Aspects of Floral Development in Philodendron Grandifolium and Philodendron Megalophyllum (Araceae)

ASPECTS OF FLORAL DEVELOPMENT IN PHILODENDRON GRANDIFOLIUM AND PHILODENDRON MEGALOPHYLLUM (ARACEAE)

Denis Barabe´ 1 and Christian Lacroix

Institut de Recherche en Biologie Ve´ge´tale, Jardin Botanique de Montre´al, 4101 Sherbrooke Est, Montre´al, Que´bec H1X 2B2, Canada; and Department of Biology, University of Prince Edward Island, 550 University Avenue, Charlottetown, Prince Edward Island C1A 4P3, Canada

This study deals specifically with floral organogenesis and the development of the inflorescence of Philo- dendron grandifolium and Philodendron megalophyllum. Pistillate flowers are initiated on the lower portion of the inflorescence, and the staminate flowers are initiated on the distal portion. The presence of extracellular calcium oxalate is observed on the surface of immature stamens of P. megalophyllum. An intermediate zone consisting of sterile male flowers and bisexual flowers with fused or free carpels and staminodes is also present on the inflorescences. This zone is located between the male and female floral zones. In general, the portion of bisexual flowers facing the male zone forms staminodes, and the portion facing the female zone develops an incomplete gynoecium with few carpels. In P. grandifolium, the incomplete separation of some staminodes from the gynoecial portion of the whorl shows that they belong to the same whorl as the carpels. The bisexual flowers of P. grandifolium and P. megalophyllum are believed to be a case of homeosis in which carpels have been replaced by sterile stamens on the same whorl.

Keywords: ﬂower, inﬂorescence, homeosis, development.

Introduction on the inflorescence. They are located at the junction between the female portion and the male portion of the inflorescence. The family Araceae comprises 105 genera and more than Developmental studies have shown that carpels and stami- 3300 species (Mayo et al. 1997). Members of this family are nodes are inserted on the same whorl on bisexual flowers (e.g., characterized by two main types of inflorescences: (1) those Mayo 1986; Boubes and Barabe´ 1996; Barabe´ and Lacroix with bisexual flowers, as represented in the genus Anthurium, 1999, 2000). This phenomenon can be explained as the re- and (2) those with unisexual flowers, as represented in the placement of carpels by staminodes, and it represents an ex- genus Philodendron. Inflorescences of the Philodendron type ceptional case of homeosis (e.g., Barabe´ and Lacroix 1999; consist of female flowers located in the lower portion and male Barabeét al. 2000). flowers in the upper portion. Several species with unisexual In the atypical bisexual flowers of Philodendron, there is a flowers (representing a number of genera) have been investi- lot of variation in the number of carpels replaced by stami- gated by a variety of authors from the perspective of floral nodes among species. For example, in Philodendron solimoe- anatomy and developmental morphology (Engler and Krause sense, an average of 3.2 carpels are replaced by one staminode. 1912; Eckardt 1937; Eyde et al. 1967; Hotta 1971; Barahona In Philodendron fragrantissimum, this number is reduced to Carvajal 1977; Uhlarz 1982, 1986; French 1985a, 1985b, 1.5 and represents a more or less one-to-one shift (Barabeét 1986a, 1986b; Mayo 1986, 1989; Barabe´ and Forget 1988; al. 2000). The high degree of variability in the mode of ex- Carvell 1989; Buzgo´ 1994; Boubes and Barabe´ 1997). Re- pression of carpel/staminode in homeotic bisexual flowers is cently, Barabe´ and collaborators (Barabeánd Bertrand 1996; not only observed between species belonging to different sub- Barabeánd Lacroix 1999; Barabeét al. 2000) used the flower genera, such as P. solimoesense (Meconostigma) and P. fra- of the Philodendron type as a model to analyze theoretical grantissimum (Philodendron) but is also observed between spe- aspects of morphogenesis, such as the phenomena of homeosis cies of the same subgenera and even among individuals and morphogenetic gradient. They observed that the nature of belonging to the same species. How can we explain this var- floral organs on different types of flowers depends on the po- iation? To answer this question, comparative developmental sition of the flowers on the inflorescence. In other words, the studies between a greater number of species belonging to the nature of floral organs is independent of the whorl on which same subgenera must be initiated. It is from this perspective it is initiated. that the floral development of Philodendron grandifolium and In the genus Philodendron, bisexual flowers, called “mon- stro¨sen Blu¨ten” by Engler and Krause (1912), are also present Philodendron megalophyllum will allow us to provide new data supporting the morphological nature of bisexual flowers in the genus Philodendron. More precisely, we intend to ad- 1 Author for correspondence; telephone 514-872-1436; fax 514- dress the following questions in the context of the phenomenon 872-3765; e-mail [email protected]. of homeosis: Are there different types of bisexual flowers in Manuscript received June 2000; revised manuscript received August 2000. terms of substitution ratios (i.e., number of carpels replaced

