Abstract
The epidermal salt glands of the leaf of Distichlis spicata ‘Yensen 4a’ (Poaceae) have a direct contact with one or two water-storing parenchyma cells, which act as collecting cells. A vacuole occupying almost the whole volume of the collecting cell has a direct exit into the extracellular space (apoplast) through the invaginations of the parietal layer of the cytoplasm, which is interrupted in some areas so that the vacuolar-apoplastic continuum is separated only by a single thin membrane, which looks as a valve. On the basis of ultrastructural morphological data (two shapes of the extracellular channels, narrow and extended, are found in basal cells), the hypothesis on the mechanical nature of the salt pump in the basal cell of Distichlis leaf salt gland is proposed. According to the hypothesis, a driving force giving ordered motion to salt solution from the vacuole of the collecting cell through the basal cell of the salt gland to cap cell arises from the impulses of a mechanical compression–expansion of plasma membrane, which penetrates the basal cell in the form of extracellular channels. The acts of compression–expansion of these extracellular channels can be realized by numerous microtubules present in the basal cell cytoplasm.
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Abbreviations
- BC:
-
Basal cell
- CC:
-
Cap cell
- COC:
-
Collecting cells
- Ec:
-
Extracellular channel
- Gc:
-
Granular complex
- M:
-
Mitochondrion
- Me:
-
Mesophyll cells
- Mt:
-
Microtubules
- P:
-
Plastid
- V:
-
Vacuole
References
Barhoumi Z, Djebali W, Abdelly C, Chaibi W, Smaoui A (2008) Ultrastructure of Aeluropus littoralis leaf salt glands under NaCl stress. Protoplasma 233:195–202
Bell HL, Columbus JT (2008) Proposal for an expanded Distichlis (Poaceae, Chloridoideae): support from molecular, morphological, and anatomical characters. System Bot 33:536–551
Biel KY, Yensen NP (2005a) The hypothesis of halosynthesis, photoprotection, soil remediation via salt-conduction, and potential medical benefits. In: Khlebopros RG, Soukhovolsky VG (eds) Complex systems under extreme conditions. Krasnoyarsk, Russia, pp 86–115
Biel KY, Yensen NP (2005b) The hypothesis of photo-halosynthesis and its application for some agricultural and medical problems. In: Martirosyan DM (ed) Functional foods for cardiovascular diseases. Functional foods can help reduce the risks of cardiovascular diseases. Richardson, Texas, USA, pp 215–227
Biel KY, Yensen NP (2006) Salt removal by conductor plants. Patent Pending, submitted to the United States Patent and Trademark Office, p 26
Biel KY, Fomina IR (2009) The effect of sodium chloride concentration on photosynthesis, respiration and pigment content in systems of whole-shoot-leaf blades versus leaf-blade slices in saltgrass Distichlis spicata (Poaceae), in preparation
Blackman LM, Overall RL (2001) Structure and function of plasmodesmata. Aust J Plant Physiol 28:709–727
Campbell N, Thomson WW (1975) Chloride localization in the leaf of Tamarix. Protoplasma 83:1–14
Campbell N, Thomson WW (1976) The ultrastructure of Frankenia salt glands. Ann Bot 40:681–686
Campbell N, Thomson WW, Platt K (1974) The apoplastic pathway of transport to salt glands. J Exp Bot 25:61–69
Canny MJ (1998) Applications of the compensating pressure theory of water transport. Amer J Bot 85:897–909
Chentsov YuS (1978) Obshchaya tsitologiya (general cytology). Publ House Moscow State University, Moscow
D’yachenko AI, Shabelnikov VG (1985) Mathematical models of gravitation effects on the lungs’ functions. In: Ugolev AM, Genin AM (eds) Problemy kosmicheskoi biologii (problems of space biology), vol 51. Nauka, Moscow
Esau K (1977) Anatomy of seed plants. John Wiley and Sons, New York
Fahn A (1979) Secretory tissues in plants. Academic, London
Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963
Flowers TJ, Hagibagheri MA, Clipson NJW (1986) Halophytes. Quart Rev Biol 61:313–337
