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(American Journal of Botany. 2003;90:1124-1130.)
© 2003 Botanical Society of America, Inc.

Structure and Development

Floral development and phyllotactic variation in Ceratophyllum demersum (Ceratophyllaceae)1

Akitoshi Iwamoto2, Akiko Shimizu and Hideaki Ohba

University Museum, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan

Received for publication December 13, 2002. Accepted for publication March 11, 2003.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The floral development of staminate and pistillate flowers of Ceratophyllum demersum was observed, with particular focus on the phyllotactic variation in staminate flowers, using scanning electronic microscopy (SEM). We discerned patterns of development of some important new morphological features, e.g., the difference and discontinuity between the organ initiation in stamens and that in bracts (or tepals) and the initial presence of a mucilaginous appendage on each pistil. Female flowers are considered to be very specialized through reduction. In male flowers stamen initiation changes between early and late floral development. The four or five stamens in the outermost whorl initiate first on the abaxial and lateral sides of the floral apex and only later on the adaxial side (unidirectional). Later the inner stamens initiate spirally, and this is the main pattern in the stamen initiation. Members of each whorl differ among themselves in time of initiation and in ultimate size. The phyllotactic variation in staminate flowers of Ceratophyllum, suggested by previous studies, is derived from the variation in stamen number and the difference of stamen initiation between the early and later stages. The development in Ceratophyllum has some similarities to those of ANITA plants except for Nymphaeales.

Key Words: Ceratophyllaceae • Ceratophyllum demersum • floral development • floral phyllotaxy • Japan


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Within the angiosperms, floral phyllotaxy varies considerably, but tends to be more or less constant within a taxon, although it differs between taxa. Differences in floral phyllotaxy have been significant therefore in determining higher level classifications within the angiosperms (Ronse Decraene and Smets, 1994 ). Although floral phyllotaxy is usually stable within a species, in some plants, particularly in achlamydeous species, it varies even within an individual (Endress, 1987a ). Therefore, detailed studies of the floral variation in those species may shed light on the mechanisms and trends of floral development throughout the angiosperms.

The floral structure of Ceratophyllum demersum has been observed by several authors (Aboy, 1936 ; Sehgal and Ram, 1981 ; Shamrov, 1981 , 1983 ; Endress, 1994a , b , 2001 ). In particular, Endress (1994a) pointed out that the stamens in the staminate flowers are arranged in variable phyllotactic patterns: spiral, trimerous, and tetramerous. This observation is significant for our understanding and interpretation of the mechanisms of floral phyllotaxy in the angiosperms.

According to Endress (1994a) , Ceratophyllum demersum is one of the species that has drastic difference in floral phyllotaxy; it may thus be a suitable subject for a key study of phyllotactic variation within a single species. His conclusions were, however, based only on observations of cross sections of mature flowers, which may have led to misconceptions or misinterpretations of floral phyllotaxy, because the observed patterns may have been a distortion of the initial pattern caused by growth and differentiation (Zagorska, 1994 ). It is essential, therefore, to observe floral development from its earliest stages, excluding the influence of any distortion during maturation, especially because previous studies have not focused on the early stages of floral development (Shamrov, 1981 ; Rutishauser and Sattler, 1987 ).

Additionally, the floral structure of Ceratophyllum itself is still unclear in many respects, especially the nature of the enigmatic organ enclosing the staminate and pistillate flower (Les, 1986 , 1993 ) and polycarpellarity (Endress, 1994a ). Furthermore, Ceratophyllum was recently placed in a key position within the phylogeny of angiosperms based on the results of molecular analyses (Chase et al., 1993 ; Qiu et al., 1993 , 1999 , 2000 ; Soltis et al., 1997 , 1999 , 2000 ), making it all the more important that the floral structure of Ceratophyllum be reexamined so that we have a better understanding of floral evolution in the angiosperms.

