Molecular Breeding

, 35:87 | Cite as

Toward the identification of genes underlying maize QTLs for lignin content, focusing on colocalizations with lignin biosynthetic genes and their regulatory MYB and NAC transcription factors

  • Yves BarrièreEmail author
  • Audrey Courtial
  • Marçal Soler
  • Jacqueline Grima-Pettenati


The identification of genes controlling lignin content is of crucial importance for breeding maize with improved feeding value and yielding more bioenergy after fermentation into alcohol or methane. Up to now, the gene families mostly impacting observed variations in cell wall lignin content have not yet been identified. However, genes involved in monolignol biosynthesis and polymerization, and the MYB and NAC transcription factors that regulate their activities, are promising candidates. In order to test this hypothesis, colocalizations between genes of these families and QTLs for lignin content originating from nine RIL families were investigated, based on gene and QTL physical positions. Ninety-three lignin QTLs were thus collected which corresponded to 44 non-overlapping positions. Among these positions, 11 were jointly shared by three or four RIL progenies, while lignin QTLs were observed for only one progeny in 16 positions. In addition to the few genes described in maize, candidate genes involved in monolignol biosynthesis and regulation of secondary wall lignification were searched for as orthologs of genes with such functions from several species including Arabidopsis, eucalyptus, poplar, and rice. Altogether, 50 ZmMYB-, 49 ZmNAC-, and 95 monolignol-related genes were considered as putative candidates. ZmMYB genes were found colocalizing with lignin QTLs in 25 positions, ZmNAC in 22 positions, and both ZmMYB and ZmNAC genes were present together in 12 QTL positions. Finally, 74 % of ZmMYB and 63 % of ZmNAC putatively involved in secondary wall regulation colocalized with or were close to lignin QTLs. Similarly, 66 % of genes involved in monolignol biosynthesis colocalized with QTL positions, whereas fewer colocalizations were observed for laccases and peroxidases putatively involved in lignin polymerization. In addition, the maize ortholog of the EgMYB2/AtMYB46 secondary cell wall master regulator was not highlighted in this study, possibly indicating significant divergences in the regulation of lignification between grasses and dicotyledonous plants. In contrast, based on gene number and colocalizations with lignin QTLs, orthologs of EgMYB1/AtMYB4 genes seem to have a greater importance in maize and grasses than in dicotyledonous species during secondary wall biosynthesis and deposition.


Maize QTL Candidate gene Lignin Monolignol MYB NAC 



4-Coumarate-CoA ligase


p-coumaroyl-shikimate/quinate 3-hydroxylase


Cinnamate 4-hydroxylase


Cinnamyl alcohol dehydrogenase


Caffeic acid O-methyltransferase


Caffeoyl-CoA O-methyltransferase


Cinnamoyl-CoA reductase


Caffeoyl shikimate esterase


Ferulate 5-hydroxylase


Hydroxycinnamoyl-CoA shikimate/quinate hydroxycinnamoyl transferase


Phenylalanine amonia lyase

H unit

p-hydroxyphenyl lignin unit

G unit

Guaiacyl lignin unit

S unit

Syringyl lignin unit


Quantitative trait locus


Logarithm (base 10) of odds




Megabase pair



Andrea Cardinal, Haixiao Hu, and Matthew Krakowsky are greatly thanked for providing unpublished complementary data allowing a larger compilation of maize lignin QTLs. The French Ministry of Research, the seed companies involved in the French Genomic project “Génoplante”, and the seed companies involved in the PROMAÏS—INRA network (Advanta, Caussade Semences, Limagrain Genetics, MaïsAdour, Monsanto SAS, Pioneer Génétique, Pau Euralis, R2n RAGT Semences, SDME KWS France, Syngenta seeds) are thanked for their contributions to funding the French works quoted in this review.

Supplementary material

11032_2015_275_MOESM1_ESM.xls (60 kb)
Supplementary material 1 (XLS 59 kb)


