AOBPreview originally published online on September 12, 2005
Annals of Botany 2005 96(6):1109-1119; doi:10.1093/aob/mci262
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Anatomical Features and Ultrastructure of Deschampsia antarctica (Poaceae) Leaves from Different Growing Habitats
WANOWSKA1,2,*
1 Department of Plant Physiology and Biotechnology, University of Warmia and Mazury, Oczapowskiego 1A, 10-719 Olsztyn, Poland, 2 Department of Antarctic Biology, Polish Academy of Sciences, Ustrzycka 10/12, 02-141 Warsaw, Poland and 3 Department of Plant Anatomy and Cytology, Maria-Curie Sk
odowska University, Akademicka 19, 20-033 Lublin, Poland
* For correspondence. E-mail i.gielwanowska{at}uwm.edu.pl
Received: 29 October 2004 Returned for revision: 21 January 2005 Accepted: 27 July 2005 Published electronically: 12 September 2005
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ABSTRACT |
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• Background and Aims The leaf anatomy and ultrastructure of Deschampsia antarctica (Poaceae) plants growing in three different habitats (a dry site in the Antarctic tundra, a wet site in a zone exposed to sea spray and a greenhouse) were investigated. The ultrastructure of the leaves of D. antarctica has not been studied before.
• Methods Semi-thin sections of the D. antarctica leaves were stained with toluidine blue and viewed using a light microscope. Ultra-thin sections stained with uranyl acetate and lead citrate were examined using a transmission electron microscope.
• Key Results Plants growing in the Antarctic tundra and in a greenhouse had stronger xerophytic features than those growing at the seashore. The stress response of D. antarctica plants growing in the wet environment, exposed to high salinity and flooding, included: irregular mesophyll cells, large intercellular spaces in the parenchymatic layer, bulliform epidermal cells and vascular bundles surrounded with deformed outer and inner bundle sheaths of leaves. The highest number of sclerenchymatic fibres is characteristic of the leaves of plants growing in a greenhouse, whereas the smallest was of plants growing in a wet habitat. Stress conditions can disturb the formation of sclerenchymatic fibres. In plants growing in the Maritime Antarctic the chloroplasts of the mesophyll cells of leaves are of an irregular shape, with pockets or invaginations inside the organelles and outgrowths. Both of them make the surfaces of chloroplasts larger, and result in an increase in the amount of substances exchanged between the chloroplasts and cytoplasm or the other organelles. The leaf mesophyll cells of D. antarctica plants growing in Antarctica contain atypical structures including numerous vesicles of different sizes and concentrically arranged membranes.
• Conclusions The anatomical and ultrastructural features of the leaf and their changes under stress conditions are considered in relation to the adaptations of D. antarctica to the climate conditions in the Maritime Antarctic.
