2). Tatiane da Franca Silva thanks CNPq for the financial support (Grant 448042/2014-2). Amanda Fanelli is indebted to CNPq for a doctorate fellowship (Grant 142474/2015-0).


  1. Agarwal T, Grotewold E, Doseff AI, Gray J (2016) MYB31/MYB42 Syntelogs exhibit divergent regulation of phenylpropanoid genes in maize, sorghum and rice. Sci Rep 6:28502PubMedPubMedCentralCrossRefGoogle Scholar
  2. Alejandro S, Lee Y, Tohge T, Sudre D, Osorio S, Park J, Bovet L, Lee Y, Geldner N, Fernie AR, Martinoia E (2012) AtABCG29 is a monolignol transporter involved in lignin biosynthesis. Curr Biol CB 22:1207–1212. doi: 10.1016/j.cub.2012.04.064 PubMedCrossRefGoogle Scholar
  3. Barros J, Serk H, Granlund I, Pesquet E (2015) The cell biology of lignification in higher plants. Ann Bot 115:1053–1074. doi: 10.1093/aob/mcv046 PubMedPubMedCentralCrossRefGoogle Scholar
  4. Barros J, Serrani-Yarce JC, Chen F, Baxter D, Venables BJ, Dixon RA (2016) Role of bifunctional ammonia-lyase in grass cell wall biosynthesis. Nat Plants 2:16050. doi: 10.1038/nplants.2016.50 PubMedCrossRefGoogle Scholar
  5. Berthet S, Demont-Caulet N, Pollet B, Bidzinski P, Cézard L, Le Bris P, Borrega N, Hervé J, Blondet E, Balzergue S, Lapierre C, Jouanin L (2011) Disruption of LACCASE4 and 17 results in tissue-specific alterations to lignification of Arabidopsis thaliana stems. Plant Cell 23:1124–1137. doi: 10.1105/tpc.110.082792 PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bomal C, Bedon F, Caron S, Mansfield SD, Levasseur C, Cooke JEK, Blais S, Tremblay L, Morency M-J, Pavy N, Grima-Pettenati J, Séguin A, MacKay J (2008) Involvement of Pinus taeda MYB1 and MYB8 in phenylpropanoid metabolism and secondary cell wall biogenesis: a comparative in planta analysis. J Exp Bot 59:3925–3939. doi: 10.1093/jxb/ern234 PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bonawitz ND, Chapple C (2010) The genetics of lignin biosynthesis: connecting genotype to phenotype. Annu Rev Genet 44:337–363. doi: 10.1146/annurev-genet-102209-163508 PubMedCrossRefGoogle Scholar
  8. Bout S, Vermerris W (2003) A candidate-gene approach to clone the sorghum Brown midrib gene encoding caffeic acid O-methyltransferase. Mol Genet Genomics 269:205–214. doi: 10.1007/s00438-003-0824-4 PubMedGoogle Scholar
  9. Carpita NC, McCann MC (2008) Maize and sorghum: genetic resources for bioenergy grasses. Trends Plant Sci 13:415–420. doi: 10.1016/j.tplants.2008.06.002 PubMedCrossRefGoogle Scholar
  10. Cass CL, Peraldi A, Dowd PF, Mottiar Y, Santoro N, Karlen SD, Bukhman YV, Foster CE, Thrower N, Bruno LC, Moskvin OV, Johnson ET, Willhoit ME, Phutane M, Ralph J, Mansfield SD, Nicholson P, Sedbrook JC (2015) Effects of PHENYLALANINE AMMONIA LYASE (PAL) knockdown on cell wall composition, biomass digestibility, and biotic and abiotic stress responses in Brachypodium. J Exp Bot 66:4317–4335. doi: 10.1093/jxb/erv269 PubMedPubMedCentralCrossRefGoogle Scholar
  11. Cesarino I, Araujo P, Domingues Junior AP, Mazzafera P (2012a) An overview of lignin metabolism and its effect on biomass recalcitrance. Braz J Bot 35:303–311CrossRefGoogle Scholar
  12. Cesarino I, Araujo P, Sampaio Mayer JL, Paes Leme AF, Mazzafera P (2012b) Enzymatic activity and proteomic profile of class III peroxidases during sugarcane stem development. Plant Physiol Biochem 55:66–76. doi: 10.1016/j.plaphy.2012.03.014 PubMedCrossRefGoogle Scholar
