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Anatomy and development of the fern sporophyte.

II. Introduction

This paper is a review of recent research on the anatomy, morphology, and development of the fern sporophyte. We examine some areas in which particularly significant progress has been made with regard to major questions about the structure and development in the ferns. The studies cited illustrate several different approaches to problems of plant development, from detailed histological and ultrastructural investigations to experimental and quantitative cytohistochemical studies.

The anatomy and morphology of the fern sporophyte have long been of keen interest to biologists. The early research activity in laboratories in continental Europe (e.g., Hofmeister, 1857; see Sadebeck, 1898) spread to Britain and the United States during the 19th and early 20th centuries (Bower, 1889, 1923; Campbell, 1895). The extensive older literature is largely descriptive and comparative in focus, with emphasis on the systematic and, after Darwin, the phylogenetic interpretation of the data. These classic studies constitute the basic foundation for all of the subsequent investigations of comparative fern morphology. Today, research into the anatomy and morphology of ferns is being carried out in many countries.

During a mid-20th-century period of increased experimental studies of ferns, some laboratories began to challenge traditional concepts of the developmental anatomy of fern sporophytes. These issues centered on the processes of development at the shoot and root apical meristems and the formation and differentiation of the derivative tissues. Fern shoot, root, and leaf apical meristems had long been understood to possess single apical initial cells; these divide to produce derivatives that give rise to the other cells and tissues of their respective meristems. During the 1960s and 1970s, some studies seemed to contradict such a role for the apical cell in shoot and root development. The ensuing vigorous debate and its eventual resolution have provided probably the most dramatic controversy in fern anatomy in recent decades.

The following discussion is restricted to aspects of the structure and development of the vegetative body of the fern sporophyte. Most of the issues covered here focus on processes of development at the shoot and root apical meristems, including leaf initiation and early development, branch shoot initiation, and the early development of shoot vascular tissue patterns. The study of the patterns of initiation of leaf primordia and branch shoots at the shoot apical meristem is central to the analysis of shoot developmental morphology and to the interpretation of the organography relationships of the shoot system. Despite numerous studies and despite the central importance of understanding meristems to the interpretation of the organography of the plant body, there remain to this day major gaps in our understanding.

Many of the earlier workers, in their attempts to identify evolutionary trends, tended to stress the comparative structure of the different patterns of shoot vascular systems or steles found among ferns. Such descriptive anatomical work continues, and though it represents a potentially very fruitful source of systematic characters for phylogenetic analysis, it will not be reviewed in detail here.

More briefly we refer to questions concerning the relationship of stem, leaf, and root meristem activity to the development of vascular tissue in mature organs. In addition, the relationship between structure and function in the ferns is explored by recent studies of stem structure and xylem water flow in ferns. The functional integration of the shoot vascular system in relation to the physiological ecology of the plant is a recently developed area of study. Functional anatomy is another important subject area for future research. Ferns are potentially good subjects for the study of xylem conductivity in relation to structure, for they show a wide range of shoot morphologies and stem anatomies as well as diversity in growth habit and habitat.

The ferns, although arguably one of the less "important" groups of vascular plants in modern floras, have played a major and unique role in the development of theories of vascular plant shoot organization and evolution (viz. the apical cell concept and stelar theories), and the studies of development in ferns may well contribute to the formulation of general concepts of vascular plant morphology. The structure of the apices and the patterns of formation of vascular tissue in ferns appear simpler than those seen in seed plants. Detailed study of ferns, therefore, may provide some basis for better understanding the underlying principles of morphogenesis for vascular plants in general and for the more complex seed plants in particular. There is a continuing need for detailed descriptive work. Clearly, a sound understanding of the phenomenology of normal development is required for good experimental design and correct interpretation of experimentally modified development.

III. Shoot Apical Meristem

Over the past decade, significant progress has been made in understanding the organization and functioning of the meristems of the fern sporophyte. Whereas in the 1970s discussion still focused on interpreting the activity of the shoot apical cell, detailed studies since that time have clarified this issue and led to a reaffirmation of the traditional view of the role of the apical cell.

The traditional interpretation of shoot apical organization in ferns identified the apical cell of the shoot as the single initial cell from which all other cells in the shoot meristem are derived (Hofmeister, 1857; Bower, 1889, 1923; Bierhorst, 1977). This view was challenged in the 1960s and 1970s by studies that indicated that the apical cell is mitotically inactive. Further, in some cases it was interpreted to be polyploid, and thus could not be functional as an apical initial, although it might instead have a regulatory role (for reviews see White, 1971, 1979; Gifford, 1983, 1985; Bhambie & Puri, 1985). Concurrently, other workers also tended to deemphasize the apical cell when describing the structure of fern shoot apices. A survey of the cytohistological organization of the fern shoot apex (McAlpin & White, 1974) led to an attempt to reduce the focus on the apical cell and instead to emphasize the overall functional zonation of cells at the shoot apex. Descriptions of the histological patterns seen in sections of the pteridophyte shoot apex allowed closer comparisons with the zonate meristems of gymnosperms and angiosperms. Parallels were drawn between the putatively quiescent apical cell of the shoot (and the root, see below) and the multicellular quiescent zones of the shoot and root apices of seed plants (McAlpin & White, 1974; Stevenson, 1976a, 1976b, 1978). Such studies prompted a vigorous response (e.g., Bierhorst, 1977) which rejected the revised interpretations of fern shoot apical organization and supported the traditional view of the histogenetic activity of the apical cell with descriptions and illustrations of a broad sample of fern species.

