Organogenesis of Flowers
The diversity, complexity and dynamics of floral development
Fundamental Issues and my Contributions
Floral development, especially the development of floral organs (organogenesis), has been studied for centuries. In 1857 (two years before Charles Darwin’s On the Origin of Species), the French botanist Jean-Baptiste Payer published the monumental Traité d’organogénie comparée de la fleur. As far as I can see, this work remains the most comprehensive treatise on floral development (organogenesis) up to the present time. It has, however, some shortcomings for which Payer cannot be blamed. Since microscopic photography was not yet sufficiently developed at that time, he could provide only drawings. And since the resolution and magnification of microscopes was rather limited, his observations were not always free of errors. However, overall they appear remarkably and admirably accurate.
In the 20th century in 1973 I published the Organogenesis of Flowers. A Photographic Text-Atlas. (Since this book has much in common with Payer’s, some of my French colleagues called me the Payer of the 20th century or the modern Payer). My book is not as comprehensive as Payer’s: it describes the floral development of only 50 different species of flowering plants, whereas Payer’s Traité includes over three hundred. But as the title of my book indicates, it documents the stages of floral development photographically by a special epi-illumination technique that I developed in my laboratory (Sattler 1968). This technique displays floral development in three dimensions (photograph taken by Dr. Usher Posluszny). Posluszny, Scott, and Sattler (1980) have further improved this technique, and Dadpour et al. (2008) developed a digital version. Dr. Somayeh Naghiloo used this digital version in her research on floral development and because of the astounding beauty of her photos won awards in international photo competitions.
Although I am the author of Organogenesis of Flowers, I have to emphasize that many students and technicians have greatly contributed to it. Dr. Alastair D. Macdonald contributed 6 chapters and Ms. Vera Block 8. Other students and technicians also made important contributions. I am most grateful to all contributors (see Acknowledgements in the book).
As far as I know, so far nobody has published a photographic text-atlas on floral development that is more comprehensive. But many papers have been published on the floral development of a great variety of species and many of these papers document the stages of floral development by means of scanning electron microscopy and/or microscopic sections. For an incomplete bibliography see, for example, Greyson (1994) and Leins & Erbar (2010).
The flower has been defined in different ways and thus different floral concepts have been proposed, which has led to great complexity (see, for example, Macdonald and Sattler 1973). Many authors seem to be unaware or ignorant of this complexity. Thus, in most textbooks and research papers a flower is simply defined as consisting of an axis with sterile and fertile appendages that are considered homologues of leaves. The sterile appendages form the perianth that often consists of sepals and petals or tepals (and sometimes may be absent). The fertile appendages are the stamens (microsporophylls) and carpels (megasporophylls) that carry and enclose the ovules (but see Brückner (2000) for many different definitions of the carpel concept).
This common definition of the flower appears rather limited in view of the observed diversity and complexity of floral development. In the androecium, stamens cannot be generally equated with microsporophylls (fertile phyllomic appendages) because they show a continuum from flat (phyllomic) to radial (caulomic) structures. Only the phyllomic stamens can be called microsporophylls, the others along the continuum resemble microsporophylls less and less as they become more and more caulomic (stem-like). The continuum also extends towards branchlets (fertile shoots) in androecia in which common primordia give rise to stamen fascicles (Rutishauser and Sattler 1985, Sattler 1988, Sattler and Jeune 1992, Leins and Erbar 2010). Therefore, it seems debatable whether all flowers have only one axis. At least some flowers may be more or less polyaxial.
