Advertisement

Root Hairs pp 85-102 | Cite as

Plant Cell Wall Biogenesis During Tip Growth in Root Hair Cells

  • E. NielsenEmail author
Part of the Plant Cell Monographs book series (CELLMONO, volume 12)

Abstract

In plants, cells are surrounded by a rigid cell wall, which restricts changes in cell shape and size; therefore, polarized secretion and deposition of cell wall components take on a particular importance during plant growth and development. In recent years, significant advances have been made in discovering and characterizing enzymes and proteins involved in the synthesis of many of the main cell wall polysaccharides. However, despite these advances little is known of the membrane-trafficking pathways responsible for polarized secretion in plants, and how the specific delivery of cell wall components to regions of cell expansion is controlled. In root hair cells, the majority of new cell wall deposition occurs in a highly polarized manner at the expanding tips of these cells. Additionally, reinforcement of the cell wall and deposition of secondary cell wall components occur selectively in the more distal portions of the root hair cell. In this chapter we will discuss some of the major classes of polysaccharides and structural proteins that are found in plant cell walls and relevant evidence for their selective deposition and function during plant cell wall biogenesis during root hair tip growth.

Keywords

Root Hair Cell Wall Component Secondary Cell Wall Cellulose Microfibril Pectic Polysaccharide 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

I thank David Cavalier, Oliver Lerouxel, and Ken Keegstra for sharing their unpublished results, and Byung-Ho Kang for providing the immunoelectron micrograph of RabA4b-labeled secretory vesicles containing cargo recognized by the CCCRC-M1 antibodies. This work was supported by a Department of Energy grant DE-FG02–03ER15412.