  13. Cesarino I, Araujo P, Sampaio Mayer JL, Vicentini R, Berthet S, Demedts B, Vanholme B, Boerjan W, Mazzafera P (2013) Expression of SofLAC, a new laccase in sugarcane, restores lignin content but not S: G ratio of Arabidopsis lac17 mutant. J Exp Bot 64:1769–1781. doi: 10.1093/jxb/ert045 PubMedCrossRefGoogle Scholar
  14. Chen F, Dixon RA (2007) Lignin modification improves fermentable sugar yields for biofuel production. Nat Biotechnol 25:759–761. doi: 10.1038/nbt1316 PubMedCrossRefGoogle Scholar
  15. Courtois-Moreau CL, Pesquet E, Sjödin A, Muñiz L, Bollhöner B, Kaneda M, Samuels L, Jansson S, Tuominen H (2009) A unique program for cell death in xylem fibers of Populus stem. Plant J 58:260–274. doi: 10.1111/j.1365-313X.2008.03777.x PubMedCrossRefGoogle Scholar
  16. Del Río JC, Marques G, Rencoret J, Martínez ÁT, Gutiérrez A (2007) Occurrence of naturally acetylated lignin units. J Agric Food Chem 55:5461–5468. doi: 10.1021/jf0705264 PubMedCrossRefGoogle Scholar
  17. Del Río JC, Prinsen P, Rencoret J, Nieto L, Jiménez-Barbero J, Ralph J, Martínez ÁT, Gutiérrez A (2012a) Structural characterization of the lignin in the cortex and pith of elephant grass (Pennisetum purpureum) stems. J Agric Food Chem 60:3619–3634. doi: 10.1021/jf300099g PubMedCrossRefGoogle Scholar
  18. Del Río JC, Rencoret J, Prinsen P, Martinez AT, Ralph J, Gutierrez A (2012b) Structural characterization of wheat straw lignin as revealed by analytical pyrolysis, 2D-NMR, and reductive cleavage methods. J Agric Food Chem 60:5922–5935. doi: 10.1021/jf301002n PubMedCrossRefGoogle Scholar
  19. Del Río JC, Lino AG, Colodette JL, Lima CF, Gutiérrez A, Martínez ÁT, Lu F, Ralph J, Rencoret J (2015) Differences in the chemical structure of the lignins from sugarcane bagasse and straw. Biomass Bioenergy 81:322–338. doi: 10.1016/j.biombioe.2015.07.006 CrossRefGoogle Scholar
  20. Dima O, Morreel K, Vanholme B, Kim H, Ralph J, Boerjan W (2015) Small glycosylated lignin oligomers are stored in Arabidopsis leaf vacuoles. Plant Cell 27:695–710. doi: 10.1105/tpc.114.134643 PubMedPubMedCentralCrossRefGoogle Scholar
  21. Escamilla-Treviño LL, Shen H, Hernandez T, Yin Y, Xu Y, Dixon RA (2013) Early lignin pathway enzymes and routes to chlorogenic acid in switchgrass (Panicum virgatum L.). Plant Mol Biol 84:565–576. doi: 10.1007/s11103-013-0152-y PubMedCrossRefGoogle Scholar
  22. Fernández-Pérez F, Pomar F, Pedreño MA, Novo-Uzal E (2015) The suppression of AtPrx52 affects fibers but not xylem lignification in Arabidopsis by altering the proportion of syringyl units. Physiol Plant 154:395–406. doi: 10.1111/ppl.12310 PubMedCrossRefGoogle Scholar
  23. Fornalé S, Shi X, Chai C, Encina A, Irar S, Capellades M, Fuguet E, Torres J-L, Rovira P, Puigdomènech P, Rigau J, Grotewold E, Gray J, Caparrós-Ruiz D (2010) ZmMYB31 directly represses maize lignin genes and redirects the phenylpropanoid metabolic flux. Plant J 64:633–644. doi: 10.1111/j.1365-313X.2010.04363.x PubMedCrossRefGoogle Scholar
  24. Gray J, Caparrós-Ruiz D, Grotewold E (2012) Grass phenylpropanoids: regulate before using! Plant Sci 184:112–120. doi: 10.1016/j.plantsci.2011.12.008 PubMedCrossRefGoogle Scholar
  25. Ha CM, Escamilla-Trevino L, Yarce JCS, Kim H, Ralph J, Chen F, Dixon RA (2016) An essential role of caffeoyl shikimate esterase in monolignol biosynthesis in Medicago truncatula. Plant J 86:363–375. doi: 10.1111/tpj.13177 PubMedCrossRefGoogle Scholar
  26. Halpin C, Holt K, Chojecki J, Oliver D, Chabbert B, Monties B, Edwards K, Barakate A, Foxon GA (1998) Brown-midrib maize (bm1)—a mutation affecting the cinnamyl alcohol dehydrogenase gene. Plant J 14:545–553. doi: 10.1046/j.1365-313X.1998.00153.x PubMedCrossRefGoogle Scholar
