Summary
In this review we integrate the information available on the cell biology of root hair formation with recent findings from the analysis of root hair mutants ofArabidopsis thaliana. The mature Arabidopsis root epidermis consists of root-hair-producing cells and non-root-hair-producing cells. Root hair growth begins with a swelling of the outer epidermal wall. It has been postulated that this is due to a pH-mediated localised cell wall loosening. From the bulge a single root hair emerges which grows by tip growth. The root hair tip consists of a vesicle-rich zone and an organelle-rich subapical zone. The vesicles supply new plasma membrane and cell wall material for elongation. The cytoskeleton and its associated regulatory proteins such as profilin and spectrin are proposed to be involved in the targeting of vesicles. Ca2+ influxes and gradients are present in hair tips, but their function is still unclear. Mutants have been isolated with lesions in various parts of the root hair developmental pathway from bulge identity and initiation, to control of tip diameter and extent and polarity of elongation.
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Abbreviations
- [Ca2+]c :
-
cytosolic calcium concentration
- MT:
-
microtubule
- PM:
-
plasma membrane
- VRZ:
-
vesicle-rich zone
- WT:
-
wild type
References
Bednarska E (1989) The effect of exogenous Ca2+ ions on pollen grain germination and pollen tube growth. Sex Plant Reprod 2: 53–58
Belford DS, Preston RD (1961) The structure and growth of root hairs. J Exp Bot 12: 157–168
Benkert R, Obermeyer G, Bentrup F-W (1997) The turgor pressure of growing lily pollen tubes. Protoplasma 198: 1–8
Berger F, Hung CY, Dolan L, Schiefelbein JW (1998) Control of cell division in the root epidermis ofArabidopsis thaliana. Dev Biol 194: 235–245
Bibikova TN, Zhigilei A, Gilroy S (1997) Root hair growth inArabidopsis thaliana is directed by calcium and an endogenous polarity. Planta 203: 495–505
—, Jacob T, Dahse I, Gilroy S (1998) Localized changes in apoplastic and cytoplasmic pH are associated with root hair development inArabidopsis thaliana. Development 125: 2925–2934
—, Blancaflor EB, Gilroy S (1999) Microtubules regulate tip growth and orientation in root hairs ofArabidopsis thaliana. Plant J 17: 657–665
Braun M, Baluška F, Von Witsch M, Menzel D (1999) Redistribution of actin, profilin and phosphatidylinositol-4,5-bisphosphate in growing and maturing root hairs. Planta 209: 435–443
Campbell P, Braam J (1999) Xyloglucan endotransglycosylases: diversity of genes, enzymes and potential wall-modifying functions. Trends Plant Sci 4: 361–366
Carroll AD, Moyen C, Van Kesteren P, Tooke F, Battey NH, Brownlee C (1998) Ca2+, annexins, and GTP modulate exocytosis from maize root cap protoplasts. Plant Cell 10: 1267–1276
Chan AY, Bailly M, Zebda N, Segall JE, Condeelis JS (2000) Role of cofilin in epidermal growth factor-stimulated actin polymerisation and lamellipod protrusion. J Cell Biol 148: 531–542
Condeelis J (1993) Life at the leading edge: the formation of cell protrusions. Annu Rev Cell Biol 9: 411–444
Cormack RGH (1962) Development of root hairs in angiosperms. Bot Rev 28: 446–464
Cosgrove DJ (1997a) Assembly and enlargement of the primary cell wall in plants. Annu Rev Cell Dev Biol 13: 171–201
— (1997b) Relaxation in a high stress environment: the molecular basis of extensible cell walls and cell enlargement. Plant Cell 9: 1031–1041
Cossart P (1995) Actin-based bacterial motility. Curr Opin Cell Biol 7: 94–101
Cyr RJ (1994) Microtubules in plant morphogenesis: role of the cortical array. Annu Rev Cell Biol 10: 153–180
