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Localization of potential ion transport pathways in vesicular trichome cells of Atriplex halimus L.

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Abstract

The secreting glandular trichomes are recognized as an efficient structure that alleviates salt effects on Atriplex halimus. They are found on buds, young green stems, and leaves. They occupy both the leaf surfaces and give them a whitish color. Their histogenesis and ultrastructure were investigated in the third young leaves. They appear in early stage of plant development and its initiation continuous until just the leaf final development state. Each trichome contains two parts; a stalk which has high electron opacity, embedded in epidermal cells, and bears a second one which is unicellular, called bladder cell and has a low electron density. The bladder cell appears as a huge vacuole and the well-reduced cytoplasm which is pushed close to the wall, contains only a few organelles. Concurrently, the use of silver chloride precipitation technique shows that, in secretion process, salt follows a symplasmatic pathway which is consolidated by the presence of numerous plasmodesmata between the stalk cell(s), and the bladder one and the neighboring mesophyll cells. In addition, according to lanthanum-tracer study, salt can be excreted apoplastically. In fact, the heavy element can be transported via endocytosis vesicles, and by Golgi, endoplasmic reticulum, and lysosome (G.E.R.L.) network toward the storage vacuoles.

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Abbreviations

bc:

Bladder cell

d:

Dictyosome

ec:

Epidermal cell

er:

Endoplasmic reticulum

gv:

Golgien vesicle

l:

Lysosome

m:

Mitochondrion

n:

Nucleus

ne:

Nucleus envelope

p:

Plastid

pds:

Plasmodesmata

pl:

Plasmalemma

pv:

Pinocytosis vesicle

rer:

Rough endoplasmic reticulum

sc:

Stalk cell

v:

Vacuole

vs:

Vesicles

w:

Wall

References

  • Atkinson MR, Polya GM (1967) Salt stimulated adenosine triphosphatases from carrot, beet, and chara Australis. Aust J Biol Sci 20:1069–1086

    CAS  Google Scholar 

  • Bajji M, Kinet JM, Lutts S (1998) Salt stress effects on roots and leaves of Atriplex halimus L. and their corresponding callus cultures. Plant Sci 137:131–142

    Article  CAS  Google Scholar 

  • Baker DA, Hall JL (1973) Pinocytosis, ATPase, and ion uptake by plant cells. New Phytol 72:1281–1291

    Article  CAS  Google Scholar 

  • Barhoumi Z, Djebali W, Smaoui A, Chaïbi W, Abdelly C (2007) Contribution of NaCl excretion to salt resistance of Aeluropus littoralis (Willd) Parl. J Plant Physiol 164:842–850

    Article  PubMed  CAS  Google Scholar 

  • Barnabas AD (1994) Apoplastic and symplastic pathways in leaves and roots of the seagrass Halodule uninervis (Foressk.) Aschers. Aquat Bot 47:155–174

    Article  Google Scholar 

  • Black RF (1954) The leaf anatomy of Australian members of the genus Atriplex. Aust J bot 2:269–286

    Article  Google Scholar 

  • Clarkson DT, Sanderson J (1971) Inhibition of the uptake and long-distance transport of calcium by aluminium and other polyvalent cations. J Exp Bot 23:837–851

    Article  Google Scholar 

  • Coulomb C (1971) Processus lytique dans les vacuoles des cellules radiculaires méristématiques de la scorsonère (Scorzonera hispanica): Thèse de spécialité, Université d’Aix Marseille II

  • Coulomb C, Coulomb Ph (1973) Cheminement intracellulaire des particules d’or colloïdal après pénétration favorisée par le “Triton WR 1339” dans les cellules des méristèmes radiculaires de la courge. C R Acad Sc 277:165–168

    CAS  Google Scholar 

  • Coulomb C, Coulomb Ph (1975) Etude autoradiographique préliminaire de la pénétration du Triton WR 1339 tritié dans les cellules du méristème radiculaire de la courge. C R Acad Sc 288:1083–1086

    Google Scholar 

  • Fisher J, Hodges TK (1969) Monovalent ion stimulated adenosine triphosphatase from oat root. Plant Physiol 44:385–395

    Article  PubMed  CAS  Google Scholar 

  • Galle P (1974) Rôle des lysosomes et des mitochondries dans les phénomènes de concentration et d’élimination d’éléments minéraux (uranium et or) par le rein. J Microsc 19:17–24

    CAS  Google Scholar 

  • Gierth M, Stelzer R, Lehmann H (1999) An analytical microscopical study of the role of the exodermis in apoplastic Rb+ (K+) transport in barley roots. Plant Soil 207:209–218

