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Intracellular Organization: A Prerequisite for Root Hair Elongation and Cell Wall Deposition

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Plant Cell Monographs

Part of the book series: Plant Cell Monographs

Abstract

Cell growth requires not only production of matter, but in addition, the targeting, transport, and delivery of this matter to the site of cell expansion. Thus, a proper organization of cell structure, the cytoarchitecture, is a necessity for cell elongation. The actual process of cell growth in a cell under turgor pressure is Golgi vesicle membrane insertion into the plasma membrane and, at the same time, discharge of its contents into the existing cell wall at the site of wall expansion. If one of these prerequisites is missing, growth will not occur. Thus, the Golgi vesicle is the unit of cell growth. The tip-growing cell with robust cell expansion at a defined site is a model system “par excellence” to study this process. In this chapter, we discuss the so-called tip-growth unit, i.e., the assemblage of nucleus, endoplasmic reticulum, polysomes, Golgi bodies, Golgi vesicles, exocytosis machinery, clathrin-coated vesicles, endosomes, and mitochondria that specifically accumulate in the (sub)apical region of tip-growing root hairs, all working in concert to enable apical growth. The last paragraph of this chapter reviews methods used for the visualization of cellulose microfibrils.

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References

  • Baker Sugiyama J, Miles MJ 1998) Surface structure of native cellulose microcrystals by AFM. Appl Phys A 66:S559– S563

    ADS  CAS  Google Scholar 

  • Bibikova TN, Blancaflor EB, Gilroy S (1999) Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana. Plant J 17:657– 665

    Article  PubMed  CAS  Google Scholar 

  • Blancaflor EB, Wang YS, Motes CM (2006) Organization and function of the actin cytoskeleton in developing root cells. Int Rev Cytol 252:219–264

    Article  PubMed  CAS  Google Scholar 

  • Cardenas L, Vidali L, Dominguez J, Perez H, Sanchez F, Hepler PK, Quinto C (1998) Rearrangement of actin microfilaments in plant root hairs responding to Rhizobium etli nodulation signals. Plant Physiol 116:871–877

    Article  CAS  Google Scholar 

  • de Ruijter NCA, Rook MB, Bisseling T, Emons AMC (1998) Lipochito-oligosaccharides re- initiate root hair tip growth in Vicia sativa with high calcium and spectrin-like antigen at the tip. Plant J 13:341–350

    Article  Google Scholar 

  • de Ruijter NCA, Bisseling T, Emons AMC (1999) Rhizobium Nod factors induce an increase in sub-apical fine bundles of actin filaments in Vicia sativa root hairs within minutes. Mol Plant Microbe Interact 12:829–832

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Dhonukshe P, Aniento F, Hwang I, Robinson DG, Mravec J, Stierhof YD, Friml J (2007) Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr Biol 17:520–527

    Article  PubMed  CAS  Google Scholar 

  • Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, Scheres B (1993) Cellular-organization of the Arabidopsis-Thaliana root. Dev Biol 119:71–84

    CAS  Google Scholar 

  • Emons AMC (1985) Plasma-membrane rosettes in root hairs of Equisetum hyemale. Planta 163:350–359

    Article  Google Scholar 

  • Emons AMC (1986) Cell-wall texture in root hairs of the genus Equisetum. Can J Bot-Revue Canadienne De Botanique 64:2201–2206

    Article  Google Scholar 

  • Emons AMC (1987a) A mathematical-model for helicoidal cell-wall deposition. Acta Botanica Neerl 36:147–148

    Google Scholar 

  • Emons AMC (1987b) The cytoskeleton and secretory vesicles in root hairs of equisetum and limnobium and cytoplasmic streaming in root hairs of equisetum. Ann Bot 60:625–632

    Google Scholar 

  • Emons AMC (1988) Methods for visualizing cell-wall texture. Acta Botanica Neerl 37:31–38

    Google Scholar 

  • Emons AMC (1989) Helicoidal microfibril deposition in a tip-growing cell and microtubule alignment during tip morphogenesis – a dry-cleaving and freeze-substitution study. Can J Bot-Revue Canadienne De Botanique 67:2401–2408

    Google Scholar 

  • Emons AMC (1994) Winding threads around plant-cells – a geometrical model for microfibril deposition. Plant Cell Environ 17:3–14

    Article  Google Scholar 

  • Emons AMC, Wolters Arts AMC (1983) Cortical microtubules and microfibril deposition in the cell-wall of root hairs of equisetum-hyemale. Protoplasma 117:68–81

    Article  Google Scholar 

  • Emons AMC, Derksen J (1986) Microfibrils, microtubules and microfilaments of the trichoblast of equisetum hyemale. Acta Botanica Neerl 35:311–320

    Google Scholar 

  • Emons AMC, Traas JA (1986) Coated pits and coated vesicles on the plasma-membrane of plant-cells. Eur J Cell Biol 41:57–64

