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Root hairs: Specialized tubular cells extending root surfaces

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Abstract

Root hairs are tubular extensions of epidermal cells that have their origin either in any protoderm cell or in specialized protoderm cells called trichoblasts. These latter cells are the result of an asymmetric cytokinesis determined by the positioning of a pre-prophase band of microtubules. The smaller sibling cell is the trichoblast and specializes physiologically and structurally prior to root hair outgrowth. Several genes are involved in the initiation and outgrowth of root hairs. Elongation of root hairs is by tip growth, and, correlated with this, cytoplasmic organelles and cytoskeletal elements show a polarized distribution; the apical dome consists of numerous vesicles, many associated with cell wall synthesis. The relationship between cellulose microfibril deposition and the pattern of cortical microtubules has received considerable attention, as has the role of the cytoskeleton and calcium in controlling cytoplasmic streaming. Root hairs extend the absorbing surface of the root and therefore have been studied in terms both of physiological characteristics of the plasma membrane and uptake of water and of various ions in the soil solution. Many plant species develop soil sheaths (rhizosheaths) which protect the root surface from desiccation and harbour various microorganisms; root hairs are intimately involved in these sheaths. Various growth regulators have been studied in terms of their effect on the structure and function of root hairs. Root hairs play a significant role in the interaction between plants and nitrogen-fixing microorganisms (e.g.,Rhizobium, Frankia) and symbiotic mycorrhizal fungi.

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Literature Cited

  • Abeysekera, R. M. &M. E. McCully. 1993. The epidermal surface of the maize root tip. I. Development in normal roots. New Phytol.125: 413–429.

    Article  Google Scholar 

  • Abutalybov, M. G. &T. S. Akhundova. 1982. Cytokinin participation in regulation of potassium ion activity in root epidermal cells. Soviet Pl. Physiol.29: 395–402.

    Google Scholar 

  • Ahmad, M. &M. Cailloux. 1971. The effects of malonate on absorption of water by root hairs ofAvena sativa. Canad. J. Bot.49: 521–528.

    CAS  Google Scholar 

  • — &M. Cailloux. 1972. Effects of some respiratory inhibitors on water flux in root hairs ofAvena sativa. Canad. J. Bot.50: 575–579.

    Article  CAS  Google Scholar 

  • Arondel, V. &J. C. Kader. 1990. Lipid transfer in plants. Experientia46: 579–585.

    Article  PubMed  CAS  Google Scholar 

  • Avers, C. J. 1963. Fine structure ofPhleum root meristem cells. II. Mitotic asymmetry and cellular differentiation. Amer. J. Bot.50: 140–148.

    Article  Google Scholar 

  • Ayling, S. M. &R. C. Butler. 1993. Time-series analysis of measurements on living cells illustrated by analysis of particle movement in the cytoplasm of tomato root hairs. Protoplasma172: 124–131.

    Article  Google Scholar 

  • —,C. Brownlee &D. T. Clarkson. 1994. The cytoplasmic streaming response of tomato root hairs to auxin; observations of cytosolic calcium levels. J. Pl. Physiol.143: 184–188.

    CAS  Google Scholar 

  • Baon, J. B., S. E. Smith &A. M. Alston. 1994. Growth response and phosphorus uptake of rye with long and short root hairs: Interactions with mycorrhizal infection. Pl. & Soil167: 247–254.

    Article  CAS  Google Scholar 

  • Barbieri, P., A. Bernardi, E. Galli &G. Zanetti. 1988. Effects of inoculation with different strains ofAzospirillum brasiliense on wheat roots development. Pages 181–188in W. Klingmüller (ed.),Azospirillum. IV. Genetics, physiology, ecology. Springer-Verlag, Berlin.

    Google Scholar 

  • Barley, K. P. &A. D. Rovira. 1970. The influence of root hairs on the uptake of phosphate. Commun. Soil Sci. Pl. An.1: 287–292.

    CAS  Google Scholar 

  • Bashan, Y. 1991. Changes in membrane potential of intact soybean root elongation zone cells induced byAzospirillum brasiliense. Canad. J. Microbiol.37: 958–963.

    Google Scholar 

  • — &H. Levanony. 1990. Current status ofAzospirillum inoculation technology:Azospirillum as a challenge for agriculture. Canad. J. Microbiol.36: 591–608.

    CAS  Google Scholar 

  • —,L. Alcarez-Melendez &G. Toledo. 1992. Responses of soybean and cowpea root membranes to inoculation withAzospirillum brasiliense. Symbiosis13: 217–228.

    Google Scholar 

  • —,Y. Ream, H. Levanony &A. Sade. 1989. Nonspecific responses in plant growth, yield, and root colonization of noncereal crop plants to inoculation withAzospirillum brasiliense Cd. Canad. J. Bot.67: 1317–1324.

    Article  Google Scholar 

  • Bauer, W. D. 1981. Infection of legumes by rhizobia. Annual Rev. Pl. Physiol.32: 407–449.

    Article  CAS  Google Scholar 

  • Baylis, G. T. 1975. The magnolioid mycorrhiza and mycotrophy in root systems derived from it. Pages 373–389in F. E. Sanders, B. Mosse, & P. B. Tinker (eds.), Endomycorrhizas. Academic Press, London.

    Google Scholar 

  • Belford, D. S. &R. D. Preston. 1961. The structure and growth of root hairs. J. Exp. Bot.12: 157–168.

    Article  CAS  Google Scholar 

  • Bell, P. F., R. L. Chaney &J. S. Angle. 1988. Staining localization of ferric reduction on roots. J. Pl. Nutr.11: 1237–1252.

    CAS  Google Scholar 

  • Bender, G. L., M. Nayuda, W. Goydych &B. Rolfe. 1987a. Early infection events in the nodulation of the non-legumeParasponia andersonii byBradyrhizobium. Pl. Sci.51: 285–293.

    Article  Google Scholar 

  • —,W. Goydych, B. Rolfe &M. Nayuda. 1987b. The role ofRhizobium conserved and host specific nodulation genes in the infection of the non-legumeParasponia andersonii. Molec. Gen. Genet.210: 299–306.

    Article  CAS  Google Scholar 

  • Berry, A. M. &M. E. McCully. 1990. Callose-containing deposits in relation to root-hair infections ofAlnus rubra by Frankia. Canad. J. Bot.68: 798–802.

    Google Scholar 

  • — &J. G. Torrey. 1983. Root hair deformation in the infection process ofAlnus rubra. Canad. J. Bot.61: 2863–2876.

    Google Scholar 

  • —,L. McIntyre &M. E. McCully. 1986. Fine structure of root hair infection leading to nodulation in theFrankia-Alnus symbiosis. Canad. J. Bot.64: 292–305.

    Article  Google Scholar 

  • Berti, A. &H. Felle. 1985. Cytoplasmic pH of root hair cells ofSinapis alba recorded by a pH-sensitive microelectrode. Does fusicoccin stimulate the proton pump by cytoplasmic acidification? J. Exp. Bot.36: 1142–1149.

    Article  Google Scholar 

  • Bhat, K. K. S. &P. H. Nye. 1973. Diffusion of phosphate to plant roots in soil. I. Quantitative autoradiography of the depletion zone. Pl. & Soil38: 161–175.

    Article  CAS  Google Scholar 

  • Bhuvaneswari, T. V., B. G. Turgeon &W. D. Bauer. 1980. Early events in the infection of soybean (Glycine max L. Merr) byRhizobium japonicum. I. Localization of infectible root cells. Pl. Physiol.66: 1027–1031.

    CAS  Google Scholar 

  • Bienfait, H. F., J. Duivenvoorden &W. Verkerke. 1982. Ferric reduction by roots of chlorotic bean plants: Indication for an enzymatic process. J. Pl. Nutr.5: 451–456.

    CAS  Google Scholar 

  • Bittner, A. &C. Buschmann. 1983. Uptake and translocation of K+, Ca2+ and Mg2+ by seedlings ofRaphanus sativus L. treated with kinetin. Z. Pflanzenphysiol.109: 181–189.

    CAS  Google Scholar 

  • Boddey, R. M. &J. Döbereiner. 1982. Association ofAzospirillum and other diazotrophs with tropical graminae. Pages 28–47in 12th International Congress on Soil Science symposia papers. Vol. 1, 8–16 Feb. 1982. New Delhi. International Society of Soil Science, Food and Agriculture Organization, Rome.

