xylem of early angiosperms : nuphar

American Journal of Botany 96(1): 207–215. 2009.
XYLEM OF EARLY ANGIOSPERMS:
NUPHAR (NYMPHAEACEAE) HAS NOVEL TRACHEID
MICROSTRUCTURE1
Sherwin Carlquist,2,4 Edward L. Schneider,2 and C. Barre Hellquist3
2Santa
Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, California 93105 USA; and 3Biology Department,
Massachusetts College of Liberal Arts, North Adams, Massachusetts 01220 USA
SEM studies of xylem of stems of Nuphar reveal a novel feature, not previously reported for any angiosperm. Pit membranes
of tracheid end walls are composed of coarse fibrils, densest on the distal (outside surface, facing the pit of an adjacent cell) surface
of the pit membrane of a tracheid, thinner, and disposed at various levels on the lumen side of a pit membrane. The fibrils tend to
be randomly oriented on the distal face of the pit membrane; the innermost fibrils facing the lumen take the form of longitudinally
oriented strands. Where most abundantly present, the fibrils tend to be disposed in a spongiform, three-dimensional pattern. Pores
that interconnect tracheids are present within the fibrillar meshwork. Pit membranes on lateral walls of stem tracheids bear variously diminished versions of this pattern. Pits of root tracheids are unlike those of stems in that the lumen side of pit membranes
bears a reticulum revealed on the outer surface of the tracheid after most of the thickness of a pit membrane is shaved away by the
sectioning process. No fibrillar texturing is visible on the root tracheid pits when they are viewed from the inside of a tracheid.
Tracheid end walls of roots do contain pores of various sizes in pit membranes. These root and stem patterns were seen in six species representing the two sections of Nuphar, plus one intersectional hybrid, as well as in one collection of Nymphaea, included
for purposes of comparison. Differences between root and stem tracheids with respect to microstructure are consistent in all species studied. Microstructural patterns reported here for stem tracheid pits of Nymphaeaceae are not like those of Chloranthaceae,
Illiciaceae, or other basal angiosperms. They are not referable to any of the patterns reported for early vascular plants. The adaptational nature of the pit membrane structure in these tracheids is not apparent; microstructure of pit membranes in basal angiosperms is more diverse than thought prior to study with SEM.
Key words: basal angiosperms; fibrils; Nuphar; Nymphaeaceae; microstructure; pit membranes; tracheids; xylem.
Nuphar is a genus of great potential interest due to its phylogenetic position in angiosperms. Nuphar is sister to all other
genera of Nymphaeaceae (Les et al., 1999). In turn, Nymphaeales, comprising Cabombaceae, Nymphaeaceae, and Hydatellaceae (Saarela et al., 2007), is sister to all angiosperms except
Amborellaceae based on DNA data (Soltis et al., 2000)
Amborella was found to be vesselless by Bailey and Swamy
(1948). Results based on SEM studies confirm the exclusive
presence of tracheids in the wood (Carlquist and Schneider,
2001). End walls of Amborella tracheids have pit membranes
intact, but with small circular porosities larger than plasmodesmata (Carlquist and Schneider, 2001). Similar results were obtained in Bubbia (Carlquist, 1983) and Tetracentron (Carlquist,
1988). Porose pit membranes were reported in end walls of tracheids in Nuphar and other Nymphaeaceae (Schneider et al.,
1995). All the above taxa qualify as vesselless on the basis of
SEM study. The pores in end walls of those tracheids represent
some tendency toward vessel-like structure, but in physiological
terms, pit membranes, although porose, are relatively intact, and
thus one should term them tracheids. Similar considerations apply to the xylem of most ferns (Carlquist and Schneider, 2007).
The distinction between tracheids and vessel elements does
blur in secondary xylem of Chloranthaceae and Illiciaceae, however. End walls of presumptive vessel elements retain extensive
pit membrane remnants in the four genera of Chloranthaceae:
Ascarina (Carlquist, 1990), Chloranthus (Carlquist, 1992a),
Hedyosmum (Carlquist, 1992b), and Sarcandra (Carlquist,
1
Manuscript received 17 January 2008; revision accepted 21 May 2008.
