THE STRUCTURE OF THE CUTICLE IN RELATION TO CUTICULAR TRANSPIRATION IN LEAVES OF THE HALOPHYTE SUAEDA MARITIMA (L.) DUM.
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1 New Phytol. (1983) 94, THE STRUCTURE OF THE CUTICLE IN RELATION TO CUTICULAR TRANSPIRATION IN LEAVES OF THE HALOPHYTE SUAEDA MARITIMA (L.) DUM. BY M. A. HAJIBAGHERI, J. L. HALL* AND T. J, FLOWERS School of Biological Sciences, The University of Sussex, Brighton, BNl 9QG {Accepted 21 December 1982) SUMMARY Both cuticle and cell wall of the epidermal cells of leaves of Suaeda maritima showed a considerable increase in thickness (approximately 1-8 times) in plants grown in the presence of 0-34 M sodium chloride when compared with plants grown without added sodium chloride. Differences in the structure of the cuticle were also observed. The rate of transpiration in the dark was markedly reduced with increasing concentrations of salt in the external medium. Cuticular transpiration appears to be related to cuticular thickness and to fall with increasing salinity. INTRODUCTION The cuticle has an important role as a bounding layer between the body of the plant and its environment. It has been ascribed a function in the prevention of the loss of plant components by leaching and as a supplement to the action of stomata in regulating the passage of water from within the plant to the atmosphere. The cuticle lies over and merges into outer walls of epidermal cells. Outside the epidermal cell wall itself a band of more or less pure pectin continuous with that of the anticlinal walls of the epidermal cells is generally believed to lie. Outside this occurs the so-called cutinized layer or cuticular layer, in which cellulose and pectin are encrusted with cutin. The outermost layers of this multilayered wall consist of the cuticle proper (cuticularized layer) made up mainly or entirely of cutin covered with a thin layer of more or less pure wax (Roelofsen, 1952; Esau, 1953; Sitte and Rennier, 1963; Crips, 1965; Martin and Juniper, 1970). There have been several reports on the structure of the cuticle (but none on halophytes) as revealed by transmission electron microscopy showing a fine lamellation of the cuticle proper (Chafe and Wardrop, 1973; Sargent, 1976; Wattendorf and Holloway, 1980). There is, however, very little experimental evidence concerning the effects of salinity on the characteristics of the cuticle of halophytes and the related physiological consequences of exposure to salinity. In view of this fact, the present paper reports on the structure of the cuticle and on cuticular transpiration in the leaves of the halophyte Suaeda maritima (L.) Dum. grown either in the presence or absence of sodium chloride. M A T E R I A L S AND M E T H O D S Seeds of S. maritima (L.) Dum. were grown as previously described (Flowers, 1972) in the presence ('salt' plants) or absence ('non-salt' plants) of 0-34 M sodium chloride added to the culture solution. * Present address: Department of Biology, Building 44, The University of Southampton, SO9 5NH, UK X/83/ $03.00/0 ^ ^^83 The New Phytologist
2 126 M. A, H A J I B A G H E R I ef a/. Transmission electron microscopy Mature leaves of salt and non-salt plants (56 days old) were used for electron microscopy. Small pieces (3 to 5 mm) of tissue were cut from the middle portion of leaves and fixed in 5 % glutaraldehyde for 2 5 h followed by 1 % OSO4 overnight (both in 50 mm sodium cacodylate/acetate buffer, ph 7). After dehydration through a graded ethanol series (20 min each in 25, 50, 75, 90 and 2x100% ethanol, two 20 min changes in propylene oxide), the tissue was embedded in TAAB resin (TAAB Labs Reading, UK). Thin sections (90 to 150nm) were post-stained with uranyl acetate lead citrate. The tissues were examined with a Jeol loos electron microscope at 60 kv. Estimation of the cuticle and epidermal cell wall thickness Electron micrographs (magnification, x 20000) of the adaxial surface of the cuticle and epidermal cell wall in cross-sectional view were magnified 18-7 times using a photographic enlarger to project the image onto a wall (total magnification, X ). Measurements of the thickness of the cuticle and epidermal cell wall were then made at their thinnest point. Scanning electron microscopy Fresh mature leaves were examined by a modification of the method of Baker and HoUoway (1971). Specimens (4 to 8 mm) were mounted on aluminium stubs with double-sided adhesive tape (care being taken to avoid damage to the cuticle) and coated with gold in a S,150 sputter coater. They were examined with a Jeol JMS35c scanning electron microscope at 25 kv. Cuticular transpiration The rate of cuticular transpiration was measured using 56-day-old plants grown individually in small pots of sand. Each pot was enclosed in a second pot half-filled with culture solution and weighed each hour during an 8 h dark period. For each treatment, six replicates of uniform plants were used. Transpiration rates were expressed on the basis of leaf area, which was estimated assuming the leaf of S. maritima to be a half cylinder (Siadat-Pour, 1978). The mean diameters of different leaves with given