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1 Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, California 93105 USA
Received for publication February 16, 1999. Accepted for publication June 3, 1999.
ABSTRACT
Perforation plates are reported in aerial and subaerial axes of Psilotum nudum and in aerial axes of Tmesipteris obliqua. In Psilotum, both perforations lacking pit membranes and perforations with pit membrane remnants were observed. Perforation plates in Psilotum may consist wholly of one type or the other. In Tmespteris, perforations have threadlike pit membranes or consist of porose pit membranes. Wide perforations alternating with narrow pits, a conformation observed in various ferns, were observed in Psilotum (subaerial axes). In Psilotum, perforations are more common in metaxylem than in protoxylem; perforations in protoxylem consist of primary wall areas containing small circular porosities or relatively large circular to oval perforations. There are no modifications in the secondary wall framework of protoxylem or metaxylem in Psilotum or Tmesipteris that would permit one to distinguish presence of perforations or perforation plates with light microscopy, and scanning electron microscopy (SEM) is required for demonstration of porose walls or perforations. The tracheary elements of the Psilotaceae studied have no features not also observed in other ferns with SEM.
Key Words: perforation plates • pit membranes • Psilotaceae • Psilotum • Tmesipteris • tracheary elements • vessel elements • xylem
Although long regarded as representatives of a group not closely related to other extant groups of vascular plants, Psilotaceae have been considered related to ferns by some authors on the basis of morphology and anatomy (e.g., Bierhorst, 1977
), but other authors find that morphology and anatomy do not support a filicinean position for Psilotaceae (Kaplan, 1977
; Wagner, 1977
). Gensel (1977)
argues for a nonfilicinean position of Psilotaceae on the basis of paleobotanical studies. More recently, analyses of DNA evidence have found weak to moderately close associations between Psilotaceae and Ophioglossaceae (Manhart, 1995
; Pryer, Smith, and Skog, 1995
), but in Manhart's (1995)
cladogram, Ophioglossaceae and Psilotaceae are in a clade removed from other families commonly regarded as constituting Filicineae. In this latter construction, therefore, ferns are polyphyletic. Regardless of the precise nature of affinities between Psilotaceae and ferns, comparison between tracheary elements of Psilotaceae and those of ferns is desirable. "Ferns" in the present paper refers to extant leptosporangiate and eusporangiate ferns, the Filicineae of various authors. Bierhorst (1977)
claimed that there are no features in Psilotaceae not also found in ferns. Does this generalization extend to the structure of tracheary elements?
Our earlier papers in this series have shown that vessels in ferns are widespread, ranging from fern families commonly regarded as specialized, such as Dryopteridaceae (Carlquist, Schneider, and Yatskievych, 1997
; Carlquist and Schneider, 1998
; Schneider and Carlquist, 1998
) and Pteridaceae (Carlquist and Schneider, 1997
), as well as those regarded as primitive, such as the eusporangiate fern families Ophioglossaceae (Schneider and Carlquist, 1999
) and Marattiaceae (Carlquist and Schneider, 1999
). Some ferns have tracheids as well as vessels in xylem (Carlquist and Schneider, 2000), but vessel presence in ferns is obviously very pervasive. The occurrence of vessels in Psilotaceae should therefore not be surprising. The concept of "vessel element" is changing as SEM (scanning electron microscopy) studies reveal a multiplicity of types, but one can, for the present, include tracheary elements in which perforation plates with pit membranes are absent, or in which various types of porose or weblike pit membrane remnants are present; pores in pit membranes of perforations are understood to be larger than those of plasmodesmata. This definition has been implicit since the discovery of extensive pit membrane remnants in perforation plates of primitive dicotyledons (Carlquist, 1992
).
