Journal of Plant Growth Regulation

, Volume 21, Issue 4, pp 352–367 | Cite as

Root Caps and Rhizosphere

  • Martha C. Hawes
  • Glyn Bengough
  • Gladys Cassab
  • Georgina Ponce
Thematic Article

Abstract

In this paper we discuss recent work on the physiological, molecular, and mechanical mechanisms that underlie the capacity of root caps to modulate the properties of the rhizosphere and thereby foster plant growth and development. The root cap initially defines the rhizosphere by its direction of growth, which in turn occurs in response to gradients in soil conditions and gravity. The ability of the root cap to modulate its environment is largely a result of the release of exudates and border cells, and so provides a potential method to engineer the rhizosphere. Factors affecting the release of border cells from the outer surface of the root cap, and function of these cells and their exudates in the rhizosphere, are considered in detail. Release of border cells into the rhizosphere depends on soil matric potential and mechanical impedance, in addition to a host of other environmental conditions. There is good evidence of unidentified feedback signals between border cells and the root cap meristem, and some potential mechanisms are discussed. Root border cells play a significant mechanical role in decreasing frictional resistance to root penetration, and a conceptual model for this function is discussed. Root and border cell exudates influence specific interactions between plant hosts and soil organisms, including pathogenic fungi. The area of exudates and border cell function in soil is an exciting and developing one that awaits the production of appropriate mutant and transgenic lines for further study in the soil environment.

Keywords

Root caps Rhizosphere Plant growth 

References

  1. 1.
    Aiken, RM, Smucker, AJM 1996Root system regulation of whole plant growth.Annu Rev Phytopathol34325346PubMedCrossRefGoogle Scholar
  2. 2.
    Atkinson, TG, Neal, JL, Larson, RI 1975

    Genetic control of the rhizosphere microflora of wheat.

    Bruehl, GW eds. Biology and Control of Soil-borne Plant Pathogens.American Phytopathological SocietySt. Paul MN116122
    Google Scholar
  3. 3.
    Baluška, F, Volkmann, D, Barlow, PW 1996aSpecialized zones of development in roots: view from the cellular level.Plant Physiol11234Google Scholar
  4. 4.
    Baluška, F, Volkmann, D, Hauskrecht, M, Barlow, PW 1996bRoot cap mucilage and extracellular calcium as modulators of cellular growth in postmitotic growth zones of the maize root apex.Bot Acta1092534Google Scholar
  5. 5.
    Barlow, PW 1975

    The root cap.