lengths were determined using contact prints of the leaves from plants grown at various salinities. RESULTS Electron micrographs of the epidermal region of S. maritima showed a multilayered cuticle for plants grown both with and without sodium chloride (Plate 1). The cuticle of S. maritima leaves from plants grown both in the presence and absence of sodium chloride was made up of a thin lamellated cuticle proper (cuticularized layer) and a thick cutinized layer with the difference that the cutinized layer for plants grown under saline conditions was thicker (Plate lc, D). Outside the epidermal wall was a pectic layer which showed no apparent variation with changes in salinity. The thickness of the whole cuticle was significantly greater (1-6 times) in plants grown with sodium chloride than in plants grown without sodium chloride (Table 1 and Plate la, B). The epidermal wall thickness also increased by some 1-8 times when the plants were grown with sodium chloride. There was a significant difference (1-8 times) in the combined thickness of cuticle
3 Cuticular structure in Suaeda maritima 127 Table 1. The effect of sodium chloride in the culture solution on cuticle and epidermal wall thickness in S. maritima Added sodium chloride (M) Thickness of cuticle (jim) Thickness of epidermal wall (/tm) Total of cuticle and epidermal thickness (jim) Cuticle:epidermal wall 0174 ± ± ± ± ± ± The values represent the average of 25 replicates for each treatment ±s.d. Each replicate consisted of a single section from a separate plant. Table 2. Mean values of the rate of cuticular transpiration of S. maritima during an 8-h dark period Cuticular transpiration rate (mg H2O h~^ cmt^) Socium chloride (M) 3-7 ± ± ± ±0-05 Culture solution Plants were grown in culture solution containing various concentrations of sodium chloride. Mean±s.d. and epidermal wall of plants grown in the presence and absence of sodium chloride (Table 1). However, the relative thickness of the two layers remained largely unaffected by the presence of sodium chloride (Table 1). The wax surface of the leaf The appearance of the cuticular surface was found to differ considerably between plants grown in the presence or absence of sodium chloride. Scanning electron micrographs (Plate 2) showed that the wax plates appeared generally thicker, wider and more upright after growth with sodium chloride in comparison with plants grown in culture solution alone. The stomata in plants grown with sodium chloride were at a lower density (a result of increased leaf volume) than in plants grown without sodium chloride and were distributed at random over the whole leaf surface for plants from both growth conditions (Plate 2A, B). Cuticular transpiration The rate of cuticular transpiration of S. maritima, expressed per unit leaf area, was reduced with increasing salt concentration in the external medium (Table 2). The cuticular transpiration was significantly less (35 % reduction) in plants grown with 0-34 M sodium chloride compared to those grown in culture solution alone. DISCUSSION Uphof (1941) noted that the epidermis of xero-succulents and coastal halophytes is characterized by a thick cuticle and a cover of waxy layers. The present paper a ANP 94
4 M. A. HAJIBAGHERI et al. 128 CU B CW CP Plate 1. A, B: Electron micrographs of the outer epidermal wall of a 5. maritima leaf from a plant grown with (A) sodium chloride and (B) without sodium chloride, cw. Cell wall; cu, cuticle. X C, D: electronmicrographsof sections through the adaxial surface of leaves of S. maritima for plants grown in the presence (C) and absence (D) of sodium chloride, illustrating an outer lamellate layer (cp, cuticle proper) with a thick cutinized layer (cl): cw, cell wall; P, pectin layer. X
5 Cuticular structure in Suaeda maritima 129 Plate 2. Scanning electron micrographs of the adaxial surface of a leaf of S. maritima grown with (A) and without (B) salt at a magnification of x 160 and with (C) and without (D) salt at a magnification of x
6 I3O M. A. H A J I B A G H E R I gf a/. indicates that salinity has a marked eflfect on the thickness of both the cuticle and epidermal cell wall of S. maritima leaf cells. The thickness of both the cuticle and epidermal wall was nearly doubled for plants grown with sodium chloride in the culture solution compared with plants grown without sodium chloride. A similar increase to that reported herein has been noted in another halophyte, Atriplex patula, by Longstreth and Nobel (1979). Epidermal wall thickness observed by light microscopy increased 1-62 times on addition of 0*1 M sodium chloride to the external medium. However, St. Omer and Schlesinger (1980) found increases in the thickness of the leaf and stem cuticle were not significant in Jaumea carnosa (by light microscopy) under conditions of increasing salinity (from 0 to 150 mm sodium chloride). Ahmad and Wainwright (1976) reported that the surface of mature leaves of Agrostis stolonifera from different habitats varied according to the exposure to saline spray. In peanut (Arachis hypogaea) grown in normal and salinized soils, salt treatment induced accumulation of