  27. Handakumbura PP, Hazen SP (2012) Transcriptional regulation of grass secondary cell wall biosynthesis: playing catch-up with Arabidopsis thaliana. Plant Physiol 3:74. doi: 10.3389/fpls.2012.00074 Google Scholar
  28. Hatfield R, Ralph J, Grabber JH (2008) A potential role for sinapyl p-coumarate as a radical transfer mechanism in grass lignin formation. Planta 228:919–928. doi: 10.1007/s00425-008-0791-4 PubMedCrossRefGoogle Scholar
  29. Jin H (2000) Transcriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis. EMBO J 19:6150–6161. doi: 10.1093/emboj/19.22.6150 PubMedPubMedCentralCrossRefGoogle Scholar
  30. Lam PY, Zhu F-Y, Chan WL, Liu H, Lo C (2014) Cytochrome P450 93G1 is a flavone synthase II that channels flavanones to the biosynthesis of tricin O-linked conjugates in rice. Plant Physiol 165:1315–1327. doi: 10.1104/pp.114.239723 PubMedPubMedCentralCrossRefGoogle Scholar
  31. Lam PY, Liu H, Lo C (2015) Completion of tricin biosynthesis pathway in rice: cytochrome P450 75B4 is a unique chrysoeriol 5′-hydroxylase. Plant Physiol 168:1527–1536. doi: 10.1104/pp.15.00566 PubMedPubMedCentralCrossRefGoogle Scholar
  32. Lan W, Lu F, Regner M, Zhu Y, Rencoret J, Ralph SA, Zakai UI, Morreel K, Boerjan W, Ralph J (2015) Tricin, a flavonoid monomer in monocot lignification. Plant Physiol 167:1284–1295. doi: 10.1104/pp.114.253757 PubMedPubMedCentralCrossRefGoogle Scholar
  33. Lan W, Morreel K, Lu F, Rencoret J, Del Río JC, Voorend W, Vermerris W, Boerjan WA, Ralph J (2016a) Maize tricin-oligolignol metabolites and their implications for monocot lignification. Plant Physiol. doi: 10.1104/pp.16.02012 PubMedPubMedCentralGoogle Scholar
  34. Lan W, Rencoret J, Lu F, Karlen SD, Smith BG, Harris PJ, del Río JC, Ralph J (2016b) Tricin-Lignins: Occurrence and Quantitation of Tricin in Relation to Phylogeny. Plant J n/a–n/a. doi: 10.1111/tpj.13315 Google Scholar
  35. Lee Y, Rubio MC, Alassimone J, Geldner N (2013) A mechanism for localized lignin deposition in the endodermis. Cell 153:402–412. doi: 10.1016/j.cell.2013.02.045 PubMedCrossRefGoogle Scholar
  36. Lewis N, Yamamoto E (1990) Lignin: occurrence, biogenesis and biodegradation. Annu Rev Plant Physiol Plant Mol Biol 41:455–496. doi: 10.1146/annurev.pp.41.060190.002323 PubMedCrossRefGoogle Scholar
  37. Li L, Hill-Skinner S, Liu S, Beuchle D, Tang HM, Yeh C-T, Nettleton D, Schnable PS (2015) The maize brown midrib4 (bm4) gene encodes a functional folylpolyglutamate synthase. Plant J 81:493–504. doi: 10.1111/tpj.12745 PubMedPubMedCentralCrossRefGoogle Scholar
  38. Li M, Pu Y, Yoo CG, Ragauskas AJ (2016) The occurrence of tricin and its derivatives in plants. Green Chem 18:1439–1454. doi: 10.1039/C5GC03062E CrossRefGoogle Scholar
  39. Liu C-J (2012) Deciphering the enigma of lignification: precursor transport, oxidation, and the topochemistry of lignin assembly. Mol Plant 5:304–317. doi: 10.1093/mp/ssr121 PubMedCrossRefGoogle Scholar
  40. Lowe K, Wu E, Wang N, Hoerster G, Hastings C, Cho M-J, Scelonge C, Lenderts B, Chamberlin M, Cushatt J, Wang L, Ryan L, Khan T, Chow-Yiu J, Hua W, Yu M, Banh J, Bao Z, Brink K, Igo E, Rudrappa B, Shamseer PM, Bruce W, Newman L, Shen B, Zheng P, Bidney D, Falco SC, RegisterIII JC, Zhao Z-Y, Xu D, Jones TJ, Gordon-Kamm WJ (2016) Morphogenic regulators baby boom and wuschel improve monocot transformation. Plant Cell. doi: 10.1105/tpc.16.00124 PubMedPubMedCentralGoogle Scholar