    Torrey, JGClarkson, DT eds. The development and function of rootsAcademic PressLondon2154
    Google Scholar
  6. 6.
    Barlow, PW, Parker, JS 1996Microtubular cytoskeleton and root morphogenesis.Plant Soil1872336CrossRefGoogle Scholar
  7. 7.
    Barlow, PW 2003The root cap: cell dynamics, cell differentiation and cap function.J Plant Growth Regulation21261286doi:10.1007/s00344-002-0034-zCrossRefGoogle Scholar
  8. 8.
    Battey, NH, James, NC, Greenland, AJ, Brownlee, C 1999Exocytosis and endocytosis.Plant Cell11643659PubMedCrossRefGoogle Scholar
  9. 9.
    Bengough, AG, Crose, C, Pritchard, J 1997aA biophysical analysis of root growth under mechanical stress.Plant Soil189155164CrossRefGoogle Scholar
  10. 10.
    Bengough, AG, Kirby, JM 1999Tribology of the root cap in maize and peas.New Phytol142421425CrossRefGoogle Scholar
  11. 11.
    Bengough, AG, McKenzie, BM 1997Sloughing of root cap cells decreases the frictional resistance to maize root growth.J Exper Bot48885893CrossRefGoogle Scholar
  12. 12.
    Bengough, AG, Mullins, CE 1990Mechanical impedance to root-growth—a review of experimental techniques and root growth responses.J Soil Sci41341358CrossRefGoogle Scholar
  13. 13.
    Bengough, AG, Mullins, CE 1991Penetrometer resistance, root penetration resistance and root elongation rate in 2 sandy loam soils.Plant Soil1315966Google Scholar
  14. 14.
    Bengough, AG, Mullins, CE, Wilson, G 1997bEstimating soil frictional resistance to metal probes and its relevance to the penetration of soil by roots.Eur J Soil Sci48603612CrossRefGoogle Scholar
  15. 15.
    Brigham, LA, Flores, HE 1999Cell-specific production and antimicrobial activity of naphthoquinones in roots of Lithospermum erythrorhizon.Plant Physiol119417428PubMedCrossRefGoogle Scholar
  16. 16.
    Brigham, LA, Woo, HH, Nicoll, SM, Hawes, MC 1995Differential expression of protesin and mRNAs from border cells and root tips of pea.Plant Physiol109457463PubMedGoogle Scholar
  17. 17.
    Brigham, LA, Woo, HH, Wen, F, Hawes, MC 1998Meristem- specific suppression of mitosis and a global switch in gene expression in the root cap of pea by endogenous signals.Plant Physiol11812231231PubMedCrossRefGoogle Scholar
  18. 18.
    Chen, R, Guan, C, Boonsirichai, K, Masson, PH 2002Complex physiological and molecular processs underlying root gravitropism.Plant Mol Biol49305317PubMedCrossRefGoogle Scholar
  19. 19.
    Chen, R, Rosen, E, Masson, PH 1999Gravitropism in higher plants.Plant Physiol120343350PubMedCrossRefGoogle Scholar
  20. 20.
    Clowes, FAL 1976Cell production by root caps.New Phytol77399407CrossRefGoogle Scholar
  21. 21.
    Clowes, FAL 1978Origin of the quiescent center in Zea mays.New Phytol80409419CrossRefGoogle Scholar
  22. 22.
    Clowes, FAL 1980Mitosis in the root cap of Zea mays.New Phytol857987CrossRefGoogle Scholar
  23. 23.
    Correll, MJ, Kiss, JZ 2002Interactions between gravitropism and phototropism in plants.J Plant Growth Reg2189101CrossRefGoogle Scholar
  24. 24.
    Curl, EA, Truelove, B 1986The Rhizosphere.Springer-VerlagBerlinGoogle Scholar
  25. 25.
    Darwin, C 1880The power of movement in plants.John MurreyLondonGoogle Scholar
  26. 26.
    Driouich, A, Faye, L, Staehelin, A 1993The plant Golgi apparatus: a factory for complex polysaccharides and glycoproteins.Trends Biol Sci18210214CrossRefGoogle Scholar
  27. 27.
    Eapen, D, Barroso, ML, Campos, ME, Ponce, G, Corkidi, G, Duhrovsky, JG, Cassab, GI 2002A negative root hydrotropic mutant that responds positively to gravitropism in Arabidopsis thaliana.Plant Physiol128207212(in press)Google Scholar
  28. 28.
    Feldman, LJ 1976The de novo origin of the quiescent center in regenerating root apices of Zea mays.Planta128207212CrossRefGoogle Scholar
  29. 29.
    Feldman, LJ 1984Regulation of root development.Annu Rev Plant Physiol35223242PubMedCrossRefGoogle Scholar
  30. 30.
    Firn, RD, Digby, J 1997Solving the puzzle of gravitropism—has a lost piece been found?Planta213D159S163CrossRefGoogle Scholar
  31. 31.
    Gochnauer, MB, Sealey, LJ, McCully, ME 1990Do detached root cap cells influence bacteria associated with maize roots?Plant Cell Environ13793801CrossRefGoogle Scholar
  32. 32.
    Goldberg, N, Hawes, MC, Stanghellini, M 1989Specific attraction to and infection of cotton root cap cells by zoospores of Pythium dissotocum.Can J Bot6717601767CrossRefGoogle Scholar
  33. 33.
    Griffin, GJ, Hale, MG, Shay, FJ 1976Nature and quantity of sloughed organic matter produced by roots of axenic peanut plants.Soil Biol Biochem82932CrossRefGoogle Scholar
  34. 34.
    Guinel, FC, McCully, ME 1986Some water-related physical properties of maize root cap mucilage.Plant Cell Environ9657666CrossRefGoogle Scholar
  35. 35.
    Guinel, FC, McCully, ME 1987The cells shed by the root cap of Zea: their origin and some structural and physiological properties.Plant Cell Environ10565578Google Scholar
  36. 36.
    Gunawardena, U, Hawes, MC 2002Tissue-specific localization of root infection by fungal pathogens.Molec Plant Microb Int1511281136CrossRefGoogle Scholar
  37. 37.
    Haberlandt, G 1914Physiological plant antomy.MacMillan and CoLondonGoogle Scholar
  38. 38.
    Hawes, MC 1990Living plant cells released from the root cap: a regulator of microbial populations in the rhizosphere?Plant Soil1291927CrossRefGoogle Scholar
  39. 39.
    Hawes, MC, Brigham, LA 1992Impact of root border cells on microbial populations in the rhizosphere.Adv Plant Pathol8119148Google Scholar
  40. 40.
    Hawes, MC, Brigham, LA, Nicoll, SM, Stephenson, MB 1994Plant genes controlling the release of root exudates.Biotechnol Plant Prot4110Google Scholar
  41. 41.
    Hawes, MC, Brigham, LA, Woo, HH, Zhu, Y, Wen, F 1996Root border cells.Biol Plant-Microbe Int8509514Google Scholar
  42. 42.
    Hawes, MC, Brigham, LA, Woo, HH, Zhu, Y, Wen, F 1997