Key words: Deschampsia antarctica, anatomical features, mesophyll cells, ultrastructure, stress condition, Poaceae, Antarctica, phenotypic plasticity, phenotypic response
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INTRODUCTION |
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The Antarctic is one of the most severe natural habitats in the world, especially for plants. Specific environmental conditions have restricted the number of native angiosperm species to only two—Colobanthus quitensis (Caryophyllaceae) and Deschampsia antarctica (Poaceae). Deschampsia antarctica, Antarctic hairgrass (family Poaceae), is the only natural grass species growing in the Antarctic geobotanical zone, widespread all over the Maritime Antarctic (Longton, 1988
; Barcikowski et al., 1999). This wintergreen plant grows mainly in the vicinity of penguin colonies and the gathering places of large mammals, where it usually forms extensive closed swards in larger or smaller clusters (Allen and Heal, 1970; Leonardi et al., 1987; Barcikowski et al., 1999; Lewis Smith, 2003). Due to its relatively wide ecological range, D. antarctica has been the object of studies in many fields of biology: ecology, taxonomy, morphology, anatomy, reproduction, physiology, biochemistry and molecular biology (Greene, 1970; Moore, 1970; Corner, 1971; Greene and Holtom, 1971; Edwards, 1972, 1974, 1975; Jellings et al., 1983; Edwards and Lewis Smith, 1988; Zúñiga et al., 1994, 1996; Convey, 1996; Barcikowski et al., 1999; Day et al., 1999; Romero et al., 1999; Bravo et al., 2001; Bystrzejewska, 2001; Nkongolo et al., 2001; Alberdi et al., 2002; Zwolska and Rakusa-Suszczewski, 2002; Lewis Smith, 2003; Chwedorzewska et al., 2004; Giewanowska and Szczuka, 2005). This special interest in so many biological disciplines is stimulated by the atypical, severe climatic conditions of the Antarctic region where D. antarctica occurs (Edwards and Lewis Smith, 1988; Casaretto et al., 1994; Zúñiga et al., 1996; Romero et al., 1999). The harsh climatic conditions in Antarctica should induce various mechanisms responsible for plant development and survival. On the other hand, there is no convincing evidence that the species in question has developed unique metabolic adaptation and survival strategies, differing from other cold- or frost-tolerant plants (Lewis Smith, 2003). Nevertheless, this Antarctic species seems to be physiologically and biochemically well adapted to various, rapidly changing growth conditions and the effects of various abiotic factors such as high and low radiation, deficient precipitation and drought, flooding, salinity, variable (sometimes extremely low) temperatures accompanied by frost, frozen ground, snow- and ice-cover (Zúñiga et al., 1996; Barcikowski et al., 1999; Day et al., 1999; Bravo et al., 2001; Bystrzejewska, 2001; Nkongolo et al., 2001; Alberdi et al., 2002; Zwolska and Rakusa-Suszczewski, 2002; Lewis Smith, 2003; Chwedorzewska et al., 2004).
Pratt and Lewis Smith (1982) and Falkengren-Grerup et al. (1995) reported certain seasonal trends in the chemical composition of Antarctic plants. The authors focused on the biochemical adaptation of these plants to severe ambient conditions with extremely low temperatures. The unusually high accumulation of sucrose and fructans mainly at the end of the Antarctic summer is considered one of the protective mechanisms against low temperature in D. antarctica (Zúñiga et al., 1996). Two different strategies to resist low temperatures were determined in both the Antarctic angiosperms by Montiel and Cowan (1993) and Bravo et al. (2001). The reactions to this abiotic stress coincide with the amount of soluble carbohydrates, starch and proline. The growth and reproduction of Antarctic vascular plants under stress conditions are considered with respect to abiotic factors such as desiccation and high UV-B radiation (Day et al., 1999; Ruhland and Day, 2000; Rozema et al., 2001, 2002; Van de Staaij et al., 2002). Given its significance, the influence of abiotic factors on photosynthesis has also been thoroughly investigated (Tieszen et al., 1981; Edwards and Lewis Smith, 1988; Körner and Larcher, 1988; Larcher, 1995; Day et al., 1999; Montiel et al., 1999; Xiong et al., 1999; Bravo et al., 2001; Bystrzejewska, 2001; Lewis Smith, 2001; Alberdi et al., 2002).
The anatomy and morphology of both Antarctic angiosperms, i.e. Colobanthus quitensis and Deschampsia antarctica, have been studied recently. Using light and scanning electron microscopes, Romero et al. (1999) described a strong variation in the anatomical characteristics of the leaf surface and cross-section between D. antarctica plants growing in natural conditions and their laboratory clones. Detailed studies of the leaf micromorphology in the Antarctic pearlwort were carried out by Mantovani and Vieira (2000) as was a preliminary investigation of the morphology and anatomy of D. antarctica – by Barcikowski et al. (2001).
The ultrastructural features of mesophyll cell organelles are considered in relation to the phenotypic plasticity of D. antarctica to the climatic conditions in the Maritime Antarctic (Giewanowska and Szczuka, 2005). This paper fouses on the differences in the leaf anatomical structure of D. antarctica growing in different habitats and influenced by abiotic factors.