  1. Barrière Y, Emile JC, Traineau R, Surault F, Briand M, Gallais A (2004a) Genetic variation for organic matter and cell wall digestibility in silage maize. Lessons from a 34-year long experiment with sheep in digestibility crates. Maydica 49:115–126Google Scholar
  2. Barrière Y, Ralph J, Méchin V, Guillaumie S, Grabber JH, Argillier O, Chabbert B, Lapierre C (2004b) Genetic and molecular basis of grass cell wall biosynthesis and degradability. II. Lessons from brown-midrib mutants. CR Biol 327:847–860CrossRefGoogle Scholar
  3. Barrière Y, Riboulet C, Méchin V, Maltese S, Pichon M, Cardinal AJ, Lapierre C, Lübberstedt T, Martinant JP (2007) Genetics and genomics of lignification in grass cell walls based on maize as a model system. Genes Genomes Genomics 1:133–156Google Scholar
  4. Barrière Y, Thomas J, Denoue D (2008) QTL mapping for lignin content, lignin monomeric composition, p-hydroxycinnamate content, and cell wall digestibility in the maize recombinant inbred line progeny F838 × F286. Plant Sci 175:585–595CrossRefGoogle Scholar
  5. Barrière Y, Méchin V, Lafarguette F, Manicacci D, Guillon F, Wang H, Lauressergues D, Pichon M, Bosio M, Tatout C (2009) Toward the discovery of maize cell wall genes involved in silage maize quality and capacity to biofuel production. Maydica 54:161–198Google Scholar
  6. Barrière Y, Méchin V, Denoue D, Bauland C, Laborde J (2010) QTL for yield, earliness and cell wall digestibility traits in topcross experiments of F838 × F286 RIL progenies. Crop Sci 50:1761–1772CrossRefGoogle Scholar
  7. Barrière Y, Méchin V, Lefevre B, Maltese S (2012) QTLs for agronomic and cell wall traits in a maize RIL progeny derived from a cross between an old Minnesota13 line and a modern Iodent line. Theor Appl Genet 125:531–549CrossRefPubMedGoogle Scholar
  8. Barrière Y, Chavigneau H, Delaunay S, Courtial A, Bosio M, Lassagne H, Derory J, Lapierre C, Méchin V, Tatout C (2013) Different mutations in the ZmCAD2 gene underlie the maize brown-midrib1 (bm1) phenotype with similar effects on lignin characteristics and have potential interest for bioenergy production. Maydica 58:6–20Google Scholar
  9. Berthet S, Demont-Caulet N, Pollet B, Bidzinski P, Cezard L, Le Bris P, Borrega N, Herve 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 23:1124–1137CrossRefPubMedCentralPubMedGoogle Scholar
  10. Bosch M, Mayer CD, Cookson A, Donnison IS (2011) Identification of genes involved in cell wall biogenesis in grasses by differential gene expression profiling of elongating and non-elongating maize internodes. J Exp Bot 62:3545–3561CrossRefPubMedCentralPubMedGoogle Scholar
  11. Cardinal AJ, Lee M, Moore KJ (2003) Genetic mapping and analysis of quantitative trait loci affecting fiber and lignin content in maize. Theor Appl Genet 106:866–874PubMedGoogle Scholar
  12. Cassan-Wang H, Goué N, Saidi MN, Legay S, Sivadon P, Goffner D, Grima-Pettenati J (2013) Identification of novel transcription factors regulating secondary cell wall formation in Arabidopsis. Front Plant Sci 4:189CrossRefPubMedCentralPubMedGoogle Scholar
  13. Chavigneau H, Goué N, Courtial A, Jouanin L, Reymond M, Méchin V, Barrière Y (2012) QTL for floral stem lignin content and degradability in three recombinant inbred line (RIL) progenies of Arabidopsis thaliana and search for candidate genes involved in cell wall biosynthesis and degradability. Open J Genet 2:7–30CrossRefGoogle Scholar
  14. Chen Y, Liu H, Ali F, Scott MP, Ji O, Frei UK, Lübberstedt T (2012) Genetic and physical fine mapping of the novel brown midrib gene bm6 in maize (Zea mays L.) to a 180 kb region on chromosome 2. Theor Appl Genet 125:1223–1235CrossRefPubMedGoogle Scholar