    Google Scholar 

  • Bole, J. B. 1973. Influence of root hairs in supplying soil phosphorus to wheat. Canad. J. Soil Sci.53: 169–175.

    CAS  Google Scholar 

  • Bonfante-Fasolo, P., S. Perroto, B. Testa &A. Faccio. 1987. Ultrastructural localization of cell surface sugar residues in ericoid mycorrhizal fungi by gold-labelled lectins. Protoplasma139: 25–35.

    Article  Google Scholar 

  • Bonnett, H. T. Jr. &E. H. Newcomb. 1966. Coated vesicles and other cytoplasmic components of growing root hairs of radish. Protoplasma62: 59–75.

    Article  Google Scholar 

  • Brewin, N. 1991. Development of the legume root nodule. Annual Rev. Cell Biol.7: 191–226.

    CAS  Google Scholar 

  • Brown, A. &W. A. Sinclair. 1981. Colonization and infection of primary roots of Douglas-fir seedlings by the ectomycorrhizal fungusLaccaria laccata. Forest Sci.27(1): 111–124.

    Google Scholar 

  • Buckhout, T. J., P. F. Bell, D. G. Luster &R. L. Chaney. 1989. Iron-stress induced redox activity in tomato (Lycopersicum esculentum Mill.) is localized on the plasma membrane. Pl. Physiol.90: 151–156.

    CAS  Google Scholar 

  • Buckley, R. 1982. Sand rhizosheath of an arid zone grass. Pl. & Soil66: 417–421.

    Article  Google Scholar 

  • Burggraaf, A. J. P., J. Van der Linden &T. Tak. 1983. Studies on the localization of infectible cells onAlnus glutinosa roots. Pl. & Soil74: 175–188.

    Article  Google Scholar 

  • Caetano-Anolés, G., D. K. Crist-Estes &W. D. Bauer. 1988. Chemotaxis ofRhizobium meliloti to the plant flavone luteolin requires functional nodulation genes. J. Bacteriol.170: 3164.

    Google Scholar 

  • Cailloux, M. 1972. Metabolism and the absorption of water by root hairs. Canad. J. Bot.50: 557–573.

    Article  CAS  Google Scholar 

  • Callaham, D. A. &J. G. Torrey. 1977. Prenodule formation and primary nodule development in roots ofComptonia (Myricaceae). Canad. J. Bot.55: 2306–2318.

    Article  Google Scholar 

  • ——. 1981. The structural basis for infection of root hairs ofTrifolium repens byRhizobium. Canad. J. Bot.59: 1647–1664.

    Google Scholar 

  • —,W. Newcomb, J. G. Torrey &R. L. Peterson. 1979. Root hair infection in actinomycete-induced root nodule initiation inCasuarina, Myrica andComptonia. Bot. Gaz.140: 51–59.

    Article  Google Scholar 

  • Caradus, J. R. 1979. Selection for root hair length in white clover (Trifolium repens L.). Euphytica28: 489–494.

    Article  Google Scholar 

  • Chandler, M. R. 1978. Some observations on infection ofArachis hypogaea L. byRhizobium. J. Exp. Bot.29: 749–755.

    Article  Google Scholar 

  • —,A. Date &R. J. Roughly. 1982. Infection and root-nodule development inStylosanthes species byRhizobium. J. Exp. Bot.33: 47–57.

    Article  Google Scholar 

  • Chaney, R. L. &P. F. Bell. 1987. Complexity of iron nutrition: Lessons for plant-soil interaction research. J. Pl. Nutr.10: 963–994.

    CAS  Google Scholar 

  • —,Y. Chen, C. E. Green, M. J. Holden, P. F. Bell, D. G. Luster &J. S. Angle. 1992. Root hairs on chlorotic tomatoes are an effect of chlorosis rather than part of the adaptive Fe-stress response. J. Pl. Nutr.15: 1857–1875.

    CAS  Google Scholar 

  • Clarkson, D. T. 1985. Factors affecting mineral nutrient acquisition by plants. Annual Rev. Pl. Physiol.36: 77–115.

    Article  CAS  Google Scholar 

  • —. 1991. Root structure and sites of ion uptake. Pages 417–453in Y. Waisel, A. Eshel, & U. Kafkai (eds.), Plant roots, the hidden half. Marcel Dekker, New York.

    Google Scholar 

  • —,C. Brownlee &S. M. Ayling. 1988. Cytoplasmic calcium measurements in intact higher plants cells: Results from fluorescence ratio imaging of fura-2. J. Cell Sci.91: 71–80.

    CAS  Google Scholar 

  • Cooper, K. M. &R. M. Brown Jr. 1981. Growth of radish root hairs in substances which alter cellulose synthesis. J. Cell Biol.91: 146a.

    Article  Google Scholar 

  • Cormack, R. G. H. 1949. The development of root hairs in angiosperms. Bot. Rev. (Lancaster)15: 583–612.

    Article  Google Scholar 

  • —. 1962. The development of root hairs in angiosperms II. Bot. Rev. (Lancaster)28: 446–464.

    CAS  Google Scholar 

  • Crossett, A. N. &D. J. Campbell. 1975. The effects of ethylene in the root environment upon the development of barley. Pl. & Soil42: 453–464.

    Article  CAS  Google Scholar 

  • Crossman, S. M. &W. A. Hill. 1987. Inoculation of sweet potato withAzospirillum. Hort. Sci.22: 420–422.

    Google Scholar 

  • Cutter, E. G. &L. J. Feldman. 1970a. Trichoblasts inHydrocharis I. Origin, differentiation, dimensions and growth. Amer. J. Bot.57: 190–201.

    Article  Google Scholar 

  • ——. 1970b. Trichoblasts inHydrocharis II. Nucleic acids, proteins and a consideration of cell growth in relation to endopolyploidy. Amer. J. Bot.57: 202–211.

    Article  Google Scholar 

  • — &C.-Y. Hung. 1972. Symmetric and asymmetric mitosis and cytokinesis in the root tip ofHydrocharis morsus-ranae L. J. Cell Sci.11: 723–737.

    PubMed  CAS  Google Scholar 

  • Czernik, C. A. &C. J. Avers. 1964. Phosphatase activity and cellular differentiation inPhleum root meristem. Amer. J. Bot.51: 424–431.

    Article  CAS  Google Scholar 

  • Dart, P. J. 1971. Scanning electron microscopy of plant roots. J. Exp. Bot.22: 163–168.

    Article  Google Scholar 

  • Dazzo, F., G. Truchet, R. Hollingsworth, E. Hrabak, H. S. Pankratz, S. Philip-Hollingsworth, J. Salzwedel, K. Chapman, L. Appenzeller, A. Squartini, D. Gerhold &G. Orgambide. 1991.Rhizobium lipopolysaccharide modulates infection thread development in white clover root hairs. J. Bacteriol.17: 5371–5384.

    Google Scholar 

  • —,W. E. Yanke &W. J. Brill. 1978. Trifoliin: ARhizobium recognition protein from white clover. Biochim. Biophys. Acta539: 276–286.

    PubMed  CAS  Google Scholar 

  • Derksen, J. &A. M. Emons. 1990. Microtubules in tip growth systems. Pages 147–181in I. B. Heath (ed.), Tip growth in plant and fungal cells. Academic Press, San Diego.

    Google Scholar 

  • De Vos, C. R., H. J. Lubberding &H. F. Bienfait. 1986. Rhizosphere acidification as a response to iron deficiency in bean plants. Pl. Physiol.81: 842–846.

    Article  Google Scholar 

  • Diaz, C., P. van, R. Bakhuizen, G. J. Logman, E. J. Lugtenberg &J. Kijne. 1986. Correlation between infection byRhizobium leguminosarum and lectin on the surface ofPisum sativum L. roots. Planta168: 350–359.

    Article  CAS  Google Scholar 

  • —,L. Melchers, P. Hooykaas, B. Lugtenberg &J. Kijne. 1989. Root lectin as a determinant of host-plant specificity in theRhizobium-legume symbiosis. Nature338: 579–581.

    Article  CAS  Google Scholar 

  • Dosier, L. W. &J. L. Riopel. 1977. Differential enzyme activity during trichoblast differentiation inElodea canadensis. Amer. J. Bot.64: 1049–1056.

    Article  CAS  Google Scholar 

  • ——. 1978. Origin, development, and growth of differentiating trichoblasts inElodea canadensis. Amer. J. Bot.65: 813–822.