More recent experimental and descriptive studies consistently affirm the classical concept that the apical cell does divide as the single initial cell of the apical meristem. The studies comprise a fairly wide systematic survey of ferns, and have used a broad range of methods including autoradiography of labeled thymidine, DNA cytospectrophotometry, colchicine-induced metaphase accumulation, and determinations of cell cycle and mitotic indices. Measurements of the mitotic index, cell division cycles, and nuclear DNA for different shoot apical zones of Ceratopteris, Azolla, and Nephrolepis indicate that the shoot apical cell in these species divides as frequently as or more actively than subjacent cells (Gifford et al., 1979; Polito, 1979, 1980; Gifford & Polito, 1981; Seilhean & Michaux-Ferriere, 1985; Seilhean, 1986). In contrast, a very slow cell cycle was reported in shoot apical cells of adult Pteris cretica (Michaux-Ferriere, 1981a). As various workers have noted, the division rate of an apical cell relative to those of the subjacent and surrounding cells is necessarily related to the shape of the meristem. Slender conical shoot apices will have a relatively actively dividing apical cell, whereas broad apical meristems will contain comparatively slow ones (Polito, 1979; Seilhean & Michaux-Ferriere, 1985; Seilhean, 1986; Piquerez & Michaux-Ferriere, 1986; Hebant-Mauri, 1993). Cell cycle rates may change sharply during ontogeny; for example, in juvenile plants of Polypodium both the axial and lateral meristem zones show similarly high division activity, but the axial zone of adult plants has a low mitotic index with a cell cycle twice that of the lateral zone (Michaux-Ferriere, 1981b).

Probably the most convincing line of evidence for the traditional concept of the shoot apical cell comes from detailed interpretations of cell lineages in the apical meristem. Sections and clearings of shoot apices commonly show the apex to be composed of recognizable blocks of cells (segments or merophytes), each the product of a single derivative cell of the apical cell. The arrangement of these segments is frequently a regular spiral, indicating a regular sequence of divisions of the apical cell [ILLUSTRATION FOR FIGURE 1 OMITTED]. Shoot apical segmentation patterns have been described by numerous authors for numerous species of ferns, representing a reasonably broad survey of fern groups. Many of these descriptions are found in the older literature (Hofmeister, 1857; Klein, 1884; Bower, 1889, 1923; Campbell, 1895, 1911; Conard, 1908; Bartoo, 1930; von Guttenberg, 1966). Relatively few recent workers have studied the apical segmentation of fern shoots. However, Bierhorst (1977) presented evidence of apical segmentation patterns from cleared and stained apices of many fern species in his defense of the traditional fern shoot apex. Additionally, apical segmentation has been described and illustrated for apical meristems of ferns including Hymenophyllaceae, Dicksonia, Ceratopteris, Stromatopteris, and Lomagramma (Hebant-Mauri, 1973, 1975, 1977, 1984, 1993; Hebant-Mauri & Veillon, 1989; Hebant-Mauri & Gay, 1993). Similarly detailed descriptions have been provided for the shoot apices of Histiopteris, Hypolepis, Dennstaedtia, Adiantum, and Osmunda (Imaichi, 1977, 1980, 1982, 1984, 1988).

In most of the above cases, the apical cell is described as having an inverted-pyramid, tetrahedral shape with the derivative segments being cut off by divisions parallel to the three proximal faces [ILLUSTRATION FOR FIGURE 1 OMITTED]. Noteworthy exceptions to this appear to be the water ferns (Azollaceae, Salviniaceae, and Marsileaceae), which are reported to possess prominent apical cells with two cutting faces (Croxdale, 1978, 1979; von Guttenberg, 1966; Schmidt, 1978). The two series of apical segments are strongly correlated with the dorsiventral symmetry of the shoot system. For the Marsileaceae, these interpretations require further documentation, since earlier studies clearly indicate a three-sided apical cell in Marsilea (Schneider, 1913).

The classical apical cell concept thus is broadly applicable to the shoot apical meristems of leptosporangiate ferns and Osmunda. The situation in the eusporangiate ferns of the Ophioglossaceae and Marattiaceae seems to be less clear. Groups of several apical initials have been reported in meristems of adult plants of some of these species whereas other apices of the same species have single apical cells (Campbell, 1911; Bower, 1923; Bhambie & Puri, 1985). It is likely, however, that even these species typically have single apical initial cells. Recent detailed investigations of shoot development in Botrychium (Imaichi, 1989; Imaichi & Nishida, 1986) indicate that a regularly segmenting tetrahedral shoot apical cell is usually identifiable. Similarly, a study of shoot apices of Angiopteris, has found that both large and small shoots usually have regularly segmenting single apical cells but that some (cultivated) shoots show irregular cell patterns in which it was difficult to recognize an apical cell (Imaichi, 1986). Similar investigations of apical segmentation in other eusporangiate ferns would be worthwhile. The apical meristems of Ophioglossaceae and Marattiaceae show histological zonation comparable with that of other ferns (Stevenson, 1976b, 1978).

A recent survey that analyzed several different structural parameters of fern shoot apical meristems recognized two broad categories of meristems based on their profile in longitudinal section (Hebant-Mauri, 1993). Convex meristems range from very sharp to rounded in shape and tend to characterize fast-growing slender stems with a loose phyllotaxy. Concave meristems differ in that the central dome of the meristem occupies the center of a depression surrounded by raised tissues; concave meristems are found in plants with thicker, slower-growing stems with a tight phyllotactic spiral. The surfaces of convex meristems show the outlines of relatively few shoot apical segments, whereas in concave meristems identifiable segments can be traced far from the apical cell. To some extent, this difference is attributable to the fact that concave meristems tend to be much larger and are composed of many more cells (Hebant-Mauri, 1993).

Among the other groups of pteridophytes, Equisetum, Psilotum, and species of Selaginella possess more or less prominent shoot apical cells, whereas Lycopodium and Isoetes lack distinctive apical initials (e.g., von Guttenberg, 1966). It has been suggested that apical meristems with and without single apical cells are two fundamentally different, nonhomologous types that define two separate evolutionary lineages of land plants (Philipson, 1990). Contrary to this view, it seems much more likely that the basic structural and developmental similarities shared by shoots of all groups of vascular plants reflect their common phylogenetic origin. Shoot apical meristems of ferns and seed plants are similar in important ways, despite the difference in the apical initial cells.