  15. Courtial A, Soler M, Chateigner-Boutin AL, Reymond M, Méchin V, Wang H, Grima-Pettenati J, Barrière Y (2013a) Breeding grasses for silage feeding value or capacity to biofuel production: an updated list of genes involved in maize secondary cell wall biosynthesis and assembly. Maydica 58:67–102Google Scholar
  16. Courtial A, Thomas J, Reymond M, Méchin V, Grima-Pettenati J, Barrière Y (2013b) Targeted linkage map densification to improve cell wall related QTL detection and interpretation in maize. Theor Appl Genet 126:1151–1165CrossRefPubMedGoogle Scholar
  17. Courtial A, Méchin V, Reymond M, Grima-Pettenati J, Barrière Y (2014) Colocalizations between several QTLs for cell wall degradability and composition in the F288 × F271 early maize RIL progeny raise the question of the nature of the possible underlying determinants and breeding targets for biofuel capacity. Bioenerg Res 7:142–156CrossRefGoogle Scholar
  18. Craven-Bartle B, Pascual MB, Cánovas FM, Avila C (2013) A Myb transcription factor regulates genes of the phenylalanine pathway in maritime pine. Plant J 74:755–766CrossRefPubMedGoogle Scholar
  19. Damaj MB, Kumpatla SP, Emani C, Beremand PD, Reddy AS, Rathore KS, Buenrostro-Nava MT, Curtis IS, Thomas TL, Mirkov TE (2010) Sugarcane DIRIGENT and O-methyltransferase promoters confer stem-regulated gene expression in diverse monocots. Planta 231:1439–1458CrossRefPubMedGoogle Scholar
  20. De Obeso M, Caparrós-Ruiz D, Vignols F, Puigdomenech P, Rigau J (2003) Characterisation of maize peroxidases having differential patterns of mRNA accumulation in relation to lignifying tissues. Gene 309:23–33CrossRefPubMedGoogle Scholar
  21. Du H, Feng BR, Yang SS, Huang YB, Tang YX (2012) The R2R3-MYB transcription factor gene family in maize. PLoS ONE 7:e37463CrossRefPubMedCentralPubMedGoogle Scholar
  22. Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15:573–581CrossRefPubMedGoogle Scholar
  23. Escamilla-Treviño LL, Shen H, Uppalapati SR, Ray T, Tang Y, Hernandez T, Yin Y, Xu Y, Dixon RA (2010) Switchgrass (Panicum virgatum) possesses a divergent family of cinnamoyl CoA reductases with distinct biochemical properties. New Phytol 185:143–155CrossRefPubMedGoogle Scholar
  24. Fornalé S, Shi X, Chai C, Encina A, Irar S, Capellades M, Fuguet E, Torres JL, 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 64:633–644CrossRefPubMedGoogle Scholar
  25. Foucart C, Jauneau A, Gion JM, Amelot N, Martinez Y, Panegos P, Grima-Pettenati J, Sivadon P (2009) Overexpression of EgROP1, a Eucalyptus vascular-expressed Rac-like small GTPase, affects secondary xylem formation in Arabidopsis thaliana. New Phytol 183:1014–1029CrossRefPubMedGoogle Scholar
  26. Francoz E, Ranocha P, Nguyen-Kim H, Jamet E, Burlat V, Dunand (2014) Roles of cell wall peroxidases in plant development. Phytochemistry. doi: 10.1016/j.phytochem.2014.07.020
  27. Goering HK, Van Soest PJ (1970) Forage fiber analysis (Apparatus, reagents, procedures and some applications). U.S. Department of Agriculture. Handbook no. 379, pp 1–20Google Scholar
  28. Goicoechea M, Lacombe E, Legay S, Mihaljevic S, Rech P, Jauneau A, Lapierre C, Pollet B, Verhaegen D, Chaubet-Gigot N, Grima-Pettenati J (2005) EgMYB2, a new transcriptional activator from Eucalyptus xylem, regulates secondary cell wall formation and lignin biosynthesis. Plant J 43:553–567CrossRefPubMedGoogle Scholar
  29. Grabber JH, Quideau S, Ralph J (1996) p-Coumaroylated syringyl units in maize lignin; implications for β-ether cleavage by thioacidolysis. Phytochemistry 43:1189–1194CrossRefGoogle Scholar
  30. Grabber JH, Ralph J, Lapierre C, Barrière Y (2004) Genetic and molecular basis of grass cell-wall degradability. I. Lignin-cell wall matrix interactions. CR Biol 327:455–465CrossRefGoogle Scholar
  31. Grant EH, Fujino T, Beers EP, Brunner AM (2010) Characterization of NAC domain transcription factors implicated in control of vascular cell differentiation in Arabidopsis and Populus. Planta 232:337–352CrossRefPubMedGoogle Scholar
