Advertisement

pp 1-38 | Cite as

Biosynthesis and Regulation of Secondary Cell Wall

  • Ignacio ZarraEmail author
  • Gloria Revilla
  • Javier Sampedro
  • Elene R. Valdivia
Chapter
Part of the Progress in Botany book series

Abstract

Secondary plant cell walls are produced by specialized plant cell types required for mechanical support and water transport. They are a microfibril-based composite constituted by celluloses, hemicelluloses, and lignins. Cellulose microfibrils are associated with hemicelluloses leading to the formation of a polysaccharide network that is impregnated by lignin. They are thick and un-extensible, unlike primary walls. The formation of secondary cell walls involves a series of overlapping events as changes in the biosynthetic machinery of their components: microtubule reorganization, formation of cellulose synthase complexes that synthesize cellulose microfibrils with different characteristics, a shift from pectin to secondary wall hemicelluloses involving xylans or mannans with different side-chain decoration, and synthesis of monolignols and polymerization for lignin production. All the abovementioned processes require a precise regulation not only of each event on its own but also to achieve the integration and coordination of the whole. The main actors in the current model of secondary wall regulation are the transcription factors that act as master switches. They are organized in a hierarchical way where NAC transcription factors are at the top of the network and MYB and others are downstream in the signaling cascade.

References

  1. Achnine L, Blancaflor EB, Rasmussen S, Dixon RA (2004) Colocalization of L-phenylalanine ammonia-lyase and cinnamate 4-hydroxylase for metabolic channeling in phenylpropanoid biosynthesis. Plant Cell 16:3098–3109Google Scholar
  2. Albersheim P, Darvill A, Roberts K, Sederoff R, Staehelin A (2011) Plant cell walls: from chemistry to biology. Garland Science, Taylor & Francis Group, New YorkGoogle Scholar
  3. 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 22:1207–1212Google Scholar
  4. Anders N, Wilkinson MD, Lovegrove A, Freeman J, Tryfona T, Pellny TK, Weimar T, Mortimer JC, Stott K, Baker JM, Defoin-Platel M, Shewry PR, Dupree P, Mitchell RAC (2012) Glycosyl transferases in family 61 mediate arabinofuranosyl transfer onto xylan in grasses. Proc Natl Acad Sci U S A 109:989–993Google Scholar
  5. Arioli T, Peng L, Betzner AS, Burn J, Wittke W, Herth W, Camilleri C, Hofte H, Plazinski J, Birch R, Cork A, Glover J, Redmond J, Williamson RE (1998) Molecular analysis of cellulose biosynthesis in Arabidopsis. Science 279:717–720Google Scholar
  6. Barnes WJ, Anderson CT (2018) Cytosolic invertases contribute to cellulose biosynthesis and influence carbon partitioning in seedlings of Arabidopsis thaliana. Plant J 94:956–974Google Scholar
  7. Barros J, Serk H, Granlund I, Pesquet E (2015) The cell biology of lignification in higher plants. Ann Bot 115:1053–1074Google Scholar
  8. 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.  https://doi.org/10.1038/nplants.2016.50CrossRefGoogle Scholar
  9. Bashline L, Li S, Gu Y (2014) The trafficking of the cellulose synthase complex in higher plants. Ann Bot 114:1059–1067Google Scholar
  10. Bassard JE, Richert L, Geerinck J, Renault H, Duval F, Ullmann P, Schmitt M, Meyer E, Mutterer J, Boerjan W, De Jaeger G, Mely Y, Goossens A, Werck-Reichhart D (2012) Protein-protein and protein-membrane associations in the lignin pathway. Plant Cell 24:4465–4482Google Scholar
  11. Bennett T, van den Toorn A, Sanchez-Perez GF, Campilho A, Willemsen V, Snel B, Scheres B (2010) SOMBRERO, BEARSKIN1, and BEARSKIN2 regulate root cap maturation in Arabidopsis. Plant Cell 22:640–654Google Scholar
  12. Berthet S, Demont-Caulte 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 23:1124–1137Google Scholar
  13. Bhargava A, Mansfield SD, Hall HC, Douglas CJ, Ellis BE (2010) MYB75 functions in regulation of secondary cell wall formation in the Arabidopsis inflorescence stem. Plant Physiol 154:1428–1438Google Scholar
  14. Bischoff V, Selbig J, Scheible W (2010) Involvement of TBL/DUF231 proteins into cell wall biology. Plant Signal Behav 5:1057–1059Google Scholar
  15. Blee KA, Choi JW, O’Connell AP, Schuch W, Lewis NG, Bolwell P (2003) A lignin-specific peroxidase in tobacco whose antisense suppression leads to vascular tissue modification. Phytochemistry 64:163–176Google Scholar
  16. Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Physiol 54:519–546Google Scholar
  17. Boija E, Lundquist A, Edwards K, Johansson G (2007) Evaluation of bilayer disks as plant membrane models in partition studies. Anal Biochem 364:145–152Google Scholar
  18. Bomal C, Bedon F, Caron S, Mansfield SD, Levasseur C, Cooke JEK, Blais S, Tremblay L, Morency MJ, 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 59:3925–3939Google Scholar
  19. Bonawitz ND, Chapple C (2010) The genetics of lignin biosynthesis: connecting genotype to phenotype. Annu Rev Genet 44:337–363Google Scholar
  20. Borah P, Kurana JP (2018) The OsFBK1 E3 ligase subunit affects anther and root secondary cell wall thickenings by mediating turnover of a cinnamoyl-CoA reductase. Plant Physiol 176:2148–2165Google Scholar
  21. Brett C (2000) Cellulose microfibrils in plants: biosynthesis, deposition, and integration into the cell wall. Int Rev Cytol 199:161–199Google Scholar
  22. Bromley JR, Busse-Wicher M, Tryfona T, Mortimer JC, Zhang Z, Brown DM, Dupree P (2013) GUX1 and GUX2 glucuronyltransferases decorate distinct domains of glucuronoxylan with different substitution patterns. Plant J 74:423–434Google Scholar
  23. Brown DM, Zeef LAH, Ellis J, Goodacre R, Turner SR (2005) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17:2281–2295Google Scholar
  24. Brown DM, Goubet F, Wong VW, Goodacre R, Stephens E, Dupree P, Turner SR (2007) Comparison of five xylan synthesis mutants reveals new insight into the mechanisms of xylan synthesis. Plant J 52:1154–1168Google Scholar