    Root border cells: phenomenology of signal exchange.

    Flores, HELynch, JPEissenstat, D eds. Radical biology: advances and perspectives on the function of plant roots.Amer Soc Plant PhysiolRockville MD
    Google Scholar
  43. 43.
    Hawes, MC, Brigham, LA, Wen, F, Woo, HH, Zhu, Y,  et al. 1998Function of root border cells in plant health: pioneers in the rhizosphere.Annu Rev Phytopathol36311327PubMedCrossRefGoogle Scholar
  44. 44.
    Hawes, MC, Gunawardena, U, Miyasaka, S, Zhao, X 2000The role of root border cells in plant defense.Trends Plant Sci5128132PubMedCrossRefGoogle Scholar
  45. 45.
    Hawes, MC, Lin, HJ 1990Correlation of pectolytic enzyme activity with the programmed release of cells from root caps of pea.Plant Physiol9418551859PubMedCrossRefGoogle Scholar
  46. 46.
    Hawes, MC, Pueppke, SG 1986Sloughed peripheral root cap cells: yield from different species and callus formation from single cells.Am J Bot7314661473CrossRefGoogle Scholar
  47. 47.
    Hawes, MC, Pueppke, SG 1987Correlation between binding of Agrobacterium tumefaciens by root cap cells and susceptibility of plants to crown gall.Plant Cell Rep6287290CrossRefGoogle Scholar
  48. 48.
    Hawes, MC, Smith, L 1989Requirement for chemotaxis in pathogenicity of Agrobacterium tumefaciens on roots of soil-grown plants.J Bacteriol17156685671PubMedGoogle Scholar
  49. 49.
    Hawes, MC, Stephenson, MB 1994Correlation of pectin methylesterase activity in root caps of pea with root border cell separation.Plant Physiol106739745PubMedGoogle Scholar
  50. 50.
    Hawes, MC, Wheeler, HE 1982Factors affecting victorin-induced cell death: temperature and plasmolysis.Physiol Plant Pathol20137144CrossRefGoogle Scholar
  51. 51.
    Ijima, M, Griffiths, B, Bengough, AG 2000Sloughing of cap cells and carbon exudation from maize seedling roots in compacted sand.New Phytol145477482CrossRefGoogle Scholar
  52. 52.
    Jiang, K, Feldman, LJ 2003Root meristem establishment and maintenance: the role of auxins.J Plant Growth Regulation21432440doi:10.1007/s00344-002-0037-9CrossRefGoogle Scholar
  53. 53.
    Jenkins, G 1998Signal transduction networks and the integration of responses to environmental stimuli.Adv Bot Res2955Google Scholar
  54. 54.
    Kerk, NM, Feldman, LJ 1995A biochemical model for the initiation and maintenance of the quiescent center: implication for organization of root meristems.Development12128252833Google Scholar
  55. 55.
    Kirby, JM, Bengough, AG 2002Influence of soil strength on root growth: experiments and analysis using a critical-state model.Eur J Soil Sci53119127CrossRefGoogle Scholar
  56. 56.
    Knudson, L 1919Viability of detached root cap cells.Am J Bot6309310CrossRefGoogle Scholar
  57. 57.
    Kochian, L 1995Cellular mechanisms of aluminum toxicity and resistance in plants.Annu Rev Plant Physiol Plant Mol Biol46237260CrossRefGoogle Scholar
  58. 58.
    Konings, H 1995Gravitropism of roots: an evaluation of progress during the last three decades.Acta Bot Neerl44195223Google Scholar
  59. 59.
    Lynch, J 1995Root architecture and plant productivity.Plant Physiol109713PubMedGoogle Scholar
  60. 60.
    MacCleery, SA, Kiss, JZ 1999Plastid sedimentation kinetics in roots of wild-type and starch-deficient mutants of Arabidopsis.Plant Physiol120183192PubMedCrossRefGoogle Scholar
  61. 61.
    Matsuyama, T, Yasumura, N, Nunakoshi, M, Yamada, Y, Hashimoto, T 1999Maize genes specifically expressed in the outermost cells of root cap.Plant Cell Physiol40469476PubMedGoogle Scholar
  62. 62.
    McCully, ME, Boyer, JR 1997The expansion of maize root cap mucilage during hydration. 3. Changes in water potential and water content.Physiol Plantarum99169177CrossRefGoogle Scholar
  63. 63.
    Miyasaka, S, Hawes, MC 2000Possible role of root border cells in tolerance of roots to aluminum.Plant Physiol12519781987CrossRefGoogle Scholar
  64. 64.
    Moody, SF, Clarke, AE, Bacic, A 1988Structural analysis of secreted slime from wheat and cowpea roots.Phytochem2728572861CrossRefGoogle Scholar
  65. 65.
    Moore, R, Evans, ML 1986How roots perceive and respond to gravity.Am J Bot73574587PubMedCrossRefGoogle Scholar
  66. 66.
    Moore, R, McClelen, CE 1983Ultrastructural aspects of cellular differentiation in the root cap of Zea mays.Can J Bot6115661572CrossRefGoogle Scholar
  67. 67.
    Mosse, B 1975