Gamalei YuV (2004) Transportnaya sistema sosudistykh rastenii (transport system of vascular plants). Publ House S-Petersburg State University, S-Petersburg
Gamalei YuV (2007) The role of mesophyll cell tonoplast in determining the route of phloem loading. Thirty years of the studies of phloem loading. Russian J Plant Physiol 54:1–9
Gamalei YuV, Pakhomova MV (2002) Electron-microscopic evidence of the vacuolar nature of phloem exudates. Russian J Plant Physiol 49:159–171
Gamalei YuV, Van Bel AJE, Pakhomova MV, Sjutkina AV (1994) Effect of temperature on the conformation of the endoplasmic reticulum and on starch accumulation in leaves with the symplasmic minor-vein configuration. Planta 194:443–453
Ganning BES, Hardham AR (1982) Microtubules. Ann Rev Plant Physiol 33:651–698
Kwok E, Hanson MR (2004) Stromulas and the dynamic nature of plastid morphology. J Microscopie 214:124–137
Levering CA, Thomson WW (1971) The ultrastructure of the salt gland of Spartina foliosa. Planta 97:183–196
Liphschitz N, Waisel Y (1974) Existence of salt glands in various genera of the Graminaceae. New Phytol 73:507–513
Naidoo Y, Naidoo G (1998) Salt glands of Sporobolus virginicus: morphology and ultrastructure. S Afr J Bot 64:198–204
Oross JW, Thomson WW (1982) The ultrastructure of the salt glands of Cynodon and Distichlis (Poaceae). Amer J Bot 69:939–949
Overall RL, Blackman LM (1996) A model of the macromolecular structure of plasmodesmata. Trends Plant Sci 1:307–311
Semenova GA (1978) The ultrastructural organization of the eyespot of Chlamydomonas. Tsitologiya 20:603–607
Semenova GA (2005) Electron opaque contents of thylakoids in chloroplasts of tansy Tanacetum vulgare L. Tsitologiya 47:510–518
Shimony C, Fahn A, Reinhold L (1973) Ultrastructure and ion gradients in the salt glands of Avicennia marina. New Phytol 72:27–36
Thomson WW (1975) The structure and function of salt glands. In: Poljakoff-Mayber A and Gale J (eds) Plants in saline environments. Ecological Studies, vol 15. Springer, Berlin, Heidelberg, New York, pp 118–146
Thomson WW, Liu LL (1967) Ultrastructural features of the salt glands of Tamarix aphylla L. Planta 73:201–220
Thomson WW, Faradey CD, Oross JW (1988) Salt glands. In: Baker DA, Hall JL (eds) Soluble transport in plant cells and tissues. Longman, London, pp 498–537
Van Gestel K, Köhler RH, Verbelen JP (2002) Plant mitochondria move on F-actin, but their positioning in the cortical cytoplasm depends on both F-actin and microtubules. J Exp Bot 53:659–667
Waisel Y (1972) Biology of halophytes. Academic, New York and London
Yensen NP (1985) Saline agriculture and new halophyte crops. In: Proceedins of the 61st annual meeting of the Southwestern and Rocky Mountain Division, AAAS, March 27. Rocky Mountain, pp 19–23
Yensen NP, Biel KY (2006) Soil remediation via salt-conduction and the hypothesis of halosynthesis and photoprotection. In: Khan MA and Weber DJ (eds) Ecophysiology of high salinity tolerant plants. Tasks for vegetation science—40. Published by Springer, pp 313–344
Zholkevich VN, Gusev NA, Kaplya AV, Pakhomova GE, Pilshchikova NV, Samuilov FD, Slavnii PC, Shmatko IG (1989) Vodnyi obmen v rasteniyakh (water exchange in plants). Nauka, Moscow
Zholkevich VN, Emel’yanova IB, Sushchenko SV (2005) Self-oscillations of water transport in the plant root. Dokl Biol Sci 403:269–271
Acknowledgment
We have dedicated this paper to the memory of our friend and colleague, Dr. Nicholas Patrick Yensen, who made a tremendous contribution into research of Distichlis, but unfortunately succumbed to a battle with pancreatic cancer on August 24, 2006.
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The authors declare that they have no conflict of interest.
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Semenova, G.A., Fomina, I.R. & Biel, K.Y. Structural features of the salt glands of the leaf of Distichlis spicata 'Yensen 4a' (Poaceae). Protoplasma 240, 75–82 (2010). https://doi.org/10.1007/s00709-009-0092-1
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DOI: https://doi.org/10.1007/s00709-009-0092-1