Secondary cell walls: Biosynthesis and manipulation

Journal of Experimental Botany

Volumn 67, Issue 2, 2016, Pages 515-531

  Kumar, Manoj ^a   Campbell, Liam ^a   Turner, Simon ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Biofuels; cellulose; lignin; lignin engineering; regulation; SCW; xylan; xylan engineering

Indexed keywords

HEMICELLULOSE; LIGNIN; POLYSACCHARIDE;

CELL WALL; METABOLISM; PLANT; PLANT CELL;

CELL WALL; LIGNIN; PLANT CELLS; PLANTS; POLYSACCHARIDES;

EID: 84959907387     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erv533     Document Type: Review

References (172)

1. AbuQamar S, Chen X, Dhawan R, Bluhm B, Salmeron J, Lam S, Dietrich RA, Mengiste T. (2006). Expression profiling and mutant analysis reveals complex regulatory networks involved in Arabidopsis response to Botrytis infection. The Plant Journal 48, 28-44
2. Alejandro S, Lee Y, Tohge T, et al. (2012). AtABCG29 is a monolignol transporter involved in lignin biosynthesis. Current Biology 22, 1207-1212
3. Anders N, Wilkinson MD, Lovegrove A, et al. (2012). Glycosyl transferases in family 61 mediate arabinofuranosyl transfer onto xylan in grasses. Proceedings of the National Academy of Sciences, USA 109, 989-993
4. Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K. (2004). Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. The Plant Cell 16, 3460-3479
5. Andersson-Gunneras S, Mellerowicz EJ, Love J, Segerman B, Ohmiya Y, Coutinho PM, Nilsson P, Henrissat B, Moritz T, Sundberg B. (2006). Biosynthesis of cellulose-enriched tension wood in Populus: global analysis of transcripts and metabolites identifies biochemical and developmental regulators in secondary wall biosynthesis. The Plant Journal 45, 144-165
6. Atanassov, II, Pittman JK, Turner SR. (2009). Elucidating the mechanisms of assembly and subunit interaction of the cellulose synthase complex of Arabidopsis secondary cell walls. Journal of Biological Chemistry 284, 3833-3841
7. Atmodjo MA, Sakuragi Y, Zhu X, Burrell AJ, Mohanty SS, Atwood JA III, Orlando R, Scheller HV, Mohnen D. (2011). Galacturonosyltransferase (GAUT)1 and GAUT7 are the core of a plant cell wall pectin biosynthetic homogalacturonan: galacturonosyltransferase complex. Proceedings of the National Academy of Sciences, USA 108, 20225-20230
8. Audenaert K, De Meyer GB, Höfte MM. (2002). Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiology 128, 491-501
9. Azpiroz R, Wu Y, LoCascio JC, Feldmann KA. (1998). An Arabidopsis brassinosteroid-dependent mutant is blocked in cell elongation. The Plant Cell 10, 219-230
10. Barros J, Serk H, Granlund I, Pesquet E. (2015). The cell biology of lignification in higher plants. Annals of Botany 115, 1053-1074
11. Bartley LE, Peck ML, Kim S-R, et al. (2013). Overexpression of a BAHD acyltransferase, OsAt10, alters rice cell wall hydroxycinnamic acid content and saccharification. Plant Physiology 161, 1615-1633
12. Baucher M, Monties B, Van Montagu M, Boerjan W. (1998). Biosynthesis and genetic engineering of lignin. Critical Reviews in Plant Sciences 17, 125-197
13. Berthet S, Demont-Caulet N, Pollet B, et al. (2011). Disruption of LACCASE4 and 17 results in tissue-specific alterations to lignification of Arabidopsis thaliana stems. The Plant Cell 23, 1124-1137
14. Blee KA, Wheatley ER, Bonham VA, Mitchell GP, Robertson D, Slabas AR, Burrell MM, Wojtaszek P, Bolwell GP. (2001). Proteomic analysis reveals a novel set of cell wall proteins in a transformed tobacco cell culture that synthesises secondary walls as determined by biochemical and morphological parameters. Planta 212, 404-415
15. Boerjan W, Ralph J, Baucher M. (2003). Lignin biosynthesis. Annual Review of Plant Biology 54, 519-546
16. Bonawitz ND, Chapple C. (2010). The genetics of lignin biosynthesis: connecting genotype to phenotype. Annual Review of Genetics 44, 337-363
17. Brenner WG, Ramireddy E, Heyl A, Schmulling T. (2012). Gene regulation by cytokinin in Arabidopsis. Frontiers in Plant Science 3, 8
18. Bromley JR, Busse-Wicher M, Tryfona T, Mortimer JC, Zhang ZN, Brown DM, Dupree P. (2013). GUX1 and GUX2 glucuronyltransferases decorate distinct domains of glucuronoxylan with different substitution patterns. The Plant Journal 74, 423-434
