Plant Biol (Stuttg) 2002; 4(2): 234-249
DOI: 10.1055/s-2002-25736
Original Paper
Georg Thieme Verlag Stuttgart ·New York

Aluminum Exclusion Mechanism in Root Tips of Maize (Zea mays L.): Lysigeny of Aluminum Hyperaccumulator Cells

M. D. Vázquez
  • Departamento de Biología Animal, Vegetal y Ecología, Unidad de Fisiología Vegetal, Facultad de Ciencias, Universidad Autónoma de Barcelona, 08193 Bellaterra (Cerdanyola del Vallés), Barcelona, Spain
Further Information

Publication History

August 21, 2001

January 17, 2002

Publication Date:
26 April 2002 (online)

Abstract

Ultrastructural studies, together with X-ray microanalytical, immunocytochemical and cytochemical analysis performed in root tips of Al-resistant (C-525 M) and Al-sensitive (Adour 250, HS 7777 and BR 201 F) maize plants (Zea mays L.), after 96 h exposure to 20 μM Al, showed qualitatively similar results in the four cultivars.

Al was identified in electron-opaque precipitates, which were insoluble even in EDTA chelate. They also contained an elevated proportion of P and also of K and Ca, some traces of Mn, Fe and Zn and sometimes of Mg. This elemental composition is similar to that described for phytin (Al-phytin), and the precipitates were localized in the two principal extraplasmatic compartments: cell walls and vacuoles. Al-phytin was detected in swollen areas of cell walls in membraneous concentric configurations, resembling myelin figures, probably rich in phosphatidyl inositol, which also intervene in the vacuolar internalization of Al-phytin and are similar to a peculiar form of endocytosis (not previously described). Abnormal apoplastic protuberances containing abundant electron-opaque Al-phytin deposits, agglutinated by callose (immunocytochemically identified), were shown in cortex cells with high mitotic activity (around 1 - 1.5 mm from cap root). Al-hyperaccumulator cells parallel to the root axis were correlated with longitudinal lysigenous intercellular spaces after cell death and dissolution (lysigeny). Indicators of activated lysigeny, as low levels of Al and callose (in agreement with other authors) and high levels of phosphoinositides, can mark Al-resistant genotypes, contrary to Al-sensitive genotypes, probably derived from a partially activated or even inactivated lysigeny.

The lysigeny of Al hyperaccumulator cells constitutes new ultrastructural evidence of an Al exclusion mechanism, supporting biochemical results reported by other investigators.