In the gynoecium, ovules are not always born on appendages (carpels), but in some species may arise on the floral axis. This means that besides the typically carpellate flowers acarpellate flowers can be distinguished (Sattler 1974, Brückner 1991, 2000, p. 180). If, however, we change the traditional definition of the carpel as an appendage that encloses and bears ovule(s) and redefine it as an appendage that encloses ovule(s) and may or may not bear them, then most (but not all) of the acarpellate flowers can be considered carpellate. We proposed this redefinition long ago (Sattler and Perlin 1982) and alluded to it again later (Sattler and Lacroix 1988). Greyson (1994) and Leins & Erbar (2010) also used this redefinition. It simplifies matters, but it must be clear that according to this redefinition a carpel can no longer be generally equated with a megasporophyll because it may or may not be a megasporophyll depending on whether it bears or does not bear the megaspore producing ovule(s). Furthermore, it must be clear that even according to the redefinition of the carpel, there are still gynoecia without carpels (acarpellate gynoecia) (Sattler 1974). Examples of such acapellate gynoecia can be found in Stylidium and Balanophora (Sattler 1973, 1974). I have discussed evolutionary developmental processes through which these and other patterns may have arisen (Sattler 1974, 1992).
The protective enclosure of ovules constitutes a characteristic feature of flowering plants, which for this reason have been called angiosperms, plants with enclosed seeds, in contrast to gymnosperms with exposed seeds. It needs to be stressed that the enclosure of the ovules and seeds has been achieved through several different ways. Only one of these ways involved the formation of the classical carpel (megasporophyll). Another way was the formation of gynoecial appendages that enclosed ovules but did not bear them. And yet other ways have been reported in the literature (see, for example, Sattler 1974). Brückner (2000, pp. 176-180) noted ten different interpretations of the gynoecium involving different carpel concepts. See also Lorch (1963) for a historical review of carpel concepts and problems engendered by these concepts.
In spite of much detailed developmental evidence of cauline placentae and ovules that are borne on the floral apex, there are authors who still ignore all this evidence or claim that it does not exist. For example, Endress completely denies this evidence. He stated categorically: "Ovules are part of and enclosed in carpels in all living angiosperms…From what we know at present, there are no "cauline" ovules in extant angiosperms" (Endress 2019, p. 201). I invite readers to look at photos in the literature that show in great detail how in some taxa the floral apex or a part of it becomes transformed into an ovule. Such instances have been reported by Macdonald and Sattler (1973), Posluszny and Sattler (1976), Pauzé and Sattler (1979), Sattler and Perlin (1982), Sattler and Lacroix (1988) and others. Endress claims that in these cases the floral apex constitutes the base or the root of the gynoecium, which means that it is no longer a floral apex. However, it has the typical organization of a floral apex, and it is this typically organized floral apex that becomes gradually transformed into the ovule. The ovule is not "glued on," an idea that Endress falsely attributes to us. And declaring the floral apex as the base of the gynoecium lacks any evidence. It just serves as an unsubstantiated ad hoc hypothesis to deny the cauline origin of these ovules. To force these gynoecia into a carpellate pattern one has to draw imaginary lines through the floral apex (see Sattler 1974, Fig. 2). Endress claims that these lines are not imaginary, but he does not present any factual evidence for this. (Endress also makes false accusations. He claims that Sattler (1974) did not refer to carpellate and acarpellate gynoecia, but there is much reference to both in that publication. He claims that I "drew an unbiological borderline between carpellate and acarpellate gynoecia," whereas I considered "the difference between carpellate and acarpellate gynoecia as a difference of degree" (Sattler 1974, p. 24). He criticizes me for being primarily interested in ontogeny. Can't we choose any more our field of primary interest without being told that, as he put it, it "makes no sense"? Although our primary interest was indeed in ontogeny, we pointed out implications for evolution and phylogeny, but we did not indulge in phylogenetic speculations, we just indicated possibilities. The study of ontogeny still provides more reliable information than phylogenetic hypotheses. But we leave it up to phylogeneticists to use the results of our ontogenetic investigations as they please, and we don't accuse them of being primarily interested in phylogeny).