    Article  Google Scholar 

  • Gruner N, Neumon (1966) Anion stimulated ATPase from bean roots. Physiologica Pl 19:678

    Article  Google Scholar 

  • Hall JC (1970) Pinocytosis vesicles and ion transport in plant cells. Nature 226:1253–1254

    Article  PubMed  CAS  Google Scholar 

  • Hewitt EJ (1966) Sand and water culture methods used in the study of plant nutrition. Commonw Bur Hortic Tech Commun 22:431–446

    Google Scholar 

  • Holtzman E, Novikoff AB, Villaverde H (1967) Lysosomes and G.E.R.L. in normal and chromolytic neurons of the rat ganglion nodosin. J Cell Biol 33:419–436

    Article  PubMed  CAS  Google Scholar 

  • Karimi SH, Ungar IA (1989) Development of epidermal salt hairs in Atriplex triangularis wild. in response to salinity, light intensity, and aeration. Bot Gaz 150:68–71

    Article  Google Scholar 

  • Komnicke H, Bierther M (1969) On the histochemical localisation of ions by electron microscopy, with special reference to the chloride reaction. Histochemie 180:337–362

    Google Scholar 

  • Kylin A, Gee R (1970) Adenosine triphosphatase activities in leaves of the mangrove Avicenna nitida Iacp. Influence of sodium to potassium ratios and salt concentrations. Plant Physiol 45:169–172

    Article  PubMed  CAS  Google Scholar 

  • La Clair II CW (1982) Wound-healing motility in the green alga Ernodesmis: calcium ions and metabolic energy are required. Planta 156:466–474

    Article  Google Scholar 

  • Le Houérou H (2000) Utilization of fodder trees and shrubs in the arid and semiarid zones of West Asia and North Africa. Arid Soil Res Rehabil 14:101–135

    Google Scholar 

  • Lehmann H, Stelzer R, Holzamer S, Kunz U, Gierth M (2000) Analytical electron microscopical investigations on the apoplastic pathways of lanthanum transport in barley roots. Planta 211:816–822

    Article  PubMed  CAS  Google Scholar 

  • Levering CA, Thomson WW (1971) The ultrastructure of salt gland of Spartina foliosa. Planta 97:183–196

    Article  Google Scholar 

  • Livne A, Levin N (1967) Tissue respiration and mitochondrial oxidative phosphorylation of NaCl treated pea seedlings. Plant Physiol 42:407–414

    Article  PubMed  CAS  Google Scholar 

  • Malone C, Koeppe DE, Miller RJ (1974) Localization of lead accumulated by corn plants. Plant Physiol 53:388–394

    Article  PubMed  CAS  Google Scholar 

  • Marty F (1974) Vacuome et sécretion intracellulaire. Thèse de Doctorat d’Etat, Université d’Aix-Marseille II, Luminy

  • Mozafar A, Goodin JR (1970) Vesiculated hairs: a mechanism for salt tolerance in Atriplex halimus L. Plant Physiol 45:62–65

    Article  PubMed  CAS  Google Scholar 

  • Nagahashi G, Thomson WW, Leonard RT (1974) The casparian strip as a barrier to the movement of lanthanum in corn roots. Science 183:670–671

    Article  PubMed  CAS  Google Scholar 

  • Naido Y, Naido G (2008) Localisation of potential ion transport pathways in the salt glands of the halophyte Sporobolus virginicus. In: Khan MA, Weber DL (eds) Ecophysiology of high salinity tolerant plants. Springer, New York, pp 173–185

    Google Scholar 

  • Novikoff AB, Essner E, Quintana N (1963) Relations of endoplasmic reticulum Golgi apparatus and lysosomes. Soc Fr Microsc Electr, Coll Ann Orsay. J Microscopie 2–3

  • Osmond CB, Lüttge U, West KR, Pallaghy CK, Shachar-Hill B (1969) Ion absorption in Atriplex leaf tissue. II. Secretion of ions to epidermal bladders. Aust J Biol Sci 22:797–814

    CAS  Google Scholar 

  • Osmond CB, Bjorkman O, Anderson DJ (1980) Physiological processes in plant ecology. Springer, Berlin

    Google Scholar 

  • Peterson TA, Swanson ES, Hull RJ (1986) Use of lanthanum to trace apoplastic solute transport in intact plants. J Exp Bot 37:807–822

    Article  CAS  Google Scholar 

  • Reynolds RS (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J Cell Biol 17:208–213

