Plant Evo-Devo of the Gynoecium: Heterotopy, redefinition of the carpel, and a topographic approach



Morpho Evo-Devo of the Gynoecium: Heterotopy, redefinition of the carpel, and a topographic approach


Rolf Sattler


Abstract: For more than two centuries we have had countless debates, sometimes acrimonious, about the nature of the gynoecium. A pivotal question has been whether all angiosperms possess carpels (closed megasporophylls) or if there exist also acarpellate gynoecia lacking carpels. We can resolve these debates if we don’t define the carpel as an appendage that bears and encloses the placenta or a single ovule but redefine it instead simply an appendage that encloses the placenta or a single ovule. This redefinition may, however, lead to confusions because often it may not be clear whether the traditional (classical) definition or the redefinition is implied. Therefore, a topographic approach is proposed that is aligned with the redefinition. According to this approach, gynoecia comprise gynoecial appendages and placentae or ovule(s) that may be a formed in different positions. Heterotopy refers to these different positions. In the context of evo-devo, which explores evolutionary changes in development, with regard to the gynoecium, morpho evo-devo delves into spatial shifts of the placentae or ovule(s) leading to heterotopy. Furthermore, it considers shifts in timing (heterochrony) and other processes leading to heteromorphy. Recognizing spatial shifting of the placentae or a single ovule and other evolutionary processes opens up new vistas in the search for the ancestor(s) of angiosperms and their gynoecia.

Keywords: Plant evo-devo, plant morpho evo-devo, gynoecium, carpel, gynoecial appendage, spatial shifting, heterotopy, topographic approach, fossil angiosperms and pre-angiosperms, flower concept


1. Introduction

Plant Evo-Devo investigates the evolution of plant development. It integrates evolutionary theory, morphology, and molecular genetics. Morpho evo-devo emphasizes the morphological aspects of evo-devo
(Wanninger 2015, Petrone-Mendoza et al. 2023). Thus, in this article the focus will be on the morphological evolutionary changes in the development of the gynoecium.
According to mainstream thinking, the gynoecium consists of carpels. However, the carpel concept can be unambiguously applied only to a limited extent. I shall therefore present a redefinition of the carpel that applies to a much greater extent; and in line with and as an elaboration of this redefinition, I shall propose a topographic approach to the gynoecium that overcomes problems and pseudo-problems in gynoecial morphology. Heterotopy of ovules and placentae, due to spatial shifting, plays a crucial role in the topographic approach, in morpho evo-devo, and the search for the ancestral condition of the gynoecium.

2. Definition of the Carpel

Classical morphology originated with Goethe’s Metamorphosis of Plants (Goethe 1790). It still dominates morphological thinking up to the present time. According to classical morphology, a carpel is an appendage that bears and encloses ovule(s), it is a closed megasporophyll (e.g., Endress 2019, Kaplan 2022). But in an extensive review of the literature, Brückner (2000) distinguished ten different interpretations of the carpel or gynoecial unit based on different interpretations of the gynoecium and its presumed evolutionary and phylogenetic origin. Since the 19th century, these divergent interpretations have led to nearly countless arguments and controversies. Lorch (1963), in a historical overview of the carpel concept, concluded that "even on its own, classical morphology upon advancing toward smaller and less obvious targets would have found itself confronted with the breakdown of the concept of the carpel.” Thus, first I want to examine problems and pseudo-problems with the classical carpel concept.