    A microbiologist's point of view.

    Walker, N eds. Soil microbiology,John WileyNew York3966
    Google Scholar
  68. 68.
    Neal, JL, Atkinson, TG, Larson, RI 1970Changes in rhizosphere microflora of spring wheat induced by disomic substitution of a chromosome.Can J Microbiol16153158PubMedCrossRefGoogle Scholar
  69. 69.
    Neal, JL, Larson, RI, Atkinson, TG 1973Changes in rhizosphere populations of selected physiological groups of bacteria related to substitution of specific pairs of chromosomes in spring wheat.Plant Soil39209212CrossRefGoogle Scholar
  70. 70.
    Ponce, G, Lujan, R, Campos, ME, Reyes, A, Nieto-Sotelo, J, Feldman, LJ, Cassab, GI 2000Three maize root-specific genes are not correctly expressed in regenerated caps in the absence of the quiescent center.Planta2112333PubMedCrossRefGoogle Scholar
  71. 71.
    Price I. 2002. Characterization of a rhizosphere galactosidase from Pisum sativum L. M.S. Thesis, University of Arizona.Google Scholar
  72. 72.
    Read, DB, Gregory, PJ, Bell, AE 1999Physical properties of axenic maize root mucilage.Plant Soil2118791CrossRefGoogle Scholar
  73. 73.
    Rogers, HT, Pearson, RW, Pierre, WH 1942The source and phosphatase activity of exoenzyme systems of corn and tomato roots.Soil Sci54353365CrossRefGoogle Scholar
  74. 74.
    Rosen, E, Chen, R, Masson, PH 1999Root gravitropism: a complex response to a simple stimulus?Trends Plant Sci4407412PubMedCrossRefGoogle Scholar
  75. 75.
    Rougier, M 1981

    Secretory activity of the root cap.