  41. Lu F, Karlen SD, Regner M, Kim H, Ralph SA, Sun R-C, Kuroda K, Augustin MA, Mawson R, Sabarez H, Singh T, Jimenez-Monteon G, Zakaria S, Hill S, Harris PJ, Boerjan W, Wilkerson CG, Mansfield SD, Ralph J (2015) Naturally p-hydroxybenzoylated lignins in palms. BioEnergy Res 8:934–952. doi: 10.1007/s12155-015-9583-4 CrossRefGoogle Scholar
  42. Marita JM, Hatfield RD, Rancour DM, Frost KE (2014) Identification and suppression of the p-coumaroyl CoA:hydroxycinnamyl alcohol transferase in Zea mays L. Plant J 78:850–864. doi: 10.1111/tpj.12510 PubMedPubMedCentralCrossRefGoogle Scholar
  43. Marriott PE, Gómez LD, McQueen-Mason SJ (2016) Unlocking the potential of lignocellulosic biomass through plant science. New Phytol 209:1366–1381. doi: 10.1111/nph.13684 PubMedCrossRefGoogle Scholar
  44. Martins PK, Nakayama TJ, Ribeiro AP, Cunha BADB, Nepomuceno AL, Harmon FG, Kobayashi AK, Molinari HBC (2015a) Setaria viridis floral-dip: a simple and rapid Agrobacterium-mediated transformation method. Biotechnol Rep 6:61–63. doi: 10.1016/j.btre.2015.02.006 CrossRefGoogle Scholar
  45. Martins PK, Ribeiro AP, Cunha BADB, Kobayashi AK, Molinari HBC (2015b) A simple and highly efficient Agrobacterium-mediated transformation protocol for Setaria viridis. Biotechnol Rep 6:41–44. doi: 10.1016/j.btre.2015.02.002 CrossRefGoogle Scholar
  46. McCarthy RL, Zhong R, Ye Z-H (2009) MYB83 is a direct target of SND1 and acts redundantly with MYB46 in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell Physiol 50:1950–1964. doi: 10.1093/pcp/pcp139 PubMedCrossRefGoogle Scholar
  47. Meyermans H, Morreel K, Lapierre C, Pollet B, Bruyn AD, Busson R, Herdewijn P, Devreese B, Beeumen JV, Marita JM, Ralph J, Chen C, Burggraeve B, Montagu MV, Messens E, Boerjan W (2000) Modifications in lignin and accumulation of phenolic glucosides in poplar xylem upon down-regulation of caffeoyl-coenzyme a O-methyltransferase, an enzyme involved in lignin biosynthesis. J Biol Chem 275:36899–36909. doi: 10.1074/jbc.M006915200 PubMedCrossRefGoogle Scholar
  48. Mitsuda N, Iwase A, Yamamoto H, Yoshida M, Seki M, Shinozaki K, Ohme-Takagi M (2007) NAC transcription factors, NST1 and NST3, are key of the formation of secondary walls in woody tissues of Arabidopsis. Plant Cell 19:270–280. doi: 10.1105/tpc.106.047043 PubMedPubMedCentralCrossRefGoogle Scholar
  49. Moura JCMS, Bonine CAV, Viana JOF, Dornelas MC, Mazzafera P (2010) Abiotic and biotic stresses and changes in the lignin content and composition in plants. J Integr Plant Biol 52:360–376. doi: 10.1111/j.1744-7909.2010.00892.x PubMedCrossRefGoogle Scholar
  50. Noda S, Koshiba T, Hattori T, Yamaguchi M, Suzuki S, Umezawa T (2015) The expression of a rice secondary wall-specific cellulose synthase gene, OsCesA7, is directly regulated by a rice transcription factor, OsMYB58/63. Planta 242:589–600. doi: 10.1007/s00425-015-2343-z PubMedCrossRefGoogle Scholar
  51. Petrik DL, Karlen SD, Cass CL, Padmakshan D, Lu F, Liu S, Le Bris P, Antelme S, Santoro N, Wilkerson CG, Sibout R, Lapierre C, Ralph J, Sedbrook JC (2014) p-Coumaroyl-CoA:monolignol transferase (PMT) acts specifically in the lignin biosynthetic pathway in Brachypodium distachyon. Plant J 77:713–726. doi: 10.1111/tpj.12420 PubMedPubMedCentralCrossRefGoogle Scholar
  52. Ragauskas AJ, Beckham GT, Biddy MJ, Chandra R, Chen F, Davis MF, Davison BH, Dixon RA, Gilna P, Keller M, Langan P, Naskar AK, Saddler JN, Tschaplinski TJ, Tuskan GA, Wyman CE (2014) Lignin valorization: improving lignin processing in the biorefinery. Science 344:709. doi: 10.1126/science.1246843 CrossRefGoogle Scholar