Although six species are recognized within Ceratophyllum, there is little difference in the floral structure between these six species (Les, 1986 ). Therefore, the distinct character of the floral development in the genus Ceratophyllum can be discussed based on the observation of one species, Ceratophyllum demersum.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Plant material
Living plants of Ceratophyllum demersum L. were collected at two sites in Japan (Masaki-cho, Hashima-shi, Gifu Prefecture, and Sakamoto, Yamamoto-cho, Watari-gun, Miyagki Prefecture) and cultivated at the Koishikawa Botanical Garden (Botanical Garden, Graduate School of Science, the University of Tokyo, Tokyo, Japan) to provide ready access to flowers at various developmental stages.

Voucher specimens are preserved in the herbarium of the University Museum at the University of Tokyo (TI).

Fixation
Before fixation, the materials were cleaned using an ultrasonic cleaner (Yamato 1210 BRANSON, Yamato, Japan) to remove mucilaginous substances that might interfere with observations.

All materials were fixed with formalin : acetic acid : alcohol (FAA) containing less ethanol and formalin than usual (absolute ethanol, 30%; water, 62%; glacial acetic acid, 5%; formalin, 3%). Standard FAA (absolute ethanol, 50–70%; glacial acetic acid, 5%; and formalin, 5–7%) caused too much shrinkage for good preservation and observation. All samples were fixed for at least 12 h at 4°C.

Scanning electron microscopy (SEM)
Materials fixed at various developmental stages were dissected with tweezers and a micromanipulator (MM-333, Narishige, Japan) under a stereoscope.

The dissected tissues were dehydrated in an ethanol series, after which the ethanol was replaced with isoamyl acetate, then dried with a critical point dryer (HCP-2, Hitachi, Japan), and coated with Pt/Pd using a sputter coater (Ion Sputter E-1030, Hitachi, Japan).

The coated materials were observed with two types of SEM: S4500 (Hitachi, Japan) and S-2250N (Hitachi, Japan) at 5 kV. The S-2250N can be used at lower magnifications (x20–x30) than S4500 and is therefore suitable for observing relatively large objects in their entirety.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Development of pistillate flowers
Ceratophyllum demersum is monoecious and pistillate flowers are usually produced at each solitary node, but rarely staminate flowers are produced at the same node (see also Sehgal and Ram, 1981 ). Each flower is composed of one pistil and surrounded by more than 10 bracts.

The pistillate flower at an extra-axillary position is intermediate between a dome and a short cylinder at a very early stage of development (Fig. 1). A circinate groove or constriction appears at the midpoint of the cylinder and divides the bud into an apical and a basal part (Fig. 1). The apical part becomes the primordium for the pistil (black arrow), while the basal part gives rise to an aggregation of bracts (white arrow).



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  		Figs. 1–6. Floral development of pistillate flower of Ceratophyllum demersum at successive stages (SEM micrographs). Abaxial side is at the bottom of each figure. 1. Primordium of pistillate flower at early stage. Black arrow points to initiating stigma slit. White arrow points to initiating bract. Note circinate indentation around midsection of primordium. 2. Stigma slit developed. Several bract primordia initiated at base. 3. Developing bracts capped by mucilaginous appendages. Arrow points to mucilaginous appendage on pistil. 4. Adaxial side of pistil starting to elongate (arrow). 5. Adaxial side elongating more. 6. Adaxial side continuing to elongate and neck appearing between stigma and ovary. Note horns developed on apices of bracts. Scale bars = 50 µm. Figure abbreviations for Figs. 1–20: A, apex of floral meristem; B, bract; F, flower bud; H, horn; L, leaf or leaf primordium; M, mucilaginous appendage; S, stem of main shoot; SAM, shoot apical meristem; St, stamen or stamen primordium; Sti, stigma; Sty, style; V, vegetative bud

