Plant Cell Wall Polysaccharides: Structure and Biosynthesis

  • Michael A. Held
  • Nan Jiang
  • Debarati Basu
  • Allan M. Showalter
  • Ahmed Faik
Living reference work entry
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Abstract

Plant cells are surrounded by cell walls consisting of complex networks of polysaccharides and glycoproteins. Cell walls play a vital role in a plant’s development and its interactions with the environment. The biosynthesis of cell walls is fueled by carbon fixed by solar energy during photosynthesis. The amount of carbon fixed annually is estimated to ~2 × 1011 tonnes (Hall. Solar energy use through biology – past, present and future. Sol Energy 22:307–328, 1979). Thus, plant cell walls represent a valuable sustainable carbon source for human activities. Plants use complex mechanisms that require the coordinated action of hundreds of glycosyltransferases and other enzymes involved in sugar substrate interconversion to build cell wall polysaccharides. This chapter will focus on discussing current advances in the biosynthesis and structures of these wall polysaccharides, including cellulose, a variety of hemicellulosic polymers, pectins, and structural hydroxyproline-rich glycoproteins (extensins and arabinogalactan-proteins). These polymers are organized into complex but dynamic networks that are still the subject of extensive research. Much work is still needed to determine the functions of many glycosyltransferases involved in building these polymers. In addition, how plant cells manage to secrete and organize them into such complex networks remains a mystery. Thus, the future holds exciting discoveries in the field of plant cell wall polysaccharide biosynthesis.

Keywords

Polysaccharide Glycosyltransferase Cellulose Hemicellulose Pectin Glycoprotein 
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Notes

Acknowledgments

A.M.S. gratefully acknowledges financial support from the National Science Foundation (grant no. 0918661) and an Ohio University Baker Fund Award. AF acknowledges support from the the National Science Foundation award (#IOS 1145887). This work was supported by a facility constructed with funds from Research Facilities Improvement Program Grant Number C06 RR-014575-01 from the National Center for Research Resources, National Institutes of Health.

References

  1. Albersheim P, Darvill A, Roberts K, Sederoff R, Staehelin A (2010) Plant cell walls: from chemistry to biology. Garland Science, Taylor Francis Group, New YorkGoogle Scholar
  2. Amor Y, Haigler CH, Johnson S, Wainscott M, Delmer DP (1995) A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. Proc Natl Acad Sci U S A 92:9353–9357Google Scholar
  3. 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 RA (2012) Glycosyl transferases in family 61 mediate arabinofuranosyl transfer onto xylan in grasses. Proc Natl Acad Sci U S A 109:989–993Google Scholar
  4. Anderson MA, Stone BA (1975) A new substrate for investigating the specificity of beta-glucan hydrolases. FEBS Lett 52:202–207Google Scholar
  5. Andersson SI, Samuelson O, Ishihara M, Shimizu K (1983) Structure of the reducing end-groups in spruce xylan. Carbohydr Res 111:283–288Google Scholar
  6. Appenzeller L, Doblin M, Barreiro R, Wang H, Niu X, Kollipara K, Carrigan L, Tomes D, Chapman M, Dhugga KS (2004) Cellulose synthesis in maize: isolation and expression analysis of the cellulose synthase (CesA) gene family. Cellulose 11:287–299Google Scholar
  7. Arioli T, Peng L, Betzner AS, Burn J, Wittke W, Herth W, Camilleri C, Höfte H, Plazinski J, Birch R, Cork A, Glover J, Redmond J, Williamson RE (1998) Molecular Analysis of Cellulose Biosynthesis in Arabidopsis. Science 279:717–720Google Scholar
  8. Atalla RH, Vanderhart DL (1984) Native cellulose: a composite of two distinct crystalline forms. Science 223:283–285Google Scholar
  9. Atmodjo MA, Sakuragi Y, Zhu X, Burrell AJ, Mohanty SS, Atwood JA 3rd, 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. Proc Natl Acad Sci U S A 108:20225–20230Google Scholar
  10. Atmodjo M, Hao Z, Mohnen D (2013) Evolving views of pectin biosynthesis. Annu Rev Plant Biol 64:747–779Google Scholar
  11. Balakshin M, Capanema E, Gracz H, H-m C, Jameel H (2011) Quantification of lignin-carbohydrate linkages with high-resolution NMR spectroscopy. Planta 233:1097–1110Google Scholar
  12. Bartley LE, Peck ML, Kim SR, Ebert B, Manisseri C, Chiniquy DM, Sykes R, Gao L, Rautengarten C, Vega-Sanchez ME, Benke PI, Canlas PE, Cao P, Brewer S, Lin F, Smith WL, Zhang X, Keasling JD, Jentoff RE, Foster SB, Zhou J, Ziebell A, An G, Scheller HV, Ronald PC (2013) Overexpression of a BAHD acyltransferase, OsAt10, alters rice cell wall hydroxycinnamic acid content and saccharification. Plant Physiol 161:1615–1633Google Scholar
  13. Basu D, Liang Y, Liu X, Himmeldirk K, Faik A, Kieliszewski M, Held M, Showalter AM (2013) Functional identification of a hydroxyproline-o-galactosyltransferase specific for arabinogalactan protein biosynthesis in Arabidopsis. J Biol Chem 288:10132–10143Google Scholar
  14. Beeckman T, Przemeck GK, Stamatiou G, Lau R, Terryn N, De Rycke R, Inzé D, Berleth T (2002) Genetic complexity of cellulose synthase A gene function in Arabidopsis embryogenesis. Plant Physiol 130:1883–1893Google Scholar
  15. Benfey PN, Linstead PJ, Roberts K, Schiefelbein JW, Hauser MT, Aeschbacher RA (1993) Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. Development 119:57–70Google Scholar
  16. Benziman M, Haigler CH, Brown RM, White AR, Cooper KM (1980) Cellulose biogenesis: polymerization and crystallization are coupled processes in Acetobacter xylinum. Proc Natl Acad Sci 77:6678–6682Google Scholar
  17. Bosca S, Barton CJ, Taylor NG, Ryden P, Neumetzler L, Pauly M, Roberts K, Seifert GJ (2006) Interactions between MUR10/CesA7-dependent secondary cellulose biosynthesis and primary cell wall structure. Plant Physiol 142:1353–1363Google Scholar
  18. Bourne Y, Henrissat B (2001) Glycoside hydrolases and glycosyltransferases: families and functional modules. Curr Opin Struct Biol 11:593–600Google Scholar
  19. Bowling AJ, Brown RM Jr (2008) The cytoplasmic domain of the cellulose-synthesizing complex in vascular plants. Protoplasma 233:115–127Google Scholar
  20. Brady JD, Fry SC (1997) Formation of di-isodityrosine and loss of isodityrosine in the cell walls of tomato cell-suspension cultures treated with fungal elicitors or H2O2. Plant Physiol 115:87–92Google Scholar
  21. Brady JD, Sadler IH, Fry SC (1998) Pulcherosine, an oxidatively coupled trimer of tyrosine in plant cell walls: its role in cross-link formation. Phytochemistry 47:349–353Google Scholar
  22. Breton C, Snajdrova L, Jeanneau C, Koca J, Imberty A (2006) Structures and mechanisms of glycosyltransferases. Glycobiology 16:29R–37RGoogle Scholar
  23. Bromley JR, Busse-Wicher M, Tryfona T, Mortimer JC, Zhang Z, Brown DM, Dupree P (2013) GUX1 and GUX2 glucuronyltransferases decorate distinct domains of glucuronoxylan with different substitution patterns. Plant J 74:423–434Google Scholar
  24. Brown RM Jr, Montezinos D (1976) Cellulose microfibrils: visualization of biosynthetic and orienting complexes in association with the plasma membrane. Proc Natl Acad Sci 73:143–147Google Scholar
  25. Brown RM Jr, Saxena IM, Kudlicka K (1996) Cellulose biosynthesis in higher plants. Trends Plant Sci 1:149–156Google Scholar
  26. Brown DM, Zeef LA, Ellis J, Goodacre R, Turner SR (2005) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17:2281–2295Google Scholar
  27. Brown DM, Goubet F, Wong VW, Goodacre R, Stephens E, Dupree P, Turner SR (2007) Comparison of five xylan synthesis mutants reveals new insight into the mechanisms of xylan synthesis. Plant J 52:1154–1168Google Scholar
  28. Brown DM, Zhang Z, Stephens E, Dupree P, Turner SR (2009) Characterization of IRX10 and IRX10-like reveals an essential role in glucuronoxylan biosynthesis in Arabidopsis. Plant J 57:732–746Google Scholar
  29. Buckeridge MS, Crombie HJ, Mendes CJM, Reid JSG, Gidley MJ, Vieira CCJ (1997) A new family of oligosaccharides from the xyloglucan of Hymenaea courbaril L. (Leguminosae) cotyledons. Carbohydr Res 303:233–237Google Scholar
  30. Buckeridge MS, Vergara CE, Carpita NC (1999) The mechanism of synthesis of a mixed-linkage (1→3), (1→4)beta-d-glucan in maize evidence for multiple sites of glucosyl transfer in the synthase complex. Plant Physiol 120:1105–1116Google Scholar
  31. Buckeridge MS, dos Santos HP, Aurelio M, Tine S (2000a) Mobilisation of storage cell wall polysaccharides in seeds. Plant Physiol Biochem 38:141–156Google Scholar
  32. Buckeridge MS, Dietrich SMC, de Lima DU (2000b) Galactomannans as the reserve carbohydrate in legume seeds. Dev Crop Sci 26:283–316Google Scholar
  33. Buckeridge MS, Vergara CE, Carpita NC (2001) Insight into multi-site mechanisms of glycosyl transfer in (1→4)beta-d-glycans provided by the cereal mixed-linkage (1→3), (1→4)beta-d-glucan synthase. Phytochemistry 57:1045–1053Google Scholar
  34. Buckeridge MS, Rayon C, Urbanowicz B, Tiné MAS, Carpita NC (2004) Mixed linkage (1→3),(1→ 4)-β-D-glucans of grasses. Cereal Chem 81:115–127Google Scholar
  35. Buliga GS, Brandt DA, Fincher GB (1986) The sequence statistics and solution conformation of a barley (1/3,1/4)-beta-d-glucan. Carbohydr Res 157:139–156Google Scholar