  53. Ralph J (2010) Hydroxycinnamates in lignification. Phytochem Rev 9:65–83. doi: 10.1007/s11101-009-9141-9 CrossRefGoogle Scholar
  54. Ralph J, Hatfield RD, Quideau S, Helm RF, Grabber JH, Jung H-JG (1994) Pathway of p-coumaric acid incorporation into maize lignin as revealed by NMR. J Am Chem Soc 116:9448–9456. doi: 10.1021/ja00100a006 CrossRefGoogle Scholar
  55. Ralph J, Grabber JH, Hatfield RD (1995) Lignin-ferulate cross-links in grasses: active incorporation of ferulate polysaccharide esters into ryegrass lignins. Carbohydr Res 275:167–178. doi: 10.1016/0008-6215(95)00237-N CrossRefGoogle Scholar
  56. Ralph J, Lundquist K, Brunow G, Lu F, Kim H, Schatz PF, Marita JM, Hatfield RD, Ralph SA, Christensen JH, Boerjan W (2004) Lignins: natural polymers from oxidative coupling of 4-hydroxyphenyl-propanoids. Phytochem Rev 3:29–60. doi: 10.1023/B:PHYT.0000047809.65444.a4 CrossRefGoogle Scholar
  57. Rencoret J, Ralph J, Marques G, Gutierrez A, Martinez AT, del Rio JC (2013) Structural characterization of lignin isolated from coconut (Cocos nucifera) coir fibers. J Agric Food Chem 61:2434–2445. doi: 10.1021/jf304686x PubMedCrossRefGoogle Scholar
  58. Riboulet C, Guillaumie S, Mechin V, Bosio M, Pichon M, Goffner D, Lapierre C, Pollet B, Lefevre B, Martinant JP, Barriere Y (2009) Kinetics of phenylpropanoid gene expression in maize growing internodes: relationships with cell wall deposition. Crop Sci 49:211–223. doi: 10.2135/cropsci2008.03.0130 CrossRefGoogle Scholar
  59. Rosler J, Krekel F, Amrhein N, Schmid J (1997) Maize phenylalanine ammonia-lyase has tyrosine ammonia-lyase activity. Plant Physiol 113:175–179. doi: 10.1104/pp.113.1.175 PubMedPubMedCentralCrossRefGoogle Scholar
  60. Saballos A, Ejeta G, Sanchez E, Kang C, 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 181:783–795. doi: 10.1534/genetics.108.098996 PubMedPubMedCentralCrossRefGoogle Scholar
  61. Saballos A, Sattler SE, Sanchez E, Foster TP, Xin Z, Kang C, Pedersen JF, 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. doi: 10.1111/j.1365-313X.2012.04933.x PubMedCrossRefGoogle Scholar
  62. Saha P, Blumwald E (2016) Spike-dip transformation of Setaria viridis. Plant J 86:89–101. doi: 10.1111/tpj.13148 PubMedCrossRefGoogle Scholar
  63. 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 178:229–238. doi: 10.1016/j.plantsci.2010.01.001 CrossRefGoogle Scholar
  64. Scully ED, Gries T, Sarath G, Palmer NA, Baird L, Serapiglia MJ, Dien BS, Boateng AA, Ge Z, Funnell-Harris DL, Twigg P, Clemente TE, Sattler SE (2016) Overexpression of SbMyb60 impacts phenylpropanoid biosynthesis and alters secondary cell wall composition in Sorghum bicolor. Plant J 85:378–395. doi: 10.1111/tpj.13112 PubMedCrossRefGoogle Scholar
  65. Shen H, He X, Poovaiah CR, Wuddineh WA, Ma J, Mann DGJ, Wang H, Jackson L, Tang Y, Neal Stewart C, Chen F, Dixon RA (2012) Functional characterization of the switchgrass (Panicum virgatum) R2R3-MYB transcription factor PvMYB4 for improvement of lignocellulosic feedstocks. New Phytol 193:121–136. doi: 10.1111/j.1469-8137.2011.03922.x PubMedCrossRefGoogle Scholar
  66. Shen H, Mazarei M, Hisano H, Escamilla-Trevino L, Fu C, Pu Y, Rudis MR, Tang Y, Xiao X, Jackson L, Li G, Hernandez T, Chen F, Ragauskas AJ, Stewart CN, Wang Z-Y, Dixon RA (2013) A genomics approach to deciphering lignin biosynthesis in switchgrass. Plant Cell 25:4342–4361. doi: 10.1105/tpc.113.118828 PubMedPubMedCentralCrossRefGoogle Scholar