  32. Gray J, Caparrós-Ruiz D, Grotewold E (2012) Grass phenylpropanoids: regulate before using! Plant Sci 184:112–120CrossRefPubMedGoogle Scholar
  33. Grima-Pettenati J, Soler M, Camargo E, Wang H (2012) Transcriptional regulation of the lignin biosynthetic pathway revisited: new players and insights. In: Jouanin L, Lapierre C (eds) Advances in botanical research, vol 61, Chapter 6. Academic Press, Waltham, pp 173–218Google Scholar
  34. Guillaumie S, San-Clemente H, Deswarte C, Martinez Y, Lapierre C, Murigneux A, Barrière Y, Pichon M, Goffner D (2007a) MAIZEWALL. Database and developmental gene expression profiling of cell wall biosynthesis and assembly in maize. Plant Physiol 143:339–363CrossRefPubMedCentralPubMedGoogle Scholar
  35. Guillaumie S, Pichon M, Martinant JP, Bosio M, Goffner D, Barrière Y (2007b) Differential expression of phenylpropanoid and related genes in brown-midrib bm1, bm2, bm3, and bm4 young near-isogenic maize plants. Planta 226:235–250CrossRefPubMedGoogle Scholar
  36. Guillaumie S, Mzid R, Méchin V, Léon C, Hichri I, Destrac-Irvine A, Trossat-Magnin C, Delrot S, Lauvergeat V (2010) The grapevine transcription factor WRKY2 influences the lignin pathway and xylem development in tobacco. Plant Mol Biol 72:215–234CrossRefPubMedGoogle Scholar
  37. Guillet-Claude C, Birolleau-Touchard C, Manicacci D, Rogowsky PM, Rigau J, Murigneux A, Martinant JP, Barrière Y (2004) Nucleotide diversity of the ZmPox3 maize peroxidase gene: relationships between a MITE insertion in exon 2 and variation in forage maize digestibility. BMC Genet 5:19CrossRefPubMedCentralPubMedGoogle Scholar
  38. Hall H, Ellis B (2013) Transcriptional programming during cell wall maturation in the expanding Arabidopsis stem. BMC Plant Biol 13:14CrossRefPubMedCentralPubMedGoogle Scholar
  39. Hatfield R, Ralph J, Grabber JH (2008) A potential role for sinapyl p-coumarate as a radical transfer mechanism in grass lignin formation. Planta 228:919–928CrossRefPubMedGoogle Scholar
  40. Herrero J, Fernández-Pérez F, Yebra T, Novo-Uzal E, Pomar F, Pedreño MA, Cuello J, Guéra A, Esteban-Carrasco A, Zapata JM (2013) Bioinformatic and functional characterization of the basic peroxidase 72 from Arabidopsis thaliana involved in lignin biosynthesis. Planta 237:1599–1612CrossRefPubMedGoogle Scholar
  41. Hirano K, Aya K, Morinaka Y, Nagamatsu S, Sato Y, Antonio BA, Namiki N, Nagamura Y, Matsuoka M (2013) Survey of genes involved in rice secondary cell wall formation through a co-expression network. Plant Cell Physiol 54:1803–1821CrossRefPubMedGoogle Scholar
  42. Hu H (2011) QTL analysis of stalk strength in maize RIL population BEHO. Master thesis, National Maize Improvement Center of China, China Agricultural University, Beijing, China (in Chinese with English abstract)Google Scholar
  43. Hu H, Meng Y, Wang H, Liu H, Chen S (2012) Identifying quantitative trait loci and determining closely related stalk traits for rind penetrometer resistance in a high-oil maize population. Theor Appl Genet 124:1439–1447CrossRefPubMedGoogle Scholar
  44. Hu H, Liu W, Fu Z, Homann L, Technow F, Wang H, Song C, Li S, Melchinger AE, Chen S (2013) QTL mapping of stalk bending strength in a recombinant inbred line maize population. Theor Appl Genet 126:2257–2266CrossRefPubMedGoogle Scholar
  45. Kawaoka A, Ebinuma H (2001) Transcriptional control of lignin biosynthesis by tobacco LIM protein. Phytochemistry 57:1149–1157CrossRefPubMedGoogle Scholar
  46. Kim WC, Ko JH, Han KH (2012) Identification of a cis-acting regulatory motif recognized by MYB46, a master transcriptional regulator of secondary wall biosynthesis. Plant Mol Biol 78:489–501CrossRefPubMedGoogle Scholar