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MATERIALS AND METHODS |
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Plant material
Plants of Deschampsia antarctica Desv. growing in natural conditions were collected in the vicinity of the Polish H. Arctowski Antarctic Station (62°09·41'S, 58°28·10'W), on King George Island (the South Shetland Islands), during the Antarctic summer (mainly in January 2002). Two different habitats were chosen: the dry site was located in a flat area of the Antarctic tundra, approx. 300 m from the seashore and outside influence of any present penguin colony or resting places of sea mammals; the wet site was about 30 m from the seashore, in the vicinity of a penguin colony and resting places of sea animals, thus enriched with nutrients, and subjected to sea spray and flooding. Ten D. antarctica plants were collected from both types of microhabitats: five from the dry, exposed inland site and five from the wet, nutrient-rich maritime site. The plants were collected with a small amount of native soil and placed in plastic containers during their transportation to Poland, where they were potted in fertile, horticultural soil and grown in a greenhouse in the garden of the Department of Plant Physiology and Biotechnology of the University of Warmia and Mazury in Olsztyn.
Light and electron microscopy
Whole plants of D. antarctica were collected in the field and immediately taken from the greenhouse into the laboratory for fixation. The time between the plants being collected and the fixation procedure started was approx. 10–15 min. In the laboratory, fully developed leaves (2nd or 3rd leaf) were selected, from which fragments 2–3 mm in length were sectioned for fixation in 3·5 % glutaraldehyde in 0·1 M phosphate buffer (pH 7·0) for 10 h at room temperature. After a short rinse with 0·1 M phosphate buffer (two exchanges), the plant material was post-fixed overnight in 2·5 % osmium tetroxide. The fixed tissue was then washed in buffer, dehydrated in a graded ethanol series, transferred to mixtures with increasing ratios of Poly Bed 812 resin, and finally embedded in pure Poly Bed 812 resin. Both semi-thin and ultra-thin sections were prepared on a Reichert (Ultracut-R) microtome. Semi-thin sections (1–2 µm) were stained with toluidine blue and viewed with a light microscope. Ultra-thin sections cut with a diamond knife were stained on grids with uranyl acetate and lead citrate, and examined in a JEOL Jem 100S transmission electron microscope. Nine or ten fragments of different leaves were employed in the study of the ultrastructure for each of the growth conditions.
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RESULTS |
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The plants growing on exposed elevations are only 2–3 cm in height (Fig. 1A). During the growing season the innovation in the caespitose clump develops two or three short, folded xeromorphic leaves, almost completely hidden in the leaf sheath (Figs 1B, C and 2A). The epidermis covering the leaves has thicker walls on the abaxial side, and thinner walls and numerous stomata on the adaxial side. Under the abaxial epidermis, in each rib, there is a small group (two or three cells) of sclerenchymatic fibres; there are no such fibres under the adaxial epidermis. The leaf mesophyll of D. antarctica is not differentiated into palisade and spongy mesophyll. Its cells are of a regular shape and similar size. The leaves of such plants usually have three ribs with single, centrally arranged vascular bundles. Each bundle is surrounded by a layer of parenchymatic cells with chloroplasts (parenchymatic sheath) and a layer of sclerenchymatic cells (mestome sheath). The bundles are collateral; their structure is typical of grasses, yet with poorly differentiated xylem and few tracheal elements (Figs 1C and 2A).