References

  • 01 Ashton,  F. M.. (1976);  Mobilization of storage proteins of seeds.  Ann. Rev. Plant Physiol.. 27 95-117
  • 02 Battey,  N. H.,, James,  N. C.,, Greenland,  A. J.,, and Brownlee,  C.. (1999);  Exocytosis and endocytosis.  The Plant Cell. 11 643-659
  • 03 Benes,  I., and Metlicka,  R.. (1970) Use of artificial membranes. Cell Membrane Transport, Principles and Techniques. Kotyk, A. and Janacek, K., eds. New York; Plenum Press pp. 304-305
  • 04 Blumwald,  E.,, and Gelli,  A.. (1997) Secondary inorganic ion transport at the tonoplast. The Plant Vacuole; In Advances in Botanical Research . Leigh, R. A. and Sanders, D., eds.; Callow J. A., ed. California and London; Academic Press pp. 401-413
  • 05 Chang,  Y. C.,, Yamamoto,  Y.,, and Matsumoto,  H.. (1999);  Accumulation of aluminium in the cell wall pectin in cultured tobacco (Nicotiana tabacum L.) cells treated with a combination of aluminium and iron.  Plant Cell and Environment. 22 1009-1017
  • 06 Chrispeels,  M. J.. (1991);  Sorting of proteins in the secretory system.  Ann. Rev. Plant Physiol. and Plant Mol. Biol.. 42 21-53
  • 07 Coté,  G. G., and Crain,  R. C.. (1993);  Biochemistry of phosphoinositides.  Ann. Rev. Plant Physiol. and Plant Mol. Biol.. 44 333-356
  • 08 Davies,  K. L.,, Davies,  M. S.,, and Francis,  D.. (1991);  The influence of an inhibitor of phytochelatin synthesis on root growth and root meristematic activity in Festuca rubra L. in response to Zinc.  New Phytol.. 118 565-570
  • 09 Davis,  A. D.,, Weatherby,  T. M.,, and Lenz,  P. H.. (1999) Speedy plankton: myelinated axons in calanoid copepods (crustacea). Microscopy and Microanalysis. Bailey, G. W., Jerome, W. G., McKernan, S., Mansfield, J. F., and Price, R. L., eds. Portland, Oregon; Springer pp. 1308-1309
  • 10 Delhaize,  E.,, Ryan,  P. R.,, and Randall,  P. J.. (1993);  Aluminum tolerance in wheat (Triticum aestivum L.) II. Aluminum-stimulated excretion of malic acid from root apices.  Plant Physiol.. 103 695-702
  • 11 Delhaize,  E., and Ryan,  P. R.. (1995);  Aluminum toxicity and tolerance in plants.  Plant Physiol.. 107 315-321
  • 12 Drew,  M. C.,, Jackson,  M. B.,, and Giffard,  S. C.. (1979);  Ethylene-promoted rooting and development of cortical air-spaces (aerenchyma) in roots may be adaptive responses to flooding in Zea mays L.  Planta. 147 83-88
  • 13 Drew,  M. C.. (1997);  Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia.  Annu. Rev. Plant Physiol. Plant Mol. Biol.. 48 223-250
  • 14 Drew,  M. C.,, He,  C. J.,, and Morgan,  P. W.. (2000);  Programmed cell death and aerenchyma formation in roots.  Trends in plant Science. 5 (3) 123-127
  • 15 Drøbak,  B. K.. (1996) Metabolism of plant phosphoinositides and other inositol-containing lipids. Membranes: Specialized Functions in Plants. Smallwood, M., Knox, J. P., and Bowles, D. J., eds. Oxford; BIOS Scientific Publishers pp. 195-210
  • 16 Eleftheriou,  E. P.,, Moustakas,  M.,, and Fragiskos,  N.. (1993);  Aluminate-induced changes in morphology and ultrastructure of Thinopyrum roots.  J. of Exp. Botany. 44 (259) 427-436
  • 17 Erickson,  R. O., and Sax,  K. B.. (1956);  Rates of cell division and cell elongation in the growth of the primary root of Zea mays. .  Proc. Amer. Phil. Soc.. 100 499-514
  • 18 Fineran,  B. A.. (1971);  Ultrastructure of vacuolar inclusions in root tips.  Protoplasma. 72 1-18
  • 19 Gunsé,  B.,, Poschenrieder,  C.,, and Barceló,  J.. (2000);  The role of ethylene metabolism in the short-term responses to aluminium by roots of two maize cultivars different in Al-resistance.  Env. and Exp. Botany. 43 73-81
