AOBPreview originally published online on September 4, 2002
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Annals of Botany 90: 489-493, 2002
© 2002 Annals of Botany Company
Epifluorescent and Histochemical Aspects of Shoot Anatomy of Typha latifolia L., Typha angustifolia L. and Typha glauca Godr.
1 Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT 06269, USA and 2 Department of Biology, State University of New York at Oswego, Oswego, NY 13126, USA
* For correspondence. E-mail Hilary.McManus{at}uconn.edu
Received: 6 February 2002; Returned for revision: 13 May 2002; Accepted: 26 June 2002 Published electronically: 4 September 2002
ABSTRACT
Using epifluorescent and histochemical techniques, we examined anatomical differences in the shoot organs of Typha latifolia, T. angustifolia and T. glauca. The leaf lamina of T. latifolia and T. glauca had enlarged epidermal cells and a thickened cuticle above the subepidermal vascular bundles; that of T. angustifolia lacked these characteristics. Leaf sheaths were similar among the species and all lacked the epidermal thickenings found in the lamina. The fertile stems had typical scattered vascular bundles with a band of fibres that was most prominent in T. glauca. The sterile stems were only 1 cm in length and contained a multiseriate hypodermis and a uniseriate endodermis over part of their length. The rhizomes were similar except for a pronounced band of fibres surrounding the central core in T. angustifolia. The rhizome was also characterized by an outer cortical region with a large multiseriate hypodermis/exodermis and a uniseriate endodermis with Casparian bands, suberin lamellae and secondarily thickened walls.
Key words: Typha, anatomy, leaf, stems, rhizomes, epidermis, endodermis, hypodermis, cattail.
INTRODUCTION
Typha spp. are highly productive aquatic plants that grow in a variety of habitats throughout wetlands worldwide. They are able to occupy pond and lake margins, fresh and brackish marshes, ditches and reservoirs contaminated with industrial wastes (Sharitz et al., 1980). The three species that occur in central New York State are Typha latifolia L., T. angustifolia L. and T. glauca Godr. All three species can occur in the same stand, but are segregated according to water depth (Marsh, 1962; Grace and Wetzel, 1981). Typha latifolia, a broadleaf cattail with thick and spreading rhizomes, is restricted to shallow waters; T. angustifolia is a narrow-leaf cattail with more slender and creeping rhizomes and grows in the same type of habitats as T. latifolia, but can withstand deeper waters (Marsh, 1962; Harms and Ledingham, 1986; Thieret and Luken, 1996). Typha glauca is the hybrid of T. latifolia x T. angustifolia (Marsh, 1962; Kuehn and White, 1999; Kuehn et al., 1999) and occurs wherever T. latifolia and T. angustifolia are found in the same stand, but can also withstand deeper waters than T. latifolia and is more resistant to strong winds than both its putative parental species (Marsh, 1962; Thieret and Luken, 1996). Generally, the three species can be distinguished according to their differing habitats and morphological differences (Smith, 1961; Marsh, 1962; Thieret and Luken, 1996). Although Smith (1961) listed 15 morphological characters distinguishing T. latifolia, T. angustifolia and T. glauca, no important anatomical differences were noted. As reported here, we have found differences among these Typha species in selected anatomical traits in the shoots; these traits may assist in explaining the habitat differences in the three species and the dominance of T. glauca in wetlands throughout northeastern North America. Our findings also form the basis of new areas of study in the genus Typha.
MATERIALS AND METHODS
Specimens, consisting of rhizomes, fertile stalks, leaf sheaths and leaves of Typha latifolia L., T. angustifolia L. and T. glauca Godr. were harvested from clonal communities in New York state from 1997 to 1999, and placed in cold storage at 4 °C. Specimens of T. latifolia were collected from a small wetland 400 m from the east end of Old State Rd at New York State Highway 104A in Cayuga County, those of T. angustifolia from a roadside ditch at the intersection of New York State Highway 104 and New York State Highway 3 in Hannibal in Oswego County, and those of T. glauca from Broadway Road marsh in Wayne County. Within each location some of the harvested rhizomes had been immersed in water.
For each species, organs of 24–36 plants were examined and the procedures of Seago et al. (1999) were followed. Free-hand sections were obtained by razor blade and stained for suberin lamellae with Sudan red 7B, for lignin with phloroglucinol–HCl, for pectins, lignins and tannins with toluidine blue O, for polysaccharides with iodine potassium iodide–sulfuric acid and for cutin with Sudan IV. These specimens were viewed under brightfield on a Nikon Labophot microscope. Sections were also stained for suberin with fluorol yellow, for suberin, lignin and callose with 0·05 % berberine hemisulfate counter-stained with aniline blue or toluidine blue O, or left unstained and viewed under ultraviolet light on a Zeiss Axiophot epifluorescence microscope with an excitation filter UV-G 365 nm, chromatic beam splitter FT 395 nm and barrier filter 425 nm. Acid digestion of the rhizomes was also used to examine the endodermis and hypodermis for Casparian bands. Images of all specimens were recorded on Kodak Ektachrome 200 or Kodacolor 200. Internegatives were taken to produce colour or black and white prints.