Endress' insistence that all angiosperms have carpels in spite of the contradictory evidence that we and others have provided, which he tries to accommodate through an unsubstantiated ad hoc hypothesis, appears to have rather deep roots that go beyond scientific evidence. Carpels are phyllomes
and if stamens are also considered phyllomes, then the classical theory of the flower as a modified monaxial shoot can be retained. This theory or model appears simple and fits well into the simple classical model of whole plants such as flowering plants, according to which they consist of only three mutually exclusive organ categories: root, stem (caulome), and leaf (phyllode), including their homologues such as stamens and carpels. Thus, insisting that carpels and stamens are phyllomes, reifies the categorical organ trinity of classical morphology. This trinity has dominated plant morphology for a long time in spite of much contradictory evidence. It can be traced back to Goethe (1790). However, Goethe could see beyond it (see below), Endress and others cannot. Endress and others present it in evolutionary and phylogenetic clothes, which upon scrutiny cannot hide that it is not only simple but simplistic since it does not sufficiently take account of contradictory data.
Considering the enormous diversity and complexity of floral development that have been documented by many authors including us, the usefulness of the common simplistic definition of the flower as an axis that bears sterile and fertile phyllomes (stamens and/or carpels) appears rather limited. But it has some value because many appendages found in flowers appear phyllomic (leaf homologues); but others may be caulomic (stem homologues) or more or less intermediate between phyllomes, caulomes and other categories such as branches. Therefore, understanding the enormous structural diversity in terms of a continuum between these categories appears closer to reality than a purely categorical approach.
Claßen-Bockhoff (2016) also concluded that "the shoot concept of the flower...should be questioned." And she proposed that, "flowers are sporangia bearing units rather than short shoots with floral organs" because "from the functional point of view, stamens and carpels are sporangiophores and as such 'de novo' structures not necessarily homologous with vegetative leaves." As pointed out above, the androecial sporangiophores are more or less branched. For example, those that form stamen fascicles are more highly branched than those that form individual stamens. The gynoecial sporangiophores may be more or less or not at all integrated with the gynoecial appendages. When they are not at all integrated with the gynoecial appendages as it is the case in acarpellate gynoecia, the gynoecial appendages are sterile and the placentae or ovules are borne on the floral apex. In that case the notion of a sporangiophore does not seem applicable, unless one considers the floral apex and the placenta as a sporangiophore.
Even Goethe, who is often considered the founder of the classical monaxial concept of the flower, made some remarks that contradict this concept and go beyond it. He wrote: "The pistil, the receptacle, and the fruit all belong to the system of the eyes [i. e. branches]" (quoted by Cusset 1982, p. 27), which means that the pistil is not just an appendage or appendages, but the homologue of a branch or branches. As a result, with regard to the gynoecium, the flower becomes a polyaxial system. Also, already in The Metamorphosis of Plants (1790, Section 87), Goethe wrote: "It is well known that the activity of such a bud [that develops in the axil of a leaf] has a great similarity to that of the ripe seed." Again, this means that since a seed, like a bud, includes a secondary axis, the flower becomes a polyaxial system at least with regard to the gynoecium (for more on this topic see Philosophy of Plant Morphology). For other authors who deviated from the classical monaxial interpretation of the flower see Cusset (1982).
However, the question of what is a phyllome or a branch may be superseded. According to anaphytosis, the theory of anaphytes (Schultz 1843), flowers are branching systems that result from the processes of branching and articulation. Branching here is simply understood as the formation of a new primordium that develops into an article (segment). Thus, there is no need to categorize these primordia in terms of phyllomes, caulomes, and shoots. This theory appears compatible with process morphology, especially if the articles between two branching points are understood as process combinations (see below). For this theory it is not necessary that the structures of the flower are reduced to the categories of classical morphology such as caulome (stem) and phyllome (leaf), nor does it require reference to 'de novo' structures, except for sporangia, because according to this theory each different structure is more or less 'de novo'; therefore no fundamental distinction is made between structures that are 'de novo' and those that are more or less similar.