19. Brown DM, Goubet F, Vicky WWA, Goodacre R, Stephens E, Dupree P, Turner SR. (2007). Comparison of five xylan synthesis mutants reveals new insight into the mechanisms of xylan synthesis. The lant Journal 52, 1154-1168
20. Brown D, Wightman R, Zhang ZN, Gomez LD, Atanassov I, Bukowski JP, Tryfona T, McQueen-Mason SJ, Dupree P, Turner S. (2011). Arabidopsis genes IRREGULAR XYLEM (IRX15) and IRX15L encode DUF579-containing proteins that are essential for normal xylan deposition in the secondary cell wall. The Plant Journal 66, 401-413
21. 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. The Plant Cell 17, 2281-2295
22. Burton RA, Fincher GB. (2014). Plant cell wall engineering: applications in biofuel production and improved human health. Current Opinion in Biotechnology 26, 79-84
23. 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 2-fold helical screw in the secondary plant cell wall of Arabidopsis thaliana. The Plant Journal 79, 492-506
24. Carpita N, Tierney M, Campbell M. (2001). Molecular biology of the plant cell wall: searching for the genes that define structure, architecture and dynamics. Plant Molecular Biology 47, 1-5
25. Carroll A, Somerville C. (2009). Cellulosic biofuels. Annual Review of Plant Biology 60, 165-182
26. Cecchetti V, Altamura MM, Brunetti P, Petrocelli V, Falasca G, Ljung K, Costantino P, Cardarelli M. (2013). Auxin controls arabidopsis anther dehiscence by regulating endothecium lignification and jasmonic acid biosynthesis. The Plant Journal 74, 411-422
27. Chapelle A, Morreel K, Vanholme R, Le-Bris P, Morin H, Lapierre C, Boerjan W, Jouanin L, Demont-Caulet N. (2012). Impact of the absence of stem-specific beta-glucosidases on lignin and monolignols. Plant Physiology 160, 1204-1217
28. Chen F, Dixon RA. (2007). Lignin modification improves fermentable sugar yields for biofuel production. Nature Biotechnology 25, 759-761
29. Chen Z, Hong X, Zhang H, Wang Y, Li X, Zhu JK, Gong Z. (2005). Disruption of the cellulose synthase gene, AtCesA8/IRX1, enhances drought and osmotic stress tolerance in Arabidopsis. The Plant Journal 43, 273-283
30. Chiniquy D, Sharma V, Schultink A, et al. (2012). XAX1 from glycosyltransferase family 61 mediates xylosyltransfer to rice xylan. Proceedings of the National Academy of Sciences, USA 109, 17117-17122
31. Chiniquy D, Varanasi P, Oh T, et al. (2013). Three novel rice genes closely related to the Arabidopsis IRX9, IRX9L, and IRX14 genes and their roles in xylan biosynthesis. Frontiers in Plant Science 4, 83
32. Chundawat SPS, Beckham GT, Himmel ME, Dale BE. (2011). Deconstruction of lignocellulosic biomass to fuels and chemicals. Annual Review of Chemical and Biomolecular Engineering 2, 121-145
33. Crowell EF, Bischoff V, Desprez T, Rolland A, Stierhof YD, Schumacher K, Gonneau M, Hofte H, Vernhettes S. (2009). Pausing of Golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis. The Plant Cell 21, 1141-1154
34. de Jager SM, Menges M, Bauer UM, Murray JAH. (2001). Arabidopsis E2F1 binds a sequence present in the promoter of S-phase-regulated gene AtCDC6 and is a member of a multigene family with differential activities. Plant Molecular Biology 47, 555-568
35. del Pozo JC, Boniotti MB, Gutierrez C. (2002). Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin-SCFAtSKP2 pathway in response to light. The Plant Cell 14, 3057-3071
36. del Pozo JC, Diaz-Trivino S, Cisneros N, Gutierrez C. (2006). The balance between cell division and endoreplication depends on E2FC-DPB, transcription factors regulated by the ubiquitin-SCFSKP2A pathway in Arabidopsis. The Plant Cell 18, 2224-2235
37. Del Pozo JC, Diaz-Trivino S, Cisneros N, Gutierrez C. (2007). The E2FC-DPB transcription factor controls cell division, endoreplication and lateral root formation in a SCF-dependent manner. Plant Signaling and Behavior 2, 273-274
38. Denancé N, Ranocha P, Oria N, et al. (2013). Arabidopsis wat1 (walls are thin1)-mediated resistance to the bacterial vascular pathogen, Ralstonia solanacearum, is accompanied by cross-regulation of salicylic acid and tryptophan metabolism. The Plant Journal 73, 225-239