One view discussed by proponents of the mitotically quiescent apical cell concept and others has been that the apical cell may play an important role in regulating the activities of the shoot apical meristem (White, 1979; Gifford 1983, 1985; Michaux-Ferriere & Hallet, 1985). It has been reported that the apical cell in an adult shoot of Pteris has a very slow cell cycle but shows high levels of RNA metabolism, which would be in keeping with such a regulatory role (Michaux-Ferriere, 1981 a). The large numbers of plasmodesmata between cells in the apex may function in the transfer of developmental information from cell to cell and zone to zone. It is probable, of course, that an actively dividing apical initial cell could also be producing substances that influence or control the behavior of surrounding cells. It is suggested that such a role may account for the commonly seen enlarged nucleus and nucleolus in the apical cell. The sometimes reported "polyploid" levels of DNA in shoot and root apical cells may instead reflect some other method of DNA amplification such as polyteny (Vallade & Bugnon, 1979; Kurth & Gifford, 1985). If true, the mechanism by which polyteny can occur in dividing meristematic initials should be investigated, since, as has been noted, it would seem to require modification of current concepts of the cell cycle (Kurth & Gifford, 1985).

The two competing views of the fern shoot apex - one stressing the apical cell and its derivatives, the other emphasizing the histological zonation of the apex - can be reconciled as reflecting two aspects of the same pattern of organization. The shoot apical cell is critical to the functioning of the apical meristem in its role as the single apical initial cell, but focusing on the apical cell and its divisions will not give a complete picture of apical organization and function. The fern shoot apical meristem is also fundamentally a complex, cytohistologically zoned structure.

Most leptosporangiate ferns share a common shoot apical organizational pattern, in which a superficial layer of large anticlinally elongate cells overlies a zone of smaller isodiametric cells. Cells of the different layers differ in staining properties, and the apical cell and surrounding surface layer cells have larger nuclei and greater vacuolation than the subsurface cells. Proximal to the shoot apex and at its perimeter are distinct meristematic zones transitional to the developing tissues of the cortex, stele, and pith [ILLUSTRATION FOR FIGURE 2 OMITTED].

Although the basic structure of the shoot apical meristem seems to be similar for leptosporangiate ferns, the terminology and concepts used by different authors to characterize the apical zonation has varied. Although the most appropriate terminology is clearly debatable, we tend to favor positional, descriptive terms (e.g., "central cells," "surface layer" or "prismatic cell layer," and "subsurface layer") over terms reflecting inferred histogenic roles.

In contrast to the concept of the fern shoot apex as a zoned meristem are recent investigations that describe in great detail the histological organization and development of the shoot apex in Matteuccia (Ma & Steeves, 1994, 1995). Based on an analysis of the strong differences among shoot apical layers in cellular staining properties, ultrastructure, and cytochemistry, the authors interpret the apical cell and the surface layer of prismatic cells to be a single-layered promeristem (strictly defined as the only self-perpetuating layer of undifferentiated meristematic cells in the apex). All subsurface cells of the apex are identified as prestelar tissues in early stages of differentiation: a central group of pith mother cells and more peripheral provascular tissue. It is doubtful whether the terminology used to describe the Matteuccia apex would be as appropriate in analyzing structurally similar shoot apices of ferns with protosteles or ferns with highly dissected or polycyclic steles. It can also be argued that the histological data from these studies actually fit very well with concepts of shoot apical zonation that employ less restrictive definitions of "apical meristem." Clearly, in any meristem with a small number of initial cells, the existence of zonation among their derivatives strongly implies that some cellular differentiation is taking place. Presumably, similar considerations would apply to the zonate structures seen in shoot apices of seed plants.

In its zonate organization, the fern shoot apex as a whole seems to be functionally comparable with the apical meristems of seed plants. Both aspects - apical cell segmentation and apical zonation - are important to an understanding of the organization, dynamics, and development of the fern shoot apex, and both should be treated in descriptive studies of the shoot apex (e.g., as by Hagemann, 1964; Hebant-Mauri, 1993). In one and the same apex one can distinguish basic developmental phenomena operating at cellular and histological (unicellular vs. supracellular or multicellular) levels. On the one hand, the regular divisions of the shoot apical cell and its derivatives, and the initiation and activity of the leaf apical cells, are clearly important. On the other, the basic patterns of shoot histogenesis and vascular tissue development, the control of phyllotaxy and the sites of leaf initiation are phenomena that reflect the integrated functioning of the shoot apex as a whole and may be essentially independent of cell lineages.

One of the more interesting current problems in plant morphology is the apparent conflict between the concept of the plant body as a structure composed of discrete cells and views that plant form and morphogenesis are phenomena operating at an organismal level, not a cellular one (Kaplan & Hagemann, 1991; Hagemann, 1992; Kaplan, 1992; Cooke & Lu, 1992; Sitte, 1992). Detailed analysis of development at fern shoot apices, and of other plant organs that seem to show variable relationships between cell lineages and morphology, would be one approach to exploring this question.

IV. Leaf Development

A primary area of focus in developmental studies of the fern shoot apex has been the origin and early development of the appendages of the shoot, the leaves and lateral branches. There have been several important contributions to the study of fern leaf development and structure in recent years.

Although some issues have been clarified, there is still no satisfactory explanation of the morphogenetic factors that control the regular formation of leaves at the shoot apex. It might easily be supposed that there should be a definite relationship between the segments of the shoot apex and the sites of leaf initiation and hence the phyllotactic arrangements of leaves on the shoot. The available evidence indicates, however, that in at least some species of ferns there is no strict correlation between shoot apical segmentation and phyllotaxy (Hebant-Mauri, 1975, 1993). In addition to these fern examples, a recent study has similarly found that there is no particular relationship between apical segments and leaves in developing shoots of Selaginella (Jernstedt et al., 1994). On the other hand, in at least some species of ferns it is reported that there is a more or less regular relationship between leaf initiation sites and shoot apical segmentation (Bartoo, 1930; Hebant-Mauri, 1973, 1977, 1993). In Marsileaceae, for example, the leaf primordia, lateral branch meristems, and root primordia are all reported to be initiated in specific positions within each of the shoot apical segments (Schmidt, 1978). The leaves, shoots, and roots arise in separate sectors that are delimited by the first anticlinal divisions of the shoot apical segments (Schmidt, 1978).