 
A slight concavity develops on the pistillate primordium (Fig. 1, black arrow) and eventually becomes a slit (Fig. 2), which is easily identified as the potential stigma. A mucilaginous appendage on the stigma appears at an intermediate stage (Fig. 3, arrow), but it later completely abscises, leaving no vestige (Figs. 7, 8). In the early developmental stages, the adaxial and abaxial sides of the pistil do not differ (Figs. 1–3) except for the mucilaginous appendage, but eventually the adaxial side of the pistil exceeds the abaxial side (Figs. 4–8). In a strict sense, the elongated structure can be considered to be part of the stigma of one carpel. The stigmatic slit is at the summit of the ovary when the adaxial side begins to elongate (Figs. 4, 5) and later moves upward, with the style elongating (Figs. 7, 8). A groove on the stigma is eventually visible from the stigmatic slit to the top of the pistil in the final stage of development (Fig. 8).



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  		Figs. 7–8. SEM micrographs. 7. Style elongating. Arrow indicates position of abscised mucilaginous appendage. 8. Mature pistillate flower. Double-headed arrow indicates length of stigmatic groove. Scale bars = 500 µm

 
Whorled primordia that will become an aggregation of bracts are initiated simultaneously at a same level (Fig. 2), followed by development of mucilaginous appendages on their apices (Fig. 3). A pair of horns later develops at a submargin on each bract (Fig. 6). The bracts then expand and the mucilaginous appendages elongate (Figs. 7, 8).

Development of staminate flowers
Staminate flowers are also usually produced at each solitary node, but less often two or more staminate flowers at the same node (see also Sehgal and Ram, 1981 ; Rutishauser and Sattler, 1987 ). Each flower is composed of more than 10 stamens and surrounded by more than 10 bracts.

Initially, a domed floral meristem is formed at an extra-axillary position. The apex of the dome is not concave, as in the pistillate flower, but convex (Fig. 9, arrow). Next, an indentation appears between the upper and basal portions, and the stamen primordia are initiated on the upper portion; bract primordia are initiated in a whorl on the basal portion (Fig. 10). The bract primordia are clearly different in shape from the stamen primordia. All bracts are produced at the same level (whorled), while clear whorls are not observed in the sequence of stamen development (Fig. 10). At the next stage, the difference becomes clearer (Fig. 11). The primordia of the bracts elongate to cover the apex of the flower, and a mucilaginous appendage develops at the apex of each bract. The primordia of the stamens keep the same shape during these stages (Figs. 10, 11).



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  		Figs. 9–14. Floral organogenesis in staminate flower (SEM micrographs). 9. Domed floral meristem initiating at node (arrow). 10. Outer stamens and bract primordia initiating at base simultaneously. 11. Bracts with mucilaginous appendages developed. 12. Inner stamens initiating (arrows) and outer stamens developed. Bracts with developing mucilaginous appendages and horns. 13. Enlarged outer stamens enclosing center of flower. 14. Enlarged stamens and reoriented bracts. Scale bars = 50 µm (Figs. 9–12 ), 500 µm (Figs. 13, 14 )

 
The additional stamens are then initiated and mucilaginous appendages appear on the outer stamens (Fig. 12; young inner stamens indicated by arrows; see also Early development of staminate flowers later). The bracts develop subapical horns lateral to the mucilaginous appendage (Fig. 12). The number of horns on each bract is usually two, but some bracts have three or four horns (Fig. 13).

As the flower develops, the outer stamens enlarge, develop horns, and grow to enclose the apex of the staminate flower (Fig. 13). Two horns are produced on each stamen, the same as on the bracts. Finally, the stamens enlarge in girth to the extent that the bracts change their orientation from vertical (erect) to horizontal (spreading) (Fig. 14). At this stage, the mucilaginous appendages on the outer stamens usually abscise, and the horns become relatively insignificant, although they persist as small raised bumps (Fig. 14). The stamens ultimately dehisce to release their pollen into the water (see also Endress, 1994). In very rare cases, some stamens are fused (Figs. 15, 16). Because fused stamens are rare, we were unable to obtain a sequence of flowers showing their development.