39. Desprez T, Juraniec M, Crowell EF, Jouy H, Pochylova Z, Parcy F, Hofte H, Gonneau M, Vernhettes S. (2007). Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 104, 15572-15577
40. Dhugga KS, Barreiro R, Whitten B, et al. (2004). Guar seed betamannan synthase is a member of the cellulose synthase super gene family. Science 303, 363-366
41. 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. The Plant Journal 19, 691-697
42. Ehlting J, Mattheus N, Aeschliman DS, et al. (2005). Global transcript profiling of primary stems from Arabidopsis thaliana identifies candidate genes for missing links in lignin biosynthesis and transcriptional regulators of fiber differentiation. The Plant Journal 42, 618-640
43. Endler A, Kesten C, Schneider R, Zhang Y, Ivakov A, Froehlich A, Funke N, Persson s. (2015). A mechanism for sustained cellulose synthesis during salt stress. Cell 162, 1353-1364
44. Eudes A, Sathitsuksanoh N, Baidoo EEK, George A, Liang Y, Yang F, Singh S, Keasling JD, Simmons BA, Loqué D. (2015). Expression of a bacterial 3-dehydroshikimate dehydratase reduces lignin content and improves biomass saccharification efficiency. Plant Biotechnology Journal 13, 1241-1250
45. Fernandes AN, Thomas LH, Altaner CM, Callow P, Forsyth VT, Apperley DC, Kennedy CJ, Jarvis MC. (2011). Nanostructure of cellulose microfibrils in spruce wood. Proceedings of the National Academy of Sciences, USA 108, E1195-E1203
46. Fukuda H. (1997). Tracheary element differentiation. The Plant Cell 9, 1147-1156
47. Gao Y, Zhang Y, Zhang D, Dai X, Estelle M, Zhao Y. (2015). Auxin binding protein 1 (ABP1) is not required for either auxin signaling or Arabidopsis development. Proceedings of the National Academy of Sciences, USA 112, 2275-2280
48. Gardiner JC, Taylor NG, Turner SR. (2003). Control of cellulose synthase complex localization in developing xylem. The Plant Cell 15, 1740-1748
49. Goubet F, Barton CJ, Mortimer JC, Yu XL, Zhang ZN, Miles GP, Richens J, Liepman AH, Seffen K, Dupree P. (2009). Cell wall glucomannan in Arabidopsis is synthesised by CSLA glycosyltransferases, and influences the progression of embryogenesis. The Plant Journal 60, 527-538
50. Gu Y, Kaplinsky N, Bringmann M, Cobb A, Carroll A, Sampathkumar A, Baskin TI, Persson S, Somerville CR. (2010). Identification of a cellulose synthase-associated protein required for cellulose biosynthesis. Proceedings of the National Academy of Sciences, USA 107, 12866-12871
51. Gutierrez R, Lindeboom JJ, Paredez AR, Emons AMC, Ehrhardt DW. (2009). Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nature Cell Biology 11, 797-U743
52. Halpin C. (2004). Investigating and manipulating lignin biosynthesis in the postgenomic era. Advances in Botanical Research Incorporating Advances in Plant Pathology 41, 63-106
53. Hao ZY, Mohnen D. (2014). A review of xylan and lignin biosynthesis: foundation for studying Arabidopsis irregular xylem mutants with pleiotropic phenotypes. Critical Reviews in Biochemistry and Molecular Biology 49, 212-241
54. Heckmann S, Lermontova I, Berckmans B, De Veylder L, Baeumlein H, Schubert I. (2011). The E2F transcription factor family regulates CENH3 expression in Arabidopsis thaliana. The Plant Journal 68, 646-656
55. Held MA, Jiang N, Basu D, Showalter AM, Faik A. (2015). Plant cell wall polysaccharides: structure and biosynthesis. In: Ramawat KG, Mérillon J-M, eds. Polysaccharides: bioactivity and biotechnology . Berlin: Springer, 3-54
56. Hernandez-Blanco C, Feng DX, Hu J, et al. (2007). Impairment of cellulose synthases required for Arabidopsis secondary cell wall formation enhances disease resistance. The Plant Cell 19, 890-903
57. Herrero J, Esteban Carrasco A, Miguel Zapata J. (2014). Arabidopsis thaliana peroxidases involved in lignin biosynthesis: in silico promoter analysis and hormonal regulation. Plant Physiology and Biochemistry 80, 192-202
58. Herth W. (1985). Plasma-membrane rosettes involved in localized wall thickening during xylem vessel formation of Lepidium sativum L. Planta 164, 12-21