    Article  Google Scholar 

  • Duell, R. W. &G. R. Peacock. 1985. Rhizosheaths on mesophytic grasses. Crop Sci.25: 880–883.

    Google Scholar 

  • Emons, A. M. C. 1982. Microtubules do not control microfibril orientation in a helicoidal wall. Protoplasma113: 85–87.

    Article  Google Scholar 

  • —. 1985. Plasma-membrane rosettes in root hairs ofEquisetum hyemale. Planta163: 350–359.

    Article  Google Scholar 

  • —. 1987. The cytoskeleton and secretory vesicles in root hairs ofEquisetum andLimnobium and cytoplasmic streaming in root hairs ofEquisetum. Ann. Bot.60: 625–632.

    Google Scholar 

  • —. 1989. Helicoidal microfibril deposition in a tip-growing cell and microtubule alignment during tip morphogenesis: A dry cleaving and freeze substitution study. Canad. J. Bot.67: 2401–2408.

    Google Scholar 

  • — &J. Derksen. 1986. Microfibrils, microtubules and microfilaments of the trichoblast ofEquisetum hyemale. Acta Bot. Neerl.35: 311–320.

    Google Scholar 

  • — &N. van Maaren. 1987. Helicoidal cell wall texture in root hairs. Planta170: 145–151.

    Article  Google Scholar 

  • — &A. M. C. Wolters-Arts. 1983. Cortical microtubules and microfibril deposition in the cell wall of root hairs ofEquisetum hyemale. Protoplasma117: 68–81.

    Article  Google Scholar 

  • Ewens, M. &R. A. Leigh. 1985. The effect of nutrient solution composition on the length of root hairs of wheat (Triticum aestivum L.). J. Exp. Bot.36: 713–724.

    Article  CAS  Google Scholar 

  • Fallik, E., Y. Okon &M. Fisher. 1988. Growth response of maize roots toAzospirillum inoculation: Effect of soil organic matter content, number of rhizosphere bacteria and timing of inoculation. Soil. Biol. Biochem.20: 45–49.

    Article  Google Scholar 

  • Felle, H. 1982. Effects of fusicoccin upon membrane potential, resistance and current-voltage characteristics in root hairs ofSinapis alba. Pl. Sci. Lett.25: 219–225.

    Article  CAS  Google Scholar 

  • —. 1987. Proton transport and pH control inSinapis alba root hairs: A study carried out with double-barrelled pH microelectrodes. J. Exp. Bot.38: 340–354.

    Article  CAS  Google Scholar 

  • —,A. Tretyn &G. Wagner. 1992. The role of the plasma-membrane Ca2+-ATPase in Ca2+ homeostasis inSinapis alba root hairs. Planta188: 306–313.

    Article  CAS  Google Scholar 

  • Fisher, R. F. &S. R. Long. 1992.Rhizobium-plant signal exchange. Nature357: 655–660.

    Article  PubMed  CAS  Google Scholar 

  • Foehse, D. &A. Jungk. 1983. Influence of phosphate and nitrate supply on root hair formation of rape, spinach and tomato plants. Pl. & Soil74: 359–368.

    Article  CAS  Google Scholar 

  • Foster, R. C. 1982. The fine structure of epidermal cell mucilages of roots. New Phytol.91: 727–740.

    Article  Google Scholar 

  • Franssen, H., I. Vijn, W. Yang &T. Bisseling. 1992. Developmental aspects of the Rhizobium-legume symbiosis. Pl. Molec. Biol.19: 89–107.

    Article  CAS  Google Scholar 

  • Fyson, A., P. Kerr, J. N. A. Lott &A. Oaks. 1988. The structure of the rhizosphere of maize seedling roots, a cryogenic scanning electron microscopy study. Canad. J. Bot.66: 2431–2435.

    Google Scholar 

  • Gassmann, W. &J. I. Schroeder. 1994. Inward-rectifying K+ channels in root hairs of wheat. A mechanism for aluminum-sensitive low affinity K+ uptake. Pl. Physiol.105: 1399–1408.

    CAS  Google Scholar 

  • Giddings, T. H. Jr. &L. A. Staehelin. 1991. Microtubule-mediated control of microfibril deposition: A reexamination of the hypothesis. Pages 85–99in C. W. Lloyd (ed.), The cytoskeletal basis of plant growth and form. Academic Press, London.

    Google Scholar 

  • Gloudemans, T., T. V. Bhuvaneswari, M. Moerman, T. van Brussel, A. van Kammen &T. Bisseling. 1989. Involvement ofRhizobium leguminosarum nodulation genes in gene expression in pea root hairs. Pl. Molec. Biol.12: 157–167.

    Article  CAS  Google Scholar 

  • Gochnauer, M. B., M. E. McCully &H. Labbé. 1989. Different populations of bacteria associated with sheathed and bare regions of roots of field-grown maize. Pl. & Soil144: 107–120.

    Article  Google Scholar 

  • Grabov, A. &M. Böttger. 1994. Are redox reactions involved in regulation of K+ channels in the plasma membrane ofLimnobium stoloniferum root hairs? Pl. Physiol.105: 927–935.

    CAS  Google Scholar 

  • Graham, J. H., R. T. Leonard &J. A. Menge. 1981. Membrane-mediated decrease in root exudation responsible for phosphorus inhibition of vesicular-arbuscular mycorrhiza formation. Pl. Physiol.68: 548–552.

    CAS  Google Scholar 

  • Greaves, M. P. &J. F. Darbyshire. 1972. The ultrastructure of the mucilaginous layer on plant roots. Soil Biol. Biochem.4: 443–449.

    Article  Google Scholar 

  • Gunning, B. E. S., A. R. Hardham &J. E. Hughes. 1978. Pre-prophase bands of microtubules in all categories of formative and proliferative cell division inAzolla roots. Planta143: 145–160.

    Article  Google Scholar 

  • Haahtela, K., T. Laakso &T. Korhonen. 1986. Associative nitrogen fixation byKlebsiella spp.: Adhesion sites and inoculation effects on grass roots. Appl. Environm. Microbiol.52: 1074–1079.

    CAS  Google Scholar 

  • —,R. Rönkkö, T. Laakso &P. Williams. 1990. Root-associatedEnterobacter andKlebsiella inPoa pratensis: Characterization of an iron-scavenging system and a substance stimulating root hair production. Molec. Pl.-Microbe Interact.3(6): 358–365.

    CAS  Google Scholar 

  • Hadas, R. &Y. Okon. 1987. Effect ofAzospirillum brasiliense inoculation on root morphology and respiration in tomato seedlings. Biol. Fertil. Soils5: 241–247.

    Article  Google Scholar 

  • Harari, A., J. Kigel &Y. Okon. 1988. Involvement of IAA in the interactions betweenAzospirillum brasiliense andPanicum miliaceum roots. Pl. & Soil110: 275–282.

    Article  CAS  Google Scholar 

  • Harris, W. M. 1979. Ultrastructural observations on the trichoblasts ofEquisetum. Amer. J. Bot.66: 673–684.

    Article  Google Scholar 

  • Hartwig, U. A., C. A. Maxwell, C. M. Joseph &D. A. Phillips. 1990. Chrysoeriol and luteolin released from alfalfa seeds inducenod genes inRhizobium meliloti. Pl. Physiol.92: 116–122.

    CAS  Google Scholar 

  • Head, G. C. 1964. A study of “exudation” from the root hairs of apple by time-lapse cine-photomicrography. Ann. Bot.28: 495–498.

    Google Scholar 

  • Heath, I. B. 1990. Tip growth in plant and fungal cells. Academic Press, San Diego.

    Google Scholar 

  • — &R. W. Seagull. 1982. Oriented cellulose fibrils and the cytoskeleton: A critical comparison of models. Pages 163–182in C. W. Lloyd (ed.), The cytoskeleton in plant growth and development. Academic Press, London.

    Google Scholar 

  • Higashi, S. &M. Abe. 1980. Scanning electron microscopy ofRhizobium trifolii infection sites on root hairs of white clover. Appl. Environm. Microbiol.40(6): 1094–1099.

    CAS  Google Scholar 

  • Hirsch, A. 1992. Developmental biology of legume nodulation. New Phytol.122: 211–237.

    Article  Google Scholar 

  • Hochmuth, G. J., W. H. Gabelman &G. C. Gerloff. 1985. A gene affecting tomato root morphology. Hort. Science20: 1099–1101.