  36. Burk DH, Ye ZH (2002) Alteration of oriented deposition of cellulose microfibrils by mutation of a katanin-like microtubule-severing protein. Plant Cell 14:2145–2160Google Scholar
  37. Burk DH, Liu B, Zhong R, Morrison WH, Ye ZH (2001) A Katanin-like protein regulates normal cell wall biosynthesis and cell elongation. Plant Cell 13:807–827Google Scholar
  38. Burn JE, Hocart CH, Birch RJ, Cork AC, Williamson RE (2002) Functional analysis of the cellulose synthase genes CesA1, CesA2, and CesA3 in Arabidopsis. Plant Physiol 129:797–807Google Scholar
  39. Burton RA, Shirley NJ, King BJ, Harvey AJ, Fincher GB (2004) The CesA gene family of barley. Quantitative analysis of transcripts reveals two groups of co-expressed genes. Plant Physiol 134:224–236Google Scholar
  40. Burton RA, Wilson SM, Hrmova M, Harvey AJ, Shirley NJ, Medhurst A, Stone BA, Newbigin EJ, Bacic A, Fincher GB (2006) Cellulose synthase-like CslF genes mediate the synthesis of cell wall (1→3), (1→4)-beta-d-glucans. Science 311:1940–1942Google Scholar
  41. Burton RA, Jobling SA, Harvey AJ, Shirley NJ, Mather DE, Bacic A, Fincher GB (2008) The genetics and transcriptional profiles of the cellulose synthase-like HvCslF gene family in barley. Plant Physiol 146:1821–1833Google Scholar
  42. Burton RA, Collins HM, Kibble NA, Smith JA, Shirley NJ, Jobling SA, Henderson M, Singh RR, Pettolino F, Wilson SM, Bird AR, Topping DL, Bacic A, Fincher GB (2011) Over-expression of specific HvCslF cellulose synthase-like genes in transgenic barley increases the levels of cell wall (1,3;1,4)-β-d-glucans and alters their fine structure. Plant Biotechnol J 9:117–135Google Scholar
  43. Caffall KH, Mohnen D (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res 344:1879–1900Google Scholar
  44. Camirand A, Maclachlan G (1986) Biosynthesis of the fucose-containing xyloglucan nonasaccharide by pea microsomal membranes. Plant Physiol 82:379–383Google Scholar
  45. Campbell JA, Davies GJ, Bulone V, Henrissat B (1997) A classification of nucleotide-diphospho-sugar glycosyltransferases based on amino acid sequence similarities. Biochem J 326:929–939Google Scholar
  46. Caño-Delgado A, Penfield S, Smith C, Catley M, Bevan M (2003) Reduced cellulose synthesis invokes lignification and defense responses in Arabidopsis thaliana. Plant J 34:351–362Google Scholar
  47. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37(Database issue):D233–D238Google Scholar
  48. Carpita NC (1996) Structure and biogenesis of the cell walls of grasses. Annu Rev Plant Physiol Plant Mol Biol 47:445–476Google Scholar
  49. Carpita NC (2011) Update on mechanisms of plant cell wall biosynthesis: how plants make cellulose and other (1→4)-beta-d-glycans. Plant Physiol 155:171–184Google Scholar
  50. Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30Google Scholar
  51. Carpita NC, McCann M (2000) The cell wall. In: Buchanan BB, Gruissem W, Jones RJ (eds) Biochemistry and molecular biology of plants. American Society of Plant Biologists, Rockville, pp 25–109Google Scholar
  52. Carpita NC, McCann MC (2010) The maize mixed-linkage (1→3), (1→4)-beta-d-glucan polysaccharide is synthesized at the Golgi membrane. Plant Physiol 153:1362–1371Google Scholar
  53. Cavalier DM, Keegstra K (2006) Two xyloglucan xylosyltransferases catalyze the addition of multiple xylosyl residues to cellohexaose. J Biol Chem 281:34197–34207Google Scholar
  54. Cavalier DM, Lerouxel O, Neumetzler L, Yamauchi K, Reinecke A, Freshour G, Zabotina OA, Hahn MG, Burgert I, Pauly M, Raikhel NV, Keegstra K (2008) Disrupting two Arabidopsis thaliana xylosyltransferase genes results in plants deficient in xyloglucan, a major primary cell wall component. Plant Cell 20:1519–1537Google Scholar
  55. Charnock SJ, Davies GJ (1999) Structure of the nucleotide-diphospho-sugar transferase, SpsA from Bacillus subtilis, in native and nucleotide-complexed forms. Biochemistry 38:6380–6385Google Scholar
  56. Chen J, Varner JE (1985) Isolation and characterization of cDNA clones for carrot extensin and a proline-rich 33-kDa protein. Proc Natl Acad Sci U S A 82:4399–4403Google Scholar
  57. 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. Plant J 43:273–283Google Scholar
  58. Chen S, Ehrhardt DW, Somerville CR (2010) Mutations of cellulose synthase (CESA1) phosphorylation sites modulate anisotropic cell expansion and bidirectional mobility of cellulose synthase. Proc Natl Acad Sci U S A 107:17188–17193Google Scholar
  59. 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 109:17117–17122Google Scholar
  60. Chiniquy D, Varanasi P, Oh T, Harholt J, Katnelson J, Singh S, Auer M, Simmons B, Adams PD, Scheller HV, Ronald PC (2013) Three novel rice genes closely related to the Arabidopsis IRX9, IRX9L, and IRX14 genes and their roles in xylan biosynthesis. Front Plant Sci 4:83Google Scholar
  61. Chou YH, Pogorelko G, Zabotina OA (2012) Xyloglucan xylosyltransferases XXT1, XXT2, and XXT5 and the glucan synthase CSLC4 form Golgi-localized multiprotein complexes. Plant Physiol 159:1355–1366Google Scholar
  62. Coates JC, Laplaze L, Haseloff J (2006) Armadillo-related proteins promote lateral root development in Arabidopsis. Proc Natl Acad Sci U S A 103:1621–1626Google Scholar
  63. Cocuron JC, Lerouxel O, Drakakaki G, Alonso AP, Liepman AH, Keegstra K, Raikhel N, Wilkerson CG (2007) A gene from the cellulose synthase-like C family encodes a β-1,4 glucan synthase. Proc Natl Acad Sci U S A 104:8550–8555Google Scholar
  64. Coutinho PM, Deleury E, Davies GJ, Henrissat B (2003) An evolving hierarchical family classification for glycosyltransferases. J Mol Biol 328:307–317Google Scholar
  65. Crowell EF, Bischoff V, Desprez T, Rolland A, Stierhof YD, Schumacher K, Gonneau M, Höfte H, Vernhettes S (2009) Pausing of Golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis. Plant Cell 21:1141–1154Google Scholar
  66. Crowell EF, Gonneau M, Stierhof Y, Höfte H, Vernhettes S (2010) Regulated trafficking of cellulose synthases. Curr Opion Plant Biol 13:700–705Google Scholar
  67. Dai X, You C, Chen G, Li X, Zhang Q, Wu C (2011) OsBC1L4 encodes a COBRA-like protein that affects cellulose synthesis in rice. Plant Mol Biol 75:333–345Google Scholar
  68. Daras G, Rigas S, Penning B, Milioni D, McCann MC, Carpita NC, Fasseas C, Hatzopoulos P (2009) The thanatos mutation in Arabidopsis thaliana cellulose synthase 3 (AtCesA3) has a dominant-negative effect on cellulose synthesis and plant growth. New Phytol 184:114–126Google Scholar
  69. Davis J, Brandizzi F, Liepman AH, Keegstra K (2010) Arabidopsis mannan synthase CSLA9 and glucan synthase CSLC4 have opposite orientations in the Golgi membrane. Plant J 64:1028–1037Google Scholar
  70. de O Buanafina MM (2009) Feruloylation in grasses: current and future perspectives. Mol Plant 2:861–72Google Scholar
  71. DeAngelis PL (1999) Molecular directionality of polysaccharide polymerization by the Pasteurella multocida hyaluronan synthase. J Biol Chem 274:26557–26562Google Scholar
  72. DeAngelis PL, Papaconstantinou J, Weigel PH (1993) Molecular cloning, identification and sequence of the hyaluronan synthase gene from Group A Streptococcus pyogenes. J Biol Chem 268:19181–19184Google Scholar
  73. del Bem L, Vincentz M (2010) Evolution of xyloglucan-related genes in green plants. BMC Evol Biol 10:341Google Scholar
  74. Delmer DP (1999) Cellulose biosynthesis: exciting times for a difficult field of study. Annu Rev Plant Physiol Plant Mol Biol 50:245–276Google Scholar
  75. Desnos T, Orbovic V, Bellini C, Kronenberger J, Caboche M, Traas J, Hofte H (1996) Procuste1 mutants identify two distinct genetic pathways controlling hypocotyl cell elongation, respectively in dark and light-grown Arabidopsis seedlings. Development 122:683–693Google Scholar
  76. Desprez T, Vernhettes S, Fagard M, Refrégier G, Desnos T, Aletti E, Py N, Pelletier S, Höfte H (2002) Resistance against herbicide isoxaben and cellulose deficiency caused by distinct mutations in same cellulose synthase isoform CESA6. Plant Physiol 128:482–490Google Scholar
  77. 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 beta-mannan synthase is a member of the cellulose synthase super gene family. Science 303:363–366Google Scholar
  78. Dilokpimol A, Geshi N (2014) Arabidopsis thaliana glucuronosyltransferase in family GT14. Plant Signal Behav 9:e28891Google Scholar
  79. Dilokpimol A, Poulsen CP, Vereb G, Kaneko S, Schulz A, Geshi N (2014) Galactosyltransferases from Arabidopsis thaliana in the biosynthesis of type II arabinogalactan: molecular interaction enhances enzyme activity. BMC Plant Biol 14:90Google Scholar
  80. Ding SY, Himmel ME (2006) The maize primary cell wall microfibril: a new model derived from direct visualization. J Agric Food Chem 54:597–606Google Scholar
  81. Ding SY, Liu YS, Zeng Y, Himmel ME, Baker JO, Bayer EA (2012) How does plant cell wall nanoscale architecture correlate with enzymatic digestibility? Science 338:1055–1060Google Scholar
  82. Diotallevi F, Mulder B (2007) The cellulose synthase complex: a polymerization driven supramolecular motor. Biophys J 92:2666–2673Google Scholar
  83. Djerbi S, Lindskog M, Arvestad L, Sterky F, Teeri TT (2005) The genome sequence of black cottonwood (Populus trichocarpa) reveals 18 conserved cellulose synthase (CesA) genes. Planta 221:739–746Google Scholar
  84. Doblin MS, Kurek I, Jacob-Wilk D, Delmer DP (2002) Cellulose biosynthesis in plants: from genes to rosettes. Plant Cell Physiol 43:1407–1420Google Scholar