4
Author for correspondence (e-mail: [email protected])
1987). Various degrees of pit membrane presence also occur
in end walls of vessel elements of Illicium (Carlquist and
Schneider, 2002). In the genera of these two families, pit membrane remnants may be intact in end walls of some otherwise
vessel-like tracheary elements, while other vessel elements retain extensive flakes, webs, or porose sheets of primary wall material, and yet others vessel elements have few pit membrane
remnants in end walls. Primary xylem and earlier-formed secondary xylem in Chloranthaceae and Illiciaceae show greater
degrees of retention of pit membranes in end walls of tracheary
elements. Thus, Swamy and Bailey (1950) reported Sarcandra
to be vesselless. Had they examined material with a greater accumulation of secondary xylem, they might have found vessels.
The aforementioned genera of angiosperms represent expressions intermediate between what are tracheids and vessel elements as generally defined. The textbook definitions of these
cell types do not take into account such intermediacy, because
the terminology is still structured on the basis of light microscopy. Woods of a number of woody angiosperms have vessels
that characteristically retain pit membrane remnants in perforations of cells can readily be termed vessel elements (Carlquist,
1992c; Carlquist and Schneider, 2004). Thus, with the instances
mentioned, one can demonstrate a zone of intermediacy between tracheids and vessel elements, illustrating “non-missing
links” that one would, in fact, expect to find in angiosperms that
possess a preponderance of primitive character states.
The phylogenetic interest of Nuphar and the availability of
excellent living materials of the majority of species of the genus
have induced us to re-examine Nuphar xylem with SEM. Our
earlier work was performed with an SEM of limited resolution
capacity. In addition, new technical procedures for specimen
preparation (Carlquist and Schneider, 2007) offer more reliable
doi:10.3732/ajb.0800348
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American Journal of Botany
results than hitherto available for showing the nature of pit
membranes in tracheary elements and thus for examining xylem evolution in early angiosperms. One might expect that microstructure of xylem of Nuphar would represent ancestral
conditions for angiosperm xylem. However, xylem structure
evolves sensitively with respect to ecology and habit (Carlquist,
1975). Nuphar’s phylogenetic position does not guarantee that
the xylem of Nuphar is an archive of primitive features. We
must be prepared to realize that each group among primitive
angiosperms has its own patterns, and its survival to the present
has included stories of divergence, rather than retention of ancestral conditions.
MATERIALS AND METHODS
The following collections form the basis for the current study. We follow
the taxonomic system of Padgett (2007).
Nuphar section Astyla Padgett: N. advena (Ait.) Ait. subsp. advena—Freshwater tidal area of Hudson River, north of Rodgers Island, Greenport, Columbia
Co., New York, USA. 3 September 2001, C. B. Hellquist 16722 (GH). N. advena subsp. advena—Backwater on west side of Sideling Hill Creek at Varner
Gap, Route 454, 7 miles WSW of Burke Valley, Fulton Co., Pennsylvania,
USA. 21 June 1987. Hellquist 17082 (GH). N. advena subsp. ozarkana (G. S.
Mill. and Standl.) Padgett—Cultivated on W side of West Road, Adams, Berkshire Co., Massachusetts, USA from material collected by Donald Padgett.
Hellquist 17083 (MASS). N. polysepala Engelm.—Cultivated at Santa Barbara
Botanic Garden from material cultivated at Black Lake, Nipomo Mesa, along
Highway 1, Santa Barbara Co., California, , USA (SBBG). N. variegata Engelm. ex Durand: Cultivated on W side of West Road, Adams, Berkshire Co.,
Massachusetts. Hellquist 17084 (MASS).