    Google Scholar 

  • Hofer, R.-M. 1991. Root hairs. Pages 129–148in Y. Waisel, A. Eshel, U. Kafkai (eds.), Plant roots, the hidden half. Marcel Dekker, New York.

    Google Scholar 

  • Horvath, B., R. Heidstra, M. Lados, M. Moerman, H. Spaink, J-C. Promé, A. van Kammen &T. Bisseling. 1993. Lipo-oligosaccharides ofRhizobium induce infection-related early nodulin gene expression in pea root hairs. Pl. J.4: 727–733.

    Article  CAS  Google Scholar 

  • Huang, B., G. B. North &P. S. Nobel. 1993. Soil sheaths, photosynthate distribution to roots, and rhizosphere water relations forOpuntia ficus-indica. Intl. J. Pl. Sci.154: 425–431.

    Article  Google Scholar 

  • Itoh, S. &S. A. Barber. 1983. A numerical solution of whole plant nutrient uptake for soil-root systems with root hairs. Pl. & Soil70: 403–413.

    Article  CAS  Google Scholar 

  • Jain, D. K., &D. G. Patriquin. 1984. Root hair deformation, bacterial attachment, and plant growth in wheat-Azospirillum associations. Canad. J. Microbiol.48: 1208–1213.

    CAS  Google Scholar 

  • Jakobsen, K., S. Klemsdal, R. B. Aalen, M. Bosnes, D. Alexander &O. Olsen. 1989. Barley aleurone cell development: Molecular cloning of aleurone-specific cDNAs from immature grains. Pl. Molec. Biol.12: 285–293.

    Article  CAS  Google Scholar 

  • Jones, H., A. D. Tomos, R. A. Leigh &R. G. Wyn Jones. 1983. Water relation parameters of epidermal and cortical cells in the primary root ofTriticum aestivum L. Planta158: 230–236.

    Article  Google Scholar 

  • Kapulnik, Y., Y. Okon &Y. Henis. 1985. Changes in root morphology of wheat caused byAzospirillum inoculation. Canad. J. Microbiol.31: 881–887.

    Google Scholar 

  • —,S. Sarig, I. Nur &Y. Okon. 1983. Effect ofAzospirillum inoculation on yield on field-grown wheat. Canad. J. Microbiol.29: 895–899.

    Google Scholar 

  • Kawata, S. &W. Chung. 1979. On the formation of root hairs in crown roots of rice plants especially on the fine structure of epidermal cells. Jap. J. Crop Sci.48: 115–122.

    Google Scholar 

  • Kijne, J. W. 1992. TheRhizobium infection process. Pages 349–398in G. Stacey, R. H. Burris & H. J. Evans (eds.), Biological nitrogen fixation. Chapman and Hall, New York.

    Google Scholar 

  • —,G. Smit, C. L. Diaz &B. J. Lugtenberg. 1988. Lectin-enhanced accumulation of manganese-limitedRhizobium leguminosarum cells on pea root hair tips. J. Bacteriol.170: 2994–3000.

    PubMed  CAS  Google Scholar 

  • Knowlton, S., A. Berry &J. G. Torrey. 1980. Evidence that associated soil bacteria may influence root hair infection of actinorhizal plants byFrankia. Canad. J. Microbiol.26: 971–977.

    CAS  Google Scholar 

  • Kottke, I. &F. Oberwinkler. 1986a. Mycorrhiza of forest trees—structure and function. Trees1986: 1–24.

    Google Scholar 

  • ——. 1986b. Root-fungus interactions observed on the initial stages of mantle formation and Hartig net establishment in mycorrhizas ofAmanita muscaria onPicea abies in pure culture. Canad. J. Bot.64: 2348–2354.

    Google Scholar 

  • Kramer, D., W. P. Anderson &J. Preston. 1978. Transfer cells in the root epidermis ofAtriplex hastata L. as a response to salinity: A comparative cytological and x-ray microprobe investigation. Austral. J. Pl. Physiol.5: 739–747.

    CAS  Google Scholar 

  • —,V. Römheld, E. Landsberg &H. Marschner. 1980. Induction of transfer-cell formation by iron deficiency in the root epidermis ofHelianthus annuus L. Planta147: 335–339.

    Article  CAS  Google Scholar 

  • Krause, A. &W. J. Broughton. 1992. Proteins associated with root-hair deformation and nodule initiation inVigna unguiculata. Molec. Pl.-Microbe Interact.5(1): 96–103.

    CAS  Google Scholar 

  • —,C. Sigrist, I. Dehning, H. Sommer &W. J. Broughton. 1994. Accumulation of transcripts encoding a lipid transfer-like protein during deformation of nodulation-competentVigna unguiculata root hairs. Molec. Pl.-Microbe Interact.7(3): 411–418.

    CAS  Google Scholar 

  • Krieg, N. R. &J. Döbereiner. 1986. The genusAzospirillum. Pages 96–104in N. R. Krieg & J. G. Holt (eds.), Bergey’s manual of systematic bacteriology. Vol. 1. Williams and Wilkins, Baltimore.

    Google Scholar 

  • Kurkdjian, A., G. Leitz, P. Manigautt, A. Harim &K. O. Greulich. 1993. Non-enzymatic access to the plasma membrane ofMedicago root hairs by laser microsurgery. J. Cell Sci.105: 263–268.

    Google Scholar 

  • Lackie, S. M., S. R. Bowley &R. L. Peterson. 1988. Comparison of colonization among half-sib families ofMedicago sativa L. byGlomus versiforme (Daniels & Trappe) Berch. New Phytol.108: 477–482.

    Article  Google Scholar 

  • Lakshmi-Kumari, M., C. S. Singh &N. S. Subba-Rao. 1974. Root hair infection and nodulation in lucerne (Medicago sativa) as influenced by salinity and alkalinity. Pl. & Soil40: 261–268.

    Article  CAS  Google Scholar 

  • Lalonde, M. 1977. Infection process of theAlnus root nodule symbiosis. Pages 569–589in W. Newton, J. R. Postgate & C. Rodriquez-Barrueco (eds.), Recent developments of nitrogen fixation. Academic Press, London.

    Google Scholar 

  • —. 1980. Techniques and observations of the nitrogen-fixingAlnus root nodule symbiosis. Pages 421–434in N. S. Subba Rao (ed.), Recent advances in biological nitrogen fixation. Edward Arnold, London.

    Google Scholar 

  • Lancelle, S. &J. G. Torrey. 1984. Early development of Rhizobium-induced root nodules ofParasponia rigida. I. Infection and early nodule initiation. Protoplasma123: 26–37.

    Article  Google Scholar 

  • Landsberg, E.-C. 1982. Transfer cell formation in root epidermis: A prerequisite for Fe-efficiency? J. Pl. Nutr.5: 415–432.

    CAS  Google Scholar 

  • —. 1986. Function of rhizodermal transfer cells in the Fe stress response mechanisms ofCapsicum annuum L. Pl. Physiol.82: 511–517.

    CAS  Google Scholar 

  • —. 1989. Proton efflux and transfer cell formation as a response to Fe deficiency of soybean in nutrient solution culture. Pl. & Soil114: 53–61.

    Article  CAS  Google Scholar 

  • Law, I. &B. Strijdom. 1984. Role of lectins in the specific recognition ofRhizobium byLotononis bainesii. Pl. Physiol.74: 779–785.

    CAS  Google Scholar 

  • Leavitt, R. G. 1904. Trichomes of the root in vascular cryptogams and angiosperms. Proc. Boston Soc. Nat. Hist.31: 273–313.

    Google Scholar 

  • Lei, J., K. Wong, &Y. Piché. 1991. Extracellular concanavalin A-binding sites during early interactions betweenPinus banksiana and two closely related genotypes of the ectomycorrhizal basidiomyceteLaccaria bicolor. Mycol. Res.95: 357–363.

    CAS  Google Scholar 

  • Lerouge, P., P. Roche, C. Faucher, F. Maillet, G. Truchet, J.-C. Promé &J. Dénarié. 1990. Symbiotic host-specificity ofRhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature344: 781–784.

    Article  PubMed  CAS  Google Scholar 

  • Levanony, H. &Y. Bashan. 1989. Enhancement of cell division in wheat root tips and growth of root elongation zone induced byAzospirillum brasiliense Cd. Canad. J. Bot.67: 2213–2216.