References

  1. Aloni Delmer DP, Benziman M 1982) Achievement of high rates of in vitro synthesis of 1, 4-beta-D-glucan: activation by cooperative interaction of the Acetobacter xylinum enzyme system with GTP, polyethylene glycol, and a protein factor. Proc Natl Acad Sci USA 79:6448–6452PubMedCrossRefGoogle Scholar
  2. Andeme-Onzighi C, Sivaguru M, Judy-March J, Baskin TI, Driouich A (2002) The reb1–1 mutation of Arabidopsis alters the morphology of trichoblasts, the expression of arabinogalactan-proteins and the organization of cortical microtubules. Planta 215:949–958PubMedCrossRefGoogle Scholar
  3. Arioli T, Peng L, Betzner AS, Burn J, Wittke W, Herth W, Camilleri C, Hofte H, Plazinski J, Birch R, Cork A, Glover J, Redmond J, Williamson RE (1998) Molecular analysis of cellulose biosynthesis in Arabidopsis. Science 279:717–720PubMedCrossRefGoogle Scholar
  4. Baskin TI (2005) Anisotropic expansion of the plant cell wall. Annu Rev Cell Dev Biol 21:203–222PubMedCrossRefGoogle Scholar
  5. Baumberger N, Ringli C, Keller B (2001) The chimeric leucine-rich repeat/extensin cell wall protein LRX1 is required for root hair morphogenesis in Arabidopsis thaliana. Genes Dev 15:1128–1139PubMedCrossRefGoogle Scholar
  6. Baumberger N, Steiner M, Ryser U, Keller B, Ringli C (2003) Synergistic interaction of the two paralogous Arabidopsis genes LRX1 and LRX2 in cell wall formation during root hair development. Plant J 35:71–81PubMedCrossRefGoogle Scholar
  7. Bernal AJ, Jensen JK, Harholt J, Sorensen S, Moller I, Blaukopf C, Johansen B, de Lotto R, Pauly M, Scheller HV, Willats WG (2007) Disruption of ATCSLD5 results in reduced growth, reduced xylan and homogalacturonan synthase activity and altered xylan occurrence in Arabidopsis. Plant J 52(5):791–802PubMedCrossRefGoogle Scholar
  8. Bernhardt C, Tierney ML (2000) Expression of AtPRP3, a proline-rich structural cell wall protein from Arabidopsis, is regulated by cell-type-specific developmental pathways involved in root hair formation. Plant Physiol 122:705–714PubMedCrossRefGoogle Scholar
  9. Bosch M, Hepler PK (2005) Pectin methylesterases and pectin dynamics in pollen tubes. Plant Cell 17:3219–3226PubMedCrossRefGoogle Scholar
  10. Bosch M, Hepler PK (2006) Silencing of the tobacco pollen pectin methylesterase NtPPME1 results in retarded in vivo pollen tube growth. Planta 223:736–745PubMedCrossRefGoogle Scholar
  11. Bosch M, Cheung AY, Hepler PK (2005) Pectin methylesterase, a regulator of pollen tube growth. Plant Physiol 138:1334–1346PubMedCrossRefGoogle Scholar
  12. Bradley DJ, Kjellbom P, Lamb CJ (1992) Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell 70:21–30PubMedCrossRefGoogle Scholar
  13. 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 311:1940–1942PubMedCrossRefGoogle Scholar
  14. Carol RJ, Dolan L (2002) Building a hair: tip growth in Arabidopsis thaliana root hairs. Philos Trans R Soc Lond B Biol Sci 357:815–821PubMedCrossRefGoogle Scholar
  15. Carol RJ, Dolan L (2006) The role of reactive oxygen species in cell growth: lessons from root hairs. J Exp Bot 57:1829–1834PubMedCrossRefGoogle Scholar
  16. Cavalier DM, Keegstra K (2006) Two xyloglucan xylosyltransferases catalyze the addition of multiple xylosyl residues to cellohexaose. J Biol Chem 281:34197–34207PubMedCrossRefGoogle Scholar
  17. 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 USA 82:4399–4403PubMedCrossRefGoogle Scholar
  18. Cho HT, Cosgrove DJ (2002) Regulation of root hair initiation and expansin gene expression in Arabidopsis. Plant Cell 14:3237–3253PubMedCrossRefGoogle Scholar
  19. Cosgrove DJ (1997) Relaxation in a high-stress environment: the molecular bases of extensible cell walls and cell enlargement. Plant Cell 9:1031–1041PubMedCrossRefGoogle Scholar
