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Biosynthesis and Regulation of Secondary Cell Wall

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Progress in Botany Vol. 81

Part of the book series: Progress in Botany ((BOTANY,volume 81))

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.

Communicated by Francisco M. Cánovas

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References

  • 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 16:3098–3109

    CAS  PubMed  PubMed Central  Google Scholar 

  • Albersheim P, Darvill A, Roberts K, Sederoff R, Staehelin A (2011) Plant cell walls: from chemistry to biology. Garland Science, Taylor & Francis Group, New York

    Google Scholar 

  • 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 22:1207–1212

    CAS  PubMed  Google Scholar 

  • 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 109:989–993

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 279:717–720

    CAS  PubMed  Google Scholar 

  • Barnes WJ, Anderson CT (2018) Cytosolic invertases contribute to cellulose biosynthesis and influence carbon partitioning in seedlings of Arabidopsis thaliana. Plant J 94:956–974

    CAS  PubMed  Google Scholar 

  • Barros J, Serk H, Granlund I, Pesquet E (2015) The cell biology of lignification in higher plants. Ann Bot 115:1053–1074

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.2016.50

    Article  CAS  PubMed  Google Scholar 

  • Bashline L, Li S, Gu Y (2014) The trafficking of the cellulose synthase complex in higher plants. Ann Bot 114:1059–1067

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 24:4465–4482

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 22:640–654

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 23:1124–1137

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 154:1428–1438

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bischoff V, Selbig J, Scheible W (2010) Involvement of TBL/DUF231 proteins into cell wall biology. Plant Signal Behav 5:1057–1059

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 64:163–176

    CAS  PubMed  Google Scholar 

  • Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Physiol 54:519–546

    CAS  Google Scholar 

  • Boija E, Lundquist A, Edwards K, Johansson G (2007) Evaluation of bilayer disks as plant membrane models in partition studies. Anal Biochem 364:145–152

    CAS  PubMed  Google Scholar 

  • 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 59:3925–3939

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bonawitz ND, Chapple C (2010) The genetics of lignin biosynthesis: connecting genotype to phenotype. Annu Rev Genet 44:337–363

    CAS  PubMed  Google Scholar 

  • 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 176:2148–2165

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brett C (2000) Cellulose microfibrils in plants: biosynthesis, deposition, and integration into the cell wall. Int Rev Cytol 199:161–199

    CAS  PubMed  Google Scholar 

  • 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 74:423–434

    CAS  PubMed  Google Scholar 

  • 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 17:2281–2295

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 52:1154–1168

    CAS  PubMed  Google Scholar 

  • 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 79:492–506

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 329:635–645

    CAS  PubMed  Google Scholar 

  • 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 4:189

    PubMed  PubMed Central  Google Scholar 

  • 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 64:1769–1781

    CAS  PubMed  Google Scholar 

  • 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 58:44–51

    CAS  Google Scholar 

  • 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 108:21253–21258

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 109:1772–1777

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 73:201–211

    CAS  PubMed  Google Scholar 

  • 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 26:876–893

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

  • 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 29:1907–1926

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 109:17117–11122

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861

    CAS  PubMed  Google Scholar 

  • Cosgrove D, Jarvis M (2012) Comparative structure and biomechanics of plant primary and secondary cell walls. Front Plant Sci 3:204

    PubMed  PubMed Central  Google Scholar 

  • 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 123:453–461

    CAS  PubMed  PubMed Central  Google Scholar 

  • Delmer DP (1999) Cellulose biosynthesis: exciting times for a difficult field of study. Annu Rev Plant Physiol Plant Mol Biol 50:245–276

    CAS  PubMed  Google Scholar 

  • 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 303:363–366

    CAS  PubMed  Google Scholar 

  • Didi V, Jackson P, Hejátko J (2015) Hormonal regulation of secondary cell wall formation. J Exp Bot 66:5015–5027

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Du J, Mansfield SD, Shawn D, Groover AT (2009) The Populus homeobox gene ARBORKNOX2 regulates cell differentiation during secondary growth. Plant J 60:1000–1014

    CAS  PubMed  Google Scholar 

  • 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:e17458

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 19:691–697

    CAS  PubMed  Google Scholar 

  • 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 56:242–254

    CAS  PubMed  Google Scholar 

  • Fernández-Pérez F, Pomar F, Pedreño MA, Novo-Uzal E (2015) Supression of Arabidopsis peroxidase 72 alters cell wall and phenylpropanoid metabolism. Plant Sci 239:192–199