Nuphar section Nuphar: N. japonica DC.—Cultivated on W side of West
Road, Adams, Berkshire Co., Massachusetts, USA. Hellquist 17085 (MASS).
N. microphylla (Pers.) Fernald—In Rice Lac (Lac-du-Bois), south side of Route
313, east of Lac du Bonnet, 50°17′N, 95°41′W, Manitoba, Canada. 28 July
1996, C. B. Hellquist & J. Wiersema 16159 (GH). N. pumila (Timm) DC.—
Small pond on Mount Sinjuha, Siberia, Russia. August 1963, Crow et al 93–
369 (NHA).
Hybrid: N. ×rubrodisca Morong (= N. microphylla × N. variegata). Cultivated on W side of West Road, Adams, Berkshire Co., Massachusetts, USA
from material collected in Vermont, USA. Hellquist 17086 (MASS).
Nymphaea: N. cv ‘Marliac Carnea’—Cultivated at Lotusland Foundation,
Montecito, Santa Barbara Co., California, USA. (Living collections accession
number 1992–417).
All materials were available in fresh condition from cultivated specimens.
Portions of roots and stems were preserved in 50% aqueous ethanol. Sections
were cut by hand with a single-edged razor blade, washed with three changes of
distilled water, placed between clean glass slides with pressure sufficient to
produce flatness, and dried on a warming table at 50°C. Portions of the dried
sections that appeared to contain xylem in longisection were placed onto electroconductive pads on aluminum stubs, sputter-coated with gold, and examined
with a Hitachi S2600N SEM. The sections averaged between 1–2 mm thickness, and thus were sufficiently thick so that handling was unlikely to result in
excessive breakage of xylem cells. Such breakage can occur in thin sections,
such as paraffin sections when they are prepared for study with light microscopy. Hand sections made with a single-edged razor blade show views of the
inside surfaces of tracheids as well outside surfaces; various layers of a primary
wall can be seen in portions of outer surfaces that are shaved away. The methods employed here are essentially the same as those in recent studies of ferns
(Carlquist and Schneider, 2007) and are similar to those of Sano (2005). To
observe whether pit membranes of Nuphar stems were lignified, we examined
sections cut by hand and stained with safranin-fast green by means of light
microscopy.
The term stem here is considered equivalent to rhizome. All observations
refer to metaxylem tracheids unless otherwise specified. The term fibril is used
for strands of wall material shown in pit membranes because these structures
are much thicker in diameter than the microfibils that have been demonstrated
in cell walls by means of transmission electron microscopy. The term porosity
and the adjective porose are used to describe holes in the primary walls (pit
membranes) of tracheid end walls.
RESULTS
Roots—End walls of N. advena subsp. ozarkana root tracheids
have porose pit membranes. The photograph of end wall pits
(Fig. 1) reveals that the pit membranes are thin, with pores of
various sizes. No membrane portions are shaved away in this
view: such action would show in the surfaces of the secondary
wall. Lateral walls of N. advena subsp. ozarkana (Fig. 2) have
smooth membranes, as seen from the inside of a tracheid.
The tracheid pits of N. polysepala (Fig. 3) are clearly porose.
The pit membranes, seen from an outer surface of a tracheid,
may have experienced some removal of an adjacent wall, but the
reticulate appearance is valid for at least that wall layer. The
same is true for N. japonica (Fig. 4), in which portions of the pit
membranes near lateral ends of pits (upper right) are less porose,
suggesting the reticulate layer is paired with a nonporose layer.
In Nymphaea, similar conditions are evident. Both of the
views shown here (Figs. 5, 6) are from outer surfaces of root
tracheids, and both are probably lateral walls. The occurrence of
a nonporose wall portion (Fig. 5, left) suggests that the porose
portion of the wall represents shaving away of a wall layer. A
similar appearance is evident in Fig. 6. The nonporose pit membrane at right may represent a parenchyma–tracheid interface.