    Tanner, WLoewus, FA eds. Encyclopedia of plant physiology, New Series, Vol 13B. Plant carbohydrates II.Springer-VerlagBerlin542574
    Google Scholar
  76. 76.
    Sievers, A, Braun, M 1996

    The root cap: structure and function.

    Waisel, YEshel, AKafkafi, U eds. Plant roots: The hidden half, 2nd edMarcel Dekker, IncNew York3149
    Google Scholar
  77. 77.
    Takahashi, H,  et al. 1997Hydrotropisrn: the current state of our knowledge.J Plant Res110163169PubMedCrossRefGoogle Scholar
  78. 78.
    Tsugeki, R, Fedoroff, MV 1999Genetic ablation of root cap cells in Arabidopsis.Proc Natl Acad Sci USA961294112946PubMedCrossRefGoogle Scholar
  79. 79.
    Tsutsumi, D, Kosugi, K, Mizuyama, T 2003Effect of hydrotropism on root system development in soybean (Glycine max): growth experiments and a model simulation.J Plant Growth Regul21441458doi:10.1007/s00344-003-0006-7CrossRefGoogle Scholar
  80. 80.
    van den Berg, C, Hage, W, Willemson, V 1997

    The acquisition of cell fate in the Arabidopsis thaliana root meristem.

    Altman, AWaisel, Y eds. Biology of Root Formation and DevelopmentPlenum PressNew York2129
    Google Scholar
  81. 81.
    Vermeer, J, McCully, ME,  et al. 1982The rhizosphere in Zea: new insight into its structure and development.Planta1564561CrossRefGoogle Scholar
  82. 82.
    Wang, H, Li, J, Bostock, RM, Gilchrist, DG 1999Apoptosis: a functional paradigm for programmed plant cell death induced by a host selective phytotoxin and invoked during development.Plant Cell8375391CrossRefGoogle Scholar
  83. 83.
    Wen, F, Zhu, Y, Hawes, MC 1999Effect of pectin methylesterase gene expression on pea root development.Plant Cell1111291140PubMedCrossRefGoogle Scholar
  84. 84.
    Wolverton, C, Ishikawa, H, Evans, ML 2002The kinetics of root gravitropism: dual motors and sensors.J Plant Growth Reg21102112CrossRefGoogle Scholar
  85. 85.
    Woo, HH, Hawes, MC 1999Meristem-localized inducible expression of a UDP-glycosyltransferase gene is essentialy for plant growth and development in pea and alfalfa.Plant Cell1123032315PubMedCrossRefGoogle Scholar
  86. 86.
    Zhang, W, Cheng, W, Wen, M 1995Detachment of root cap cells of maize and its effects on the relationship between root and rhizosphere.Acta Phytophysiol Sin21340346Google Scholar
  87. 87.
    Zhao, X, Schmitt, M, Hawes, MC 2000Species dependent effects of border cell and root tip exudates on nematode behavior.Phytopathology9012391245PubMedCrossRefGoogle Scholar
  88. 88.
    Zhu, T, Rost, TL 2000Directional cell-to-cell communication in the Arabidopsis root apical meristem. III. Plasmodesmata turnover and apoptosis in meristem and root cap cells during four weeks after germination.Protoplasma21399107CrossRefGoogle Scholar
  89. 89.
    Zhu, Y, Pierson III, LSP, Hawes, MC 1997Induction of microbial genes for pathogenesis and symbiosis by chemicals from root border cells.Plant Physiol11516911698PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • Martha C. Hawes
    • 1
  • Glyn Bengough
    • 2
  • Gladys Cassab
    • 3
  • Georgina Ponce
    • 3
  1. 1.Department of Plant PathologyUniversity of Arizona, Tucson, Arizona 85721USA
  2. 2.Scottish Crop Research Institute, DundeeScotland DD2 5DA
  3. 3.UNAM/iBT, CuernavacaMexico

Personalised recommendations