  67. Shigeto J, Kiyonaga Y, Fujita K, Kondo R, Tsutsumi Y (2013) Putative cationic cell-wall-bound peroxidase homologues in Arabidopsis, AtPrx2, AtPrx25, and AtPrx71, are involved in lignification. J Agric Food Chem 61:3781–3788. doi: 10.1021/jf400426g PubMedCrossRefGoogle Scholar
  68. Sonbol F-M, Fornalé S, Capellades M, Encina A, Touriño S, Torres J-L, Rovira P, Ruel K, Puigdomènech P, Rigau J, Caparrós-Ruiz D (2009) The maize ZmMYB42 represses the phenylpropanoid pathway and affects the cell wall structure, composition and degradability in Arabidopsis thaliana. Plant Mol Biol 70:283–296. doi: 10.1007/s11103-009-9473-2 PubMedCrossRefGoogle Scholar
  69. Tang HM, Liu S, Hill-Skinner S, Wu W, Reed D, Yeh C-T, Nettleton D, Schnable PS (2014) The maize brown midrib2 (bm2) gene encodes a methylenetetrahydrofolate reductase that contributes to lignin accumulation. Plant J 77:380–392. doi: 10.1111/tpj.12394 PubMedPubMedCentralCrossRefGoogle Scholar
  70. Taylor-Teeples M, Lin L, de Lucas M, Turco G, Toal TW, Gaudinier A, Young NF, Trabucco GM, Veling MT, Lamothe R, Handakumbura PP, Xiong G, Wang C, Corwin J, Tsoukalas A, Zhang L, Ware D, Pauly M, Kliebenstein DJ, Dehesh K, Tagkopoulos I, Breton G, Pruneda-Paz JL, Ahnert SE, Kay SA, Hazen SP, Brady SM (2015) An Arabidopsis gene regulatory network for secondary cell wall synthesis. Nature 517:571–575. doi: 10.1038/nature14099 PubMedCrossRefGoogle Scholar
  71. Tohge T, Watanabe M, Hoefgen R, Fernie AR (2013) The evolution of phenylpropanoid metabolism in the green lineage. Crit Rev Biochem Mol Biol 48:123–152. doi: 10.3109/10409238.2012.758083 PubMedCrossRefGoogle Scholar
  72. Valdivia ER, Herrera MT, Gianzo C, Fidalgo J, Revilla G, Zarra I, Sampedro J (2013) Regulation of secondary wall synthesis and cell death by NAC transcription factors in the monocot Brachypodium distachyon. J Exp Bot 64:1333–1343. doi: 10.1093/jxb/ers394 PubMedPubMedCentralCrossRefGoogle Scholar
  73. Van Acker R, Vanholme R, Storme V, Mortimer JC, Dupree P, Boerjan W (2013) Lignin biosynthesis perturbations affect secondary cell wall composition and saccharification yield in Arabidopsis thaliana. Biotechnol Biofuels 6:46. doi: 10.1186/1754-6834-6-46 PubMedPubMedCentralCrossRefGoogle Scholar
  74. van der Weijde T, Alvim Kamei CL, Torres AF, Vermerris W, Dolstra O, Visser RGF, Trindade LM (2013) The potential of C4 grasses for cellulosic biofuel production. Front Plant Sci 4:107. doi: 10.3389/fpls.2013.00107 PubMedPubMedCentralGoogle Scholar
  75. Vanholme R, Morreel K, Ralph J, Boerjan W (2008) Lignin engineering. Curr Opin Plant Biol 11:278–285. doi: 10.1016/j.pbi.2008.03.005 PubMedCrossRefGoogle Scholar
  76. Vanholme R, Morreel K, Darrah C, Oyarce P, Grabber JH, Ralph J, Boerjan W (2012) Metabolic engineering of novel lignin in biomass crops. New Phytol 196:978–1000. doi: 10.1111/j.1469-8137.2012.04337.x PubMedCrossRefGoogle Scholar
  77. Vanholme R, Cesarino I, Rataj K, Xiao Y, Sundin L, Goeminne G, Kim H, Cross J, Morreel K, Araujo P, Welsh L, Haustraete J, McClellan C, Vanholme B, Ralph J, Simpson GG, Halpin C, Boerjan W (2013) Caffeoyl shikimate esterase (CSE) is an enzyme in the lignin biosynthetic pathway in Arabidopsis. Science 341:1103–1106. doi: 10.1126/science.1241602 PubMedCrossRefGoogle Scholar
  78. Vargas L, Cesarino I, Vanholme R, Voorend W, de Lyra Soriano Saleme M, Morreel K, Boerjan W (2016) Improving total saccharification yield of Arabidopsis plants by vessel-specific complementation of caffeoyl shikimate esterase (cse) mutants. Biotechnol Biofuels 9:139. doi: 10.1186/s13068-016-0551-9 PubMedPubMedCentralCrossRefGoogle Scholar
