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3 Department of Biology, SUNY, College at Oswego, New York USA 13126; 4 Department of Biology, University of Waterloo, Waterloo, Ontario, Canada N2L 3G1
Received for publication July 6, 1999. Accepted for publication October 26, 1999.
ABSTRACT
Adventitious roots of marsh-grown Pontederia cordata were examined to determine cortical development and structure. The innermost layer of the ground meristem forms the endodermis and aerenchymatous cortex. The outermost layer of the early ground meristem undergoes a precise pattern of oblique and periclinal cell divisions to produce a single or double layer of prohypodermis with an anchor cell for each radial file of aerenchyma cells. At maturity, endodermal cell walls are modified only by narrow Casparian bands. The central regions of the ground meristem become proaerenchyma and exhibit asymmetric cell division and expansion. They produce an aerenchymatous zone with barrel-shaped large cells and irregularly shaped small cells traversing the aerenchyma horizontally along radii; some crystalliferous cells with raphides are present in the aerenchyma. The walls of the hypodermis are modified early by polyphenols. The outermost layer of the hypodermis later matures into an exodermis with Casparian bands that are impermeable to berberine, an apoplastic tracer dye. The nonexodermal layer(s) of the hypodermis has suberin-modified walls. Radial files of aerenchyma are usually connected by narrow protuberances near their midpoints, the aerenchyma lacunae having been produced by expansion of cells along walls lining intercellular spaces. We are terming this type of aerenchyma development, which is neither schizogenous nor lysigenous, "differential expansion."
Key Words: aerenchyma • apoplastic permeability • endodermis • hypodermis • Pontederia cordata • Pontederiaceae • root development
Structural features of the root apical meristem of members of the Pontederiaceae, including Pontederia cordata, were reviewed as long ago as 1887 by Schönland. Roots in members of this family typically have three or four tiers of apical initials: a tier of rootcap initials (or calyptrogen), one or two tiers of ground meristem-protoderm initials (periblem-dermatogen), and a tier of procambium or stelar initials (plerome). This has been confirmed by Charlton (1980)
, although Lee (1958)
argued that a three-tiered meristem with one layer of initials for the ground meristem-protoderm tip was characteristic of the Pontederiaceae, like Eichhornia, and that all other patterns represented nonmedian sections of the apex. In his study of vascular patterns in adventitious roots of P. cordata, Charlton (1980)
described the origin and location of primary and secondary raphide cells in the outer portions of the ground meristem. He also found that a quiescent center extended ~70 µm behind the junction between the rootcap and the ground meristem-protoderm tip.
To date, a comprehensive developmental and structural characterization of the cortex has not been made in any member of the Pontederiaceae. Root cortical structure in some members (Hasman and 
nanç, 1957
; Charlton, 1975, 1980
; Tomlinson, 1982
) has been described, but these studies need to be extended to include relationships among the endodermis, aerenchyma, and hypodermis, and to describe cell wall compositions and cell patterns of cortical regions. Many species, including those in wetlands, are known to possess an exodermis, i.e., a hypodermis with a Casparian band (Perumalla, Peterson, and Enstone, 1990
; Peterson and Perumalla, 1990
).
We are engaged in an extensive study of the cortices of wetland plants that occupy somewhat different habitats within marsh communities to determine whether there are corresponding differences in endodermis, hypodermis, and aerenchyma as suggested by Justin and Armstrong (1987). Earlier studies focused on Typha glauca Godr., T. angustifolia L., and Hydrocharis morsus-ranae L., growing in cattail marshes (Seago, Peterson, and Enstone, 1999a
; Seago et al., 1999b
). The former have mats with extensive adventitious roots in the mat and underlying muck, whereas the latter lies on the surface with free-floating, adventitious roots. The subject of the present study, Pontederia cordata, grows in small to large clusters of plants with emergent leaves and inflorescences. They have rhizomes with many adventitious roots arising from leaf bases and growing in sandy gravel or mud under water. In the present paper, the patterns of origin of the ground meristem, endodermis, aerenchyma, and hypodermis are described for Pontederia cordata and compared to those features of other wetland species.