3. Do all Gynoecia have Carpels?


According to mainstream thinking (classical morphology), one of the defining characteristics of angiosperms is the possession of classical carpels (closed megasporophyhlls). Hence, all gynoecia in angiosperms are considered carpellate. However, based on developmental studies, this claim has been contradicted or has at least become questionable. Of course, many taxa of angiosperms have classical carpels (megasprophylls), but for a considerable number of other taxa, it is difficult or impossible to apply the classical carpel concept (see, for example, Sattler and Lacroix 1988). Developmental investigations indicate that in these cases the centre of the gynoecium is transformed into a single ovule or a placenta that bears the ovules (see, for example, Macdonald and Sattler 1973, Sattler and Lacroix 1988), or an ovule is formed in the axil of gynoecial primordia (Pauzé and Sattler 1979, Zhang et al. 2019). Nonetheless, classical morphologists such as Endress (2019) and Kaplan (2022) insist that all gynoecia are carpellate. Endress (2019) claimed that in gynoecia with a terminal ovule or placenta (where the ovule or placenta arises in the centre of the gynoecium) the young carpels “are 'rooted' within the remaining floral apex." How can he delimit these carpellary roots from the floral apex? It seems difficult or impossible to draw a line between the floral apex and carpel primordia. Enquiring about the limit of primordia were none exists in nature seems to be a pseudo-problem. To avoid this pseudo-problem, one could postulate a congenital fusion of the base of the carpel primordium with underlying tissue and the floral apex so that carpellary tissue would cover the floral apex (see Sattler 1974). But congenital fusion is a “fusion,” that, by definition, is in principle unobservable because usually it does not involve any observable fusion. Hence, the admission of this concept removes the empirical basis of morphology. Furthermore, if a central terminal ovule is claimed to belong to a carpel, the question would be to which one when more than one is present. For example, in
Myrica gale, the gynoecium has two gynoecial appendages and one terminal ovule (Macdonald and Sattler 1973). If these two gynoecial appendages are interpreted as carpels, then the ovule should belong to one of them, shouldn’t it? But to which one? No known observation, including vascularization, indicates that the ovule is more closely connected to one of the two carpels. Thus, it is left hanging in between.
In any case, concerning the concept of congenital fusion, from the perspective of morpho evo-devo, the challenge is to discover the observable developmental processes that are subsumed and often hidden by the concept of congenital fusion. Sattler (1978) distinguished the following processes: zonal growth, heterotopy, meristem extension, and interprimordial growth (meristem fusion). Sokoloff et al. (2018, p. 18) equate congenital fusion with zonal growth, which is only one of the processes subsumed under the concept of congenital fusion. But note that zonal growth does not imply any kind of fusion. Heterotopy also does not involve any kind of fusion. neither does meristem extension. Only interprimodial growth involves the fusion of meristems, a process that can be observed. Thus, among all the processes subsumed under the concept of congenital fusion, interprimordial growth seems to be the only one that constitutes a process of fusion. But invoking interprimordial growth between the base of gynoecial primordia and the floral apex would not render a basal ovule or a central placenta carpelllary because the floral apex would remain in the centre. However, further clarification of developmental processes subsumed under the term congenital fusion appears desirable. In any case, for morpho evo-devo the basis must be the elucidation of developmental processes that change during evolution and that are at least in principle observable. If this condition is not fulfilled, morpho evo-devo and morphology lose their empirical basis. But my aim is to place morpho evo-devo and morphology on an empirical basis.
One might avoid the problem of congenital fusion by assuming that as a result of the formation of gynoecial primordia the floral apex is used up and thus disappears so that the base of the gyoecial primordia extends into the centre of the gynoecium. However, in taxa such as
Basella rubra (Sattler and Lacroix 1988), the centre of the gynoecium retains the organization of a typical floral apex, which then is gradually transformed into an ovule. Hence, the gynoecium has been considered acarpellate. Nonetheless, the controversy about acarpellate gynoecia continues (e.g. Endress 2019, Sattler and Rutishuaser 2023). But a redefinition of the carpel and a topographic approach can end and supersede this longstanding controversy.