47 48 INTERNATIONAL JOURNAL OF PLANT SCIENCES by number of staminodes or vice versa)? Do carpel and stam- a Cambridge S604 scanning electron microscope (SEM) with inode primordia belonging to the same whorl have a different digital imaging capabilities (SEMICAPS). mode of development than do staminodes and carpels belonging to sterile male flowers and female flowers, respectively? Is the relationship between the nature of floral organs that will Results be formed and the position of the flower on the inflorescence in P. grandifolium and P. megalophyllum similar to that of other documented cases? Morphology of the Mature Flowers Although there are a few anatomical studies of selected spe- The length of the mature spadices of both species ranges cies of the subgenus Philodendron (Barahona Carvajal 1977; from 10 to 15 cm. Both staminate and pistillate flowers have Mayo 1986, 1989), the mode of development of the flower in no perianth. The staminate flowers occupy the upper portion this subgenus, represented in this study by P. grandifolium and of the inflorescence and take up ca. 65% of the total length P. megalophyllum, remains poorly understood. Consequently, of the inflorescence, whereas the female flowers are located on new morphological and ontogenetic characters related to the the lower portion and occupy ca. 25% of the total length. In development of flowers are needed to complement anatomical the median portion of the inflorescence, there is an interme- studies of subgenus Philodendron species (see, e.g., Mayo diate zone (ca. 10% of the total length) consisting of bisexual 1986, 1989) and to add to our present knowledge of floral flowers and sterile males flowers. types within this group. In both species, modified stomata (water pores) in the sense Developmental studies often reveal particular features that of Vogel (1977) are found on the surface of the apical portion are not visible on fully developed organs. This is particularly of the stamens (fig. 1A,1B) and staminodes on male and sterile the case for secretory structures such as hydathodes, nectaries, male flowers, respectively. The epidermis of stamens and stam- and water pores in the sense of Vogel (1977) and Endress inodes consists of pegged and rigged cells (fig. 1B). (1996). The presence of stomata on stamens and staminodes The bisexual flowers generally consist of carpels and stam- has been observed in different species of Philodendron, such inodes inserted on the same whorl. The portion of the bisexual as Philodendron acutatum (Boubes and Barabe´ 1996) and P. flower facing the male zone consists of staminodes, and the solimoesense (Barabeánd Lacroix 1999). However, there were portion facing the female zone consists of an incomplete gy- no indications concerning the accumulation of calcium oxalate noecium (figs. 1C,5F–5H). On mature flowers, like that rep- crystals on anthers in Philodendron. With this study, we intend resented in figure 1C, it is difficult to determine whether the to present evidence for the presence of extracellular calcium staminode(s) and carpels are inserted on the same whorl. How- oxalate crystals in P. megalophyllum. ever, during the early stages of development, this phenomenon The general aims of this study are (1) to compare the de- is visible (see section on floral development of bisexual flow- velopment of flowers of P. grandifolium and P. megalophyllum ers). The presence of mature atypical organs having both stam- to that of other members of the same subgenus in order to test inodal and pistillate characters (figs. 1C,4H) is a more or less our current assumptions on the phenomenon of homeosis in common feature in the intermediate zone of the inflorescence. the Araceae and (2) to further document the liberation of cal- These organs are characterized by a discontinuous stigmatic cium oxalate crystals by floral organs. surface and staminodal-like tissue. The mature female flowers have a prominent stigmatic sur- Material and Methods face (fig. 1D,1E; fig. 4F,4G). A large quantity of secretions are consistently observed between the papillae on the stigmatic Philodendron grandifolium Brongn. ex Regel and Philoden- surface (fig. 1F). dron megalophyllum Schott belong to the subgenus Philoden- dron, section Philodendron, subsection Philodendron (Croat 1997). Specimens used for this study were collected by D. Development of the Inflorescence Barabeín French Guiana (Petit-Saut dam) in November 1997 and July 1998 (voucher specimens were deposited at MT: Bar- The inflorescence primordium of Philodendron grandifol- abe´62, Barabe´67). Specimens growing at the Montreal Bo- ium is more or less cylindrical in shape during early stages of tanical Garden were also collected in April 2000 (registration initiation (fig. 2A). The different types of flowers are initiated numbers 2382-92 [P. megalophyllum] and 2415-92 and 2032- acropetally along the axis of the inflorescence. Pistillate flowers 97 [P. grandifolium]). Inflorescences at various stages of de- will develop on the basal portion of the inflorescence, and velopment were collected, dissected under a stereomicroscope staminate flowers will develop on the terminal portion. The to expose the spadix, and fixed in formalin–acetic acid–alcohol primordia of the female zone are initiated more or less si- (1:1:9byvolume) and were later transferred and stored in multaneously (fig. 2A) and cover approximately three-fourths 70% ethanol. of the inflorescence at this very early stage. At the stage when Twenty-nine samples of P. grandifolium and 21 samples of all the floral primordia have been initiated, the different types P. megalophyllum were dehydrated in a graded ethanol series of flowers are all approximately the same size (fig. 2B). It is to absolute ethanol. They were then dried in a LADD model interesting to note that there is no discontinuity in the phyl-