MATERIALS AND METHODS
Whole plants or roots of Pontederia cordata L. (pickerel weed) were harvested from the Broadway Road marsh, Wolcott, Wayne County, New York, or Black Creek Marsh, Kakat Road, Cayuga County, New York, during June to September of most years in the 1990s. Specimens used to assess apical organization and ground meristem ontogeny were usually fixed in FPA (formalin: propionic acid: ethyl alcohol), processed by standard techniques, embedded in paraplast, sectioned on a rotary microtome, and stained with safranin and fast green (Seago and Marsh, 1989
). Freehand sections of fresh specimens at various positions along adventitious roots were used to examine the state of aerenchyma organization and to test for cell wall features of the endodermis and hypodermis. Histochemical tests for lignin were toluidine blue O and phloroglucinol-HCl (Seago et al., 1999b
); cellulose was also demonstrated by toluidine blue O and IKI-H2SO4. Casparian bands were revealed by staining with berberine and counterstaining with either aniline blue or toluidine blue O, and suberin lamellae were revealed by Fluorol yellow examined under ultraviolet epifluorescence and by Sudan red 7B in brightfield (Seago et al., 1999b
).
The apoplastic permeability of the hypodermis and endodermis was tested with berberine. Six roots were excised at three positions behind the apex (short, 20–50 mm; medium, 50–100 mm; long, 150–200 mm), sealed, and immersed in 0.05% berberine hemisulfate solution and either rinsed and sectioned directly or post-treated with 0.09 mol/L potassium thiocyanate to produce crystals of berberine thiocyanate (Enstone and Peterson, 1992
). The technique for injection of berberine was reported in Seago et al. (1999b)
. The presence of crystals or berberine staining in the walls, viewed under epifluorescence, indicated that they were permeable to this tracer. Control sections were either unstained or fully stained with 0.05% berberine hemisulfate after sectioning.
All epifluorescence work was done on a Zeiss Axiophot epifluorescence microscope with excitation filter UV-G365, chromatic beam splitter FT395, and barrier filter LP420. Brightfield microscopy was done on a Nikon Labophot microscope. The presence of Casparian bands was confirmed by acid digestion treatment, and the specimens were viewed under darkfield microscopy, according to the procedures in Seago et al. (1999b)
. Raphide crystals were demonstrated in permanent slide preparations on a Swift phase contrast microscope by employing the 10x objective lens with the 100 phase substage annulus to achieve a dark field. Microscopic images were recorded on Kodacolor ISO 200, Ektacolor ISO 100, and Ektachrome ISO 200 or 400 films. Then color or black and white internegatives were produced to make color or black and white prints, respectively. Over 200 roots were examined during the course of this study.
RESULTS
The root system of Pontederia cordata is homorhizic; adventitious roots arise from leaf bases on the rhizome. The roots and rhizomes grow in the substrate of mud or sandy gravel under varying depths of water. New roots form from early June to mid-September. For most cell and tissue analyses, three lengths of roots were investigated: short (20–50 mm), mid-length (50–100 mm), and long (150–200 mm).
Organization of the apical meristem
The root apical meristem of adventitious roots is of the closed type, usually with three tiers of initials: rootcap, cortical-epidermal, and stelar initials (Fig. 1A–B). The tip of the ground meristem-protoderm (i.e., the cortical-epidermal initials) is a single tier of two to four cells wide distal to the stelar initials (Fig. 1B). In some roots, there is a one-two-tier organization of cortical-epidermal initials in which there is only one central cell flanked by two cell tiers in median longitudinal section. For some mid-length roots, there are four tiers of apical initials with separate tiers of cortical initials and epidermal initials. All long roots have three tiers of initials with one tier of cortical-epidermal initials, as in Fig. 1B.
