SEM studies on vessels in ferns. 11. Ophioglossum

With scanning electron microscopy (SEM), the nature of metaxylem vessel elements and tracheids was examined in Ophioglossum crotalophomides, 0. pendulum subsp. falcatum , and 0. vulgatum roots and rhizomes. Vessels were identified in all species. End walls of vessel elements, which bear perforations, are like lateral wall pitting of those elements in the secondary wall framework and differ only in absence of pit membranes or presence of pit membrane remnants. Some of the perforations contain pit membrane remnants that have large pores, small porosities, or are threadlike or weblike in structure. Dimorphic perforations were found in some vessel elements of rhizomes of 0. pendulum subsp. falcatum. Tracheids are very likely present in addition to vessels in all three species. The secondary wall framework of both tracheids and vessels is basically scalariform, although deviations in pattern are present. Vessel elements of Ophiglossum are entirely comparable to those of leptosporangiate ferns.     

Sem studies on vessels in ferns. 12. Marattiaceae, with comments on vessel patterns in eusporangiate ferns

Scanning electron microscopy (SEM) of tracheary elements of roots of five species from four genera of Marattiaceae and of the rhizome of one species revealed vessel elements present in all. The secondary wall framework of perforation plates is the same as that of lateral wall pitting for vessel elements in all species. Thus, no specialization is present in perforation plates of Marattiaceae compared to the simplified morphology of perforation plates of some leptosporangiate ferns (e.g., Dryopteridaceae, Polypodiaceae, and Pteridaceae). The difference between lateral wall pitting and perforation plates in tracheary elements of Marattiaceae cannot be seen by light microscopy (in which pit membranes are transparent), but is evident with SEM. Diversity in structure of perforation plates (especially the alternation of wide and narrow perforations within a plate) and presence of web-like pit membrane remnants are evident. Vessels are widespread in both leptosporangiate and eusporangiate ferns, although specialization in perforation plates (e.g., bars few and more widely spaced in lateral wall pitting of a given vessel element) is to be expected only in ferns of habitats with marked fluctuation in water availability. Vessels of Marattiaceae lack such specializations and are thus are correlated with the mesic habitats characteristic for the family.     

SEM studies on vessels in ferns. 17. Psilotaceae

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.     

SEM studies on vessels in ferns. 2. Pteridium

Xylem from roots and rhizomes of two infraspecific taxa of Pteridium aquilinum was studied by means of scanning electron microscopy (SEM). All tracheary elements proved to be vessels. End wall perforation plates were all scalariform, lacked pit membrane remnants in at least the central part of the perforation plate, and varied with respect to width of bars, from wide to tenuous, and with respect to presence of pit membrane remnants. In addition, porose pit membranes on walls that are likely all lateral vessel-to-vessel walls must be considered to be perforations also, although different from those on end walls. Lateral wall perforation plates, hypothesized by one worker on the basis of tylosis presence but denied by another on the basis of light microscopy, were confirmed by demonstration of pores with SEM. In addition, lateral walls of Pteridium vessels bear some grooves interconnecting pit apertures; this feature is newly figured by SEM for ferns. Lateral wall pitting that is not porose may either have striate thickenings of the primary wall or be smooth. Vessel presence and degree of specialization in Pteridium vessels may bear a relationship to the wide ecological tolerances of the genus.     

Pit membrane remnants in perforation plates and other vessel details of Cornales

Perforation plates and other vessel details as studied with scanning electron microscopy (SEM) have been reported for four species of Cornaceae (s.l.): similar features are shown by the four, suggesting that a more extensive sampling of the family might reveal similar phenomena. Perforation plates contain pit membrane remnants in the form of threads or, less commonly, laminar portions perforated by pores. When least well-represented, the pit membrane remnants are restricted to lateral ends of perforations and to the perforations transitional to lateral wall pitting. Perforations are all clearly bordered. Helical thickenings that do not form a continuous gyre are reported for the vessel walls ofAucuba. The presence of pit membrane remnants in vessel elements of Cornaceae correlates with the mesic habitats occupied by species in this family. The presence and type of pit membrane remnants reported by us in the three genera is very similar, although pit membrane remnants are doubtless a symplesiomorphy and thus not an indicator of relationships. The presence of pit membrane remnants in the three genera, however, does attest to the primitiveness of wood and other features of Cornaceae s.l.     