    Google Scholar 

  • Emons AMC, Mulder BM (1998) The making of the architecture of the plant cell wall: how cells exploit geometry. Proc Natl Acad Sci USA 95:7215–7219

    Article  PubMed  ADS  CAS  Google Scholar 

  • Emons AM, Mulder BM (2000) How the deposition of cellulose microfibrils builds cell wall architecture. Trends Plant Sci 5:35–40

    Article  PubMed  CAS  Google Scholar 

  • Emons AMC, Schel JHN, Mulder BM (2002) The geometrical model for microfibril deposition and the influence of the cell wall matrix. Plant Biol 4:22–26

    Article  CAS  Google Scholar 

  • Footer MJ, Kerssemakers JW, Theriot JA, Dogterom M (2007) Direct measurement of force generation by actin filament polymerization using an optical trap. Proc Natl Acad Sci USA 104:2181–2186

    Article  PubMed  ADS  CAS  Google Scholar 

  • Frey-Wyssling A, Mühlethaler K (1949) Über den feinbau der zellwand von wurzelhaaren. Mikroskopie 4:257–266

    Google Scholar 

  • Giannone G, Dubin-Thaler BJ, Rossier O, Cai Y, Chaga O, Jiang G, Beaver W, Dobereiner HG, Freund Y, Borisy G, Sheetz MP (2007) Lamellipodial actin mechanically links myosin activity with adhesion-site formation. Cell 128:561–575

    Article  PubMed  CAS  Google Scholar 

  • Gisbergen. (2007)

    Google Scholar 

  • Haas TJ, Sliwinski MK, Martinez DE, Preuss M, Ebine K, Ueda T, Nielsen E, Odorizzi G, Otegui MS (2007) The Arabidopsis AAA ATPase SKD1 is involved in multivesicular endosome function and interacts with its positive regulator LYST-INTERACTING PROTEIN5. Plant Cell 19:1295–1312

    Article  PubMed  CAS  Google Scholar 

  • Heidstra R, Yang WC, Yalcin Y, Peck S, Emons AM, vanKammen A, Bisseling T (1997) Ethylene provides positional information on cortical cell division but is not involved in Nod factor-induced root hair tip growth in Rhizobium-legume interaction. Dev Biol 124:1781–1787

    CAS  Google Scholar 

  • Holweg CL (2007) Living markers for actin block myosin-dependent motility of plant organelles and auxin. Cell Motil Cytoskeleton 64:69–81

    Article  PubMed  CAS  Google Scholar 

  • Kennedy CJ, Cameron GJ, Sˇturcova´ A, Apperley DC, Altaner C, Wess TJ, Jarvis MC (2007) Microfibril diameter in celery collenchyma cellulose: x-ray scattering and NMR evidence. Cellulose 14:235–246

    Article  CAS  Google Scholar 

  • Ketelaar T, Emons AMC (2001) The cytoskeleton in plant cell growth: lessons from root hairs. New Phytol 152:409–418

    Article  CAS  Google Scholar 

  • Ketelaar T, de Ruijter NCA, Emons AMC (2003) Unstable F-actin specifies the area and microtubule direction of cell expansion in Arabidopsis root hairs. Plant Cell 15:285–292

    Article  PubMed  CAS  Google Scholar 

  • Ketelaar T, Anthony RG, Hussey PJ (2004) Green fluorescent protein-mTalin causes defects in actin organization and cell expansion in Arabidopsis and inhibits actin depolymerizing factor’s actin depolymerizing activity in vitro. Plant Physiol 136:3990–3998

    Article  PubMed  CAS  Google Scholar 

  • Ketelaar T, Faivre-Moskalenko C, Esseling JJ, de Ruijter NCA, Grierson CS, Dogterom M, Emons AMC (2002) Positioning of nuclei in Arabidopsis root hairs: an actin-regulated process of tip growth. Plant Cell 14:2941–2955

    Article  PubMed  CAS  Google Scholar 

  • McCann MC, Wells B, Roberts K (1990) Direct visualization of cross-links in the primary plant cell wall. J Cell Sci 96:323–334

    Google Scholar 

  • McCann MC, Stacey NJ, Wilson R, Roberts K (1993) Orientation of macromolecules in the walls of elongating carrot cells. J Cell Sci 106(Pt 4):1347–1356

    PubMed  CAS  Google Scholar 

  • Miller DD, de Ruijter NCA, Emons AMC (1997) From signal to form: aspects of the cytoskeleton plasma membrane cell wall continuum in root hair tips. J Exp Bot 48:1881–1896

    CAS  Google Scholar 

  • Miller DD, de Ruijter NCA, Bisseling T, Emons AMC (1999) The role of actin in root hair morphogenesis: studies with lipochito-oligosaccharide as a growth stimulator and cytochalasin as an actin perturbing drug. Plant J 17:141–154

    Article  CAS  Google Scholar 

  • Miller DD, Leferink-ten Klooster HB, Emons AM (2000a) Lipochito-oligosaccharide nodulation factors stimulate cytoplasmic polarity with longitudinal endoplasmic reticulum and vesicles at the tip in vetch root hairs. Mol Plant Microbe Interact 13:1385–1390