  20. Cosgrove DJ (1999) Enzymes and other agents that enhance cell wall extensibility. Annu Rev Plant Physiol Plant Mol Biol 50:391–417PubMedCrossRefGoogle Scholar
  21. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861PubMedCrossRefGoogle Scholar
  22. Cosgrove DJ, Li ZC (1993) Role of expansin in cell enlargement of oat coleoptiles (Analysis of developmental gradients and photocontrol). Plant Physiol 103:1321–1328PubMedGoogle Scholar
  23. Cosgrove DJ, Li LC, Cho HT, Hoffmann-Benning S, Moore RC, Blecker D (2002) The growing world of expansins. Plant Cell Physiol 43:1436–1444PubMedCrossRefGoogle Scholar
  24. 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 122:683–693PubMedGoogle Scholar
  25. Desprez T, Juraniec M, Crowell EF, Jouy H, Pochylova Z, Parcy F, Hofte H, Gonneau M, Vernhettes S (2007) Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 104:15572–15577PubMedCrossRefGoogle Scholar
  26. 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 303:363–366PubMedCrossRefGoogle Scholar
  27. Di Matteo A, Giovane A, Raiola A, Camardella L, Bonivento D, De Lorenzo G, Cervone F, Bellincampi D, Tsernoglou D (2005) Structural basis for the interaction between pectin methylesterase and a specific inhibitor protein. Plant Cell 17:849–858PubMedCrossRefGoogle Scholar
  28. Diet A, Link B, Seifert GJ, Schellenberg B, Wagner U, Pauly M, Reiter WD, Ringli C (2006) The Arabidopsis root hair cell wall formation mutant lrx1 is suppressed by mutations in the RHM1 gene encoding a UDP-L-rhamnose synthase. Plant Cell 18:1630–1641PubMedCrossRefGoogle Scholar
  29. Dolan L (2001) How and where to build a root hair. Curr Opin Plant Biol 4:550–554PubMedCrossRefGoogle Scholar
  30. Downes BP, Steinbaker CR, Crowell DN (2001) Expression and processing of a hormonally regulated beta-expansin from soybean. Plant Physiol 126:244–252PubMedCrossRefGoogle Scholar
  31. Dumais J, Long SR, Shaw SL (2004) The mechanics of surface expansion anisotropy in Medicago truncatula root hairs. Plant Physiol 136:3266–3275PubMedCrossRefGoogle Scholar
  32. Emons A (1989) Helicoidal microfibril deposition in a tip-growing cell and microtubule alignment during rip morphogenesis: a dry-cleaving and freeze -substitution study. Can J Bot 67:2401–2408Google Scholar
  33. Emons AM (1985) Plasma membrane rosettes in root hairs of Equisetum hyemale. Planta 163:350–359CrossRefGoogle Scholar
  34. Emons AMC, van Maaren N (1987) Helicoidal cell wall texture in root hairs. Planta 170:145–151CrossRefGoogle Scholar
  35. Emons AM, Mulder BM (2000) How the deposition of cellulose microfibrils builds cell wall architecture. Trends Plant Sci 5:35–40PubMedCrossRefGoogle Scholar
  36. Fagard M, Desnos T, Desprez T, Goubet F, Refregier G, Mouille G, McCann M, Rayon C, Vernhettes S, Hofte H (2000) PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis. Plant Cell 12:2409–2424PubMedCrossRefGoogle Scholar
  37. 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 99:7797–802PubMedCrossRefGoogle Scholar
  38. Favery B, Ryan E, Foreman J, Linstead P, Boudonck K, Steer M, Shaw P, Dolan L (2001) KOJAK encodes a cellulose synthase-like protein required for root hair cell morphogenesis in Arabidopsis. Genes Dev 15:79–89PubMedCrossRefGoogle Scholar
  39. Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JDG, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446PubMedCrossRefGoogle Scholar
  40. Fowler TJ, Bernhardt C, Tierney ML (1999) Characterization and expression of four proline-rich cell wall protein genes in Arabidopsis encoding two distinct subsets of multiple domain proteins. Plant Physiol 121:1081–1092PubMedCrossRefGoogle Scholar
  41. Francisco SM, Tierney ML (1990) Isolation and characterization of a proline-rich cell wall protein from soybean seedlings. Plant Physiol 94:1897–1902PubMedCrossRefGoogle Scholar