For a considerable time, a major debate centered on the concept that the newly initiated primordia at the shoot apex are not initially "determined" as leaves and could be transformed into shoot apices. Numerous experiments were designed to manipulate the determination of such primordia as leaves or as shoots (for reviews see Cutter, 1965; White, 1979; Kuehnert & Larson, 1983; Steeves & Sussex, 1989; Steeves et al., 1993). In recent studies of shoot formation on excised Osmunda leaf primordia cultured in vitro, the shoots that are obtained have been interpreted as either 1) induced buds formed on the adaxial side of the leaf apex (Kuehnert & Larson, 1983) or 2) the result of an actual conversion of the leaf apex into a shoot apex (Steeves et al., 1993). The difference in these views is perhaps largely a matter of interpretation; the developmental stages illustrated appear to be similar. In both, the primordium apex becomes divided into an abaxial (or terminal) leaf meristem and a shoot apex which arises on the adaxial side, not far from the original leaf apical cell. In one interpretation, the original leaf meristem remains foliar and initiates a new shoot close to its apex (Kuehnert & Larson, 1983). On the other hand, in a very recent study the leaf apex is reported to lose its apical cell organization and become broadened. The broadened apex then separates into two meristems: an abaxial leaf apex and an adaxial shoot apex (Steeves et al., 1993). The critical issue in this debate appears to be whether or not the abaxial, leaf-forming meristem represents the direct continuation of the original leaf apex. The question hinges on whether the original leaf apical cell is truly lost and a new leaf apex formed. It does seem clear that the shoot apex is newly organized from the adaxial part of the leaf apical meristem. The morphological significance of this phenomenon is debatable; the formation of shoots or buds from leaf meristems of intact ferns of several species has long been known (e.g., Kupper, 1906; McVeigh, 1937; Gupta & Bhambie, 1992).

The initiation and early development of fern leaf primordia has been described for several species, including Hymenophyllaceae (Hebant-Mauri, 1973, 1984, 1990; Hagemann, 1988), Dicksonia (Hebant-Mauri, 1975), Ceratopteris (Hebant-Mauri, 1977), Stromatopteris (Hebant-Mauri & Veillon, 1989), Salvinia (Croxdale, 1978, 1979, 1981), Marsileaceae (Schmidt, 1978), Dennstaedtiaceae (Imaichi, 1980, 1982, 1983, 1984), Adiantum (Imaichi, 1988; Gupta & Bhambie, 1992), Botrychium (Imaichi & Nishida, 1986; Imaichi, 1989), Lygodium (Mueller, 1982a), Platycerium (Lee, 1989), and Gleicheniaceae (Hagemann & Schulz, 1978). Additionally, Bierhorst (1977) described and illustrated stages of leaf initiation in various species in several fern families. Although these studies show broad areas of agreement regarding early leaf development, there are also important points of disagreement.

Bierhorst (1973, 1977) described the leaves of several groups of ferns as "non-appendicular fronds." Such leaves are said to arise by the transformation of a shoot tip or by a dichotomy of a shoot rather than by forming as lateral outgrowths of the shoot apex, as is characteristic of other plants. Non-appendicular fronds were regarded as a primitive stage in the evolution of fern shoot systems. This concept was developed in connection with Bierhorst's view that the Psilotaceae are true ferns with non-appendicular "leaves" (the aerial shoots of the usual morphological interpretation), comparable to the leaves of Stromatopteris and other relatively primitive ferns. Regardless of the ultimate systematic disposition of Psilotum and Tmesipteris, Bierhorst's interpretations seem to be incorrect, at least for living ferns. Contrary to Bierhorst's report, in Hymenophyllaceae, Stromatopteris, Gleicheniaceae, and Dennstaedtiaceae (see citations above), leaf initiation is described as occurring in lateral positions on the shoot apical meristem in essentially the same way as in other ferns.

A more subtle disagreement concerns the nature of the earliest stage of leaf development and the related question of the boundary between foliar and cauline tissues at the base of the leaf primordium. Many workers over the years have described an essentially unicellular pattern of leaf initiation, in which one cell of the surface layer of the shoot apex, the "leaf mother cell" of Bierhorst (1977), becomes enlarged and undergoes a series of oblique anticlinal divisions to become the new leaf apical cell [ILLUSTRATION FOR FIGURE 3 OMITTED]. This pattern is supported both by numerous early descriptions (Hofmeister, 1857; Kny, 1875; Klein, 1884; Conard, 1908; Schneider, 1913; Bartoo, 1930) and by more recent research (Hebant-Mauri, 1973, 1984, 1993; Bierhorst, 1977; Croxdale, 1978, 1979, 1981; Imaichi, 1980, 1982, 1983, 1984, 1988; Imaichi & Nishida, 1986; Mueller, 1982a; Gopalakrishnan & Nayar, 1990). Others, however, regard the leaf as essentially multicellular from its initiation, arising from a variously characterized group of cells on the shoot apex (Wardlaw, 1949; Cutter, 1956; Steeves & Briggs, 1958; Hagemann, 1964, 1965; McAlpin & White, 1974; Hagemann & Schulz, 1978; Lee, 1989; Gupta & Bhambie, 1992; Ma & Steeves, 1994).

To some extent these disagreements are terminological rather than substantive. An example of this is the distinction between the view that the base of the leaf primordium may be derived from cells of the shoot apex not produced by the leaf apical cell (Imaichi, 1980, 1988) and the view that only the derivatives of the leaf apical cell can be regarded as truly foliar, regardless of the contribution of "cauline tissue" to the apparent leaf base (Bierhorst, 1977; Hebant-Mauri, 1984, 1993; [ILLUSTRATION FOR FIGURE 4 OMITTED]). More substantial questions involve the apparently real differences among the species described. To what extent is there a common pattern of development? What are the earliest detectable stages of leaf initiation, and what is the actual sequence of developmental stages? Are there major differences among species, or are the descriptive differences due to different methods and different observers? Some reports indicate that a delay in periclinal division by some of the superficial prismatic cells of the shoot apex is the earliest recognizable stage of leaf initiation (Hebant-Mauri, 1973, 1975, 1977, 1984). In Dicksonia, leaf initiation occurs within a small group of cells that are somewhat larger than neighboring cells (Hebant-Mauri, 1975). Research in our laboratory has shown that in species of Dennstaedtia, Hypolepis, and Microlepia, the earliest identifiable stage of leaf initiation involves a more or less well-defined localized expansion of the shoot apex at the future leaf site (Turner, 1985). Within this elevated area there are typically several enlarged superficial cells, one of which becomes the leaf initial cell. Thus, there appears to be a general, multicellular leaf initiation phenomenon preceding the essentially unicellular events establishing the leaf initial cell. It is likely that the underlying developmental processes are fundamentally similar in species with multicellular and species with unicellular leaf initiation.