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The external appearance of plants growing in wet, fertile sites, in the vicinity of sea animals, 30–40 m from the shoreline, is different. They are 6–7 cm in height; their leaves (five to eight) with flat blades having three to seven ribs, remain green for a long time (Fig. 1D, E). The leaves of these plants are two to three times longer and broader compared with those found in dry, nutrient-deficient habitats. They also contain more groups of sclerenchymatic fibres (five to seven) under the abaxial epidermis and well-developed bulliform cells on the adaxial side (Figs 1E, F and 2B). Mesophyll is composed of cells of various shapes, more regular under the epidermis, elongated and irregular near the bundle. The parenchymatic sheath cells are also irregular, and the walls of mestome sheath cells are rather thin (Fig. 1E, F). A well-developed phloem and xylem (with distinguishable proto- and metaxylem) are visible in the vascular bundle (Fig. 1F). There are large intercellular spaces between the irregular cells, and the parenchyma looks like aerenchyma. Two-year-old D. antarctica plants brought from the Antarctic, grown in a greenhouse at 16–18 °C, developed enormous leaves, 22 cm in length (Fig. 1G), with big groups (12–14) of sclerenchymatic fibres under the abaxial epidermis (Fig. 1H), and with small streaks of sclerenchyma under the adaxial epidermis. However, no bulliform cells were found in the adaxial epidermis. The vascular bundle was well developed in each rib. Worth noticing are, moreover, metaxylem vessels with considerable lumens, present also in the marginal parts of the leaf. A big air tube is present in the protoxylem. Regular cells and large intercellular spaces occur in the mesophyll. Thick cell walls (outside tangential and radial) and thick cuticle in the abaxial epidermis should be also noted. The plants grown at 16–18 °C did not form inflorescences, although they were stimulated by vernalization.
The ultrastructural analyses of the mesophyll of all morphological types of D. antarctica plants show accumulations of osmophilic, granular and fibrous material of varying density in intercellular spaces (Fig. 2E, arrowheads). The deformations more common in the mesophyll cell plastids and mitochondria of the plants growing in the wet habitat differ from those occurring in the plants originating from dry sites. Their chloroplast shows numerous regular, small concavities (Fig. 3A) and larger, irregular (Fig. 3B) or thin, long protrusions (Fig. 3C). Considerable differences between mitochondria can also be observed: some of them are regular, spherical or oval, whereas the surface of others is irregular, with smaller or bigger concavities (Fig. 3B, C, E). They differ in structure and density. In some of them the matrix is dense and granular (Fig. 3B, D), whereas in others it is much looser (Fig. 3E).
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Smaller and bigger vesicles, and concentrically arranged membranes are visible in the loose cytoplasm (Fig. 4A). There are also areas with dense cytoplasm. In the dense cytoplasm, near big groups of ribosomes, mitochondria and chloroplasts, there are droplets, vesicles and multi-vesicular bodies of various sizes (Fig. 4A–C). Some vesicles with brighter, loose contents can be also seen.
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In plants growing in the greenhouse the chloroplasts and mitochondria are visible side by side (Fig. 5A, B). The chloroplasts shows small, regular concavities with different material (Fig. 5C, D, E). Considerable differences between ball-shaped material can also be observed: some of them are electron light, whereas the content of others is osmophilic and electron dense (Fig. 5F). Smaller and bigger parts of material are visible in the cytoplasm, near the cell wall (Fig. 5G, H).
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DISCUSSION |
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Deschampsia antarctica plants growing in three different sites, i.e. a dry site in the Antarctic tundra, a wet site in an area exposed to sea spray and in a greenhouse, showed clear differences in size (Table 1). Moreover, the leaf blades of D. antarctica from the Antarctic tundra were strongly folded and V-shaped, in comparison with those of the other plants. The V-shaped folded leaf blades of D. antarctica are natural and comparable with those of other graminaceous species (Körner and Larcher, 1988
; Romero et al., 1999). The results obtained indicate similarity between leaves of plants from the Antarctic tundra, and high mountain and polar tundra ecosystems. The function of the V-shaped leaf blades in the Antarctic habitat is extensively discussed by Romero et al. (1999).
