Botanical Journal of the Linnean Society, 72: 115‑148. With 8
plates and 3 figures
Reproduced here with the
permission of the author
The floral anatomy of Victoria Schomb.
E. L. SCHNEIDER
OBSERVATIONS – Continued
Various aspects of organogenesis and histogenesis
Studies dealing with the various aspects of early floral development in Victoria are sparse in the literature. Troll (1933) described the early development of the gynoecium and Knoch, in his work of 1899, described in some detail the various aspects of organogenesis that are to be considered here. Knoch's descriptions are essentially accurate, but are old and in need of further amplification and reinterpretation in light of modern morphological concepts.
In Victoria, the shoot apical meristem exhibits indeterminate growth and gives rise to both floral and leaf primordia laterally; each of these groups of organ primordia is in a separate genetic helix. Cutter (1961) described and illustrated both the spatial and temporal relationships between the inception of leaf and flower primordia from the shoot (rhizome) apex in Victoria. As she noted, each flower has its inception to the anodic (left) side in the axil of an older leaf and that adaxial to each floral primordium is the primordium of a younger leaf (Plate 5A).
In attempting to obtain longitudinal sections of early floral primordia, median sections of the rhizome apex were obtained. In the (rhizome) apex a uniseriate tunica (t) is observed (Plate 5B). All rhizome apices observed were broad (0.5 mm) and revealed fairly clear cytohistological zonation in the form of a peripheral meristem, a pith or central meristem, and a broad homogeneous central cluster of subapical initials. The first indication of leaf or flower inception is the occurrence of periclinal divisions in the C1 and C2 layers of the peripheral meristem to one side of the apex. At this stage, there are no discernible differences between leaf or floral primordia. Additional divisions in the C3, C4 and possibly C5 peripheral meristem layers follow, and these divisions, accompanied by anticlinal divisions in the protoderm, account for cylindrical leaf and floral primordia. Once the primordia have been established, differential asymmetrical growth makes the leaf primordia easily distinguishable from the cylindrical shape retained by the floral primordia (Plate 5C).
Once established, the meristem of the young floral primordium weakly demonstrates, in smaller proportion, the cytological organization found in the rhizome apex. No bracts were observed on the floral axis such as those which occur in species of Nuphar (Moseley, 197 1).
The first primordium to appear from the floral apex is that of the anterior sepal (i.e. the sepal abaxial to the shoot apex (Plate 5D)). After the initiation of the anterior sepal, the two lateral sepals arise simultaneously, followed by the posterior sepal. The sepals are formed, then, as are the other floral organs, in a greatly suppressed helical anthotaxy and in a modified acropetal sequence.
The initiation of each sepal occurs in the same fashion. Anticlinal divisions of the protodermal layer are accompanied by periclinal divisions in the C1 and C2 layers. Repeated divisions of cells formed by the initiating divisions soon give the appearance of a raised subspherical primordium, which soon elongates through the activity of subapical cells which act as initials. Further growth in the sepals, although apparently diffuse, has not been studied here.
Following sepal initiations, the floral meristem becomes momentarily dome‑shaped (Plate 6A), and meristematic activity is greatest within this region. Then five or six helices of petals are initiated in acropetal sequence. During the inception of these floral organs, the floral apex increases in diameter and becomes temporarily flattened (Plate 6B). Coinciding with this flattening, cytological zonation becomes obscured. Noticeably, the peripheral and central meristematic regions become less clearly defined in such a manner that differences are essentially eliminated and the entire region below the structurally unaltered tunica appears homogeneous.
The initiation of each petal is similar to that of a sepal. The tunica (protodermal) layer divides anticlinally; the first and second layers of the subtunica (Cl and C2) divide periclinally. The petal protuberance then appears subspherical and develops similarly to the sepals, with maturation occurring in acropetal sequence (Plate 6B).
Following the inception of the innermost petal, a striking transformation occurs in the homogeneous layer. The cells become enlarged, highly vacuolated and at least momentarily quiescent (Plate 6C). As this occurs, the meristematic activity shifts centrifugally and forms an intercalary meristematic ring which completely surrounds the now quiescent floral apex. Prior to, and during this shift in meristematic activity, correlated changes occur within both the receptacular region and the floral axis (peduncle). Diffuse cell division and cellular enlargement in the receptacle continues (cf. Plates 5C and 6A) and procambial differentiation becomes clear. In the floral axis, schizogenous formation of air canals begins, and the incipient establishment of the basal intercalary meristem of the peduncle is evident.