4. Redefining the Carpel

Instead of concluding that there are carpellate and acarpellate gynoecia, an alternative would be a redefinition of the carpel concept in such a way that most of the acarpelllate or questionable gynoecia would become carpellate. According to one redefinition, the carpel is a gynoecial appendage that encloses ovule(s) but does not necessarily bear them (Sattler and Lacroix 1988; Greyson 1994; Leins and Erbar 2010, in their glossary only). With regard to Caryophyllales, Ronse De Craene (2021) pointed out a "progressive detachment of ovules from the carpellary tissue." Also in the Caryophyllales, Cresens and Smets (1989) referred to "topographically cauline placentation."
It seems what matters most is that the placenta or ovule(s) are enclosed and whether they are borne on the gynoecial appendage or the floral apex is not of great importance for the survival of the species. Therefore, instead of claiming that all angiosperms have carpels that bear ovules, I conclude that most angiosperms have gynoecial appendages that alone or in conjunction with underlying tissues, enclose ovules. The enclosure of ovules then becomes the defining characteristic for most angiosperms.
Although this redefinition of the carpel concept is broader than the classical carpel concept and supersedes problems and pseudo-problems of the latter, it still has a potential weakness, because in any particular case someone might ask whether the ovule(s) are borne on the carpel or on the floral apex. But how do we answer this question? We would have to delimit the carpel primordium from the floral apex. It is, however, difficult or even impossible to delimit growth centres such as the carpel primordium and the floral apex. And therefore it may be difficult or impossible to decide whether ovule(s) are borne on the carpel or the floral apex. To overcome this problem, which may be a pseudo-problem,
we proposed to redefine a carpel simply "as an appendage which ENCLOSES ovule(s)" (Sattler and Perlin 1982, p. 181). This redefinition does not require difficult or impossible delimitations and therefore I consider it the most appropriate redefinition. When I refer to redefinition, this one is meant.
Although this redefinition of the carpel broadens the scope of the term, it may lead to confusion unless we always specify whether the term is used in the classical sense as a closed megasporophyll or as redefined. Therefore, instead of the term carpel, I propose using the terms gynoecial appendage and gynoecial primordium that does not require further specification. In my book Organogenesis of Flowers (Sattler 1973), I consistently used these terms. Referring to gynoecial appendages and gynoecial primordia does not imply whether an ovule or placenta is borne on them. These terms specify only the formation of a primordium that develops into an appendage, which is an observable phenomenon. The formation of a placenta or an ovule is then an independent event. The topographic approach is predicated on this distinction of the formation of a gynoecial appendage on the one hand and a placenta or ovule on the other, which is based on the observation of the heterotopy of placentae and ovules. Croizat (1960) already emphasized the importance of this distinction, and Santos and Wang [24] referred to the Unifying Theory (Wang 2018), according to which the carpel is not a closed megasporophyll but “ a composite organ comprising two parts of different nature.” Vasculature has also been used as supporting evidence for this notion (Li et al. 2020).

