, Volume 238, Issue 4, pp 627–642 | Cite as

Hemicellulose biosynthesis

  • Markus Pauly
  • Sascha Gille
  • Lifeng Liu
  • Nasim Mansoori
  • Amancio de Souza
  • Alex Schultink
  • Guangyan Xiong


One major component of plant cell walls is a diverse group of polysaccharides, the hemicelluloses. Hemicelluloses constitute roughly one-third of the wall biomass and encompass the heteromannans, xyloglucan, heteroxylans, and mixed-linkage glucan. The fine structure of these polysaccharides, particularly their substitution, varies depending on the plant species and tissue type. The hemicelluloses are used in numerous industrial applications such as food additives as well as in medicinal applications. Their abundance in lignocellulosic feedstocks should not be overlooked, if the utilization of this renewable resource for fuels and other commodity chemicals becomes a reality. Fortunately, our understanding of the biosynthesis of the various hemicelluloses in the plant has increased enormously in recent years mainly through genetic approaches. Taking advantage of this knowledge has led to plant mutants with altered hemicellulosic structures demonstrating the importance of the hemicelluloses in plant growth and development. However, while we are on a solid trajectory in identifying all necessary genes/proteins involved in hemicellulose biosynthesis, future research is required to combine these single components and assemble them to gain a holistic mechanistic understanding of the biosynthesis of this important class of plant cell wall polysaccharides.


Cell walls Polysaccharide Glycosyltransferase Hemicellulose Mannan Xylan Xyloglucan Mixed-linkage glucan 



We would like to mention the funding sources that supported the authors. S.G., G.X., A. de S., N.M. were supported by a grant from the Energy Biosciences Institute; A.S. by the Dickinsen Chair for wood science and technology for M.P.; L.L. by the Department of Energy grant: ER65037-1036816.


  1. Albersheim P, Darvill A, Roberts K, Sederoff R, Staehelin A (2010) Plant cell walls: from chemistry to biology. Garland Science, New YorkGoogle Scholar
  2. 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 USA 109:989–993PubMedGoogle Scholar
  3. Anderson CT, Carroll A, Akhmetova L, Somerville C (2010) Real-time imaging of cellulose reorientation during cell wall expansion in Arabidopsis roots. Plant Physiol 152:787–796PubMedGoogle Scholar
  4. Anderson CT, Wallace IS, Somerville CR (2012) Metabolic click-labeling with a fucose analog reveals pectin delivery, architecture, and dynamics in Arabidopsis cell walls. Proc Natl Acad Sci USA 109:1329–1334PubMedGoogle Scholar
  5. Bar-Peled M, O’Neill MA (2011) Plant nucleotide sugar formation, interconversion, and salvage by sugar recycling. Annu Rev Plant Biol 62:127–155PubMedGoogle Scholar
  6. Bauer WD, Talmadge KW, Keegstra K, Albersheim P (1973) The structure of plant cell walls: II. The hemicellulose of the walls of suspension-cultured sycamore cells. Plant Physiol 51:174–187PubMedGoogle Scholar
  7. Baydoun EA, Waldron KW, Brett CT (1989) The interaction of xylosyltransferase and glucuronyltransferase involved in glucuronoxylan synthesis in pea (Pisum sativum) epicotyls. Biochem J 257:853–858PubMedGoogle Scholar
  8. Benova-Kakosova A, Digonnet C, Goubet F, Ranocha P, Jauneau A, Pesquet E, Barbier O, Zhang Z, Capek P, Dupree P, Liskova D, Goffner D (2006) Galactoglucomannans increase cell population density and alter the protoxylem/metaxylem tracheary element ratio in xylogenic cultures of Zinnia. Plant Physiol 142:696–709PubMedGoogle Scholar
  9. Bischoff V, Nita S, Neumetzler L, Schindelasch D, Urbain A, Eshed R, Persson S, Delmer D, Scheible WR (2010a) TRICHOME BIREFRINGENCE and its homolog AT5G01360 encode plant-specific DUF231 proteins required for cellulose biosynthesis in Arabidopsis. Plant Physiol 153:590–602PubMedGoogle Scholar
  10. Bischoff V, Selbig J, Scheible WR (2010b) Involvement of TBL/DUF231 proteins into cell wall biology. Plant Signal Behav 5:1057–1059PubMedGoogle Scholar
  11. Breton C, Mucha J, Jeanneau C (2001) Structural and functional features of glycosyltransferases. Biochimie 83:713–718PubMedGoogle Scholar