Stems— The pits in end walls of stem tracheids of Nuphar
differ markedly from those of roots. This is shown dramatically by the views of N. advena subsp. advena (Hellquist
17802). From the inside of the tracheid, one can see, closest to
the lumen, major thick strands of coarse fibrils that run in an
axial direction in the tracheid (Fig. 7). These fibrils have thickness on a different order of magnitude from those seen in primary cell walls with transmission electron microscopy. Exterior
to the major strands is a network is a three-dimensional network
of strands, penetrated by holes that apparently extend through
to an adjacent tracheid. These features are confirmed when one
views end-wall pit membranes from the outer surface of the
tracheid (Fig. 8). In this pit membrane, the dense spongiform
nature of the pit membrane is evident. Note that the primary
wall between pit membranes (Fig. 8, top and bottom), portions
underlying secondary wall strips and therefore between pit
membranes, are homogeneous and do not have any meshwork.
The section shown in Fig. 9 illustrates the outer surface of a
tracheid, shaved away by sectioning more at right than at left.
Not surprisingly, the longitudinal strands are exposed where
more has been shaved away, whereas pit membrane portions at
left have (at low magnification) a meshwork much like that
seen in the membrane in Fig. 8.
A view of the inner tracheid surface of a stem of N. advena
subsp. ozarkana (Fig. 10) illustrates several pits with longitudinal strands nearer to the lumen, with a dense perforated meshwork (darker gray) farther back toward the outside of the cell.
Narrow pits with slanting longitudinal strands probably are related to the sinuous contour of some tracheids in stems, as opposed to the very straight ones seen in roots. This same condition
is illustrated for the stem tracheid pit membranes shown for N.
advena subsp. advena, Hellquist 16722 (Fig. 11). The longitudinal strands in Fig. 11 are notably coarse and may group together. Other pit portions of tracheids from the same collection
(Fig. 12) have a meshworklike structure, but with fewer longitudinal strands.
Diminution of longitudinal strands in a pit membrane is
shown in stem tracheids of N. variegata (Fig. 13). This pit
membrane is probably a lateral wall pit. Correlatively with less-
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Carlquist et al.—Early angiosperm xylem
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Figs. 1–6. SEM micrographs of pits of tracheary elements of roots. 1. Nuphar advena subsp. ozarkana, porose end wall pits, viewed from inside of
tracheid. 2. N. advena subsp. ozarkana, nonporose lateral wall pits, viewed from inside of tracheid. 3. N. polysepala, end wall of tracheid, viewed from
outer surface of tracheid. 4. N. japonica, end wall pits, viewed from outside of tracheid. 5. Nymphaea ‘Marliac carnea,’ end wall pits, viewed from outside
of tracheid. 6. Nymphaea ‘Marliac carnea,’ lateral wall tracheid to parenchyma pits; wall of facing cell has been removed by sectioning from pits at left.
Bars = 5 µm.
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Figs. 7–12. Views of pits from stem tracheids of Nuphar advena. Figs. 7–9. N. advena subsp. advena, Hellquist 17082. 7. Portions of pits from end
wall, seen from inside of tracheid; coarse longitudinal strands traverse the pit aperture. 8. Portion of pit from end wall, seen from outside of tracheid;
coarse fibrils disposed in spongiform manner. 9. Pits from end wall, seen from outside of tracheid; spongiform portion of pit membrane mostly sectioned
away (fragments, at left), showing some longitudinal strands. 10. N. advena subsp. ozarkana, narrow pits as seen from inside of tracheid. Figs. 11–12. N.
advena subsp. advena, views of pits from inside tracheids. 11. View showing thick nature and grouping of coarse fibrils. 12. Area lacking longitudinally
oriented strands (probably pit facing parenchyma cell), showing random nature of fibril meshwork with some porosities at left. Bars: Figs. 7–11, 5 µm;
Fig. 12, 2 µm.