  85. Doblin MS, Pettolino FA, Wilson SM, Campbell R, Burton RA, Fincher GB, Newbigin E, Bacic A (2009) A barley cellulose synthase-like CSLH gene mediates (1,3;1,4)-beta-d-glucan synthesis in transgenic Arabidopsis. Proc Natl Acad Sci U S A 106:5996–6001Google Scholar
  86. Doering A, Lathe R, Persson S (2012) An update on xylan synthesis. Mol Plant 5:769–771Google Scholar
  87. Dudareva N, D'Auria JC, Nam KH, Raguso RA, Pichersky E (1998) Acetyl-CoA:benzylalcohol acetyltransferase-an enzyme involved in floral scent production in Clarkia breweri. Plant J 14:297–304Google Scholar
  88. Duff RB (1965) The occurrence of apiose in Lemna (duckweed) and other Angiosperms. Biochem J 94:768–772Google Scholar
  89. Ebingerrova A, Hromadkova Z, Heinze T (2005) Hemicellulose. Adv Polym Sci 186:1–67Google Scholar
  90. Ebringerova A, Heinze T (2000) Xylan and xylan derivatives – biopolymers with valuable properties, 1. Naturally occurring xylans structures, isolation procedures and properties. Macromol Rapid Commun 21:542–556Google Scholar
  91. Egelund J, Petersen BL, Motawia MS, Damager I, Faik A, Olsen CE, Ishii T, Clausen H, Ulvskov P, Geshi N (2006) Arabidopsis thaliana RGXT1 and RGXT2 encode Golgi-localized (1,3)-a-d-xylosyltransferases involved in the synthesis of pectic rhamnogalacturonan II. Plant Cell 18:2593–2607Google Scholar
  92. Egelund J, Obel N, Ulvskov P, Geshi N, Pauly M, Bacic A, Petersen BL (2007) Molecular characterization of two Arabidopsis thaliana glycosyltransferase mutants, rra1 and rra2, which have a reduced residual arabinose content in a polymer tightly associated with the cellulosic wall residue. Plant Mol Biol 64:439–449Google Scholar
  93. Ellis C, Karafyllidis I, Wasternack C, Turner JG (2002) The Arabidopsis mutant cev1 links cell wall signaling to jasmonate and ethylene responses. Plant Cell 14:1557–1566Google Scholar
  94. Endler A, Persson S (2011) Cellulose synthases and synthesis in Arabidopsis. Mol Plant 4:199–211Google Scholar
  95. Fagard M, Desnos T, Desprez T, Goubet F, Refregier G, Mouille G, McCann M, Rayon C, Vernhettes S, Höfte H (2000) PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis. Plant Cell 12:2409–2423Google Scholar
  96. Faik A (2010) Xylan biosynthesis: news from the grass. Plant Physiol 153:396–402Google Scholar
  97. Faik A (2013) Chapter 1: “Plant cell wall structure-pretreatment” the critical relationship in biomass conversion to fermentable sugars. In: Green biomass pretreatment for biofuels production, SpringerBriefs in molecular science. Springer, Dordrecht, pp 1–30Google Scholar
  98. Faik A, Chileshe C, Sterling J, Maclachlan G (1997) Xyloglucan galactosyl- and fucosyltransferase activities from pea epicotyl microsomes. Plant Physiol 114:245–254Google Scholar
  99. Faik A, Bar-Peled M, DeRocher AE, Zeng W, Perrin RM, Wilkerson C, Raikhel NV, Keegstra K (2000) Biochemical characterization and molecular cloning of an alpha-1,2-fucosyltransferase that catalyzes the last step of cell wall xyloglucan biosynthesis in pea. J Biol Chem 275:15082–15089Google Scholar
  100. Faik A, Price NJ, Raikhel NV, Keegstra K (2002) An Arabidopsis gene encoding an alpha-xylosyltransferase involved in xyloglucan biosynthesis. Proc Natl Acad Sci U S A 99:7797–7802Google Scholar
  101. Faik A, Jiang N, Held M (2013) Xylan biosynthesis in plants, simply complex. In: Carpita NC, Buckeridge MS, McCann MC (eds) Plants and bioenergy. Springer, New York, pp 153–181Google Scholar
  102. Farrokhi N, Burton RA, Brownfield L, Hrmova M, Wilson SM, Bacic A, Fincher GB (2006) Plant cell wall biosynthesis: genetic, biochemical and functional genomics approaches to the identification of key genes. Plant Biotechnol J 4:145–167Google Scholar
  103. Fincher GB (2009a) Revolutionary times in our understanding of cell wall biosynthesis and remodeling in the grasses. Plant Physiol 149:27–37Google Scholar
  104. Fincher GB (2009b) Exploring the evolution of (1,3;1,4)-beta-d-glucans in plant cell walls: comparative genomics can help! Curr Opin Plant Biol 12:140–147Google Scholar
  105. Fincher GB, Stone BA (2004) Chemistry of nonstarch polysaccharides. In: Wrigley C, Corke H, Walker CE (eds) Encyclopedia of grain science. Elsevier, Oxford, pp 206–222Google Scholar
  106. Fincher GB, Lock PA, Morgan MM, Lingelbach K, Wettenhall RE, Mercer JF, Brandt A, Thomsen KK (1986) Primary structure of the (1→3,1→4)-beta-d-glucan 4-glucohydrolase from barley aleurone. Proc Natl Acad Sci U S A 83:2081–2085Google Scholar
  107. Freemont PS (2000) Ubiquitination: RING for destruction? Curr Biol 10:R84–R87Google Scholar
  108. Fry SC, York WS, Albersheim P, Darvill A, Hayashi T, Joseleau JP, Kato Y, Lorences EP, Maclachlan GA, McNeil M, Mort AJ, Reid JSG, Seitz HU, Selvendran RR, Voragen AGJ, White AR (1993) An unambiguous nomenclature for xyloglucan- derived oligosaccharides. Physiol Plant 89:1–3Google Scholar
  109. Fujiwara H, Tanaka Y, Yonekura-Sakakibara K, Fukuchi-Mizutani M, Nakao M, Fukui Y, Yamaguchi M, Ashikari T, Kusumi T (1998) cDNA cloning, gene expression and subcellular localization of anthocyanin 5-aromatic acyltransferase from Gentiana triflora. Plant J 16:421–431Google Scholar
  110. Galletti R, Denoux C, Gambetta S, Dewdney J, Ausubel FM, De Lorenzo G, Ferrari S (2008) The AtrbohD-mediated oxidative burst elicited by oligogalacturonides in Arabidopsis is dispensable for the activation of defense responses effective against Botrytis cinerea. Plant Physiol 148:1695–1706Google Scholar
  111. Gardiner JC, Taylor NG, Turner SR (2003) Control of cellulose synthase complex localization in developing xylem. Plant Cell 15:1740–1748Google Scholar
  112. Gebert M, Dresselhaus T, Sprunck S (2008) F-actin organization and pollen tube tip growth in Arabidopsis are dependent on the gametophyte-specific Armadillo repeat protein ARO1. Plant Cell 20:2798–2814Google Scholar
  113. Geshi N, Johansen JN, Dilokpimol A, Rolland A, Belcram K, Verger S, Kotake T, Tsumuraya Y, Kaneko S, Tryfona T, Dupree P, Scheller HV, Höfte H, Mouille G (2013) A galactosyltransferase acting on arabinogalactan protein glycans is essential for embryo development in Arabidopsis. Plant J 76:128–137Google Scholar
  114. Gibeaut DM, Carpita NC (1991) Tracing cell wall biogenesis in intact cells and plants: selective turnover and alteration of soluble and cell wall polysaccharides in grasses. Plant Physiol 97:551–561Google Scholar
  115. Gibeaut DM, Carpita NC (1993) Synthesis of (1–>3), (1–>4)-beta-d-glucan in the Golgi apparatus of maize coleoptiles. Proc Natl Acad Sci U S A 90:3850–3854Google Scholar
  116. Gibeaut DM, Pauly M, Bacic A, Fincher GB (2005) Changes in cell wall polysaccharides in developing barley (Hordeum vulgare) coleoptiles. Planta 221:729–738Google Scholar
  117. Giddings TH, Brower DL, Staehelin LA (1980) Visualization of particle complexes in the plasma membrane of Micrasterias denticulata associated with the formation of cellulose fibrils in primary and secondary cell walls. J Cell Biol 84:327–339Google Scholar
  118. Gille S, Pauly M (2012) O-acetylation of plant cell wall polysaccharides. Front Plant Sci 3:12Google Scholar
  119. Gille S, Hänsel U, Ziemann M, Pauly M (2009) Identification of plant cell wall mutants by means of a forward chemical genetic approach using hydrolases. Proc Natl Acad Sci U S A 106:14699–14704Google Scholar
  120. Gille S, de Souza A, Xiong GY, Benz M, Cheng K, Schultink A, Reca IB, Pauly M (2011) O-acetylation of Arabidopsis hemicellulose xyloglucan requires AXY4 or AXY4L, proteins with a TBL and DUF231 domain. Plant Cell 23:4041–4053Google Scholar
  121. Gille S, Sharma V, Baidoo EEK, Keasling JD, Scheller HV, Pauly M (2013) Arabinosylation of a yariv-precipitable cell wall polymer impacts plant growth as exemplified by the Arabidopsis glycosyltransferase mutant ray1. Mol Plant 6:1369–1372Google Scholar
  122. Glaser L, Brown DH (1957) The synthesis of chitin in cell-free extracts of Neurospora crassa. J Biol Chem 228:729–742Google Scholar
  123. Goicoechea M, Lacombe E, Legay S, Mihaljevic S, Rech P, Jauneau A, Lapierre C, Pollet B, Verhaegen D, Chaubet-Gigot N, Grima-Pettenati J (2005) EgMYB2, a new transcriptional activator from Eucalyptus xylem, regulates secondary cell wall formation and lignin biosynthesis. Plant J 43:553–567Google Scholar
  124. Gordon R, Maclachlan G (1989) Incorporation of UDP-[14C]glucose into xyloglucan by Pea membranes. Plant Physiol 91:373–378Google Scholar
  125. Goubet F, Council LN, Mohnen D (1998) Identification and partial characterization of the pectin methyltransferase “homogalacturonan-methyltransferase” from membranes of tobacco cell suspensions. Plant Physiol 116:337–347Google Scholar
  126. Goubet F, Misrahi A, Park SK, Zhang Z, Twell D, Dupree P (2003) AtCSLA7, a cellulose synthase-like putative glycosyltransferase, is important for pollen tube growth and embryogenesis in Arabidopsis. Plant Physiol 131:547–557Google Scholar
  127. Gu Y, Somerville C (2010) Cellulose synthase interacting protein. Plant Signal Behav 5:1571–1574Google Scholar
  128. 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. Proc Natl Acad Sci U S A 107:12866–12871Google Scholar
  129. Guerriero G, Fugelstad J, Bulone V (2010) What do we really know about cellulose biosynthesis in higher plants? J Int Plant Biol 52:161–175Google Scholar