  12. Breton C, Snajdrova L, Jeanneau C, Koca J, Imberty A (2006) Structures and mechanisms of glycosyltransferases. Glycobiology 16:29r–37rPubMedGoogle Scholar
  13. 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 74:423–434PubMedGoogle Scholar
  14. 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 52:1154–1168PubMedGoogle Scholar
  15. 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 57:732–746PubMedGoogle Scholar
  16. Brown D, Wightman R, Zhang Z, 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. Plant J 66:401–413PubMedGoogle Scholar
  17. Buckeridge MS (2010) Seed cell wall storage polysaccharides: models to understand cell wall biosynthesis and degradation. Plant Physiol 154:1017–1023PubMedGoogle Scholar
  18. Buckeridge MS, Crombie HJ, Mendes CJ, Reid JS, Gidley MJ, Vieira CC (1997) A new family of oligosaccharides from the xyloglucan of Hymenaea courbaril L. (Leguminosae) cotyledons. Carbohydr Res 303:233–237PubMedGoogle Scholar
  19. Burton RA, Fincher GB (2012) Current challenges in cell wall biology in the cereals and grasses. Front Plant Sci 3:130PubMedGoogle Scholar
  20. 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 311:1940–1942PubMedGoogle Scholar
  21. Burton RA, Gidley MJ, Fincher GB (2010) Heterogeneity in the chemistry, structure and function of plant cell walls. Nat Chem Biol 6:724–732PubMedGoogle Scholar
  22. 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)-beta-d-glucans and alters their fine structure. Plant Biotechnol J 9:117–135PubMedGoogle Scholar
  23. Carpita NC (1996) Structure and biogenesis of the cell walls of grasses. Annu Rev Plant Physiol Plant Mol Biol 47:445–476PubMedGoogle Scholar
  24. 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 3:1–30PubMedGoogle Scholar
  25. 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 153:1362–1371PubMedGoogle Scholar
  26. Cavalier DM, Keegstra K (2006) Two xyloglucan xylosyltransferases catalyze the addition of multiple xylosyl residues to cellohexaose. J Biol Chem 281:34197–34207PubMedGoogle Scholar
  27. 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 20:1519–1537PubMedGoogle Scholar
  28. 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 USA 109:17117–17122PubMedGoogle Scholar
  29. 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 4:83PubMedGoogle Scholar
  30. 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 159:1355–1366PubMedGoogle Scholar
  31. 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 beta-1,4 glucan synthase. Proc Natl Acad Sci USA 104:8550–8555PubMedGoogle Scholar
  32. Cosgrove DJ (1998) Cell wall loosening by expansins. Plant Physiol 118:333–339PubMedGoogle Scholar
  33. Courtin CM, Delcour JA (2002) Arabinoxylans and endoxylanases in wheat flour bread-making. J Cereal Sci 35:225–243Google Scholar
  34. Cummings JH (1992) The effect of dietary fiber on fecal weight and composition. In: Spiller GA (ed) Dietary fibre in human nutrition. CRC Press, Boca Raton, pp 263–349Google Scholar
  35. 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 64:1028–1037PubMedGoogle Scholar
  36. Dea ICM, Morrison A (1975) Chemistry and interactions of seed galactomannans. In: Tipson RS, Derek H (eds) Advances in carbohydrate chemistry and biochemistry, vol 31. Academic Press, London, pp 241–312.
  37. Dhugga KS, Tiwari SC, Ray PM (1997) A reversibly glycosylated polypeptide (RGP1) possibly involved in plant cell wall synthesis: purification, gene cloning, and trans-Golgi localization. Proc Natl Acad Sci USA 94:7679–7684PubMedGoogle Scholar
  38. 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 303:363–366PubMedGoogle Scholar
  39. Dikeman CL, Fahey GC Jr (2006) Viscosity as related to dietary fiber: a review. Crit Rev Food Sci Nutr 46:649–663PubMedGoogle Scholar
  40. 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 USA 106:5996–6001PubMedGoogle Scholar
  41. Doering A, Lathe R, Persson S (2012) An update on xylan synthesis. Mol Plant 5:769–771PubMedGoogle Scholar
  42. Domozych DS, Ciancia M, Fangel JU, Mikkelsen MD, Ulvskov P, Willats WG (2012) The cell walls of green algae: a journey through evolution and diversity. Front Plant Sci 3:82PubMedGoogle Scholar