  25. Busse-Wicher M, Gomes TCF, Tryfona T, Nikolovski N, Stott K, Grantham NJ, Bolam DN, Skaf MS, Dupree P (2014) The pattern of xylan acetylation suggests xylan may interact with cellulose microfibrils as a twofold helical screw in the secondary plant cell wall of Arabidopsis thaliana. Plant J 79:492–506Google Scholar
  26. Capek P, Kubačková M, Alföldi J, Bilisics L, Lišková D, Kákoniová D (2000) Galactoglucomannan from the secondary cell wall of Picea abies L. Karst. Carbohydr Res 329:635–645Google Scholar
  27. 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 4:189Google Scholar
  28. 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 lac 17 mutant. J Exp Bot 64:1769–1781Google Scholar
  29. Chai M, Bellizzi M, Wan C, Cui Z, Li Y, Wang GL (2015) The NAC transcription factor OsSWN1 regulates secondary cell wall development in Oryza sativa. J Plant Biol 58:44–51Google Scholar
  30. Chen HC, Li Q, Shuford CM, Liu J, Muddiman DC, Sederoff RR, Chiang VL (2011) Membrane protein complexes catalyze both 4- and 3-hydroxylation of cinnamic acid derivatives in monolignol biosynthesis. Proc Natl Acad Sci U S A 108:21253–21258Google Scholar
  31. Chen F, Tobimatsu Y, Havkin-Frenkel D, Dixon RA, Ralph J (2012) A polymer of caffeyl alcohol in plant seeds. Proc Natl Acad Sci U S A 109:1772–1777Google Scholar
  32. Chen F, Tobimatsu Y, Jackson L, Nakashima J, Ralph J, Dixon RA (2013) Novel seed coat lignins in the Cactaceae: structure, distribution and implications for the evolution of lignin diversity. Plant J 73:201–211Google Scholar
  33. Chen HC, Song J, Wang JP, Lin YC, Ducoste J, Shuford CM, Liu J, Li Q, Shi R, Nepomuceno A, Isik F, Muddiman DC, Williams C, Sederoff RR, Chiang VL (2014) Systems biology of lignin biosynthesis in Populus trichocarpa: heteromeric 4-coumaric acid:coenzyme A ligase protein complex formation, regulation, and numerical modeling. Plant Cell 26:876–893Google Scholar
  34. Cheng X, Su X, Muhammad A, Li M, Zhang J, Sun Y, Li G, Jin Q, Cai Y, Lin Y (2018) Molecular characterization, evolution, and expression profiling of the Dirigent (DIR) family genes in Chinese white pear (Pyrus bretschneideri). Front Genet 9.  https://doi.org/10.3389/fgene.2018.00136
  35. Chezem WR, Memon A, Li FS, Weng JK, Clay NK (2017) SG2-Type R2R3-MYB transcription factor MYB15 controls defense-induced lignification and basal immunity in Arabidopsis. Plant Cell 29:1907–1926Google Scholar
  36. Chiniquy D, Sharma V, Schultink A, Baidoo EE, Rautengarten C, Cheng K, Carroll A, Ulvskov P, Harholt J, Keasling JD, Pauly M, Scheller HV, Ronald PC (2012) XAX1 from glycosyltransferase family 61 mediates xylosyltransfer to rice xylan. Proc Natl Acad Sci U S A 109:17117–11122Google Scholar
  37. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861Google Scholar
  38. Cosgrove D, Jarvis M (2012) Comparative structure and biomechanics of plant primary and secondary cell walls. Front Plant Sci 3:204Google Scholar
  39. Davin LB, Lewis NG (2000) Dirigent proteins and dirigent sites explain the mystery of specificity of radical precursor coupling in lignin and lignin biosynthesis. Plant Physiol 123:453–461Google Scholar
  40. Delmer DP (1999) Cellulose biosynthesis: exciting times for a difficult field of study. Annu Rev Plant Physiol Plant Mol Biol 50:245–276Google Scholar
  41. Dhugga KS, Barreiro R, Whitten B, Stecca K, Hazebroek J, Randhawa GS, Dolan M, Kinney AJ, Tomes D, Nichols S, Anderson P (2004) Guar seed β-mannan synthase is a member of the cellulose synthase super gene family. Science 303:363–366Google Scholar
  42. Didi V, Jackson P, Hejátko J (2015) Hormonal regulation of secondary cell wall formation. J Exp Bot 66:5015–5027Google Scholar
  43. 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 27:695–710Google Scholar
  44. Du J, Mansfield SD, Shawn D, Groover AT (2009) The Populus homeobox gene ARBORKNOX2 regulates cell differentiation during secondary growth. Plant J 60:1000–1014Google Scholar
  45. Du J, Miura E, Robischon M, Martinez C, Groover A (2011) The Populus class III HD ZIP transcription factor POPCORONA affects cell differentiation during secondary growth of woody stems. PLoS One 6:e17458Google Scholar
  46. Edwards ME, Dickson CA, Chengappa S, Sidebottom C, Gidley MJ, Reid JSG (1999) Molecular characterisation of a membrane-bound galactosyltransferase of plant cell wall matrix polysaccharide biosynthesis. Plant J 19:691–697Google Scholar
  47. Endo H, Yamaguchi M, Tamura T, Nakano Y, Nishikubo N, Yoneda A, Kato K, Kubo M, Kajita S, Katayama Y, Ohtani M, Demura T (2015) Multiple classes of transcription factors regulate the expression of VASCULAR-RELATED NAC-DOMAIN7, a master switch of xylem vessel differentiation. Plant Cell Physiol 56:242–254Google Scholar
  48. Fernández-Pérez F, Pomar F, Pedreño MA, Novo-Uzal E (2015) Supression of Arabidopsis peroxidase 72 alters cell wall and phenylpropanoid metabolism. Plant Sci 239:192–199Google Scholar
  49. Fornalé S, Lopez E, Salazar-Henao JE, Fernández-Nohales P, Rigau J, Caparros-Ruiz D (2014) AtMYB7, a new player in the regulation of UV-sunscreens in Arabidopsis thaliana. Plant Cell Physiol 55:507–516Google Scholar
  50. Gallego-Giraldo L, Shadle G, Shen H, Barros-Rios J, Fresquet Corrales S, Wang H, Dixon RA (2015) Combining enhanced biomass density with reduced lignin level for improved forage quality. Plant Biotechnol J 14:895–904Google Scholar
  51. Gerber L, Zhang B, Roach M, Rende U, Gorzsás A, Kumar M, Burgert I, Niittylä T, Sundberg B (2014) Deficient sucrose synthase activity in developing wood does not specifically affect cellulose biosynthesis, but causes an overall decrease in cell wall polymers. New Phytol 203:1220–1230Google Scholar
  52. Gille S, Pauly M (2012) O-Acetylation of plant cell wall polysaccharides. Front Plant Sci 3:12Google Scholar
  53. 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 43:553–567Google Scholar
  54. Gou M, Ran X, Martin DW, Liu C-J (2018) The scaffold proteins of lignin biosynthetic cytochrome P450 enzymes. Nat Plants 4:299–310Google Scholar
  55. Ha CM, Escamilla-Treviño L, Yarce JCS, Kim H, Ralph J, Chen F, Dixon RA (2016) An essential role of caffeoyl shikimate esterase in monolignol biosynthesis on Medicago truncatula. Plant J 86:363–375Google Scholar