  130. Gutierrez R, Lindeboom JJ, Paredez AR, Emons AM, Ehrhardt DW (2009) Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat Cell Biol 11:797–806Google Scholar
  131. Haigler CH, Brown RM Jr (1986) Transport of rosettes from the Golgi apparatus to the plasma membrane in isolated mesophyll cells of Zinnia elegans during differentiation to tracheary elements in suspension culture. Protoplasma 134:111–120Google Scholar
  132. Haigler CH, Ivanova-Datcheva M, Hogan PS, Salnikov VV, Hwang S, Martin K, Delmer DP (2001) Carbon partitioning to cellulose synthesis. Plant Mol Biol 47:29–51Google Scholar
  133. Haigler CH, Grimson MJ, Gervais J, Le Moigne N, Höfte H, Monasse B, Navard P (2014) Molecular modeling and imaging of initial stages of cellulose fibril assembly: evidence for a disordered intermediate stage. PLoS One 9:e93981Google Scholar
  134. Hantus S, Pauly M, Darvill AG, Albersheim P, York WS (1997) Structural characterization of novel l-galactose-containing oligosaccharide subunits of jojoba seed xyloglucans. Carbohydr Res 304:11–20Google Scholar
  135. Harholt J, Jensen JK, Verhertbruggen Y, Sogaard C, Bernard S, Nafisi M, Poulsen CP, Geshi N, Sakuragi Y, Driouich A, Knox JP, Scheller HV (2012) ARAD proteins associated with pectic Arabinan biosynthesis form complexes when transiently overexpressed in planta. Planta 236:115–128Google Scholar
  136. Harpaz-Saad S, Mcfarlane HE, Xu S, Divi UK, Forward B, Western TL, Kieber JJ (2011) Cellulose synthesis via the FEI2 RLK/SOS5 pathway and cellulose synthase 5 is required for the structure of seed coat mucilage in Arabidopsis. Plant J 68:941–953Google Scholar
  137. Harris D, Bulone V, Ding SY, DeBolt S (2010) Tools for cellulose analysis in plant cell walls. Plant Physiol 153:420–426Google Scholar
  138. Hart DA, Kindel PK (1970) A novel reaction involved in the degradation of apiogalacturonans from Lemna minor and the isolation of apiobiose as a product. Biochemistry 9:2190–2196Google Scholar
  139. Hayashi H (1989) Xyloglucans in the primary cell wall. Annu Rev Plant Physiol Plant Mol Biol 40:139–168Google Scholar
  140. Hayashi T, Maclachlan G (1984) Pea xyloglucan and cellulose : I. Macromolecular organization. Plant Physiol 75:596–604Google Scholar
  141. Hayashi T, Marsden MP, Delmer DP (1987) Pea xyloglucan and cellulose: VI. Xyloglucan-cellulose interactions in vitro and in vivo. Plant Physiol 83:384–389Google Scholar
  142. Hazen SP, Scott-Craig JS, Walton JD (2002) Cellulose synthase-like genes of rice. Plant Physiol 128:336–340Google Scholar
  143. Held MA, Tan L, Kamyab A, Hare M, Shpak E, Kieliszewski MJ (2004) Di-isodityrosine is the intermolecular cross-link of isodityrosine-rich extensin analogs cross-linked in vitro. J Biol Chem 279:55474–55482Google Scholar
  144. Held MA, Penning B, Brandt AS, Kessans SA, Yong W, Scofield SR, Carpita NC (2008) Small-interfering RNAs from natural antisense transcripts derived from a cellulose synthase gene modulate cell wall biosynthesis in barley. Proc Natl Acad Sci U S A 105:20534–20539Google Scholar
  145. Held MA, Be E, Zemelis S, Withers S, Wilkerson C, Brandizzi F (2011) CGR3: a Golgi-localized protein influencing homogalacturonan methylesterification. Mol Plant 4:832–844Google Scholar
  146. Henry RJ, Stone BA (1982) Factors influencing beta-glucan synthesis by particulate enzymes from suspension-cultured Lolium multiflorum endosperm cells. Plant Physiol 69:632–636Google Scholar
  147. Herth W (1985) Plasma-membrane rosettes involved in localized wall thickening during xylem vessel formation of Lepidium sativum L. Planta 164:12–21Google Scholar
  148. Hochholdinger F, Wen TJ, Zimmermann R, Chimot-Marolle P, da Costa e Silva O, da Costa e Silva O, Bruce W, Lamkey KR, Wienand PS, Schnable U (2008) The maize (Zea mays L.) roothairless 3 gene encodes a putative GPI-anchored, monocot-specific, COBRA-like protein that significantly affects grain yield. Plant J 54:888–898Google Scholar
  149. Hoffman M, Jia ZH, Pena MJ, Cash M, Harper A, Blackburn AR, Darvill A, York WS (2005) Structural analysis of xyloglucans in the primary cell walls of plants in the subclass Asteridae. Carbohydr Res 340:1826–1840Google Scholar
  150. Holland N, Holland D, Helentjaris T, Dhugga KS, Xoconostle-Cazares B, Delmer DP (2000) A comparative analysis of the plant cellulose synthase (CesA) gene family. Plant Physiol 123:1313–1324Google Scholar
  151. Hong JC, Nagao RT, Key JL (1989) Developmentally regulated expression of soybean proline-rich cell wall protein genes. Plant Cell 1:937–943Google Scholar
  152. Imamura T, Watanabe T, Kuwahara M, Koshijima T (1994) Ester linkages between lignin and glucuronic acid in lignin-carbohydrate complexes from Fagus crenata. Phytochemistry 37:1165–1173Google Scholar
  153. Ishii T (1997) O-acetylated oligosaccharides from pectins of potato tuber cell walls. Plant Physiol 113:1265–1272Google Scholar
  154. Ishii T, Matsunaga T (1996) Isolation and characterization of a boron-rhamnogalacturonan-II complex from cell walls of sugar beet pulp. Carbohydr Res 284:1–9Google Scholar
  155. Ishii T, Matsunaga T, Pellrin P, O'Neill MA, Darvill A, Albershiem P (1999) The plant cell wall polysaccharide rhamnogalacturonan II self-assembles into a covalently cross-linked dimer. J Biol Chem 274:13098–13104Google Scholar
  156. Iwai H, Masaoka N, Ishii T, Satoh S (2002) A pectin glucuronosyltransferase gene is essential for intracellular attachment in the plant meristem. Proc Natl Acad Sci U S A 99:16319–16324Google Scholar
  157. Izdorczyk M, Biliaderis C (1995) Cereal arabinoxylan: advances in structure and physicochemical properties. Carbohydr Polym 28:33–48Google Scholar
  158. Jacob-Wilk D, Kurek I, Hogan P, Delmer DP (2006) The cotton fiber zinc-binding domain of cellulose synthase A1 from Gossypium hirsutum displays rapid turnover in vitro and in vivo. Proc Natl Acad Sci U S A 103:12191–12196Google Scholar
  159. Jarvis MC (1984) Structure and properties of pectin gels in plant cell walls. Plant Cell Environ 7:153–164Google Scholar
  160. Jensen JK, Sørensen SO, Harholt J, Geshi N, Sakuragi Y, Møller I, Zandleven J, Bernal AJ, Jensen NB, Sørensen C, Pauly M, Beldman G, Willats WGT, Scheller HV (2008) Identification of a xylogalacturonan xylosyltransferase involved in pectin biosynthesis in Arabidopsis. Plant Cell 18:2593–2607Google Scholar
  161. Jia Z, Cash M, Darvill AG, York WS (2005) NMR characterization of endogenously O-acetylated oligosaccharides isolated from tomato (Lycopersicon esculentum) xyloglucan. Carbohydr Res 340:1818–1825Google Scholar
  162. Jing W, DeAngelis PL (2000) Dissection of the two transferase activities of the Pasteurella multocida hyaluronan synthase: two active sites exist in one polypeptide. Glycobiology 10:883–889Google Scholar
  163. Johansson MH, Samuelson O (1977) Reducing end groups in birch xylan and their alkaline degradation. Wood Sci Technol 11:251–263Google Scholar
  164. Joshi CP, Bhandari S, Ranjan P, Kalluri UC, Liang X, Fujino T, Samuga A (2004) Genomics of cellulose biosynthesis in poplars. New Phytol 164:53–61Google Scholar
  165. Kauppinen S, Christgau S, Kofod LV, Halkier T, Dörreich K, Dalbøge H (1995) Molecular cloning and characterization of a rhamnogalacturonan acetylesterase from Aspergillus aculeatus. J Biol Chem 270:27172–27178Google Scholar
  166. Keegstra K, Raikhel N (2001) Plant glycosyltransferases. Curr Opin Plant Biol 4:219–224Google Scholar
  167. Keegstra K, Talmadge KW, Bauer WD, Albersheim P (1973) The structure of plant cell walls: III. A model of the walls of suspension-cultured sycamore cells based on the interconnections of the macromolecular components. Plant Physiol 51:188–197Google Scholar
  168. Keenan MHJ, Belton PS, Matthew JA, Howson SJ (1985) A 13C-n.m.r. study of sugar beet pectin. Carbohydr Res 138:168–170Google Scholar
  169. Kennedy CJ, Cameron GJ, Šturcová A, Apperley DC, Altaner C, Wess TJ, Jarvis MC (2007) Microfibril diameter in celery collenchyma cellulose: x-ray scattering and NMR evidence. Cellulose 14:235–246Google Scholar
  170. Kiefer LL, York WS, Darvill AG, Albersheim P (1989) Xyloglucan isolated from suspension-cultured sycamore cell walls is O-acetylated. Phytochemistry 28:2105–2107Google Scholar
  171. Kieliszewski MJ, Lamport DTA (1994) Extensin: repetitive motifs, functional sites, post-translational codes, and phylogeny. Plant J 5:157–172Google Scholar
  172. Kim WC, Ko JH, Kim JY, Kim JM, Bae HJ, Han KH (2013) MYB46 directly regulates the gene expression of secondary wall-associated cellulose synthases in Arabidopsis. Plant J 73:26–36Google Scholar
  173. Kimura S, Laosinchai W, Itoh T, Cui XJ, Linder CR, Brown RM Jr (1999) Immunogold labeling of rosette terminal cellulose-synthesizing complexes in the vascular plant Vigna angularis. Plant Cell 11:2075–2085Google Scholar
  174. Kjellbom P, Snogerup L, Stöhr C, Reuzeau C, McCabe PF, Pennell RI (1997) Oxidative cross-linking of plasma membrane arabinogalactan proteins. Plant J 12:1189–1196Google Scholar
  175. Knoch E, Dilokpimol A, Tryfona T, Poulsen CP, Xiong G, Harholt J, Petersen BL, Ulvskov P, Hadi MZ, Kotake T, Tsumuraya Y, Pauly M, Dupree P, Geshi N (2013) A beta-glucuronosyltransferase from Arabidopsis thaliana involved in biosynthesis of type II arabinogalactan has a role in cell elongation during seedling growth. Plant J 76:1016–1029Google Scholar