  43. Dwivany FM, Yulia D, Burton RA, Shirley NJ, Wilson SM, Fincher GB, Bacic A, Newbigin E, Doblin MS (2009) The CELLULOSE-SYNTHASE LIKE C (CSLC) family of barley includes members that are integral membrane proteins targeted to the plasma membrane. Mol Plant 2:1025–1039PubMedGoogle Scholar
  44. Ebringerová A (2005) Hemicellulose. Adv Polym Sci 186:1–67Google Scholar
  45. Edwards M, Bowman YJ, Dea IC, Reid JS (1988) A beta-d-galactosidase from nasturtium (Tropaeolum majus L.) cotyledons. Purification, properties, and demonstration that xyloglucan is the natural substrate. J Biol Chem 263:4333–4337PubMedGoogle Scholar
  46. Edwards M, Scott C, Gidley MJ, Reid JSG (1992) Control of mannose galactose ratio during galactomannan formation in developing legume seeds. Planta 187:67–74Google Scholar
  47. Edwards ME, Dickson CA, Chengappa S, Sidebottom C, Gidley MJ, Reid JSG (1999) Molecular characterisation of a membrane-bound galactosyltransferase of plant cell wall matrix polysaccharide biosynthesis. Plant J 19:691–697PubMedGoogle Scholar
  48. Faik A (2010) Xylan biosynthesis: news from the grass. Plant Physiol 153:396–402PubMedGoogle Scholar
  49. Faik A, Bar-Peled M, DeRocher AE, Zeng WQ, 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 275:15082–15089PubMedGoogle Scholar
  50. Faik A, Price NJ, Raikhel NV, Keegstra K (2002) An Arabidopsis gene encoding an alpha-xylosyltransferase involved in xyloglucan biosynthesis. Proc Natl Acad Sci USA 99:7797–7802PubMedGoogle Scholar
  51. Fischer MH, Yu N, Gray GR, Ralph J, Anderson L, Marlett JA (2004) The gel-forming polysaccharide of psyllium husk (Plantago ovata Forsk). Carbohydr Res 339:2009–2017PubMedGoogle Scholar
  52. Fooks LJ, Fuller R, Gibson GR (1999) Prebiotics, probiotics and human gut microbiology. Int Dairy J 9:53–61Google Scholar
  53. Fry SC (1989) The structure and functions of xyloglucan. J Exp Bot 40:1–11Google Scholar
  54. Fry SC, Janice GM (1989) Toward a working model of the growing plant cell wall. Plant cell wall polymers. American Chemical Society, Washington, DC, pp 33–46Google Scholar
  55. Fry SC, Mohler KE, Nesselrode BH, Frankova L (2008a) Mixed-linkage beta-glucan: xyloglucan endotransglucosylase, a novel wall-remodelling enzyme from Equisetum (horsetails) and charophytic algae. Plant J 55:240–252PubMedGoogle Scholar
  56. Fry SC, Nesselrode BH, Miller JG, Mewburn BR (2008b) Mixed-linkage (1–>3,1–>4)-beta-d-glucan is a major hemicellulose of Equisetum (horsetail) cell walls. New Phytol 179:104–115PubMedGoogle Scholar
  57. Ghelardi E, Tavanti A, Celandroni F, Lupetti A, Blandizzi C, Boldrini E, Campa M, Senesi S (2000) Effect of a novel mucoadhesive polysaccharide obtained from tamarind seeds on the intraocular penetration of gentamicin and ofloxacin in rabbits. J Antimicrob Chemother 46:831–834PubMedGoogle Scholar
  58. Gibeaut DM, Pauly M, Bacic A, Fincher GB (2005) Changes in cell wall polysaccharides in developing barley (Hordeum vulgare) coleoptiles. Planta 221:729–738PubMedGoogle Scholar
  59. Gille S, Pauly M (2012) O-acetylation of plant cell wall polysaccharides. Front Plant Sci 3:12PubMedGoogle Scholar
  60. Gille S, Cheng K, Skinner ME, Liepman AH, Wilkerson CG, Pauly M (2011a) Deep sequencing of voodoo lily (Amorphophallus konjac): an approach to identify relevant genes involved in the synthesis of the hemicellulose glucomannan. Planta 234:515–526PubMedGoogle Scholar
  61. Gille S, de Souza A, Xiong GY, Benz M, Cheng K, Schultink A, Reca IB, Pauly M (2011b) O-acetylation of arabidopsis hemicellulose xyloglucan requires AXY4 or AXY4L, proteins with a TBL and DUF231 domain. Plant Cell 23:4041–4053PubMedGoogle Scholar
  62. 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. Plant J 60:527–538PubMedGoogle Scholar
  63. Gunl M, Pauly M (2011) AXY3 encodes a alpha-xylosidase that impacts the structure and accessibility of the hemicellulose xyloglucan in Arabidopsis plant cell walls. Planta 233:707–719PubMedGoogle Scholar
  64. Gunl M, Gille S, Pauly M (2010) OLIgo mass profiling (OLIMP) of extracellular polysaccharides. J Vis Exp. doi: 10.3791/2046 PubMedGoogle Scholar