  56. Haigler CH, Ivanova-Datcheva M, Hogan PS, Salnikov VV, Hwang S, Martin K, Delmer DP (2001) Carbon partitioning to cellulose synthesis. Plant Mol Biol 47:29–51Google Scholar
  57. Handakumbura PP, Brow K, Whitney IP, Zhao K, Sanguinet KA, Lee SJ, Olins J, Romero-Gamboa SP, Harrington MJ, Bascom CJ, MacKinnon KJ, Veling MT, Liu L, Lee JE, Vogel JP, O’Malley RC, Bezanilla M, Bartley LE, Hazen SP (2018) SECONDARY WALL ASSOCIATED MYB1 is a positive regulator of secondary cell wall thickening in Brachypodium distachyon and is not found in the Brassicaceae. Plant J 96:532–545Google Scholar
  58. Harris D, DeBolt S (2010) Synthesis, regulation and utilization of lignocellulosic biomass. Plant Biotechnol J 8:244–262Google Scholar
  59. 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 237:1599–1612Google Scholar
  60. Higuchi T, Ito Y, Kawamura I (1967) p-Hydroxyphenylpropane component of grass lignin and role of tyrosine-ammonia lyase in its formation. Phytochemistry 6:875–881Google Scholar
  61. Hill JL, Hammudi MB, Tien M (2014) The Arabidopsis cellulose synthase complex: a proposed hexamer of CESA trimers in an equimolar stoichiometry. Plant Cell 26:4834–4842Google Scholar
  62. Hirano K, Kondo M, Aya K, Miyao A, Sato Y, Antonio BA, Namiki N, Nagamura Y, Matsuoka M (2013) Identification of transcription factors involved in rice secondary cell wall formation. Plant Cell Physiol 54:1791–1802Google Scholar
  63. Hosmani PS, Kamiya T, Danku J, Naseer S, Geldner N, Guerinot ML, Salt DE (2013) Dirigent domain-containing protein is part of the machinery required for formation of the lignin-based Casparian strip in the root. Proc Natl Acad Sci U S A 110:14498–14503Google Scholar
  64. Huang D, Wang S, Zhang B, Shang-Guan K, Shi Y, Zhang D, Liu X, Wu K, Xu Z, Fu X, Zhou Y (2015) A Gibberellin-mediated DELLA-NAC signaling cascade regulates cellulose synthesis in rice. Plant Cell 27:1681–1696Google Scholar
  65. Hussey SG, Mizrachi E, Spokevicius AV, Bossinger G, Berger DK, Myburg AA (2011) SND2, a NAC transcription factor gene, regulates genes involved in secondary cell wall development in Arabidopsis fibres and increases fibre cell area in Eucalyptus. BMC Plant Biol 11:173Google Scholar
  66. Iwata T, Indrarti L, Azuma J (1998) Affinity of hemicellulose for cellulose produced by Acetobacter xylinum. Cellulose 5:215–228Google Scholar
  67. Jarvis MC (2018) Structure of native cellulose microfibrils, the starting point for nanocellulose manufacture. Philos Transact A Math Phys Eng Sci 376.  https://doi.org/10.1098/rsta.2017.0045
  68. Jin H, Cominelli E, Bailey P, Parr A, Mehrtens F, Jones J, Tonelli C, Weisshaar B, Martin C (2000) Transcriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis. EMBO J 19:6150–6161Google Scholar
  69. Karlen SD, Smith RA, Kim H, Padmakshan D, Bartuce A, Mobley JK, Free HCA, Smith BG, Harris PJ, Ralph J (2017) Highly decorated lignins in leaf tissues of the canary island date palm Phoenix canariensis. Plant Physiol 175:1058–1067Google Scholar
  70. Karlen SD, Free HCA, Padmakshan D, Smith BG, Ralph J, Harris PJ (2018) Commelinid monocotyledon lignins are acylated by p-coumarate. Plant Physiol 177:513–521Google Scholar
  71. Kataoka Y, Kondo T (1998) FT-IR microscopic analysis of changing cellulose crystalline structure during wood cell wall formation. Macromolecules 31:760–764Google Scholar
  72. Kawabe H, Ohtani M, Kurata T, Sakamoto T, Demura T (2018) Protein S-nitrosylation regulates xylem vessel cell differentiation in Arabidopsis. Plant Cell Physiol 59:17–29Google Scholar
  73. Kim WC, Ko JH, Kim JY, Kim J, Bae HJ, Han KH (2012) MYB46 directly regulates the gene expression of secondary wall-associated cellulose synthases in Arabidopsis. Plant J 73:26–36Google Scholar
  74. Kim WC, Kim JY, Ko JH, Kim J, Han KH (2013) Transcription factor MYB46 is an obligate component of the transcriptional regulatory complex for functional expression of secondary wall-associated cellulose synthases in Arabidopsis thaliana. J Plant Physiol 170:1374–1378Google Scholar
  75. 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 85:589–599Google Scholar
  76. Ko J-H, Kim W-C, Han K-H (2009) Ectopic expression of MYB46 identifies transcriptional regulatory genes involved in secondary wall biosynthesis in Arabidopsis. Plant J 60:649–665Google Scholar
  77. 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 19:1855–1860Google Scholar
  78. Kumar M, Turner S (2015) Plant cellulose synthesis: CESA proteins crossing kingdoms. Phytochemistry 112:91–99Google Scholar
  79. Kumar M, Campbell L, Turner S (2016) Secondary cell walls: biosynthesis and manipulation. J Exp Bot 67:515–531Google Scholar
  80. Lan W, Rencoret J, Lu F, Karlen SD, Smith BG, Harris PJ, del Río JC, Ralph J (2016) Tricin-lignins: occurrence and quantitation of tricin in relation to phylogeny. Plant J 88:1046–1057Google Scholar
  81. Le Roy J, Huss B, Créach A, Huss B, Hawkins S, Neutelings G (2016) Glycosylation is a major regulator of phenylpropanoid availability and biological activity in plants. Front Plant Sci 7:735Google Scholar
  82. Lee C, Teng Q, Zhong R, Yuan Y, Haghighat M, Ye ZH (2012) Tree Arabidopsis DUF579 domain-containing GXM proteins are methyltransferases catalyzing 4-O-methylation of glucuronic acid on xylan. Plant Cell Physiol 53:1934–1949Google Scholar
  83. Lee Y, Rubio MC, Alassimone J, Geldner N (2013) A mechanism for localized lignin deposition in the endodermis. Cell 153:402–412Google Scholar
  84. Lee C, Teng Q, Zhong R, Ye Z (2014) Alterations of the degree of xylan acetylation in Arabidopsis xylan mutants. Plant Signal Behav 9:e27797Google Scholar
  85. 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 188:774–786Google Scholar
  86. Li Y, Kajita S, Kawai S (2003) Down-regulation of an anionic peroxidase in transgenic aspen and its effect on lignin characteristics. J Plant Res 116:175–182Google Scholar
  87. 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 67:328–341Google Scholar
  88. Li S, Lei L, Somerville CR, Gu Y (2012a) Cellulose synthase interactive protein 1 (CSL1) links microtubules and cellulose synthase complexes. Proc Natl Acad Sci U S A 109:185–190Google Scholar