  47. Kim WC, Kim JY, Ko JH, Kang H, Han KH (2014) Identification of direct targets of transcription factor MYB46 provides insights into the transcriptional regulation of secondary wall biosynthesis. Plant Mol Biol 85:589–599CrossRefPubMedGoogle Scholar
  48. Ko JH, Kim WC, Han KH (2009) Ectopic expression of MYB46 identifies transcriptional regulatory genes involved in secondary wall biosynthesis in Arabidopsis. Plant J 60:649–665CrossRefPubMedGoogle Scholar
  49. Ko JH, Jeon HW, Kim WC, Kim JY, Han KH (2014) The MYB46/MYB83-mediated transcriptional regulatory programme is a gatekeeper of secondary wall biosynthesis. Ann Bot 114:1099–1107Google Scholar
  50. Krakowsky MD, Lee M, Coors JG (2005) Quantitative trait loci for cell-wall components in recombinant inbred lines of maize (Zea mays L.) 1: stalk tissue. Theor Appl Genet 111:337–346CrossRefPubMedGoogle Scholar
  51. Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, Fukuda H, Demura T (2005) Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 19:1855–1860CrossRefPubMedCentralPubMedGoogle Scholar
  52. Legay S, Sivadon P, Blervacq AS, Pavy N, Baghdady A, Tremblay L, Levasseur C, Ladouce N, Lapierre C, Séguin A, Hawkins S, Mackay J, Grima-Pettenati J (2010) EgMYB1, an R2R3 MYB transcription factor from Eucalyptus negatively regulates secondary cell wall formation in Arabidopsis and poplar. New Phytol 188:774–786CrossRefPubMedGoogle Scholar
  53. Li E, Wang S, Liu Y, Chen JG, Douglas CJ (2011) OVATE FAMILY PROTEIN4 (OFP4) interaction with KNAT7 regulates secondary cell wall formation in Arabidopsis thaliana. Plant J 67:328–341CrossRefPubMedGoogle Scholar
  54. Matthews J, Bhati M, Lehtomaki E, Mansfield R, Cubeddu L, MacKay J (2009) It takes two to tango: the structure and function of LIM, RING, PHD and MYND domains. Cur Pharm Des 15:3681–3696CrossRefGoogle Scholar
  55. Méchin V, Argillier O, Menanteau V, Barrière Y, Mila I, Pollet B, Lapierre C (2000) Relationship of cell wall composition to in vitro cell wall digestibility of maize inbred line stems. J Sci Food Agric 80:574–580CrossRefGoogle Scholar
  56. Méchin V, Argillier O, Hébert Y, Guingo E, Moreau L, Charcosset A, Barrière Y (2001) Genetic analysis and QTL mapping of cell wall digestibility and lignification in silage maize. Crop Sci 41:690–697CrossRefGoogle Scholar
  57. Meng H, Campbell WH (1998) Substrate profiles and expression of caffeoyl coenzyme A and caffeic acid O-methyltransferases in secondary xylem of aspen during seasonal development. Plant Mol Biol 38:513–520CrossRefPubMedGoogle Scholar
  58. Mitsuda N, Seki M, Shonozaki K, Ohme-Takagi M (2005) The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence. Plant Cell 17:2993–3006CrossRefPubMedCentralPubMedGoogle Scholar
  59. Mitsuda N, Iwase A, Yamamoto H, Yoshida M, Seki M, Shinozaki K, Ohme-Takagi M (2007) NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis. Plant Cell 19:270–280CrossRefPubMedCentralPubMedGoogle Scholar
  60. Molinari H, Pellny T, Freeman J, Shewry P, Mitchell R (2013) Grass cell wall feruloylation: distribution of bound ferulate and candidate gene expression in Brachypodium distachyon. Front Plant Sci 50:1–10Google Scholar
  61. Newman LJ, Perazza DE, Juda L, Campbell MM (2004) Involvement of the R2R3-MYB, AtMYB61, in the ectopic lignification and dark-photomorphogenic components of the det3 mutant phenotype. Plant J 37:239–250CrossRefPubMedGoogle Scholar
  62. Oda Y, Fukuda H (2014) Emerging roles of small GTPases in secondary cell wall development. Front Plant Sci 5:1–6CrossRefGoogle Scholar
  63. Ohman D, Demedts B, Kumar M, Gerber L, Gorzsás A, Goeminne G, Hedenström M, Ellis B, Boerjan W, Sundberg B (2013) MYB103 is required for FERULATE-5-HYDROXYLASE expression and syringyl lignin biosynthesis in Arabidopsis stems. Plant J 73:63–76CrossRefGoogle Scholar