Aspects of the later development of the leaf in leptosporangiate ferns have been investigated by relatively few recent workers. These reports generally add little to the classical literature on the activity of the leaf apical cell and the leaf marginal meristems and on the patterns of pinna initiation and lamina development (e.g., Bower, 1889; Sadebeck, 1898; Conard, 1908; Hagemann, 1964, 1965, 1984; von Guttenberg, 1966). Young leaf primordia in typical leptosporangiate ferns have an apical cell with two cutting faces and a lenticular outer face, and two continuous rows of marginal meristem initials that form derivatives to the upper and lower sides of the leaf [ILLUSTRATION FOR FIGURES 5, 6 OMITTED]. Leaflet initiation involves processes of meristem fractionation that are the result of localized increases in growth and localized cessation of growth by different sectors of the originally continuous leaf marginal meristems (Hagemann, 1965, 1984).

In Salvinia, the blades of the floating leaves reportedly develop by the activity of unique abaxial meristems (Croxdale, 1979); however, despite their unusual orientation, the meristems appear to be typical fern marginal meristems. The dissected submerged leaves are very different in their pattern of development (Croxdale, 1981). The initiation of the leaflets apparently differs from pinna formation in other ferns, and it should be examined in more histological detail. It seems possible that the "submerged leaf" may actually be a determinate branch shoot bearing filiform leaves (the "leaflets").

The development of the complex leaves of the climbing fern Lygodium has been described in a series of papers (Mueller, 1982a, 1982b, 1983). These leaves represent an extreme example of the tendency of ferns for foliar elaboration, showing indeterminate growth of the leaf apex, with dormant resting "leaf buds" formed by the pinna apices. The leaf is unusual in that the young pinnae develop new apical cells from marginal initial cells. The Lygodium frond is a functionally complex, foliar analogue to a twining shoot system (Mueller, 1983).

Leaf development has been described in Microgonium tahitense, a species of filmy fern with unusual peltate leaves (Hagemann, 1988). Early in leaf development, the two proximal ends of the marginal meristems become joined by the activity of the intervening cells on the adaxial side, so that a continuous meristematic ring is formed. This example is an exception to the generalization that the fusion or incorporation of meristems is rare in ferns (Hagemann, 1984, 1988).

Development of the mantle leaves of Platycerium shows some unusual features (Lee, 1989, 1990). The leaf primordia lose the leaf apical cell early; the marginal meristem initials are atypical in that they divide to produce derivatives in a uniseriate fashion, as in filmy ferns (Bower, 1889, 1923), rather than dividing to produce segments alternately to the upper and lower sides of the lamina as in other leptosporangiate ferns. Reportedly, the marginal initials later become wedge shaped and divide in the usual manner (Lee, 1989). Leaf vascular tissue differentiation has been described in this species in relation to the leaf meristems and the growth of the primordium (Lee, 1990).

A detailed investigation of leaf initiation and development in Botrychium has shown that leaf development in this genus is quite distinct from the pattern found in the leptosporangiate ferns (Imaichi & Nishida, 1986; Imaichi, 1989). The leaf apical cell is tetrahedral, forming segments on three sides. The continuous series of marginal initial cells characteristic of leptosporangiate ferns are lacking. Pinnae and pinnules arise as small multicellular mounds that later develop tetrahedral apical cells, which produce segments on three sides. The fertile spike is initiated as a single new apical cell on the adaxial side of the apical meristem of the young leaf primordium. It thus differs from the vegetative pinnae in developmental pattern (Imaichi & Nishida, 1986). The development of the basal leaf sheaths differs among species in a potentially systematically significant way (Imaichi, 1989).

In a quantitative analysis of pinnule formation in Adiantum and Cheilanthes, mitotic rates were compared for different developing leaf sectors (Zurakowski & Gifford, 1988). The cytological and physiological details of fern leaf apical and marginal meristem development remain as major areas that are still largely unexplored, however, and represent an especially promising subject for future research. Such studies would parallel and complement the many similar studies of shoot and root apical meristems, and should yield new information on the functioning of leaf meristems in terms of meristem zonation, histogenesis, leaf branching, and vascular tissue differentiation. Since the fern leaf is typically a determinate organ, the leaf apical and marginal initials may be mitotically active for only a limited time, and it therefore is likely that major changes in the leaf meristems occur early in leaf development.

V. Branch Development

In contrast with seed plants, ferns are diverse in modes of shoot branching, with axillary lateral buds being uncommon. Axillary branching is known in Botrychium and Helminthostachys of the Ophioglossaceae (Kato et al., 1988), this being one of the features that suggest a relationship with the seed plants. However, since axillary branching is most likely primitively absent in cycads (Loconte & Stevenson, 1990; Nixon et al., 1994), the similarity in branch position in Ophioglossaceae and most seed plants may well be independently derived. Near-axillary or adaxial lateral buds are found in Hymenophyllaceae (Hebant-Mauri, 1973, 1984, 1993), but shoots of most ferns are variously unbranched, "dichotomously" branched, or have lateral branch buds in nonaxillary positions (Troll, 1937).

The development of terminal or dichotomous shoot branching has been described for Gleicheniaceae (Hagemann & Schulz, 1978), Lygodium (Mueller, 1982a), and Dennstaedtia (Imaichi, 1984). There is considerable agreement among these workers regarding the general pattern: distal to all leaf primordia, the shoot apical meristem broadens, then becomes divided into two [ILLUSTRATION FOR FIGURE 7 OMITTED]; the original apical cell stops functioning as such, and a new apical cell is formed in each daughter apex. In the Gleicheniaceae, a broadened initial zone of the shoot apex (in which the apical cell has become lost or unrecognizable) divides into two, followed by division of the meristem (Hagemann & Schulz, 1978). In Lygodium and Dennstaedtia it is reported that the apical cell ceases to function as an initial, and in Lygodium the apical cell and young derivatives divide to form a group of small cells separating the two daughter meristems. An essentially similar pattern of dichotomous branching has also recently been described in Selaginella (Jernstedt et al., 1994).