  89. Li E, Bhargava A, Qiang W, Friedmann MC, Forneris N, Savidge RA, Johnson LA, Mansfield SD, Ellis BE, Douglas CJ (2012b) The Class II KNOX gene KNAT7 negatively regulates secondary wall formation in Arabidopsis and is functionally conserved in Populus. New Phytol 194:102–115Google Scholar
  90. Liang M, Davis E, Gardner D, Cai X, Wu Y (2006) Involvement of AtLAC15 in lignin synthesis is seeds and in root elongation of Arabidopsis. Planta 224:1185–1196Google Scholar
  91. Liepman AH, Wilkerson CG, Keegstra K (2005) Expression of cellulose synthase-like (Csl) genes in insect cells reveals that CslA family members encode mannan synthases. Proc Natl Acad Sci U S A 102:2221–2228Google Scholar
  92. Liu L, Shang-Guan K, Zhang B, Liu X, Yan M, Zhang L, Shi Y, Zhang M, Qian Q, Li J, Zhou Y (2013) Brittle Culm1, a COBRA-Like Protein, functions in cellulose assembly through binding cellulose microfibrils. PLoS Genet 9:e1003704Google Scholar
  93. Liu Y, You S, Taylor-Teeples M, Li WL, Schuetz M, Brady SM, Douglas CJ (2014) BEL1-LIKE HOMEODOMAIN6 and KNOTTED ARABIDOPSIS THALIANA7 interact and regulate secondary cell wall formation via repression of REVOLUTA. Plant Cell 26:4843–4861Google Scholar
  94. Liu Q, Luo L, Zheng L (2018) Lignins: biosynthesis and biological functions in plants. Int J Mol Sci 19:335.  https://doi.org/10.3390/ijms19020335CrossRefGoogle Scholar
  95. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D495Google Scholar
  96. Lu S, Li Q, Wei H, Chang MJ, Tunlaya-Anukit S, Kim H, Liu J, Song J, Sun YH, Yuan L, Yeh TF, Peszlen I, Ralph J, Sederoff RR, Chiang VL (2013) Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa. Proc Natl Acad Sci U S A 110:10848–10853Google Scholar
  97. Lundqvist J, Teleman A, Junel L, Zacchi G, Dahlman O, Tjerneld F, Stålbrand H (2002) Isolation and characterization of galactoglucomannan from spruce (Picea abies). Carbohydr Polym 48:29–39Google Scholar
  98. MacMillan CP, Birke H, Chuah A, Brill E, Tsuji Y, Ralph J, Dennis ES, Llewellyn D, Pettolino FA (2017) Tissue and cell-specific transcriptomes in cotton reveal the subtleties of gene regulation underlying the diversity of plant secondary cell walls. BMC Genomics 18:539Google Scholar
  99. Manabe Y, Nafisi M, Verhertbruggen Y, Orfila C, Gille S, Rautengarten C, Cherk C, Marcus SE, Somerville S, Pauly M, Knox JP, Sakuragi Y, Scheller HV (2011) Loss-of-function mutation of REDUCED WALL ACETYLATION2 in Arabidopsis leads to reduced cell wall acetylation and increased resistance to Botrytis cinerea. Plant Physiol 155:1068–1078Google Scholar
  100. Martínez-Abad A, Berglund J, Toriz G, Gatenholm P, Henriksson G, Lindström M, Wohlert J, Vilaplana F (2017) Regular motifs in xylan modulate molecular flexibility and interactions with cellulose surfaces. Plant Physiol 175:1579–1592Google Scholar
  101. McCarthy RL, Zhong R, Ye ZH (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 50:1950–1964Google Scholar
  102. McFarlane HE, Döring A, Persson S (2014) The cell biology of cellulose synthesis. Annu Rev Plant Biol 65:69–94Google Scholar
  103. Meents M, Watanabe Y, Samuels AL (2018) The cell biology of secondary cell wall biosynthesis. Ann Bot 121:1107–1125Google Scholar
  104. Mele G, Ori N, Sato Y, Hake S (2003) The knotted1-like homeobox gene BREVIPEDICELLUS regulates cell differentiation by modulating metabolic pathways. Genes Dev 17:2088–2093Google Scholar
  105. Mendu V, Griffiths JS, Persson S, Stork J, Downie AB, Voiniciuc C, Haughn GW, Debolt S (2011) Subfunctionalization of cellulose synthases in seed coat epidermal cells mediates secondary radial wall synthesis and mucilage attachment. Plant Physiol 157:441–453Google Scholar
  106. Miao YC, Liu CJ (2010) ATP-binding cassette-like transporters are involved in the transport of lignin precursors across plasma and vacuolar membranes. Proc Natl Acad Sci U S A 107:22728–22733Google Scholar
  107. Mitsuda N, Seki M, Shinozaki 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 17:2993–3006Google Scholar
  108. 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 19:270–280Google Scholar
  109. Molhoj M, Johansen B, Ulvskov P, Borkhardt B (2001) Expression of a membrane-anchored endo-1,4-beta-glucanase from Brassica napus, orthologous to KOR from Arabidopsis thaliana, is inversely correlated to elongation in light-grown plants. Plant Mol Biol 45:93–105Google Scholar
  110. Moreira LRS, Filho EXF (2008) An overview of mannan structure and mannan-degrading enzyme systems. Appl Microbiol Biotechnol 79:165–178Google Scholar
  111. Nakano Y, Yamaguchi M, Endo H, Rejab NA, Ohtani M (2015) NAC-MYB-based transcriptional regulation of secondary cell wall biosynthesis in land plants. Front Plant Sci 6:288Google Scholar
  112. Negi S, Tak H, Ganapathi TR (2015) Cloning and functional characterization of MusaVND1 using transgenic banana plants. Transgenic Res 24:571–585Google Scholar
  113. Negi S, Tak H, Ganapathi TR (2016) Functional characterization of secondary wall deposition regulating transcription factors MusaVND2 and MusaVND3 in transgenic banana plants. Protoplasma 253:431–446Google Scholar
  114. Negi S, Tak H, Ganapathi TR (2017) Native vascular related NAC transcription factors are efficient regulator of multiple classes of secondary wall associated genes in banana. Plant Sci 265:70–86Google Scholar
  115. Newman L, 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 37:239–250Google Scholar
  116. Newman RH, Hill SJ, Harris PJ (2013) Wide-angle x-ray scattering and solid-state nuclear magnetic resonance data combined to test models for cellulose microfibrils in mung bean cell walls. Plant Physiol 163:1558–1567Google Scholar
  117. Nicol F, His I, Jauneau A, Vernhettes S, Canut H, Höfte H (1998) A plasma membrane-bound putative endo-1,4-β-d-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. EMBO J 17:5563–5576Google Scholar
  118. 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 242:589–600Google Scholar
  119. Ohashi-Ito K, Oda Y, Fukuda H (2010) Arabidopsis VASCULAR-RELATED NAC-DOMAIN6 directly regulates the genes that govern programmed cell death and secondary wall formation during xylem differentiation. Plant Cell 22:3461–3473Google Scholar