  65. Gunl M, Neumetzler L, Kraemer F, de Souza A, Schultink A, Pena M, York WS, Pauly M (2011) AXY8 encodes an alpha-fucosidase, underscoring the importance of apoplastic metabolism on the fine structure of Arabidopsis cell wall polysaccharides. Plant Cell 23:4025–4040PubMedGoogle Scholar
  66. Ha MA, Apperley DC, Jarvis MC (1997) Molecular rigidity in dry and hydrated onion cell walls. Plant Physiol 115:593–598PubMedGoogle Scholar
  67. 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 304:11–20PubMedGoogle Scholar
  68. Harris P, Trethewey JK (2010) The distribution of ester-linked ferulic acid in the cell walls of angiosperms. Phytochem Rev 9:19–33Google Scholar
  69. Hayashi T (1989) Xyloglucans in the primary-cell wall. Annu Rev Plant Physiol Plant Molec Biol 40:139–168Google Scholar
  70. Hazen SP, Scott-Craig JS, Walton JD (2002) Cellulose synthase-like genes of rice. Plant Physiol 128:336–340PubMedGoogle Scholar
  71. Hoffman M, Jia Z, Pena MJ, Cash M, Harper A, Blackburn AR 2nd, Darvill A, York WS (2005) Structural analysis of xyloglucans in the primary cell walls of plants in the subclass Asteridae. Carbohydr Res 340:1826–1840PubMedGoogle Scholar
  72. Hornblad E, Ulfstedt M, Ronne H, Marchant A (2013) Partial functional conservation of IRX10 homologs in physcomitrella patens and Arabidopsis thaliana indicates an evolutionary step contributing to vascular formation in land plants. BMC Plant Biol 13:3PubMedGoogle Scholar
  73. Hrmova M, Fincher GB (2001) Structure-function relationships of beta-d-glucan endo- and exohydrolases from higher plants. Plant Mol Biol 47:73–91PubMedGoogle Scholar
  74. Hsieh YS, Harris PJ (2009) Xyloglucans of monocotyledons have diverse structures. Mol Plant 2:943–965PubMedGoogle Scholar
  75. Iglesias N, Abelenda JA, Rodino M, Sampedro J, Revilla G, Zarra I (2006) Apoplastic glycosidases active against xyloglucan oligosaccharides of Arabidopsis thaliana. Plant Cell Physiol 47:55–63PubMedGoogle Scholar
  76. Jensen JK, Kim H, Cocuron JC, Orler R, Ralph J, Wilkerson CG (2011) The DUF579 domain containing proteins IRX15 and IRX15-L affect xylan synthesis in Arabidopsis. Plant J 66:387–400PubMedGoogle Scholar
  77. Jensen JK, Schultink A, Keegstra K, Wilkerson CG, Pauly M (2012) RNA-Seq analysis of developing nasturtium seeds (Tropaeolum majus): identification and characterization of an additional galactosyltransferase involved in xyloglucan biosynthesis. Mol Plant 5:984–992PubMedGoogle Scholar
  78. Jia Z, Qin Q, Darvill AG, York WS (2003) Structure of the xyloglucan produced by suspension-cultured tomato cells. Carbohydr Res 338:1197–1208PubMedGoogle Scholar
  79. Jia Z, Cash M, Darvill AG, York WS (2005) NMR characterization of endogenously O-acetylated oligosaccharides isolated from tomato (Lycopersicon esculentum) xyloglucan. Carbohydr Res 340:1818–1825PubMedGoogle Scholar
  80. Johansson MH, Samuelson O (1977) Reducing end groups in birch xylan and their alkaline-degradation. Wood Sci Technol 11:251–263Google Scholar
  81. Kato Y, Matsuda K (1981) Occurrence of a soluble and low-molecular weight xyloglucan and its origin in etiolated mung bean hypocotyls. Agr Biol Chem Tokyo 45:1–8Google Scholar
  82. Kato Y, Ito J, Mitsuishi Y (2004) Further structural study of the barley and bamboo shoot xyloglucans by xyloglucanase. J Appl Glycosci 51:327–333Google Scholar
  83. Keegstra K, David C (2010) Glycosyltransferases of the GT34 and GT37 families. Annu Plant Rev Plant Polysacch Biosynth Bioeng 41:235–249Google Scholar
  84. 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 51:188–197PubMedGoogle Scholar
  85. Keppler BD, Showalter AM (2010) IRX14 and IRX14-LIKE, two glycosyl transferases involved in glucuronoxylan biosynthesis and drought tolerance in Arabidopsis. Mol Plant 3:834–841PubMedGoogle Scholar
  86. 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
  87. Kim JB, Olek AT, Carpita NC (2000) Cell wall and membrane-associated exo-beta-d-glucanases from developing maize seedlings. Plant Physiol 123:471–486PubMedGoogle Scholar