5. A Topographic Approach to the Gynoecium

The topographic approach specifies the topography, the position of placentae and ovule(s) in relation to the gynoecial primordia and gynnoecial appendages. In this approach the question is no longer whether the placenta or ovule is formed on the floral apex or not. What matters is only their position. We can distinguish the following positions: basal (=central or terminal), axillary, and appendicular; and for the latter, submarginal, ventral, dorsal, and laminar; and, for syncarpous gynoecia, free central, axile, parietal, and superficial. Intermediate positions can also be recognized such as, for example, a near basal ovular position in taxa such as Hordeum vulgare (Sattler 1973). As a result, a continuum of positions can be envisaged.
This topographic terminology has been used by taxonomists for a long time and seems to work well. Since it does not rely on a delimitation of growth centres such as the floral apex and gynoecial primordia, it transcends the classical carpel concept. It can be seen as a liberation from the limitations of the classical carpel concept that has cast a long shadow on gynoecial morphology since the publication of Goethe's Metamorphosis of Plants (1790) (that involved the carpel concept but not the term) and the introduction of the term by F. Dunal in 1817 (see Lorch 1963, p. 271). However, for many morphologists this approach may entail an evasion of interpretation. They would consider the proposed topographic approach only descriptive. But some philosophers, including Nietzsche, have pointed out that all descriptions are interpretations because all descriptions involve concepts that interpret them. Thus,
the proposed topographic approach can be seen as a topographic interpretation of the gynoecium, an interpretation that avoids the phyllome versus caulome categorizations. Furthermore, it avoids the pseudo-problem to find a boundary, such as the boundary of the gynoecial priordium, that does not exist in nature.
One great advantage of the topographic approach is that it allows adherents and defenders of opposite views, the carpellate and cauline interpretation of the gynoecium, can meet and shake hands because they can agree that in free central and basal placentation the placenta or ovule arises in the centre of the gynoecium. Understanding processes such as spatial shifting that leads to heterotopy of the placenta or ovule can be seen as more basic than the structural categories of caulome and phyllome as advocated in process morphology that is beyond structural categories (Sattler 1992).
The topographic approach can redirect research toward more productive avenues since it can liberate us from futile debates about boundaries that do not exist in nature such as the boundaries of gynoecial primordia. Thus, the distinction between carpellate and acarpellate gynoecia, phyllospory and stachyospory (Lam 1950) is transcended (see also Wang 2023). But when placentation is clearly appendicular, the classical carpel concept is still applicable and useful. But even then it is important to recognize that the carpel is not just a phyllome but a composite structure consisting of a more or less foliaceous appendage and a placenta or single ovule.
(As an autobiographical note, I might mention that my morphological thinking about the gynoecium evolved from an acceptance of the classical carpel concept in my doctoral thesis (Sattler 1962), to a distinction of carpellate and acarpellate gynoecia (Sattler 1974), to a redefinition of the carpel (Sattler and Perlin 1982), and finally, in this article, to a topographic approach).
The topographic approach and its terminology is useful in evo-devo in as much as it is based on observable developmental events and their change during evolution. If concepts such as that of the carpel are used, they must be based on developmental events that are at least in principle observable and do not rely on questionable or impossible delimitations of growth centres such as the floral apex and gynoecial primordia.

6. Morpho Evo-Devo of the Gynoecium

In plant morpho evo-devo it is important that we study first the morphological development of gynoecia, which must provide an empirical basis. Then we can ask how different gynoecia may have been transformed into one another. And we find that it is through a number of processes. One of them is spatial shifting, which implies heterotopy, especially heterotopy of the placenta or ovule(s). As a result of heterotopy, the placenta or ovule(s) may arise on the gynoecial appendages, which leads to classical carpels (closed megasporophylls), or in the axil of the gynoecial appendages, or in the centre of the gynoecium. From a topographic perspective, we would simply say that the placenta or ovule(s) may be appendicular, axillary, or basal. Furthermore, a continuum of these positions may be envisaged. A single axillary ovule occurs in Illicium lanceolatum (Zhang et al. 2019), Illicium henryi (Wang et al.) and Ochna atropurpurea (Pauzé and Sattler 1979). An ovule-bearing branch is formed in the axil of gynoecial appendages of atypical gynoecia of Michelia figo (Zhang et al. 2017). In Myrica gale (Macdonald and Sattler 1973), Basella rubra (Sattler and Lacroix 1988), and other taxa the centre of the gynoecium is transformed into an ovule, which means the ovule is basal. Sattler and Lacroix (1988, p. 926) listed many taxa in which the placenta is free central or the ovule is basal (for a more complete list contact Prof. Christian Lacroix, Biology Dept., University of Prince Edward Island, Charlottetown, P. E. I.).
According to classical morphology, appendicular placentation is considered primitive, axillary and basal or central placentation would be derived. The latter could have evolved independently several times. For example, according to Ronse De Craene (2021), even within the Caryophyllales a basal ovule evolved independently several times. Nonetheless, in other taxa, one cannot exclude the possibility of evolution in the opposite direction. And one cannot exclude the possibility that axillary, basal or central placentation may have occurred in early angiosperms or pre-angiosperms, subsequently giving rise to these placentation types in at least some taxa of extant angiosperms.