wax with reduced cuticular transpiration (Rao, Basha and Rao, 1981). The results presented here on the cuticular transpiration are consistent with these findings. For S. maritima there is a clear correlation between the decrease in the rate of transpiration in the dark and an increase in the thickness of the cuticle. However, Kamp (1930) claimed that the thickness of the cuticle and cuticular transpiration are not closely correlated and Merida, Schonherr and Schmidt (1981) using developing and mature leaves of Clivia miniata suggested cuticular resistance to transpiration is independent of the thickness of the cuticle. However, according to Fitter and Hay (1981), the rate of cuticular transpiration in plants depends upon the thickness, continuity and composition of the cuticle. Furthermore Hall (1966) found that removal of wax from apple fruits by any method caused an increase in transpiration rate. Our observations on AS. maritima leaves were consistent with the latter finding and showed that the effect of increasing salinity on cuticle thickness (1*6 times) was very close to that for the reduction in cuticular transpiration (1-5 times). A significant increase (1'6 times) in cuticular resistance may play a part in decreasing transpiration rates, a phenomenon frequently observed under saline conditions (Delf, 1912; Schratz, 1934; Uphof, 1940; Ashby and Beadle, 1957; Waisel, 1972; Kleinkopf, Wallace and Hartosock, 1976; Shalhevet et al., 1976; Siadat-Pour, 1978), and a decreased flux of water through the plant would significantly mitigate against excessive ion transport to the shoot. ACKNOWLEDGEMENTS We would like to acknowledge the help of Ali Siadat-Pour in determining the rates of transpiration and the University of Sussex for financial assistance to Mohammad Ali Hajibagheri. REFERENCES I. & WAINWRIGHT, S. J. (1976). Ecotype differences in leaf surface properties of Agrostis stolonifera from salt marsh, spray zone and inland habitats. New Phytologist, 76, ASHBY, W. C. & BEADLE, N. C. W. (1957). Studies in halophytes. Salinity factors in the growth of Australian salt bushes. Ecology, 38, BAKER, E. A. & HOLLOWAY, P. J. (1971). Scanning electron microscopy of waxes on plant surfaces. Micron, 2, 364. CHAFE, S. C. & WARDROP, A. P. (1973). Fine structural observations in the epidermis: II. The cuticle. Planta, 109, 3 9 ^ 8. CRIPS, C. C. (1965). The bipolymer cutin. Ph.D. Thesis, University of California. AHMAD,
7 Cuticular structure in Suaeda maritima 131 DELF, E. M. (1912). Transpiration in succulent plants. Annals of Botany, 26, ESAU, K. (1953). Plant Anatomy. John Wiley, New York, London and Sydney. FITTER, A. H. & HAY, R. K. M. (1981). Environmental Physiology of Plants. Academic Press, London. FLOWERS, T. J. (1972). Salt tolerance in Suaeda maritima (L.) Dum. The effect of sodium chloride on growth respiration and soluble enzymes in a comparative study with Pisum sativum h. Journal of Experimental Botany, 22, HALL, D. M. (1966). A study of the surface wax deposits on apple fruit. Australian Journal of Biological Sciences, 19, KAMP, H. (1930). Untersuchungen uber Kutikularbau and kutikulare Transpiration von B\a\Xtm.Jarhrbucher fur Wissenschaftliche Botanik, 72, KLEINKOPF, G. E., WALLACE, A. & HARTOSOCK, T. L. (1976). Salt tolerant potential source of leaf protein. Plant Science Letters, 7, LONGSTRETH, D. J. & NoBEL, P. S. (1979). Salinity effects on leaf anatomy. Plant Physiology, 63, MARTIN, J. T. & JUNIPER, B. E. (1970). The Cuticle of Plants. Edward Arnold, London. MERIDA, T., SCHONHERR, J. & SCHMIDT, H. W. (1981). Fine structure of plant cuticles in relation to waterpermeability: the fine structure of the cuticle of Clivia miniata Reg. leaves. Planta, 152, RAO, G. C, BASHA, S. K. M. & RAO, G. R. (1981). Effect of sodium chloride salinity on amount and composition of epicuticular wax and cuticular transpiration rate in peanut Arachis hypogaea Indian Journal of Experimental Biology, 19, ROELOFSEN, P. A. (1952). On the submicroscopic structures of cuticular cell walls. Acta botanica Neerlandica, 1, SARGENT, C. (1976). The occurrence of a secondary cuticle in Libertia eleganus (Iridaceae). Annals of Botany, 40, ScHRATZ, E. (1934). Beitrage zur biologie der halophyten. I. Zur keimungsphysiologie. Jahrbikher fur wissenschaftliche Botanik, 80, SHALHEVET, J.. MASS, E. V., HOFFMAN, G. J. and OGATA, G. (1976). Salinity and the hydraulic conductance of roots. Physiologia Plantarum, 38, SiADAT-PouR, A. (1978). Physiological Studies on Suaeda maritima. Ph.D. Thesis, University of Sussex. SITTE, P. & RENNIER, R. (1963). Untersuchungen an cuticularen Zellwandschichten. Planta, 60, ST. OMER, L. & SCHLESINGER, W. H. (1980). Field and greenhouse investigations of the effect of increasing salt stress on the anatomy oijaumea carnosa a salt marsh species. Americanjournal Botany,dl, UPHOF, J. CT. (1941). Halophytes. Botanical Review, 7, WAISEL, Y. (1972). Biology of Halophytes. Academic Press, London. WATTENDORF, F. & HOLLOWAY, P. J. (1980). Studies on the ultrastructure and histochemistry of plant cuticle. Annals of Botany, 46,
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