AOBPreview originally published online on March 20, 2008
Annals of Botany 2008 101(7):1027-1034; doi:10.1093/aob/mcn031
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Quantitative Developmental Analysis of Homeotic Changes in the Inflorescence of Philodendron (Araceae)
1 Institut de recherche en biologie végétale, Jardin botanique de Montréal, Université de Montréal, 4101 Sherbrooke Est, Montréal, H1X 2B2, Canada
2 Department of Biology, University of Prince Edward Island, 550 University Avenue, Charlottetown, PEI, C1A 4P3, Canada
* For correspondence. E-mail denis.barabe{at}umontreal.ca
Received: 11 January 2008 Returned for revision: 31 January 2008 Accepted: 14 February 2008 Published electronically: 20 March 2008
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Background and Aims: The inflorescence of Philodendron constitutes an interesting morphological model to analyse the phenomenon of homeosis quantitatively at the floral level. The specific goals of this study were (1) to characterize and quantify the range of homeotic transformation in Philodendron billietiae, and (2) to test the hypothesis that the nature of flowers surrounding atypical bisexual flowers (ABFs) channel the morphological potentialities of atypical bisexual flowers.
Methods: Inflorescences of P. billietiae at different stages of development were observed using SEM. The number of appendices in male, female and sterile flowers were counted on 11 young inflorescences (5–6 flowers per inflorescence). The number of staminodes and carpels on ABFs were counted on 19 inflorescences (n = 143). These data were used for regression and ANOVA analyses.
Results: There was an average of 4·1 stamens per male flower, 9·8 carpels per female flower and 6·8 staminodes per sterile male flower. There was an average of 7·3 floral appendices per atypical flower. Staminodes and carpels are inserted on the same whorl in ABFs. A negative exponential relationship was found between the average number of staminodes and the number of carpels in ABFs. If only the ABFs consisting of less than six carpels are considered, there is a linear relationship between the number of carpels and the average number of staminodes. The value of the slope of the regression equation indicates that on average, in P. billietiae, 1·36 carpels are replaced by one staminode.
Conclusions: In P. billietiae, the number of appendages in female flowers imposes a constraint on the maximum total number of appendages (carpels and staminodes) that can develop on ABFs. The quantitative analyses indicate that the average number of different types of floral appendages on an ABF and the number of organs involved in a homeotic transformation are two independent phenomena.
Key words: Philodendron, positional information, gradient, flower, homeosis, developmental constraint
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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The phenomenon of homeosis, defined in plants as the complete or partial replacement of one type of organ by an organ of different nature (Lehman and Sattler, 1992; see also Sattler, 1988, and Vergara-Silva, 2003 for a review of this concept in developmental plant morphology), is believed to play an important role in the ontogeny and phylogeny of reproductive structures (Sattler, 1994; Frohlich and Meyerowitz, 1997; Mouradov et al., 1998; Purugganan, 1998; Winter et al., 1999; Ambrose et al., 2000; Becker et al., 2000; Kramer and Irish, 2000; Theißen, 2001; Lee et al., 2003; Nagasawa et al., 2003; Ronse de Craene, 2003; Yamaguchi et al., 2004; Adam et al., 2005). The inflorescence of Philodendron constitutes an interesting morphological model to analyse the phenomenon of homeosis quantitatively at the floral level (Barabé et al., 2000, 2002, 2004).
In Philodendron, as in other members of the subfamily Aroideae, sensu Mayo et al. (1997), the female flowers are located in the lower portion of the inflorescence and the male flowers in the upper portion. These two zones are separated by a zone of sterile male flowers. Between the sterile-male zone and the female zone there is a row of atypical bisexual flowers (Engler and Krause, 1912, p. 16; Mayo, 1986, fig. 393). These atypical bisexual flowers (ABFs) consist of carpels and staminodes that are initiated on the same whorl (Barabé et al., 2004). It is important to note that the ABFs are not true functional bisexual flowers. The pistillate portion is fertile, whereas the sterile staminate portion consists of staminodes. Even though from a functional reproductive point of view these flowers remain unisexual, they can be considered as bisexual from a developmental point of view because pistillate and staminate primordia are initiated on the same flower (Barabé et al., 2004).