RESULTS
Leaves
We compared selected features of leaves of the three species of Typha (Fig. 1A–H). The leaf lamina margin of T. latifolia is oblong, often curved in shape and contains a zone of fibres at the margin with one vascular bundle embedded within the proximal curved zone of fibres (Fig. 1A). Along the abaxial and adaxial margins of the leaf the subepidermal vascular bundles are interspersed with fibre bundles in the chlorophyllous mesophyll (Fig. 1D). The epidermal cells located above each vascular/fibre bundle are enlarged and thickly cutinized (Fig. 1A and D); these give the surface of the leaf a ridged or ribbed effect.
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The lamina margin of T. angustifolia is wedge-shaped, has a thick zone of fibres at the margin and contains one to four vascular bundles embedded at the proximal edge of the zone (Fig. 1B). The subepidermal vascular bundles along the abaxial and adaxial margins of the leaf are interspersed with fibre bundles in the chlorophyllous mesophyll (Fig. 1E). The epidermis located above the vascular bundles lacks enlarged epidermal cells and extra thickened cuticle resulting in the surface being smooth to the touch (Fig. 1B and E).
Typha glauca has a lamina margin that is narrowly wedge-shaped and contains a small zone of fibres at the margin. This zone of fibres contains one or two vascular bundles at the proximal edge (Fig. 1C). Along the abaxial and adaxial margins of the leaf the subepidermal vascular bundles are interspersed with fibre bundles and smaller vascular bundles in the chlorophyllous mesophyll that are more numerous than in the other two species (Fig. 1C, F and G). The mesophyll with large vascular bundles resembles an I-beam construction connecting the adaxial and abaxial surfaces (Fig. 1C; also see Marsh, 1955). The epidermal cells located above each vascular/fibre bundle are enlarged and thickly cutinized resulting in a ridged or ribbed surface (Fig. 1C, F and G).
The leaf sheaths of all three species do not contain enlarged epidermal cells, thickened cuticle or mesophyll with chloroplasts (Fig. 1H).
Erect stems
Sections of 1–2 m fertile stems (Fig. 1I–O) were taken approx. 0·5 m below the inflorescences. The stems of all three species consist of an epidermis with a narrow hypodermis external to vascular bundles and fibre bundles (Fig. 1I–K). Large vascular bundles are located throughout the stem and a band of fibres is oriented concentrically around the stalk between the second and third rings of vascular bundles (Fig. 1I–K). The band of fibres is interrupted by vascular bundles and parenchyma. The fibre band in T. glauca is generally thicker than that in the other two species (Fig. 1K). Sections of fertile stems taken at approx. 5 mm above the base contain a multiseriate hypodermis, with three to five layers of thick-walled cells (Fig. 1N and O), which is lacking in sections taken further up the stem (Fig. 1I–K). There is no endodermis located in the base of the fertile stems (Fig. 1N and O).
The entire length of the sterile stems generally did not exceed 10 mm, and sections of sterile stems were taken approx. 5–8 mm above the base. These stems contain a multiseriate (four to five cell layers) hypodermis (Fig. 1L) and a uniseriate endodermis (Fig. 1M) that disappears close to the stem tip.
Rhizomes
The rhizomes of the three species are similar and consist of a uniseriate epidermis, an outer cortical region and a central core (Fig. 2A). The cortical region consists of a multiseriate hypodermis (Fig. 2B), aerenchymatous cortex with scattered, small bundles and a uniseriate endodermis (Fig. 2A). The hypodermis of all three species has two distinct zones that contain suberin and lignin (Fig. 2B). There is evidence of Casparian bands (Fig. 2C) and suberin lamellae (Fig. 2D) throughout the hypodermis, making this an ‘exodermis’. All cells of the hypodermis have secondarily lignified walls (Fig. 2E).
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Vascular bundles are only found in the hypodermis in the vicinity of leaf bases (Fig. 2A, C and F). At the position where leaf bases are attached to the rhizome, the inner zone of the hypodermis is continuous with the whole hypodermis of the rhizome adjacent to the leaf base (Fig. 2F).