The morphology of tracheary elements in Psilotaceae as seen with SEM is important for several reasons. Psilotaceae are distinctive in lacking roots but in having axis systems with subaerial and aerial portions; we are therefore concerned with differences or similarities between tracheary elements of subaerial axes as compared to those of aerial axes in the two genera. Ferns of highly xeromorphic situations have vessels with perforations larger than pits, as in Pteridium (Carlquist and Schneider, 1997
) or Woodsia (Carlquist and Schneider, 1998
; Schneider and Carlquist, 1998
). In ferns of habitats that are not highly seasonal in water availability, the vessels mostly have perforations identical with pits in all respects but absence of pit membranes (in part or entirely) within the perforations. In the nonxeric ferns, presence of vessels can be detected only by means of study with SEM. More importantly, the types of vessel elements represented by the nonxeric ferns do not show degrees of specialization related to degree of phylogenetic position (Carlquist and Schneider, 1999
). However, some nonxeric genera we have studied do have features characteristic of a particular family, as in the curious cushions of primary wall material at angles of vessels in Marattiaceae (Carlquist and Schneider, 1999
). In our studies of tracheary elements of Psilotaceae, therefore, we are interested not merely in occurrence of any characters that might be distinctive, but whether any such features might be related to xeromorphy or mesomorphy.
MATERIALS AND METHODS
Material of Psilotum nudum (L.) Griseb. was collected from plants in and around the greenhouse and lathhouse area of the University of California at Santa Barbara. Psilotum nudum has naturalized here not only in pots, but in the ground as well. The material of Tmesipteris obliqua Chinnock was collected in Bunyip State Park of the Eastern Highlands, Victoria, Australia by C. M. Edwards (Voucher MEL 2042185). The material of both genera was preserved in aqueous 50% ethanol.
Macerations of stelar regions of aerial and subaerial axes were prepared by means of Jeffrey's Solution; macerations were stored in 50% ethanol. Macerations were spread onto aluminum stubs, air dried, sputter-coated, and examined with a Bausch and Lomb Nanolab SEM.
Pit membranes of tracheary elements in Psilotaceae are unusually delicate, and experience various degrees of rupture when exposed at high magnification to the SEM electron beam. We attempted to minimize this exposure (by limiting times of observation under high power) so as to obtain images of intact membranes whenever possible. Some perforations lack any vestiges of pit membranes (e.g., Figs. 3, 4, 10, 11, 13, 14), and we believe these to be genuine. The presence of delicate threads (Figs. 17, 18) is interpreted as an intact condition. A tear can be seen, Fig. 8, right, but we believe that the porose pit membrane to the left of this tear is essentially natural, much as with the porose pit membranes figured with SEM by Morrow and Dute (1998)
for Botrychium.
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Details of tracheary elements of subaerial axes of Psilotum nudum are shown in Figs. 1–8. The end wall facets of the tracheary element shown in Fig. 1 appears imperforate. In fact, some of the scalariform pits on the left facet are porose, as shown in Fig. 6. At higher magnifications (Fig. 7) the pores can be seen, but rupture by exposure to the electron beam prevented obtaining photographs of entirely intact membranes. The end wall of the facet at left in Fig. 1 can be regarded as an incipient perforation plate; openings in pit membranes larger than those of Figs. 6 and 7 would be required to designate perforations as present. Similar small porosities in a pit membrane are illustrated in Fig. 8. The two pit membranes of Figs. 6 and 8 shows that porosities may be found in one pit membrane but may be absent in an adjacent pit membrane. The tracheary element lateral wall of Fig. 2 is entirely free of pores, at least pores we could resolve with our equipment. The pit membranes, although imperforate, show irregular membrane surfaces attributable to processing. The narrow scalariform facets of Figs. 3 and 4 appear entirely natural, and perforations are therefore present. In Fig. 3, the perforations vary somewhat in size. In Fig. 4, however, perforations alternate with one or more narrow pits with intact membranes, as though this dimorphism permitted larger size of some perforations to be achieved. Alternation of wider perforations with narrow pits in a perforation plate is relatively common in ferns in our experience (e.g., Angiopteris and Danaea of Marattiaceae, Carlquist and Schneider, 1999
). The tracheary element of Fig. 5 shows intact imperforate pit membranes. The shapes and configurations of pits in this tracheary element can be described as transitional between alternate and scalariform; such transitions were described for pitting of Psilotum tracheids by Bierhorst (1960)
.