Our previous studies have allowed us to analyse the range of homeotic transformations in the genus Philodendron and to deduce common patterns of development in ABFs belonging to different species (Boubes and Barabé, 1996; Barabé et al., 2000, 2002, 2004). The ABFs arise through the homeotic replacement of carpels with staminodes. However, is this pattern of development common to all species of Philodendron? The great number of species belonging to the genus Philodendron (approx. 700) does not allow us to claim that the developmental morphology is similar for all species (Barabé and Lacroix, 2008). Although the overall developmental morphology of the inflorescence of Philodendron is consistent (Mayo, 1989), one may expect to find some variability in the number of appendages involved in the homeotic process in a genus consisting of several hundred of species.
In species of Philodendron studied previously, it was hypothesized that the number of appendages present in sterile and female flowers tends to act as a constraint on the number of appendages in ABFs (Barabé and Lacroix, 2008). How does the number of carpels in female flowers influence the morphology of atypical bisexual flowers found in this zone of transition? This question has been addressed in a quantitative analysis of species characterized by female flowers with a small number of carpels (4–6) or a great number of carpels (28). The variations appearing in ABFs have been quantified in a few species (P. fragrantissum, P. melinonii, P. pedatum, P. squamiferum, P. solimoesense) to determine if there is a common pattern in the homeotic shift in ABFs (Barabé et al., 2004). It was shown that on average the number of carpels replaced by a staminode can vary from one (e.g. P. squamiferum) to 2·6 (P. solimoesense).
The previous analyses were based on a small number of samples and did not take into account species such as Philodendron billietiae with female flowers having a number of carpels that falls between the extremes measured in other studies. The lack of quantitative developmental studies in the genus Philodendron is due in great part to the difficulty in obtaining enough material to analyse the range of early stages of development statistically. However, we were recently able to obtain enough samples of Philodendron billietiae at different stages of development to extend our survey. The analysis of this species allows us to deduce certain rules of homeotic transformation that could potentially be generalized across the genus Philodendron.
Our hypothesis is that the number of appendages present in female flowers acts as a border condition or constraint on the number of appendages that develop in ABFs. The main goal of this study was to determine if there is a theoretical limit to the potential number of appendages that can appear in ABFs.
As pointed out previously (Barabé et al., 2004), given the morphological complexity and the mode of growth of the inflorescence of the Araceae, it is not possible to test this hypothesis experimentally under controlled conditions. However, since the number of appendages involved in the formation of female flowers, sterile male flowers, male flowers and ABFs varies considerably between species, the above hypothesis can be tested by making a quantitative comparison between species with different numbers of floral appendages in female, male or sterile male flowers. For example, is the empirical rule of organ replacement calculated in P. melinonii, P. pedatum, P. squamiferum and P. solimoesense also valid in a species with an intermediate number of female flower appendages? Do the female flowers exert a constraint on the number of appendages that can potentially form in ABFs of all species of Philodendron?
In the general context of the development of the inflorescence and flowers of the Araceae, the specific goals of this study were: (1) to characterize and quantify the range of homeotic transformation in Philodendron billietiae; (2) to test the hypothesis that the nature of flowers surrounding atypical bisexual flowers channel the morphological potentialities of atypical bisexual flowers; (3) to determine if there is an empirical homeotic transformation rule in the inflorescence of Philodendron; and (4) to integrate the developmental morphology of the inflorescence of Philodendron billietiae in the general framework of floral homeosis in angiosperms.
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MATERIAL AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Samples
Philodendron billietiae Croat belongs to the subgenus Philodendron (Croat, 1997). Specimens used for this study were collected in French Guiana (Petit-Saut road) in 2006 and 2007 (voucher specimen deposited at MT: Barabé 36). Inflorescences at various stages of development were dissected under a stereo microscope to expose the spadix, fixed in formalin–acetic acid–alcohol (1:1:9 by volume), and then transferred and stored in 70 % ethanol.