7. Gynoecia of Fossil Angiosperms and Pre-Angiosperms

The recognition of various positions of the placenta and ovule(s) is not only important for an understanding of gynoecial morphology in extant angiosperms but is also highly relevant for the search for fossil angiosperms and pre-angiosperms. As long as we are blinded by the assumption that all angiosperms have classical carpels (closed megasporophylls), we will look for fossils whose gynoecia resemble classical carpels at least in some ways, maybe megasprophylls that are not yet completely closed. However, bearing in mind the diversity of placentation and ovular position, we are not locked into this view; we can also envisage other possibilities. Thus
Combina gen. nov., discovered in the middle Triassic by Santos and Wang (2022), can be considered a precursor of angiosperms. Combina has an axillary ovule that is almost fully enveloped by a bract. This condition resembles the one reported in taxa such as Illicium as noted above. If this condition is ancestral to the angiospermous gynoecium, then classical carpels (closed megasporophylls) would have evolved through shifting (heterotopy) of the ovule onto the margin of the gynoecial appendage and an increase in its number as it can be seen, for example, in a pea pod. Having many ovules instead of only one axillary one could be seen as advantageous.
Santos and Wang (2022, Fig. 4) proposed an evolutionary trend leading from the fossil Drepanolepis, whose ovule is in the axil of a bract that does not enclose it, to Combina where the bract almost completely encloses the ovule, and then to taxa like Illicium where the ovule is fully enclosed. If this hypothesis can be confirmed, the question remains whether this was the only way how the gynoecium of angiosperms originated or whether additional ways existed as proposed by some authors (e.g., Croizat 1960, 1964; Heads 1984). Wang (2023) concluded: “New knowledge of angiosperms, fossil and extant, seems to suggest that the multiphyly of angiosperms cannot be excluded from the alternative list for the time being.”
In any case, angiosperms have their placenta or ovule(s) enclosed. This enclosure might have evolved in different ways. Wang (2023) referred to a great diversity of ovule-enclosing ways in angiosperms.” Archaefructus, a fossil angiosperm from the early Cretaceous (Sun et al. 2002) has carpels (closed megasporophylls), but they are unusual because the ovules are inserted along the midrib of the carpel (Wang 2018). Their number varies from one to twelve (ibid.). If there is only one ovule, where exactly is it positioned? If it is positioned at or near the axil of the carpel, it would be similar to the position of the axillary ovule of Combina and Illicium. Then, starting with the axillary ovule of Combina, the carpel of Archaefructus could have evolved through an amplification of the number of ovules along the midrib of the carpel. Subsequently, spatial shifting of ovule formation from the midrib towards the margins could have produced the conduplicate angiospermous carpel such as the pea pod. Furthermore, spatial shifting of axillary ovule formation into a ventral median position of an ascidiate carpel could have led to gynoecia of primitive angiosperms such as that of Amborella. Further shifting into the centre of the gynoecium could have produced the basal ovule in gynoecia such as that of Myrica. However, the basal ovule in Myrica and other taxa might also be considered primitive. The Middle Jurassic Qingganninginfructus formosa had a single basal bitegmic ovule (Han et al. 2023). Hence in the Jurassic we find already basal ovules. Furthermore, the Triassic Nubilora, “although not a bona fide angiosperm” (Wang 2019), had ovules directly borne on the floral axis (Wang 2018, Santos and Wang 2022). Taiyuanostachia from the early Permian had ovules and seeds enclosed in lateral appendages (Wang and Fu 2023), but the exact position of the ovules is unknown.
Several alternative hypotheses regarding the origin of angiosperms have been advanced (see, for example, Soltis et al. 2018, Taia 2022). But although the proposed perspective seems more supported by the fossil record, it too remains hypothetical. Nevertheless, we can at least conclude that heterotopy of placentae and ovules occurred in both extant and fossil angiosperms. And this heterotopy includes appendicular, axillary, and basal (central) positions. The latter two appear to be most easily understood through a topographic approach or at least through a redefinition of the carpel, if one wants to retain this term; but, as I suggested, the term “gynoecial appendage” would be preferable.