  42. Franssen HJ, Nap JP, Gloudemans T, Stiekema W, Van Dam H, Govers F, Louwerse J, Van Kammen A, Bisseling T (1987) Characterization of cDNA for nodulin-75 of soybean: a gene product involved in early stages of root nodule development. Proc Natl Acad Sci USA 84:4495–4499PubMedCrossRefGoogle Scholar
  43. Freshour G, Clay RP, Fuller MS, Albersheim P, Darvill AG, Hahn MG (1996) Developmental and tissue-specific structural alterations of the cell-wall polysaccharides of arabidopsis thaliana roots. Plant Physiol 110:1413–1429PubMedGoogle Scholar
  44. Freshour G, Bonin CP, Reiter WD, Albersheim P, Darvill AG, Hahn MG (2003) Distribution of fucose-containing xyloglucans in cell walls of the mur1 mutant of Arabidopsis. Plant Physiol 131:1602–1612PubMedCrossRefGoogle Scholar
  45. Galway ME, Heckman JW, Jr. Schiefelbein JW (1997) Growth and ultrastructure of Arabidopsis root hairs: the rhd3 mutation alters vacuole enlargement and tip growth. Planta 201: 209–218PubMedCrossRefGoogle Scholar
  46. 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 134:111–120CrossRefGoogle Scholar
  47. Hong JC, Nagao RT, Key JL (1989) Developmentally regulated expression of soybean proline-rich cell wall protein genes. Plant Cell 1:937–943PubMedCrossRefGoogle Scholar
  48. Ito H, Nishitani K (1999) Visualization of EXGT-mediated molecular grafting activity by means of a fluorescent-labeled xyloglucan oligomer. Plant Cell Physiol 40:1172–1176Google Scholar
  49. Jarvis MC (1984) Structure and properties of pectin gels in plant cell walls. Plant Cell Environ 7:153–164Google Scholar
  50. Jarvis MC (1992) Control of thickness of collenchyma cell walls by pectins. Planta 187:218–220CrossRefGoogle Scholar
  51. Jiang L, Yang SL, Xie LF, Puah CS, Zhang XQ, Yang WC, Sundaresan V, Ye D (2005) VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell 17:584–596PubMedCrossRefGoogle Scholar
  52. Jones MA, Shen JJ, Fu Y, Li H, Yang Z, Grierson CS (2002) The Arabidopsis Rop2 GTPase is a positive regulator of both root hair initiation and tip growth. Plant Cell 14:763–776PubMedCrossRefGoogle Scholar
  53. Kim CM, Park SH, Je BI, Park SH, Park SJ, Piao HL, Eun MY, Dolan L, Han CD (2007) OsCSLD1, a cellulose synthase-like D1 gene, is required for root hair morphogenesis in rice. Plant Physiol 143:1220–1230PubMedCrossRefGoogle Scholar
  54. Kimura S, Laosinchai W, Itoh T, Cui X, Linder CR, Brown RM, Jr. (1999) Immunogold labeling of rosette terminal cellulose-synthesizing complexes in the vascular plant vigna angularis. Plant Cell 11:2075–2086PubMedCrossRefGoogle Scholar
  55. Lee KJ, Sakata Y, Mau SL, Pettolino F, Bacic A, Quatrano RS, Knight CD, Knox JP (2005) Arabinogalactan proteins are required for apical cell extension in the moss Physcomitrella patens. Plant Cell 17:3051–3065PubMedCrossRefGoogle Scholar
  56. 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 102:2221–2226PubMedCrossRefGoogle Scholar
  57. Lu H, Chen M, Showalter AM (2001) Developmental expression and perturbation of arabinogalactan-proteins during seed germination and seedling growth in tomato. Physiol Plant 112:442–450PubMedCrossRefGoogle Scholar
  58. Matthysse AG, White S, Lightfoot R (1995) Genes required for cellulose synthesis in Agrobacterium tumefaciens. J Bacteriol 177:1069–1075PubMedGoogle Scholar
  59. McQueen-Mason S, Durachko DM, Cosgrove DJ (1992) Two endogenous proteins that induce cell wall extension in plants. Plant Cell 4:1425–1433PubMedCrossRefGoogle Scholar
  60. McQueen-Mason SJ, Cosgrove DJ (1995) Expansin mode of action on cell walls. Analysis of wall hydrolysis, stress relaxation, and binding. Plant Physiol 107:87–100PubMedGoogle Scholar