Microscopy
Twelve inflorescences of P. billietiae were dehydrated in a graded ethanol series to absolute ethanol. They were then dried in a LADD model 28000 critical-point dryer using CO2 as a transitional fluid, mounted on metal stubs, and grounded with conductive silver paint. Specimens were sputter coated with gold/palladium to approximately 30 nm using a Denton Vacuum Desk II sputter coater, and viewed with a Cambridge S604 scanning electron microscope (SEM) with digital imaging capabilities (SEMICAPS®).
Quantitative analysis
The number of appendices in male, female and sterile flowers were counted on 11 young inflorescences (5–6 flowers per inflorescence). The number of staminodes and carpels on atypical bisexual flowers (ABFs) visible on an inflorescence were counted on eight specimens using the SEM and on 11 specimens using a binocular stereo microscope. These data were used for regression and ANOVA analyses. The normal distribution of residuals and homoscedasticity were verified before the application of statistical tests. All analyses were performed using STATISTICA [Statistica 6·0 (2001), StatSoft Inc., Tulsa, OK).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Floral developmental morphology
Morphology of the mature flowers
The length of the mature spadices of P. billietiae ranged from 16 to 18 cm (Fig. 1A). Both staminate and pistillate flowers lack a perianth. The staminate flowers occupy the upper portion of the inflorescence and make up more-or-less 50 % of the total length of the inflorescence (Fig. 1A, B), whereas the female flowers are located on the lower portion and occupy approx. 40 % of the total length (Fig. 1A, E). Modified stomata in the sense of Vogel (1977) are found on the surface of the apical portion of the stamens (Fig. 1C) and staminodes on male and sterile male flowers, respectively. The epidermis of stamens and staminodes consists of pegged and ridged cells giving the surface a rough appearance (Fig. 1B). Mature female flowers have a prominent stigmatic surface (Fig. 1E).
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Between the male and the female portions of the inflorescence, there is an intermediate zone (approx. 10 % of the total length of the spadix) consisting of sterile male flowers and atypical bisexual flowers (Fig. 1A, D). Atypical bisexual flowers are inserted at the boundary between the sterile-male zone and the female zone. They generally consist of carpels and staminodes inserted on the same whorl. In mature flowers, it is difficult to determine whether the staminode(s) and carpels are inserted on the same whorl (Fig. 1D). However, during early stages of development this phenomenon is visible (see Fig. 4G; see section on floral development of atypical bisexual flowers, below). The portion of the bisexual flower facing the male zone consists of staminodes, and the portion facing the female zone consists of an incomplete gynoecium (Fig. 4G).
Inflorescence and floral development
The inflorescence of P. billietiae is more-or-less cylindrical in shape during early stages of development (Fig. 2A, B). The different types of flowers are initiated acropetally along the axis of the inflorescence (Fig. 2A). Pistillate flowers develop near the basal portion of the inflorescence and staminate flowers develop on the terminal portion. At this stage of development, the primordia of the intermediate zone are not as clearly outlined as those of the other two zones (Fig. 2A). The floral primordia of the female zone cover approximately one-quarter of the inflorescence at this very early stage (Fig. 2A). Once all the floral primordia have been initiated, the different types of flowers are all approximately the same size and form a regular lattice on the surface of the inflorescence (Fig. 2B, C). At this point, there is no discontinuity in the phyllotactic pattern of the flowers across the different zones of the inflorescence. Pistillate flowers, sterile male flowers, atypical bisexual flowers and staminate flowers are inserted on the same phyllotactic spirals in the lattice (Fig. 2C). The flowers of the intermediate zone appear more-or-less organized in comparison to the male and female zones (Fig. 2C). The fusion of primordia belonging to the same parastichy (Fig. 2C, marked *) or two different parastichies (marked **) can sometimes be observed. When the floral organs are initiated, the regular arrangement of the flowers of the male and sterile zone and the recognition of symmetrical patterns become less evident (Fig. 2D).
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Stamen primordia are initiated simultaneously on the periphery of more-or-less circular floral primordia (Fig. 3A). There is an average of 4·1 (± 0·71, s.d.; n = 61) stamens (range 3–6) per flower (Fig. 3B, C). During later stages of development, the floral primordia come in contact with each other and the size of the stamens increases to the point that they eventually occupy all the available space between flowers (Fig. 3D, E).