Dichotomous branching patterns that superficially are similar to the above occur in species of Dennstaedtia and Microlepia. In these species, however, the shoot apical cell is interpreted as dividing to form two branch apical cells (Turner, 1985). This may be the first demonstration of dichotomy, in the strictest sense of the definition, among pteridophytes. The existence of this type of dichotomy among ferns has previously been supported (Bierhorst, 1977); the relevant illustrations, however, merely showed putative apical cells close to one another at the shoot tip, which provides insufficient proof of their mode of origin. Regardless of the fate of the apical cell, the shoots of all of these species may be regarded as dichotomous, in the sense that the branching is an essentially equal subdivision of the shoot apical meristem.

Lateral branching in ferns occurs in various positions, either cauline or at the base of the leaf primordia. Branches in Hymenophyllaceae arise from single superficial cells of the shoot apex adjacent to the newly initiated leaf; they are essentially axillary in position, but subsequent correlative growth of the shoot, leaf, and branch may cause the branch to be displaced to the adaxial base of the petiole or to the internode above the axil (Hebant-Mauri, 1973, 1984, 1993). Unicellular lateral branch initiation has also been described in Salviniaceae (cf. Croxdale, 1978, 1981), Marsileaceae (Schneider, 1913), Nephrolepis (Sperlich, 1908), and Polypodium (Klein, 1884; but see Hagemann, 1976). Early branch initiation in other species involves a multicellular patch of cells (Wardlaw, 1943a, 1943b; Hebant-Mauri, 1975; Croxdale, 1976; Hagemann & Schulz, 1978; Imaichi, 1980, 1982, 1983, 1985; Hebant-Mauri & Gay, 1993). Detailed studies have been done of the development of the epipetiolar lateral branches of the dennstaedtioid ferns Hypolepis and Histiopteris (Imaichi, 1980, 1982, 1983, 1985). In these species the buds are initiated as clusters of cells at the base of the leaf primordium [ILLUSTRATION FOR FIGURE 8 OMITTED], and they form in a zone of tissue that is adjacent to the tissues derived from the leaf apical cell; this adjacent sector is nevertheless considered to be foliar, since it contributes to the base of the developing leaf. These branches have in some cases been found to be even more intimately related to the meristematic development of the leaf than previously described (Turner, 1985). Buds can and do arise in tissue derived from the leaf apical cell, and they involve the derivatives of the leaf apical and marginal meristems. Buds with such a direct developmental connection with the leaf may indeed be regarded as truly phyllogenous.

Branching in ferns is diverse from a functional point of view as well as from a morphological one, in that the lateral buds of different ferns may or may not be dormant initially. Although Wardlaw's (1943a, 1943b) "detached meristems" were characterized as simple groups of cells that remain undifferentiated, in ferns such as Hypolepis the lateral buds develop directly into organized, active branch shoot apices. A substantial body of experimental work has investigated the control of dormancy and apical dominance in Marsilea (e.g., Chenou-Fleury, 1975; Sossountzov, 1976; Sossountzov & Chenou, 1978; Chenou et al., 1978, 1982; Habricot & Sossountzov, 1984a, 1984b; Sossountzov & Habricot, 1985; Sossountzov et al., 1985). These studies indicate that bud inhibition and bud activation are closely connected with changes in the patterns of solute transport in the shoot and that the transfer cells in the stele play an important role in this system. Differences in DNA content and cell cycle stages are said to characterize dormant and activated buds of Polypodium (Michaux-Ferriere, 1984).

VI. Root Development

Recent research on the structure and function of the root apical meristem has progressed along lines similar to those taken by studies of the shoot apex. The long-accepted concept of the role of apical cells in shoot and root apices of pteridophytes was sharply challenged during the 1970s, when it was proposed that the root apical cell is mitotically quiescent, perhaps polyploid, perhaps only regulatory in function (see White, 1979; Gifford, 1983, 1985). As in the case of the shoot apical meristem, recent studies of the root apex consistently support the classical concept of the apical cell as the functional apical initial of the root meristem. These studies of the organization and dynamics of the root meristem are based on several lines of evidence, including observations on apical meristem cytohistological zonation, ultrastructure, cell cycle durations, mitotic indices, DNA microspectrophotometry, incorporation of radioactively labeled DNA precursors, and interpretations of cell lineages. Ferns studied include Marsilea (Kuligowski-Andres, 1977; Vallade & Bugnon, 1979; Kurth, 1981; Lin & Raghavan, 1991), Regnellidium (Eastman & Peterson, 1985), Azolla (Gunning et al., 1978a, 1978b; Nitayangkura et al., 1980; Gunning, 1981; Kurth & Gifford, 1985), Asplenium (Gifford, 1991), Osmunda (Freeberg & Gifford, 1984), and Ophioglossum (Peterson & Brisson, 1977). The data from these studies support the view that the root apical cell is mitotically active and that its divisions are the ultimate histogenic source of the tissues of the root.

The most compelling evidence for the traditional view of the root (and shoot) apical cell are the observed regular arrangements of the groups of cells making up the apex. These patterns indicate that the root apical cell divides to form a series of derivatives or merophytes that undergo regular sequences of further divisions to produce the tissue layers of the root (e.g., Gunning et al., 1978c; Gifford, 1991; Lin & Raghavan, 1991; Gunning, 1982).

The precise, predictable pattern of cell lineages in the root apical cell derivatives in Azolla has provided the basis for one of the most sophisticated analyses of cell and tissue development available for any vascular plant organ. In an extensive series of papers, Gunning and his co-workers described in detail the segmentation of the apical cell and the subsequent divisions of the merophytes, and the ultrastructure of the root apical meristem (Gunning et al., 1978a, 1978b, 1978c). Quantitative nuclear and cytoplasmic changes in specific cell layers of young roots (Barlow et al., 1982) were reported, and changes in densities of plasmodesmata (Gunning, 1978) and in number and structure of chloroplasts (Whatley & Gunning, 1981) in differentiating root cells were described. A major focus of these studies has been the role of microtubules in development. Preprophase bands of microtubules precisely predict the position of new cell wall formation in dividing cells (Gunning et al., 1978a). The role of cortical microtubules in cytomorphogenesis, the initiation of new microtubules, the regulation of their formation, and the determination of the sites at which they are formed have been investigated in detail (Gunning et al., 1978b; Hardham & Gunning, 1979; Gunning, 1980, 1981, 1982; Busby & Gunning, 1983).