  120. Ohashi-Ito K, Iwamoto K, Fukuda H (2018) LOB DOMAIN-CONTAINING PROTEIN 15 positively regulates expression of VND7, a master regulator of tracheary elements. Plant Cell Physiol 59:989–996Google Scholar
  121. Öhman D, Demedts B, Kumar M, Gerber L, Gorzsás A, Goeminne G, Hedenström M, Ellis B, Boerjan W, Sundberg B (2012) MYB103 is required for FERULATE-5-HYDROXYLASE expression and syringyl lignin biosynthesis in Arabidopsis stems. Plant J 73:63–76Google Scholar
  122. Ohtani M, Nishikubo N, Xu B, Yamaguchi M, Mitsuda N, Goué N, Shi F, Ohme-Takagi M, Demura T (2011) A NAC domain protein family contributing to the regulation of wood formation in poplar. Plant J 67:499–512Google Scholar
  123. Paredez AR, Somerville CR, Ehrhardt DW (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312:1491–1495Google Scholar
  124. Pascual MB, Llebrés MT, Craven-Bartle B, Cañas RA, Cánovas FM, Ávila C (2017) PpNAC1, a main regulator of phenylalanine biosynthesis and utilization in maritime pine. Plant Biotechnol J 16:1094–1104Google Scholar
  125. 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 36:743–754Google Scholar
  126. Pawar PM, Ratke C, Balasubramanian VK, Chong S, Gandla ML, Adriasola M, Sparrman T, Hedenström M, Szwaj K, Derba-Maceluch M, Gaertner C, Mouille G, Ezcurra I, Tenkanen M, Jönsson LJ, Mellerowicz EJ (2017) Downregulation of RWA genes in hybrid aspen affects xylan acetylation and wood saccharification. New Phytol 214:1491–1505Google Scholar
  127. Pear JR, Kawagoe Y, Schreckengost WE, Delmer DP, Stalker DM (1996) Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase. Proc Natl Acad Sci U S A 93:12637–12642Google Scholar
  128. Pedreira J, Herrera MT, Zarra I, Revilla G (2011) The overexpression of AtPrx37, an apoplastic peroxidase, reduces growth in Arabidopsis. Physiol Plant 141:177–187Google Scholar
  129. Peña MJ, Zhong R, Zhou GK, Richardson EA, O’Neill MA, Darvill AG, York WS, Ye ZH (2007) Arabidopsis irregular xylem8 and irregular xylem9: implications for the complexity of glucuronoxylan biosynthesis. Plant Cell 19:549–563Google Scholar
  130. Peña MJ, Kulkarni AR, Backe J, Boyd M, O’Neill MA, York W (2016) Structural diversity of xylans in the cell walls of monocots. Planta 244:589–606Google Scholar
  131. Perkins M, Smith RA, Samuels L (2019) The transport of monomers during lignification in plants: anything goes to how? Curr Opin Biotechnol 56:69–74Google Scholar
  132. Purushotham P, Cho SH, Díaz-Moreno SM, Kumar M, Nixon BT, Bulone V, Zimmer J (2016) A single heterologously expressed plant cellulose synthase isoform is sufficient for cellulose microfibril formation in vitro. Proc Natl Acad Sci U S A 113:11360–11365Google Scholar
  133. Raes J, Rohde A, Christensen JH, van der Peer Y, Boerjan W (2003) Genome-wide characterization of the lignification toolbox in Arabidopsis. Plant Physiol 133:1051–1071Google Scholar
  134. 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-hydroxyphenylpropanoids. Phytochem Rev 3:29–60Google Scholar
  135. Rao X, Dixon RA (2018) Current models for transcriptional regulation of secondary cell wall biosynthesis in grasses. Front Plant Sci 9:399.  https://doi.org/10.3389/fpls.2018.00399CrossRefGoogle Scholar
  136. Ratke C, Terebieniec BK, Winestrand S, Debra-Maceluch M, Grahn T, Schiffthaler B, Ulvcrona T, Özparpucu M, Rüggeberg M, Lundqvist SO, Street NR, Jönsson LJ, Mellerowicz EJ (2018) Downregulating aspen xylan biosynthetic GT43 genes in developing wood stimulates growth via reprograming of the transcriptome. New Phytol 219:230–245Google Scholar
  137. Rennie EA, Scheller HV (2014) Xylan biosynthesis. Curr Opin Biotechnol 26:100–107Google Scholar
  138. Rogers LA, Dubos C, Cullis IF, Surman C, Poole M, Willment J, Mansfield SD, Campbell MM (2005) Light, the circadian clock, and sugar perception in the control of lignin biosynthesis. J Exp Bot 56:1651–1663Google Scholar
  139. Ruel K, Nishiyama Y, Joseleau J (2012) Crystalline and amorphous cellulose in the secondary walls of Arabidopsis. Plant Sci 193–194:48–61Google Scholar
  140. Sakamoto S, Takata N, Oshima Y, Yoshida K, Taniguchi T, Mitsuda N (2016) Wood reinforcement of poplar by rice NAC transcription factor. Sci Rep 6:19925Google Scholar
  141. Sánchez-Rodríguez C, Bauer S, Hématy K, Saxe F, Ibáñez AB, Vodermaier V, Konlechner C, Sampathkumar A, Rüggeberg M, Aichinger E, Neumetzler L, Burgert I, Somerville C, Hauser M, Persson S (2012) CHITINASE-LIKE1/POM-POM1 and its homolog CTL2 are glucan-interacting proteins important for cellulose biosynthesis in Arabidopsis. Plant Cell 24:589–607Google Scholar
  142. Sato H, Sakamoto S, Mitsuda N, Ohme-Takagi M, Takamizo T (2018) Improvement of cell wall digestibility in tall fescue by Oryza sativa SECONDARY WALL NAC DOMAIN PROTEIN2 chimeric repressor. Mol Breed 38:36Google Scholar
  143. Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289Google Scholar
  144. Schindelman G, Morikami A, Jung J, Baskin TI, Carpita NC, Derbyshire P, McCann MC, Benfey PN (2001) COBRA encodes a putative GPI-anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis. Genes Dev 15:1115–1127Google Scholar
  145. Schmitz AJ, Begcy K, Sarath G, Walia H (2015) Rice Ovate Family Protein 2 (OFP2) alters hormonal homeostasis and vasculature development. Plant Sci 241:177–188Google Scholar
  146. Schoch G, Goepfert S, Morant M, Hehn A, Meyer D, Ullmann P, Werck-Reichhart D (2001) CYP98A3 from Arabidopsis thaliana is a 3′-hydroxylase of phenolic esters, a missing link in the phenylpropanoid pathway. J Biol Chem 276:36566–36574Google Scholar
  147. Schultink A, Naylor D, Dama M, Pauly M (2015) The role of the plant-specific ALTERED XYLOGLUCAN9 protein in Arabidopsis cell wall polysaccharide O-acetylation. Plant Physiol 167:1271–1283Google Scholar
  148. 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 (2015) Overexpression of SbMyb60 impacts phenylpropanoid biosynthesis and alters secondary cell wall composition in Sorghum bicolor. Plant J 85:378–395Google Scholar
  149. Sederoff RR, MacKay JJ, Ralph J, Hatfield D (1999) Unexpected variation in lignin. Curr Opin Plant Biol 2:145–152Google Scholar