59. Hill JL Jr, Hammudi MB, Tien M. (2014). The Arabidopsis cellulose synthase complex: a proposed hexamer of CESA trimers in an equimolar stoichiometry. The Plant Cell 26, 4834-4842
60. Himmel ME, Ding SY, Johnson DK, Adney WS, Nimlos MR, Brady JW, Foust TD. (2007). Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315, 804-807
61. Hosokawa M, Suzuki S, Umezawa T, Sato Y. (2001). Progress of lignification mediated by intercellular transportation of monolignols during tracheary element differentiation of isolated Zinnia mesophyll cells. Plant and Cell Physiology 42, 959-968
62. Hossain Z, McGarvey B, Amyot L, Gruber M, Jung J, Hannoufa A. (2012). DIMINUTO 1 affects the lignin profile and secondary cell wall formation in Arabidopsis. Planta 235, 485-498
63. Hussey SG, Mizrachi E, Creux NM, Myburg AA. (2013). Navigating the transcriptional roadmap regulating plant secondary cell wall deposition. Frontiers in Plant Science 4, 325
64. Hutchison CE, Li J, Argueso C, et al. (2006). The Arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. The Plant Cell 18, 3073-3087
65. Ishiguro S, Kawai-Oda A, Ueda J, Nishida I, Okada K. (2001). The DEFECTIVE IN ANTHER DEHISCENCE1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. The Plant Cell 13, 2191-2209
66. Jansson S, Douglas CJ. (2007). Populus: a model system for plant biology. Annual Review of Plant Biology 58, 435-458
67. Jensen JK, Johnson NR, Wilkerson CG. (2014). Arabidopsis thaliana IRX10 and two related proteins from psyllium and Physcomitrella patens are xylan xylosyltransferases. The Plant Journal 80, 207-215
68. Jensen MK, Kjaersgaard T, Nielsen MM, Galberg P, Petersen K, O?Shea C, Skriver K. (2010). The Arabidopsis thaliana NAC transcription factor family: structure-function relationships and determinants of ANAC019 stress signalling. Biochemical Journal 426, 183-196
69. Jones L, Ennos AR, Turner SR. (2001). Cloning and characterization of irregular xylem4 (irx4): a severely lignin-deficient mutant of Arabidopsis. The Plant Journal 26, 205-216
70. Jung KW, Kim YY, Yoo KS, Ok SH, Cui MH, Jeong BC, Yoo SD, Jeung JU, Shin JS. (2013). A cystathionine-β-synthase domain-containing protein, CBSX2, regulates endothecial secondary cell wall thickening in anther development. Plant and Cell Physiology 54, 195-208
71. Jung KW, Oh S-I, Kim YY, Yoo KS, Cui MH, Shin JS. (2008). Arabidopsis histidine-containing phosphotransfer factor 4 (AHP4) negatively regulates secondary wall thickening of the anther endothecium during flowering. Molecules and Cells 25, 294-300
72. Ko D, Kang J, Kiba T, et al. (2014). Arabidopsis ABCG14 is essential for the root-to-shoot translocation of cytokinin. Proceedings of the National Academy of Sciences, USA 111, 7150-7155
73. Kosugi S, Ohashi Y. (2002). Interaction of the Arabidopsis E2F and DP proteins confers their concomitant nuclear translocation and transactivation. Plant Physiology 128, 833-843
74. 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 and Development 19, 1855-1860
75. Kumar M, Turner S. (2015a). Cell wall biosynthesis. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902. a0001683.pub2
76. Kumar M, Turner S. (2015b). Plant cellulose synthesis: CESA proteins crossing kingdoms. Phytochemistry 112, 91-99
77. Lee C, Zhong RQ, Ye ZH. (2012). Arabidopsis family GT43 members are xylan xylosyltransferases required for the elongation of the xylan backbone. Plant and Cell Physiology 53, 135-143
78. Lee CH, Zhong RQ, Richardson EA, Himmelsbach DS, McPhail BT, Ye ZH. (2007). The PARVUS gene is expressed in cells undergoing secondary wall thickening and is essential for glucuronoxylan biosynthesis. Plant and Cell Physiology 48, 1659-1672
79. Li J, Yu M, Geng L-L, Zhao J. (2010). The fasciclin-like arabinogalactan protein gene, FLA3, is involved in microspore development of Arabidopsis. The Plant Journal 64, 482-497
80. 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. Proceedings of the National Academy of Sciences, USA 102, 2221-2226
81. Liu L, Shang-Guan K, Zhang B, et al. (2013). Brittle Culm1, a COBRAlike protein, functions in cellulose assembly through binding cellulose microfibrils. PLoS Genetics 9, e1003704
