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Structure and Development |
Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh EH3 5LR, UK
Received for publication July 9, 2004. Accepted for publication January 5, 2005.
ABSTRACT
Molecular phylogenies have associated Bataceae with Salvadoraceae and Koeberliniaceae in an expanded Brassicales. Despite a long taxonomic history, the knowledge of the flower of Batis is still fragmentary. The floral development of pistillate and staminate inflorescences of Batis maritima was investigated to understand homologies of floral structures and to discuss the phylogenetic position of Bataceae within the Brassicales. There has been considerable controversy in the past about the male flower, especially on the nature of the petals and the tubular structure enclosing the flower. Developmental evidence confirms that the male flower is built on a basic tetramerous bauplan and that the tubular structure is derived from four congenitally fused sepal lobes with the three anterior lobes highly reduced. The development of petals and stamens is unidirectional, and the androecium initiates the median stamens before the lateral stamens, suggesting the existence of two whorls. The pistillate flowers are reduced to the bare minimum with two transversal carpels enclosed by a bract. Partial inflorescences function as a swollen dispersal unit. The vestigial stipules probably represent colleters and are not homologous with true stipules. Several characters of Batis are reminiscent of the Brassicaceae, although a link with Salvadoraceae and Koeberliniaceae cannot be excluded.
Key Words: Brassicales • dioecy • floral ontogeny • Gyrostemonaceae • flower structure • phylogeny • reduction • stipules
Batis (with two species) and Gyrostemonaceae have traditionally been related to Centrospermae (e.g., Kunth, 1817
; Chant, 1978
) on the basis of misleading homoplasies, such as adaptations to similar coastal habitats as Chenopodiaceae and the sharing of a similar habit. However, the position of Batis was repeatedly questioned, without convincing argumentation. Batis has been associated with following families and orders: Chenopodiaceae, Coniferae, Ephedraceae, Phytolaccaceae, Amaranthaceae, Polygonaceae, Gyrostemonaceae, Salicaceae, Podostemonaceae, Urticaceae, Empetraceae, Verbenaceae, Hamamelidaceae, Juglandaceae, Fagales, and Rhoeadales (Brassicales); details are given by Uphof (1930)
, Johnson (1935)
, and Eckardt (1959)
. Bataceae was often placed—with or without Gyrostemonaceae—in a separate order Bat(id)ales to stress its differences with the other families of the Centrospermae (e.g., Eckardt, 1964
; Chant, 1978
; Cronquist, 1981
; Takhtajan, 1997
). In the seventies, Mabry and coworkers (e.g., Mabry, 1977
) convincingly demonstrated that both Bataceae and Gyrostemonaceae did not share the biochemical and micromorphological characteristics of the Centrospermae (e.g., betalains, sieve-element plastids, palynology). The discovery of glucosinolates and myrosin cells in both families led to their association with Capparales, first by Ettlinger and Kjaer (1968)
and Dahlgren (1977)
, and this was later confirmed by molecular studies on the chloroplast genome (Rodman et al., 1993
, 1996
, 1998
). However, in these studies there is no evidence, neither molecular nor morphological, for a close association of Bataceae and Gyrostemonaceae. Batis was associated with Salvadoraceae and Koeberliniaceae in a separate clade, and Gyrostemonaceae was placed in the core Capparales in close affinity with Resedaceae. Pulle (1952)
and Eckardt (1959)
had already suggested a link of Batis with the Brassicaceae on morphological grounds, such as the diagonal position of "petals" in the staminate flowers, the two transverse carpels with false septa in the pistillate flowers, and the presence of rudimentary stipules. Takhtajan (1997)
preferred to retain Bataceae in a monotypic Batales close to Capparales.
Batis is a curious genus of two species, having highly distinctive staminate and pistillate flowers. Batis maritima differs from B. argillicola in a number of features such as being dioecious vs. monoecious, in the absence vs. presence of short axes bearing the flowers, and in the resemblance of bracts to vegetative leaves in the latter (van Royen, 1956
; Eckardt, 1959
). B. argillicola is restricted to New Guinea and Australia, while B. maritima occurs in the New World (sub)tropics.