  150. Shigeto J, Tsutsumi Y (2016) Diverse functions and reactions of class III peroxidases. New Phytol 209:1395–1402Google Scholar
  151. Simmons TJ, Mortimer JC, Bernardinelli OD, Pöppler A, Brown SP, Deazevedo ER, Dupree R, Dupree P (2016) Folding of xylan onto cellulose fibrils in plant cell walls revealed by solid-state NMR. Nat Commun 7:13902.  https://doi.org/10.1038/ncomms13902CrossRefGoogle Scholar
  152. Somerville C (2006) Cellulose synthesis in higher plants. Annu Rev Cell Dev Biol 22:53–78Google Scholar
  153. Sonbol FM, Fornalé S, Capellades M, Encina A, Touriño S, Torres JL, 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.  https://doi.org/10.1007/s11103-009-9473-2CrossRefGoogle Scholar
  154. Soyano T, Thitamadee S, Machida Y, Chua NH (2008) ASYMMETRIC LEAVES2-LIKE19/LATERAL ORGAN BOUNDARIES DOMAIN30 and ASL20/LBD18 regulate tracheary element differentiation in Arabidopsis. Plant Cell 20:3359–3373Google Scholar
  155. Speicher TL, Li PZ, Wallace IS (2018) Phosphoregulation of the plant cellulose synthase complex and cellulose synthase-like proteins. Plan Theory 7:52Google Scholar
  156. Stephen AM (1983) Other plant polysaccharides. In: Aspinall GO (ed) The polysaccharides, vol 2. Academic Press, New York, pp 97–193Google Scholar
  157. Šturcová A, His I, Apperley DC, Sugiyama J, Jarvis MC (2004) Structural details of crystalline cellulose from higher plants. Biomacromolecules 5:1333–1339Google Scholar
  158. Sun X, Wang C, Xiang N, Li X, Yang S, Du J, Ynag Y, Yang Y (2017) Activation of secondary cell wall biosynthesis by miR319-targeted TCP4 transcription factor. Plant Biotechnol J 15:1284–1294Google Scholar
  159. Sun Q, Liu X, Yang J (2018) MicroRNA528 affects lodging resistance of maize by regulating lignin biosynthesis under nitrogen-luxury conditions. Mol Plant 11:806814Google Scholar
  160. Szyjanowicz PM, McKinnon I, Taylor NG, Gardiner J, Jarvis MC, Turner SR (2004) The irregular xylem 2 mutant is an allele of korrigan that affects the secondary cell wall of Arabidopsis thaliana. Plant J 37:730–740Google Scholar
  161. Takahashi J, Rudsander UJ, Hedenström M, Banasiak A, Harholt J, Amelot N, Immerzeel P, Ryden P, Endo S, Ibatullin FM, Brumer H, del Campillo E, Master ER, Scheller HV, Sundberg B, Teeri TT, Mellerowicz EJ (2009) Korrigan1 and its aspen homolog PttCel9A1 decrease cellulose crystallinity in Arabidopsis stem. Plant Cell Physiol 50:1099–1115Google Scholar
  162. Takeuchi M, Kegasa T, Watanabe A, Tamura M, Tsutsumi Y (2018) Expression analysis of transporter genes for screening candidate monolignol transporters using Arabidopsis thaliana cell suspensions during tracheary element differentiation. J Plant Res 131:297–305Google Scholar
  163. Taylor NG (2007) Identification of cellulose synthase AtCesA7 (IRX3) in vivo phosphorylation sites-a potential role in regulating protein degradation. Plant Mol Biol 64:161–171Google Scholar
  164. Taylor NG (2008) Cellulose biosynthesis and deposition in higher plants. New Phytol 178:239–252Google Scholar
  165. 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 (2014) An Arabidopsis gene regulatory network for secondary cell wall synthesis. Nature 517:571–575Google Scholar
  166. Teleman A, Nordström M, Tenkanen M, Jacobs A, Dahlman O (2003) Isolation and characterization of O-acetylated glucomannans from aspen and birch wood. Carbohydr Res 338:525–534Google Scholar
  167. Tian Q, Wang X, Li C, Lu W, Yang L, Jiang Y, Luo K (2013) Functional characterization of the poplar R2R3-MYB transcription factor PtoMYB216 involved in the regulation of lignin biosynthesis during wood formation. PLoS One 8:e76369Google Scholar
  168. Tobimatsu Y, Schuetz M (2019) Lignin polymerization: how do plants manage the chemistry so well? Curr Opin Biotechnol 56:75–81Google Scholar
  169. Tobimatsu Y, Chen F, Nakashima J, Escamilla-Treviño LL, Jackson L, Dixon RA, Ralph J (2013) Coexistence but independent biosynthesis of catechyl and guaiacyl/syringyl lignin polymers in seed coats. Plant Cell 25:2587–2600Google Scholar
  170. Townsley B, Sinha N, Kang J (2013) KNOX1 genes regulate lignin deposition and composition in monocots and dicots. Front Plant Sci 4:121Google Scholar
  171. Tsuyama T, Kawai R, Shitan N, Matoh T, Sugiyama J, Yoshinaga A, Tabake K, Fujita M, Yazaki K (2013) Proton-dependent coniferin transport, a common major transport event in differentiating xylem tissue of woody plants. Plant Physiol 162:918–926Google Scholar
  172. Turner S, Kumar M (2018) Cellulose synthase complex organization and cellulose microfibril structure. Phil Trans R Soc A 376:20170048Google Scholar
  173. Turner SR, Somerville CR (1997) Collapsed xylem phenotype of Arabidopsis identifies mutants deficient in cellulose deposition in the secondary cell wall. Plant Cell 9:689–701Google Scholar
  174. Urbanowicz BR, Peña MJ, Ratnaparkhe S, Avci U, Backe J, Steet HF, Foston M, Li H, O’Neill MA, Ragauskas AJ, Darvill AG, Wyman C, Gilbert HJ, York WS (2012) 4-O-methylation of glucuronic acid in Arabidopsis glucuronoxylan is catalyzed by a domain of unknown function family 579 protein. Proc Natl Acad Sci U S A 109:14253–14258Google Scholar
  175. Urbanowicz BR, Peña MJ, Moniz HA, Moremen KW, York WS (2014) Two Arabidopsis proteins synthesize acetylated xylan in vitro. Plant J 80:197–206Google Scholar
  176. Vain T, Crowell EF, Timpano H, Biot E, Desprez T, Mansoori N, Gonneau M, Vernhettes S (2014) The cellulose KORRIGAN is part of the cellulose synthase complex. Plant Physiol 165:1521–1532Google Scholar
  177. 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 64:1333–1343Google Scholar
  178. Vandavasi VG, Putnam DK, Zhang Q, Petridis L, Heller WT, Nixon BT, Haigler CH, Kalluri U, Coates L, Langan P, Smith JC, Meiler J, O’Neill H (2016) A Structural study of CESA1 catalytic domain of Arabidopsis cellulose synthesis complex: evidence for CESA trimers. Plant Physiol 170:123–135Google Scholar
  179. Vanholme R, Cesarino I, Rataj K, Xiao Y, Sundin L, Goeminne G, Kim H, Cross J, Moreel K, Araujo P, Welsh L, Haustraete J, McClellan C, Vanholme B, Ralph J, Simpson GS, Halpin C, Boerjan W (2013) Caffeoyl shikimate esterase (CSE) is an enzyme in the lignin biosynthetic pathway in Arabidopsis. Science 341:1103–1106Google Scholar