  176. Knoch E, Dilokpimol A, Geshi N (2014) Arabinogalactan proteins: focus on carbohydrate active enzymes. Front Plant Sci 11:198Google Scholar
  177. Komalavilas P, Mort AJ (1989) The acetylation at O-3 of GalA in the rhamnose-rich portion of pectins. Carbohydr Res 189:261–272Google Scholar
  178. Konishi T, Takeda T, Miyazaki Y, Ohnishi-Kameyama M, Hayashi T, O'Neill MA, Ishii T (2007) A plant mutase that interconverts UDP-arabinofuranose and UDP-arabinopyranose. Glycobiology 17:345–354Google Scholar
  179. Kouwijzer M, Schols HA, PeÂrez S (1996) Acetylation of rhamnogalacturonan I and homogalacturonan: theoretical calculations. In: Visser J, Voragen AGJ (eds) Pectins and pectinases. Elsevier Science, Amsterdam, pp 57–65Google Scholar
  180. Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, Fukuda H, Demura T (2005) Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 19:1855–1860Google Scholar
  181. Kulkarni AR, Pena MJ, Avci U, Mazumder K, Urbanowicz BR, Pattathil S, Yin Y, O'Neill MA, Roberts AW, Hahn MG, Xu Y, Darvill AG, York WS (2012) The ability of land plants to synthesize glucuronoxylans predates the evolution of tracheophytes. Glycobiology 22:439–451Google Scholar
  182. Kurek I, Kawagoe Y, Jacob-Wilk D, Doblin M, Delmer D (2002) Dimerization of cotton fiber cellulose synthase catalytic subunits occurs via oxidation of the zinc-binding domains. Proc Natl Acad Sci U S A 99:11109–11114Google Scholar
  183. Lairson LL, Henrissat B, Davies GJ, Withers SG (2008) Glycosyltransferases: structures, functions, and mechanisms. Annu Rev Biochem 77:521–555Google Scholar
  184. Lane DR, Wiedemeier A, Peng L, Höfte H, Vernhettes S, Desprez T, Hocart CH, Birch RJ, Baskin TI, Burn JE, Arioli T, Betzner AS, Williamson RE (2001) Temperature-sensitive alleles of RSW2 link the KORRIGAN endo-1, 4-beta-glucanase to cellulose synthesis and cytokinesis in Arabidopsis. Plant Physiol 126:278–288Google Scholar
  185. Lau JM, McNeil M, Darvill AG, Albersheim P (1985) Structure of the backbone of rhamnogalacturonan I, a pectic polysaccharide in the primary cell walls of plants. Carbohydr Res 137:111–125Google Scholar
  186. Lee S, Choi H, Suh S, Doo IS, Oh KY, Choi EJ, Schroeder Taylor AT, Low PS, Lee Y (1999) Oligogalacturonic acid and chitosan reduce stomatal aperture by inducing the evolution of reactive oxygen species from guard cells of tomato and Commelina communis. Plant Physiol 121:147–152Google Scholar
  187. Lee C, Teng Q, Huang W, Zhong R, Ye ZH (2009) Down-regulation of PoGT47C expression in poplar results in a reduced glucuronoxylan content and an increased wood digestibility by cellulase. Plant Cell Physiol 50:1075–1089Google Scholar
  188. Lee C, Teng Q, Zhong R, Ye ZH (2011) The four Arabidopsis reduced wall acetylation genes are expressed in secondary wall-containing cells and required for the acetylation of xylan. Plant Cell Physiol 52:1289–1301Google Scholar
  189. Lee C, Teng Q, Zhong R, Yuan Y, Haghighat M, Ye ZH (2012) Three Arabidopsis DUF579 domain-containing GXM proteins are methyltransferases catalyzing 4-O-methylation of glucuronic acid on xylan. Plant Cell Physiol 53:1934–1949Google Scholar
  190. Lei L, Li S, Gu Y (2012) Cellulose synthase complexes: composition and regulation. Front Plant Sci 3:75Google Scholar
  191. Lerouge P, O'Neill MA, Darvill AG, Albersheim P (1993) Structural characterization of endo-glycanase-generated oligoglycosyl side chains of rhamnogalacturonan I. Carbohydr Res 243:359–371Google Scholar
  192. Li Y, Qian Q, Zhou Y, Yan M, Sun L, Zhang M, Fu Z, Wang Y, Han B, Pang X, Chen M, Li J (2003) BRITTLE CULM1, which encodes a COBRA-like protein, affects the mechanical properties of rice plants. Plant Cell 15:2020–2031Google Scholar
  193. Li X, Cordero I, Caplan J, Mølhøj M, Reiter WD (2004) Molecular analysis of 10 coding regions from Arabidopsis that are homologous to the MUR3 xyloglucan galactosyltransferase. Plant Physiol 134:940–950Google Scholar
  194. Liang Y, Basu D, Pattathil S, Xu W-L, Venetos A, Martin SL, Faik A, Hahn MG, Showalter AM (2013) Biochemical and physiological characterization of fut4 and fut6 mutants defective in arabinogalactan-protein fucosylation in Arabidopsis. J Exp Bot 64:5537–5551Google Scholar
  195. 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 102:2221–2226Google Scholar
  196. Liwanag AJM, Ebert B, Verhertbruggen Y, Rennie EA, Rautengarten C, Oikawa A, Andersen MC, Clausen MH, Scheller HV (2012) Pectin biosynthesis: GALS1 in Arabidopsis thaliana is a β-1,4-galactan β-1,4-galactosyltransferase. Plant Cell 24:5024–5036Google Scholar
  197. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2014) The Carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490–D495Google Scholar
  198. Longland JM, Fry SC, Trewavas AJ (1989) Developmental control of apiogalacturonan biosynthesis and UDP-apiose production in a duckweed. Plant Physiol 90:972–976Google Scholar
  199. Madson M, Dunand C, Li X, Verma R, Vanzin GF, Caplan J, Shoue DA, Carpita NC, Reiter WD (2003) The MUR3 gene of Arabidopsis encodes a xyloglucan galactosyltransferase that is evolutionarily related to animal exostosins. Plant Cell 15:662–1670Google Scholar
  200. Manabe Y, Nafisi M, Verhertbruggen Y, Orfila C, Gille S, Rautengarten C, Cherk C, Marcus SE, Somerville S, Pauly M, Knox JP, Sakuragi Y, Scheller HV (2011) Loss-of-function mutation of REDUCED WALL ACETYLATION2 in Arabidopsis leads to reduced cell wall acetylation and increased resistance to Botrytis cinerea. Plant Physiol 155:1068–1078Google Scholar
  201. Manabe Y, Verhertbruggen Y, Gille S, Harholt J, Chong S-L, Pawar PM-A, Mellerowicz EJ, Tenkanen M, Cheng K, Pauly M, Scheller HV (2013) RWA proteins play vital and distinct roles in cell wall O-acetylation in Arabidopsis thaliana. Plant Physiol 163:1107–1117Google Scholar
  202. Matsunaga T, Ishii T, Matsumoto S, Higuchi M, Darvill AG, Albersheim P, O'Neill MA (2004) Occurrence of the primary cell wall polysaccharide rhamnogalacturonan II in pteridophytes, lycophytes, and bryophytes. Implications for the evolution of vascular plants. Plant Physiol 134:339–351Google Scholar
  203. McCann MC, Defernez M, Urbanowicz BR, Tewari JC, Langewisch T, Olek A, Wells B, Wilson RH, Carpita NC (2007) Neural network analyses of infrared spectra for classifying cell wall architectures. Plant Physiol 143:1314–1326Google Scholar
  204. McClendon JH (1964) Evidence for the pectic nature of the middle lamella of potato tuber cell walls based on chromatography of macerating enzymes. Am J Bot 51:628–633Google Scholar
  205. McDougall GJ, Fry SC (1994) Fucosylated xyloglucan in suspension-cultured cells of the graminaceous monocotyledon, Festuca arundinacea. J Plant Physiol 143:591–595Google Scholar
  206. McNeil M, Darvill AG, Albersheim P (1980) Structure of plant cell walls: X. Rhamnogalacturonan I, a structurally complex pectic polysaccharide in the walls of suspension-cultured sycamore cells. Plant Physiol 66:1128–1134Google Scholar
  207. McNeil M, Darvill AG, Fry SC, Albersheim P (1984) Structure and function of the primary cell walls of plants. Annu Rev Biochem 53:625–663Google Scholar
  208. Mendu V, Griffiths J, Persson S, Stork J, Downie B, Voiniciuc C, Haughn G, Debolt S (2011) Subfunctionalization of cellulose synthases in seed coat epidermal cells mediate secondary radial wall synthesis and mucilage attachment. Plant Physiol 157:441–453Google Scholar
  209. Mohnen D (2008) Pectin structure and biosynthesis. Curr Opin Plant Biol 11:266–277Google Scholar
  210. Moller I, Sørensen I, Bernal AJ, Blaukopf C, Lee K, Øbro J, Pettolino F, Roberts A, Mikkelsen JD, Knox JP, Bacic A, Willats WG (2007) High-throughput mapping of cell-wall polymers within and between plants using novel microarrays. Plant J 50:1118–1128Google Scholar
  211. Moreira LR, Filho EX (2008) An overview of mannan structure and mannan-degrading enzyme systems. Appl Microbiol Biotechnol 79:165–178Google Scholar
  212. Morgan JL, Strumillo J, Zimmer J (2013) Crystallographic snapshot of cellulose synthesis and membrane translocation. Nature 493:181–186Google Scholar
  213. Mortimer JC, Miles GP, Brown DM, Zhang ZN, Segura MP, Weimar T, Yu XL, Seffen KA, Stephens E, Turner SR, Dupree P (2010) Absence of branches from xylan in Arabidopsis gux mutants reveals potential for simplification of lignocellulosic biomass. Proc Natl Acad Sci U S A 107:17409–17414Google Scholar
  214. Mouille G, Robin S, Lecomte M, Pagant S, Höfte H (2003) Classification and identification of Arabidopsis cell wall mutants using Fourier-Transform InfraRed (FTIR) microspectroscopy. Plant J 35:393–404Google Scholar
  215. Mouille G, Ralet MC, Cavelier C, Eland C, Effroy D, Hématy K, McCartney L, Truong HN, Gaudon V, Thibault JF, Marchant A, Höfte H (2007) Homogalacturonan synthesis in Arabidopsis thaliana requires a Golgi-localized protein with a putative methyltransferase domain. Plant J 50:605–614Google Scholar
  216. Mueller SC, Brown RM (1980) Evidence for an intramembrane component associated with a cellulose microfibril-synthesizing complex in higher plants. J Cell Biol 84:315–326Google Scholar
  217. Mutwil M, Debolt S, Persson S (2008) Cellulose synthesis: a complex complex. Curr Opin Plant Biol 11:252–257Google Scholar
  218. Nakamura A, Furuta H, Maeda H, Takao T, Nagamatsu Y (2002) Structural studies by stepwise enzymatic degradation of the main backbone of soybean soluble polysaccharides consisting of galacturonan and rhamnogalacturonan. Biosci Biotechnol Biochem 66:1301–1313Google Scholar