  88. Kong Y, Zhou G, Avci U, Gu X, Jones C, Yin Y, Xu Y, Hahn MG (2009) Two poplar glycosyltransferase genes, PdGATL1.1 and PdGATL1.2, are functional orthologs to PARVUS/AtGATL1 in Arabidopsis. Mol Plant 2:1040–1050PubMedGoogle Scholar
  89. Kooiman P (1961) The constitution of tamarindus-amyloid. Recl Trav Chim Pay B 80:849–865Google Scholar
  90. Lee C, O’Neill MA, Tsumuraya Y, Darvill AG, Ye ZH (2007a) The irregular xylem9 mutant is deficient in xylan xylosyltransferase activity. Plant Cell Physiol 48:1624–1634PubMedGoogle Scholar
  91. Lee C, Zhong R, Richardson EA, Himmelsbach DS, McPhail BT, Ye ZH (2007b) The PARVUS gene is expressed in cells undergoing secondary wall thickening and is essential for glucuronoxylan biosynthesis. Plant Cell Physiol 48:1659–1672PubMedGoogle Scholar
  92. Lee C, Teng Q, Huang W, Zhong R, Ye ZH (2009a) The poplar GT8E and GT8F glycosyltransferases are functional orthologs of Arabidopsis PARVUS involved in glucuronoxylan biosynthesis. Plant Cell Physiol 50:1982–1987PubMedGoogle Scholar
  93. Lee CH, Teng Q, Huang WL, Zhong RQ, Ye ZH (2009b) The F8H glycosyltransferase is a functional paralog of FRA8 involved in glucuronoxylan biosynthesis in Arabidopsis. Plant Cell Physiol 50:812–827PubMedGoogle Scholar
  94. Lee C, Teng Q, Huang W, Zhong R, Ye ZH (2010) The Arabidopsis family GT43 glycosyltransferases form two functionally nonredundant groups essential for the elongation of glucuronoxylan backbone. Plant Physiol 153:526–541PubMedGoogle Scholar
  95. Lee C, Teng Q, Zhong R, Ye ZH (2012a) Arabidopsis GUX proteins are glucuronyltransferases responsible for the addition of glucuronic acid side chains onto xylan. Plant Cell Physiol 53:1204–1216PubMedGoogle Scholar
  96. Lee C, Teng Q, Zhong R, Yuan Y, Haghighat M, Ye ZH (2012b) Three Arabidopsis DUF579 domain-containing GXM proteins are methyltransferases catalyzing 4-O-methylation of glucuronic acid on xylan. Plant Cell Physiol 53:1934–1949PubMedGoogle Scholar
  97. Lee C, Zhong R, Ye ZH (2012c) Arabidopsis family GT43 members are xylan xylosyltransferases required for the elongation of the xylan backbone. Plant Cell Physiol 53:135–143PubMedGoogle Scholar
  98. Lee C, Zhong R, Ye ZH (2012d) Biochemical characterization of xylan xylosyltransferases involved in wood formation in poplar. Plant Signal Behav 7:332–337PubMedGoogle Scholar
  99. Leonard R, Pabst M, Bondili JS, Chambat G, Veit C, Strasser R, Altmann F (2008) Identification of an Arabidopsis gene encoding a GH95 alpha1,2-fucosidase active on xyloglucan oligo- and polysaccharides. Phytochemistry 69:1983–1988PubMedGoogle Scholar
  100. 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 USA 102:2221–2226PubMedGoogle Scholar
  101. Liepman AH, Nairn CJ, Willats WGT, Sorensen I, Roberts AW, Keegstra K (2007) Functional genomic analysis supports conservation of function among cellulose synthase-like a gene family members and suggests diverse roles of mannans in plants. Plant Physiol 143:1881–1893PubMedGoogle Scholar
  102. Liwanag AJ, 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 beta-1,4-galactan beta-1,4-galactosyltransferase. Plant Cell 24:5024–5036PubMedGoogle Scholar
  103. 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 15:1662–1670PubMedGoogle Scholar
  104. Manna S, Mcanalley BH (1993) Determination of the position of the O-acetyl group in a beta-(1–>4)-mannan (acemannan) from Aloe-barbardensis Miller. Carbohydr Res 241:317–319PubMedGoogle Scholar
  105. McCann MC, Roberts K (1991) Architecture of the primary cell wall. In: Lloyd CW (ed) The cytoskeletal basis of plant growth and form. Academic Press, London, pp 109–129Google Scholar
  106. Meier H, Reid JSG (1982) Reserve polysaccharides other than starch in higher plants. In: Loewus F, Tanner W (eds) Plant carbohydrates I, vol 13/A. Encyclopedia of plant physiology. Springer, Berlin, pp 418–471. doi: 10.1007/978-3-642-68275-9_11
  107. Meikle PJ, Hoogenraad NJ, Bonig I, Clarke AE, Stone BA (1994) A (1–>3,1–>4)-beta-glucan-specific monoclonal antibody and its use in the quantitation and immunocytochemical location of (1–>3,1–>4)-beta-glucans. Plant J 5:1–9PubMedGoogle Scholar