  61. Miller DD, Norbert CA et al (1997) From signal to form: aspects of the cytoskeleton-plasma membrane-cell wall continuum in root hair tips. J Exp Bot 48:1881–1896Google Scholar
  62. Mohnen D (1999) Biosynthesis of pectins and galactomannans. In: Nakanishi K, Meth-Cohn O (eds) Comprehensive natural products chemistry, vol 3. Elsevier, Amsterdam, pp 497–527CrossRefGoogle Scholar
  63. Newcomb EH, Bonnett HT (1965) Cytoplasmic microtubules and cell wall microfibril orientation in root hairs of radish. J Cell Biol 27:575–589PubMedCrossRefGoogle Scholar
  64. Nguema-Ona E, Andeme-Onzighi C, Aboughe-Angone S, Bardor M, Ishii T, Lerouge P, Driouich A (2006) The reb1–1 mutation of Arabidopsis. Effect on the structure and localization of galactose-containing cell wall polysaccharides. Plant Physiol 140:1406–1417PubMedCrossRefGoogle Scholar
  65. 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
  66. Oka T, Nemoto T, Jigami Y (2007) Functional analysis of Arabidopsis thaliana RHM2/MUM4, a multidomain protein involved in UDP-D-glucose to UDP-L-rhamnose conversion. J Biol Chem 282:5389–5403PubMedCrossRefGoogle Scholar
  67. 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 USA 93:12637–12642PubMedCrossRefGoogle Scholar
  68. Perrin R, Wilkerson C, Keegstra K (2001) Golgi enzymes that synthesize plant cell wall polysaccharides: finding and evaluating candidates in the genomic era. Plant Mol Biol 47:115–130PubMedCrossRefGoogle Scholar
  69. Petersen A, Becker WM, Moll H, Blumke M, Schlaak M (1995) Studies on the carbohydrate moieties of the timothy grass pollen allergen Phl p I. Electrophoresis 16:869–875PubMedCrossRefGoogle Scholar
  70. Pike RN, Bagarozzi D Jr, Travis J (1997) Immunological cross-reactivity of the major allergen from perennial ryegrass (Lolium perenne), Lol p I, and the cysteine proteinase, bromelain. Int Arch Allergy Immunol 112:412–414PubMedCrossRefGoogle Scholar
  71. Preuss ML, Santos-Serna J, Falbel TG, Bednarek SY, Nielsen E (2004) The Arabidopsis Rab GTPase RabA4b localizes to the tips of growing root hair cells. Plant Cell 16:1589–1603PubMedCrossRefGoogle Scholar
  72. Preuss ML, Schmitz AJ, Thole JM, Bonner HK, Otegui MS, Nielsen E (2006) A role for the RabA4b effector protein PI-4Kbeta1 in polarized expansion of root hair cells in Arabidopsis thaliana. J Cell Biol 172:991–998PubMedCrossRefGoogle Scholar
  73. Purugganan MM, Braam J, Fry SC (1997) The Arabidopsis TCH4 xyloglucan endotransglycosylase. Substrate specificity, pH optimum, and cold tolerance. Plant Physiol 115:181–190PubMedCrossRefGoogle Scholar
  74. Reiter WD, Vanzin GF (2001) Molecular genetics of nucleotide sugar interconversion pathways in plants. Plant Mol Biol 47:95–113PubMedCrossRefGoogle Scholar
  75. Reiter WD, Chapple CC, Somerville CR (1993) Altered growth and cell walls in a fucose- deficient mutant of Arabidopsis. Science 261:1032–1035PubMedCrossRefGoogle Scholar
  76. Richmond TA, Somerville CR (2000) The cellulose synthase superfamily. Plant Physiol 124:495–498PubMedCrossRefGoogle Scholar
  77. Richmond TA, Somerville CR (2001) Integrative approaches to determining Csl function. Plant Mol Biol 47:131–143PubMedCrossRefGoogle Scholar
  78. Saxena IM, Lin FC, Brown RM Jr (1990) Cloning and sequencing of the cellulose synthase catalytic subunit gene of Acetobacter xylinum. Plant Mol Biol 15:673–683PubMedCrossRefGoogle Scholar
  79. Scheible WR, Pauly M (2004) Glycosyltransferases and cell wall biosynthesis: novel players and insights. Curr Opin Plant Biol 7:285–295PubMedCrossRefGoogle Scholar
  80. Schiefelbein JW (2000) Constructing a plant cell. The genetic control of root hair development. Plant Physiol 124:1525–1531PubMedCrossRefGoogle Scholar