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  		Figs. 15–16. Fused stamens (SEM micrographs). 15. Maturing staminate flower with fused stamens. 16. Staminate flower with fused stamens at later stage than in Fig. 15 . Fused stamens with horns. Scale bars = 500 µm

 
Early development of staminate flowers
The staminate flower buds (and the pistillate and vegetative buds) at first appear near the shoot apical meristem (SAM) (Figs. 17, 18). The leaves (of the hypotheses on the identity of the organ we refer to here, adopt the most acceptable hypothesis that the organ is a "true" leaf; see also Rutishauser, 1999 ) are initiated in a whorl, and the staminate flower buds are initiated in the nodes. The primordia of the staminate flowers and leaves are so closely aggregated that they come into contact with each other. In particular, the adaxial side of the staminate flowers adheres to the leaf primordia above (Fig. 18, arrows).



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  		Figs. 17–20. Shoot tips and floral primordia (SEM micrographs). 17. Shoot tip with young flower, vegetative bud primordia, and leaf primordia. 18. Shoot tip with covering older leaves removed. Young leaf primordia are initiating in whorls. Vegetative bud is bract-subtended and axillary, but staminate flower bud is not bract-subtended. 19, 20. Staminate floral buds showing stamen primordia abaxially and laterally, but none adaxially. Adaxial side of staminate flower covered with leaf. Four stamens appearing on free area (abaxial side). The abaxial side is at the bottom of each figure. Scale bars = 50 µm

 
In the little later stage, the adaxial side of the staminate bud is covered with the leaf primordium (Fig. 19). Dissection of leaf primordia shows that no stamens are initially produced on the adaxial side of the floral apex, while some stamens clearly develop on the abaxial and lateral side (Figs. 20, 21). In later stages, some stamen primordia are initiated on the adaxial side also (Figs. 22, 23); that is, this sequence of the stamen initiation in the outermost whorl is unidirectional. The initiation of bract primordia is also delayed on the adaxial side, i.e., the bract primordium on the abaxial side (Fig. 21, black arrow) develops more than that on the adaxial side (Fig. 21, white arrow). After these stages, the stamen primordia appear in the inner part of the flower, being initiated centripetally (Figs. 24–26).



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  		Figs. 21–26. Floral development at early stages in staminate flowers (SEM micrographs). The abaxial side is at the bottom of each figure. Numbers in figures follow the initiation sequence of primordia. 21. Staminate primordia produced only on the abaxial (black arrow) and lateral side. Bract primordia development on the adaxial side (white arrow) delayed. 22. Stamen primordium appeared on the adaxial side. 23. Two stamen primordia initiated on the adaxial side. Primordia on the abaxial and lateral sides have enlarged. 24. Inner stamen primordia initiated centripetally. Outer stamens initiating mucilaginous appendage on tips. 25, 26. Outer stamens enlarged. The growth of the stamen on the adaxial side was delayed. Scale bars = 50 µm

 
The meristems shown in Figs. 20–26 indicate that the development in the outermost whorl of the staminate flowers is unidirectional and the numbers of the stamens in the outermost is unstable; e.g., some flower have four outer stamens (Fig. 22), others have five stamens (Fig. 23).

Structure of staminate flowers
At later stages, in the outermost whorl, mature, staminate flowers usually exhibit various patterns (Figs. 27–30). Some are symmetrical (as in Figs. 27, 28), but others appear to be asymmetric (Figs. 29, 30).