  64. Park SH, Mei CS, Pauly M, Ong RG, Dale BE, Sabzikar R, Fotoh H, Nguyen T, Sticklen M (2013) Downregulation of maize cinnamoyl-coenzyme a reductase via RNA interference technology causes brown midrib and improves ammonia fiber expansion-pretreated conversion into fermentable sugars for biofuels. Crop Sci 52:2687–2701CrossRefGoogle Scholar
  65. Parker G, Schofield R, Sundberg B, Turner S (2003) Isolation of COV1, a gene involved in the regulation of vascular patterning in the stem of Arabidopsis. Development 130:2139–2148CrossRefPubMedGoogle Scholar
  66. Patzlaff A, McInnis S, Courtenay A, Surman C, Newman LJ, Smith C, Bevan MW, Mansfield S, Whetten RW, Sederoff RR, Campbell MM (2003) Characterisation of a pine MYB that regulates lignification. Plant J 36:743–754CrossRefPubMedGoogle Scholar
  67. Rengel D, San Clemente H, Servant F, Ladouce N, Paux E, Wincker P, Couloux A, Sivadon P, Grima-Pettenati J (2009) A new genomic resource dedicated to wood formation in Eucalyptus. BMC Plant Biol 9:36CrossRefPubMedCentralPubMedGoogle Scholar
  68. Riboulet C, Fabre F, Denoue D, Martinant JP, Lefevre B, Barrière Y (2007) QTL mapping and candidate gene research for lignin content and cell wall digestibility in a flint recombinant inbred line progeny harvested at silage stage. In Riboulet C (ed) Recherche des déterminants biochimiques et moléculaires de la réticulation des parois et de l’ingestibilité du maïs fourrage. PhD, Université de Poitiers, FranceGoogle Scholar
  69. Riboulet C, Fabre F, Dénoue D, Martinant JP, Lefevre B, Barrière Y (2008) QTL mapping and candidate gene research for lignin content and cell wall digestibility in a topcross of a flint recombinant inbred line progeny harvested at silage stage. Maydica 53:1–9Google Scholar
  70. Riboulet C, Guillaumie S, Méchin V, Bosio M, Pichon M, Goffner D, Lapierre C, Pollet B, Lefèvre B, Martinant JP, Barrière Y (2009) Kinetics of phenylpropanoid gene expression in maize growing internodes: relationships with cell wall deposition. Crop Sci 49:211–223CrossRefGoogle Scholar
  71. Roussel V, Gibelin C, Fontaine AS, Barrière Y (2002) Genetic analysis in recombinant inbred lines of early dent forage maize. II—QTL mapping for cell wall constituents and cell wall digestibility from per se value and top cross experiments. Maydica 47:9–20Google Scholar
  72. 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 70:818–830CrossRefPubMedGoogle Scholar
  73. Salazar MM, Nascimento LC, Camargo EL, Gonçalves DC, Neto JL, Marques WL, Teixeira PJ, Mieczkowski P, Mondego JM, Carazzolle MF, Deckmann AC, Pereira GA (2013) Xylem transcription profiles indicate potential metabolic responses for economically relevant characteristics of Eucalyptus species. BMC Genom 22(14):201CrossRefGoogle Scholar
  74. Salvi S, Sponza G, Morgante M, Tomes D, Niu X, Fengler KA, Meeley R, Ananiev EV, Svitashev S, Bruggemann E, Li B, Hainey CF, Radovic S, Zaina G, Rafalski JA, Tingey SV, Miao GH, Phillips RL, Tuberosa R (2007) Conserved noncoding genomic sequences associated with a flowering-time quantitative trait locus in maize. Proc Natl Acad Sci USA 104:11376–11381CrossRefPubMedCentralPubMedGoogle Scholar
  75. Saulnier L, Guillon F, Chateigner-Boutin AL (2012) Cell wall deposition and metabolism in wheat grain. J Cereal Sci 56:91–108CrossRefGoogle Scholar