As activity continues within the intercalary ring meristem, a 'cup‑shaped' meristematic tissue region appears and, while it enlarges, six or seven helices of appendicular organs (i.e. outer staminodia, stamens and inner staminodia, respectively) are initiated (Plate 6D). The initiation of these floral organs appears to be basipetal; that is, at any instant during their development, older organs will be found (Plates 6D and 7A), toward the rim of the cup and younger ones closer to the bottom of the cup and the quiescent apex. Morphologically, however, these appendages arise in an acropetal sequence in reference to the original floral apical meristem; hence, the manner of organogenesis is similar to that in hypogynous flowers with acropetal initiation and maturation of floral parts. In section (Plate 7A), the meristematic cup appears as a shallow, ill‑defined mantle of dark‑staining cells approximately three or four cell‑layers in depth. This meristematic mantle is not, however, so clearly defined as the mantle forms described in the hypogynous flowers of Aquilegia (Tepfer, 195 3) and Nuphar (Moseley, 197 1) or the epigynous flowers of Downingia (Kaplan, 1967). Furthermore, the transition to the mantle organization seems to be very gradual, and of longer duration in Victoria than in the preceding genera. Whether this should be interpreted as (i) specialized with regard to the aquatic habitat, rapid growth, large size and developmental architecture (epigyny) or (ii) a primitive feature is not known. Although cytological zonation within the meristematic mantle is not recognizable, stratification is present. The outer mantle layer (tunica) is continuous with the protoderm of the earlier‑formed organs and undergoes only anticlinal divisions. The second layer of the mantle (M1) is a fairly discrete cell layer which undergoes predominantly anticlinal divisions, except possibly at the site of organ initiation. Beneath these two layers are the third (M2) and fourth (M3) strata of cells. The initiation of the outer staminodia, stamens, and inner staminodia (Plate 7A) involves anticlinal divisions of the tunica layer (T) accompanied by both anticlinal and periclinal divisions of the third and fourth (M2 and M3) layers.
From the onset of staminal initiation, the enlarged, vacuolated cells of the original floral meristem reestablish their meristematic activity. Such activity is restricted to this region and is not involved in the initiation or formation of the gynoecium. These meristematic cells function as an intercalary meristem and raise the original floral apex extremely rapidly (cf. Plates 6D and 7B, C) to a position which is temporarily above the points of attachment of all floral organs. This floral apex at maturity assumes a conical shape and is found projecting from the centre of the stigmatic cup in the mature flower (Plate 2B, Fig. 1). Following the inception and establishment of the innermost staminodia, differential growth of the surrounding tissues, as well as the continued activity of the intercalary ring meristem, raises these organs so that they appear to be 'pushed' to the top of, and eventually over, the rim of the cup (cf. Plates 6D and 7B, C). As the staminal organs are elevated by the activity of the ring meristem, radiating ridges become distinguishable around the inner portions of the cup (Plate 7B). These radiating ridges, derived from periclinal divisions of the second, third and fourth (M2, M3 and M4) layers of the mantle, are the sites of gynoecial initiation. Each ridge, which is separated from adjacent ones by narrow shallow intercarpellary grooves, initially has the mantle organization. From the radiating ridges arise the stylar processes, the stigmatic regions, the distal ventral carpellary regions and the distal locular regions, in acropetal sequence (Plate 7C). As these portions of the gynoecium differentiate, the meristematic activity becomes restricted to the lowermost inner and chronologically older portions (bottom) of the cup. This general pattern of floral development and gynoecial differentiation in Victoria (Fig. 2) closely resembles that which occurs in Nymphaea (Syncarpiae) as described by Moseley (1961). Development of the gynoecium from this stage onwards is less well understood; but apparently, once the distal portions of the locules are initiated, the locular regions become extended basipetally by the differentiation of primary meristematic tissue (Esau, 1965) which is derived from the ring meristem (Plate 7C, Fig. 2). As the gynoeciurn differentiates further, it does so in an integrated manner with both the associated peripheral vascular strands and the ground tissue. In Victoria, as in Nymphaea (Moseley, 1961), there is no postgenital adnation of the carpels to the receptacular central core, or of the appendicular organs to the gynoecium.