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Apoplastic permeability
To determine whether or not root tissues with Casparian bands can limit apoplastic movement, the permeabilities of the endodermis and hypodermis to berberine were tested on material brought into the laboratory from the field. In the absence of tracer, the walls display a blue autofluorescence when irradiated with ultraviolet light (Fig. 4A). When sections are stained directly with berberine hemisulfate, all walls fluoresce yellow (Fig. 4B). Injection of berberine hemisulfate into the aerenchyma results in staining all cells from the outer hypodermal walls to the endodermis (Fig. 4C). This result was confirmed by external application of berberine to whole roots followed by potassium thiocyanate prior to sectioning; the presence of numerous crystals of berberine thiocyanate (Fig. 4D) reveals that the hypodermal and cortical apoplast is permeable to berberine in short- and medium-length roots (up to 150 mm). Proximal to 150 mm from the tip, the inward movement of berberine is blocked at the outer walls of the exodermis (Fig. 4E).
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Structure of the mature central cortex
The mature aerenchyma, in longitudinal section, exhibits complexes of large and small cells in which the ramified small cells (Fig. 6A) form an irregular, radial network traversing the cortex from the boundary with the nonaerenchymatous inner cortex to the anchor cell of the hypodermis. Adjoining radial files are readily apparent in thick, longitudinal sections (Fig. 6A). The large, barrel-shaped cells always remain intact (i.e., noncollapsed), even when crystals have earlier formed in them. The aerenchyma zone also shows enlarged, radially aligned cells with the vertical ends of a few small cells, resulting from the intrusive growth of the small cells, interspersed among the large cells (Figs. 3B–C, 4B–C, 5E–F). The cells exhibit lateral protuberances on each radial side (Figs. 4B–C, 5E), resulting in interrupted lacunae in the aerenchyma. When roots are sectioned, the integrity of the aerenchyma is usually disrupted and the lateral connections between adjacent radial files are not always visible. There are no obvious intercellular spaces or lacunae between the large and small aerenchyma cells within a radial file of cortex in the longitudinal dimension.
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DISCUSSION
Apical meristem and early development of the cortex
The organization of the root apical meristem in Pontederia cordata is generally typical for a monocotyledonous plant. Clowes (1985)
found that the related Eichornia crassipes (Mart.) Solms. had a single tier for the tip of the cortex and epidermis, but Charlton (1980)
illustrated a root meristem of P. cordata with a separate tier for the epidermal initials. As Byrne and Heimsch (1968)
found in species of the dicotyledonous Linum, the number of tiers of initials in the apical meristem can vary. The present study indicates that the region of initials in the apical meristem of Pontederia cordata is also variable in that the epidermis and cortex may arise from a single tier of initials or from two separate tiers.
The developmental patterns within the ground meristem, ultimately leading to a cortex with an endodermis, several layers of thick-walled inner cortex, an aerenchyma of two cell types, and a hypodermis with an exodermis (summarized in Fig. 7), have not been described previously (see Seago and Marsh, 1989
; Sifton, 1945, 1957
; Tomlinson, 1982
; Justin and Armstrong, 1987
). However, the general pattern of a set of periclinal divisions in the outermost file of ground meristem giving rise to a hypodermis with at least two cell layers at most positions outside the aerenchyma (Fig. 7A–B) is consistent with the hypothesis put forth by Seago and Marsh (1989)
for hypodermal origin in wetland plants.
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). A second set of cell divisions in the ground meristem produces the prohypodermis, in which flank cells are formed by oblique divisions and anchor cells by periclinal divisions. Periclinal division in the flank cells produces another layer of cells. The exodermis is derived from flank cells and the outer derivative of the periclinal division, which produces the anchor cell (Fig. 7A–B). The third set of divisions in the ground meristem produces the large and small cells of the proaerenchyma (Fig. 7C–D). Further, localized cell expansion around intercellular spaces leads to lacuna formation. This strongly suggests that different genes may be operative in these cell divisions and, in at least some aspects of differentiation, in the hypodermal and aerenchymatous zones of the cortex (e.g., Koning et al., 1991
; Dietrich, Radke, and Harada, 1992
; Bögre et al., 1999
). Since Dietrich, Radke, and Harada (1992)
have shown a cortex-specific gene acting in roots of a nonwetland plant, Brassica napus, we expect that more genes and gene products specific to the root cortex, especially for cell division controls and cell differentiation, will be discovered.