    PubMed  Google Scholar 

  • 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 55:507–516

    PubMed  Google Scholar 

  • 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 14:895–904

    PubMed  Google Scholar 

  • 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 203:1220–1230

    CAS  PubMed  Google Scholar 

  • Gille S, Pauly M (2012) O-Acetylation of plant cell wall polysaccharides. Front Plant Sci 3:12

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 43:553–567

    CAS  PubMed  Google Scholar 

  • Gou M, Ran X, Martin DW, Liu C-J (2018) The scaffold proteins of lignin biosynthetic cytochrome P450 enzymes. Nat Plants 4:299–310

    CAS  PubMed  Google Scholar 

  • 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 86:363–375

    CAS  PubMed  Google Scholar 

  • Haigler CH, Ivanova-Datcheva M, Hogan PS, Salnikov VV, Hwang S, Martin K, Delmer DP (2001) Carbon partitioning to cellulose synthesis. Plant Mol Biol 47:29–51

    CAS  PubMed  Google Scholar 

  • 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 96:532–545

    CAS  PubMed  Google Scholar 

  • Harris D, DeBolt S (2010) Synthesis, regulation and utilization of lignocellulosic biomass. Plant Biotechnol J 8:244–262

    CAS  PubMed  Google Scholar 

  • 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 237:1599–1612

    CAS  PubMed  Google Scholar 

  • Higuchi T, Ito Y, Kawamura I (1967) p-Hydroxyphenylpropane component of grass lignin and role of tyrosine-ammonia lyase in its formation. Phytochemistry 6:875–881

    CAS  Google Scholar 

  • Hill JL, Hammudi MB, Tien M (2014) The Arabidopsis cellulose synthase complex: a proposed hexamer of CESA trimers in an equimolar stoichiometry. Plant Cell 26:4834–4842

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 54:1791–1802

    CAS  PubMed  Google Scholar 

  • 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 110:14498–14503

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 27:1681–1696

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 11:173

    CAS  PubMed  PubMed Central  Google Scholar 

  • Iwata T, Indrarti L, Azuma J (1998) Affinity of hemicellulose for cellulose produced by Acetobacter xylinum. Cellulose 5:215–228

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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 19:6150–6161

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 175:1058–1067

    CAS  PubMed  PubMed Central  Google Scholar 

  • Karlen SD, Free HCA, Padmakshan D, Smith BG, Ralph J, Harris PJ (2018) Commelinid monocotyledon lignins are acylated by p-coumarate. Plant Physiol 177:513–521

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kataoka Y, Kondo T (1998) FT-IR microscopic analysis of changing cellulose crystalline structure during wood cell wall formation. Macromolecules 31:760–764

    CAS  Google Scholar 

  • Kawabe H, Ohtani M, Kurata T, Sakamoto T, Demura T (2018) Protein S-nitrosylation regulates xylem vessel cell differentiation in Arabidopsis. Plant Cell Physiol 59:17–29

    CAS  PubMed  Google Scholar 

  • 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 73:26–36

    PubMed  Google Scholar 

  • 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 170:1374–1378

    CAS  PubMed  Google Scholar 

  • 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 85:589–599

    CAS  PubMed  Google Scholar 

  • 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 60:649–665

    CAS  PubMed  Google Scholar 

  • 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 19:1855–1860

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar M, Turner S (2015) Plant cellulose synthesis: CESA proteins crossing kingdoms. Phytochemistry 112:91–99

    CAS  PubMed  Google Scholar 

  • Kumar M, Campbell L, Turner S (2016) Secondary cell walls: biosynthesis and manipulation. J Exp Bot 67:515–531

    CAS  PubMed  Google Scholar 

  • 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 88:1046–1057

    CAS  PubMed  Google Scholar 

  • 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 7:735

    PubMed  PubMed Central  Google Scholar 

  • 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 53:1934–1949

    CAS  PubMed  Google Scholar 

  • Lee Y, Rubio MC, Alassimone J, Geldner N (2013) A mechanism for localized lignin deposition in the endodermis. Cell 153:402–412

    CAS  PubMed  Google Scholar 

  • Lee C, Teng Q, Zhong R, Ye Z (2014) Alterations of the degree of xylan acetylation in Arabidopsis xylan mutants. Plant Signal Behav 9:e27797

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 188:774–786

    CAS  PubMed  Google Scholar 

  • 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 116:175–182

    CAS  PubMed  Google Scholar 

  • 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 67:328–341

    CAS  PubMed  Google Scholar 

  • 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 109:185–190

    CAS  PubMed  Google Scholar 

  • 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 194:102–115

    CAS  PubMed  Google Scholar 

  • 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 224:1185–1196

    CAS  PubMed  Google Scholar 

  • 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 102:2221–2228

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e1003704

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 26:4843–4861

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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/ijms19020335