One reason, among others, why the common simplistic definition of the flower as a modified short shoot persists to a great extent: patterns that contradict this simplistic definition are forced to conform to it by means of the concept of “congenital fusion.” But this kind of “fusion” refers to a variety of processes, some of which misrepresent developmental and evolutionary processes, referring to fusion where none is observable (Sattler 1974, 1978). Instead one or several of the following developmental and evolutionary processes may have been operative:
1. Change of the relative position of primordial inception (spatial shifting), which leads to heterotopy (that may be related to ectopic gene expression);
2. Change of timing (temporal shifting), which implies heterochrony;
3. Zonal growth (intercalary growth) and other modifications, which lead to heteromorphy (Zimmermann 1959, Sattler 1992).
Using the concept of congenital fusion may obscure these processes, which means it may obscure the hologenetic view of evolution (Zimmermann 1959) according to which evolution needs to be understood as a change in the development of organisms as it is emphasized in evolutionary developmental biology (evo-devo). For these reasons, I have proposed to replace the concept of congenital fusion by concepts that refer to processes that are at least in principle observable (Sattler 1974, 1978). Some authors such as Greyson (1994) and Leins & Erbar (2010) have adopted my proposal (see also Leins 1972 and Leins, Merxmüller and Sattler 1972).
Like almost all research on floral development, most of our research implied a structure-process dichotomy, which means that structures and processes are distinguished: structures exhibit processes. However, using data from floral development, I introduced a process morphology that transcends this dichotomy because according to process morphology structures do not have processes, they are processes (Sattler 1988). Thus, floral morphology can be understood in terms of process morphology that demonstrates a dynamic continuum.
Nowadays, in our genocentric age, floral development is investigated mainly in terms of molecular genetics. Although these investigations can shed some light on floral development, they are limited for at least two reasons: 1. So far only relatively few species have been analyzed in terms of molecular genetics, and 2. Flowers are much more than just genes. Therefore, descriptive and comparative studies of the diversity, complexity and dynamics of floral development remain important for a more complete understanding of flowers.
We also have to keep in mind that whatever we describe through language and/or mathematics is somewhat removed (abstracted) from reality. Words are not the things they refer to; language and mathematics (a form of language), like a map, are not the territory they refer to as has been clearly pointed out by Korzybski through his structural differential, which shows that "whatever you might say something "is", it is not." Hence, whatever ups might say a flower is, it is not. Language can at best represent aspects of a flower, but not the thing-in-itself as Kant has pointed out long ago. The thing-in-itself as an integral part of ultimate reality remains unnamable, unspeakable. Hence the importance of silence (see also From Plant Morphology to Infinite Issues (including Ken Wilber and Korzybski).
Buddha’s “flower sermon” also underlines the importance of silence. It has been said that one day, as usual, a crowd had gathered to listen to the Buddha. But he did not speak, he held a flower in his hand. The crowd became rather restless as he kept looking at the flower in silence. Finally, Mahakashyap, one of his disciples, started laughing. Then Buddha gave him the flower and said to the crowd: “Whatever can be said through words, I have said to you, and that which cannot be said through words, I give to Mahakashyap. The key cannot be communicated verbally...What is the key? Silence and laughter is the key - silence within, laughter without. And when laughter comes out of silence, it is not of this world, it is divine” (Osho: Meditation. The first and the last freedom, pp. 190-191). Mahakashyap has been considered the founder of Zen Buddhism, which emphasizes the limitations of language and thought.
Brückner, C. 1991. Zur Interpretation des Karpells - eine Übersicht. Gleditschia 19: 3-14.
Brückner, C. 2000. Clarification of carpel number in Papaverales, Capparales, and Berberidaceae. Botanical Review 66 (2): 155-307.
Claßen-Bockhoff, R. 2016. The shoot concept of the flower: Still up to date? Flora 221: 46-53.
Cusset, G. 1982. The conceptual bases of plant morphology. Acta Biotheortica 31A: 8-86.
Dadpour M. R., Grigorian W., Nazemieh A., Valizadeh M. 2008. Application of epi-illumination light microscopy for study of floral ontogeny in fruit trees. International Journal of Botany 4, 49–55.
Endress, P. K. 2019. The morphological relationship between carpels and ovules in angiosperms: pitfalls of morphological interpretation. Botanical Journal of the Linnean Society 189: 201-227.