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Carlquist et al.—Early angiosperm xylem
ening of longitudinal strands, there are no porosities evident in
this membrane, which thus appears to be a pit membrane interconnecting a tracheid with a parenchyma cell. An end wall tracheid pit of N. variegata (Fig. 14), seen from the inside of the
tracheid, has an abundance of longitudinal strands, which merge
with the porose, denser portion (darker gray) farther away from
the cell lumen. The portion shown in Fig. 14 illustrates that the
longitudinal strands are not in a layer separate from the background meshwork, but merge with it.
Similar features are illustrated by the stem tracheids of N.
polysepala. The narrow pits in Fig. 15 dramatically illustrate
the three-dimensional nature of the coarse fibrils in the pit; rendering these photographically is difficult, in fact, because distal
portions of the meshwork are recessed so far behind the longitudinal strands. Longitudinal strands and porosities can even be
seen in protoxylem tracheids of N. polysepala (Fig. 16). The
presence of the strands in protoxylem might not be expected
because of the elongation one often sees in protoxylem tracheids. Such elongation, which often fractures the primary wall
into fragments, may not occur because the stems of Nuphar
polysepala are very thick and elongate so little during growth.
A section of the outer surface of a tracheid (Fig. 17) reveals the
result of sectioning. The three-dimensionality of the pit membranes is evident because the meshwork strands have been cut
by the sectioning process; the cut ends point upward. Note that
no meshwork is present on the primary wall portions that underlie strips of secondary wall (one portion of secondary wall
left, at upper right). A portion of a pit membrane at a higher
magnification (Fig. 18) shows a clearly spongiform structure.
The sections, made by hand, and stained with safranin and fast
green, did not demonstrate to us any lignification in the pit
membranes of N. polycephala stem tracheids. However, our
preparations were not ideal, and our observations of this material are tentative.
Stem tracheids in Nuphar section Nuphar have a wide range
of structure. The end-wall pit membranes of N. japonica (Fig. 19)
show patchiness in distribution of porosities. These pit membranes also show a relative paucity of longitudinal fibril strands.
Pit membranes of N. japonica when seen from the outer surface
of a tracheid (Fig. 20) have some strands of moderate prominence on a compact meshwork background in which porosities
can be seen. In N. microphylla, pit membranes on end walls of
tracheids as seen from the inside of the cell have inconspicuous
longitudinal strands superimposed on a flat meshwork, much as
in N. japonica. The lateral walls of N. microphylla stem tracheids have a reticulate structure (Fig. 21) facing the solid, untextured wall of an adjacent parenchyma cell.
Stem tracheids of N. pumila have prominent longitudinal
strands on the inner surfaces of pit membranes of end walls
(Fig. 22). When part of a pit membrane is sliced away by sectioning (Fig. 23), the nature of the coarse fibrils is revealed. At
the top of Fig. 23, the secondary wall is intact; the secondary
wall at the bottom of the pit has been removed by sectioning.
Related to this, many of the fibrils are cut in the lower half of
the photograph. Although there may have been some displacement of the fibrils as a result of the sectioning, the three-dimensional nature of the meshwork is clearly evident throughout the
photograph. Pores that interconnect the adjacent tracheids are
evident in the pit membrane.
The stem tracheids of Nymphaea have essentially the same
microstructural features as in Nuphar. Examination of an
end wall pit membrane as seen from the inside of a tracheid
(Fig. 24) shows that longitudinally oriented fibrils are pre-
211
dominate, but they do not occur at a level different from that
of the randomly oriented fibrils with which they are intermixed. Porosities are clearly evident in the meshwork. A
view of the outside of a Nymphaea stem tracheid end wall
(Fig. 25) shows a reticulate network. The reticulum probably
represents only a portion of a pit membrane between two
adjacent tracheids. A denser aggregation of fibrils, as in Fig.
24, would be expected if the entirety of a pit membrane were
present. A wall layer has evidently been sectioned away in
this preparation.