  219. Newman RH, Hill SJ, Harris PJ (2013) Wide-angle x-ray scattering and solid-state nuclear magnetic resonance data combined to test models for cellulose microfibrils in mung bean cell walls. Plant Physiol 163:1558–1567Google Scholar
  220. Nicol F, His I, Jauneau A, Vernhettes S, Canut H, Höfte H (1998) A plasma membrane-bound putative endo-1,4-beta-d-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. EMBO J 17:5563–5576Google Scholar
  221. Nühse TS, Stensballe A, Jensen ON, Peck SC (2004) Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database. Plant Cell 16:2394–2405Google Scholar
  222. O’Neill MA, York WS (2003) The composition and structure of plants primary cell walls. In: Rose JKC (ed) The plant cell wall. Blackwell, Oxford, pp 1–54Google Scholar
  223. Ogawa-Ohnishi M, Matsushita W, Matsubayashi Y (2013) Identification of three hydroxyproline O-arabinosyltransferases in Arabidopsis thaliana. Nat Chem Biol 9:726–730Google Scholar
  224. Oikawa A, Joshi HJ, Rennie EA, Ebert B, Manisseri C, Heazlewood JL, Scheller HV (2010) An integrative approach to the identification of Arabidopsis and rice genes involved in xylan and secondary wall development. PLoS One 5:e15481Google Scholar
  225. Olek AT, Rayon C, Makowski L, Kim HR, Ciesielski P, Badger J, Paul LN, Ghosh S, Kihara D, Crowley M, Himmel ME, Bolin JT, Carpita NC (2014) The structure of the catalytic domain of a plant cellulose synthase and its assembly into dimers. Plant Cell 26:2996–3009, tpc:114Google Scholar
  226. O'Neill MA, Warrenfeltz D, Kates K, Pellerin P, Doco T, Darvill AG, Albersheim P (1996) Rhamnogalacturonan II, a pectic polysaccharide in the walls of growing plant cell, forms a dimmer that is covalently cross-linked by a borate ester. In vitro conditions for the formation and hydrolysis of the dimmer. J Biol Chem 271:22923–22930Google Scholar
  227. O'Neill MA, Eberhard S, Albersheim P, Darvill A (2001) Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth. Science 294:846–849Google Scholar
  228. O'Neill MA, Ishii T, Albersheim P, Darvill AG (2004) Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide. Annu Rev Plant Biol 55:109–139Google Scholar
  229. Osawa T, Sugiura N, Shimada H, Hirooka R, Tsuji A, Shirakawa T, Fukuyama K, Kimura M, Kimata K, Kakuta Y (2009) Crystal structure of chondroitin polymerase from Escherichia coli K4. Biochem Biophys Res Commun 378:10–14Google Scholar
  230. Osorio S, Castillejo C, Quesada MA, Medina-Escobar N, Brownsey GJ, Suau R, Heredia A, Botella MA, Valpuesta V (2008) Partial demethylation of oligogalacturonides by pectin methyl esterase 1 is required for eliciting defence responses in wild strawberry (Fragaria vesca). Plant J 54:43–55Google Scholar
  231. Ovodova RG, Golovchenko VV, Shashkov AS, Popov SV, Ovodov YS (2000) Structural studies and physiological activity of lemnan, a pectin from Lemna minor L. Russ J Bioorg Chem 26:669–676Google Scholar
  232. Ozawa M, Baribault H, Kemler R (1989) The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. EMBO J 8:1711–1717Google Scholar
  233. Pagant S, Bichet A, Sugimoto K, Lerouxel O, Desprez T, McCann M, Lerouge P, Vernhettes S, Höfte H (2002) KOBITO1 encodes a novel plasma membrane protein necessary for normal synthesis of cellulose during cell expansion in Arabidopsis. Plant Cell 14:2001–2013Google Scholar
  234. Paredez AR, Somerville CR, Ehrhardt DW (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312:1491–1495Google Scholar
  235. Pauly M, Scheller HV (2000) O-acetylation of plant cell wall polysaccharides: identification and partial characterization of a rhamnogalacturonan O-acetyl transferase from potato suspension-cultured cells. Planta 210:659–667Google Scholar
  236. Pauly M, Qin Q, Greene H, Albersheim P, Darvill A, York WS (2001) Changes in the structure of xyloglucan during cell elongation. Planta 212:842–850Google Scholar
  237. Pear JR, Kawagoe Y, Schreckengost WE, Delmer DP, Stalker DM (1996) Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase. Proc Natl Acad Sci U S A 93:12637–12642Google Scholar
  238. Peaucelle A, Braybrook S, Hofte H (2012) Cell wall mechanics and growth control in plants: the role of pectins revisited. Front Plant Sci 3:121Google Scholar
  239. Pena MJ, Zhong R, Zhou GK, Richardson EA, O'Neill MA, Darvill AG, York WS, Ye ZH (2007) Arabidopsis irregular xylem8 and irregular xylem9: implications for the complexity of glucuronoxylan biosynthesis. Plant Cell 19:549–563Google Scholar
  240. Pena MJ, Darvill AG, Eberhard S, York WS, O'Neill MA (2008) Moss and liverwort xyloglucans contain galacturonic acid and are structurally distinct from the xyloglucans synthesized by hornworts and vascular plants. Glycobiology 18:891–904Google Scholar
  241. Pena MJ, Kong Y, York WS, O'Neill MA (2012) A galacturonic acid-containing xyloglucan is involved in Arabidopsis root hair tip growth. Plant Cell 24:4511–4524Google Scholar
  242. Penning BW, Hunter CT 3rd, Tayengwa R, Eveland AL, Dugard CK, Olek AT, Vermerris W, Koch KE, McCarty DR, Davis MF, Thomas SR, McCann MC, Carpita NC (2009) Genetic resources for maize cell wall biology. Plant Physiol 151:1703–1728Google Scholar
  243. Perrin RM, DeRocher AE, Bar-Peled M, Zeng W, Norambuena L, Orellana A, Raikhel V, Keegstra K (1999) Xyloglucan fucosyltransferase, an enzyme involved in plant cell wall biosynthesis. Science 284:1976–1979Google Scholar
  244. Perrin RM, Jia Z, Wagner TA, O'Neill MA, Sarria R, York WS, Raikhel NV, Keegstra K (2003) Analysis of xyloglucan fucosylation in Arabidopsis. Plant Physiol 132:768–778Google Scholar
  245. Perrone P, Hewage CM, Thomson AR, Bailey K, Sadler IH, Fry SC (2002) Patterns of methyl and O-acetyl esterification in spinach pectins: new complexity. Phytochemistry 60:67–77Google Scholar
  246. Persson S, Wei H, Milne J, Page GP, Somerville CR (2005) Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. Proc Natl Acad Sci U S A 102:8633–8638Google Scholar
  247. Persson S, Paredez A, Carroll A, Palsdottir H, Doblin M, Poindexter P, Khitrov N, Auer M, Somerville CR (2007) Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proc Natl Acad Sci U S A 104:15566–15571Google Scholar
  248. Pippen EL, McCready RM, Owens HS (1950) Gelation properties of partially acetylated pectins. J Am Chem Soc 72:813–816Google Scholar
  249. Piston F, Uauy C, Fu L, Langston J, Labavitch J, Dubcovsky J (2010) Down-regulation of four putative arabinoxylan feruloyltransferase genes from family PF02458 reduces ester-linked ferulate content in rice cell walls. Planta 231:677–691Google Scholar
  250. Popper ZA (2008) Evolution and diversity of green plant cell walls. Curr Opin Plant Biol 11:286–292Google Scholar
  251. Popper ZA, Fry SC (2003) Primary cell wall composition of bryophytes and charophytes. Ann Bot 91:1–12Google Scholar
  252. Qi X, Behrens BX, West PR, Mort AJ (1995) Solubilization and partial characterization of extensin fragments from cell walls of cotton suspension cultures: evidence for a covalent cross-link between extensin and pectin. Plant Physiol 108:1691–1701Google Scholar
  253. Qu Y, Egelund J, Gilson PR, Houghton F, Gleeson PA, Schultz CJ, Bacic A (2008) Identification of a novel group of putative Arabidopsis thaliana beta-(1,3)-galactosyltransferases. Plant Mol Biol 68:43–59Google Scholar
  254. Ralet MC, Crepeau MJ, Buchholt HC, Tibault JF (2003) Polyelectrolyte behaviour and calcium binding properties of sugar beet pectins differing in their degrees of methylation and acetylation. Biochem Eng J 16:191–201Google Scholar
  255. Ralet MC, Cabrera JC, Bonnin E, Quemener B, Hellin P, Thibault JF (2005) Mapping sugar beet pectin acetylation pattern. Phytochemistry 66:1832–1843Google Scholar
  256. Ratnayake S, Beahan CT, Callahan DL, Bacic A (2013) The reducing end sequence of wheat endosperm cell wall arabinoxylans. Carbohydr Res 386:23–32Google Scholar
  257. Ray PM (1980) Cooperative action of beta-glucan synthetase and UDP-xylose xylosyl transferase of Golgi membranes in the synthesis of xyloglucan-like polysaccharide. Biochim Biophys Acta 629:431–444Google Scholar
  258. Ray B, Loutelier-Bourhis C, Lange C, Condamine E, Driouich A, Lerouge P (2004) Structural investigation of hemicellulosic polysaccharides from Argania spinosa: characterisation of a novel xyloglucan motif. Carbohydr Res 339:201–208Google Scholar
  259. Renard CC, Jarvis MC (1999) Acetylation and methylation of homogalacturonans 1: optimisation of the reaction and characterization of the products. Carbohydr Polym 39:201–207Google Scholar
  260. Rennie EA, Scheller HV (2014) Xylan biosynthesis. Curr Opin Biotechnol 26:100–107Google Scholar
  261. Rennie EA, Hansen SF, Baidoo EE, Hadi MZ, Keasling JD, Scheller HV (2012) Three members of the Arabidopsis glycosyltransferase family 8 are xylan glucuronosyltransferases. Plant Physiol 159:1408–1417Google Scholar
  262. Richmond TA, Somerville CR (2000) The cellulose synthase superfamily. Plant Physiol 124:495–498Google Scholar
  263. Ridley BL, O'Neill MA, Mohnen D (2001) Pectins: structure, biosynthesis, and oligogalacturonide related signaling. Phytochemistry 57:929–967Google Scholar
  264. Roberts AW, Roberts EM, Delmer DP (2002) Cellulose synthase (CesA) genes in the green alga Mesotaenium caldariorum. Eukaryot Cell 1:847–855Google Scholar