82. Liu ZY, Persson S, Sanchez-Rodriguez C. (2015). At the border: the plasma membrane-cell wall continuum. Journal of Experimental Botany 66, 1553-1563
83. Lorenzo O, Chico JM, Sánchez-Serrano JJ, Solano R. (2004). JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. The Plant Cell 16, 1938-1950
84. MacMillan CP, Mansfield SD, Stachurski ZH, Evans R, Southerton SG. (2010). Fasciclin-like arabinogalactan proteins: specialization for stem biomechanics and cell wall architecture in Arabidopsis and Eucalyptus. The Plant Journal 62, 689-703
85. Mariconti L, Pellegrini B, Cantoni R, Stevens R, Bergounioux C, Cella R, Albani D. (2002). The E2F family of transcription factors from Arabidopsis thaliana-novel and conserved components of the retinoblastoma/E2F pathway in plants. Journal of Biological Chemistry 277, 9911-9919
86. Marriott PE, Sibout R, Lapierre C, Fangel JU, Willats WGT, Hofte H, Gomez LD, McQueen-Mason SJ. (2014). Range of cellwall alterations enhance saccharification in Brachypodium distachyon mutants. Proceedings of the National Academy of Sciences, USA 111, 14601-14606
87. Mele G, Ori N, Sato Y, Hake S. (2005). The knotted1-like homeobox gene BREVIPEDICELLUS regulates cell differentiation by modulating metabolic pathways. Genes and Development 19, 412-412
88. Mellerowicz EJ, Baucher M, Sundberg B, Boerjan W. (2001). Unravelling cell wall formation in the woody dicot stem. Plant Molecular Biology 47, 239-274
89. Miao Y-C, Liu C-J. (2010). ATP-binding cassette-like transporters are involved in the transport of lignin precursors across plasma and vacuolar membranes. Proceedings of the National Academy of Sciences, USA 107, 22728-22733
90. Mitchell RAC, Dupree P, Shewry PR. (2007). A novel bioinformatics approach identifies candidate genes for the synthesis and feruloylation of arabinoxylan. Plant Physiology 144, 43-53
91. 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. The Plant Cell 19, 270-280
92. 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. The Plant Cell 17, 2993-3006
93. Mortimer JC, Miles GP, Brown DM, et al. (2010). Absence of branches from xylan in Arabidopsis gux mutants reveals potential for simplification of lignocellulosic biomass. Proceedings of the National Academy of Sciences, USA 107, 17409-17414
94. Nakano Y, Yamaguchiz M, Endo H, Rejab NA, Ohtani M. (2015). NACMYB-based transcriptional regulation of secondary cell wall biosynthesis in land plants. Frontiers in Plant Science 6, 288
95. Nishiyama Y. (2009). Structure and properties of the cellulose microfibril. Journal of Wood Science 55, 241-249
96. Ooka H, Satoh K, Doi K, et al. (2003). Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Research 10, 239-247
97. Paque S, Mouille G, Grandont L, et al. (2014). AUXIN BINDING PROTEIN1 links cell wall remodeling, auxin signaling, and cell expansion in arabidopsis. The Plant Cell 26, 280-295
98. Pauly M, Gille S, Liu LF, Mansoori N, de Souza A, Schultink A, Xiong GY. (2013). Hemicellulose biosynthesis. Planta 238, 627-642
99. Pauly M, Keegstra K. (2010). Plant cell wall polymers as precursors for biofuels. Current Opinion in Plant Biology 13, 305-312
100. Pena MJ, Zhong RQ, 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. The Plant Cell 19, 549-563
101. Persson S, Caffall KH, Freshour G, Hilley MT, Bauer S, Poindexter P, Hahn MG, Mohnen D, Somerville C. (2007a). The Arabidopsis irregular xylem8 mutant is deficient in glucuronoxylan and homogalacturonan, which are essential for secondary cell wall integrity. The Plant Cell 19, 237-255
102. Persson S, Paredez A, Carroll A, Palsdottir H, Doblin M, Poindexter P, Khitrov N, Auer M, Somerville CR. (2007b). Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proceedings of the National Academy of Sciences, USA 104, 15566-15571
103. Persson S, Wei HR, Milne J, Page GP, Somerville CR. (2005). Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. Proceedings of the National Academy of Sciences, USA 102, 8633-8638
104. Pesquet E, Zhang B, Gorzsas A, et al. (2013). Non-cell-autonomous postmortem lignification of tracheary elements in Zinnia elegans. The Plant Cell 25, 1314-1328