    Article  CAS  Google Scholar 

  • Miller DD, Leferink-ten Klooster HB, Emons AMC (2000b) Lipochito-oligosaccharide nodulation factors stimulate cytoplasmic polarity with longitudinal endoplasmic reticulum and vesicles at the tip in vetch root hairs. Mol Plant Microbe Interact 13:1385–1390

    Article  CAS  Google Scholar 

  • Mogilner A, Rubinstein B (2005) The physics of filopodial protrusion. Biophys J 89:782–795

    Article  PubMed  CAS  Google Scholar 

  • Mulder BM, Emons AMC (2001) A dynamical model for plant cell wall architecture formation. J Math Biol 42:261–289

    Article  PubMed  CAS  MathSciNet  MATH  Google Scholar 

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

    Article  PubMed  ADS  CAS  Google Scholar 

  • Pluymakers HJ (1982) A helicoidal cell wall texture in root hairs of Limnobium stoloniferum. Protoplasma 112:107–116

    Article  Google Scholar 

  • Refrégier G, Pelletier S, Jaillard D, Höfte H (2004) Interaction between wall deposition and cell elongation in dark-grown hypocotyl cells in Arabidopsis. Plant Physiol 136:959–968

    Article  Google Scholar 

  • Roland JC, Vian B, Reis D (1975) Observations with cytochemistry and ultracryotomy on the fine structure of the expanding walls in actively elongating plant cells. J Cell Sci 19:239–259

    PubMed  CAS  Google Scholar 

  • Sieberer B, Emons AMC (2000) Cytoarchitecture and pattern of cytoplasmic streaming in root hairs of Medicago truncatula during development and deformation by nodulation factors. Protoplasma 214:118–127

    Article  Google Scholar 

  • Sieberer BJ, Timmers ACJ, Lhuissier FGP, Emons AMC (2002) Endoplasmic Microtubules configure the subapical cytoplasm and are required for fast growth of Medicago truncatula root hairs. Plant Physiol 130:977–988

    Article  PubMed  CAS  Google Scholar 

  • Sieberer BJ, Timmers AC, Emons AM (2005a) Nod factors alter the microtubule cytoskeleton in Medicago truncatula root hairs to allow root hair reorientation. Mol Plant Microbe Interact 18:1195–1204

    Article  CAS  Google Scholar 

  • Sieberer BJ, Ketelaar T, Esseling JJ, Emons AM (2005b) Microtubules guide root hair tip growth. New Phytol 167:711–719

    Article  CAS  Google Scholar 

  • Sieberer BJ, Ketelaar T, Esseling JJ, Emons AMC (2005c) Microtubules guide root hair tip growth. New Phytol 167:711–719

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Van Bruaene N, G, Joss Van Oostveldt P (2004) Reorganization and in vivo dynamics of microtubules during Arabidopsis root hair development. Plant Physiol 136:3905–3919

    Article  PubMed  CAS  Google Scholar 

  • van der Honing HS, Emons AM, Ketelaar T (2007) Actin based processes that could determine the cytoplasmic architecture of plant cells. Biochim Biophys Acta 1773:604–614

    Article  PubMed  CAS  Google Scholar 

  • Vos JW, Dogterom M, Emons AMC (2004) Microtubules become more dynamic but not shorter during preprophase band formation: a possible “search-and-capture” mechanism for microtubule translocation. Cell Motil Cytoskeleton 57:246–258

    Article  PubMed  Google Scholar 

  • Wang X, Teng Y, Wang Q, Li X, Sheng X, Zheng M, Samaj J, Baluska F, Lin J (2006) Imaging of dynamic secretory vesicles in living pollen tubes of Picea meyeri using evanescent wave microscopy. Plant Physiol 141:1591–1603

    Article  PubMed  CAS  Google Scholar 

  • Weerasinghe RR, Bird DM, Allen NS (2005) Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus. Proc Natl Acad Sci USA 102:3147–3152

    Article  PubMed  ADS  CAS  Google Scholar 

  • Wel NNVD, Putman CAJ, Noort SJT, Grooth BGD, Emons AMC (1996) Atomic force microscopy of pollen grains, cellulose microfibrils, and protoplasts. Protoplasma 194:29–39

    Article  Google Scholar 

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Acknowledgment

We thank Dr. David Barker, Castanet Tolosan, France, for his useful comments on this chapter, and Dr. John Esseling for the drawing of Fig. 1. T.K. was supported by VENI fellowship 863.04.003 from the Dutch Science Foundation (NWO).

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Correspondence to A. M. Emons .

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© 2008 Springer-Verlag

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Emons, A.M., Ketelaar, T. (2008). Intracellular Organization: A Prerequisite for Root Hair Elongation and Cell Wall Deposition. In: Plant Cell Monographs. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7089_2008_4

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  • DOI: https://doi.org/10.1007/7089_2008_4

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