28,000 critical-point dryer using CO2, mounted on metal lotactic pattern between the different zones of the inflorescence. stubs, and grounded with conductive silver paint. Specimens Pistillate flowers, sterile male flowers, bisexual flowers, and were sputter-coated with gold/palladium to ca. 30 nm using a staminate flowers are inserted on the same contact parastichies Denton Vacuum Desk II sputter-coater and were viewed with (fig. 2B, arrows). Fig. 1 Morphology of mature structures on the inflorescence of Philodendron megalophyllum. A, Top view of mature stamen showing stomata, some of which are found in depressions (arrowheads). Bar p 75 mm. B, Higher magnification of stamen, similar to A, showing peglike morphology and ridged surface of epidermal cells (arrowhead p s tomate). Bar p 15 mm. C, Intermediate zone on mature inflorescence showing the location of atypical floral organs (At) and bisexual flowers consisting of a gynoecium (G) and staminodes (St). At this stage, it is difficult to determine which appendages belong to which flowers. Bar p 300 mm. D, Top view of stigmatic surface (asterisk) of a female flower. Bar p 300 mm. E, Close-up of stigmatic surface showing papillae (arrowheads). Bar p 75 mm. F, Top view of mature female flower (F) covered with a mucilaginous substance (arrowheads). Bar p 300 mm. 50 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Fig. 2 Early stages of development of the inflorescence and male flowers of Philodendron grandifolium. A, Side view of early stage of development of the inflorescence showing the initiation of floral primordia (small bumps), most of which represent pistillate flowers (bracket). Bar p 300 mm. B, Side view of inflorescence on which all floral primordia have been initiated. At this stage of development, the different floral zones cannot be clearly delimited. Arrows p c ontact parastichies. Bar p 750 mm. C, Early stage of stamen initiation (arrowheads) on male flowers. Bar p 150 mm. D, Later stage of development than seen in C, showing larger stamen primordia (arrowheads) numbering four to six per flower. Bar p 150 mm.