105. Petersen PD, Lau J, Ebert B, et al. (2012). Engineering of plants with improved properties as biofuels feedstocks by vessel-specific complementation of xylan biosynthesis mutants. Biotechnology for Biofuels 5, 84
106. Pogorelko G, Lionetti V, Fursova O, Sundaram RM, Qi M, Whitham SA, Bogdanove AJ, Bellincampi D, Zabotina OA. (2013). Arabidopsis and Brachypodium distachyon transgenic plants expressing Aspergillus nidulans acetylesterases have decreased degree of polysaccharide acetylation and increased resistance to pathogens. Plant Physiology 162, 9-23
107. Ralph J. (2010). Hydroxycinnamates in lignification. Phytochemistry Reviews 9, 65-83
108. Ralph J, Lundquist K, Brunow G, et al. (2004). Lignins: natural polymers from oxidative coupling of 4-hydroxyphenylpropanoids. Phytochemistry Reviews 3, 29-60
109. Ranocha P, Denancé N, Vanholme R, et al. (2010). Walls are thin1 (WAT1), an Arabidopsis homolog of Medicago truncatula NODULIN21, is a tonoplast-localized protein required for secondary wall formation in fibers. The Plant Journal 63, 469-483
110. Ranocha P, Dima O, Nagy R, et al. (2013). Arabidopsis WAT1 is a vacuolar auxin transport facilitator required for auxin homoeostasis. Nature Communications 4, 2625
111. Ren Y, Hansen SF, Ebert B, Lau J, Scheller HV. (2014). Site-directed mutagenesis of IRX9, IRX9L and IRX14 proteins involved in xylan biosynthesis: glycosyltransferase activity is not required for IRX9 function in Arabidopsis. PLoS One 9, e105014
112. Rennie EA, Scheller HV. (2014). Xylan biosynthesis. Current Opinion in Biotechnology 26, 100-107
113. Sanchez-Vallet A, Lopez G, Ramos B, et al. (2012). Disruption of abscisic acid signaling constitutively activates Arabidopsis resistance to the necrotrophic fungus Plectosphaerella cucumerina. Plant Physiology 160, 2109-2124
114. Sanders PM, Bui AQ, Weterings K, McIntire KN, Hsu YC, Lee PY, Truong MT, Beals TP, Goldberg RB. (1999). Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sexual Plant Reproduction 11, 297-322
115. Scheller HV, Ulvskov P. (2010). Hemicelluloses. Annual Review of Plant Biology 61, 263-289
116. Schneider B, Herth W. (1986). Distribution of plasma-membrane rosettes and kinetics of cellulose formation in xylem development of higher-plants. Protoplasma 131, 142-152
117. Schuetz M, Benske A, Smith RA, Watanabe Y, Tobimatsu Y, Ralph J, Demura T, Ellis B, Samuels AL. (2014). Laccases direct lignification in the discrete secondary cell wall domains of protoxylem. Plant Physiology 166, 798-U489
118. Shigeto J, Itoh Y, Hirao S, Ohira K, Fujita K, Tsutsumi Y. (2015). Simultaneously disrupting AtPrx2, AtPrx25 and AtPrx71 alters lignin content and structure in Arabidopsis stem. Journal of Integrative Plant Biology 57, 349-356
119. Showalter AM. (1993). Structure and function of plant-cell wall proteins. The Plant Cell 5, 9-23
120. Smith RA, Schuetz M, Roach M, Mansfield SD, Ellis B, Samuels L. (2013). Neighboring parenchyma cells contribute to Arabidopsis xylem lignification, while lignification of interfascicular fibers is cell autonomous. The Plant Cell 25, 3988-3999
121. Somerville C, Youngs H, Taylor C, Davis SC, Long SP. (2010). Feedstocks for lignocellulosic biofuels. Science 329, 790-792
122. Sorek N, Sorek H, Kijac A, Szemenyei HJ, Bauer S, Hematy K, Wemmer DE, Somerville CR. (2014a). The Arabidopsis COBRA protein facilitates cellulose crystallization at the plasma membrane. Journal of Biological Chemistry 289, 34911-34920
123. Sorek N, Yeats TH, Szemenyei H, Youngs H, Somerville CR. (2014b). The implications of lignocellulosic biomass chemical composition for the production of advanced biofuels. Bioscience 64, 192-201
124. Strabala TJ, MacMillan CP. (2013). The Arabidopsis wood model-the case for the inflorescence stem. Plant Science 210, 193-205
125. Stracke R, Werber M, Weisshaar B. (2001). The R2R3-MYB gene family in Arabidopsis thaliana. Current Opinion in Plant Biology 4, 447-456
126. Sun Y, Fan XY, Cao DM, et al. (2010). Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Developmental Cell 19, 765-777