Troll considered the entire locular region of Victoria to be formed basally from the radiating meristematic ridges, which he considered to be carpel primordia. He also interpreted the locular region of Nymphaea to be formed in the same manner. As Moseley (1961) has pointed out, however, the locular region is not entirely produced by the radiating ridges but only initiated by them. This point must not be misinterpreted. The radiating ridges develop from the circular promeristem. The radiating ridges then initiate locular formation, but the locular regions develop basipetally from the circular promeristem. Once the locular region is established, then development of the gynoeciurn is essentially acropetal.
Victoria is syncarpous, at least basally, and the carpels are adnate to the central receptacular floral apex. In the basal region, there is no indication of phyletic or post‑genital fusion between adjacent carpels. The connation of carpels is congenital and complete, except for the adaxial grooves which are present throughout development; hence there is no indication of apocarpy (i.e. intercarpellary spaces) as believed by Troll. In the more distal portions of the gynoecium, however, indication that phyletic fusion has occurred between adjacent septa is present in the form of fused epidermes. This fusion of septa is present from the first and is not postgenital.
In the basal portions of the stigmatic
cup, the ventral carpellary surfaces are initially apposed but not fused
The apposition of ventral surfaces is extensive and involves numerous cells. In
the more distal carpellary regions, it is difficult to ascertain whether or not
the carpels are initially open. There is little doubt, however, that in this
region the ventral surfaces are, at least to varying degrees, less tightly
apposed than in the basal portion.
The cell layers which are involved in the initiation of the appendicular organs also contribute to the formation of the compact parenchymatous sheath (Plates 2B and 7B, D; Fig.1) which is found associated with, and peripheral to, the procambial (i.e. gynoecial) strands. Ontogenetic evidence that this parenchymatous sheath is totally appendicular (i.e. that it represents the congenitally fused bases of the appendicular organs), such as that which occurs in certain Ericaceous flowers (Eames, 1931; Palser, 1951, 1954; Douglas, 1957), is lacking. It is not, however, totally receptacular, such as the type reported in Calycanthus (Dengler, 1972), Rosa (Jackson, 1934), Pereskia (Sharma, 1949), certain genera of the Santalaceae, e.g. Darbya (Smith & Smith, 1942a,b), and the Cactaceae (Leinfellner, 1941; Boke, 1964). In Victoria, diffuse zonal growth (Puri, 1952) occurs outside the floral stele (procambium) and does not form an inner inverted strand as described in these other genera. Rather, it involves both the primary meristematic tissue formed from the promeristematic cup and the primary meristematic tissue formed outside the procambial strands (i.e. receptacular cortical tissue) by the original floral promeristem. This accounts for an outer ovary wall which is composed of both appendicular and some receptacular tissue in the more proximal region.
That growth proceeds at different rates during the development of different parts of the gynoecium is evident in the mature form. Initially, the locules have a greater vertical dimension than a radial one and the future stigmatic surface is nearly vertical (Plate 7C). As growth proceeds, the radial or centrifugal growth within the carpellary (gynoecial) region becomes greater than the circumferential growth. Vertical growth and circumferential growth are, of course, greater in the peripheral region of the gynoecium than further in. This accounts for the sloping wedge‑shaped locules, which are narrow tangentially but broad radially and vertically (cf. Plates 3D and 7C, D). It is also responsible for the configuration of the stigmatic cup. In V. cruziana the stigmatic cup acquires a gentle funnel‑shaped slope from the projecting floral apex to the bases of the stylar processes. In V. amazonica, however, this gradual slope is proximally 'humped'. The 'hump' conforms to the enlarged upper centripetal portion of the locule.