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  		Figs. 27–38. Outermost part of mature staminate flower in Figs. 27–30 and intermediate part in Figs. 31–34 . Phyllotactic variation in staminate flowers. Numbers in figures follow the initiation sequence of primordia (SEM micrographs). 27. Flower with trimerous-like configuration. 28. Flower with tetramerous-like configuration. 29. Irregular phyllotaxy. 30. Irregular configuration. Three stamens extraordinarily expanded. 31, 32. Trimerous-like configuration, but size of each stamen differs. 33, 34. Tetramerous-like configurations, but symmetry differs. 35–37. Innermost part of three flowers with successive spiral initiation. 38. Innermost part of mature staminate flower with Fibonacci spiral configuration. Scale bars = 500 µm (Figs. 27–30 ), 50 µm (Figs. 31–38 )

 
In the innermost portion of the staminate flowers, even in later stages, stamen primordia are still developing and the order of primordia initiation is clear. Only one type of stamen configuration was observed, successively spiral (the divergence angle between the primordia is about 110°–130°; Figs. 35–37). Repetition of this pattern results in mainly a Fibonacci spiral stamen sequence (Fig. 38). In rare cases, a spiral pattern like the Lucas pattern was observed. The definition of Fibonacci and Lucas sequences is according to Rutishauser (1998) .

In the intermediate portions of the stem the stamens are arranged in various phyllotaxies (Figs. 31–34), but the range of variation is reduced from that of the outermost part. Stamens usually occur in whorls (or pseudowhorls). Whorls are often trimerous (Figs. 31, 32) or tetramerous (Figs. 33, 34), indicating that in intermediate portions the pattern of floral development may be intermediate between that in the early stages (unidirectional) and that in a later stage (spiral); that is, it is neither strictly unidirectional nor strictly spiral initiation.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Floral development in Ceratophyllum
In Ceratophyllum, the development of the pistillate flower is very specific and similar to no other extant plants and may be related to an adaptation to a submerged life cycle, as pointed out by Jones (1931) . Endress (1994a) pointed out that some previous studies interpreted this early development on the adaxial side as being caused by the fusion of two carpels, but Endress' observations confirmed that the pistil of Ceratophyllum is composed of a single carpel. Endress (1994a) , however, showed the pistillate flower only at a stage after it had already differentiated between adaxial and abaxial. We observed the earlier stages and confirmed that the meristem of the pistil is dome-shaped at the earliest stage; no vestige is present indicating fusion of the carpels.

Additionally, pistillate flowers have been assumed to have no mucilaginous appendages (Les, 1986 , 1993 ; Endress, 1994a ), but during intermediate stages, we observed mucilaginous appendages, which later abscise. In the earliest stages, mucilaginous appendages cannot be observed, indicating that previous studies may have focused on either the earlier or later developmental stages. The leaves also have mucilaginous appendages on their tips (Rutishauser and Sattler, 1987 ; Les, 1993 ). Accordingly, all lateral organs in Ceratophyllum (leaves, stamens, pistils, bracts) have mucilaginous appendages. The presence of the mucilaginous appendage on the pistil also supports the monocarpel in the pistillate flower of Ceratophyllum demersum, because it can be found only on the abaxial side, not on the adaxial side. If this flower was syncarpous, we should find two or more appendages on the pistil.

Although previous studies referred to the development of staminate flowers in Ceratophyllum (Rutishauser and Sattler, 1987 ; Endress, 1994a , b , 2001 ), the positional relationship between stamens and bracts has not been clear. We found clear developmental differences between them and confirmed that the bracts of the staminate flowers are produced in the same way as those of the pistillate flowers. It can be concluded that the bracts of both staminate and pistillate flowers are homologous.

Organs enclosing flowers
The organs enclosing the pistils and stamens (we referred to these as bracts in the previous descriptions) have been regarded as either tepals (Sehgal and Ram, 1981 ; Rutishauser and Sattler, 1987 ; Endress, 1994a ) or bracts (Jones, 1931 ; Les, 1986 , 1993 ). In particular, Les (1986 , 1993 ) insisted that the organs of the pistillate flower occasionally subtend not one, but several flowers, based on the observations by Aboy (1936) . Les also pointed out that Sehgal and Ram (1981) found a multiple-flowered pistillate inflorescence and concluded that the enclosing structures are bracts, not tepals or sepals. Our observations do not confirm Les' views, because there are no developmental vestiges to indicate that either pistillate or staminate flowers originally derived from multiple-flowered inflorescences. The organs, however, are produced at the same node, which is similar to the initiation of whorled leaves in Ceratophyllum (Rutishauser and Sattler, 1987 ). It therefore may be concluded that the organs enclosing the stamens and pistils should be regarded as bracts derived from leaves.