Root initiation on fern rhizomes has usually been described as involving the transformation of a single cell close to the shoot apex into a new root initial. The cell layer in which roots are initiated apparently varies among species, from the immediate meristematic precursors of endodermis and outer stelar tissues (see von Guttenberg, 1966) or of the outer cortex (Stevenson, 1976a). An (almost) exogenous origin of root primordia has recently been reported in Microsorium (Sakai, 1990) and Blechnum (Gopalakrishnan & Nayar, 1990). In the former species the root apex is shown to arise immediately below the developing epidermal layer, and in the latter the root apical cell is reported to form following a series of divisions of a truly superficial cell (this lacks photographic documentation, however). Thus, it appears that whereas in some ferns the rhizome-borne roots arise in direct connection with the developing vasculature of the shoot, in other ferns a root trace must differentiate to bridge a substantial distance between the new root apex and the stem stele.

A recent paper has described in great histological detail the initiation and early development of lateral branch roots in Marsilea (Lin & Raghavan, 1991). The lateral roots are initiated as single, enlarged endodermal cells opposite the protoxylem poles of the main root tip. The mother cell of the lateral root undergoes a precise series of regular divisions to establish a new root apical cell. The root apical segments (merophytes) divide in a precise fashion to produce the precursors of the different tissue layers of the lateral root. The pericycle cells between the lateral root primordium and the parent root stele give rise to the vascular connection between the roots. Such detailed descriptive studies of histogenesis in fern organs could be the basis for future experimental studies of development at the cellular and tissue levels.

Shoot buds are formed on roots of some ferns. In Platycerium, shoots are initiated from cells close to the root apical initial but do not involve a direct transformation of root apex to shoot apex (Richards et al., 1983).

VII. Vascular Tissues

One major aspect of shoot structure that requires further study is the relationship between the vascularization of leaves and branches at the shoot tip and the organization of the vascular system in the stem. The dictyosteles of species of Diplazium and Blechnum have been found to show basic similarities to those of closed eusteles of seed plants (White & Weidlich, 1995). The major vascular bundles in the stems of these species can all be interpreted as being related to leaf vascularization. This observation is suggestive of the long-standing concept that "cauline" steles of fern shoots actually represent the proximal fusion of the leaf trace vascular bundles (e.g., Campbell, 1911, 1921).

The patterns formed by the protoxylem strands in the shoot are surprisingly variable among ferns (White, 1984). In some species there are well-developed systems of protoxylem strands that show eustele-like patterns related to leaf vascularization. In other ferns there are cauline protoxylem strands independent of those associated with the leaves, and there are also ferns in which typical protoxylem is restricted to the leaves or decurrent only a short distance into the stem (White, 1984; Ma & Steeves, 1994; Qiu et al., 1995). These different patterns are potentially significant both morphologically and systematically, but at present, insufficient data are available to draw any major conclusions.

A closely related area of investigation in which much more study is needed is the detailed examination of the developmental relationship between the formation of leaves and lateral buds at the shoot apex and the initiation and early differentiation of vascular tissue in the shoot (White, 1984). The development of the protoxylem strands in young sporophytes of tree ferns, for example, reveals that there is a close association between the development of vascular tissue and the leaf primordia in shoots of these species (White & Lucansky, unpubl. data).

The presence in some ferns of "precocious" strands of provascular tissue distal to all leaf primordia raises the question of the true nature of the relationship between leaf primordia and shoot vascularization. Observations in ferns appear to indicate a more complex causal relationship than one in which young leaves induce the formation of vascular strands in the stem or vice versa. Most observations to date indicate continuous, acropetal differentiation and maturation of vascular tissue in the fern shoot (Wardlaw, 1945; von Guttenberg, 1966; White, 1984; Ma & Steeves, 1994). However, a recent investigation of vascular development in Blechnum reports that vascular tissue is initiated first separately in the developing leaves and roots and that the stele becomes continuous by the subsequent basipetal development of interconnections among the strands (Gopalakrishnan & Nayar, 1990). This unusual observation needs further confirmation. It may well be that differences among workers in the criteria they use for the identification of differentiating meristematic tissue as "procambium" as opposed to "residual meristem" or "developing ground tissue" can lead to major differences in interpretation in such studies (e.g., Meicenheimer, 1986). For example, recent studies of vascular development in Matteuccia (Ma & Steeves, 1994, 1995) identify cells in the subsurface layer of the shoot apex itself as provascular tissue in early stages of differentiation. Genetic or biochemical markers, such as increased carboxylesterase activity (Ma & Steeves, 1995), may provide the first clear indications of the earliest vascular differentiation.

The effect of leaf primordia on cauline vascular development in Matteuccia has recently been investigated experimentally (Ma & Steeves, 1992). Shoot tips in which all leaf primordia were destroyed form a reduced, siphonostelic vascular cylinder without gaps. In this study it was found that replacing the primordia with auxin-containing anion exchange resin beads resulted in the formation of parenchymatous gaps in the stele, which also showed an increase in diameter. Thus, auxin from leaf primordia may affect the expansion of the shoot and the formation of stelar gaps rather than induce vascular tissue development in fern stems (Ma & Steeves, 1992). In intact shoots of this species, discrete groups of "leaf gap initials" interrupting the layer of developing vascular tissue were identified in association with even the youngest leaf primordia and may even precede leaf initiation (Ma & Steeves, 1994, 1995). This interpretation is compatible with the view that leaf-associated parenchyma development plays a major role in establishing the vascular pattern in Linum shoots (Meicenheimer, 1986).