  76. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, Minx P, Reily AD, Courtney L, Kruchowski SS, Tomlinson C, Strong C, Delehaunty K, Fronick C, Courtney B, Rock SM, Belter E, Du F, Kim K, Abbott RM, Cotton M, Levy A, Marchetto P, Ochoa K, Jackson SM, Gillam B, Chen W, Yan L, Higginbotham J, Cardenas M, Waligorski J, Applebaum E, Phelps L, Falcone J, Kanchi K, Thane T, Scimone A, Thane N, Henke J, Wang T, Ruppert J, Shah N, Rotter K, Hodges J, Ingenthron E, Cordes M, Kohlberg S, Sgro J, Delgado B, Mead K, Chinwalla A, Leonard S, Crouse K, Collura K, Kudrna D, Currie J, He R, Angelova A, Rajasekar S, Mueller T, Lomeli R, Scara G, Ko A, Delaney K, Wissotski M, Lopez G, Campos D, Braidotti M, Ashley E, Golser W, Kim H, Lee S, Lin J, Dujmic Z, Kim W, Talag J, Zuccolo A, Fan C, Sebastian A, Kramer M, Spiegel L, Nascimento L, Zutavern T, Miller B, Ambroise C, Muller S, Spooner W, Narechania A, Ren L, Wei S, Kumari S, Faga B, Levy MJ, McMahan L, Van Buren P, Vaughn MW, Ying K, Yeh C-T, Emrich SJ, Jia Y, Kalyanaraman A, Hsia A-P, Barbazuk WB, Baucom RS, Brutnell TP, Carpita NC, Chaparro C, Chia J-M, Deragon J-M, Estill JC, Fu Y, Jeddeloh JA, Han Y, Lee H, Li P, Lisch DR, Liu S, Liu Z, Nagel DH, McCann MC, SanMiguel P, Myers AM, Nettleton D, Nguyen J, Penning BW, Ponnala L, Schneider KL, Schwartz DC, Sharma A, Soderlund C, Springer NM, Sun Q, Wang H, Waterman M, Westerman R, Wolfgruber TK, Yang L, Yu Y, Zhang L, Zhou S, Zhu Q, Bennetzen JL, Dawe RK, Jiang J, Jiang N, Presting GG, Wessler SR, Aluru S, Martienssen RA, Clifton SW, McCombie WR, Wing RA, Wilson RK (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115CrossRefPubMedGoogle Scholar
  77. Shen H, He X, Poovaiah CR, Wuddineh WA, Ma J, Mann DG, Wang H, Jackson L, Tang Y, Stewart CN Jr, Chen F, Dixon RA (2012) Functional characterization of the switchgrass (Panicum virgatum) R2R3-MYB transcription factor PvMYB4 for improvement of lignocellulosic feedstocks. New Phytol 193:121–136CrossRefPubMedGoogle Scholar
  78. Shen H, Mazarei M, Hisano H, Escamilla-Treviño L, Fu C, Pu Y, Rudis MR, Tang Y, Xiao X, Jackson L, Li G, Hernandez T, Chen F, Ragauskas AJ, Stewart CN Jr, Wang ZY, Dixon RA (2013) A genomics approach to deciphering lignin biosynthesis in switchgrass. Plant Cell. 25:4342–4361CrossRefPubMedCentralPubMedGoogle Scholar
  79. Shigeto J, Kiyonaga Y, Fujita K, Kondo R, Tsutsumi Y (2013) Putative cationic cell-wall-bound peroxidase homologs in Arabidopsis, AtPrx2, AtPrx25 and AtPrx71, are involved in lignification. J Agric Food Chem 61:3781–3788CrossRefPubMedGoogle Scholar
  80. Soler M, Camargo EL, Carocha V, Cassan-Wang H, San Clemente H, Savelli B, Hefer CA, Paiva JA, Myburg AA, Grima-Pettenati J (2014) The Eucalyptus grandis R2R3-MYB transcription factor family: evidence for woody growth-related evolution and function. New Phytol. doi: 10.1111/nph.13039
  81. Sonbol FM, Fornalé S, Cappellades M, Encina A, Tourino S, Torres JL, Rovira P, Ruel K, Puigdomenech 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 70:283–296CrossRefPubMedGoogle Scholar
  82. Tamasloukht B, Lam MS-JWQ, Martinez Y, Tozo K, Barbier O, Jourda C, Jauneau A, Borderie G, Balzergue S, Renou JP, Huguet S, Martinant JP, Tatout C, Lapierre C, Barrière 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 62:3837–3848CrossRefPubMedCentralPubMedGoogle Scholar
  83. Tang HM, Liu S, Hill-Skinner S, Wu W, Reed D, Yeh CT, Nettleton D, Schnable PS (2014) The maize brown midrib2 (bm2) gene encodes a methylenetetrahydrofolate reductase that contributes to lignin accumulation. Plant J 77:380–392CrossRefPubMedCentralPubMedGoogle Scholar
  84. Torres AF, Noordam-Boot CMM, Dolstra O, Weijde T, Combes E, Dufour P, Vlaswinkel L, Visser RGF, Trindade LM (2014) Cell wall diversity in forage maize: genetic complexity and bioenergy potential. Bioenerg Res. doi: 10.1007/s12155-014-9507-8
  85. 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 341:1103–1106CrossRefPubMedGoogle Scholar
  86. Wang H, Avci U, Nakashima J, Hahn MG, Chen F, Dixon RA (2010) Mutation of WRKY transcription factors initiates pith secondary wall formation and increases stem biomass in dicotyledonous plants. Proc Natl Acad Sci USA 107:22338–22343CrossRefPubMedCentralPubMedGoogle Scholar