  79. Vicentini R, Bottcher A, dos Santos Brito M, dos Santos AB, Creste S, de Andrade Landell MG, Cesarino I, Mazzafera P (2015) Large-scale transcriptome analysis of two sugarcane genotypes contrasting for lignin content. PLoS One 10:e0134909PubMedPubMedCentralCrossRefGoogle Scholar
  80. Vignols F, Rigau J, Torres MA, Capellades M, Puigdomènech P (1995) The brown midrib3 (bm3) mutation in maize occurs in the gene encoding caffeic acid O-methyltransferase. Plant Cell 7:407–416. doi: 10.1105/tpc.7.4.407 PubMedPubMedCentralCrossRefGoogle Scholar
  81. Vogel J (2008) Unique aspects of the grass cell wall. Curr Opin Plant Biol 11:301–307. doi: 10.1016/j.pbi.2008.03.002 PubMedCrossRefGoogle Scholar
  82. Wang Y, Chantreau M, Sibout R, Hawkins S (2013) Plant cell wall lignification and monolignol metabolism. Front Plant Sci 4:220. doi: 10.3389/fpls.2013.00220 PubMedPubMedCentralGoogle Scholar
  83. Wang J, Feng J, Jia W, Chang S, Li S, Li Y (2015a) Lignin engineering through laccase modification: a promising field for energy plant improvement. Biotechnol Biofuels 8:145. doi: 10.1186/s13068-015-0331-y PubMedPubMedCentralCrossRefGoogle Scholar
  84. Wang Y, Bouchabke-Coussa O, Lebris P, Antelme S, Soulhat C, Gineau E, Dalmais M, Bendahmane A, Morin H, Mouille G, Legée F, Cézard L, Lapierre C, Sibout R (2015b) LACCASE5 is required for lignification of the brachypodium distachyon culm. Plant Physiol 168:192–204. doi: 10.1104/pp.114.255489 PubMedPubMedCentralCrossRefGoogle Scholar
  85. Watts KT, Mijts BN, Lee PC, Manning AJ, Schmidt-Dannert C (2006) Discovery of a substrate selectivity switch in tyrosine ammonia-lyase, a member of the aromatic amino acid lyase family. Chem Biol 13:1317–1326. doi: 10.1016/j.chembiol.2006.10.008 PubMedCrossRefGoogle Scholar
  86. Wen J-L, Sun S-L, Xue B-L, Sun R-C (2013) Quantitative structural characterization of the lignins from the stem and pith of bamboo (Phyllostachys pubescens). Holzforschung 67:613–627. doi: 10.1515/hf-2012-0162 CrossRefGoogle Scholar
  87. Wilkerson CG, Mansfield SD, Lu F, Withers S, Park J-Y, Karlen SD, Gonzales-Vigil E, Padmakshan D, Unda F, Rencoret J, Ralph J (2014) Monolignol ferulate transferase introduces chemically labile linkages into the lignin backbone. Science 344:90–93. doi: 10.1126/science.1250161 PubMedCrossRefGoogle Scholar
  88. Withers S, Lu F, Kim H, Zhu Y, Ralph J, Wilkerson CG (2012) Identification of grass-specific enzyme that acylates monolignols with p-coumarate. J Biol Chem 287:8347–8355. doi: 10.1074/jbc.M111.284497 PubMedPubMedCentralCrossRefGoogle Scholar
  89. Yamaguchi M, Kubo M, Fukuda H, Demura T (2008) VASCULAR-RELATED NAC-DOMAIN7 is involved in the differentiation of all types of xylem vessels in Arabidopsis roots and shoots. Plant J 55:652–664. doi: 10.1111/j.1365-313X.2008.03533.x PubMedCrossRefGoogle Scholar
  90. Yamaguchi M, Mitsuda N, Ohtani M, Ohme-Takagi M, Kato K, Demura T (2011) VASCULAR-RELATED NAC-DOMAIN 7 directly regulates the expression of a broad range of genes for xylem vessel formation. Plant J 66:579–590. doi: 10.1111/j.1365-313X.2011.04514.x PubMedCrossRefGoogle Scholar
  91. You T-T, Mao J-Z, Yuan T-Q, Wen J-L, Xu F (2013) Structural elucidation of the lignins from stems and foliage of arundo donax linn. J Agric Food Chem 61:5361–5370. doi: 10.1021/jf401277v PubMedCrossRefGoogle Scholar