DISCUSSION
The root tracheids of Nuphar and Nymphaea are much like
those figured in earlier studies (Schneider et al., 1995) and resemble closely the vessel-like tracheids figured for Brasenia of
the Cabombaceae (Schneider and Carlquist, 1996a). On end
walls of the root tracheids of Nuphar and Nymphaea, nontextured pit membranes containing prominent porosities are present.
The relatively large size of the porosities suggests that root xylem in Cabombaceae and Nymphaeaceae has attained a close
approach to vessel element characteristics. In woody, vesselbearing angiosperms, presence of imperforate tracheary elements allows use of criteria other than end wall characteristics:
vessel elements are wider and longer than the tracheid they accompany and often have different lateral wall pitting. Nymphaeaceae, like monocotyledons, do not have division of labor into
vessel elements plus imperforate tracheary elements, and thus
only the criterion of end-wall structure is available when categorizing these elements as tracheids or vessel elements. The
highly porose pit membranes in these two families indicate that
absence of a pit membrane over most of a perforation is a criterion of vesselhood very nearly achieved. However, end-wall pit
membranes of metaxylem root tracheids in Cabombaceae and
Nymphaeaceae seem not to be swept away by the conductive
stream and/or hydrolyzed away. The removal of most or all of
pit membranes in end walls of tracheary elements by these natural processes would seem to be a criterion by which to designate vessel elements. However, implementation of that criterion
requires use of SEM and thus may be resisted by those in search
of easy definitions.
The stem tracheary elements of Nuphar have end-wall pit
membranes that do contain porosities, but the porosities are
not large enough or abundant enough that one would be
tempted to call these cells vessel elements. The existence of
such porosities in pit membranes of stem tracheid end walls
(but not lateral walls) does suggest a rudimentary step toward acquisition of vessel elements. However, retention of
tracheids as a means of restricting spread of embolisms
within a xylary system is a strategy of some groups (most
ferns, for example), and lack of vessels should not be considered a failure to evolve conductively efficient conductive
cells (Carlquist, 1975).
The pit membranes of end walls in stem tracheids of Nuphar
and Nymphaea are remarkable for their three-dimensional networks of coarse fibrils. Similar appearances have been reported
in stem tracheids of Cabomba (Schneider and Carlquist, 1996b).
The fibrils closer to the interior of a tracheid are sparse, thick,
and longitudinally oriented, whereas those at the outside of the
pit membrane are denser and randomly oriented. The longitudinally oriented fibrils do not seem to be homologous to the longitudinal strands that occur as pit membrane remnants in vessel
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Figs. 13–18. Pits from stem tracheids of Nuphar. Figs. 13–14. N. variegata, pits seen from inside of tracheids. 13. Tracheid to parenchyma pits; fibrillar strands are slender and sparse. 14. Tracheid end wall pits; longitudinally oriented fibrillar strands predominate, fading into more random fibrillar meshwork. Figs. 15–18. N. polysepala. 15. View from inside of tracheid, showing marked three-dimensional disposition of longitudinally oriented strands in end
wall. 16. Portion of inner surface of protoxylem tracheid, with long axis oriented horizontally, showing strands and porosities on wall surface. 17. View
from outside of tracheid, showing tracheid-to-tracheid pits; secondary wall mostly sectioned away (one fragment, at upper right), revealing three-dimensional nature of pit membrane (ends of reticules broken by sectioning pale gray). 18. Pit membranes of tracheid-to-tracheid pits at higher magnification,
showing spongiform appearance. Scales: Figs. 13, 14, 5 µm; Figs. 15–18, 2 µm.