    Article  CAS  PubMed Central  Google Scholar 

  • Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D495

    Google Scholar 

  • 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 110:10848–10853

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 48:29–39

    CAS  Google Scholar 

  • 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 18:539

    PubMed  PubMed Central  Google Scholar 

  • 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 155:1068–1078

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 175:1579–1592

    PubMed  PubMed Central  Google Scholar 

  • 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 50:1950–1964

    CAS  PubMed  Google Scholar 

  • McFarlane HE, Döring A, Persson S (2014) The cell biology of cellulose synthesis. Annu Rev Plant Biol 65:69–94

    CAS  PubMed  Google Scholar 

  • Meents M, Watanabe Y, Samuels AL (2018) The cell biology of secondary cell wall biosynthesis. Ann Bot 121:1107–1125

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mele G, Ori N, Sato Y, Hake S (2003) The knotted1-like homeobox gene BREVIPEDICELLUS regulates cell differentiation by modulating metabolic pathways. Genes Dev 17:2088–2093

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 157:441–453

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 107:22728–22733

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 17:2993–3006

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 19:270–280

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 45:93–105

    CAS  PubMed  Google Scholar 

  • Moreira LRS, Filho EXF (2008) An overview of mannan structure and mannan-degrading enzyme systems. Appl Microbiol Biotechnol 79:165–178

    CAS  PubMed  Google Scholar 

  • 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 6:288

    PubMed  PubMed Central  Google Scholar 

  • Negi S, Tak H, Ganapathi TR (2015) Cloning and functional characterization of MusaVND1 using transgenic banana plants. Transgenic Res 24:571–585

    CAS  PubMed  Google Scholar 

  • Negi S, Tak H, Ganapathi TR (2016) Functional characterization of secondary wall deposition regulating transcription factors MusaVND2 and MusaVND3 in transgenic banana plants. Protoplasma 253:431–446

    CAS  PubMed  Google Scholar 

  • 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 265:70–86

    CAS  PubMed  Google Scholar 

  • 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 37:239–250

    CAS  PubMed  Google Scholar 

  • 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 163:1558–1567

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 17:5563–5576

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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 22:3461–3473

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 59:989–996

    CAS  PubMed  Google Scholar 

  • 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 73:63–76

    PubMed  Google Scholar 

  • 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 67:499–512

    CAS  PubMed  Google Scholar 

  • Paredez AR, Somerville CR, Ehrhardt DW (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312:1491–1495

    CAS  PubMed  Google Scholar 

  • 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 16:1094–1104

    PubMed  PubMed Central  Google Scholar 

  • 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 36:743–754

    CAS  PubMed  Google Scholar 

  • 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 214:1491–1505

    CAS  PubMed  Google Scholar 

  • 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 93:12637–12642

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pedreira J, Herrera MT, Zarra I, Revilla G (2011) The overexpression of AtPrx37, an apoplastic peroxidase, reduces growth in Arabidopsis. Physiol Plant 141:177–187

    CAS  PubMed  Google Scholar 

  • 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 19:549–563

    PubMed  PubMed Central  Google Scholar 

  • 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 244:589–606

    PubMed  Google Scholar 

  • Perkins M, Smith RA, Samuels L (2019) The transport of monomers during lignification in plants: anything goes to how? Curr Opin Biotechnol 56:69–74

    CAS  PubMed  Google Scholar 

  • 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 113:11360–11365

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raes J, Rohde A, Christensen JH, van der Peer Y, Boerjan W (2003) Genome-wide characterization of the lignification toolbox in Arabidopsis. Plant Physiol 133:1051–1071

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 3:29–60

    CAS  Google Scholar 

  • 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.2018.00399

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 219:230–245

    CAS  PubMed  Google Scholar 

  • Rennie EA, Scheller HV (2014) Xylan biosynthesis. Curr Opin Biotechnol 26:100–107

    CAS  PubMed  Google Scholar 

  • 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 56:1651–1663

    CAS  PubMed  Google Scholar 

  • Ruel K, Nishiyama Y, Joseleau J (2012) Crystalline and amorphous cellulose in the secondary walls of Arabidopsis. Plant Sci 193–194:48–61

    PubMed  Google Scholar 

  • Sakamoto S, Takata N, Oshima Y, Yoshida K, Taniguchi T, Mitsuda N (2016) Wood reinforcement of poplar by rice NAC transcription factor. Sci Rep 6:19925