Vestigial pit membrane remnants in perforation plates and helical thickenings in vessels of Ericaceae

Perforation plates from 15 species of 10 genera with scalarifom perforation plates, representing three subfamilies of woody Ericaceae (Rhododendroideae, Arbutoideae, Vaccinioideae) were studied with scanning electron microscopy (SEM). In most of them, pit membrane remnants were present, but these remnants were less extensive than in the ericalean families Clethraceae, Cyrillaceae, and Sarraceniaceae. Pit membrane remnants in perforations of vessels of Ericaceae are characteristically found at lateral ends of the perforations and in perforations (which may alternatively be called pits) transitional to lateral wall pitting. Pit membrane remnants were most extensive in Enkianthus. Phylogenetic and physiological factors for vestigial membrane presence in the perforations are discussed. Helical thickenings on vessel walls as seen with SEM are figured and described for Leucothoe and Pieris, and their significance is assessed.     

Pit membrane remnants in perforation plates of Hydrangeales with comments on pit membrane remnant occurrence, physiological significance and phylogenetic distribution in dicotyledons

Perforation plates from ten species of seven genera of Hydrangeales sensu Thorne were studied using scanning electron microscopy (SEM). The presence of pit membranes in perforations ranges from abundant, as in Carpenteria and Hydrangea, to minimal, as in Deutzia, Escallonia and Philadelphus. Abnormally great pit membrane presence may result from the presence of secondary compounds that inhibit lysis, as in Quintinia serrata; such interference with the natural lysis process may or may not be evident from coarseness and irregularity of pit membrane surface and of threads composing the pit membrane remnants. The presence of pit membrane remnants in perforation plates is hypothesized to be a symplesiomorphy, found in a fraction of dicotyledons with scalariform perforation plates (but still in an appreciable number of species). Pit membrane remnant presence may represent incomplete lysis of primary wall material (cellulose microfibrils) in species that occupy highly mesic habitats, where such impedance in the conductive stream does not have an appreciable negative selective value. This physiological interpretation of pit membrane remnants in perforations is enhanced by the phylogenetic distribution as well as the strongly mesic ecological preferences of species that exemplify this phenomenon in dicotyledons at large. Families with pit membrane presence in perforations are scattered throughout phylogenetic trees, but they occur most often in basal branches of major clades (superorders) or as basal branches of orders within the major clades. Further study will doubtless reveal other families and genera in which this phenomenon occurs, although it is readily detected only with SEM. Phylogenetic stages in the disappearance of pit membrane remnants from perforation plates are described, ranging from intact pit membranes except for presence of pores of various sizes, to presence of membrane remnants only at lateral ends of perforations and in one or two perforations (arguably pits) at the transition between a perforation plate and subadjacent lateral wall pitting. Developmental study of the mechanism and timing of lysis of pit membranes in perforations, and assessment of the role of the conductive stream in their removal, are needed to enhance present understanding of vessel evolution. © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society, 2004, 146 , 41–51.     

Vessels in ferns: structural, ecological, and evolutionary significance

We have studied macerated xylem of ferns, supplemented by sections, by means of scanning electron microscopy (SEM) in a series of 20 papers, the results of which are summarized and interpreted here. Studies were based mostly on macerations, but also on some sections; these methods should be supplemented by other methods to confirm or modify the findings presented. Guidelines are cited for our interpretations of features of pit membranes. Fern xylem offers many distinctive features: (1) presence of numerous vessels and various numbers of tracheids in most species; (2) presence of vessels in both roots and rhizomes in virtually all species; (3) presence of specialized end walls in vessels of only a few species; (4) multiple end-wall perforation plates in numerous species; (5) lateral-wall perforation plates in numerous species; (6) porose pit membranes associated with perforation plates in all species; and (7) pit dimorphism, yielding wide membrane-free perforations alternating with extremely narrow pits. Multiple end wall perforation plates and lateral wall perforation plates are associated with the packing of tracheary elements in fascicles in ferns: facets of tips of elements contact numerous facets of adjacent elements; all such contacts are potential sites for conduction by means of perforations. This packing differs from that in primary xylem of dicotyledons and monocotyledons. Porosities in pit membranes represent a way of interconnecting vessel elements within a rhizome or root. In addition, these porosities can interconnect rhizome vessel elements with those of roots, a feature of importance because roots are adventitious in ferns as opposed to those of vascular plants with taproots. Fully-formed or incipient (small-to-medium sized porosities in pit membranes) perforation plates are widespread in ferns. These are believed to represent (1) ease of lysis of pit membranes via pectinase and cellulase; (2) numerous potential sites for perforation plate formation because of fasciculate packing of tracheary elements; (3) evolution of ferns over a long period of time, so that lysis pathways have had time to form; (4) lack of disadvantage in perforation plate presence, regardless of whether habitat moisture fluctuates markedly or little, because ferns likely have maintaining integrity of water columns that override the embolism-confining advantage of tracheids. Although all ferns share some common features, the diversity in xylem anatomy discovered thus far in ferns suggests that much remains to be learned.     