Structure of the endodermis and exodermis
The mature endodermis in P. cordata has only Casparian bands, or state I walls (see Peterson, 1989
). The occurrence of a mature endodermis in the state I condition without additional wall modifications may not be unusual for roots of wetland plants (Seago, Peterson, and Enstone, unpublished data; Seago, Peterson, and Enstone, 1999a
). Our limited studies on P. cordata and Hydrocharis morsus-ranae (Seago, Peterson, and Enstone, 1999a
), have shown that, when the endodermis matures only to state I (with Casparian bands only), the inner cortex has thickened primary walls. These walls may provide structural support to the inner cortex to compensate for the lack of suberin lamellae and thick secondary walls in the endodermis. In contrast, in Typha angustifolia and T. glauca, the endodermis matures to state III with suberin lamellae and lignified secondary walls as well as Casparian bands, and the root is without thickened inner cortical primary walls (Seago et al., 1999b
). Many more species need to be investigated before definite correlations between root anatomy in this aspect can be achieved.
The structures of the exodermis and its neighboring cells in P. cordata present a strong contrast to the structure of the endodermis. The type of exodermis in P. cordata can best be described as uniseriate and uniform (Kroemer, 1903
); the cells of the exodermis are uniform in length, confirming an earlier report of Shishkoff (1987)
who investigated one unnamed genus in the Pontederiaceae. However, it is part of a complex hypodermis in which the internal layers are nonuniform, consisting of different sizes of cells. Casparian bands occupy about a third of the anticlinal walls in both the endodermis and exodermis. Since exodermal cells are larger than endodermal cells, their Casparian bands are likewise larger. The occurrence of suberin lamellae in addition to Casparian bands in the exodermis is typical for this layer (see Kroemer, 1903
; Peterson and Enstone, 1996
), but the deposition of additional wall materials (state III development) is not so uniform (see Kroemer, 1903
; Peterson and Enstone, 1996
; Seago et al., 1999b
). Further wall development may be related to whether or not suberin lamellae sever the plasmodesmata of the cells, causing mortality before additional wall material is laid down (Fengshan Ma, personal communication). In P. cordata, suberin lamellae appear much earlier than mature Casparian bands. This is unusual according to a survey by Perumalla, Peterson, and Enstone (1990)
and Peterson and Perumalla (1990)
, who found that these developed rather synchronously in many species. However, we previously found in Typha that the appearance of Casparian bands, demonstrated by fluorescent staining methods, was delayed until after the appearance of suberin lamellae for inner layers of the complex exodermis (Seago et al., 1999b
). Despite the unusual sequence of development, the impermeability of the exodermis to the apoplastic dye berberine indicated that its Casparian band was functional. Such distance of maturation of exodermal Casparian bands from the root tip may not be unusual for wetland plants (see Seago et al., 1999b
).
The general temporal correlation between Casparian band and suberin lamella deposition (see Barnabas and Peterson, 1992
; Peterson and Enstone, 1996
; Enstone and Peterson, 1997
) may have a genetic basis. The findings of Held et al. (1993)
that an mRNA for O-methyltransferase, involved in suberin synthesis, accumulates in the developing endodermis and exodermis of Zea mays suggest that the same gene is operative in exodermal wall production when both Casparian bands and suberin lamellae are being deposited.
Details of the chemical composition of Casparian bands, suberin lamellae, and secondary walls have been lacking until Schreiber et al. (Schreiber et al., 1994; Zeier and Schreiber, 1997, 1998
; Zeier et al., 1999
; Schreiber et al., in press
) chemically quantified the amounts of lignin and suberin in endodermal and exodermal cell walls. Since wall modifications are evident long before the wall loses its permeability in the exodermis of P. cordata, it would be instructive to examine the walls of this tissue chemically to determine their composition at different stages of development.