  265. Rombouts FM, Thibault JF (1986) Enzymatic and chemical degradation and the fine structure of pectins from sugar-beet pulp. Carbohydr Res 154:189–203Google Scholar
  266. Roudier F, Schindelman G, DeSalle R, Benfey PN (2002) The COBRA family of putative GPI-anchored proteins in Arabidopsis. A new fellowship in expansion. Plant Physiol 130:538–548Google Scholar
  267. Roudier F, Fernandez AG, Fujita M, Himmelspach R, Borner GH, Schindelman G, Song S, Baskin TI, Dupree P, Wasteneys GO, Benfey PN (2005) COBRA, an Arabidopsis extracellular glycosyl-phosphatidyl inositol-anchored protein, specifically controls highly anisotropic expansion through its involvement in cellulose microfibril orientation. Plant Cell 17:1749–1763Google Scholar
  268. Round AN, Rigby NM, MacDougall AJ, Morris VJ (2010) A new view of pectin structure revealed by acid hydrolysis and atomic force microscopy. Carbohydr Res 345:487–497Google Scholar
  269. Saito F, Suyama A, Oka T, Yoko-O T, Matsuoka K, Jigami Y, Shimma YI (2014) Identification of novel peptidyl serine -galactosyltransferase gene family in plants. J Biol Chem 289:20405–20420Google Scholar
  270. Sato S, Kato T, Kakegawa K, Ishii T, Liu YG, Awano T, Takabe K, Nishiyama Y, Kuga S, Sato S, Nakamura Y, Tabata S, Shibata D (2001) Role of the putative membrane-bound endo-1, 4-beta-glucanase KORRIGAN in cell elongation and cellulose synthesis in Arabidopsis thaliana. Plant Cell Physiol 42:251–263Google Scholar
  271. Saurin AJ, Borden KL, Boddy MN, Freemont PS (1996) Does this have a familiar RING? Trends Biochem Sci 21:208–14Google Scholar
  272. Saxena IM, Lin FC, Brown RM Jr (1990) Cloning and sequencing of the cellulose synthase catalytic subunit gene of Acetobacter xylinum. Plant Mol Biol 15:673–683Google Scholar
  273. Saxena IM, Brown RM Jr, Fevre M, Geremia RA, Henrissat B (1995) Multidomain architecture of beta-glycosyl transferases: implications for mechanism of action. J Bacteriol 177:1419–1424Google Scholar
  274. Saxena IM, Brown RM Jr, Dandekar T (2001) Structure-function characterization of cellulose synthase: relationship to other glycosyltransferases. Phytochemistry 57:1135–1148Google Scholar
  275. Sburlati A, Cabib E (1986) Chitin synthetase 2, a presumptive participant in septum formation in Saccharomyces cerevisiae. J Biol Chem 261:15147–15152Google Scholar
  276. Scheible WR, Eshed R, Richmond T, Delmer D, Somerville CR (2001) Modifications of cellulose synthase confer resistance to isoxaben and thiazolidinone herbicides in Arabidopsis ixr1 mutants. Proc Natl Acad Sci U S A 98:10079–10084Google Scholar
  277. Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289Google Scholar
  278. Schindelman G, Morikami A, Jung J, Baskin TI, Carpita NC, Derbyshire P, McCann MC, Benfey PN (2001) COBRA encodes a putative GPI-anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis. Genes Dev 15:1115–1127Google Scholar
  279. Schols H, Voragen A (1994) Hairy (ramified) regions of pectins occurrence of pectic hairy regions in various plant-cell wall materials and their degradability by rhamnogalacturonase. Carbohydr Res 256:83–95Google Scholar
  280. Schols HA, Geraeds CC, Searle-Van-Leeuwen MF, Kormelink FJ, Voragen AGJ (1990) Rhamnogalacturonase: a novel enzyme that degrades the hairy regions of pectins. Carbohydr Res 206:105–115Google Scholar
  281. Seifert GJ, Roberts K (2007) The biology of arabinogalactan proteins. Annu Rev Plant Biol 58:137–161Google Scholar
  282. Senkhamparn N, Bakx EJ, Verhoef R, Schols HA, Sajjaanantakul T, Voragen AG (2009) Okra pectin contains an unusual substitution of its rhamnosyl residues with acetyl and alpha-linked galactosyl groups. Carbohydr Res 344:1842–1851Google Scholar
  283. Sethaphong L, Haigler CH, Kubicki JD, Zimmer J, Bonetta D, DeBolt S, Yingling YG (2013) Tertiary model of a plant cellulose synthase. Proc Natl Acad Sci U S A 110:7512–7517Google Scholar
  284. Shipp M, Nadella R, Gao H, Farkas V, Sigrist H, Faik A (2008) Glyco-array technology for efficient monitoring of plant cell wall glycosyltransferase activities. Glycoconj J 25(1):49–58Google Scholar
  285. Showalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell 5:9–23Google Scholar
  286. Showalter AM (2001) Arabinogalactan-proteins: structure, expression and function. Cell Mol Life Sci 58:1399–1417Google Scholar
  287. Shpak E, Barbar E, Leykam JF, Kieliszewski MJ (2001) Contiguous hydroxyproline residues direct hydroxyproline arabinosylation in Nicotiana tabacum. J Biol Chem 276:11272–11278Google Scholar
  288. Slabaugh E, Davis JK, Haigler CH, Yingling YG, Zimmer J (2014) Cellulose synthases: new insights from crystallography and modeling. Trends Plant Sci 19:99–106Google Scholar
  289. Somerville C (2006) Cellulose synthesis in higher plants. Annu Rev Cell Dev Biol 22:53–78Google Scholar
  290. St Pierre B, Laflamme P, Alarco AM, De Luca V (1998) The terminal O-acetyltransferase involved in vindoline biosynthesis defines a new class of proteins responsible for coenzyme A dependent acyl transfer. Plant J 14:703–713Google Scholar
  291. Staudte RG, Woodward JR, Fincher GB, Stone BA (1983) Water-soluble (1/3), (1/4)-β-d-glucans from barley (Hordeum vulgare) endosperm III distribution of cellotriosyl and cellotetraosyl residues. Carbohydr Polym 3:299–312Google Scholar
  292. Sterling JD, Atmodjo MA, Inwood SE, Kumar Kolli VS, Quigley HF, Hahn MG, Mohnen D (2006) Functional identification of an Arabidopsis pectin biosynthetic homogalacturonan galacturonosyltransferase. Proc Natl Acad Sci U S A 103:5236–5241Google Scholar
  293. Stevenson TT, Darvill AG, Albersheim P (1988) Structural features of the plant cell-wall polysaccharide rhamnogalacturonan-II. Carbohydr Res 182:207–226Google Scholar
  294. Stork J, Harris D, Griffiths J, Williams B, Beisson F, Li-Beisson Y, Mendu V, Haughn G, DeBolt S (2010) CELLULOSE SYNTHASE9 serves a nonredundant role in secondary cell wall synthesis in Arabidopsis epidermal testa cells. Plant Physiol 153:580–589Google Scholar
  295. Strasser R, Bondili JS, Vavra U, Schoberer J, Svoboda B, Glössl J, Léonard R, Stadlmann J, Altmann F, Steinkellner H, Mach L (2007) A unique beta1,3-galactosyltransferase is indispensable for the biosynthesis of N-glycans containing Lewis a structures in Arabidopsis thaliana. Plant Cell 19:2278–2292Google Scholar
  296. Sugiyama J, Vuong R, Chanzy H (1991) Electron diffraction study on the two crystalline phases occurring in native cellulose from an algal cell wall. Macromolecules 24:4168–4175Google Scholar
  297. Sullivan S, Ralet MC, Berger A, Diatloff E, Bischoff V, Gonneau M, Marion-Poll A, North HM (2011) CESA5 is required for the synthesis of cellulose with a role in structuring the adherent mucilage of Arabidopsis seeds. Plant Physiol 156:1725–1739Google Scholar
  298. Suzuki S, Li L, Sun YH, Chiang VL (2006) The cellulose synthase gene superfamily and biochemical functions of xylem-specific cellulose synthase-like genes in Populus trichocarpa. Plant Physiol 142:1233–1245Google Scholar
  299. Tan L, Showalter AM, Egelund J, Hernandez-Sanchez A, Doblin MS, Bacic A (2012) Arabinogalactan-proteins and the research challenges for these enigmatic plant cell surface proteoglycans. Front Plant Sci 27:140Google Scholar
  300. Tan L, Eberhard S, Pattathil S, Warder C, Glushka J, Yuan C, Hao Z, Zhu X, Avci U, Miller JS, Baldwin D, Pham C, Orlando R, Darvill A, Hahn MG, Kieliszewski MJ, Mohnen D (2013) An Arabidopsis cell wall proteoglycan consists of pectin and arabinoxylan covalently linked to an arabinogalactan protein. Plant Cell 25:270–287Google Scholar
  301. Tanaka K, Murata K, Yamazaki M, Onosato K, Miyao A, Hirochika H (2003) Three distinct rice cellulose synthase catalytic subunit genes required for cellulose synthesis in the secondary wall. Plant Physiol 133:73–83Google Scholar
  302. Taylor NG (2007) Identification of cellulose synthase AtCesA7 (IRX3) in vivo phosphorylation sites-a potential role in regulating protein degradation. Plant Mol Biol 64:161–171Google Scholar
  303. Taylor NG (2008) Cellulose biosynthesis and deposition in higher plants. New Phytol 178:239–252Google Scholar
  304. Taylor NG, Scheible WR, Cutler S, Somerville CR, Turner SR (1999) The irregular xylem3 locus of Arabidopsis encodes a cellulose synthase required for secondary cell wall synthesis. Plant Cell 11:769–779Google Scholar
  305. Taylor NG, Laurie S, Turner SR (2000) Multiple cellulose synthase catalytic subunits are required for cellulose synthesis in Arabidopsis. Plant Cell 12:2529–2539Google Scholar
  306. Taylor NG, Howells RM, Huttly AK, Vickers K, Turner SR (2003) Interactions among three distinct CesA proteins essential for cellulose synthesis. Proc Natl Acad Sci U S A 100:1450–1455Google Scholar
  307. Timmers J, Vernhettes S, Desprez T, Vincken J-P, Visser RGF, Trindade LM (2009) Interactions between membrane-bound cellulose synthases involved in the synthesis of the secondary cell wall. FEBS Lett 583:978–982Google Scholar
  308. Tlapak-Simmons VL, Baron CA, Weigel PH (2004) Characterization of the purified hyaluronan synthase from Streptococcus equisimilis. Biochemistry 43:9234–9242Google Scholar
  309. Tryfona T, Theys TE, Wagner T, Stott K, Keegstra K, Dupree P (2014) Characterisation of FUT4 and FUT6 α-(1→2)-fucosyltransferases reveals that absence of root arabinogalactan fucosylation increases Arabidopsis root growth salt sensitivity. PLoS One 9:e93291Google Scholar