  108. Mishra MU, Khandare JN (2007) Tamarind seed polysaccharides: biodegradable polymer for colonic drug delivery. In: Second International Conference and Indo-Canadian Satellite symposium on pharmaceutical science, technology, practice and natural products, conference chronicle, DDSGoogle Scholar
  109. Mishra A, Malhotra AV (2009) Tamarind xyloglucan: a polysaccharide with versatile application potential. J Mater Chem 19:8528–8536Google Scholar
  110. Moore P, Staehelin LA (1988) Immunogold localization of the cell-wall-matrix polysaccharides rhamnogalacturonan I and xyloglucan during cell expansion and cytokinesis in Trifolium pratense L.; implication for secretory pathways. Planta 174:433–445Google Scholar
  111. Mortimer JC, Miles GP, Brown DM, Zhang Z, Segura MP, Weimar T, Yu X, 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 USA 107:17409–17414PubMedGoogle Scholar
  112. Naran R, Chen G, Carpita NC (2008) Novel rhamnogalacturonan I and arabinoxylan polysaccharides of flax seed mucilage. Plant Physiol 148:132–141PubMedGoogle Scholar
  113. Nishitani K (1992) Endo-xyloglucan transferase, a novel enzyme which mediates transglycosylation reaction between xyloglucan molecules (chapter). In: Plant cell walls as biopolymers with physiological functions. pp 263–268Google Scholar
  114. Nishitani K, Tominaga R (1992) Endo-xyloglucan transferase, a novel class of glycosyltransferase that catalyzes transfer of a segment of xyloglucan molecule to another xyloglucan molecule. J Biol Chem 267:21058–21064PubMedGoogle Scholar
  115. Park YB, Cosgrove DJ (2012a) Changes in cell wall biomechanical properties in the xyloglucan-deficient xxt1/xxt2 mutant of Arabidopsis. Plant Physiol 158:465–475PubMedGoogle Scholar
  116. Park YB, Cosgrove DJ (2012b) A revised architecture of primary cell walls based on biomechanical changes induced by substrate-specific endoglucanases. Plant Physiol 158:1933–1943PubMedGoogle Scholar
  117. Pauly M, Keegstra K (2008) Cell-wall carbohydrates and their modification as a resource for biofuels. Plant J 54:559–568PubMedGoogle Scholar
  118. Pauly M, Keegstra K (2010) Plant cell wall polymers as precursors for biofuels. Curr Opin Plant Biol 13:305–312PubMedGoogle Scholar
  119. Pauly M, Albersheim P, Darvill A, York WS (1999a) Molecular domains of the cellulose/xyloglucan network in the cell walls of higher plants. Plant J 20:629–639PubMedGoogle Scholar
  120. Pauly M, Andersen LN, Kauppinen S, Kofod LV, York WS, Albersheim P, Darvill A (1999b) A xyloglucan-specific endo-beta-1,4-glucanase from Aspergillus aculeatus: expression cloning in yeast, purification and characterization of the recombinant enzyme. Glycobiology 9:93–100PubMedGoogle Scholar
  121. Pauly M, Eberhard S, Albersheim P, Darvill A, York WS (2001a) Effects of the mur1 mutation on xyloglucans produced by suspension-cultured Arabidopsis thaliana cells. Planta 214:67–74PubMedGoogle Scholar
  122. Pauly M, Qin Q, Greene H, Albersheim P, Darvill A, York WS (2001b) Changes in the structure of xyloglucan during cell elongation. Planta 212:842–850PubMedGoogle Scholar
  123. 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 19:549–563PubMedGoogle Scholar
  124. 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 18:891–904PubMedGoogle Scholar
  125. 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 24:4511–4524PubMedGoogle Scholar
  126. Perrin RM, DeRocher AE, Bar-Peled M, Zeng WQ, Norambuena L, Orellana A, Raikhel NV, Keegstra K (1999) Xyloglucan fucosyltransferase, an enzyme involved in plant cell wall biosynthesis. Science 284:1976–1979PubMedGoogle Scholar
  127. 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 132:768–778PubMedGoogle Scholar
  128. Persson S, Caffall KH, Freshour G, Hilley MT, Bauer S, Poindexter P, Hahn MG, Mohnen D, Somerville C (2007) The Arabidopsis irregular xylem8 mutant is deficient in glucuronoxylan and homogalacturonan, which are essential for secondary cell wall integrity. Plant Cell 19:237–255PubMedGoogle Scholar
  129. Popper ZA, Fry SC (2003) Primary cell wall composition of bryophytes and charophytes. Ann Bot 91:1–12PubMedGoogle Scholar
  130. Popper ZA, Fry SC (2008) Xyloglucan-pectin linkages are formed intra-protoplasmically, contribute to wall-assembly, and remain stable in the cell wall. Planta 227:781–794PubMedGoogle Scholar