Viewed longitudinally and in
7D), the outer portions of the locule in Victoria are seen to be more vertically extended, both distally and
proximally, than the inner ones. This is in contrast to the profiles exhibited
in Nuphar, Nymphaea and Euryale, although the last genus shows
interesting transitions between that found in the former two genera and Victoria. This profile is best
correlated with the early repression of apical growth and change to the
peripheral region of the flower, and the associated distal elaboration of both
the carpellary region and the appendicular organs. Although gynoecial
initiation is highly synchronized, growth proceeds at a greater rate in the
locular regions than in the more distal carpellary regions. As a consequence of
this differential growth, the locular region is first to be fully formed, then
the stigmatic region and the stylar processes follow respectively. The adnate
stylar processes develop acropetally and at maturity are long and laterally
compressed. Basally, these structures are broad and fleshy, but during their
development, hyponastic growth occurs and the upper portions become incurved
and arch horizontally, along with the inner staminodia, over the stigmatic cup.
At maturity, the cells of the stylar processes contain an abundant quantity of granular starch in
addition to dextrose (Knoch, 1899).
During the early development of the gynoecium, the surfaces of the locular region, the ventral surfaces and the future stigmatic region are continuous and outlined as a highly meristematic protoderm layer. Beneath the locular protoderm layer are at least two additional layers from which the ovules are initiated centrifugally along the lateral walls. Their initiation occurs when the locular region is incompletely formed and continues as the locular region expands radially and vertically. The initiation of a single ovule starts with a periclinal division of a cell in the second and probably the third layer below the protoderm. Subsequent divisions result in a funicular protuberance which projects downward and from which the ovule proper arises. By the time of anthesis, each ovule is anatropous with the curvature occurring at the tip of the funiculus (Plate 8A). Further aspects of ovule development and embryology have previously been investigated (Khanna, 1967) and will not be discussed here.
In Victoria, the stigmatic tissue is functionally related to the laminar placentation and to the morphological structure of the gynoecium. Morphologically, the stigmatic tissue occupies the free distal surface of the syncarpous gynoecium (Plate 2B, Fig. 1), extending from the projecting floral axis to the bases of the stylar processes. This tissue develops from the highly meristematic protodermal layer which is present in the early stages of gynoecial development and which is continuous with the protoderm of the appressed ventral carpellary surfaces and the inner surface of each locule. During floral development those protodermal cells which cover the surface of the future stigmatic cup undergo repeated periclinal divisions, with subsequent strong cellular elongation of at least the outermost layer and sometimes the immediately underlying layer. These periclinal divisions occur, however, in discontinuous irregular patches and make the stigmatic surface, at maturity, appear bumpy (Plate 8B). During their development, these patches are compact, not separated into epidermal columns as they are initially in Nuphar and Nymphaea. As in Nuphar and Nymphaea, however, the periclinal divisions are greatest along the free marginal crests of each carpel and less frequent or absent along the apposed ventral surfaces as well as over the region where the dorsal carpellary surfaces have phylogenetically fused. This gives the appearance at maturity of raised double ridges alternating with shallow grooves, both of which extend radially from the floral apex to the carpellary processes. The outermost terminal cell of the stigmatic tissue, whether raised by periclinal divisions or not, is always elongated. The outermost free wall of these cells is variable in shape, typically low mounded or ill‑defined papillose. These cells are best considered secretory, for, prior to anthesis, a mucilaginous substance can be found covering the entire stigmatic cup. In mature flowers and fruits numerous pollen grains were observed adhering to this substance.
The protodermal cells of the appressed ventral carpellary surfaces, as well as those lining each locule, undergo a similar development. Prior to pollination and concomitant with the development of the stigmatic tissue, each protodermal cell elongates perpendicular to the appressed or free (locular) surface. In comparison with the development of the stigmatic tissue, the elongation is not, typically, preceded by periclinal divisions. The elongation is not regular, however, since some of the cells either enlarge unevenly or elongate more than their neighbouring cells. As this irregular elongation and enlargement of the protodermal cells continues, the ventral carpellary surfaces become irregularly appressed, creating separated regions. Following the separation, a mucilaginous substance, similar to that which occurs on the stigmatic surface, is secreted into the separated regions (Plate 8C). It is difficult to ascertain whether this secretion is 'intracellular', such as the type which occurs in Nuphar (Moseley, 1965), or strictly intercellular; nevertheless, mucilage production and secretion continues until each locule becomes full and the now irregularly appressed ventral surfaces become lined with mucilaginous material. Since the mucilaginous material is similar to the material observed on the surface of the stigmatic cup and is produced from structurally similar cells which are continuous with the stigmatic tissue, the cells must be regarded as integral portions of the transmitting tissue (Eames, 1961).