Derksen J (1996) Pollen tubes: a model system for plant cell growth. Act Bot Neerl 109: 341–345
—, Rutten T, van Amstel T, De Win A, Doris F, Steer M (1995) Regulation of pollen tube growth. Act Bot Neerl 44: 93–119
de Ruijter NCA, Emons AMC (1999) Actin-binding proteins in plant cells. Plant Biol 1: 326–335
—, Rook MB, Bisseling T, Emons AMC (1998) Lipochito-oligosac-charides reinitiate root hair tip growth inVicia sativa with high calcium and spectrin-like antigen at the tip. Plant J 13: 341–350
Dolan L, Duckett CM, Grierson C, Linstead P, Schneider K, Lawson E, Dean C, Roberts K (1994) Clonal relationships and cell patterning in the root epidermis ofArabidopsis. Development 120: 2465–2474
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 67: 2401–2408
Favery B, Ryan E, Foreman J, Linstead P, Boudonck K, Shaw P, Steer M, Dolan L (2001)KOJAK is a cellulose synthase-like gene required for root hair cell morphogenesis inArabidopsis. Genes Dev 15: 79–89
Fry SC, Smith RC, Renwick KF, Martin DJ, Hodge SK, Matthews SK (1992) Xyloglucan endotransglycosylase, a new wall-loosening enzyme activity from plants. Biochem J 282: 821–828
Galway ME, Heckman JW Jr, Schiefelbein JW (1997) Growth and ultrastructure ofArabidopsis root hairs: therhd3 mutation alters vacuole enlargement and tip growth. Planta 201: 209–218
—, Lane DC, Schiefelbein JW (1999) Defective control of growth rate and cell diameter in tip-growing root hairs of therhd4 mutant ofArabidopsis thaliana. Can J Bot 77: 494–507
Gibbon BC, Kovar DR, Staiger CJ (1999) Latrunculin B has different effects on pollen germination and tube growth. Plant Cell 11: 2349–2363
Gilroy S, Jones DL (2000) Through form to function: root hair development and nutrient uptake. Trends Plant Sci 5: 56–60
Grierson CS, Roberts K, Feldmann K, Dolan L (1997) TheCOW1 locus ofArabidopsis acts afterRHD2, and in parallel withRHD3 andTIP1, to determine the shape, rate of elongation and number of root hairs produced from each site of hair-formation. Plant Physiol 115: 981–990
Heath JB (1995) Integration and regulation of hyphal tip growth. Can J Bot 73 Suppl: S131-S139
Heidemann SR (1996) Cytoplasmic mechanisms of axonal and dendritic growth in neurons. Int Rev Cytol 165: 235–296
Herrmann A, Felle H (1995) Tip growth in root hair cells ofSinapis alba L.: significance of internal and external Ca2+ and pH. New Phytpl 129: 523–533
Hurd DD, Saxton WM (1996) Kinesin mutations cause motor neurons disease phenotypes by disrupting fast axonal transport inDrosophila. Genetics 144: 1075–1085
Jones DL, Shaff JE, Kochian LV (1995) Role of calcium and other ions in directing root hair tip growth inLimnobium stoloniferum. Planta 197: 672–680
Kaminskyji SGW, Heath IB (1995) Integrin and spectrin homologues and cytoplasm wall adhesion in tip growth. J Cell Sci 108: 849–856
Kirchner J, Woehlke G, Schliwa M (1999) Universal and unique features of kinesin motors: insights from a comparison of fungal and animal conventional kinesins. Biol Chem 380: 915–921
Kost B, Mathur J, Chua N-H (1999a) Cytoskeleton in plant development. Curr Opin Plant Biol 2: 462–470
—, Lemichez E, Spielhofer P, Hong Y, Tolias K, Carpenter C, Chua N-H (1999b) Rac homologues and compartmentalized phosphatidylinositol 4,5-bisphosphate act in a common pathway to regulate polar pollen tube growth. J Cell Biol 145: 317–330
Kutschera U (1994) The current status of the acid-growth hypothesis. New Phytol 126: 549–569
Lehmler C, Steinberg G, Snetselaar KM, Schliwa M, Kahmann R, Bolker M (1997) Identification of a motor protein required for filamentous growth inUstilago maydis. EMBO J 16: 3464–3473