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The presence of extracellular calcium oxalate crystals, as described by Barabé et al. (2004), can be observed on the upper surface of young stamens (Fig. 3F). These crystals were not observed on mature structures. The accumulation of extracellular calcium oxalate crystals occurs during the early stages of development of floral organs, when an inflorescence has reached approx. 15 % of its final length.
During early stages of development, female floral primordia have a hemispherical shape (Fig. 4A). The carpel primordia are initiated on the periphery of the floral primordia. During later stages of development, the entire ovary wall of typical flowers is formed by the concrescence of the walls of adjacent carpels (Fig. 4B, C). There is an average number of 9·8 (± 1·05, s.d; n = 68) carpels (range 7–12) per flower. The small holes that are visible on the periphery of floral primordia during later stages of development represent the upper portion of the stylar canals (Fig. 4D). Even though the carpels are concrescent, individual stylar canals are found in the mature ovary up to a level directly below the stigmatic surface.
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The sterile male flowers and atypical bisexual flowers (ABFs) form a transition zone between typical male and female flowers. The staminodes of sterile male flowers are initiated on the periphery of the floral primordium in the same manner as the male flowers (Fig. 4E). There is an average number of 6·8 (± 0·90, s.d., n = 67) staminodes (range 5–8) per sterile male flower. During early stages of development, the primordia of sterile male flowers and ABFs have approximately the same shape as the primordia of staminate flowers (Figs 3B and 4F). Although the floral organs of the sterile male flowers and ABFs are initiated later than those of the pistillate flowers, their relative rate of growth is faster than that of the other types of flowers. Consequently, sterile male flowers and ABFs are larger than female flowers at maturity due mainly to the expansion of the staminodes (Fig 4G).
ABFs form a more-or-less continuous single row on the inflorescence and are located directly below the sterile male flowers (Figs 4G and 5A). The floral organs are initiated on the periphery of a discoid floral primordium, and their nature, number and form vary considerably (Fig. 5A). There is an average of 7·3 (± 1·20, s.d.; n = 143) floral appendices (range 5–11) per flower. The types of floral organs produced on bisexual flowers depend greatly on their proximity to the other floral zones. The female organs of ABFs tend to be initiated on the side of the flower adjacent to the female zone and the male organs are initiated on the side of the flower closer to the sterile-male floral zone (Fig. 5B–D). In our samples, the number of carpels in ABFs ranged from one to ten and the number of staminodes from one to seven. Even though floral organs are easily identifiable to specific flowers during early stages of development, it becomes difficult to determine which staminodes belong to which flowers during later stages of development (Figs 4G and 5E).
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The staminodes and carpels on ABFs are inserted in a single whorl in a ring formation (Fig. 5B, C). Some flowers have more carpels (Fig. 5B, flowers ‘A’ and ‘B’) while others have more staminodes (Fig. 5D, flower ‘B’). In many ABFs, there is an incomplete separation between staminodes and carpels. Figure 5D shows an ABF where the staminode is united to the gynoecium by a portion of the ovary wall (arrow). It is often difficult to determine whether the aberrant structures correspond to an open carpel or a staminode. For example, in Fig. 5C, the flower on the right side of the micrograph (arrow) consists of one staminode, five closed carpels and two aberrant structures corresponding to open carpels (see arrows). From a morphological point of view, these aberrant structures could also be interpreted as staminodial primordia that are incompletely separated from adjacent carpels. In Figure 5D, ABFs (‘A’ and ‘B’) have an anamorphous configuration where the delimitation between carpels and staminodes is not clear. These morphological observations provide strong evidence that staminodes and carpels are inserted on the same whorl in ABFs.
Quantitative relationships between staminodes and carpels in ABFs
There is a negative correlation between the average number of staminodes and the number of carpels in ABFs (Fig. 6). An ANOVA analysis indicated that there is a link between the number of carpels and the number of staminodes. If we take into account all ABFs (number of carpels ranging from one to ten) there is an exponential relationship of the form y = 6·65e–0.20x between the mean number of staminodes (y) and the number of carpels (x). The regression is quasi-linear from one to five carpels. The non-linearity of the relationship is particularly accentuated in flowers with a high number of carpels (6–10).