Both staminate and pistillate flowers of Batis are highly reduced. Staminate flowers are enclosed in bud by a large tubular structure that ruptures apically at anthesis, four diagonally inserted petaloid appendages, and four stamens alternating with the petals (Fig. 32). A pistillode is absent or is represented by a small conelike protuberance. Pistillate flowers consist of two short styles with a mass of papillate trichomes; the main body of the flowers is embedded and indistinguishable from the mass of the inflorescence. Line drawings of mature flowers are given in Eckardt (1964)
and Cronquist (1981)
.
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—represents a calyx (e.g., Torrey, 1853
; Payer, 1858
; Dammer, 1893
; Johnson, 1935
; Takhtajan, 1997
), while others maintained that it represents a bract (e.g., van Tieghem, 1903
) or a variable number of bracteoles (van Heel, 1958
; Eckardt, 1959
). The four stamens alternate with four whitish spathulate appendages, variously called petals (e.g., Torrey, 1853
), staminodia (Dammer, 1893
; Johnson, 1935
), tepals (van Heel, 1958
; Cronquist, 1981
), or an extrastaminal disk (van Tieghem, 1903
). The interpretation of the androecium is also controversial. Van Tieghem stated that the stamens are inserted in two dimerous whorls (diplostemony), while others maintain that there is only one whorl of four stamens (haplostemony). There is unanimity, however, between authors that the pistillate flower represents a naked structure made up of two carpels and four ovules separated by false septa.
The questions about the nature of the floral organs in the staminate flowers necessitate a new in-depth investigation of the development of the flower, as they relate to characters that have much systematic value. Johnson (1935)
studied the development of staminate inflorescences of Batis maritima using serial microtome sections. The scanning electron microscope (SEM) permits a much more detailed investigation of the development of the inflorescence. This study aims to fill the gaps and provide more evidence for the position of Bataceae in the Brassicales.
MATERIALS AND METHODS
Flower buds of pistillate and staminate plants of Batis maritima L. were collected in April 2003 in the same location, growing in a disturbed mangrove area on the southern shore of Caye Caulker off the mainland of Belize. Material was fixed in a mixture of 85 cc 70% alcohol, 5 cc formaldehyde and 10 cc acetic acid (FAA) and later transferred to 70% ethanol. Inflorescence buds were dissected under a Wild MZ8 stereomicroscope (Leica, Wetzlar, Germany), dehydrated in an absolute ethanol and acetone series, and critical point dried with a K850 Critical Point Dryer (Emitech Ltd, Ashford, Kent, UK). Material was coated with platinum using a K575X sputter coater (Emitech Ltd) and observed with a Supra 55VP SEM (LEO Electron Microscopy Ltd, Cambridge, UK). Reference material (871 La, 872 La) as well as herbarium specimens (Ronse De Craene 1447, 1448) are kept at RBGE.
RESULTS
Batis maritima is an annual subshrub of mangroves and tidal coastal sands. Fleshy, strongly branching axes form prostrate mats and the inflorescences are erect, rather like Suaeda (Chenopodiaceae). Staminate and pistillate inflorescences are borne on separate plants and resemble each other in being spike-like and (sub)terminal. The arrangement of leaves and inflorescences is strictly decussate. Leaves as well as inflorescence bracts bear small appendages described as stipules, but reminiscent of colleters. On mature leaves these are minute and drop off easily.