  92. Zhao Q, Nakashima J, Chen F, Yin Y, Fu C, Yun J, Shao H, Wang X, Wang Z-Y, Dixon RA (2013) LACCASE is necessary and nonredundant with PEROXIDASE for lignin polymerization during vascular development in Arabidopsis. Plant Cell 25:3976–3987. doi: 10.1105/tpc.113.117770 PubMedPubMedCentralCrossRefGoogle Scholar
  93. Zhong R, Ye Z-H (2012) MYB46 and MYB83 Bind to the SMRE sites and directly activate a suite of transcription factors and secondary wall biosynthetic genes. Plant Cell Physiol 53:368–380. doi: 10.1093/pcp/pcr185 PubMedCrossRefGoogle Scholar
  94. Zhong R, Ye Z-H (2014) Complexity of the transcriptional network controlling secondary wall biosynthesis. Plant Sci 229:193–207. doi: 10.1016/j.plantsci.2014.09.009 PubMedCrossRefGoogle Scholar
  95. Zhong R, Ye Z-H (2015) Secondary cell walls: biosynthesis, patterned deposition and transcriptional regulation. Plant Cell Physiol 56:195–214. doi: 10.1093/pcp/pcu140 PubMedCrossRefGoogle Scholar
  96. Zhong R, Demura T, Ye Z-H (2006) SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell 18:3158–3170. doi: 10.1105/tpc.106.047399 PubMedPubMedCentralCrossRefGoogle Scholar
  97. Zhong R, Richardson EA, Ye Z-H (2007) The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. Plant Cell 19:2776–2792. doi: 10.1105/tpc.107.053678 PubMedPubMedCentralCrossRefGoogle Scholar
  98. Zhong R, Lee C, Zhou J, McCarthy RL, Ye Z-H (2008) A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell 20:2763–2782. doi: 10.1105/tpc.108.061325 PubMedPubMedCentralCrossRefGoogle Scholar
  99. Zhong R, Lee C, Ye Z-H (2010) Global analysis of direct targets of secondary wall NAC master switches in Arabidopsis. Mol Plant 3:1087–1103. doi: 10.1093/mp/ssq062 PubMedCrossRefGoogle Scholar
  100. Zhong R, Lee C, McCarthy RL, Reeves CK, Jones EG, Ye Z-H (2011a) Transcriptional activation of secondary wall biosynthesis by rice and maize NAC and MYB transcription factors. Plant Cell Physiol 52:1856–1871. doi: 10.1093/pcp/pcr123 PubMedCrossRefGoogle Scholar
  101. Zhong R, McCarthy RL, Lee C, Ye Z-H (2011b) Dissection of the transcriptional program regulating secondary wall biosynthesis during wood formation in poplar. Plant Physiol 157:1452–1468. doi: 10.1104/pp.111.181354 PubMedPubMedCentralCrossRefGoogle Scholar
  102. Zhong R, Yuan Y, Spiekerman JJ, Guley JT, Egbosiuba JC, Ye Z-H (2015) Functional characterization of NAC and MYB transcription factors involved in regulation of biomass production in switchgrass (Panicum virgatum). PLoS One 10:e0134611PubMedPubMedCentralCrossRefGoogle Scholar
  103. Zhou J-M, Gold ND, Martin VJJ, Wollenweber E, Ibrahim RK (2006) Sequential O-methylation of tricetin by a single gene product in wheat. Biochim Biophys Acta-Gen Subj 1760:1115–1124. doi: 10.1016/j.bbagen.2006.02.008 CrossRefGoogle Scholar
  104. Zhou J, Lee C, Zhong R, Ye Z-H (2009) MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. Plant Cell 21:248–266. doi: 10.1105/tpc.108.063321 PubMedPubMedCentralCrossRefGoogle Scholar
  105. Zhou J, Zhong R, Ye Z-H (2014) Arabidopsis NAC domain proteins, VND1 to VND5, are transcriptional regulators of secondary wall biosynthesis in vessels. PLoS One 9:e105726. doi: 10.1371/journal.pone.0105726 PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2016

Authors and Affiliations

  1. 1.Departamento de Botânica, Instituto de BiociênciasUniversidade de São PauloSão PauloBrazil
  2. 2.Centro Avançado da Pesquisa Tecnológica do Agronegócio de Cana, CP 206Ribeirão PretoBrazil
  3. 3.Departamento de Biotecnologia, Escola de Engenharia de LorenaUniversidade de São Paulo (EEL-USP), CP 116LorenaBrazil

Personalised recommendations