Lloyd CW, Wells B (1985) Microtubules are at the tips of root hairs and form helical patterns corresponding to inner wall fibrils. J Cell Sci 75: 225–238
Machesky LM, Insall RH (1999) Signaling to actin dynamics. J Cell Biol 26: 146 (2): 267–272
Masucci JD, Schiefelbein JW (1994) Therhd6 mutation ofArabidopsis thaliana alters root-hair initiation through an auxin- and ethylene-associated process. Plant Physiol 106: 1335–1346
Meyerowitz EM (1987)Arabidopsis thaliana. Annu Rev Genet 21: 93–111
Miller DD, Norbert CA, 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
— — —, 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
Money NP, Harold FM (1993) Two water molds can grow without measurable turgor pressure. Planta 190: 426–430
Newcomb EH, Bonnett HT (1965) Cytoplasmic microtubule and wall microfibril orientation in root hairs of radish. J Cell Biol 27: 575–589
Nicol F, Jauneau A, Vernhettes S, Canut H, Hofte H (1998) A plasma membrane-bound putative endo-1,4-β-D-glucanase is required for normal wall assembly and cell elongation inArabidopsis. EMBO J 17: 5563–5576
Oppenheimer DG, Pollock MA, Vacik J, Szymanski DB, Ericson B, Feldmann K, Marks MD (1997) Essential role of a kinesin-like protein inArabidopsis trichome morphogenesis. Proc Natl Acad Sci USA 94: 6261–6266
Rayle DL, Cleland RE (1992) The acid growth theory of auxin-induced cell elongation is alive and well. Plant Physiol 99: 1271–1274
Reiss H-D, Herth W (1985) Nifedipine-sensitive calcium channels are involved in polar growth of lily pollen tubes. J Cell Sci 76: 247–254
Rothkegel M, Mayboroda O, Rohde M, Wucherpfennig C, Valenta R, Jockusch BM (1996) Plant and animal profilins are functionally equivalent and stabilize microfilaments in living animal cells. J Cell Sci 109: 83–90
Ryan E, Grierson CS, Cavell A, Steer M, Dolan L (1998)TIP1 is required for both tip growth and non-tip growth inArabidopsis. New Phytol 138: 49–58
Schiefelbein JW, Somerville C (1990) Genetic control of root hair development inArabidopsis thaliana. Plant Cell 2: 235–243
—, Galway M, Masucci J, Ford S (1993) Pollen tube and root-hair tip growth is disrupted in a mutant ofArabidopsis thaliana. Plant Physiol 103: 979–985
Schnepf E (1993) Spitzenwachstum: Moosprotonemen als Modell für die Bildung von Zellwänden. Naturwissenschaften 80: 302–313
Seiler S, Plamann M, Schliwa M (1999) Kinesin and dynein mutants provide novel insights into the roles of vesicle traffic during cell morphogenesis inNeurospora. Curr Biol 12: 779–785
Staiger CJ, Yuan M, Valenta R, Shaw PJ, Warn RM, Lloyd CW (1994) Microinjected profilin affects cytoplasmic streaming in plant cells by rapidly depolymerising actin microfilaments. Curr Biol 4: 215–219
Tabish M, Siddiqui ZK, Nishikawa K, Siddiqui SS (1995) Exclusive expression of C.elegans osm-3 kinesin gene in chemosensory neurons open to the external environment. J Mol Biol 247: 377–389
Wang H, Lockwood SK, Hoeltzel MF, Schiefelbein JW (1997) TheROOT HAIR DEFECTIVES gene encodes an evolutionarily conserved protein with GTP-binding motifs and is required for regulated cell enlargement inArabidopsis. Genes Dev 11: 799–811
Wymer CL, Bibikova TN, Gilroy S (1997) Cytoplasmic free calcium distributions during the development of root hairs ofArabidopsis thaliana. Plant J 12: 427–439
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Dedicated to Professor Brian E. S. Gunning on the occasion of his 65th birthday
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Ryan, E., Steer, M. & Dolan, L. Cell biology and genetics of root hair formation inArabidopsis thaliana . Protoplasma 215, 140–149 (2001). https://doi.org/10.1007/BF01280310
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DOI: https://doi.org/10.1007/BF01280310