  131. Popper ZA, Michel G, Herve C, Domozych DS, Willats WG, Tuohy MG, Kloareg B, Stengel DB (2011) Evolution and diversity of plant cell walls: from algae to flowering plants. Annu Rev Plant Biol 62:567–590PubMedGoogle Scholar
  132. Rao PS, Srivastava HC (1973) Tamarind in industrial gums, 2nd edn. In: Whistler RL (ed) Academic Press, New York, pp 369–411Google Scholar
  133. 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 339:201–208PubMedGoogle Scholar
  134. Reiter WD, Chapple C, Somerville CR (1997) Mutants of Arabidopsis thaliana with altered cell wall polysaccharide composition. Plant J 12:335–345PubMedGoogle Scholar
  135. 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 159:1408–1417PubMedGoogle Scholar
  136. Rodriguez-Gacio MDC, Iglesias-Fernandez R, Carbonero P, Matilla AJ (2012) Softening-up mannan-rich cell walls. J Exp Bot 63:3975–3988Google Scholar
  137. Rolando M, Valente C (2007) Establishing the tolerability and performance of tamarind seed polysaccharide (TSP) in treating dry eye syndrome: results of a clinical study. BMC Ophthalmol 7:5PubMedGoogle Scholar
  138. Rose JK, Braam J, Fry SC, Nishitani K (2002) The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature. Plant Cell Physiol 43:1421–1435PubMedGoogle Scholar
  139. Sampedro J, Sieiro C, Revilla G, Gonzalez-Villa T, Zarra I (2001) Cloning and expression pattern of a gene encoding an alpha-xylosidase active against xyloglucan oligosaccharides from Arabidopsis. Plant Physiol 126:910–920PubMedGoogle Scholar
  140. Sampedro J, Gianzo C, Iglesias N, Guitian E, Revilla G, Zarra I (2012) AtBGAL10 is the main xyloglucan beta-galactosidase in Arabidopsis, and its absence results in unusual xyloglucan subunits and growth defects. Plant Physiol 158:1146–1157PubMedGoogle Scholar
  141. Sarossy Z, Blomfeldt TOJ, Hedenqvist MS, Koch CB, Ray SS, Plackett D (2012) Composite films of arabinoxylan and fibrous sepiolite: morphological, mechanical, and Baffler properties. Acs Appl Mater Inter 4:3378–3386Google Scholar
  142. Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289PubMedGoogle Scholar
  143. Schroder R, Wegrzyn TF, Bolitho KM, Redgwell RJ (2004) Mannan transglycosylase: a novel enzyme activity in cell walls of higher plants. Planta 219:590–600PubMedGoogle Scholar
  144. Seeberger PH, Werz DB (2007) Synthesis and medical applications of oligosaccharides. Nature 446:1046–1051PubMedGoogle Scholar
  145. Shimizu K, Ishihara M (1983) Hemicellulases of brown rotting fungus, Tyromyces-Palustris. 5. Isolation and characterization of oligosaccharides from the hydrolyzate of larch wood glucomannan with endo-beta-d-mannanase. Agr Biol Chem Tokyo 47:949–955Google Scholar
  146. Sims IM, Munro SL, Currie G, Craik D, Bacic A (1996) Structural characterisation of xyloglucan secreted by suspension-cultured cells of Nicotiana plumbaginifolia. Carbohydr Res 293:147–172PubMedGoogle Scholar
  147. Smith RC, Fry SC (1991) Endotransglycosylation of xyloglucans in plant cell suspension cultures. Biochem J 279(Pt 2):529–535PubMedGoogle Scholar
  148. Somerville C, Bauer S, Brininstool G, Facette M, Hamann T, Milne J, Osborne E, Paredez A, Persson S, Raab T, Vorwerk S, Youngs H (2004) Toward a systems approach to understanding plant cell walls. Science 306:2206–2211PubMedGoogle Scholar
  149. Sorensen I, Pettolino FA, Wilson SM, Doblin MS, Johansen B, Bacic A, Willats WG (2008) Mixed-linkage (1–>3), (1–>4)-beta-d-glucan is not unique to the Poales and is an abundant component of Equisetum arvense cell walls. Plant J 54:510–521PubMedGoogle Scholar
  150. 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 USA 103:5236–5241PubMedGoogle Scholar
  151. Strasser R, Mucha J, Mach L, Altmann F, Wilson IB, Glossl J, Steinkellner H (2000) Molecular cloning and functional expression of beta1, 2-xylosyltransferase cDNA from Arabidopsis thaliana. FEBS Lett 472:105–108PubMedGoogle Scholar
  152. Suzuki S, Li LG, 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 142:1233–1245PubMedGoogle Scholar