Staminate inflorescence
Bracts are the first organs to emerge on the inflorescence apical meristem. Bract primordia are globular at first but they become rapidly dorsiventrally flattened and triangular (Fig. 2). Two small lateral appendages, colleters, appear when bract primordia are well differentiated and have produced an elliptical primordium in their axil (Figs. 2, 3 [arrows], 4, 5, 7, 8). The appendages grow during the development of bracts and attain a size of about 50 µm in diameter; they appear to be secretory. As the flower primordium develops the appendages are pushed to the adaxial side against the inflorescence axis while they remain connected with the bract (Figs. 1, 2, 3, 7, 8). The flowers consequently appear to be inserted on the bract. Flowers are initiated as ellipsoidal primordia and are tightly pressed between bract and inflorescence axis (Figs. 1–5). As a result the flowers develop in an angle of 90° to the inflorescence axis, almost in a vertical plane (Fig. 3). The pressure of the bracts, as well as gravity, influence the sequence of initiation and maturation of organs in the flower. Flowers become rapidly triangular in shape by extensive upward growth of the topside of the flower (Figs. 1, 2, 5 [left flower]). The apical part (morphologically the adaxial side) is pressed against the bract above, leading to a trapezoid shape (Figs. 2, 3, 5). A transversal furrow appears in the upper third of the flower separating the upper outgrowth from the rest of the flower (Figs. 1, 4, 5). The furrow deepens and the surrounding tissue extends in both adaxial and abaxial directions so that a continuous rim is differentiated. The upper lip, representing the adaxial side, grows as a caplike hood while the abaxial lower side of the flower does not extend much in size. The lower lip of the flower appears weakly two-lobed (Figs. 6, 7); in older buds a third lobe is visible between the two initial lobes (Figs. 8, 9). The lower lip occasionally shows no differentiation of lobes (Fig. 3). In older stages the lobes on the lower lip are undistinguishable (Figs. 11, 12, 17). This tubular structure eventually forms a sheath, an organ of dubious affinity, which acts as a calyx and protects the rest of the flower (Figs. 1, 2, 4, 11, 17, 22). By continuous marginal growth the rim eventually encloses the central part of the flower and remains visible as a narrow transversal slit (Figs. 4, 8, 11). During further development of the flower the sheath attains considerable size and resembles a mitre (Figs. 11, 17). A second furrow is delimited along the apical margin of the sheath, and the flower opens by the irregular splitting of this zone in four unequal lobes (Figs. 11, 22). The tubular sheath has to be removed cautiously to reveal the inner organs. On a rectangular floral primordium two large petal primordia are differentiated in the upper corners in a rapid sequence, followed by two lower primordia (Figs. 9, 10, 12). Petal primordia grow rapidly and the upper primordia enclose the lower in an imbricate descending aestivation (Figs. 11, 20, 32). At later stages the petal lobes become lifted by the development of a basal claw—mature petals are conspicuously clawed organs (Fig. 24).
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Pistillate inflorescence
Pistillate inflorescences appear as compact flattened units; flowers are embedded in the tissue of the inflorescence, comparable to a pineapple, and consist of two lateral appendages enclosing a central slit leading to an inferior ovary. Boat-shaped inflorescences arise in alternating pairs in the axil of bracts on a main growing axis; lower or higher on the main stem vegetative growth apices are differentiated (Fig. 25). Vegetative leaves as well as outer bracts of the partial inflorescences bear lateral colleter-like structures identical to the staminate inflorescences, but these are absent from fertile bracts on the inflorescences (Figs. 25–29). The bracts drop off rapidly and a scar remains visible on the inflorescence (Figs. 26–29). Two lateral appendages are initiated in the axil of bracts arising pairwise in the same sequence as on staminate inflorescences (Figs. 26–29). The appendages, representing carpel primordial, grow as two transversal crescents enclosing a slit (Figs. 25–27). They remain free from each other and differentiate marginal hairs acting as a stigmatic surface (Fig. 27). While the lower part of the inflorescence is inflated with fully embedded gynoecia the top of the inflorescence bears only sterile bracts (Figs. 26, 29).