  • 20 Hall,  J. L.,, Flowers,  T. J.,, and Roberts,  R. M.. (1974) Plant cell structure and metabolism: The golgi body. London; Longman Group Limited pp. 373-396
  • 21 Harvey,  D. M. R.. (1982);  Freeze substitution.  J. Microsc.. 127 209-221
  • 22 Horst,  W. J.,, Asher,  C. J.,, Cakmak,  J.,, Szulkiewicz,  P.,, and Wissemeier,  A. H.. (1991) Short-term responses of soybean roots to aluminium. Plant-Soil Interactions at Low pH. Wright, R. J., Baligar, V. C., and Murrmann, R. P., eds. Dordrecht, Boston, London; Kluwer Academic Publishers pp. 733-739
  • 23 Horst,  W. J.,, Püschel,  A. K.,, and Schmohl,  N.. (1997);  Induction of callose formation is a sensitive marker for genotypic aluminium sensitivity in maize.  Plant Soil. 192 23-30
  • 24 Jost,  P.,, Waggoner,  A. S.,, and Griffith,  O. H.. (1971) Structure and function of biological membranes. Biological Membranes: An Overview at the Molecular Level. Rothfield, L. I., ed. New York; Academic Press pp. 83-144
  • 25 Justin,  S., and Armstrong,  W.. (1987);  The anatomical characteristics of roots and plant response to soil flooding.  New Phytol.. 106 465-495
  • 26 Kauss,  H.. (1996) Callose synthesis. Membranes: Specialized Functions in Plants. Smallwood, M., Knox, J. P., and Bowles, D. J., eds. Oxford; Bios Scientific Publishers pp. 77-89
  • 27 Kochian,  L. V.. (1995);  Cellular mechanisms of aluminum toxicity and resistance in plants.  Annu. Rev. Plant Physiol. Plant Mol. Biol.. 46 237-260
  • 28 Kollmeier,  M.,, Felle,  H. H.,, and Horst,  W. J.. (2000);  Genotypical differences in aluminum resistance of maize are expressed in the distal part of the transition zone. Is reduced basipetal auxin flow involved in inhibition of root elongation by aluminum?.  Plant Physiology. 122 945-956
  • 29 Kollmeier,  M.,, Dietrich,  P.,, Bauer,  C. S.,, Horst,  W. J.,, and Hedrich,  R.. (2001);  Aluminum activates a citrate-permeable anion channel in the aluminum-sensitive zone of the maize root apex. A comparison between an aluminum-sensitive and an aluminum resistant cultivar.  Plant Physiology. 126 397-410
  • 30 Krotz,  R. M.,, Evangelou,  B. P.,, and Wagner,  G. J.. (1989);  Relationships between cadmium, zinc, Cd-peptide, and organic acid in tobacco suspension cells.  Plant Physiology. 91 180-187
  • 31 Lazof,  D. B.,, Rincon,  M.,, Rufty,  T. W.,, Mckown,  C. T.,, and Carter,  T. E.. (1994);  Aluminium accumulation and associated effects on 15NO3 - influx in roots of two soybean genotypes differing in Al tolerance.  Plant Soil. 164 291-297
  • 32 Lazof,  D. B.,, Goldsmith,  J. G.,, Rufty,  T. W.,, and Linton,  R. W.. (1996);  The early entry of Al into cells of intact soybean roots. A comparison of three developmental root regions using secondary ion mass spectrometry imaging.  Plant Physiol.. 112 1289-1300
  • 33 Lazof,  D. B.,, Goldsmith,  J. G.,, and Linton,  R. W.. (1997);  The in situ analysis of intracellular aluminum in plants.  Prog. Bot.. 58 112-149
  • 34 Lewis,  P. R., and Knight,  D. P.. (1977) General cytochemical methods. Staining methods for sectioned material. Practical Methods in Electron Microscopy. Glauert, A. M., ed. Amsterdam; Elsevier/North-Holland pp. 77-135
  • 35 Lindberg,  S., and Griffiths,  G.. (1993);  Aluminium effects on ATPase activity and lipid composition of plasma membranes in sugar beet roots.  Journal of Experimental Botany. 44 (267) 1543-1550
  • 36 Loewus,  F. A., and Loewus,  M. W.. (1983);  myo-Inositol: its biosynthesis and metabolism.  Ann Rev Plant Physiol. 34 137-1161