  153. Takeda T, Furuta Y, Awano T, Mizuno K, Mitsuishi Y, Hayashi T (2002) Suppression and acceleration of cell elongation by integration of xyloglucans in pea stem segments. Proc Natl Acad Sci USA 99:9055–9060PubMedGoogle Scholar
  154. Taketa S, Yuo T, Tonooka T, Tsumuraya Y, Inagaki Y, Haruyama N, Larroque O, Jobling SA (2012) Functional characterization of barley betaglucanless mutants demonstrates a unique role for CslF6 in (1,3;1,4)-beta-d-glucan biosynthesis. J Exp Bot 63:381–392PubMedGoogle Scholar
  155. Talbott LD, Ray PM (1992) Molecular size and separability features of pea cell wall polysaccharides: implications for models of primary wall structure. Plant Physiol 98:357–368PubMedGoogle Scholar
  156. 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 25:270–287PubMedGoogle Scholar
  157. Thompson DS (2005) How do cell walls regulate plant growth? J Exp Bot 56:2275–2285PubMedGoogle Scholar
  158. Truswell AS (2002) Cereal grains and coronary heart disease. Eur J Clin Nutr 56:1–14PubMedGoogle Scholar
  159. 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 USA 109:14253–14258PubMedGoogle Scholar
  160. Valent BS, Albersheim P (1974) The structure of plant cell walls: v. On the binding of xyloglucan to cellulose fibers. Plant Physiol 54:105–108PubMedGoogle Scholar
  161. 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 USA 99:3340–3345PubMedGoogle Scholar
  162. Vega-Sanchez 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 159:56–69PubMedGoogle Scholar
  163. Vega-Sanchez M, Verhertbruggen Y, Scheller HV, Ronald P (2013) Abundance of mixed linkage glucan in mature tissues and secondary cell walls of grasses. Plant Signal Behav 8:e23143PubMedGoogle Scholar
  164. Verhertbruggen Y, Yin L, Oikawa A, Scheller HV (2011) Mannan synthase activity in the CSLD family. Plant Signal Behav 6:1620–1623PubMedGoogle Scholar
  165. 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 195:585–595PubMedGoogle Scholar
  166. Wang Y, Alonso AP, Wilkerson CG, Keegstra K (2012) Deep EST profiling of developing fenugreek endosperm to investigate galactomannan biosynthesis and its regulation. Plant Mol Biol 79:243–258PubMedGoogle Scholar
  167. 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
  168. Williams MAK, Foster TJ, Martin DR, Norton IT, Yoshimura M, Nishinari K (2000) A molecular description of the gelation mechanism of konjac mannan. Biomacromolecules 1:440–450PubMedGoogle Scholar
  169. 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. Plant J 57:718–731PubMedGoogle Scholar
  170. 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 Physiol 153:542–554PubMedGoogle Scholar
  171. 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. doi: 10.1093/mp/sst014 Google Scholar
  172. York WS, O’Neill MA (2008) Biochemical control of xylan biosynthesis—which end is up? Curr Opin Plant Biol 11:258–265PubMedGoogle Scholar
  173. York WS, Oates JE, van Halbeek H, Darvill AG, Albersheim P, Tiller PR, Dell A (1988) Location of the O-acetyl substituents on a nonasaccharide repeating unit of sycamore extracellular xyloglucan. Carbohydr Res 173:113–132PubMedGoogle Scholar
  174. Zabotina OA, van de Ven WTG, Freshour G, Drakakaki G, Cavalier D, Mouille G, Hahn MG, Keegstra K, Raikhel NV (2008) Arabidopsis XXT5 gene encodes a putative alpha-1,6-xylosyltransferase that is involved in xyloglucan biosynthesis. Plant J 56:101–115PubMedGoogle Scholar
  175. Zabotina OA, Avci U, Cavalier D, Pattathil S, Chou YH, Eberhard S, Danhof L, Keegstra K, Hahn MG (2012) Mutations in multiple XXT genes of Arabidopsis reveal the complexity of xyloglucan biosynthesis. Plant Physiol 159:1367–1384PubMedGoogle Scholar
  176. Zeng W, Jiang N, Nadella R, Killen TL, 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 154:78–97PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Markus Pauly
    • 1
    • 2
  • Sascha Gille
    • 1
  • Lifeng Liu
    • 2
  • Nasim Mansoori
    • 1
  • Amancio de Souza
    • 1
    • 2
  • Alex Schultink
    • 2
  • Guangyan Xiong
    • 1
  1. 1.Energy Biosciences InstituteUniversity of CaliforniaBerkeleyUSA
  2. 2.Department of Plant and Microbial BiologyUniversity of CaliforniaBerkeleyUSA

Personalised recommendations