January 2009]
Carlquist et al.—Early angiosperm xylem
213
Figs. 19–25. Pits from stem tracheids of Nuphar (19–23) and Nymphaea (24–25). Figs. 19, 20. Nuphar japonica. 19. View from inside of tracheid,
tracheid-to-tracheid pits, showing relative sparsity of coarse fibril strands. 20. View from outside of tracheid; some coarser fibrils appear on surface of
otherwise uniform (but porose) pit membranes. 21. N. microphylla: tracheid to parenchyma interface, wall shaved away above, revealing porose nature of
membrane on tracheid side. Figs. 22, 23. N. pumila, views of inner surfaces of end wall pits. 22. Appearance typical of end wall pits, with longitudinally
oriented strands superimposed on porose meshwork pit membrane. 23. Secondary wall and portion of pit shaved away (lower half of photograph), allowing
broken fibril ends to separate from three-dimensional meshwork of pit membrane. Figs. 24–25. Nymphaea ‘Marliac carnea,’ views of tracheid end walls.
24. Coarse fibrils form porose meshwork on a pit membrane seen from inside of tracheid. 25. View from outer surface of tracheid: highly porose reticulate
appearance may reflect removal of wall layer by sectioning process. Scales: Figs. 19–24, 2 µm; Fig. 25, 5 µm.
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Table 1.
American Journal of Botany
[Vol. 96
Comparison of tracheary element wall microstructures in Nymphaeaceae and woody angiosperms.
Nymphaeaceae: Stem tracheids inner surface remnants of perforation plates
Woody angiosperms: Pit membrane microstructure
In primary xylem tracheids
On all tracheid walls
Composed of coarse fibrils
Two-layered wall in pits: reticulate outer plus axial strands inside
Reticulate layer spongiform with pores
Axially oriented strands superimposed on the reticulate layer
In secondary xylem vessel elements
In perforation plates of vessels only
Composed of thin fibrils
One-layered wall
Laminar with pores or, if fibrils sparser, variously network-like
Axially oriented strands remnants of the reticulate layer after hydrolysis of the
primary wall
elements of Illicium (Carlquist and Schneider, 2002), various
Chloranthaceae (Carlquist, 1987, 1990, 1992a, b) or other genera
(Carlquist, 1992c). The differences are summarized in Table 1.
The S-, G-, and P-type pits of tracheids in earlier vascular plants
(Hartman and Banks, 1980; Kenrick and Crane, 1997; Friedman and Cook, 2000) clearly differ from what one sees in
Nuphar stems.
The distinction in structure between the stem tracheids of
Nuphar and Nymphaea and those of the root is puzzling. The
roots of Nuphar are adventitious, so that the conductive characteristics of the two organs, although coordinated, might show
some differences. However, that consideration would apply to
monocotyledons, in which differences of degree in pit membrane remnant presence may be found with respect to organography (Carlquist and Schneider, 2006). No difference in
microstructure of tracheary elements with respect to organography is as yet evident in monocotyledons, however, even in
aquatic genera such as Acorus (Carlquist and Schneider, 1997).
The root tracheids of Nymphaeaceae have microstructure typical
of that found in monocotyledons as well as in dicotyledons. The
stem tracheids of Nuphar and Nymphaea show a change in that
basic pattern, an elaboration. At present, that change can be considered an autapomorphy developed within Nymphaeaceae. The
systematic distribution of the stem tracheid peculiarities within
Nymphaeaceae (and variations of them) is not yet available, and
we hope that further studies in progress will clarify the occurrence of the features we have described. Also needed are definitive studies of whether any lignification is present in the complex
pit membranes of Nuphar and Nymphaea stem tracheids.
The physiological significance of the stem tracheids of
Nuphar and Nymphaea may clarify as our knowledge of the systematic distribution of the Nuphar-type stem tracheids, or variants of them, develops. At the very least, the occurrence of the
patterns described here for Nuphar shows that diversity of tracheary elements in basal angiosperms is more diverse than previously thought and that studies of microstructure with SEM are
highly desirable to demonstrate the variations present. The microstructure of stem tracheids in Nuphar illustrates the point that
additional information about the anatomical structure of early
angiosperms may not provide unifying features that simplify
analysis of phylogeny. Rather, over the lengthy times available
to these groups for evolution of structures suited to ecology and
habit, distinctive features have evolved. This is the situation that
confronts us in the stem tracheid microstructure of Nuphar.
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