  • 37 Llugany,  M.,, Massot,  N.,, Wissemeier,  A. H.,, Poschenrieder,  C.,, Horst,  W. J.,, and Barceló,  J.. (1994);  Aluminium tolerance of maize cultivars as assessed by callose production and root elongation.  Z. Pflanzenernähr. Bodenk.. 157 447-451
  • 38 Llugany,  M.,, Poschenrieder,  C.,, and Barceló,  J.. (1995);  Monitoring of aluminium-induced inhibition of root elongation in four maize cultivars differing in tolerance to induced and proton toxicity.  Physiología Plantarum. 93 265-271
  • 39 Marty,  F.. (1997) The Biogenesis of vacuoles: insights from microscopy. The plant vacuole; In Advances in Botanical research. Leigh, R. A. and Sanders, D., eds.; Callow, J. A., ed. California and London; Academic Press pp. 1-33
  • 40 Marschner,  H.. (1986) Mineral nutrition of higher plants. London; Academic Press pp. 1-674
  • 41 Martinoia,  E., and Ratajczak,  R.. (1997) Transport of organic molecules across the tonoplast. The Plant Vacuole; Advances in Botanical Research. Leigh, R. A. and Sanders, D., eds.; Callow, J. A., ed. California and London; Academic Press pp. 366-390
  • 42 Matile,  P., and Moore,  H.. (1968);  Vacuolation: origin and development of the lysosomal apparatus in root tip cells.  Planta (Berlin). 80 159-175
  • 43 Matile,  P.. (1997) The vacuole and cell senescence. The Plant Vacuole; Advances in Botanical Research. Leigh, R. A. and Sanders, D., eds.; Callow J. A., ed. California and London; Academic Press pp. 87-107
  • 44 Meharg,  A. A.. (1994);  Opinion: Integrated tolerance mechanisms: constitutive and adaptive plant responses to elevated metal concentrations in the environment.  Plant Cell and Environment. 17 989-993
  • 45 Mentré,  P., and Escaig,  F.. (1988);  Localization of cations by pyroantimonate. I. Influence of fixation on distribution of calcium and sodium. An approach by analytical ion microscopy.  J. of Histochem. Cytochem.. 36 (1) 49-54
  • 46 Mentré,  P., and Halpern,  S.. (1988);  Localization of cations by pyroantimonate. II. Electron probe microanalysis of calcium and sodium in skeletal muscle of mouse.  J. of Histochem. Cytochem.. 36 (1) 55-64
  • 47 Mikus,  M.,, Bobak,  M.,, and Lux,  A.. (1992);  Structure of protein bodies and elemental composition of phytin from dry germ of maize (Zea mays L.).  Bot. Acta. 105 26-33
  • 48 Mikus,  M.,, Lux,  A.,, Crans,  D. C.,, Shi,  P. K.,, and Kristin,  J.. (1995) Comparison of phytate in radicle, plumule, scutellum and endosperm of Zea mays and Zea diploperennis seeds. Structure and Function of Roots. Baluska, F., Ciamporova, M., Gasparikova, O., Barlow, and P. W., eds. Dordrecht, Boston, London; Kluwer Academic Publishers pp. 175-180
  • 49 Miyasaka,  S. C.,, Buta,  J. G.,, Howell,  R. K.,, and Foy,  C. D.. (1991);  Mechanism of aluminium tolerance in snapbeans.  Plant Physiol.. 96 737-743
  • 50 Moog,  P. R.. (1998);  Flooding tolerance of Carex species. I. Root structure.  Planta. 207 189-198
  • 51 Mueller,  W. C.,, Morgham,  A. T.,, and Roberts,  E. M.. (1994);  Immunocytochemical localization of callose in the vascular tissue of tomato and cotton plants infected with Fusarium oxysporum. .  Can. J. Bot.. 72 505-509
  • 52 Nebenführ,  A.,, Frohlick,  J. A.,, and Staehelin,  A.. (2000);  Redistribution of golgi stacks and other organelles during mitosis and cytokinesis in plant cells.  Plant Physiol.. 124 135-152
  • 53 Oud,  J. L., and Nanninga,  N.. (1995) The relation between cell size, chromosome length and the orientation of chromosomes in dividing root cortex cells. Structure and Function of Roots. Baluska, F., Ciamporova, M., Gasparikova, O., and Barlow, P. W., eds. Dordrecht, Boston, London; Kluwer Academic Publishers pp. 33-39