8. Processes in Morpho Evo-Devo of the Gynoecium

Since morpho evo-devo investigates developmental changes in evolution, it leads to the processes underlying these developmental changes. As pointed out above, one important process is spatial shifting (heterotopy). Within extant Angiosperms, positional shifts may have occurred in various directions [8] (Sattler and Lacroix 1988). Once the placenta or ovule(s) have been enclosed, such shifts would not endanger the survival of such species.
Besides spatial shifting (heterotopy), another process is temporal shifting (heterochrony). An extreme example of heterochrony occurs in
Balanophora elongata: the embryo sac develops already within an elongate floral apex (p. 531). (Zimmermann 1959, p. 531). Hence, no gynoecial appendages and ovules are formed.
In addition to heterotopy and heterochrony, Zimmermann (1959) referred to heteromorphy. The following processes leading to heteromorphy, played an important role in morpho evo-devo of the gynoecium (for details see Sattler 1974, Greyson 1994, Leins and Erbar 2010, Ronse De Craaene 2018, 2021):
1. Differentiation, such as the differentiation of the gynoecial appendages into ovary, style, and stigma.
2. Varying proportions, such as the varying proportions of ovary, style, stigma, and other components (e.g., Ronse De Craene 2021).
3. Zonal growth and interprimordial growth Sattler 1978, Leins and Erbar 2010).
4. Postgenital fusions between various organs. In contrast to congenital fusion, which usually is in principle unobservable, postgenital fusion is observable.
5. Reduction or amplification in size and number, as, for example, the size of the gynoecial appendages and the number of ovules.
6. Transference of function (Corner 1958). For example, in
Stylidium adnatum the function of the style has been transferred to the androecial tube (Sattler 1973, 1974).
Takhtajan (1972), like Zimmermann (1959), also a forerunner of plant morpho evo-devo, distinguished the processes of deviation, prolongation and abbreviation. Heterotopy and the above processes (# 1-6) would be examples of deviation, whereas prolongation and abbreviation would be examples of heterochrony.
Considering all relevant processes provides a more complete picture of morpho evo-devo of the gynoecium.

9. Morpho Evo-Devo and the Concept of the Flower

Morpho evo-devo of the gynoecium is also relevant to the concept of the flower. According to the predominant classical morphology, "a flower is a reproductive short shoot bearing microsporophylls (stamens)… and megasporophylls (carpels) as its appendages or leaf homologues" (Kaplan 2022, p. 1069, edited by Peter Endress). In view of the available developmental data, this definition is no longer generally valid. The appendages of the androecium range from leaf-like to stem-like and even short shoot-like structures (Rutishauser and Sattler 1985, Sattler 1988). And it is questionable whether all gynoecia consist of closed megasporophylls. How then can we define the flower?
According to Claßen-Bockhoff ( 2016), the flower is the "sporangia bearing tip of the shoot," in which "stamens and carpels are sporangiophores and as such 'de novo' structures not necessarily homologous with vegetative leaves." Whereas one can see the androecium as consisting of sporangiophores that may be more or less leaf-like, stem-like, short shoot-like, or don't fit any of the classical categories, the gynoecium is more complex consisting of more or less leaf-like appendages (gynoecial appendages) that enclose the sporangiophores, which in the simplest case consist only of one ovule and in more elaborate cases of a placenta with ovules. As pointed out above, the position of the placentae and ovules is variable. In gynoecia with classical carpels the sporangiophores are formed on the carpels, whereas in other gynoecia, for example, in Myrica, they are basal, or as, for example, in Illicium, they are axillary. Alternatively, one could consider the gynoecial sporangiophore as a dual structure consisting of a more or less foliaceous appendage and a sporangia-bearing structure.
According to process morphology, stamens and carpels, gynoecial appendages, placentae and ovules are seen as process combinations that need not be fitted into the classical categories of stem and leaf (Sattler 1988, 1992, Sattler and Rutishauser 2023).