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DISCUSSION
The lateral appendages on leaves and bracts of Batis have been described as vestigial stipules (e.g., Johnson, 1935
; van Heel, 1958
; Eckardt, 1959
, 1964
; Cronquist, 1981
; Takhtajan, 1997
) while other authors have reported them to be absent (van Tieghem, 1903
). They remain small, wither at maturity, and are easily overlooked. In a number of genera of Brassicales having rudimentary stipules (e.g., Pentadiplandra, Tovaria), the stipules emerge simultaneously with the middle part of the leaves and are initially much larger than the leaf lamina (Ronse De Craene, 2002
). In Batis the stipules arise after the initiation of the leaf or bract and remain always smaller than the leaves. They are reminiscent of colleters that, as hinted by Johnson (1935)
in his description, have an obvious function in keeping the buds sufficiently moist during early development. They resemble the colleters found in Caricaceae, which occupy the position of stipules and are probably phylogenetically linked with stipules (Ronse De Craene and Smets, 1999
). Dickison and Rutishauser (1990)
demonstrate the serial link between fully developed stipules and their replacement by colleters in Cunoniaceae. A similar trend exists in Rubiaceae (L. Ronse De Craene, unpublished data).
Table 1 gives a comparative list of characters of Bataceae and putatively related families. Bataceae show an extreme dimorphism between staminate and pistillate flowers. The central cone of the staminate flower may represent a vestigial gynoecium (Fig. 18; "cone obtus": van Tieghem, 1903
). There are no remains of stamens in the pistillate flowers. Similar cases of extreme dimorphism have arisen on a few occasions in the Brassicales, such as Caricaceae (Ronse De Craene and Smets, 1999
) or Gyrostemonaceae (Eckardt, 1971
; Hufford, 1996
). The pistillate flowers of Batis show an extreme reduction linked with wind pollination: pistillate inflorescences act as units for pollen reception, providing several receptors over their surface, and function as units for dispersal, probably using sea currents and tides.
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, using microtome section series. His description of successive organ initiation is accurate for the development of the tubular envelope; he also described the development of a circular primordium enclosing the bud along a median line. The resulting two lips are unequal, the upper with a long crest, and the dehiscence of the tubular envelope at maturity is through a new rupture in the upper lobe.
Different interpretations have been given for the structure enclosing the flower. Torrey (1853)
, Payer (1858)
, Dammer (1893)
, and Johnson (1935)
considered the tubular envelope to be a calyx, consisting of one or two median sepals. For other authors the tubular envelope represents a spathe-like circular phyllome (van Tieghem, 1903
), a single bract (Eckardt, 1959
), or two or more bracteoles (van Heel, 1958
; Eckardt, 1964
). Evidence for a single appendage was sought in the single adaxial vascular bundle supplying the perianth (e.g., van Tieghem, 1903
; Johnson, 1935
), although van Heel (1958)
reports the presence of a vascular bundle in each of the halves of the circular phyllome of Batis argillicola. The interpretation of the envelope as a circular phyllome or bracteoles is difficult to support, as these are absent in pistillate flowers and in the closest relatives of Batis, Salvadoraceae and Koeberliniaceae. The interpretation of the tubular envelope as a calyx makes more sense. Apart from the vasculature, there is no evidence to suggest that it represents a single organ. Besides the development of a large apical lip, the lower lip consists of 2–3 slightly oblique lobes, as could be recognized in a number of buds (Figs. 6–9). This suggests the existence of at least 3–4 organs, and it can be postulated that the lateral and abaxial lobes have been reduced in evolution and occasionally do not arise at all. The conspicuous unidirectional development of the flower, linked with its near-vertical insertion, favors the development of the adaxial side over the abaxial and it is the upper, more developed side only that has a vascular connection to the inflorescence axis. The three lower lobes, or by concrescence the single median lobe, are to be interpreted as originally two lateral and one median sepal, linking the perianth to an originally tetramerous plan (Fig. 32). In Batis argillicola the tubular envelope is occasionally four- or three-lobed (van Heel, 1958
).