  • 54 Paris,  N.,, Stanley,  M.,, Jones,  R. L.,, and Rogers,  J. C.. (1996);  Plant cells contain two funtionally distinct vacuolar compartments.  Cell. 85 563-572
  • 55 Parker,  D. R.,, Zelazny,  L. W.,, and Kinraide,  T. B.. (1987);  Improvements to the program GEOCHEM.  Soil Sci. Soc. Am. J.. 51 488-491
  • 56 Pellet,  D. M.,, Grunes,  D. L.,, and Kochian,  L. V.. (1995);  Organic acid exudation as an aluminum-tolerance mechanism in maize (Zea mays L.).  Planta. 196 788-795
  • 57 Pellet,  D. M.,, Papernik,  L. A.,, and Kochian,  L. V.. (1996);  Multiple aluminum-resistance mechanisms in wheat. Roles of root apical phosphate and malate exudation.  Plant Physiol.. 112 591-597
  • 58 Piñeros,  M. A., and Kochian,  L. V.. (2001);  A patch-clamp study on the physiology of aluminum toxicity and aluminum tolerance in maize: identification and characterization of Al3+-induced anion channels.  Plant Physiology. 125 292-305
  • 59 Rengel,  Z.. (1992 a);  Role of calcium in aluminium toxicity.  New Phytol.. 121 499-513
  • 60 Rengel,  Z.. (1992 b);  Disturbance of cell Ca2+ homeostasis as a primary trigger of Al toxicity syndrome.  Plant Cell and Environment. 15 931-938
  • 61 Reynolds,  E. S.. (1963);  The use of lead citrate at high pH as an electron opaque stain in electron microscopy.  J. Cell Biol.. 17 208-210
  • 62 Rincón,  M., and González,  R. A.. (1992);  Aluminum partitioning in intact roots of aluminum-tolerant and aluminum-sensitive wheat (Triticum aestivum L.) cultivars.  Plant Physiol.. 99 1021-1028
  • 63 Ryan,  P. R.,, Ditomaso,  J. M.,, and Kochian,  L. V.. (1993);  Aluminum toxicity in roots: an investigation of spatial sensitivity and the role of the root cap.  J. Exp. Bot.. 44 437-446
  • 64 Ryan,  P. R.,, Delhaize,  E.,, and Jones,  D. L.. (2001);  Function and mechanism of organic anion exudation from plant roots.  Annu. Rev. Plant Physiol. Plant Mol. Biol.. 25 527-560
  • 65 Salt,  D. E., and Wagner,  G. J.. (1993);  Cadmium transport across tonoplast of vesicles from oat roots.  Journal of Biological Chemistry. 268 297-302
  • 66 Salt,  D. E.,, Smith,  R. D.,, and Raskin,  I.. (1998);  Phytoremediation.  Ann. Rev. Plant Physiol. Plant Mol. Biol.. 49 643-668
  • 67 Sivaguru,  M., and Horst,  W. J.. (1998);  The distal part of the transition zone is the most aluminum-sensitive apical root zone of maize.  Plant Physiology. 116 155-163
  • 68 Sivaguru,  M.,, Baluska,  F.,, Volkmann,  D.,, Felle,  H. H.,, and Horst,  W. J.. (1999);  Impacts of aluminum on the cytoskeleton of the maize root apex. Short-term effects on the distal part of the transition zone.  Plant Physiology. 119 1073-1082
  • 69 Sivaguru,  M.,, Fijiwara,  T.,, Samaj,  J.,, Baluska,  F.,, Yang,  Z.,, Osawa,  H.,, Maeda,  T.,, Mori,  T.,, Volkmann,  D.,, and Matsumoto,  H.. (2000);  Aluminum-induced 1-3-β-D-glucan inhibits cell-to-cell trafficking of molecules through plasmodesmata.  A New Mechanism of Aluminum Toxicity in Plants. 124 991-1005
  • 70 Spurr,  A. R.. (1969);  A low-viscosity epoxy resin embedding medium for electron microscopy.  J. Ultrastr. Res.. 26 31-43
  • 71 Strange,  J., and Macnair,  R.. (1991);  Evidence for a role for the cell membrane in copper tolerance of Mimulus guttatus Fischer ex DC.  New Phytol.. 119 383-388
  • 72 Taylor,  G. J.. (1988) The physiology of aluminum phytotoxicity. Metal Ions in Biological Systems. Aluminum and its Role in Biology. Sigel, H.and Sigel, A., eds. New York; Marcel Dekker Inc. pp. 123-163
  • 73 Tice,  K. R.,, Parker,  D. R.,, and Demason,  D. A.. (1992);  Operationally defined apoplastic and symplastic aluminum fractions in root tips of aluminum-intoxicated wheat.  Plant Physiol.. 100 309-318