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The average number of staminodes is significantly different between bisexual flowers having one-to-five carpels and flowers having six-to-ten carpels. The average number of staminodes decreases as the number of carpels increase. However, if we consider only the ABFs with less than six carpels (first part of the curve) there is a linear relationship between the number of carpels (x) and the average number of staminodes (y), represented by the equation y = 6·0–0·73x (Fig. 7) or x = 8·2–1·36y. The value of the slope of these equations indicates that on average, in P. billietiae, 0·73 staminodes replace one carpel (first equation), or 1·36 carpels are replaced by one staminode (second equation). The equation x = 8·2 –1·36y indicates that the average theoretical total number of carpels (1·36 staminodes + carpels) is equal to 8·2. (C.I. ± 0·02).
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Based on this result, if we replace one staminode by 1·36 carpels in each ABF, we obtain the curve presented in Fig. 8. This clearly shows that with up to five carpels the substitution does not change the total theoretical number of appendages (between 8 and 8·5). However, above five carpels, the theoretical total number increases rapidly, due to the greater number of carpels.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Floral development
The pattern of floral development on the inflorescence of P. billietiae is comparable to that previously described in other species of Philodendron (Barabé et al., 2004). The development of atypical bisexual flowers (ABFs) in P. billietiae also follows what has been observed in other species: there is a homeotic transformation of carpels into staminodes on the same whorl (Barabé et al., 2004). The existence of sterile stamens (staminodes) and carpels on the same whorl in ABFs of Philodendron indicates that the identity of organs that will be formed is independent of the floral whorl on which they arise. This is in accordance with the idea that floral organ identity is whorl independent (Coen and Meyerowitz, 1991; Bossinger and Smyth, 1996). In the case of P. billietiae, the nature of the floral organs that will be formed depends on their position along the axis of the inflorescence.
The average total number of appendages on ABFs may exceed that of staminodes on sterile male flowers but is never greater than the number of carpels on female flowers. Additionally, the number of staminodes in ABFs is always lower than the number of staminodes in sterile male flowers. The negative exponential relationship between the average number of staminodes and the number of carpels (Fig. 6) shows that in ABFs with more than five carpels the potential to form staminodes is considerably reduced. The diminution in the number of staminodes is faster than the increase in the number of carpels. This indicates that the total number of appendages on ABFs is influenced to a greater extent by female flowers than sterile male flowers. The number of appendages in female flowers may consequently be imposing a constraint on the maximum total number of appendages (carpels and staminodes) that can develop on ABFs (Barabé and Lacroix, 2008). On the other hand, the number of staminodes in sterile male flowers constrains the maximum number of staminodes that can develop in ABFs. Previously it has been shown that the total number of appendages in ABFs is strongly correlated with the number of appendages in female flowers (R2 > 0·94; Barabé et al., 2004). Based on these results, it might be concluded that ABFs represent modified female flowers (Barabé and Lacroix, 2001, 2008; Barabé et al., 2004). This could explain why the number of appendages in ABFs never exceeds that of female flowers. The number of appendages in ABFs would therefore depend on the ‘femaleness’ of the abnormal flowers while the type of appendages (carpels or staminodes) that form on the floral primordia would depend on their position on the inflorescence; see Barabé and Lacroix (2008) for an analysis of this phenomenon in the context of constraints at different hierarchical levels.
In P. billietiae, the pathway of floral differentiation (male or female) may be interpreted in terms of morphogenetic gradient and concentration of hormones acting more or less simultaneously at a particular point along the inflorescences, as has been hypothesized for the other species of Philodendron (Barabé et al., 2000, 2004). Since the flowers that develop in the zone of ABFs may be experiencing the influence of both sets of conditions that lead to the formation of female flowers and sterile male flowers, it can be hypothesized that the row of ABFs is located at the threshold of transition between two or more substances that cause a fluctuation in the number and nature of appendages (Barabé and Lacroix, 2008).