127. Sun Y, Veerabomma S, Fokar M, Abidi N, Hequet E, Payton P, Allen RD. (2015). Brassinosteroid signaling affects secondary cell wall deposition in cotton fibers. Industrial Crops and Products 65, 334-342
128. Szyjanowicz PMJ, 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. The Plant Journal 37, 730-740
129. Taylor NG. (2007). Identification of cellulose synthase AtCesA7 (IRX3) in vivo phosphorylation sites- A potential role in regulating protein degradation. Plant Molecular Biology 64, 161-171
130. Taylor NG, Howells RM, Huttly AK, Vickers K, Turner SR. (2003). Interactions among three distinct CesA proteins essential for cellulose synthesis. Proceedings of the National Academy of Sciences, USA 100, 1450-1455
131. Taylor-Teeples M, Lin L, de Lucas M, et al. (2015). An Arabidopsis gene regulatory network for secondary cell wall synthesis. Nature 517, 571-575
132. Tokunaga N, Sakakibara N, Umezawa T, Ito Y, Fukuda H, Sato Y. (2005). Involvement of extracellular dilignols in lignification during tracheary element differentiation of isolated Zinnia mesophyll cells. Plant and Cell Physiology 46, 224-232
133. Tsuyama T, Kawai R, Shitan N, Matoh T, Sugiyama J, Yoshinaga A, Takabe K, Fujita M, Yazaki K. (2013). Proton-dependent coniferin transport, a common major transport event in differentiating xylem tissue of woody plants. Plant Physiology 162, 918-926
134. Turner S, Gallois P, Brown D. (2007). Tracheary element differentiation. Annual Review of Plant Biology 58, 407-433
135. Turner SR, Taylor N, Jones L. (2001). Mutations of the secondary cell wall. Plant Molecular Biology 47, 209-219
136. Uggla C, Moritz T, Sandberg G, Sundberg B. (1996). Auxin as a positional signal in pattern formation in plants. Proceedings of the National Academy of Sciences, USA 93, 9282-9286
137. Urbanowicz BR, Pena MJ, Moniz HA, Moremen KW, York WS. (2014). Two Arabidopsis proteins synthesize acetylated xylan in vitro. The Plant Journal 80, 197-206
138. Urbanowicz BR, Pena MJ, Ratnaparkhe S, et al. (2012). 4-O-methylation of glucuronic acid in Arabidopsis glucuronoxylan is catalyzed by a domain of unknown function family 579 protein. Proceedings of the National Academy of Sciences, USA 109, 14253-14258
139. Vain T, Crowell EF, Timpano H, et al. (2014). The cellulase KORRIGAN is part of the cellulose synthase complex. Plant Physiology 165, 1521-1532
140. Van Acker R, Leple JC, Aerts D, et al. (2014). Improved saccharification and ethanol yield from field-grown transgenic poplar deficient in cinnamoyl-CoA reductase. Proceedings of the National Academy of Sciences, USA 111, 845-850
141. Vanholme R, Cesarino I, Rataj K, et al. (2013). Caffeoyl shikimate esterase (CSE) is an enzyme in the lignin biosynthetic pathway in Arabidopsis. Science 341, 1103-1106
142. Vanholme R, Demedts B, Morreel K, Ralph J, Boerjan W. (2010). Lignin biosynthesis and structure. Plant Physiology 153, 895-905
143. Vanholme R, Morreel K, Ralph J, Boerjan W. (2008). Lignin engineering. Current Opinion in Plant Biology 11, 278-285
144. Vermerris W, Abril A. (2015). Enhancing cellulose utilization for fuels and chemicals by genetic modification of plant cell wall architecture. Current Opinion in Biotechnology 32, 104-112
145. Vogel J. (2008). Unique aspects of the grass cell wall. Current Opinion in Plant Biology 11, 301-307
146. Von Malek B, van Der Graaff E, Schneitz K, Keller B. (2002). The Arabidopsis male-sterile mutant dde2-2 is defective in the ALLENE OXIDE SYNTHASE gene encoding one of the key enzymes of the jasmonic acid biosynthesis pathway. Planta 216, 187-192
147. Watanabe Y, Meents MJ, McDonnell LM, Barkwill S, Sampathkumar A, Cartwright HN, Demura T, Ehrhardt DW, Samuels AL, Mansfield SD. (2015). Visualization of cellulose synthases in Arabidopsis secondary cell walls. Science 350, 198-203
148. Wightman R, Marshall R, Turner SR. (2009). A cellulose synthasecontaining compartment moves rapidly beneath sites of secondary wall synthesis. Plant and Cell Physiology 50, 584-594
149. Wightman R, Turner S. (2010). Trafficking of the cellulose synthase complex in developing xylem vessels. Biochemical Society Transactions 38, 755-760