    Article  PubMed  CAS  Google Scholar 

  • Robards AW, Robb ME (1974) The entry of ions and molecules into roots: an investigation using electron-opaque tracers. Planta 120:1–12

    Article  CAS  Google Scholar 

  • Schröder M, Kunz U, Stelzer R, Lehmann H (2002) On the evidence of a diffusion barrier in the outer cortex apoplast of cress-roots (Lepidium sativum), demonstrated by analytical electron microscopy. J Plant Physiol 159:1197–1204

    Article  Google Scholar 

  • Shabala S, Neman I (2000) Salinity effects on the activity of plasma membrane H+ and Ca2+ transporters in bean leaf mesophyll: masking role of the cell wall. Ann Bot 85:681–686

    Article  CAS  Google Scholar 

  • Sharma ML (1982) Aspects of salinity and water relations of Australian Chenopods. In: Sen DN, Rajpurohit KS (eds) Contributions to the ecology of halophytes. Junk, The hague, pp 155–172

    Google Scholar 

  • Shimony C, Fahn A, Reinhold L (1973) Ultrastructure and ion gradients in the salt glands of Avicennia marina (Forssk.) Vienh. New Phytol 72:27–36

    Article  CAS  Google Scholar 

  • Shone MGT, Clarkson DT, Sanderson J, Wood AV (1973) A comparison of the uptake and translocation of some organic molecules and ions in higher plants. In: Anderson WP (ed) Ion transport in plants. Academic, London, pp 571–582

    Google Scholar 

  • Somaru R, Naidoo Y, Naidoo G (2002) Morphology and ultrastructure of the leaf salt glands of Odyssea paucinervis (Stapf) (Poaceae). Flora 197:67–57

    Google Scholar 

  • Stelzer R, Lehmann H (1993) Recent developments in electron microscopical techniques for studying ion localization in plant cells. Plant Soil 155:33–43

    Article  Google Scholar 

  • Sutclifee JF (1962) Mineral salts absorption in plants. Pergamon, Oxford

    Google Scholar 

  • Thomson W, Platt-Aloia K (1979) Ultrastructural transitions associated with the development of the bladder cells of the trichomes of Atriplex. Cytobios 25:105–114

    PubMed  CAS  Google Scholar 

  • Thomson WW, Berry WL, Liu LL (1969) Localization and secretion of salt by the salt glands of Tamarix aphylla. Botany 63:310–317

    CAS  Google Scholar 

  • Thomson WW, Platt KA, Campbell N (1973) The use of lanthanum to delineate the apoplastic continuum in plants. Cytobios 8:57–62

    PubMed  CAS  Google Scholar 

  • Van Steveninck RFM, Chenowith ARF (1972) Ultrastructural localisation of ions: I. Effect of high external sodium chloride concentration on the apparent distribution of chloride in leaf parenchyma cells of barley seedlings. Aust J Biol Sci 25:499–516

    Google Scholar 

  • Wheeler H, Hanchey P (1971) Pinocytosis and membrane dilution in uranyl treated plants roots. Science 171:68–77

    Article  PubMed  CAS  Google Scholar 

  • Wheeler H, Baker BL, Hanchey P (1972) Pinocytosis in root cap cells exposed to uranyl salts. Ann J Bot 59:858–868

    Article  CAS  Google Scholar 

  • Ziegler H, Lüttge U (1966) Die salz drüsen von Limonium vulgare. I. Mitteilung: Die feinstruktur. Planta 70:193–206

    Article  CAS  Google Scholar 

  • Ziegler H, Lüttge U (1967) Die salz drüsen von Limonium vulgare. II. Mitteilung Die lokalizierung des chlorids. Planta 74:1–17

    Article  Google Scholar 

Download references

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Authors and Affiliations

  1. Laboratoire des Plantes Extremôphiles, Centre de Biotechnologie de la Technopole de Borj-Cedria, BP 901, Hammam-Lif, 2050, Tunisia

    Abderrazak Smaoui, Zouhaier Barhoumi, Mokded Rabhi & Chedly Abdelly

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  1. Abderrazak Smaoui
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  2. Zouhaier Barhoumi
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  3. Mokded Rabhi
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  4. Chedly Abdelly
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Correspondence to Zouhaier Barhoumi.

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Smaoui, A., Barhoumi, Z., Rabhi, M. et al. Localization of potential ion transport pathways in vesicular trichome cells of Atriplex halimus L.. Protoplasma 248, 363–372 (2011). https://doi.org/10.1007/s00709-010-0179-8

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  • DOI: https://doi.org/10.1007/s00709-010-0179-8

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