    Article  Google Scholar 

  • Lew, R. R. 1991. Electrogenic transport properties of growingArabidopsis root hairs. The plasma membrane proton pump and potassium channels. Pl. Physiol.97: 1527–1534.

    Article  CAS  Google Scholar 

  • —. 1994. Regulation of electrical coupling betweenArabidopsis root hairs. Planta193: 67–73.

    Article  CAS  Google Scholar 

  • Lewis, D. G. &J. P. Quirk. 1967. Phosphate diffusion in soil and uptake by plants. III. P31-movement and uptake by plants as indicated by P32-autoradiography. Pl. & Soil26: 445–453.

    Article  CAS  Google Scholar 

  • Lewis, R. F. &N. V. Rothwell. 1964. Implications of nucleolar differences in the root epidermis among several grass species. Amer. J. Bot.51: 1107–1113.

    Article  Google Scholar 

  • Linderman, R. G. 1992. Vesicular-arbuscular mycorrhizae and soil microbial interactions. Pages 45–70in G. J. Bethlenfalvay & R. G. Linderman (eds.), Mycorrhizae in sustainable agriculture. Amererican Society of Agronomy.

  • Liu, Q. &A. M. Berry. 1991. The infection process and nodule initiation in theFrankia-Ceanothus root nodule symbiosis: A structural and histochemical study. Protoplasma163: 82–92.

    Article  Google Scholar 

  • Lloyd, C. W. 1983. Helical microtubular arrays in onion root hairs. Nature305: 311–313.

    Article  PubMed  CAS  Google Scholar 

  • —. 1984. Toward a dynamic helical model for the influence of microtubules on wall patterns in plants. Intl. Rev. Cytol.86: 1–51.

    Google Scholar 

  • —. 1987. The plant cytoskeleton: The impact of fluorescence microscopy. Annual Rev. Pl. Physiol.38: 119–139.

    Article  CAS  Google Scholar 

  • —. 1991. The cytoskeletal basis of plant growth and form. Academic Press, London.

    Google Scholar 

  • — &B. Wells. 1985. Microtubules are at the tips of root hairs and form helical patterns corresponding to inner wall fibrils. J. Cell Sci.75: 225–238.

    PubMed  CAS  Google Scholar 

  • —,K. J. Pearce, D. J. Rawlins, R. W. Ridge &P. J. Shaw. 1987. Endoplasmic microtubules connect the advancing nucleus to the tip of legume root hairs, but F-actin is involved in basipetal migration. Cell Motility & Cytoskel.8: 27–36.

    Article  Google Scholar 

  • Lowary, P. A. &C. J. Avers. 1965. Nucleolar variation during differentiation ofPhleum root epidermis. Amer. J. Bot.52: 199–203.

    Article  Google Scholar 

  • Malloch, D. W., K. A. Pirozynski &P. H. Raven. 1980. Ecological and evolutionary significance of mycorrhizal symbioses in vascular plants (a review). Proc. Natl. Acad. Sci. U.S.A.77: 2113–2118.

    Article  PubMed  CAS  Google Scholar 

  • Mansour, S. R. &J. G. Torrey. 1991. Frankia-spores of strain HFPCgI4 as inoculum for seedlings ofCasuarina glauca. Canad. J. Bot.69: 1251–1256.

    Article  Google Scholar 

  • Massicotte, H. B., R. L. Peterson &L. H. Melville. 1989a. Hartig net structure of ectomycorrhizae synthesized betweenLaccaria bicolor (Tricholomataceae) and two hosts:Betula alleghaniensis (Betulaceae) andPinus resinosa (Pinaceae). Amer. J. Bot.76: 1654–1667.

    Article  Google Scholar 

  • ———. 1989b. Ontogeny ofAlnus rubra-Alpova diplophloeus ectomycorrhiza. I. Light microscopy and scanning electron microscopy. Canad. J. Bot.67: 191–200.

    Google Scholar 

  • —,L. H. Melville &R. L. Peterson. 1987. Scanning electron microscopy of ectomycorrhizae: Potential and limitations. Scan. Microscop.1: 1439–1454.

    Google Scholar 

  • Maxwell, C. A., U. A. Hartwig, C. M. Joseph &D. A. Phillips. 1989. A chalcone and two related flavonoids released from alfalfa roots inducenod genes ofRhizobium meliloti. Pl. Physiol.91: 842–847.

    Article  CAS  Google Scholar 

  • McCully, M. E. &M. J. Canny. 1985. Localization of translocated14C in roots and root exudates of field-grown maize. Physiol. Pl.65: 380–392.

    Article  CAS  Google Scholar 

  • ——. 1988. Pathways and processes of water and nutrient movement in roots. Pl. & Soil111: 159–170.

    Article  CAS  Google Scholar 

  • McIver, J., M. Djordjevic, J. Weinman, G. Bender &B. Rolfe. 1989. Extensions of host range ofRhizobium leguminosarum bv. trifolii caused by point mutations in nodD that result in alterations in regulatory function and recognition of inducer molecules. Molec. Pl.-Microbe Interact.2: 97–106.

    CAS  Google Scholar 

  • Meekes, H. T. H. M. 1985. Ultrastructure, differentiation and cell wall texture of trichoblasts and root hairs ofCeratopteris thalictroides (L.) Brongn. (Parkeriaceae). Aquatic Bot.21: 347–362.

    Article  Google Scholar 

  • Metsavainio, K. 1931. Untersuchungen über das Wurzelsystem der Moorpflanzen. Ann. Soc. Zool.-Bot. Fenn. Vanamo1: 1–417.

    Google Scholar 

  • Miller, I. M. &D. D. Baker. 1986. Nodulation of actinorrhizal plants byFrankia strains capable of both root hair infection and intercellular penetration. Protoplasma131: 82–91.

    Article  Google Scholar 

  • Mirza, J. I., G. M. Olsen, T.-H. Iversen &E. P. Maher. 1984. The growth and gravitropic responses of wild-type and auxin-resistant mutants ofArabidopsis thaliana. Physiol. Pl.60: 516–522.

    Article  Google Scholar 

  • Misra, R. K., A. M. Alston &A. R. Dexter. 1988. Role of root hairs in phosphorus depletion from a macrostructured soil. Pl. & Soil107: 11–18.

    Article  CAS  Google Scholar 

  • Molina, A. &F. Garcia-Olmedo. 1993. Developmental and pathogen-induced expression of three barley genes encoding lipid transfer proteins. Pl. J.4: 983–991.

    Article  CAS  Google Scholar 

  • —,A. Segura &F. Garcia-Olmedo. 1993. Lipid transfer proteins (nsLTPs) from barley and maize leaves are potent inhibitors of bacterial and fungal plant pathogens. FEBS Lett.316: 119–122.

    Article  PubMed  CAS  Google Scholar 

  • Moog, P. R., T. A. W. van der Kooij, W. Brüggemann, J. W. Schiefelbein &P. J. C. Kuiper. 1995. Responses to iron deficiency inArabidopsis thaliana: The turbo iron reductase does not depend on the formation of root hairs and transfer cells. Planta195: 505–513.

    Article  PubMed  CAS  Google Scholar 

  • Morgenstern, E. &Y. Okon. 1987. The effect ofAzospirillum brasiliense and auxin on root morphology in seedlings ofSorghum bicolor ×Sorghum sudanense. Arid. Soil Res. Rehabil.1: 115–127.

    Google Scholar 

  • Mort, A. J. &P. B. Grover. 1988. Characterization of root hair cell walls as potential barriers to the infection of plants by rhizobia. The carbohydrate component. Pl. Physiol.86: 638–641.

    CAS  Google Scholar 

  • Murry, L. E. &M. L. Christianson. 1987. Phylogenetic comparison of large nuclear DNA contents of differentiated cells in the roots ofEquisetum, Tradescantia andHordeum. Amer. J. Bot.74: 1772–1778.

    Article  Google Scholar 

  • ——,S. H. Alfinito &S. J. Garger. 1987. Characterization of the nuclear DNA ofHordeum vulgareroot hairs: Amplification disappears under salt stress. Amer. J. Bot.74: 1779–1786.

    Article  CAS  Google Scholar 

  • Nap, J.-P. &T. Bisseling. 1989. Nodulin function and nodulin gene regulation in root nodule development. Pages 181–229in P. M. Gresshoff (ed.), The molecular biology of symbiotic nitrogen fixation. CRC Press, Florida.

    Google Scholar 

  • ——. 1990. Developmental biology of a plant-prokaryotic symbiosis: The legume root nodule. Science250: 948–954.