Floral Development stamens. These exudates form more or less globular masses on the epidermal surface (fig. 3A,3B, arrowheads) and appear Staminate flowers. The stamen primordia are initiated si- to correspond to an oxalate package (a mass of crystals or multaneously on the periphery of more or less circular floral raphides clusters) in the sense of D’Arcy et al. (1996). De- primordia (fig. 2C, arrowheads) on one whorl in both P. grandifolium and Philodendron megalophyllum.InP. grandifol- pressions can also be observed on the surface of the nearly ium, there are generally five or six stamen primordia per mature stamens (fig. 3C). At the bottom of each depression flower; in rare cases, there may be four stamen primordia (fig. there is an open pore (fig. 3D). 2C,2D). During later stages of development, the floral pri- Pistillate flowers. During early stages of development, fe- mordia come in contact with each other (fig. 2D). In addition, male floral primordia have a hemispherical shape (fig. 4A). the size of the stamens increases considerably during these The carpel primordia are initiated on the periphery of the floral stages of development, to the point that they will eventually primordia in both species. Carpel primordia on individual occupy all the available space between flowers, as seen in figure flowers have an inward-facing horseshoe shape (fig. 4B). Dur- 3A in P. megalophyllum. ing later stages of development, the entire ovary wall is formed In the case of P. megalophyllum, calcium oxalate crystals by the concrescence of the walls of adjacent carpels (fig. 4C, are visible on the surface of the apical portion of nearly mature 4D). In the case of P. grandifolium, there are generally seven Fig. 3 Specific features of nearly mature flowers of Philodendron megalophyllum. A, Top view of nearly mature stamens (S) showing the accumulation of extracellular calcium oxalate crystals (arrowheads). Bar p 75 mm. B, Close-up of oxalate crystals seen in A (arrowheads). Bar p 7.5 mm. C, Top view of surface of stamen (S) at or near maturity. Note the large number of small depressions on the surface. Bar p 300 mm. D, Close-up of a depression similar to those highlighted in C. Note the presence of a stomatal opening (arrowhead) at the base of the depression. Bar p 75 mm. E, Top view of nearly mature flower showing five independent stylar canals (arrowheads). Bar p 150 mm. F,Top view of female flower showing the extension of the stylar tube resulting in one opening (arrowhead). Bar p 150 mm. G, Side view of numerous mature female flowers (F) at the base of the inflorescence axis. Bar p 750 mm. Fig. 4 Developmental morphology of female flowers of Philodendron grandifolium. A, Early stage of initiation of female flowers (F). Note the regular arrangement of floral primordia (arrows) in parastichies on the surface of the inflorescence. Bar p 75 mm. B, Early stage of initiation of horseshoe-shaped carpels (arrowheads) on individual floral primordia. Bar p 75 mm. C, Ovarian cavities (arrowheads) are more clearly visible at this stage of development. Bar p 75 mm. D, Later stage of development than C, showing a more continuous and prominent ovary wall surrounding the locules (arrowheads). Bar p 150 mm. E, Top view of female or bisexual flowers showing the extension of the stylar tube resulting in one opening (arrowheads). Bar p 300 mm. F, Early stages of development of stigmatic surface (arrowheads). Bar p 300 mm. G, Mature stigmatic surface of flower. The stylar tube is no longer visible at this stage of development (arrowhead). Bar p 300 mm. H, Mature atypical floral organs (At) with discontinuous stigmatic surfaces (arrowheads). Bar p 300 mm. BARABE´ & LACROIX—FLORAL DEVELOPMENT IN PHILODENDRON 53 or eight carpels per flower (fig. 4C,4D), and rarely, there are continuous. This is an indication that the staminodes and the six carpels. In P. megalophyllum, we found an average of five carpels belong to the same whorl. In general, the two types of carpels per gynoecium (fig. 3E). The small holes that are visible organs are separate and only continuous at the base (fig. 5D, during later stages of development represent the upper portion flowers A and B; fig. 5E, BF), as is normally the case for flower of the stylar canals (fig. 3E). Although the carpels are con- parts inserted on a single whorl. However, in some cases, there crescent, the stylar canals remain free in the mature ovary to is an incomplete separation between staminodes and carpel just below the stigma. The formation of the compitum results (fig. 5F, arrow). in one opening during the final stages of floral development (fig. 3F; fig. 4E,4F). The formation of papillae on the stigmatic Discussion surface takes place when the ovary is nearly mature in both species (figs. 3G,4F). Calcium Oxalate Crystals Sterile staminate flowers.InP. grandifolium, the sterile male flowers (SMFs) and bisexual flowers (BFs) of the inter- With the exception of Philodendron pedatum (D. Barabe´ mediate zone occupy ca. 10%–15% of the total length of the and C. Lacroix, unpublished data), the stamens of Philoden- inflorescence. These flowers form a transition zone between dron megalophyllum have a feature that, to our knowledge, typical male and female flowers. During early stages of de- has not been reported in the genus Philodendron: the presence velopment, the primordia of SMFs and BFs have the same of extracellular calcium oxalate crystals on the surface of sta- morphology as pistillate and staminate flowers in both species mens. D’Arcy et al. (1996) noted that the stamens of Anthur- (fig. 5A,5B), and they are approximately the same size as ium pallidiflorum delivered calcium oxalate and pollen to- staminate floral primordia and female floral primordia (figs. gether when touched with a moistened microscope slide. 