The whorl outside the stamens has been variously interpreted as petals (Torrey, 1853
; Payer, 1858
; Bayer and Appel, 2002
), staminodes (Dammer, 1893
; Johnson, 1935
; Eckardt, 1959
), tepals (van Heel, 1958
; Cronquist, 1981
), or an extrastaminal disk (Van Tieghem, 1903
). Van Tieghem (1903)
does not provide much evidence in favor of the interpretation of the "petals" as flattened emergences forming scales of an extrastaminal disk. A disc commonly arises late in ontogeny, and the floral development of Batis maritima clearly demonstrates the early initiation and differentiation of a whorl of well-differentiated organs. The spathulate shape of the organs surrounding the stamens may be supportive of the interpretation of the organs as staminodes. However, staminodial structures commonly have a retarded development compared to stamens. The presence of a single vascular bundle (occasionally in B. maritima: Eckardt, 1959
; always in B. argillicola: van Heel, 1958
) and their earlier initiation are further arguments for considering the appendages as true petals. In my opinion the organs are best interpreted as petals by their position, their initiation sequence and rapid growth, and their aestivation and development of a claw, which is commonly found in the Brassicales.
Flowers with a unidirectional initiation generally develop from the adaxial to the abaxial side within each whorl or from the abaxial to the adaxial side (e.g., Tucker, 1984
, 1999
). Like Batis, unidirectional initiation of organs also proceeds from the adaxial to the abaxial side in Resedaceae (Sobick, 1983
) and Cleomaceae (Erbar and Leins, 1997a
). However, contrary to the unidirectional initiation expected within a single whorl, both median stamens appear before the transversal stamens in Batis. Although all stamens attain an almost equal size, their initiation appears as two whorls, supporting the interpretation of van Tieghem. The stamen arrangement is reminiscent of that of certain Brassicaceae and Cleomaceae with only four stamens, the inner whorl being replaced by two single stamens instead of four in a distinct 2 + 4 pattern (Endress, 1992
; Erbar and Leins, 1997b
; Bowman and Smyth, 1998
).
Affinities of Bataceae
Phylogenetic studies based on morphological data (Rodman, 1991
) as well as rbcL and 18s RNA (Rodman et al., 1996
, 1998
), have consistently placed Batis as sister to Salvadoraceae with strong bootstrap support, within a clade with Koeberlinia as sister group. A combined morphological and molecular analysis obtained the same clade (L. Ronse De Craene and E. Haston, unpublished data). Synapomorphies for the Koeberlinia-Batis-Salvadora clade are the tetramerous flowers, suggesting an independent origin of tetramery for this clade, and bicarpellate gynoecium. Batis and Salvadora also share axial parenchyma bands, wide, multiseriate rays, non bordered perforation plates, unilacunar nodes with two traces, opposite leaves with colleters or reduced stipules, a micropyle formed by the inner integument, and a straight embryo (Johnson, 1935
; Carlquist, 1978
, 2002
; Kubitzki, 2003
). However, the spongy ektexine in the pollen of Batis is not found in Salvadoraceae and Koeberlinia (Tobe and Takahashi, 1995
). A further study of the rudimentary stipules of Salvadoraceae should be carried out. Characters shared between Batis and Brassicaceae are: contorted petals, two transverse carpels with parietal placentation and a false septum, and disymmetric flowers (Table 1).
Van Tieghem (1903)
interpreted the androecium of Batis as made up of two dimerous whorls, and this is what the ontogeny suggests. Flowers of Batis are disymmetric and tetramerous, as the Brassicaceae, not tetrasymmetric and tetramerous as Koeberlinia. However, no floral developmental studies are known for Salvadoraceae or Koeberliniaceae, and this represents an important lacuna in our knowledge of the clade. Ronse De Craene (2002)
suggested that pentamerous prototypes such as Pentadiplandra may have given rise to the flower structure of Brassicaceae by the median compression of the flower between bract and inflorescence axis and subsequent loss of stamens. However, it can also be suggested that the unidirectional initiation in Batis is strictly linked to the peculiar orientation of the flower during development, as the mature flower is regular. If related to Koeberlinia and Salvadora as strongly suggested by molecular data, it is obvious that the derivation of disymmetric flowers occurred at least two times in the Brassicales.
FOOTNOTES
1 The author thanks Frieda Christie for technical assistance with the SEM and financial support from the Friends of the Royal Botanic Garden Edinburgh for a fieldtrip to Belize. Comments by Peter Endress and an anonymous reviewer were much helpful. 
2 Author for correspondence (e-mail: l.ronsedecraene{at}rbge.ac.uk
)
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