    Article  PubMed  CAS  Google Scholar 

  • Newcomb, E. H. &H. T. Bonnett Jr. 1965. Cytoplasmic microtubule and wall microflbril orientation in root hairs of radish. J. Cell Biol.27: 575–589.

    Article  PubMed  CAS  Google Scholar 

  • Nye, P. H. 1966. The effect of nutrient intensity and buffering power of a soil, and the absorbing power, size and root hairs of a root, on nutrient absorption by diffusion. Pl. & Soil25: 81–105.

    Article  CAS  Google Scholar 

  • Oades, J. M. 1978. Mucilages at the root surface. J. Soil Sci.29: 1–16.

    Article  CAS  Google Scholar 

  • Okada, K. &Y. Shimura. 1992. Aspects of recent developments in mutational studies of plant signalling pathways. Cell70: 369–372.

    Article  PubMed  CAS  Google Scholar 

  • Patriquin, D. G., J. Dobereiner &D. K. Jain. 1983. Sites and processes of association between diazotrophs and grasses. Canad. J. Microbiol.29: 900–914.

    Article  Google Scholar 

  • Peterson, R. L. 1967. Differentiation and maturation of primary tissues in white mustard root tips. Canad. J. Bot.45: 319–331.

    Google Scholar 

  • —. 1992. Adaptations of root structure in relation to biotic and abiotic factors. Canad. J. Bot.70: 661–675.

    Google Scholar 

  • — &M. L. Farquhar. 1994. Mycorrhizas—Integrated development between roots and fungi. Mycologia86: 311–326.

    Article  Google Scholar 

  • Piché, Y., R. L. Peterson &C. A. Ackerley. 1983. Early development of ectomycorrhizal short roots of pine. Scan. Elec. Microscop.3: 1467–1474.

    Google Scholar 

  • Pichon, M., E.-P. Journet, A. Dedieu, F. de Billy, G. Truchet &D. Barker. 1992.Rhizobium meliloti elicits transient expression of the early nodulin gene ENOD12 in the differentiating root epidermis of transgenic alfalfa. Pl. Cell4: 1199–1211.

    CAS  Google Scholar 

  • Prin, Y. &M. Rougier. 1986. Cytological and histochemical characteristics of the axenic root surface ofAlnus glutinosa. Canad. J. Bot.64: 2216–2226.

    Article  Google Scholar 

  • Puente, M. &Y. Bashan. 1993. Effect of inoculation withAzospirillum brasiliense strains on the germination and seedling growth of the giant columnar cardon cactus (Pachycereus pringle). Symbiosis15: 49–60.

    Google Scholar 

  • Pühler, A., W. Arnold, A. Buendia-Claveria, D. Kapp, M. Keller, K. Nehaus, J. Quant, A. Roxlau &W. Weng. 1991. The role ofRhizobium meliloti exopolysaccharides EPSI and EPSII in the infection process of alfalfa nodules. Pages 189–194in H. Hennecke & D. P. S. Verma (eds.), Advances in molecular genetics of plant-microbe interactions, vol. 1. Kluwer Academic, Dordrecht.

    Google Scholar 

  • Radermacher, E. &D. Klämbt. 1993. Auxin-dependent growth and auxin-binding proteins in primary roots and root hairs of corn (Zea mays L.). J. Pl. Physiol.141: 698–703.

    CAS  Google Scholar 

  • Rasheed, J. H., M. K. Al-Mallah, E. C. Cocking &M. R. Davey. 1990. Root hair protoplasts ofLotus corniculatus L. (birdsfoot trefoil) express their totipotency. Pl. Cell Rep.8: 565–569.

    Article  Google Scholar 

  • Reiss, H.-D. &W. Hearth. 1979. Calcium gradients in tip growing plant cells visualized by chlorotetracycline fluorescence. Planta146: 615–621.

    Article  CAS  Google Scholar 

  • Reynders, I. &K. Vlassak. 1982. Use ofAzospirillum brasiliense as biofertilizer in intensive wheat cropping. Pl. & Soil66: 217–223.

    Article  Google Scholar 

  • Ridge, R. W. 1988. Freeze substitution improves the ultrastructural preservation of legume root hairs. Bot. Mag. Tokyo101: 427–441.

    Article  Google Scholar 

  • —. 1992. A model of legume root hair growth andRhizobium infection. Symbiosis14: 359–373.

    Google Scholar 

  • — &B. Rolfe. 1985.Rhizobium sp. degradation of legume root hair cell wall at the site of infection thread origin. Appl. Environm. Microbiol.50: 717–720.

    CAS  Google Scholar 

  • ——. 1986. Sequence of events during the infection of the tropical legumeMacroptilium atropurpureum Urb. by the broad-host-range, fast growingRhizobium ANU240. J. Pl. Physiol.122: 121–137.

    Google Scholar 

  • ——,Y. Jing &E. Cocking. 1992.Rhizobium nodulation of non-legumes. Symbiosis14: 345–357.

    Google Scholar 

  • Robards, A. W. 1983. General and molecular cytology. Pages 1–17 in K. Esser, K. Kubitzki, M. Runge, E. Schnepf & H. Zeigler (eds.), Progress in botany. Vol. 45. Springer-Verlag, Berlin.

    Google Scholar 

  • Römheld, V. 1987. Existence of two different strategies for the acquisition of iron in higher plants. Pages 353–374in D. van der Helm, J. B. Neilands & E. Winkelmann (eds.), Iron transport in microbes, plants and animals. Verlag Chemie, Weinhem.

    Google Scholar 

  • — &D. Kramer. 1983. Relationship between proton efflux and rhizodermal transfer cells induced by iron deficiency. Z. Pflanzenphysiol.113: 73–83.

    Google Scholar 

  • — &H. Marschner. 1981. Iron deficiency stress induced morphological and physiological changes in root tips of sunflowers. Physiol. Pl.53: 354–360.

    Article  Google Scholar 

  • Rothberg, K. G. &W. P. Cunningham. 1978. Membrane transformations in the root hairs ofRaphanus sativus. J. Cell Biol.79: 373a.

    Google Scholar 

  • Rothwell, N. V. 1964. Nucleolar size differences in the grass root epidermis. Amer. J. Bot.51: 172–179.

    Article  Google Scholar 

  • —. 1966. Evidence for diverse cell types in the apical region of the root epidermis ofPanicum virgatum. Amer. J. Bot.53: 7–11.

    Article  Google Scholar 

  • Rougier, M. 1981. Secretory activity of the root cap. Pages 542–574 in W. Tanner & F. A. Loewus (eds.), Encyclopedia of plant physiology, new series. Vol. 13B, Plant carbohydrates II. Springer Verlag, Berlin.

    Google Scholar 

  • — &A. Chaboud. 1985. Mucilages secreted by roots and their biological function. Israel J. Bot.34: 129–146.

    Google Scholar 

  • Row, H. C. &J. R. Reeder. 1957. Root-hair development as evidence of relationships among genera of the Gramineae. Amer. J. Bot.44: 596–601.

    Article  Google Scholar 

  • Samuels, A. L., M. Fernando &A. D. M. Glass. 1992. Immunofluorescent localization of plasma membrane H+-ATPase in barley roots and effects of K nutrition. Pl. Physiol.99: 1509–1514.

    CAS  Google Scholar 

  • Sargent, J. A. 1986. Cryo-preservation of roots for scanning electron microscopy. Amer. J. Bot.58: 183–185.

    Google Scholar 

  • Sarig, S., Y. Kapulnik, I. Nur &Y. Okon. 1984. Response of non-irrigatedSorghum bicolor toAzospirillum inoculation. Exp. Agric.20: 59–66.

    Google Scholar 

  • Sato, S., Y. Ogasawara &S. Sakuragi. 1995. The relationship between growth, nucleus migration and cytoskeleton in root hairs of radish. Pages 69–74in F. Baluška, M. Čamporova, O. Gaš pariková & P. W. Barlow (eds.), Structure and function of roots. Kluwer Academic, Dordrecht.

    Google Scholar 

  • Sattelmacher, B., I. Heinecke &K. H. Müling. 1993. Influence of minerals on cytoplasmic streaming in root hairs of intact wheat seedlings. Pl. & Soil155/156: 107–110.