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 24:589–607

    PubMed  PubMed Central  Google Scholar 

  • 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 38:36

    Google Scholar 

  • Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289

    CAS  PubMed  Google Scholar 

  • 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 15:1115–1127

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schmitz AJ, Begcy K, Sarath G, Walia H (2015) Rice Ovate Family Protein 2 (OFP2) alters hormonal homeostasis and vasculature development. Plant Sci 241:177–188

    CAS  PubMed  Google Scholar 

  • 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 276:36566–36574

    CAS  PubMed  Google Scholar 

  • 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 167:1271–1283

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 85:378–395

    Google Scholar 

  • Sederoff RR, MacKay JJ, Ralph J, Hatfield D (1999) Unexpected variation in lignin. Curr Opin Plant Biol 2:145–152

    CAS  PubMed  Google Scholar 

  • Shigeto J, Tsutsumi Y (2016) Diverse functions and reactions of class III peroxidases. New Phytol 209:1395–1402

    CAS  PubMed  Google Scholar 

  • 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/ncomms13902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Somerville C (2006) Cellulose synthesis in higher plants. Annu Rev Cell Dev Biol 22:53–78

    CAS  PubMed  Google Scholar 

  • 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/s11103-009-9473-2

    Article  CAS  PubMed  Google Scholar 

  • 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 20:3359–3373

    CAS  PubMed  PubMed Central  Google Scholar 

  • Speicher TL, Li PZ, Wallace IS (2018) Phosphoregulation of the plant cellulose synthase complex and cellulose synthase-like proteins. Plan Theory 7:52

    CAS  Google Scholar 

  • Stephen AM (1983) Other plant polysaccharides. In: Aspinall GO (ed) The polysaccharides, vol 2. Academic Press, New York, pp 97–193

    Google Scholar 

  • Šturcová A, His I, Apperley DC, Sugiyama J, Jarvis MC (2004) Structural details of crystalline cellulose from higher plants. Biomacromolecules 5:1333–1339

    PubMed  Google Scholar 

  • 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 15:1284–1294

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun Q, Liu X, Yang J (2018) MicroRNA528 affects lodging resistance of maize by regulating lignin biosynthesis under nitrogen-luxury conditions. Mol Plant 11:806814

    Google Scholar 

  • 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 37:730–740

    CAS  PubMed  Google Scholar 

  • 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 50:1099–1115

    CAS  PubMed  Google Scholar 

  • 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 131:297–305

    CAS  PubMed  Google Scholar 

  • Taylor NG (2007) Identification of cellulose synthase AtCesA7 (IRX3) in vivo phosphorylation sites-a potential role in regulating protein degradation. Plant Mol Biol 64:161–171

    CAS  PubMed  Google Scholar 

  • Taylor NG (2008) Cellulose biosynthesis and deposition in higher plants. New Phytol 178:239–252

    CAS  PubMed  Google Scholar 

  • 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 517:571–575

    PubMed  PubMed Central  Google Scholar 

  • 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 338:525–534

    CAS  PubMed  Google Scholar 

  • 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:e76369

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tobimatsu Y, Schuetz M (2019) Lignin polymerization: how do plants manage the chemistry so well? Curr Opin Biotechnol 56:75–81

    CAS  PubMed  Google Scholar 

  • 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 25:2587–2600

    CAS  PubMed  PubMed Central  Google Scholar 

  • Townsley B, Sinha N, Kang J (2013) KNOX1 genes regulate lignin deposition and composition in monocots and dicots. Front Plant Sci 4:121

    PubMed  PubMed Central  Google Scholar 

  • 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 162:918–926

    CAS  PubMed  PubMed Central  Google Scholar 

  • Turner S, Kumar M (2018) Cellulose synthase complex organization and cellulose microfibril structure. Phil Trans R Soc A 376:20170048

    PubMed  Google Scholar 

  • Turner SR, Somerville CR (1997) Collapsed xylem phenotype of Arabidopsis identifies mutants deficient in cellulose deposition in the secondary cell wall. Plant Cell 9:689–701

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 109:14253–14258

    CAS  PubMed  PubMed Central  Google Scholar 

  • Urbanowicz BR, Peña MJ, Moniz HA, Moremen KW, York WS (2014) Two Arabidopsis proteins synthesize acetylated xylan in vitro. Plant J 80:197–206