  180. Vélez-Bermúdez IC, Salazar-Henao JE, Fornalé S, López-Vidriero I, Franco-Zorrilla JM, Grotewold E, Gray J, Solano R, Schmidt W, Pagés M, Riera M, Caparros-Ruiz D (2015) A MYB/ZML complex regulates wound-induced lignin genes in maize. Plant Cell 27:3245–3259Google Scholar
  181. Wang HZ, Dixon RA (2012) On-off switches for secondary cell wall biosynthesis. Mol Plant 5:297–303Google Scholar
  182. 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 U S A 107:22338–22343Google Scholar
  183. Wang H, Zhao Q, Chen F, Wang M, Dixon RA (2011) NAC domain function and transcriptional control of a secondary cell wall master switch. Plant J 68:1104–1114Google Scholar
  184. Wang Y, Mortimer JC, Davis J, Dupree P, Keegstra K (2013a) Identification of an additional protein involved in mannan biosynthesis. Plant J 73:105–117Google Scholar
  185. Wang HH, Tang RJ, Liu H, Chen HY, Liu JY, Jiang XN, Zhang HX (2013b) Chimeric repressor of PtSND2 severely affects wood formation in transgenic Populus. Tree Physiol 33:878–886Google Scholar
  186. 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 (2015) LACCASE5 is required for lignification of the Brachypodium distachyon culm. Plant Physiol 168:192–204Google Scholar
  187. Whitney SEC, Brigham JE, Darke AH, Reid JSG, Gidley MJ (1998) Structural aspects of the interaction of mannan-based polysaccharides with bacterial cellulose. Carbohydr Res 307:299–309Google Scholar
  188. Wightman R, Turner SR (2008) The roles of the cytoskeleton during cellulose deposition at the secondary cell wall. Plant J 54:794–805Google Scholar
  189. Willför S, Sundberg K, Tenkanen M, Holmbom B (2008) Spruce-derived mannans – a potential raw material for hydrocolloids and novel advanced natural materials. Carbohydr Polym 72:197–210Google Scholar
  190. Wuddineh WA, Mazarei M, Zhang JY, Turner GB, Sykes RW, Decker SR, Davis MF, Udvardi MK, Stewart CN Jr (2016) Identification and overexpression of a Knotted1-like transcription factor in switchgrass (Panicum virgatum L.) for lignocellulosic feedstock improvement. Front Plant Sci 7:520Google Scholar
  191. Xiao W, Yang Y, Yu J (2018) ZmNST3 and ZmNST4 are master switches for secondary wall deposition in maize (Zea mays L.). Plant Sci 266:83–94Google Scholar
  192. Xiong G, Cheng K, Pauly M (2013) Xylan O-acetylation impacts xylem development and enzymatic recalcitrance as indicated by the Arabidopsis mutant tbl29. Mol Plant 6:1373–1375Google Scholar
  193. Xu B, Ohtani M, Yamaguchi M, Toyooka K, Wakazaki M, Sato M, Kubo M, Nakano Y, Sano R, Hiwatashi Y, Murata T, Kurata T, Yoneda A, Kato K, Hasebe M, Demura T (2014a) Contribution of NAC transcription factors to plant adaptation to land. Science 343:1505–1508Google Scholar
  194. Xu Q, Yin XR, Zeng JK, Ge H, Song M, Xu CJ, Li X, Ferguson IB, Chen KS (2014b) Activator- and repressor-type MYB transcription factors are involved in chilling injury induced flesh lignification in loquat via their interactions with the phenylpropanoid pathway. J Exp Bot 65:4349–4359Google Scholar
  195. Xu C, Fu X, Liu R, Guo L, Ran L, Li C, Tian Q, Jiao B, Wang B, Luo K (2017) PtoMYB170 positively regulates lignin deposition during wood formation in poplar and confers drought tolerance in transgenic Arabidopsis. Tree Physiol 37:1713–1726Google Scholar
  196. Yamaguchi M, Mitsuda N, Ohtani M, Ohme-Takagi M, Kato K, Demura T (2011) VASCULAR-RELATED NAC-DOMAIN7 directly regulates expression of a broad range of genes for xylem vessel formation. Plant J 66:579–590Google Scholar
  197. Yamaguchi M, Nagahage ISP, Ohtani M, Ishikawa T, Uchimiya H, Kawai-Yamada M, Demura T (2015) Arabidopsis NAC domain proteins VND-INTERACTING1 and ANAC103 interact with multiple NAC domain proteins. Plant Biotechnol 32:119–123Google Scholar
  198. Yan X, Liu J, Kim H, Liu B, Huang X, Yang Z, Lin YJ, Chen H, Yang C, Wang JP, Muddiman DC, Ralph J, Sederoff RR, Li Q, Chiang VL (2018a) CAD1 and CCR2 protein complex formation in monolignol biosynthesis in Populus trichocarpa. New Phytol.  https://doi.org/10.1111/nph.15505
  199. Yan Z, Lizhu W, Xingfen W, Bin C, Jing Z, Jing C, Zhikun L, Jun Y, Liqiang W, Jinhua W, Guiyin Z, Zhiying M (2018b) The cotton laccase GhLAC15 enhances Verticillium wilt resistance via an increase in defence-induced lignification and lignin components in the cell walls of plants. Mol Plant Pathol.  https://doi.org/10.1111/mpp.12755
  200. Yang C, Xu Z, Song J, Conner K, Vizcay Barrena G, Wilson ZA (2007) Arabidopsis MYB26/MALE STERILE35 regulates secondary thickening in the endothecium and is essential for anther dehiscence. Plant Cell 19:534–548Google Scholar
  201. Yang SD, Seo PJ, Yoon HK, Park CM (2011) The Arabidopsis NAC transcription factor VNI2 integrates abscisic acid signals into leaf senescence via the COR/RD genes. Plant Cell 23:2155–2168Google Scholar
  202. Yang F, Mitra P, Zhang L, Prak L, Verhertbruggen Y, Kim JS, Zheng K, Tang K, Auer M, Scheller HV, Loqué D (2013) Engineering secondary cell wall deposition in plants. Plant Biotechnol J 11:325–335Google Scholar
  203. Yang C, Li D, Liu X, Ji C, Hao L, Zhao X, Li X, Chen C, Cheng Z, Zhu L (2014) OsMYB103L, an R2R3-MYB transcription factor, influences leaf rolling and mechanical strength in rice (Oryza sativa L.). BMC Plant Biol 14:158Google Scholar
  204. Yang L, Zhao X, Yang F, Fan D, Jiang Y, Luo K (2016) PtrWRKY19, a novel WRKY transcription factor, contributes to the regulation of pith secondary wall formation in Populus trichocarpa. Sci Rep 6:18643Google Scholar
  205. Yang L, Zhao X, Ran L, Li C, Fan D, Luo K (2017) PtoMYB156 is involved in negative regulation of phenylpropanoid metabolism and secondary cell wall biosynthesis during wood formation in poplar. Sci Rep 7:41209Google Scholar
  206. Ye Y, Liu B, Zhao M, Wu K, Cheng W, Chen X, Liu Q, Liu Z, Fu X, Wu Y (2015) CEF1/OsMYB103L is involved in GA-mediated regulation of secondary wall biosynthesis in rice. Plant Mol Biol 89:385–401Google Scholar