Quantitative relationships
In P.billietiae, as in P. squamiferum, P. pedatum, P. melinonii and P. solimoesense, there is a significant correlation between the number of carpels and the number of staminodes in ABFs. This indicates that there is a certain degree of regularity in the number of organs involved in the homeotic transformation occuring in ABFs. The slopes of the regressions indicate that one (P. pedatum and P. squamiferum), 1·33 (P. melonii) and 2·56 (P. solimoesense) carpels are replaced by one staminode depending on the species. However, in species where the total number of appendages developing in ABFs is very small (e.g. 2–4 in P. insigne) there is an absence of correlation between the number of carpels and the number of staminodes (Barabé et al., 2004). In P. fragrantissimum, there is no significant correlation between the number of carpels and the number of staminodes in ABFs; it is also the only case where the value of the slope of the regression is superior to –1 (–0·62; table 3 in Barabé et al., 2004). In this species the total number of appendages ranges from four to eight, and there are just a few carpels that are transformed into staminodes per flower. Therefore the absence of correlation in this species could be due to the great variability in the number of carpels (1–7) in relation to the number of staminodes (1–2; Barabé et al., 2004).
In P.billietiae, the slope of the regression x = 8·2–1·36y indicates that 1·36 carpels replace one staminode when there are less than six carpels per female flowers. This is similar to what has been observed in P. melinonii (table 3 in Barabé et al., 2004), where there is an average of 4·6 carpels per female flowers and 4·2 appendages (carpel + staminodes) in ABFs. However, in P. billietiae there is an average number of 9·8 carpels in female flowers and 7·5 appendages in ABFs. Although the ratio between the average nunber of carpels in female flowers and staminodes in sterile male flowers (9·8/4·1) is higher in P. billietiae than in P. melinonii (4·8/4·6), the number of carpels (1·36 and 1·33) replaced by a staminode is essentially the same. In P. solimoesense, there are three times more carpels than staminodes, and there is on average a substitution of one staminode for 2·56 carpels (Barabé et al., 2004). This indicates that the average number of different types of floral appendages on an ABF and the number of organs involved in a homeotic transformation are two independent phenomena. This quantitative result is in accordance with recent molecular studies that have shown that organ identity and organ number per whorl are indeed controlled by two different groups of genes (e.g. Huang and Ma, 1997; Running et al., 1998).
The total average number of appendages in ABFs is probably related to the size of the floral primordium and the corresponding available space for the initiation of floral organs (See Barabé et al., 2004 for a discussion). A small change in the diameter of the floral primordium will have a greater influence on the available space (i.e. overall surface area) in larger flowers than in small flowers as far the formation of carpels is concerned. This could explain why the total number of appendages increases more rapidly in flowers with more than five carpels (Figs 6 and 8).
Even though our statistical analyses cannot predict the precise number of homeotic transformations that will take place in a given ABF, they show that there is some regularity in the homeotic transformations occuring species of Philodendron. The total number of carpels in female flowers channels the number of organs that will be involved in a homeotic transformation. However, the average number of different types of floral appendages on an ABF and the number of carpels that are replaced by a staminode are two independent phenomena.
The unique morphology of the inflorescence of Philodendron, where different types of flowers are regularly placed along a cylinder, constitutes an interesting system to study a poorly known phenomenon in angiosperm flowers: quantitatively varying homeotic transitions involving carpels and stamens on the same floral whorl. Based on available data thus far, the genus Philodendron presents us with a wide variety of structural relationships relating to mechanisms of homeosis.
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ACKNOWLEDGEMENTS |
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D. B. would like to thank the staff of the Laboratoire Environnemental de Petit Saut (French Guiana) and Alain Dejean for technical support. This research was supported in part by individual operating grants from the Natural Sciences and Engineering Research Council of Canada to D.B. and C.L.
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LITERATURE CITED |
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  Compiled by, F. Tooke, T. Chiurugwi, and N. Battey Flowering Newsletter bibliography for 2008 J. Exp. Bot., June 23, 2009; (2009) erp154v1. [Full Text] [PDF]
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