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Beside the evident differences in length, width and folding of the leaves, variations in their anatomy dependent on the growing site were observed (Table 1). Partially, the present findings concerning the leaf anatomy of hairgrass, congrent with the observations of other authors, underlined the typical xerophytic leaf features of both angiosperms occurring in the Antarctic—Deschampsia antarctica and Colobanthus quitensis (Jellings et al., 1983
; Martinez et al., 1994; Vieira and Mantovani, 1995; Romero et al., 1999; Mantovani and Vieira, 2000; Lewis Smith, 2003). Based on the present data, it can be presumed that the anatomical features of leaves are strictly connected with their different habitats. Plants growing in dry, nutrient-deficient and wind-exposed sites develop only a few, short, folded leaves with thick-walled cells. There are no bulliform cells and sclerenchymatic fibres in the adaxial epidermis. All the leaves are stiff, hard and have xeromorphic features, such as a small surface of leaf blade and thick-walled epidermis. Additionally, the plants growing in the Antarctic tundra and in the greenhouse have stronger xerophytic features. Beside slighter differentiation, the epidermal cells of these plants are covered with a thicker cuticle, as compared with plants growing near the sea. Several cell sizes and forms in the leaf epidermis of hairgrass plants growing in the Antarctic were observed by Romero et al. (1999). In these plants, the authors also found greater cell density per leaf area, in comparison with those growing in the laboratory. Similar to the present results, the differences in the epidermal structure were particularly prominent in the adaxial side of the leaves. The above xerophytic features are induced mainly by low temperatures and drought stress and occur also in plants from other cold regions (Körner and Larcher, 1988; Consault and Aiken, 1993; Lewis Smith, 2003). The most differentiated, especially on the adaxial surface, were the epidermal cells of plants growing near the sea. On the other hand, water flooding and salinity can induce changes opposite to xerophytic features. In the adaxial epidermis, big thin-walled bulliform cells develop, making the leaf blade unfold. These epidermal cells, storing large quantities of water, play a role in the reaction to the salinity stress (Levitt, 1980; Luttge, 1993). Sclerenchymatic fibres are visible only under the abaxial epidermis. Some of the features, e.g. irregular mesophyll cells, larger intercellular spaces and atypical vascular bundles, are visible in Fig. 1F. Larger intercellular spaces in the mesophyll and bulliform epidermal cells of D. antarctica growing in a wet environment seem to confirm the evident reaction to stress conditions. These conditions disturb the exchanges of gases. It is reported that irregular mesophyll cell shapes may provide an important interface favouring a more intensive CO2 exchange (Nobel and Walker, 1985; Körner and Larcher, 1988; Upadhyaya and Furness, 1994; Romero et al., 1999).
Another anatomical difference observed in the leaves of D. antarctica plants growing in the three habitats examined is the number of sclerenchymatic fibres (Table 1). Unexpectedly, the largest number of them was found in the leaves of plants growing in the greenhouse, and the smallest in the plants growing in the wet environment. Although it is not possible to evaluate the extent it seems that stress conditions can disturb the formation of sclerenchymatic fibres. The present results concerning the number of sclerenchymatic fibres are consistent with those reported by Romero et al. (1999).
The strong influence of stress conditions on the anatomy is visible in the structure of the vascular bundles. The vascular bundles of D. antarctica leaves are surrounded by two bundle sheaths (Mantovani and Vieira, 2000; Alberdi et al., 2002). The outer sheath consists of parenchymatic cells with inconspicuous chloroplasts; the inner—the mestome—is built of smaller cells with thick lignified walls (Romero et al., 1999). Similar to the results obtained by these authors, in the present study the cells of the outer sheath also contained chloroplasts, regardless of the site. The cells of the outer sheath in the leaves of plants growing near the seashore and exposed to high salinity and flooding had the most irregular shapes and were of a different size. Cell deformations were also observed in the mestome layer, in the leaves of plants from this site. One can assume that stress factors disturb the formation of the outer and particularly the inner bundle sheaths. The cell walls of the mestome layer are thickest in the greenhouse plants.