The cortex is aerenchymatous with irregular lacunae and scattered small bundles, some of which are only fibrous and others of which are vascularized (Fig. 2A and B). The cortical region is delimited on its inside by a uniseriate endodermis which contains Casparian bands (Fig. 2G), suberin lamellae (Fig. 2H) and secondarily thickened walls (Fig. 2I). The outer edge of the central core of T. angustifolia is characterized by a prominent band of fibres (Fig. 2J), which is less conspicuous in T. latifolia (Fig. 2I) and T. glauca (Fig. 2G).
DISCUSSION
Definitive anatomical characteristics were found primarily in the leaf lamina of T. latifolia, T. angustifolia and T. glauca. The lack of thickened cuticle and enlarged epidermal cells outside vascular and fibre bundles in T. angustifolia clearly distinguishes it from T. latifolia and T. glauca. Such anatomical differences were not observed by Saccardo (1895), Smith (1961) and Marsh (1962). Indeed, Smith (1961) claimed that there were no definitive anatomical differences in the leaves of these three species. However, there was a depiction of these traits in one illustration in Meyer (1933, Fig. 3 in that paper) but not in another (Fig. 6 in Meyer, 1933) for T. angustifolia. Our findings suggest that some of Meyer’s (1933) specimens may have been the hybrid T. glauca. Our observations, including the pattern of fibre bundles and marginal fibrous zones, show that the two species and the hybrid can be distinguished anatomically.
Typha leaves gain rigidity from the subepidermal vascular and fibre bundles for support in severe weather (Teale, 1949; Marsh, 1955; Rowlatt and Morshead, 1992). In addition to the general form of the leaves, diaphragms and I-beams (Teale, 1949; Marsh, 1955; Rowlatt and Morshead, 1992), the anatomical characteristics we have described (ribbing and margins) provide added strength to reduce the stresses of some wind-induced bending and twisting. The exaggerated characteristics of T. glauca may enable it to withstand harsher weather conditions with less leaf and stem breakage than its parental species. This is important because these leaves provide the air conduits for the buds, rhizomes and their roots, which are present as plants emerge from winter (Seago et al., 1999).
The fact that the leaf sheaths of the three species do not differ and do not have the epidermal and cuticular traits of the lamina suggests that the transition from sheath to lamina has interesting developmental phenomena that need to be examined.
The anatomical characteristics of the fertile stalks of the three species are similar except for the more prominent concentric, interrupted band of fibres typically found in T. glauca. This may contribute to its more pronounced ability to withstand adverse winter conditions of snow, ice and wind, especially in deeper water marshes (Marsh, 1962).
The sterile stalks of the three species did not differ. The interesting feature of these stalks is that they contain a hypodermis and endodermis that cease apically over the short length of the sterile stem. The question of the presence of complex cortical hypodermis/exodermis and endodermis in the rhizome and sterile stem and their absence in the fertile stem needs to be studied.
The rhizomes of all three species are basically similar except for the characteristic band of fibres located outside the largest vascular bundles of the central core in T. angustifolia. This band of fibres could possibly enhance the strength of the cortex. The presence of an endodermis in wetland plants such as Typha may not be unusual (Clarkson and Robards, 1975; Mauseth, 1988). While hypodermis has been illustrated in rhizomes and hypodermal Casparian bands have been demonstrated in Typha (Perumalla et al., 1990), the exodermal nature of the hypodermis has not been adequately demonstrated. Interestingly, these rhizomes are very similar to Typha roots with a multiseriate exodermis and uniseriate endodermis, each with Casparian bands, suberin lamellae and secondarily thickened walls bordering an aerenchymatous cortical region (see Seago et al., 1999). The thick, lignified hypodermal zones of the roots (Seago et al., 1999) and rhizomes (present study) of Typha plants may contribute to their ability to form the durable mats characteristic of Typha marshes (Marsh, 1962).
Considering these selected anatomical traits, the structural characters of the leaf and fertile stalk of T. glauca may allow it to withstand deeper waters and harsher weather conditions than T. angustifolia and T. latifolia. These characteristics may contribute to its ability to dominate wetlands throughout eastern North America, especially deep-water wetlands. While our findings show that T. glauca has some elaborated traits of each of its parents (Marsh, 1962; Kuehn and White, 1999; Kuehn et al., 1999), its combination of traits distinguishes it from T. latifolia and T. angustifolia.
ACKNOWLEDGEMENTS
We express our appreciation to Carol A. Peterson and Daryl E. Enstone for the use of their facilities and Zeiss Epifluorescence microscope and also Stephane L. Marty for his assistance with the plates. We would also like to thank two anonymous reviewers for their suggestions and careful revisions. This study was done by H. A. McManus as partial fulfillment of an undergraduate independent study at the State University of New York at Oswego.
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