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 165:1521–1532

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 170:123–135

    CAS  PubMed  Google Scholar 

  • 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 341:1103–1106

    CAS  PubMed  Google Scholar 

  • 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 27:3245–3259

    PubMed  PubMed Central  Google Scholar 

  • Wang HZ, Dixon RA (2012) On-off switches for secondary cell wall biosynthesis. Mol Plant 5:297–303

    CAS  PubMed  Google Scholar 

  • 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 107:22338–22343

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 68:1104–1114

    CAS  PubMed  Google Scholar 

  • Wang Y, Mortimer JC, Davis J, Dupree P, Keegstra K (2013a) Identification of an additional protein involved in mannan biosynthesis. Plant J 73:105–117

    CAS  PubMed  Google Scholar 

  • 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 33:878–886

    PubMed  Google Scholar 

  • 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 168:192–204

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 307:299–309

    CAS  Google Scholar 

  • Wightman R, Turner SR (2008) The roles of the cytoskeleton during cellulose deposition at the secondary cell wall. Plant J 54:794–805

    CAS  PubMed  Google Scholar 

  • 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 72:197–210

    Google Scholar 

  • 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 7:520

    PubMed  PubMed Central  Google Scholar 

  • Xiao W, Yang Y, Yu J (2018) ZmNST3 and ZmNST4 are master switches for secondary wall deposition in maize (Zea mays L.). Plant Sci 266:83–94

    CAS  PubMed  Google Scholar 

  • 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 6:1373–1375

    CAS  PubMed  Google Scholar 

  • 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 343:1505–1508

    CAS  PubMed  Google Scholar 

  • 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 65:4349–4359

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 37:1713–1726

    CAS  PubMed  Google Scholar 

  • 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 66:579–590

    CAS  PubMed  Google Scholar 

  • 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 32:119–123

    CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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 19:534–548

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 23:2155–2168

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 11:325–335

    CAS  PubMed  Google Scholar 

  • 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 14:158

    PubMed  PubMed Central  Google Scholar 

  • 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 6:18643

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 7:41209

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 89:385–401

    CAS  PubMed  Google Scholar 

  • 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 4:383

    PubMed  PubMed Central  Google Scholar 

  • 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 178:1011–1026

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 54:1186–1199

    CAS  PubMed  Google Scholar 

  • 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:e0146460

    PubMed  PubMed Central  Google Scholar 

  • 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/ncomms11656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 9:1535

    PubMed  PubMed Central  Google Scholar 

  • 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 177:1096–1107

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 63:100–114

    CAS  PubMed  Google Scholar 

  • 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 25:3976–3987

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 164:765–776

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 69:1125–1134

    CAS  PubMed  Google Scholar 

  • 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 53:368–380

    CAS  PubMed  Google Scholar 

  • Zhong R, Ye ZH (2015) Secondary cell walls: biosynthesis, patterned deposition and transcriptional regulation. Plant Cell Physiol 56:195–214

    CAS  PubMed  Google Scholar 

  • 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 17:3390–3408

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 18:3158–3170

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 225:1603–1611

    CAS  PubMed  Google Scholar 

  • 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 19:2776–2792

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 20:2763–2782

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong R, Lee C, Ye Z (2010a) Functional characterization of poplar wood-associated NAC domain transcription factors. Plant Physiol 152:1044–1055

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong R, Lee C, Ye ZH (2010b) Evolutionary conservation of the transcriptional network regulating secondary cell wall biosynthesis. Trends Plant Sci 15:625–632

    CAS  PubMed  Google Scholar 

  • Zhong R, Lee C, Ye ZH (2010c) Global analysis of direct targets of secondary wall NAC master switches in Arabidopsis. Mol Plant 3:1087–1103

    CAS  PubMed  Google Scholar 

  • 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 52:1856–1871

    CAS  PubMed  Google Scholar 

  • 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 157:1452–1468

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e69219

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e0134611

    PubMed  PubMed Central  Google Scholar 

  • 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 59:554–565

    CAS  PubMed  Google Scholar 

  • 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 59:2339–2349

    CAS  PubMed  Google Scholar 

  • 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 21:248–266

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e105726

    PubMed  PubMed Central  Google Scholar 

  • 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–E3587

    PubMed  PubMed Central  Google Scholar 

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Zarra, I., Revilla, G., Sampedro, J., Valdivia, E.R. (2019). Biosynthesis and Regulation of Secondary Cell Wall. In: Cánovas, F., Lüttge, U., Leuschner, C., Risueño, MC. (eds) Progress in Botany Vol. 81. Progress in Botany, vol 81. Springer, Cham. https://doi.org/10.1007/124_2019_27

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