A wide range of expressions is found in the tracheary elements of the aerial axes of Psilotum (Figs. 9–14). Some protoxylem elements have entirely imperforate primary walls (Fig. 9, right), whereas others are perforate (Fig. 10). The facet shown in Fig. 10 has both large circular perforations (above) and porose pit membranes (below). Porose pit membranes are clearly present in the tracheary element of Fig. 12. The tracheary element of Fig. 11 may be transitional between helical and scalariform, but regardless of designation, the facet at the right is composed of circular perforations and the facet at the left of intact primary walls. Scalariform tracheary elements with prominent secondary wall frameworks are shown in Fig. 9 (left), Fig. 13, and Fig. 14. We regard these scalariform elements as metaxylem. The tracheary elements of Fig. 9 and Fig. 13 are slender, so that the perforations are oval. The perforations of Fig. 13 alternate with very narrow pits, similar to perforations of Fig. 4. The ragged edges of perforations in Fig. 13 suggest minimal remnants of pit membranes. In Fig. 14, the facet at the bottom consists of perforations clear of pit membranes or nearly so, whereas a facet of another element at the top of Fig. 14 shows retention of pit membranes, which are, however, porose in places.
Our material of the subaerial axis of Tmesipteris was insufficient to provide views of more than a few tracheary elements. The ones we observed were all like those of Fig. 15, with intact pit membranes (a prominent tear is present on one pit membrane of Fig. 15). We were therefore unable to establish presence of perforation plates in our material.
Tracheary elements of the aerial axes of Tmesipteris (Figs. 16–18) showed vessel elements and incipient vessel elements. The strand of vascular tissue shown in Fig. 16 includes protoxylem elements with helical thickenings (below) as well as metaxylem elements with scalariform pitting (above). In the facet of the metaxylem element at the top of Fig. 16, porosities may be seen in some of the pit membranes. Figures 17 and 18 show a form of pit membrane we saw in several tracheary elements of the aerial axis of Tmesipteris: pit membrane remnants in the form of strands or webs. One must designate these as perforations because of the near absence of pit membranes.
DISCUSSION AND CONCLUSIONS
Our studies have established presence of vessels in the aerial and subaerial axes of Psilotum nudum and in the aerial axes of Tmesipteris obliqua. Further studies are required to see whether porose pit membranes or membrane-free perforations occur on any tracheary elements of Tmesipteris subaerial axes. In all of our preparations of Psilotaceae, we saw some tracheary elements in which perforations, if present, were not visible because part of the length of an element or several of the facets of an element were not visible. Perforations or porose pit membranes may have been present on non-exposed surfaces. However, the possibility definitely remains that both vessel elements and tracheids occur in Psilotum and in Tmesipteris.
With regard to details of secondary wall framework of tracheary elements and metaxylem pitting, our observations agree with those of Bierhorst (1960)
on Psilotum and Tmesipteris. Bierhorst could not observe perforations that are like pits in size and shape with light microscopy. We observed no end wall perforation plates more specialized (perforations appreciably larger than pits on the same element), a condition we have observed in only a few ferns, such as Pteridium (Carlquist and Schneider, 1997
) and two species of Woodsia (Carlquist and Schneider, 1998
; Schneider and Carlquist, 1998
). The ferns with specialized perforation plates are ferns of areas with marked alternation between wet and dry periods, so that well-developed perforation plates could accommodate a hypothetical rapid flow in the xylem during short wet periods. Such modifications for rapid flow are absent in Psilotum and Tmesipteris. The minimal surface area of Psilotum aerial axes and the moist, humid habitats in which Tmesipteris grows presumably minimize transpiration, so that selective pressure for specialized perforation plates would be minimal.