Goethe, J. W. von. 1790. Versuch die Metamorphose der Pflanzen zu erklären. Gotha: C. W. Ettinger (translated by Arber, A. 1946. Goethe's Botany. Chronica Botanica 10: 63-126.
Greyson, R.I. 1994. The Development of Flowers. New York/Oxford: Oxford University Press.
Leins, P. 1972. Das Karpell im ober- und unterständigen Gynoeceum. Berichte der deutschen botanischen Gesellschaft 85: 291-294.
Leins, P., Merxmüller, H. and Sattler, R. 1972. Zur Terminologie interkalarer Becherbildungen in Blüten. Berichte der deutschen botanischen Gesellschaft 85: 294.
Leins, P. and Erbar, C. 2010. Flower and Fruit. Stuttgart: Schweizerbart Science Publishers.
Lorch, J. 1963. The carpel - a case-history of an idea and a term. Centaurus 8: 269-291.
Macdonald, A. D. and Sattler, R. 1973. Floral development of Myrica gale and the controversy over floral concepts. Canadian Journal of Botany 51:1965-1976.
Payer, J.-B. 1857. Traité d’organogénie comparée de la fleur. Paris: Masson.
Posluszny, U., Scott, M.G. and Sattler, R. 1980. Revisions in the technique of epi-illumination lightmicroscopy for the study of floral and vegetative apices. Canadian Journal of Botany 58: 2491-2495.
Osho. 2004. Meditation. The first and the last freedom. New York: St. Martin’s Griffin.
Rutishauser, R. and Sattler, R. 1985. Complementarity and heuristic value of contrasting models in structural botany. 1. General considerations. Botanische Jahrbücher für Systematik 107: 415-455.
Sattler. R. 1968. A technique for the study of floral development. Canadian Journal of Botany 46: 720-722.
Sattler, R. 1973. Organogensis of Flowers. A Photographic Text-Atlas. Toronto: University of Toronto Press.
Sattler, R. 1974. A new approach to gynoecial morphology. Phytomorphology 24: 22-34.
Sattler, R. 1978. “Fusion” and “continuity” in floral morphology. Notes of the Royal Botanic Garden, Edinburgh 36: 397-405.
Sattler, R. 1988. A dynamic multidimensional approach to floral development. In: Leins, P., Tucker, S. C. and Endress, P. K. (eds.) Aspects of Floral Development. Berlin: J. Cramer/Borntraeger, pp. 1-6.
Sattler, R. 1992. Process morphology: structural dynamics in development and evolution. Canadian Journal of Botany 70: 708-714.
Sattler, R. and Perlin, L. 1982. Floral development of Bougainvillea spectabilis Willd., Boerhaavia diffusa L. and Mirabilis jalapa L. (Nyctaginaceae). Botanical Journal of the Linnean Society 84: 161-182.
Sattler, R. and Lacroix, C. 1988. Development and evolution of basal cauline placentation in Basella rubra. American Journal of Botany 75: 918-927.
Sattler, R. and Jeune, B. 1992. Multivariate analysis confirms the continuum view of pant form. Annals of Botany 69: 249-262.
Schultz, C. H. 1843. Die Anaphytose oder Verjüngung der Pflanzen. Ein Schlüssel zur Erklärung des Wachsens, Blühens und Fruchttragens, mit praktischen Rücksichten auf die Kultur der Pflanzen. Berlin.
Zimmermann, W. 1959. Die Phylogenie der Pflanzen. 2nd edition. Jena: Gustav Fischer Verlag.
See my Publications for further references on investigations of floral development carried out in my laboratory such as those by Sattler (1962, 1967, 1972), Cheung and Sattler (1967) Macdonald and Sattler (1973), Posluszny and Sattler (1973, 1974, 1976), Singh and Sattler (1972-1977), Sattler and Singh (1973-1978), Pauzé and Sattler (1978, 1979), Lacroix and Sattler (1988), and Lehmann and Sattler (1992-1997)
Latest update of this webpage on September 19, 2019.