    Article  Google Scholar 

  • Scales, P. &R. L. Peterson. 1991. Structure of ectomycorrhizae formed byWilcoxina mikolae var. mikolae withPicea mariana andBetula alleghaniensis. Canad. J. Bot.69: 2149–2157.

    Article  Google Scholar 

  • Scheres, B., C. van de Wiel, A. Zalensky, B. Horvath, H. Spaink, H. van Eck, F. Zwartkruis, A.-M. Wolters, T. Gloudemans, A. van Kammen &T. Bisseling. 1990. The ENDO12 gene product is involved in the preinfection process during the pea-Rhizobium interaction. Cell60: 281–294.

    Article  PubMed  CAS  Google Scholar 

  • Schiefelbein, J. W. &P. N. Benfey. 1991. The development of plant roots: New approaches to underground problems. Pl. Cell3: 1147–1154.

    CAS  Google Scholar 

  • — &C. Somerville. 1990. Genetic control of root hair development inArabidopsis thaliana, Pl. Cell2: 235–242.

    CAS  Google Scholar 

  • —,M. Galway, J. Masucci &S. Ford. 1993. Pollen tube and root-hair tip growth is disrupted in a mutant ofArabidopsis thaliana. Pl. Physiol.103: 979–985.

    Article  CAS  Google Scholar 

  • —,A. Shipley &P. Rowse. 1992. Calcium influx at the tip of growing root-hair cells of Arabidopsis thaliana. Planta187: 455–459.

    Article  CAS  Google Scholar 

  • Schnall, J. A. &R. S. Quatrano. 1992. Abscisic acid elicits the water-stress response in root hairs ofArabidopsis thaliana. Pl. Physiol.100: 216–218.

    Article  CAS  Google Scholar 

  • Schröter, K. &A. Sievers. 1971. Wirkung der Turgorreduktion auf den Golgi-Apparat und die Bildung der Zellwand bei Wurzelhaaren. Protoplasma72: 203–211.

    Article  Google Scholar 

  • Schultze, M., B. Quiclet-Sire, E. Kondorosi, H. Virelizier, J. Glushka, G. Endre, S. Géro &A. Kondorosi. 1992.Rhizobium meliloti produces a family of sulfated lipo-oligosaccharides exhibiting different degrees of plant host specificity. Proc. Natl. Acad. Sci.89: 192–196.

    Article  PubMed  CAS  Google Scholar 

  • Seagull, R. W. 1989. The plant cytoskeleton. C. R. C. Crit. Rev. Pl. Sci.8: 131–167.

    CAS  Google Scholar 

  • — &I. B. Heath. 1980a. The organization of cortical microtubule arrays in the radish root hair. Protoplasma103: 205–229.

    Article  Google Scholar 

  • ——. 1980b. The differential effects of cytochalasin B on microfilament populations and cytoplasmic streaming. Protoplasma103: 231–240.

    Article  CAS  Google Scholar 

  • Sequerra, J., A. Capellano, M. Faure-Raynard &A. Moiroud. 1994. Root hair infection process and myconodule formation onAlnus incana byPenicillium nodositatum. Canad. J. Bot.72: 955–962.

    Article  Google Scholar 

  • Sethi, R. S. &M. Reporter. 1981. Calcium localization pattern in clover root hair cells associated with infection process: Studies with aureomycin. Protoplasma105: 321–325.

    Article  CAS  Google Scholar 

  • Sharaya, L. S., S. N. Novik, A. N. Pariiskaya &L. V. Kalakutskii. 1987. Specific deformation of alder root hairs upon interaction with infectiousFrankia cultures. Microbiology56: 110–114.

    Google Scholar 

  • Sievers, A. 1963a. Beteiligung des Golgi-Apparates bei der Bildung der Zellwand von Wurzelhaaren. Protoplasma56: 188–192.

    Article  Google Scholar 

  • —. 1963b. Über die Feinstruktur des Plasmas wachsender Wurzelhaare. Z. Naturforsch.18: 830–836.

    Google Scholar 

  • — &E. Schnepf. 1981. Morphogenesis and polarity of tubular cells with tip growth. Pages 265–299in O. Kiermayer (ed.), Cytomorphogenesis in plants. Springer-Verlag, Vienna.

    Google Scholar 

  • Smit, G., J. Kijne &B. Lugtenberg. 1987. Involvement of both cellulose fibrils and a Ca2+-dependent adhesin in the attachment of Rhizobiumleguminosarum to pea root hairs tips. J. Bacteriol.169: 4294–4301.

    PubMed  CAS  Google Scholar 

  • —,T. Logman, M. Boerrigter, J. Kijne &B. Lugtenberg. 1989. Purification and partial characterization of theRhizobium leguminosarum biovarviciae Ca2+-dependent adhesin, which mediates the first step in attachment of cells of the familyRhizobiaceae to plant root hair tips. J. Bacteriol.171(7): 4054–4062.

    PubMed  CAS  Google Scholar 

  • Smith, K. A. &P. D. Robertson. 1971. Effect of ethylene on root extension of cereals. Nature234: 148–149.

    Article  PubMed  CAS  Google Scholar 

  • Soran, V. &G. Lazăr-Keul. 1978. Relationship between cell growth and rate of protoplasmic streaming. Cytologia43: 265–271.

    Google Scholar 

  • Sprent, J. I. 1975. Adherence of sand particles to soybean roots under water stress. New Phytol.74: 461–463.

    Article  Google Scholar 

  • —. 1989. Which steps are essential for the formation of functional legume nodules? New Phytol.111: 129–153.

    Article  Google Scholar 

  • — &S. M. de Faria. 1988. Mechanisms of infection of plants by nitrogen fixing organisms. Pl. & Soil110: 157–165.

    Article  Google Scholar 

  • — &S. G. McInroy. 1984. Effects of salinity on growth and nodulation ofArachis hypogaea. Page 546in C. Veeger & W. E. Newton (eds.), Advances in nitrogen fixation research. Martinus Nijhoff/Junk, Pudoc.

    Google Scholar 

  • — &J. A. Raven. 1985. Evolution of nitrogen-fixing symbioses. Proc. Roy. Soc. Edinburgh85B: 215–237.

    Google Scholar 

  • Sweeney, B. M. 1944. The effect of auxin on protoplasmic streaming in root hairs ofAvena. Amer. J. Bot.31: 78–80.

    Article  CAS  Google Scholar 

  • Tanaka, Y. &F. W. Woods. 1972. Root and root hair growth in relation to supply and internal mobility of calicum. Bot. Gaz.133: 29–34.

    Article  Google Scholar 

  • ——. 1973. Root and root hair growth of oats: Replaceability of calcium. Canad. J. Bot.51: 1655–1659.

    Google Scholar 

  • Tarrand, J. J., N. R. Krieg &J. Döbereiner. 1978. A taxonomic study of theSpirillium lipoferum group, with descriptions of a new genus,Azospirillum gen. nov. and two species,Azospirillum lipoferum (Beijerink) comb. nov. andAzospirillum brasiliense sp. nov. Canad. J. Microbiol.24: 967–980.

    Article  CAS  Google Scholar 

  • Terouchi, N. &K. Syōno. 1990. Hair curling induced in heterologous legumes and monocots by flavonoid-treated rhizobia. Pl. Cell Physiol.31: 113–118.

    CAS  Google Scholar 

  • Thomson, J., L. H. Melville &R. L. Peterson. 1989. Interaction between the ectomycorrhizal fungusPisolithus tinctorius and root hairs ofPicea mariana (Pinaceae). Amer. J. Bot.76: 632–636.

    Article  Google Scholar 

  • Tien, T., M. H. Gaskins &D. H. Hubbell. 1979. Plant growth substances produced byAzospirillum brasiliense and their effect on the growth of pearl millet (Pennisetum americanum L.). Appd. Environm. Microbiol.37: 1016–1024.

    CAS  Google Scholar 

  • Torrey, J. G. 1978. Nitrogen fixation by actinomycete-nodulated angiosperms. BioScience28: 586–592.

    Article  Google Scholar 

  • Traas, J. A., P. Braat, A. M. C. Emons, H. Meekes &J. Derksen. 1985. Microtubules in root hairs. J. Cell Sci.76: 303–320.

    PubMed  CAS  Google Scholar 

  • Trappe, J. M. 1982. Synoptic keys to the genera and species of zygomycetous mycorrhizal fungi. Phytopathology72: 1102–1108.

    Google Scholar 

  • Tretyn, A., G. Wagner &H. H. Felle. 1991. Signal transduction inSinapis alba root hairs: Auxins as external messengers. J. Pl. Physiol.139: 187–193.