The authors who observed disruption in growth and cell differentiation under the influence of various stress factors emphasized changes of hormonal balance in plant tissue which consist of a reduction in the concentration of growth stimulation hormones and a simultaneous increase of the concentration of ethylene, jasmonic acid and abscysic acid, i.e. the substances that slow down elongation growth, disturb cell wall lignification and accelerate tissue maturation (Levitt, 1980; Wodzicki and Wodzicki, 1980; Pharis et al., 1981; Wodzicki and Zaj
czkowski, 1983; Yamamoto et al., 1987; Nobel, 1999).
In D. antarctica plants growing in the Maritime Antarctic, the chloroplasts of the mesophyll cells are of an irregular shape, with pockets or invaginations inside the organelles (Table 1). Similar chloroplast pockets and small vesicles were described in D. antarctica by Giewanowska and Szczuka (2005). The studies of mesophyll cells in this species show that the vesicles were formed as a result of the splitting of the inner and outer chloroplast membranes, and the pockets are invaginations inside a single organelle. A single chloroplast of a mesophyll cell in a D. antarctica leaf from the wet site can contain numerous invaginations and outgrowths. Undoubtedly, both of them make the surfaces of chloroplasts larger and bring about an increase in the amount of substances exchanged between the chloroplasts and cytoplasm or the other organelles. Additionally, the surface of exchange is increased by the wrinkled chloroplast surface. The surface of exchange, enlarged this way, may be particularly important for plants growing under the severe climatic conditions of the Antarctic. The longest form of the chloroplast insets are similar to the recently described stromuli (Köhler et al., 1997) which are elongated protuberances from petunia or tobacco chloroplasts. Those fast-growing long tubules emanating from chloroplasts are recognized as interorganoid connections rendering the transfer of protein molecules possible. It has been found that mitochondria, vesicles and small vacuoles or peroxisomes adhere very tightly to the chloroplast membranes or even press against them. The tight contact between the cytoplasmic organelles and the special ability of chloroplasts to form atypical structures (invaginations, vesicles, outgrowths) or invaginations in mitochondria are considered to be a way of adapting to the specific climatic conditions of the Antarctic region (Giewanowska and Szczuka, 2005).
Undoubtedly, these conditions contribute to the very fast development of D. antarctica during the Antarctic summer (Edwards, 1974; Lewis Smith, 1994; Convey, 1996; Day et al., 1999; Romero et al., 1999; Lewis Smith, 2003). On the other hand, such phenomena are typical of all plants living in non-Antarctic conditions. The close contact between the cytoplasmic organelles is also described and discussed in literature and well-known in physiology (Köhler et al., 1997; Karp, 2002).
Beyond any doubt, such behaviour of organelles is a striking example of interdependence among different types of organelles (Karp, 2002). Organelles co-operate in different metabolic processes, e.g. oxidative metabolism. In the present observations of cell organelles, the well-developed mitochondrial cristae visible in Fig. 3B, D and E demonstrate considerable intensity of such processes.
The leaf mesophyll cells of D. antarctica plants growing in wet habitats contain atypical structures like numerous vesicles varying in size and concentrically arranged membranes. In the case of frost stress, changes in the plasma membrane are responsible for death or survival.
This study concentrated on the influence of such abiotic factors as temperature, salinity and flooding. Deschampsia antarctica and the other plants growing in the Antarctic area are exposed to various abiotic and biotic factors. Undoubtedly, the anatomical and ultrastructural changes in the leaf structure should be described taking into consideration all these stress factors. The present study provides a good basis for further research.
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ACKNOWLEDGEMENTS |
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We would like to thank Professor Rakusa-Suszczewski, Head of the Department of Antarctic Biology, Polish Academy of Sciences, for the opportunity to participate in research on the vegetation in the Maritime Antarctic, and Doctor Pawe
Loro for inviting us to join the 26th Polar Expedition organized by the Polish Academy of Sciences. This work was partially supported by the Polish Academy of Sciences (grant no. PBZ-KBN-108/P04/2004). |
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