The porose tracheary element pit membranes we have observed with SEM in Psilotaceae as well as other ferns and in monocotyledons cannot be seen with light microscopy. We were surprised by the abundance of porose pit membranes in tracheary elements of Psilotaceae. Although perforations lacking pit membranes are also present in the family, the abundance of porose pit membranes may be interpreted either as an indication of incipiency of perforation formation or lack of strong selection for perforations free of pit membranes to facilitate more rapid conduction. These two concepts are not mutually exclusive.
Tracheary elements of Psilotaceae do not possess any features not also observed in ferns sensu stricto (s.s.). This is not necessarily evidence that the Psilotaceae are ferns; it may merely reflect a limited range of character states in tracheary elements of vascular plants. However, we note with interest the occurrence in both ferns s.s. and in Psilotaceae of perforation plates in which wide perforations alternate with narrow pits with intact pit membranes. Interestingly, in DNA analyses, Psilotaceae associate more closely with Ophioglossaceae than with other groups of vascular plants (Manhart, 1995
; Pryer, Smith, and Skog, 1995
). The tracheary elements of Ophioglossum (Schneider and Carlquist, 1999
) are not unlike those of Psilotaceae. However, the tracheary elements of Botrychium are quite different. Botrychium has tracheids with distinctive circular bordered pits in which the pit membrane bears a central torus and a porose margo (Morrow and Dute, 1998
), and no vessels have been reported in Botrychium.
FOOTNOTES
LITERATURE CITED
Bierhorst, D. W. 1960 Observations on tracheary elements. Phytomorphology 10: 249–305.
———. 1977 The systematic position of Psilotum and Tmesipteris. Brittonia 29: 3–13.
Carlquist, S. 1992 Pit membrane remnants in perforation plates of primitive dicotyledons and their significance. American Journal of Botany 79: 660–672. [CrossRef][ISI]
———, and E. L. Schneider. 1997 SEM studies on vessels in ferns. 2. Pteridium. American Journal of Botany 84: 581–587.
———, and ———. 1998 SEM studies on vessels in ferns. 6. Woodsia ilvensis, with comments on vessel origin in ferns. Flora 193: 179–185. [ISI]
———, and ———. 1999 SEM studies on vessels in ferns. 12. Marattiaceae, with comments on vessel patterns in eusporangiate ferns. American Journal of Botany 86: 457–464.
———, and ———. 2000 SEM studies on vessels in ferns. 14. Ceratopteris, and the significance of widespread vessel occurrence in ferns. Aquatic Botany 66: 1–8. [CrossRef]
———, ——— and G. Yatskievych. 1997 SEM studies on vessels in ferns. 1. Woodsia obtusa (Spregel) Torrey. American Fern Journal 87: 1–8. [CrossRef][ISI]
Gensel, P. G. 1977 Morphologic and taxonomic relationships of the Psilotaceae relative to evolutionary lines in early land plants. Brittonia 29: 14–29. [CrossRef][ISI]
Kaplan, D. R. 1977 Morphological status of the shoot systems of Psilotaceae. Brittonia 29: 30–53. [CrossRef][ISI]
Manhart, J. R. 1995 Chloroplast 15S rDNA sequences and phylogenetic relationships of fern allies and ferns. American Fern Journal 85: 182–192. [CrossRef]
Morrow, A. C., and R. R. Dute. 1998 Development and structure of pit membranes in the rhizome of the woody fern Botrychium dissectum. IAWA Journal 19: 429–441.
Pryer, K. M., A. R. Smith, and J. E. Skog. 1995 Phylogenetic relationships of extant ferns based on evidence from morphology and rbcL sequences. American Fern Journal 85: 205–282. [CrossRef][ISI]
Schneider, E. L., and S. Carlquist. 1998 SEM studies on vessels in ferns. 3. Woodsia scopulina. American Fern Journal 88: 17–23.
———, and ———. 1999 SEM studies on vessels in ferns. 11. Ophioglossum. Botanical Journal of the Linnean Society 129: 105–114.
Wagner, W. H., Jr. 1977 Systematic implications of the Psilotaceae. Brittonia 29: 54–63. [CrossRef][ISI]
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