2C,4A, respectively). Hegelmaier (1871) reported the presence of oxalate packages Although the floral organs of the SMF and BF seem to be in the genera Pinellia and Arum. The mixing of crystals with initiated at the same time as those of the pistillate flowers, their pollen was also observed in Zantedeschia (Hegelmaier 1871) relative rate of growth is faster than that of the other types of and Calla (Hegelmaier 1871; Pohl 1941). This indicates that flowers as a result of the development and expansion of the a careful anatomical and developmental study of the different staminodes. As a result, SMFs and BFs eventually become types of flowers in the subfamily Aroideae could reveal other larger than pistillate flowers, especially at maturity (figs. 1C, cases in which extracellular oxalate crystals are present. 4E). The presence of stomatal pores was also observed in other The primordia of the staminodes on the SMF are initiated species of Philodendron: for example, P. acutatum, P. fra- on the periphery of the floral primordium (fig. 5C). In P. gran- grantissimum, P. melinonii, and P. solimoesense. However, difolium, there are generally six or seven—sometimes contrary to what is found on the stamens of P. megalophyllum, five—staminodes per flower (fig. 5C). no extracellular oxalate crystals and depressions were observed Bisexual flowers. Bisexual flowers form a single row on in the above species, even in the closely related species Phil- the inflorescence and are located directly below the sterile male odendron grandifolium. This seems to indicate that the ca- flowers (fig. 5B). The initiation of BFs in both species is similar pability of stamens to deliver oxalate substances is not com- to that associated with the other types of flowers discussed mon to all Philodendron. The presence of calcium oxalate above. The primordia of the floral organs are initiated on the crystals was noted also on the stigma of P. melinonii and Phil- periphery of a discoid floral primordium (fig. 5B,5D), and odendron ornatum (D. Barabe´ and C. Lacroix, unpublished their nature, number, and form vary considerably. In P. gran- data). We believe that the study of the developmental mor- difolium, the types of floral organs produced on BFs are phology of a greater number of species would show that this strongly correlated to their proximity to the other zones. The character is more frequent than it appears. female organs of BFs tend to be initiated on the side of the What is the function of these extracellular oxalate crystals? flower adjacent to the female zone, and the male organs are These have been interpreted to be the product of pseudonec- initiated on the side of the flower closer to the sterile male taries (Chase and Peacor 1987). D’Arcy et al. (1996, p. 159) zone (fig. 5D–5F). The number of carpels in BFs ranges from reported that the oxalate package “serves to enhance polli- two (fig. 5H) to five (fig. 5D, flowers A and B), and the number nation attraction through visual or chemical stimuli or both of staminodes ranges from one (fig. 5D,5G) to two (fig. 5E) and that it sustains an unreported kind of plant-pollinator or possibly three (fig. 5H). The total number of floral organs interaction.” (carpels+s taminodes) per BF is generally five or six; it is rarely We know that the accumulation of crystals on the surface less than five. In contrast to visible floral appendages, during of cells on stamens occurs before the complete development the early stages of development, it is often difficult to determine of stamens and stigmata; the typical ridged surface of epider- exactly which staminodes belong to which flowers in later mal cells is not fully developed, and the stigma is not yet stages of BF development (figs. 1C,4G,5H). formed. When the stamens reach a developmental stage similar During early stages of development, the surface area of to that represented in figure 3C, pistillate flowers look like individual BFs is approximately the same as that of female those represented in figure 3E. This shows that when the stig- flowers, regardless of the number of carpels and staminodes matic surface starts to secrete a mucilaginous substance, the involved. For example, in figures 5E and 5F, BFs cover ap- calcium oxalate crystals have already been exuded from sta- proximately the same surface area as the surrounding female mens. The oxalate crystals on incompletely developed stamens flowers, even though the number of carpels differs. seem to disappear (fig. 3C) before the female flowers become In some flowers, the stamens and the adjacent carpels are receptive (figs. 1D,1E).