Aerenchyma development
Cortical development in P. cordata roots is highly unusual. The earliest formation of diamond-shaped intercellular spaces, typical for any plant, begins schizogenously within 50 µm of the tip of the ground meristem. Beyond 1 mm behind the root tip, however, apparent asymmetric, transverse cell divisions occur in the outer two-thirds of the proaerenchymatous ground meristem (excluding the inner cortex and prohypodermis). These are followed by longitudinal and then radial cell wall expansions leading to enlargement of air spaces to form lacunae, involving radial, medial-tangential, and longitudinal expansion of the cells (Fig. 7C-D).
Cell wall expansion in the aerenchymatous zone appears to involve only the wall regions lining the diamond-shaped intercellular spaces. There appears to be no or only minimal cell wall expansion at the adjoining walls between adjacent aerenchyma cells along radial walls (Fig. 7D) and at the common tangential walls between aerenchyma cells in a radial file (Fig. 7D) and between outermost aerenchyma cells and anchor cells. The lacunae at the outermost region of aerenchyma enlarge, at least in part, by the production and then tangential expansion of the flanks cells because the outer tangential walls of the outermost aerenchyma cells in each file remain in contact with the anchor cells and not with the flank cells (Fig. 7B). Further, the early lacunar expansion begins after hypodermal wall modifications have begun, but long before exodermal Casparian band maturation with its attendant blockage of apoplastic permeability. The small cells do not represent transverse diaphragms of small cells, as seen in some wetland plant roots (e.g., in Nymphaea sp.; Conard, 1905
), and we did not find collapsed dead cells, even among those with raphides. The cells of the aerenchymatous cortex have been determined to be alive (David J. Longstreth, personal communication).
The longitudinal pattern of large and small cells in the root aerenchyma of P. cordata is unlike anything reported for wetland plant roots, but it superficially resembles a pattern of large, water-storage cells and small, network cells in the central mesophyll of Sansevieria leaves (Koller and Rost, 1988
). However, the cell pattern is observed only in longitudinal section in P. cordata roots where the root aerenchyma cells are alive, and we have no reason to believe that the large cells would function as water storage cells.
Beyond schizogeny
The tangential and radial expansion of growing aerenchyma cells and lacunar expansion are different from anything reported in the literature (cf., e.g., Sifton, 1945, 1957
; Yamasaki, 1952
; Sculthorpe, 1967
; Bristow, 1975
; Smirnoff and Crawford, 1983
; Justin and Armstrong, 1987
; Jackson and Armstrong, 1999
); there is no schizogeny or lysigeny occurring at these stages of root growth that involves lacunar expansion (Fig. 7D). Initially, the expansion of the aerenchymatous lacunae by growth of the longitudinal cell walls between points of attachment, at least in the outer cortex, is undoubtedly correlated with the production and expansion of prohypodermal flank cells between anchor cells. A situation found in roots of Rumex (Laan et al., 1989
) and Nymphaea (Conard, 1905
; Seago, unpublished data), where lacunae in the form of "honeycomb aerenchyma" (Laan et al., 1989
) develop by cell division and expansion following earlier schizogenous intercellular space formation, appears to have some similarities to the situation at the boundary between hypodermis and aerenchyma in Pontederia. In Pontederia, however, the rest of the aerenchyma does not have a "honeycomb" appearance of round or multifaceted lacunae, and obvious cell expansions elongate the lacunae radially, not in a round pattern (see Conard, 1905
). In Rumex (Laan et al., 1989
) and Nymphaea (Conard, 1905
), the lacunae arise near the apex where cells are being produced, whereas in Pontederia the lacunae appear to expand proximal to the sites of endodermal Casparian band maturation, although this still needs to be demonstrated unequivocally.