  207. Yoshida K, Sakamoto S, Kawai T, Kobayashi Y, Sato K, Ichinose Y, Yaoi K, Akiyoshi-Endo M, Sato H, Takamizo T, Ohme-Takagi M, Mitsuda N (2013) Engineering the Oryza sativa cell wall with rice NAC transcription factors regulating secondary wall formation. Front Plant Sci 4:383Google Scholar
  208. Yu L, Lyczakowski JJ, Pereira CS, Kotake T, Yu X, Li A, Mogelsvang S, Skaf MS, Dupree P (2018) The patterned structure of galactoglucomannan suggests it may bind to cellulose in seed mucilage. Plant Physiol 178:1011–1026Google Scholar
  209. Yuan Y, Teng Q, Zhong R, Ye Z (2013) The Arabidopsis DUF231 domain-containing protein ESK1 mediates 2-O- and 3-O-acetylation of xylosyl residues in xylan. Plant Cell Physiol 54:1186–1199Google Scholar
  210. Yuan Y, Teng Q, Zhong R, Haghighat M, Richardson EA, Ye Z (2016) Mutations of Arabidopsis TBL32 and TBL33 affect xylan acetylation and secondary wall deposition. PLoS One 11:e0146460Google Scholar
  211. Zhang Y, Nikolovski N, Sorieul M, Vellosillo T, McFarlane H, Dupree R, Kesten C, Schneider R, Driemeier C, Lathe R, Lampugnani E, Yu X, Ivakov A, Doblin MS, Mortimer JC, Brown SP, Persson S, Dupree P (2016) Golgi-localized STELLO proteins regulate the assembly and trafficking of cellulose synthase complexes in Arabidopsis. Nat Commun 7:11656.  https://doi.org/10.1038/ncomms11656CrossRefGoogle Scholar
  212. Zhang J, Xie M, Tuskan GA, Muchero W, Chen JG (2018a) Recent advances in the transcriptional regulation of secondary cell wall biosynthesis in the woody plants. Front Plant Sci 9:1535Google Scholar
  213. Zhang X, Dominguez PG, Kumar M, Bygdell J, Miroshnichenko S, Sundberg B, Wingsle G, Niittylä T (2018b) Cellulose synthase stoichiometry in aspen differs from Arabidopsis and Norway spruce. Plant Physiol 177:1096–1107Google Scholar
  214. Zhao Q, Gallego-Giraldo L, Wang H, Zeng Y, Ding SY, Chen F, Dixon RA (2010) An NAC transcription factor orchestrates multiple features of cell wall development in Medicago truncatula. Plant J 63:100–114Google Scholar
  215. 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 25:3976–3987Google Scholar
  216. Zhao Y, Sun J, Xu P, Zhang R, Li L (2014) Intron-mediated alternative splicing of WOOD-ASSOCIATED NAC TRANSCRIPTION FACTOR1B regulates cell wall thickening during fiber development in Populus species. Plant Physiol 164:765–776Google Scholar
  217. Zhao X, Liu N, Shang N, Zeng W, Ebert B, Rautengarten C, Zeng QY, Li H, Chen X, Beahan C, Bacic A, Heazlewood JL, Wu AM (2018) Three UDP-xylose transporters participate in xylan biosynthesis by conveying cytosolic UDP-xylose into the Golgi lumen in Arabidopsis. J Exp Bot 69:1125–1134Google Scholar
  218. 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 53:368–380Google Scholar
  219. Zhong R, Ye ZH (2015) Secondary cell walls: biosynthesis, patterned deposition and transcriptional regulation. Plant Cell Physiol 56:195–214Google Scholar
  220. Zhong R, Peña MJ, Zhou GK, Nairn J, Wood-Jones A, Richardson EA, Morrison WH III, Darvill AG, York WS, Ye ZH (2005) Arabidopsis Fragile Fiber8, which encodes a putative glucuronosyltransferase, is essential for normal secondary wall synthesis. Plant Cell 17:3390–3408Google Scholar
  221. Zhong R, Demura T, Ye ZH (2006) SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell 18:3158–3170Google Scholar
  222. Zhong R, Richardson EA, Ye ZH (2007a) Two NAC domain transcription factors, SND1 and NST1, function redundantly in regulation of secondary wall synthesis in fibers of Arabidopsis. Planta 225:1603–1611Google Scholar
  223. Zhong R, Richardson EA, Ye ZH (2007b) The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. Plant Cell 19:2776–2792Google Scholar
  224. 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 20:2763–2782Google Scholar
  225. Zhong R, Lee C, Ye Z (2010a) Functional characterization of poplar wood-associated NAC domain transcription factors. Plant Physiol 152:1044–1055Google Scholar
  226. Zhong R, Lee C, Ye ZH (2010b) Evolutionary conservation of the transcriptional network regulating secondary cell wall biosynthesis. Trends Plant Sci 15:625–632Google Scholar
  227. Zhong R, Lee C, Ye ZH (2010c) Global analysis of direct targets of secondary wall NAC master switches in Arabidopsis. Mol Plant 3:1087–1103Google Scholar
  228. Zhong R, Lee C, McCarthy RL, Reeves CK, Jones EG, Ye ZH (2011a) Transcriptional activation of secondary wall biosynthesis by rice and maize NAC and MYB transcription factors. Plant Cell Physiol 52:1856–1871Google Scholar
  229. Zhong R, McCarthy RL, Lee C, Ye ZH (2011b) Dissection of the transcriptional program regulating secondary wall biosynthesis during wood formation in poplar. Plant Physiol 157:1452–1468Google Scholar
  230. 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:e69219Google Scholar
  231. Zhong R, Yuan Y, Spiekerman JJ, Guley JT, Egbosiuba JC, Ye ZH (2015) Functional characterization of NAC and MYB transcription factors involved in regulation of biomass production in switchgrass (Panicum virgatum). PLoS One 10:e0134611Google Scholar
  232. Zhong R, Cui D, Phillips DR, Ye ZH (2018a) A novel rice xylosyltransferase catalyzes the addition of 2-O-xylosyl side chains onto the xylan backbone. Plant Cell Physiol 59:554–565Google Scholar
  233. Zhong R, Cui D, Ye ZH (2018b) Members of the DUF231 family are O-acetyltransferases catalyzing 2-O- and 3-O-acetylation of mannan. Plant Cell Physiol 59:2339–2349Google Scholar
  234. Zhou J, Lee C, Zhong R, Ye ZH (2009) MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. Plant Cell 21:248–266Google Scholar
  235. Zhou J, Zhong R, Ye ZH (2014) Arabidopsis NAC domain proteins, VND1 to VND5, are transcriptional regulators of secondary wall biosynthesis in vessels. PLoS One 9:e105726Google Scholar
  236. Zhu X, Li S, Pan S, Xin X, Gu Y (2018) CSI1, PATROL1, and exocyst complex cooperate in delivery of cellulose synthase complexes to the plasma membrane. Proc Natl Acad Sci U S A 115:E3578–E3587Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Ignacio Zarra
    • 1
    Email author
  • Gloria Revilla
    • 1
  • Javier Sampedro
    • 1
  • Elene R. Valdivia
    • 1
  1. 1.Departamento de Biología Funcional, Facultad de BiologíaUniversidad de Santiago de Compostela, Campus VidaSantiago de CompostelaSpain

Personalised recommendations