Floral phyllotaxy of staminate flowers
There is a distinct difference between the stamen initiation in flowers in the outermost whorl (unidirectional) and that in later stages (spiral), indicating that the pattern of initiation changes in stamen primordia through development. The developmental difference between the early and later stages is clearly correlated with delayed development on the adaxial side as compared with the abaxial and lateral side.

Some authors reported the staminate flower of Ceratophyllum to have basically spiral phyllotaxy (Sehgal and Ram, 1981 ; Shamrov, 1981 ; Les, 1993 ) or irregular phyllotaxy (Rutishauser and Sattler, 1987 ). Both views are partially correct; the former reports are based on observations of floral development in the inner part of staminate flowers in Ceratophyllum, while the latter are based on observations of floral development in the outermost whorl. Failure to observe floral development throughout its entire sequence has led to contrasting interpretations.

As outlined before, Endress (1994a , b , 2001 ) pointed out the phyllotactic variation in Ceratophyllum. This assertion is also the result of the failure to observe floral development throughout its entire sequence. Actually, however, Ceratophyllum has basically spiral phyllotaxy, as the inner portions indicate, although stamens only in the outermost whorl are unidirectionally initiated. The apparent phyllotactic variation should be derived from the variation in the stamen number of the outermost whorl and the change of the stamen initiation to the spiral in the inner portions. Also the intermediate floral development in intermediate portions exhibits a pattern between that in the outermost (unidirectional) and that in the innermost (spiral).

Affinity of Ceratophyllum and floral development
The affinity of Ceratophyllum is still enigmatic. The genus was once considered to be closest to Cabomba by many authors (Melchior, 1964 ; Dahlgren, 1980 ; Takhtajan, 1980 ; Cronquist, 1981 ). Les (1986 , 1988 , 1991 ), however, rejected that view based on phenetic analyses and molecular data. Our observations also indicated that floral development, including floral phyllotaxy, in Ceratophyllum is quite different from that in Cabomba (Cabomba has strictly trimerous flowers; Tucker and Douglas, 1996 ; Endress, 2001 ). Molecular phylogenetic analyses based on DNA sequences have also supported this view, indicating that there is no close relationship between these genera (Chase et al., 1993 ; Qiu et al., 1993 , 1999 , 2000 ; Soltis et al., 1997 , (1999 ; 2000 ).

Ceratophyllum was once considered to be the basalmost genus among extant angiosperms on the basis of molecular phylogenetic analyses (Chase et al., 1993 ; Qiu et al., 1993 ; Soltis et al., 1997 ), but recent more resolved and supported analyses placed it in a grade composed of eumagnoliids, monocots, and Ceratophyllum. This group is positioned between the grade composed of Amborellaceae, Nymphaeales, Illicales, Trimeniaceae, and Austrobaileyaceae, termed as ANITA (Endress, 2001 ) and the eudicot clade (Qiu et al., 1999 , 2000 ; Soltis et al., 1999 , 2000 ). The development of staminate and pistillate flowers in Ceratophyllum bears little resemblance to those of plants in the eumagnoliids and monocots. (Erbar and Leins, 1981 , 1983 , 1994 ; Dahlgren et al., 1985 ; Endress, 1987a , b ; Liang and Tucker, 1995 ; Ronse Decraene and Smets, 1995 ; Tucker and Douglas, 1996 ), although the unidirectional initiation in the outermost whorl is observed in Ceratophyllum and some Pipelales species (Liang and Tucker, 1995 ; Tucker and Douglas, 1996 ). On the other hand, the staminate floral development of Ceratophyllum is closely related to those of the ANITA plants except the Nymphaeales, because the former share some similarities with Ceratophyllum, e.g., spiral phyllotaxy and densely populated stamen primordia on a meristem (Endress, 2001 ). Thus the staminate flower of Ceratophyllum has the plesiomorphic characters of floral development within the grade, and the pistillate flower of Ceratophyllum has become very specialized and does not resemble any other species. But, even in ANITA plants, the change in the stamen initiation from unidirectional to spiral has not been observed. This change may be the unique character in Ceratophyllum.