150. Wightman R, Turner SR. (2008). The roles of the cytoskeleton during cellulose deposition at the secondary cell wall. The Plant Journal 54, 794-805
151. Wilkerson CG, Mansfield SD, Lu F, et al. (2014). Monolignol ferulate transferase introduces chemically labile linkages into the lignin backbone. Science 344, 90-93
152. Wilkins O, Nahal H, Foong J, Provart NJ, Campbell MM. (2009). Expansion and diversification of the Populus R2R3-MYB family of transcription factors. Plant Physiology 149, 981-993
153. Wu AM, Hornblad E, Voxeur A, Gerber L, Rihouey C, Lerouge P, Marchant A. (2010). Analysis of the Arabidopsis IRX9/IRX9-L and IRX14/IRX14-L pairs of glycosyltransferase genes reveals critical contributions to biosynthesis of the hemicellulose glucuronoxylan. Plant Physiology 153, 542-554
154. Wu AM, Rihouey C, Seveno M, Hornblad E, Singh SK, Matsunaga T, Ishii T, Lerouge P, Marchant A. (2009). The Arabidopsis IRX10 and IRX10-LIKE glycosyltransferases are critical for glucuronoxylan biosynthesis during secondary cell wall formation. The Plant Journal 57, 718-731
155. Xie L, Yang C, Wang X. (2011a). Brassinosteroids can regulate cellulose biosynthesis by controlling the expression of CESA genes in Arabidopsis. Journal of Experimental Botany 62, 4495-4506
156. Xie LQ, Yang CJ, Wang XL. (2011b). Brassinosteroids can regulate cellulose biosynthesis by controlling the expression of CESA genes in Arabidopsis. Journal of Experimental Botany 62, 4495-4506
157. Xiong GY, Cheng K, Pauly M. (2013). Xylan O-acetylation impacts xylem development and enzymatic recalcitrance as indicated by the Arabidopsis mutant tbl29. Molecular Plant 6, 1373-1375
158. Xiong GY, Dama M, Pauly M. (2015). Glucuronic acid moieties on xylan are functionally equivalent to O-acetyl-substituents. Molecular Plant 8, 1119-1121
159. Yamaguchi M, Goue N, Igarashi H, et al. (2010). VASCULAR-RELATED NAC-DOMAIN6 and VASCULAR-RELATED NAC-DOMAIN7 effectively induce transdifferentiation into xylem vessel elements under control of an induction system. Plant Physiology 153, 906-914
160. Yamaguchi M, Mitsuda N, Ohtani M, Ohme-Takagi M, Kato K, Demura T. (2011). VASCULAR-RELATED NAC-DOMAIN 7 directly regulates the expression of a broad range of genes for xylem vessel formation. The Plant Journal 66, 579-590
161. 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. The Plant Cell 19, 534-548
162. Yang F, Mitra P, Zhang L, et al. (2013). Engineering secondary cell wall deposition in plants. Plant Biotechnology Journal 11, 325-335
163. York WS, O'Neill MA. (2008). Biochemical control of xylan biosynthesis-which end is up? Current Opinion in Plant Biology 11, 258-265
164. Yuan Y, Teng Q, Zhong R, Ye Z-H. (2015). TBL3 and TBL31, two Arabidopsis DUF231 domain proteins, are required for 3-O-monoacetylation of xylan. Plant and Cell Physiology (in press
165. Yuan YX, Teng Q, Zhong RQ, Ye ZH. (2013). The Arabidopsis DUF231 domain-containing protein ESK1 mediates 2-O-and 3-O-acetylation of xylosyl residues in xylan. Plant and Cell Physiology 54, 1186-1199
166. Zhang J, Elo A, Helariutta Y. (2011). Arabidopsis as a model for wood formation. Current Opinion in Biotechnology 22, 293-299
167. Zhang K, Novak O, Wei Z, Gou M, Zhang X, Yu Y, Yang H, Cai Y, Strnad M, Liu C-J. (2014). Arabidopsis ABCG14 protein controls the acropetal translocation of root-synthesized cytokinins. Nature Communications 5, 3274
168. Zhao Q, Nakashima J, Chen F, Yin Y, Fu C, Yun J, Shao H, Wang X, Wang Z-Y, Dixon RA. (2013). Laccase is necessary and nonredundant with peroxidase for lignin polymerization during vascular development in Arabidopsis. The Plant Cell 25, 3976-3987
169. Zhong RQ, Demura T, Ye ZH. (2006). SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. The Plant Cell 18, 3158-3170
170. Zhong RQ, Lee CH, Ye ZH. (2010a). Functional characterization of poplar wood-associated NAC domain transcription factors. Plant Physiology 152, 1044-1055
171. Zhong RQ, Lee CH, Ye ZH. (2010b). Global analysis of direct targets of secondary wall NAC master switches in Arabidopsis. Molecular Plant 3, 1087-1103
172. Zhou JL, Lee CH, Zhong RQ, Ye ZH. (2009). MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. The Plant Cell 21, 248-266