  • 74 van Steveninck,  R. F. M.,, Babare,  A.,, Fernando,  D. R.,, and van Steveninck,  M. E.. (1995) The binding of zinc, but not cadmium, by phytic acid in roots of crop plants. Structure and Function of Roots. Baluska, F., Ciamporova, M., Gasparikova, O., and Barlow, P. W., eds. Dordrecht, Boston, London; Kluwer Academic Publishers pp. 319-326
  • 75 Vázquez,  M. D.,, Poschenrieder,  Ch.,, and Barceló,  J.. (1992);  Ultrastructural effects and localization of low cadmium concentrations in bean roots.  New Phytologist. 120 215-226
  • 76 Vázquez,  M. D.,, Poschenrieder,  Ch.,, Barceló,  J.,, Baker,  A. J. M.,, Hatton,  P.,, and Cope,  G. H.. (1994);  Compartmentation of zinc in roots and leaves of the zinc hyperaccumulator Thlaspi caerulescens. .  J. and C. Presl. Bot. Acta. 107 187-270
  • 77 Vázquez,  M. D.,, Poschenrieder,  Ch.,, Corrales,  I.,, and Barceló,  J.. (1999);  Change in apoplastic aluminum during the initial growth response to aluminum by roots of a tolerant maize variety.  Plant Physiology. 119 435-444
  • 78 Vázquez,  M. D.. (2000) Confocal laser scanning microscopy applied to root tips of Al-treated maize plants: considerations about aluminum localization by fluorescent staining. Jornadas de Microscopía Confocal a la UAB. Servei de Microscòpia Electrónica. Bellaterra. Barcelona; Universitat Autónoma de Barcelona. Abstract Book pp. 44-45
  • 79 Verkleij,  J. A. C., and Schat,  H.. (1990) Ecophysiology of metal uptake by tolerant plants. Heavy Metal Tolerance in Plants: Evolutionary Aspects. Shaw, A. J., ed. Boca Raton, FL; CRC Press pp. 179-193
  • 80 Wink,  M.. (1993);  The plant vacuole: a multifunctional compartment.  Journal of Experimental Botany. 44 231-246
  • 81 Wissemeier,  A H.,, Klotz,  F.,, and Horst,  W. J.. (1987);  Aluminium induced callose synthesis in roots of soybean (Glycine max L.).  J. Plant Physiol.. 129 487-492
  • 82 Wissemeier,  A. H.,, Difning,  A.,, Hergenröder,  A.,, Horst,  W. J.,, and Mix-Wagner,  G.. (1992);  Callose formation as parameter for assessing genotypical plant tolerance of aluminium and manganese.  Plant and Soil. 146 67-75
  • 83 Wissemeier,  A. H., and Horst,  W J.. (1995);  Effect of calcium supply on aluminium-induced callose formation, its distribution and persistence in roots of soybean (Glycine max [L.]).  J. Plant Physiol.. 129 487-492
  • 84 Woolhouse,  H. W.. (1983) Toxicity and resistance in the responses of plants to metals. Physiological Plant Ecology. III. Responses to the Chemical and Biological Environment. Encyclopaedia of Plant Physiology New Series, Vol. 12 C. Lange, O. L., Nobel, P. S., Osmond, C. B., and Ziegler, H., eds. Berlin; Springer Verlag pp. 245-300
  • 85 Zhang,  G. C., and Taylor,  G. J.. (1989);  Kinetics of aluminum uptake by excised roots of aluminum-tolerant and aluminum-sensitive cultivars of Triticum aestivum L.  Plant Physiol.. 91 1094-1099
  • 86 Zhang,  G. C., and Taylor,  G. J.. (1993);  Callose synthesis induced by aluminum stress.  Plant Physiol.. 102 (suppl. 1) 174
  • 87 Zhang,  G. C.,, Hoddinott,  J.,, and Taylor,  G. J.. (1994);  Characterization of 1,3-β-D-glucan (callose) synthesis in roots of Triticum aestivum in response to aluminum toxicity.  J. Plant Physiol.. 144 229-234
  • 88 Zhao,  F. J.,, Shen,  Z. G.,, and McGrath,  S. P.. (1998);  Solubility of zinc and interactions between zinc and phosphorus in the hyperaccumulator Thlaspi caerulescens. .  Plant Cell and Environment. 21 108-114

M. D. Vázquez

Apdo. de Correos 255
08290 Cerdanyola del Vallès, Barcelona
Spain

Email: mariadolores.vazquez@uab.es

Section Editor: W. B. Frommer

    >