  87. Wang YH, Acharya A, Burrell AM, Klein RR, Klein PE, Hasenstein KH (2013) Mapping and candidate genes associated with saccharification yield in sorghum. Genome 56:659–665CrossRefPubMedGoogle Scholar
  88. Wissenbach M, Uberlacker B, Vogt F, Becker D, Salamini F, Rohde W (1993) MYB genes from Hordeum vulgare—tissue-specific expression of chimeric MYB Promoter/Gus genes in transgenic tobacco. Plant J 4:411–422CrossRefPubMedGoogle Scholar
  89. Xu B, Escamilla-Treviño LL, Sathitsuksanoh N, Shen Z, Shen H, Zhang YH, 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
  90. Xu W, Grain D, Bobet S, Le Gourrierec J, Thévenin J, Kelemen Z, Lepiniec L, Dubos C (2014) Complexity and robustness of the flavonoid transcriptional regulatory network revealed by comprehensive analyses of MYB–bHLH–WDR complexes and their targets in Arabidopsis seed. New Phytol 202:132–144CrossRefPubMedGoogle Scholar
  91. 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 55:652–664CrossRefPubMedGoogle Scholar
  92. Yamaguchi M, Ohtani M, Mitsuda N, Kubo M, Ohme-Takagi M, Fukuda H, Demura T (2010) VND-INTERACTING2, a NAC domain transcription factor, negatively regulates xylem vessel formation in Arabidopsis. Plant Cell 22:1249–1263CrossRefPubMedCentralPubMedGoogle Scholar
  93. 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 66:579–590CrossRefPubMedGoogle Scholar
  94. Zhao K, Bartley LE (2014) Comparative genomic analysis of the R2R3 MYB secondary cell wall regulators of Arabidopsis, poplar, rice, maize, and switchgrass. BMC Plant Biol 14:135CrossRefPubMedCentralPubMedGoogle Scholar
  95. Zhao Q, Nakashima J, Chen F, Yin Y, Fu C, Yun J, Shao H, Wang X, Wang ZY, Dixon RA (2013) Laccase is necessary and nonredundant with peroxidase for lignin polymerization during vascular development in Arabidopsis. Plant Cell 25:3976–3987CrossRefPubMedCentralPubMedGoogle Scholar
  96. Zhong R, Ye ZH (2009) Transcriptional regulation of lignin biosynthesis. Plant Signal Behav 4:1–7CrossRefGoogle Scholar
  97. Zhong R, Ye ZH (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 53:368–380CrossRefPubMedGoogle Scholar
  98. Zhong R, Richardson EA, Ye ZH (2007) The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. Plant Cell 19:2776–2792CrossRefPubMedCentralPubMedGoogle Scholar
  99. Zhong R, Lee C, Zhou J, McCarthy RL, Ye ZH (2008) A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell 20:2763–2782CrossRefPubMedCentralPubMedGoogle Scholar
  100. Zhong R, Lee C, Ye ZH (2010) Global analysis of direct targets of secondary wall NAC master switches in Arabidopsis. Mol Plant 3:1087–1103CrossRefPubMedGoogle Scholar
  101. Zhong R, Lee C, McCarthy RL, Reeves CK, Jones EG, Ye ZH (2011) Transcriptional activation of secondary wall biosynthesis by rice and maize NAC and MYB transcription factors. Plant Cell Physiol 52:1856–1871CrossRefPubMedGoogle Scholar
  102. Zhong R, McCarthy RL, Haghighat M, Ye ZH (2013) The poplar MYB master switches bind to the SMRE site and activate the secondary wall biosynthetic program during wood formation. PLoS ONE 8(7):e69219CrossRefPubMedCentralPubMedGoogle Scholar
  103. Zhou J, Lee C, Zhong RQ, Ye ZH (2009) MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. Plant Cell 21:248–266CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Yves Barrière
    • 1
    Email author
  • Audrey Courtial
    • 2
    • 3
  • Marçal Soler
    • 2
  • Jacqueline Grima-Pettenati
    • 2
  1. 1.Unité de Génétique et d’Amélioration des Plantes FourragèresINRALusignanFrance
  2. 2.LRSV, Laboratoire de Recherche en Sciences Végétales, UMR5546Université Toulouse III/CNRSAuzeville, Castanet-TolosanFrance
  3. 3.Centre National de Ressources Génomiques VégétalesINRACastanet-TolosanFrance

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