PRESENCE OF VESSELS IN WOOD OF SARCANDRA (CHLORANTHACEAE); COMMENTS ON VESSEL ORIGINS IN ANGIOSPERMS

Sarcandra is the only genus of Chloranthaceae hitherto thought to be vesselless. Study of liquid-preserved material of S. glabra revealed that in root secondary xylem some tracheary elements are wider in diameter and have markedly scalariform end walls combined with circular pits on lateral walls. Examination of these wider tracheary elements with scanning electron microscope (SEM) demonstrated various degrees of pit membrane absence in the end walls. Commonly a few threadlike fibrils traverse the pits (perforations); these as well as intact nature of pit membranes in pits at ends of some perforation plates are evidence that lack of pit membranes does not result from damage during processing. Some perforations lack any remnants of pit membranes. Although perforation plates and therefore vessels are present in Sarcandra roots, no perforations were observed in tracheary elements of stems or lignotubers. Further, stem tracheids do not have the prominently scalariform end walls that the vessel elements in roots do. Presence of vessels in Sarcandra removes at least one (probably several) hypothetical events of vessel origin that must be postulated to account for known patterns of vessel distribution in angiosperms, assuming that they are primitively vesselless. Seven (perhaps fewer) vessel origin events in angiosperms could account for these patterns; two of those events (Nelumbo and monocotyledons) are different from the others in nature. Widely accepted data on trends of vessel specialization in woody dicotyledons yield an unappreciated implication: vessel specialization has happened in a highly polyphyletic manner in dicotyledons, and therefore multiple vessel origins represent a logical extension backward in time. If a group of vesselless dictyoledons ancestral to other angiosperms existed, they can be hypothesized to have had a relatively homogeneous floral plan now that Sarcandra-like plants no longer need be imagined within that group. Sarcandra and other Chloranthaceae show that the borderline between vessel absence and presence is less sharp than generally appreciated.     

PIT MEMBRANE REMNANTS IN PERFORATION PLATES OF PRIMITIVE DICOTYLEDONS AND THEIR SIGNIFICANCE

Perforations of vessel elements characteristically retain remnants of pit membranes (primary walls) in woods of species of more than 30 families of dicotyledons. Scanning electron microscopy is necessary to demonstrate presence and type of membrane remnant. Species with these remnants in perforations given in earlier literature as well as those newly reported here are listed. Perforation membrane remnants may take the form of flakes, strands, or webs, and particular types may characterize particular families (e.g., strands or bands in Illiciaceae). Some families have abundant perforation membrane remnants (e.g., Chloranthaceae, Illiciaceae). Where membranes are nearly intact, they are porose and closely resemble the porose pit membranes on end walls of Tetracentron tracheids. In Tetracentron, however, tracheary elements are monomorphic, so vessel origin cannot yet be said to have occurred. Membrane remnants in perforations are regarded as a relictual primitive feature that should be added to the list of primitive character states claimed for vessel elements in angiosperms; alternative hypotheses are considered and discussed, and evidence from DNA phylogenies is needed. In vessel-bearing dicotyledons with membrane remnants in perforations, many perforations are relatively clear, but an appreciable proportion of perforation plates do have membrane remnants.