BARABE´ & LACROIX—FLORAL DEVELOPMENT IN PHILODENDRON 55

Bisexual Flowers female characteristics (carpels) and the portion facing the male zone displays male characteristics (staminodes). All the bisex- Although the pistillate portion of the bisexual flowers is ual flowers of the Philodendron species studied to date are the fertile, the staminate portion consists of sterile stamens that result of a unique manifestation of a qualitative gradient (at are referred to as staminodes. From a functional reproductive the level of the inflorescence) affecting the nature of the ap- point of view, these flowers remain unisexual. On the other pendages that are initiated in individual flowers within that hand, from a developmental point of view, we can consider gradient. these flowers to be bisexual because pistillate and staminate The hypothesis of a hormonal gradient has been used to primordia are initiated on the same floral primordium, even explain the presence of bisexual flowers on the inflorescence if the staminate primordia develop into staminodes at a later of all the species of Philodendron studied to date. See Barabe´ stage. and Bertrand (1996), Boubes and Barabe´(1996), and Barabe´ In P. megalophyllum and P. grandifolium, we observed a et al. (2000) for a discussion of this hypothesis within the phenomenon that has not yet been reported in Philodendron framework of the theory of positional information. This gen- species: the presence of atypical organs displaying male and eral framework of floral differentiation (male and female), female characteristics (figs. 1C,4H). These intermediate or- based on the concentration of morphogen(s) at a particular gans, which represent teratological structures, have been re- point along a compact aroid inflorescence, lends itself well to ported in other angiosperm taxa (Gue´de`s 1979). The inter- further studies analyzing the morphogenetic gradients at the mediate nature of these organs indicates that they are under molecular level. the physiological influence of both the neighboring female and male organs. Homeosis The presence of bisexual flowers in the genus Philodendron was first noted by Engler and Krause (1912). Mayo (1986, fig. Recently, studies of floral development in species of Philo- 393) mentioned the presence of bisexual flowers in the species dendron belonging to subgenus Meconostigma (P. solimoe- P. # evansii. Subsequent detailed studies of the anatomy and sense) and Philodendron (P. acutatum, P. fragrantissimum, and development of bisexual flowers in the genus Philodendron P. melinonii) (Boubes and Barabe´ 1996; Barabe´ et al. 1997, were conducted in three species of the subgenus Philodendron, 2000; Barabeánd Lacroix 1999) have shown that in the case P. acutatum (Boubes and Barabe´ 1996), P. fragrantissimum of bisexual flowers, carpels have been replaced by sterile sta- (Barabeét al. 1997, 2000), and P. melinoii (Barabeánd Lacroix mens on the same whorl. This is a rare case of homeosis in 2000) and in one species of the subgenus Meconostigma, P. which one or more carpels and stamens are found on the same solimoesense (Barabe´ and Lacroix 1999). The developmental floral whorl. At this point, this developmental potential seems morphology of the bisexual flowers in P. grandifolium and P. to be unique to Philodendron. megalophyllum is similar to that of the other species studied Our observations of the homeotic shift between carpels and until now, even though the bisexual flowers of P. fragrantis- staminodes in the bisexual flowers of the intermediate zone in simum present a greater diversity in the gynoecial morphology. P. grandifolium led us to ask the following question: How Nonetheless, in P. grandifolium, the incomplete separation of many carpels are replaced by a staminode? In general, the staminodes from the gynoecial portion of the whorl (fig. 5F) sterile male flowers consist of six or seven staminodes, and the clearly shows that the staminodes and carpels belong to the female flowers have seven or eight carpels. The bisexual flowers same whorl. represented in figure 5D–5H have five to six appendages con- As was the case for the other species of Philodendron studied sisting of a variable number of carpels (C) and staminodes (St): until now (P. acutatum, P. fragrantissimum, P. melinonii, and 5C+1 St (two flowers in fig. 5D), 4 C+2 St (fig. 5F), 4 C+1 St P. solimoesense), there is a morphogenetic gradient in the in- (fig. 5G, BF), 3C+2 St (fig. 5E,5H), and 2 C+3 St (fig. 5H). termediate zone of the inflorescence corresponding to a qual- There are two ways to analyze the nature of bisexual flowers. itative variation in the nature of the appendages that are ini- One can assume that the bisexual flower is a modified female tiated. This results in a continuous morphological transition flower or a modified staminate sterile flower. The determina- in sexuality between pistillate flowers, bisexual flowers, sterile tion of the number of carpels and staminodes involved in the staminate flowers, and staminate flowers. This morphological homeotic change will not be necessarily the same in both cases. transition is even visible on individual bisexual flowers where In our previous studies (Boubes and Barabe´ 1996; Barabe´ the portion facing the female zone of the inflorescence displays and Lacroix 1999, 2000; Barabeét al. 2000), we have always