The formation of rhizome-borne roots in ferns increasingly appears to be closely related to shoot vascular tissue patterns. Two distinct modes of vascularization of rhizome-borne roots in ferns have recently been characterized and differences in their development investigated (Chau, 1985). "Gradual" root vascular connections (described in Ophioglossum, Helminthostachys, and Woodwardia) are initiated in the apical region of the shoot, and provascular tissue and protoxylem are continuous between shoot and root. "Abrupt" root vascular connections (Botrychium, Osmunda) show no such continuity of procambium and protoxylem; they develop at levels where the vascular tissue of the stem is maturing or mature. Abrupt connections resemble main root-lateral root connections, whereas gradual connections are more similar to leaf traces. Gradual connections show surprising anatomical similarities to the root-shoot transition regions of seed plants. Stevenson (1976a) also described the initiation of roots and root traces close to the shoot apex in Dennstaedtia and the association of the roots with stelar perforations, or "root gaps."

Recent studies of vascular tissue development in Botrychium (Stevenson, 1980; Chau, 1986; Takahashi & Kato, 1988) have revealed strong similarities between the radially seriate xylem in the stem and the secondary xylem of gymnosperms. There is an identifiable cambium with both fusiform and ray initials, and although significant amounts of secondary xylem develop, no secondary phloem is formed. According to one recent study, the differentiation of the cambial initials resembles that in seed plants, although the cambium does not remain meristematically active for long (Soh & Kim, 1993). The tracheids have circular-bordered pits and cross-field pitting between tracheids and ray parenchyma cells. The stele is interpreted as similar to the eusteles of seed plants. The Ophioglossales have been regarded as "living progymnosperms," related to the seed plants rather than to other ferns (Takahashi & Kato, 1988). A similar interpretation has been made for the stem vascular tissue in Helminthostachys, although a typical cambium is lacking (Takahashi & Kato, 1990).

In recent decades there have continued to be numerous studies that give more or less detailed descriptions of the mature nodal (stelar) anatomy of the vascular systems in stems or petioles of many species of ferns. Similarly, various papers have described the tracheary elements of ferns. Such descriptive studies are potentially of comparative or systematic value but will not be considered further here.

Major progress has also been made in the study of the structure and development of pteridophyte phloem tissue, particularly at ultrastructural levels. This work has recently been reviewed (see Warmbrodt, 1980; Evert, 1984, 1990; Evert et al., 1989) and will not be treated further here.

One aspect of functional (physiological) anatomy of the ferns that has attracted considerable attention in recent years has been the flow of water in the xylem. Hydraulic conductance, which can be defined as the ease with which water flows through a structure, has been estimated for several species using calculations based on the numbers and dimensions of the conducting cells and measured using simple experimental techniques (Woodhouse & Nobel, 1982; Gibson et al., 1984, 1985a, 1985b; Calkin et al., 1985, 1986). It appears that the number and diameter of the tracheids in a fern leaf or stem largely determines the xylem water flow through the organ. Generally, the measured actual conductivities are only approximately half of the calculated estimates, a deviation similar in magnitude to that shown by conifers and dicots (Calkin et al., 1985). The biophysical model used by Calkin et al. (1986) indicates that in small tracheids most of the resistance to flow is from the cell lumen, whereas the pit membranes contribute most of the resistance in large tracheids.

Recently, the conductivity of stems and leaf axes in four species of Blechnum and the closely related Salpichlaena volubilis were examined in order to study the relationship of conductivity to shoot morphology and tracheid characteristics (Veres, 1990). Stems were found to have larger hydraulic conductivities but smaller leaf-specific conductivities (LSCs, conductivity per leaf area supplied) than stipes. Short, upright stems have small conductivities and small LSCs. Elongate organs tend to show large conductivities and large LSCs. Tracheid diameter and length, pit aperture size, and the length of the tapered end of the tracheid were the tracheid characteristics most affecting conductivity. The stipes of the climbing leaves of S. volubilis have large conductivities associated with tracheids of very large dimensions (some [greater than]200 [[micro]meter] diam. and [greater than]4 cm long) and large numbers of tracheids.

The use of magnetic resonance imaging as a technique to examine water movements among different tissues and stem regions of intact, living ferns has also been explored (Veres et al., 1991). This method shows promise as a noninvasive method of looking at tissue changes during periods of water stress and rehydration of living plants.

Ferns appear to be functionally quite different from seed plants, with whole-plant conductivities up to several orders of magnitude lower. Woodhouse and Nobel (1982) suggest that the presence of tracheids rather than vessels, the relatively small numbers of tracheids, and the lack of secondary xylem restrict most ferns to being short in stature or slow growing.

VIII. Concluding Remarks

As detailed above, recent progress has contributed to a better understanding of the structure and development of the fern sporophyte. It is clear, however, that much more work can be done on these and related subjects. In particular, such areas as fern shoot and root apical meristems, where researchers have gained a much clearer idea of organization and functioning, are now suitable subjects for more detailed descriptive analysis and more sophisticated experimental manipulation.

It is anticipated that future research will increasingly emphasize more experimental approaches to the study of fern morphogenesis, including detailed investigations of the ultrastructure and molecular cell biology of development. Such studies may well help clarify questions regarding the underlying mechanisms that control development, issues that are as central to studies of organization in ferns as they are for other organisms. For example, future research may identify the mechanisms whereby an apical cell maintains its identity as it continues to form derivatives in a regular segmentation pattern. Similarly, the initiation of new organs and new apical cells and the coordinated changes among zones of meristematic cells during histogenesis and differentiation are particularly promising areas for intensive study.

Shoot organization and phyllotaxy, leaf initiation, and the development of cauline vascular tissue are complex, interrelated phenomena. These must be investigated at the cellular and histological levels as well as at the organ or primordium level and at the whole-plant level.

Despite the obvious value of experimental approaches, there is a continuing need for descriptive studies of structure and development in ferns. Detailed observations may lead to new hypotheses about developmental rules and possible mechanisms, and thus may lead to further, experimental investigations. A clear understanding of the normal pattern of development is necessary for both the proper design of experiments and the correct interpretation of their results. Eventually, these studies may lead to a more complete understanding of the processes that operate at levels between the gene and the whole organism.

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Title Annotation:Interpreting Botanical Progress
Author:White, Richard A.; Turner, Melvin D.
Publication:The Botanical Review
Date:Oct 1, 1995
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