Ceratophyllum is positioned as the sister group of the monocots by some molecular analyses (Soltis et al., 1997 ; Qiu et al., 1999 , 2000 ). Our result, however, indicates little relationship between Ceratophyllum and monocots. The staminate floral development in Ceratophyllum basically indicates a spiral sequence of primordium initiation, but the most common monocot androecial configuration is trimerous (Dahlgren et al., 1985 ). Although there are some hypotheses that the trimerous phyllotaxy in monocots should be derived from spiral phyllotaxy, the taxa concerned have stamen pairs in spiral phyllotaxy (Erbar and Leins, 1994 ; Ronse Decraene and Smets, 1994 , 1995 ). Our results reveal Ceratophyllum has no such "pair stamen." Therefore, we concluded that the trimerous flower in the monocots was not directly derived from Ceratophyllum.

The position of Ceratophyllum, however, is not supported by high consensus values (Chase et al., 1993 ; Qiu et al., 1993 , 1999 , 2000 ; Soltis et al., 1997 , 1999 , 2000 ). A better supported tree is necessary to evaluate the significance of the floral development in Ceratophyllum in more detail.


   FOOTNOTES
 
1 The authors thank Dr. Rolf Rutishauser, Institute of Systematic Botany, University of Zurich for precious advice on the manuscript, and Dr. Yasuro Kadono, Faculty of Science, Kobe University; Mr. Keisuke Okuda; and Mr. Mitsuru Usuba for supporting in collecting materials. Our thanks also go to Dr. David E. Boufford, Harvard University Herbaria, Harvard University, and Mr. Gregory Kenicer, Botanical Gardens, the University of Tokyo, for checking the English text and content. Back

2 Author for reprint requests (e-mail: akitoshi{at}um.u-tokyo.ac.jp ) Back


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Aboy H. E. 1936 A study of the anatomy and morphology of Ceratophyllum demersum. M.S. thesis, Cornell University, Ithaca, New York, USA

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Dahlgren R. M. T. H. T. Clifford P. F. Yeo 1985 The families of the monocotyledons. Springer-Verlag, Berlin, Germany

Endress P. K. 1987a Floral phyllotaxis and floral evolution. Botanische Jahrbücher für Systematik Pflanzengeschichte und Pflanzengeographie 108: 417-438

Endress P. K. 1987b The Chloranthaceae: reproductive structures and phylogenetic position. Botanische Jahrbücher für Systematik Pflanzengeschichte und Pflanzengeographie 109: 153-226

Endress P. K. 1994a Evolutionary aspects of the floral structure in Ceratophyllum. Plant Systematics and Evolution (Supplement) 8 175-183

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Endress P. K. 2001 The flowers in extant basal angiosperm and inferences on ancestral flowers. International Journal of Plant Sciences 162: 1111-1140[CrossRef][ISI]

Erbar C. P. Leins 1981 Zur Spirale in Magnolien-Blüten. Beiträge zur Biologie der Pflanzen 56: 225-241

Erbar C. P. Leins 1983 Zur Sequenz von Blütenorganen bei einigen Magnoliiden. Botanische Jahrbücher für Systematik Pflanzengeschichte und Pflanzengeographie 103: 433-449

Erbar C. P. Leins 1994 Flowers in Magnoliidae and the origin of flowers in other subclasses of the angiosperms I. The relationship between flowers of Magnoliidae and Alismatidae. Plant Systematics and Evolution (Supplement) 8 193-208

Jones E. N. 1931 The morphology and biology of Ceratophyllum demersum. Iowa Studies in Natural History 13: 11-55

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