Fig. 5 Variation in the developmental morphology of bisexual flowers of Philodendron grandifolium. The tip of the inflorescence in relation to each photograph is oriented toward the top of the plate. A, Early stage of initiation of floral primordia (small bumps) in the intermediate zone. Bar p 75 mm. B, Early stage of initiation of floral organs in the intermediate zone at the level of bisexual flowers (BF) and sterile male flowers (SMF). Bar p 150 mm. C, Sterile male flowers consisting of five to seven staminodes (arrowheads). Bar p 150 mm. D, Two bisexual flowers (A, B) each consisting of one staminode (St) and five carpels (arrowheads) inserted on a single whorl. Bar p 75 mm. E, Bisexual flower (BF) consisting of two staminodes (St) and three carpels (arrowheads), also inserted on a single whorl. Bar p 75 mm. F, Bisexual flower (BF) with four carpels (arrowheads) and one, possibly two, staminodes (St). Note that one staminode is fused with the gynoecium (arrow). Bar p 150 mm. G, In the intermediate zone, bisexual flowers (BF), sterile male flowers (SMF), and female flowers (F) are often closely associated. Bar p 150 mm. H, At later stages of development (as represented on this photo), it is difficult to determine exactly which staminodes (St) belong to specific bisexual flowers (BF). Bar p 150 mm. 56 INTERNATIONAL JOURNAL OF PLANT SCIENCES interpreted the bisexual flowers as modified female flowers. transformations involving carpels and stamens and the pres- Consequently, if we consider that the total number of ap- ence of extracellular calcium oxalate crystals on stamens. This pendages in bisexual flowers should be equivalent to the total study, in combination with previous work, shows that the Ara- number of carpels in female flowers, we can deduce that one ceae in general and the genus Philodendron in particular pre- staminode replaces one to four carpels. For example, in the sent us with a great diversity of structure/function relationships case of a flower with 4C+2 St, one staminode could replace relating to mechanisms of floral biology. Until now, the study one, two, or three carpels given the hypothesis that the total of homeosis beyond Arabidopsis and Anthirrinum has been number of appendages should be equal to seven or eight in a conducted mainly at the morphological level. However, with bisexual flower. In the case of a flower with 4C+1 St, one the development of molecular techniques, we think that it will staminode could replace three or four carpels. On the other be possible to attempt to characterize the morphogenetic gra- hand, if we consider that a bisexual flower is a modified male dients at the molecular level in the near future. sterile flower, each carpel would replace one or at most two staminodes. From this perspective, we would be dealing with a higher frequency of one to one shift or replacement. Presently, Acknowledgments it is very difficult to test these two hypotheses without a careful quantitative analysis, one that takes into account the size and D. Barabe´would like to thank Dr. Philippe Cerdan for per- the number of appendages of the different types of flowers mission to work at the Laboratoire de Petit Saut (French Gui- along the inflorescence. However, there is one morphological ana) in May and November 1997. Thanks also to Dr. Jean- conclusion that we can make from both interpretations. In Jacques de Granville for permission to work at the Herbier de bisexual flowers in P. grandifolium, a staminode can take the Guyane (ORSTOM, Cayenne) and to Dr. Alain Dejean (July place of one or more carpels. The range in number of carpels 1998), Dr. Marc Gibernau (July 1998), and Mr. Manfred Korel remains to be determined quantitatively. This variability in the (November 1997) for their help in collecting specimens. This number of carpels replaced by a staminode indicates that the research was supported in part by grants from the Natural homeotic transformation is zonal rather than a one-to-one, Sciences and Engineering Research Council of Canada to D. organ-specific replacement. Barabe´ and C. Lacroix and by the Fonds Pour la Formation The unique morphology of the inflorescence of P. grandi- de Chercheurs et l’Aide a`la Recherche (Que´bec) to a team of folium and P. megalophyllum allowed us to study two poorly the Institut de Recherche en Biologie Ve´ge´tale, of which D. known phenomena in the flowers of angiosperms: homeotic Barabeís a member.

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