These types of expansion of cells and lacunae do not readily fit into either the schizogenous or lysigenous categories of Sifton (1945, 1957)
or into the categories of Justin and Armstrong (1987)
. The term, schizogeny, does not adequately describe these situations because no further cell separations occur after intercellular space formation in the early ground meristem, which is a typical intercellular space formation in roots in general. The phenomenon of lacuna formation in Pontederia appears to be one in which there is an expansion of the earlier formed schizogenous intercellular spaces by a specific stretching of the nonconjunctive walls (walls lining the intercellular spaces) of the aerenchyma cells (see Cosgrove, 1996, 1997
). We propose the term "differential expansion" be used to describe this type of aerenchyma development. Our findings show that the development, structure, and function of root aerenchyma need to be investigated far more extensively.
Comparisons with cortical tissues in related species
The aerenchyma of other members of the Pontederiaceae appears to be similar in some respects to that of P. cordata. A transverse section of a root of Eichhornia crassipes in Peterson (1992
; see his Fig. 10) revealed sections of small cells scattered among the large cells and a few lateral protuberances connecting the radially aligned large cells, as found in P. cordata; Hasman and nanç (1957
; see their Fig. 2c) did not report such traits in E. crassipes. The aerenchyma in E. crassipes is less extensive than in P. cordata (cf. Hasman and nanç, 1957
; Peterson, 1992
). Raphides are present in the aerenchymatous zone in both E. crassipes (Hasman and nanç, 1957
) and P. cordata. Hasman and nanç (1957)
could not identify an exodermis or hypodermis, but their drawing shows what may be a uniseriate exodermis as part of a multiseriate hypodermis, somewhat like Pontederia, and there seem to be anchor cells in the innermost layer of a hypodermis. In Peterson's fluorescence image of a root of Eichhornia, there appears to be a multiseriate hypodermis with a uniseriate, but small-celled outermost layer of cells with thick outer tangential walls (see Fig. 10 in Peterson, 1992
). This apparent thickening of the outer hypodermal walls in Eichhornia thus resembles the situation in Pontederia, although the cells are very different in size. The apparent differences in the cortical patterns between these two closely related genera may be related to habitat. Eichhornia is free-floating with unanchored roots, often occurring in dense populations, whereas Pontederia is emergent with roots immersed and anchored in the substrate, occurring in less dense populations.
The relationship between habitat and the pattern of development and structure of the cortex in wetland plants and in nonwetland plants exposed to flooded conditions has been examined by Justin and Armstrong (1987)
, and we are engaged in analyses of root cortices from different habitats within wetland situations (see, e.g., Seago, Peterson, and Enstone 1999a
; Seago et al., 1999b
). It appears that roots anchored in the wet, but firm substrates of muck or sandy gravel have a hypodermis with an exodermis (Casparian bands plus suberin lamellae), often modified by secondarily thickened walls somewhere on their exodermal surfaces, as with Pontederia cordata. This probably allows the outer part of the root to withstand the abrasive effects of the substrate and of infection by phytopathologic organisms, especially when the epidermis is lost, as often occurs in both Pontederia and Typha. However, in Pontederia, the roots appear to play no major role in overwintering as they do in Typha (Seago et al., 1999b
), and this may help to explain the less complex hypodermis in the former.
Previous studies on Typha (Seago et al., 1999b
) and Hydrocharis (Seago, Peterson, and Enstone, 1999a
) and the present work with Pontederia indicate that we are only beginning to understand the development, structure, and function of the cortex in roots of wetland plants. Studies on other wetland species from other taxonomic categories and with slightly different habitat characteristics are continuing.
FOOTNOTES
1 The authors thank Donald Kelly, Rochester, New York, for preparing the drawing; Pearly Kwan, Oswego, New York, for help with the color plates; the Natural Sciences and Engineering Research Council of Canada for a Research Grant to CAP, and two anonymous reviewers for their critical comments and helpful suggestions. JLS expresses his deep appreciation to Marilyn A. Seago for her help and encouragement and to Leland C. Marsh for many helpful discussions on wetlands and wetland plants. 
2 Author for correspondence: (e-mail: seago{at}oswego.edu
).
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