10. Conclusions

In morpho evo-devo the emphasis should be on observable developmental changes and the processes that generate these changes during development and evolution. Spatial shifting (leading to heterotopy) is a basic process that gave rise to gynoecia with ovules formed in different positions: on the gynoecial appendage or in its axil or in the centre of the gynoecium. In the latter case, ovules are not “as if glued on the surface of the gynoecium or the floral apex,” as Endress (2019) misrepresented our investigations; but the floral apex, retaining at first its typical organization, is gradually transformed into a single ovule or a placenta (see, for example, Sattler and Lacroix 1988, Figs. 12-15). From the topographical perspective, one would not even refer to the floral apex, but simply to a basal ovule or a free central placenta. This view has an empirical basis; it does not require difficult or impossible delimitations of gynoecial primordia that have led to almost endless futile controversies during the last two centuries.
In addition to spatial shifting (heterotopy), temporal shifting (heterochrony), differentiation, varying proportions, interprimordial and zonal growth, reduction, amplification, and transference of function are processes that played an important role in morpho evo-devo of the gynoecium.
As a result of a morpho evo-devo perspective based on developmental studies of gynoecia, angiosperms cannot be defined by the possession of classical carpels (closed megasporophylls), although many taxa have such carpels. As the name angiosperms indicates, they are defined by having the ovules enclosed, enclosed by gynoecial appendages and in many cases by additional underlying tissue formed by zonal growth, as, for example, in inferior ovaries. Within the enclosure and protected by it, placentae and ovules could change their position without any detrimental effect on the survival of the plants.
In this article the focus has been on morpho evo-devo. This focus will have to be enlarged to include data from developmental molecular genetics (see, for example,
Reyes-Olalde et al. 2023). Based on developmental genetics, Mathews and Kramer (2012) concluded "that the carpel is a complex organ consisting of a foliaceous appendage and the placenta." When this is recognized that the carpel consists of two components, the foliaceous appendage (which I called the gynoecial appendage) and the placenta or ovule(s), then we can also recognize that the relative position of the two components may change and that this change may eclipse the classical carpel when the placenta or ovule(s) is free central, basal, or axillary.
Recognizing that in extant angiosperms ovules are not always appendicular is also relevant for the search of fossil angiosperms and pre-angiosperms. It opens up different vistas for the evolution of the gynoecium. Thus, the Triassic
Combina can be considered a possible ancestor of angiosperms. It has bracts that bear an ovule in their axil and enclose it almost completely. Spatial shifting of axillary ovule formation into a ventral median position of an ascidiate carpel could have led to gynoecia of primitive angiosperms such as that of Amborella. Spatial shifting of ovule formation into the adaxial midrib region of the enclosing appendage and an increase in the number of ovules could have produced the carpels of the early Cretaceous fossil Archaefructus. And spatial shifting of the adaxial ovules toward the margins of the gynoecial appendage could have led to the conduplicate carpel (folded megasporophyll) of extant angiosperms such as that of Magnoliaceae. If we assume a monophyletic origin of angiosperms, further shifting of ovule formation into the centre of the gynoecium could have produced gynoecia such as that of Myrica in which the ovule is basal. However, basal ovules as in Myrica might also be primitive since there is evidence of basal ovules already in the Triassic and Jurassic.
Although the origin and evolution of angiosperms and the gynoecium remains hypothetical and speculative, we can at least conclude that heterotopy of placentae and ovules occurred in both extant and fossil angiosperms. And this heterotopy includes appendicular, axillary, and basal (central) positions. The latter two appear to be most easily understood through a topographic approach or at least through a redefinition of the carpel, if one wants to retain this term; but, as I suggested, the term gynoecial appendage would be preferable.

Acknowledgements:
I am grateful to Regine Claßen-Bockhoff, Bruce Kirchoff, Louis Ronse De Craene and Rolf Rutishauser for their valuable comments and suggestions.


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See also Plant Morphology, Morphological Development (Organogenesis) of Flowers, From Plant Morphology to Infinite Issues (including Ken Wilber and Korzybski), Philosophy of Plant Morphology, and Science: its Power and Limitations.



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