  81. Schiefelbein J, Galway M, Masucci J, Ford S (1993) Pollen tube and root-hair tip growth is disrupted in a mutant of Arabidopsis thaliana. Plant Physiol 103:979–985PubMedCrossRefGoogle Scholar
  82. Schnepf E, Witte O et al (1985) Tip cell growth and the frequency and distribution of particle rosettes in the plasmalemma: experimental studies in Funaria protonema cells. Protoplasma 127:222–229CrossRefGoogle Scholar
  83. Seifert GJ, Barber C, Wells B, Dolan L, Roberts K (2002) Galactose biosynthesis in Arabidopsis: genetic evidence for substrate channeling from UDP-D-Galactose into cell wall polymers. Curr Biol 12:1840–1845PubMedCrossRefGoogle Scholar
  84. Shaw SL, Dumais J, Long SR (2000) Cell surface expansion in polarly growing root hairs of Medicago truncatula. Plant Physiol 124:959–970PubMedCrossRefGoogle Scholar
  85. Sheng J, D’Ovidio R, Mehdy MC (1991) Negative and positive regulation of a novel proline-rich protein mRNA by fungal elicitor and wounding. Plant J 1:345–354PubMedCrossRefGoogle Scholar
  86. Sherrier DJ, VandenBosch KA (1994) Secretion of cell wall polysaccharides in Vicia root hairs. Plant J 5:185–195CrossRefGoogle Scholar
  87. Steele NM, Sulova Z, Campbell P, Braam J, Farkas V, Fry SC (2001) Ten isoenzymes of xyloglucan endotransglycosylase from plant cell walls select and cleave the donor substrate stochastically. Biochem J 355:671–679PubMedGoogle Scholar
  88. Suzuki H, Wagner T, Tierney ML (1993) Differential expression of two soybean (Glycine max L.) proline-rich protein genes after wounding. Plant Physiol 101:1283–1287PubMedGoogle Scholar
  89. 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 USA 100:1450–1455PubMedCrossRefGoogle Scholar
  90. Tierney ML, Wiechert J, Pluymers D (1988) Analysis of the expression of extensin and p33-related cell wall proteins in carrot and soybean. Mol Gen Genet 211:393–399CrossRefGoogle Scholar
  91. Vissenberg K, Fry SC, Verbelen JP (2001) Root hair initiation is coupled to a highly localized increase of xyloglucan endotransglycosylase action in Arabidopsis roots. Plant Physiol 127: 1125–1135PubMedCrossRefGoogle Scholar
  92. Wada M Staehelin LA (1981) Freeze-fracture observations on the plasma membrane, the cell wall, and the cuticle of growing protonema of Adiantum capillus-veneris. Planta 151: 462–468CrossRefGoogle Scholar
  93. Wang X, Cnops G, Vanderhaeghen R, De Block S, Van Montagu M, Van Lijsebettens M (2001) AtCSLD3, a cellulose synthase-like gene important for root hair growth in arabidopsis. Plant Physiol 126:575–586PubMedCrossRefGoogle Scholar
  94. 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 142:685–695PubMedCrossRefGoogle Scholar
  95. Whitney SE, Gidley MJ, McQueen-Mason SJ (2000) Probing expansin action using cellulose/hemicellulose composites. Plant J 22:327–334PubMedCrossRefGoogle Scholar
  96. Willats WG, McCartney L, Mackie W, Knox JP (2001) Pectin: cell biology and prospects for functional analysis. Plant Mol Biol 47:9–27PubMedCrossRefGoogle Scholar
  97. Williamson RE, Burn JE, Birch R, Baskin TI, Arioli T, Betzner AS, Cork A (2001) Morphology of rsw1, a cellulose-deficient mutant of Arabidopsis thaliana. Protoplasma 215:116–127PubMedCrossRefGoogle Scholar
  98. Wyatt RE, Nagao RT, Key JL (1992) Patterns of soybean proline-rich protein gene expression. Plant Cell 4:99–110PubMedCrossRefGoogle Scholar
  99. Wymer CL, Bibikova TN, Gilroy S (1997) Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana. Plant J 12:427–439PubMedCrossRefGoogle Scholar
  100. Yuan S, Wu Y, Cosgrove DJ (2001) A fungal endoglucanase with plant cell wall extension activity. Plant Physiol 127:324–333PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2009

Authors and Affiliations

  1. 1.Department of Molecular, Cellular, and Developmental BiologyUniversity of MichiganAnn ArborUSA

Personalised recommendations