  310. Turner SR, Somerville CR (1997) Collapsed xylem phenotype of Arabidopsis identifies mutants deficient in cellulose deposition in the secondary cell wall. Plant Cell 9:689–701Google Scholar
  311. Urbanowicz BR, Rayon C, Carpita NC (2004) Topology of the maize mixed linkage (1→3), (1→4)-beta-d-glucan synthase at the Golgi membrane. Plant Physiol 134:758–768Google Scholar
  312. Urbanowicz BR, Pena MJ, Ratnaparkhe S, Avci U, Backe J, Steet HF, Foston M, Li H, O'Neill MA, Ragauskas AJ, Darvill AG, Wyman C, Gilbert HJ, York WS (2012) 4-O-methylation of glucuronic acid in Arabidopsis glucuronoxylan is catalyzed by a domain of unknown function family 579 protein. Proc Natl Acad Sci U S A 109:14253–14258Google Scholar
  313. Vain T, Crowell EF, Timpano H, Biot E, Desprez T, Mansoori N, Trindade LM, Pagant S, Robert S, Höfte H, Gonneau M, Vernhettes S (2014) The cellulase KORRIGAN is part of the cellulose synthase complex. Plant Physiol 165:1521–1532Google Scholar
  314. Van Holst GJ, Varner JE (1984) Reinforced polyproline II conformation in a hydroxyproline-rich cell wall glycoprotein from carrot root. Plant Physiol 74:247–251Google Scholar
  315. Vanzin GF, Madson M, Carpita NC, Raikhel NV, Keegstra K, Reiter WD (2002) The mur2 mutant of Arabidopsis thaliana lacks fucosylated xyloglucan because of a lesion in fucosyltransferase AtFUT1. Proc Natl Acad Sci U S A 99:3340–3345Google Scholar
  316. Vega-Sánchez ME, Verhertbruggen Y, Christensen U, Chen X, Sharma V, Varanasi P, Jobling SA, Talbot M, White RG, Joo M, Singh S, Auer M, Scheller HV, Ronald PC (2012) Loss of cellulose synthase-like F6 function affects mixed-linkage glucan deposition, cell wall mechanical properties, and defense responses in vegetative tissues of rice. Plant Physiol 159:56–69Google Scholar
  317. Velasquez SM, Ricardi MM, Gloazzo Dorosz J, Fernandez PV, Nadra AD, Pol-Fachin L, Egelund J, Gille S, Ciancia M, Verli H, Pauly M, Bacic A, Olsen EC, Ulvskov P, Petersen BL, Somerville C, Iusem ND, Estevez JM (2011) O-glycosylated cell wall extensins are essential in root hair growth. Science 33:1401–1403Google Scholar
  318. Velasquez M, Salter JS, Dorosz JG, Petersen BL, Estevez JM (2012) Recent advances on the posttranslational modifications of EXTs and their roles in plant cell walls. Front Plant Sci 15:93Google Scholar
  319. Vergara CE, Carpita NC (2001) Beta-d-glycan synthases and the CesA gene family: lessons to be learned from the mixed-linkage (1→3), (1→4)-beta-d-glucan synthase. Plant Mol Biol 47:145–160Google Scholar
  320. Vincken JP, York WS, Beldman G, Voragen AG (1997) Two general branching patterns of xyloglucan, XXXG and XXGG. Plant Physiol 114:9–13Google Scholar
  321. Voragen AGJ, Pilnik W, Thibault JF, Axelos MAV, Renard MGC (1998) Pectins. In: Dekker M (ed) Food polysaccharides and their applications. Academic, New York, pp 287–339Google Scholar
  322. Vuttipongchaikij S, Brocklehurst D, Steele-King C, Ashford DA, Gomez LD, McQueen-Mason SJ (2012) Arabidopsis GT34 family contains five xyloglucan alpha-1,6-xylosyltransferases. New Phytol 195:585–595Google Scholar
  323. Wang J, Howles PA, Cork AH, Birch RJ, Williamson RE (2006) Chimeric proteins suggest that the catalytic and/or C-terminal domains give CesA1 and CesA3 access to their specific sites in the cellulose synthase of primary walls. Plant Physiol 142:685–695Google Scholar
  324. Wang L, Guo K, Li Y, Tu Y, Hu H, Wang B, Cui X, Peng L (2010) Expression profiling and integrative analysis of the CESA/CSL superfamily in rice. BMC Plant Biol 10:282Google Scholar
  325. Wang Y, Mortimer JC, Davis J, Dupree P, Keegstra K (2013) Identification of an additional protein involved in mannan biosynthesis. Plant J 73:105–117Google Scholar
  326. Wende G, Fry SC (1997) 2-O-beta-d-xylopyranosyl-(5-O-feruloyl)-l-arabinose, a widespread component of grass cell walls. Phytochemistry 44:1019–1030Google Scholar
  327. Whitcombe A, O'Neill MA, Steffan W, Albersheim P, Darvill AG (1995) Structural characterization of the pectic polysaccharide rhamnogalacturonan-II. Carbohydr Res 271:15–29Google Scholar
  328. Wightman R, Turner S (2010) Trafficking of the plant cellulose synthase complex. Plant Physiol 153:427–432Google Scholar
  329. Willats WGT, McCartney L, Mackie W, Knox JP (2001) Pectin: cell biology and prospects for functional analysis. Plant Mol Biol 47:9–27Google Scholar
  330. Williamson RE, Burn JE, Hocart CH (2002) Towards the mechanism of cellulose synthesis. Trends Plant Sci 7:461–467Google Scholar
  331. Wong HC, Fear AL, Calhoon RD, Eichinger GH, Mayer R, Amikam D, Benziman M, Gelfand DH, Meade JH, Emerick AW, Bruner R, Ben-Bassat A, Tal R (1990) Genetic organization of the cellulose synthase operon in Acetobacter xylinum. Proc Natl Acad Sci U S A 87:8130–8134Google Scholar
  332. Woodward JR, Fincher GB, Stone BA (1983) Water-soluble (1/3), (1/4)-β-d-glucans from barley (Hordeum vulgare) endosperm II fine structure. Carbohydr Polym 3:207–225Google Scholar
  333. Wu AM, Rihouey C, Seveno M, Hörnblad 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. Plant J 57:718–731Google Scholar
  334. Wu AM, Hörnblad E, Voxeur A, Gerber L, Rihouey C, Lerouge P, Marchant A (2010a) 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 Physiol 153:542–554Google Scholar
  335. Wu Y, Williams M, Bernard S, Driouich A, Showalter AM, Faik A (2010b) Functional identification of two nonredundant Arabidopsis alpha(1,2)fucosyltransferases specific to arabinogalactan proteins. J Biol Chem 285:13638–13645Google Scholar
  336. Xiong G, Cheng K, Pauly M (2013) Xylan O-acetylation impacts xylem development and enzymatic recalcitrance as indicated by the Arabidopsis mutant tbl29. Mol Plant 6:1373–1375Google Scholar
  337. Yamauchi T, Hara T, Sonoda Y (1986) Distribution of calcium and boron in the pectin fraction of tomato leaf cell wall. Plant Cell Physiol 27:729–732Google Scholar
  338. Yang Q, Reinhard K, Schiltz E, Matern U (1997) Characterization and heterologous expression of hydroxycinnamoyl/benzoyl-CoA: anthranilate N-hydroxycinnamoyl/benzoyltransferase from elicited cell cultures of carnation, Dianthus caryophyllus L. Plant Mol Biol 35:777–789Google Scholar
  339. York WS, O'Neill MA (2008) Biochemical control of xylan biosynthesis – which end is up? Curr Opin Plant Biol 11:258–265Google Scholar
  340. York WS, Kumar Kolli VS, Orlando R, Albersheim P, Darvill AG (1996) The structure of arabinoxyloglucans produced by solanaceous plants. Carbohydr Res 285:99–128Google Scholar
  341. Yuan Y, Teng Q, Zhong R, Ye ZH (2013) The Arabidopsis DUF231 domain-containing protein ESK1 mediates 2-O- and 3-O-acetylation of xylosyl residues in xylan. Plant Cell Physiol 54:1186–1199Google Scholar
  342. Zandleven J, Beldman G, Bosveld M, Schols HA, Voragen AGJ (2006) Enzymatic degradation studies of xylogalacturonans from apple and potato, using xylogalacturonan hydrolase. Carbohydr Polym 65:495–503Google Scholar
  343. Zandleven J, Sørensen SO, Harholt J, Beldman G, Schols HA, Scheller HV, Voragen AJ (2007) Xylogalacturonan exists in cell walls from various tissues of Arabidopsis thaliana. Phytochemistry 68:1219–1226Google Scholar
  344. Zeng W, Chatterjee M, Faik A (2008) UDP-xylose stimulated glucuronyltransferase activity in wheat (Triticum aestivum L.) microsomal membranes: characterization and role in glucurono(arabino)xylan biosynthesis. Plant Physiol 147:78–91Google Scholar
  345. Zeng W, Jiang N, Nadella R, Killen RL, Nadella V, Faik A (2010) A glucurono(arabino)xylan synthase complex from wheat contains members of the GT43, GT47, and GT75 families and functions cooperatively. Plant Physiol 154:78–97Google Scholar
  346. Zhang GF, Staehelin LA (1992) Functional compartmentation of the Golgi apparatus of plant cells: immunocytochemical analysis of high-pressure frozen- and freeze-substituted sycamore maple suspension culture cells. Plant Physiol 99:1070–1083Google Scholar
  347. Zhong RQ, Ye ZH (2009) Secondary cell walls. In: eLS. Wiley, Chichester. http://www.els.net. doi:10.1002/9780470015902.a0021256
  348. Zhong R, Kays SJ, Schroeder BP, Ye ZH (2002) Mutation of a chitinase-like gene causes ectopic deposition of lignin, aberrant cell shapes, and overproduction of ethylene. Plant Cell 14:165–179Google Scholar
  349. Zhong RQ, Morrison WH, Freshour GD, Hahn MG, Ye ZH (2003) Expression of a mutant form of cellulose synthase AtCesA7 causes dominant negative effect on cellulose biosynthesis. Plant Physiol 132:786–795Google Scholar
  350. Zhong R, Demura T, Ye ZH (2006) SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell 18:3158–3170Google Scholar
  351. Zhong RQ, Richardson EA, Ye ZH (2007a) Two NAC domain transcription factors, SND1 and NST1, function redundantly in regulation of secondary wall synthesis in fibers of Arabidopsis. Planta 225:1603–1611Google Scholar
  352. Zhong RQ, Richardson EA, Ye ZH (2007b) The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. Plant Cell 19:2776–2792Google Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Michael A. Held
    • 1
  • Nan Jiang
    • 2
  • Debarati Basu
    • 2
  • Allan M. Showalter
    • 2
  • Ahmed Faik
    • 2
  1. 1.Department of Chemistry and Biochemistry; Molecular and Cellular Biology ProgramOhio UniversityAthensUSA
  2. 2.Department of Environmental and Plant Biology; Molecular and Cellular Biology ProgramOhio UniversityAthensUSA

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