    CAS  Google Scholar 

  • Trinick, M. J. 1973. Symbiosis betweenRhizobium and the nonlegume,Trema aspera. Nature244: 459–460.

    Article  Google Scholar 

  • —. 1981. The non-legume-Rhizobium association. Page 255in A. Gibson & W. Newton (eds.), Current perspectives in nitrogen fixation. Australian Academy of Science, Canberra.

    Google Scholar 

  • — &J. Galbraith. 1980. TheRhizobium requirements of the non-legumeParasponia in relation to the cross-inoculation group concept of legumes. New Phytol.86: 17–26.

    Article  Google Scholar 

  • Truchet, G. L., J. E. Sherwood, H. S. Pankrantz &F. B. Dazzo. 1986. Clover root exudate contains a particulate form of the lectin, trifolin A, which binds Rhizobiumtrifolii. Physiol. Pl.66: 575–582.

    Article  CAS  Google Scholar 

  • —,P. Roche, P. Lerouge, J. Vasse, S. Camut, F. de Billy, J-C. Promé &J. Dénarié. 1991. Sulphated lipo-polysaccharide signals ofRhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature351: 670–675.

    Article  CAS  Google Scholar 

  • Turgeon, B. G. &W. D. Bauer. 1982. Early events in the infection of the soybean by Rhizobiumjaponicum. Time course cytology of the initial infection process. Canad. J. Bot.60: 152–161.

    Google Scholar 

  • ——. 1985. Ultrastructure of infection-thread development during the infection of soybean byRhizobium japonicum. Planta163: 328–349.

    Article  Google Scholar 

  • Tyerman, S. D., P. Oats, J. Gibbs, M. Dracup &H. Greenway. 1989. Turgor volume regulation and cellular water relations ofNicotiana tabacum roots grown in high salinities. Austral. J. Pl. Physiol.16: 517–531.

    Article  Google Scholar 

  • Ullrich, C. I. &A. J. Novacky. 1990. Extra- and intracellular pH and membrane potential changes induced by K+, Cl, H2PO4−, and NO3− uptake and fusicoccin in root hairs ofLimnobium stoloniferum. Pl. Physiol.94: 1561–1567.

    CAS  Google Scholar 

  • Umali-Garcia, M., D. Hubbell, M. Gaskins &F. Dazzo. 1980. Association ofAzospirillum with grass roots. Appl. Environm. Microbiol.39: 219–226.

    CAS  Google Scholar 

  • Vakhmistrov, D. B. &E. B. Kurkova. 1979. Symplastic connections in the rhizodermis ofTrianea bogotensis. Soviet Pl. Physiol.26: 763–771.

    Google Scholar 

  • —— &I. F. Zlotnikova. 1981. Symplastic connections and intracellular activity of potassium in the rhizodermis ofRaphanus sativus. Soviet Pl. Physiol.28: 826–833.

    Google Scholar 

  • Valla, G., A. Capellano, R. Hugueney &A. Moiroud. 1989. A new species inducing myconodules onAlms roots. Pl. & Soil114: 142–146.

    Article  Google Scholar 

  • van Amstel, A. N. M. &J. Derksen. 1993. The complex helical texture of the secondary cell wall ofUrtica dioica root hairs is not controlled by microtubules: A quantitative analysis. Acta Bot. Neerl.42: 141–151.

    Google Scholar 

  • van Batenburg, F. H., R. Jonker &J. W. Kijne. 1986.Rhizobium induces marked root hair curling by redirection of tip growth: A computer simulation. Physiol. Pl.66: 476–480.

    Article  Google Scholar 

  • van Brussel, A., R. Bakhuizen, P. C. van, H. P. Spaink, T. Tak, B. J. Lugtenburg &J. Kijne. 1992. Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipo-oligosaccharides ofRhizobium. Science257: 70–72.

    Article  PubMed  Google Scholar 

  • Van de Geijn, S. &J. M. Van Maaren. 1986. A fast screening method for bacterial isolates producing substances affecting root-growth. Symbiosis2: 67–75.

    Google Scholar 

  • Vermeer, J. &M. E. McCully. 1982. The rhizosphere inZea: New insight into its structure and development. Planta156: 45–61.

    Article  Google Scholar 

  • Volkmann, D. 1984. The plasma membrane of growing root hairs is composed of zones of local differentiation. Planta163: 392–403.

    Article  Google Scholar 

  • — &P. Peters. 1995. Structural basis of root hair formation: Early development of trichoblasts and atrichoblasts. Pages 61–67 in F. Baluška, M. Ziamporová, O. Gaš pariková & P. W. Barlow (eds.), Structure and function of roots. Kluwer Academic, Dordrecht.

    Google Scholar 

  • Watt, M., M. E. McCully &M. J. Canny. 1994. Formation and stabilization of rhizosheaths ofZea mays L. Effect of soil water contact. Pl. Physiol.106: 179–186.

    CAS  Google Scholar 

  • Webster, J. &B. A. Stone. 1994. Isolation, histochemistry and monosaccharide composition of the walls of root hairs fromHeterozostera tasmanica (Martens ex Aschers.) den Hartog. Aquatic Bot.47: 29–37.

    Article  CAS  Google Scholar 

  • Weisenseel, M. H., A. Dorn &L. F. Jaffe. 1979. Natural H+ currents traverse growing roots and root hairs of barley (Hordeum vulgare L.). Pl. Physiol.64: 512–518.

    Article  CAS  Google Scholar 

  • Wen, T.-J. &P. S. Schnable. 1994. Analyses of mutants of three genes that influence root hair development inZea mays (Gramineae) suggest that root hairs are dispensable. Amer. J. Bot.81: 833–842.

    Article  Google Scholar 

  • Werker, E. &M. Kislev. 1978. Mucilage on the root surface and root hairs ofSorghum: Heterogeneity in structure, manner of production and site of accumulation. Ann. Bot.42: 809–816.

    Google Scholar 

  • Wilson, A. K., F. B. Pickett, J. C. Turner &M. Estelle. 1990. A dominant mutation inArabidopsis confers resistance to auxin, ethylene and abscisic acid. Molec. Gen. Genet.222: 377–383.

    Article  PubMed  CAS  Google Scholar 

  • Wood, S. &W. Newcomb. 1989. Nodule morphogenesis: The early infection of alfalfa (Medicago sativa) root hairs byRhizobium meliloti. Canad. J. Bot.67: 3108–3122.

    Article  Google Scholar 

  • Wullstein, L. H. 1980. Nitrogen fixation associated with rhizosheaths of Indian ricegrass used in the stabilization of Slick Rock, Colorado, tailings pile. J. Range Managern.33: 204–206.

    Google Scholar 

  • — &S. A. Pratt. 1981. Scanning electron microscopy of rhizosheaths ofOryzopsis hymenoides. Amer. J. Bot.68: 408–419.

    Article  Google Scholar 

  • —,M. L. Bruening &W. B. Bollen. 1979. Nitrogen fixation associated with sand grain root sheaths (rhizosheaths) of certain xeric grasses. Physiol. Pl.46: 1–4.

    Article  CAS  Google Scholar 

  • Zaar, K. 1979. Peroxidase activity in root hairs of cress (Lepidium sativum L.). Cytochemical localization and radioactive labelling of wall bound peroxidase. Protoplasma99: 263–274.

    Article  CAS  Google Scholar 

  • Zaat, S., A. van Brussel, T. Tak, E. Pees &B. Lugtenberg. 1987. Flavonoids induceRhizobium leguminosarum to produce nodDABC gene-related factors that cause thick, short roots and root hair responses on common vetch. J. Bacteriol.169(7): 3388–3391.

    PubMed  CAS  Google Scholar 

  • Zahran, H. H. &J. I. Sprent. 1986. Effects of sodium chloride and polyethylene glycol on root-hair infection and nodulation ofVicia faba L. plants byRhizobium leguminosarum. Planta167: 303–309.

    Article  CAS  Google Scholar 

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This manuscript is dedicated to the late Dr. R. G. H. Cormack (deceased 1995) for his pioneering work on root hairs and for stimulating the senior author’s initial interest in roots.

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Peterson, R.L., Farquhar, M.L. Root hairs: Specialized tubular cells extending root surfaces. Bot. Rev 62, 1–40 (1996). https://doi.org/10.1007/BF02868919

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