Plant Evo-Devo and Morphological Research by Rolf Sattler and Collaborators ------------------

Mainstream plant morphology, that is, classical plant morphology, appears categorical: any organ of flowering plants must be either a root, or a stem, or a leaf, or a homologue of one of them. I found that although many organs can be fitted into these categories, others appear more or less intermediate between them . As a result, one can see the diversity of plant form as a continuum that spans all the categories. I first proposed this idea in my paper:

Sattler, R. 1966. Towards a more adequate approach to comparative morphology. Phytomorphology 16: 417-429.

Subsequently, I provided a much more detailed elaboration of continuum morphology, especially with regard to the shoot, that is, stems, leaves, and emergences (outgrowths of the organs) (roots were not completely ignored since they may also occur in shoots):

Sattler, R. 1974. A new conception of the shoot of higher plants. Journal of Theoretical Biology 47: 367-382.

In retrospect I think that a more appropriate title for his paper would have been “The continuum conception of plant morphology.” I realized that - as I already mentioned in my paper - the idea of a continuum was not totally new. Other authors in the 19th and 20th centuries had recognized intermediates between categories. But since their findings and views had been largely ignored and suppressed by the scientific community of plant biologists, I was not sufficiently aware of all of my predecessors in continuum morphology. I learned much about them during a stay in Prof. Gérard Cusset's laboratory at the University of Paris in 1978.

In my Biophilosophy book (1986, p. 105) I presented the continuum model of the shoot in the form of a pyramid, that is, a tetrahedron in which shoots, stems, leaves, and emergences occupy the four corners of the tetrahedron and intermediate structures the space between the corners. Dr. Ming Anthony and I extended this model to pathological plant structures and referred to it as the pyramid model:

Anthony, M. and Sattler, R. 1990. Pathological ramification of leaves and the pyramid model of plant construction. Acta Biotheoretica 38: 165-170.

Finally, in 1992 I published a paper with Dr. Bernard Jeune that established quantitatively, by means of multivariate analysis, the continuum between the categories of root, shoot, stem, leaf, emergence, and their homologues:

Sattler, R. and B. Jeune. 1992. Multivariate analysis confirms the continuum view of plant form. Annals of Botany 69: 249-262.

As far as I know, this was the first quantitative confirmation of the morphological continuum that spans not only the categories of the three types of organs of classical plant morphology but also three of its organizational levels: the organ system (shoot), organs (roots, stems, and leaves), and outgrowths of organs (emergences). I am most grateful to Dr. Bernard Jeune for his collaboration on this project. Without his mathematical expertise I could not have accomplished this difficult undertaking. Its results went far beyond my first paper on continuum morphology (1966) - cited above - in which I used a very simple example to indicate the continuum between the stem and leaf categories.

Using a different mathematical approach and mostly different plant species, Gérard Cusset corroborated the continuum view of plant form (Cusset, G. 1994. A simple classification of the complex parts of vascular plants. Botanical Journal of the Linnnean Society 144: 229-242). Jeune and Sattler (1992) also confirmed the continuum in terms of process morphology (see below).

Although I worked mainly at the levels of organs systems, organs, and outgrowths of organs, it must be pointed out that the morphological continuum is not restricted to these levels. It can also be found at other levels of organization such as the levels of tissues and cells. For example, we demonstrated a continuum between different types of perforation plates in the cells of vessels (the water-conducting structures in plants) and pointed out its significance for the vexing problem of the origin of flowering plants:

Muhammad, A.F. and Sattler, R. 1982. Vessel structure of Gnetum and the origin of angiosperms. American Journal of Botany 69: 1004-1021.

Despite increasing evidence for continuum morphology, Kaplan's Principles of Plant Morphology (2022), the most comprehensive volume of plant morphology in the 21st century, still relies exclusively on the concepts of classical plant morphology (see Sattler, R. 2022. Kaplan's Principles of Plant Morphology: A Critical Review. The Botanical Review 88: 257-270.

Our investigations of leaf development provided much evidence for a continuum between simple leaves, stems and shoots. The following papers demonstrated so-called “leaves” that approach the symmetry of stems:

Sattler, R., Luckert, D. and Rutishauser, R. 1988. Symmetry in plants: leaf and stipule development in Acacia longipedunculata. Canadian Journal of Botany 66: 1270-1284.

Rutishauser, R. and Sattler, R. 1986. Architecture and development of the phyllode stipule whorls in Acacia longipedunculata: controversial interpretations and continuum approach. Canadian Journal of Botany 64: 1987-2019.

So-called compound “leaves” exhibit shoot features during their development. For this reason they would be called more appropriately leaf-shoot intermediates. We demonstrated the combination of leaf and shoot features for two species:

Rutishauser, R. and Sattler, R. 1997. Expression of shoot processes in leaf development of Polemonium caeruleum. Botanische Jahrbücher für Systematik 119: 563-582.

Lacroix, C.R. and Sattler, R. 1994. Expression of shoot features in early leaf development of Murraya paniculata (Rutaceae). Canadian Journal of Botany 72: 678-687.

Lacroix et al. (2003) confirmed our conclusions for other species. And more recently, on the basis of molecular genetics, Eckardt and Baum (2010) concluded that "it is now generally accepted that compound leaves express both leaf and shoot properties.” (see below in Part 2).

In Utricularia (bladderworts) we demonstrated a variety of leaf and shoot-like structures that cannot be fitted into the categories of classical plant morphology because they show a combination of features of different categories, including roots (see Sattler & Rutishauser (2023) and other papers by Rutishauser and Sattler in my list of publications).

Homology has been called the central concept of comparative morphology and therefore remains important in evo-deo. In classical morphology, whose basic concepts are still used in evo-devo, homology is conceived in terms of either/or. But in continuum morphology homology becomes a matter of degree, and thus, for example, a structure may be partially homologous to a stem, a leaf, and even a root. Such homologization seems inconceivable in classical morphology where an organ must be homologous to either a stem or a leaf or a root. Because of this insistence on categorical homology, homologization in classical terms gave rise to endless debates about the homology of intermediate structures. But, as I pointed out in the following two publications, if homology is seen as a matter of degree, these futile debates can be resolved:

Sattler, R. 1984. Homology – a continuing challenge. Systematic Botany 9: 382-394.

Sattler, R. 1994. Homology, homeosis, and process morphology in plants. In: Hall, B.K. (ed.) Homology: The Hierarchical Basis of Comparative Biology. New York: Academic Press, pp. 423-475.

Although homology as a matter of degree appears compatible with modern research in plant evo-devo and molecular genetics, as far as I know, it has not always been sufficiently recognized explicitly.

Quantitative or partial homology and continuum morphology involve fuzzy logic, whereas categorical homology and classical morphology are based on Aristotelian either/or logic. According to fuzzy logic, membership in a class is a matter of degree. Hence, a structure may be, for example, a 50%, 80%, or 100% leaf. I discussed fuzzy logic in my essays on Either/Or Logic and Beyond and in Healing Thinking through Fuzzy Logic. And I also briefly mentioned the importance of fuzzy logic (or fuzzy thinking) in my article on Agnes Arber for whom thinking in terms of degree was of great importance:

Sattler, R. 2001. Some comments on the morphological, scientific, philosophical and spiritual significance of Agnes Arber’s work and life. Annals of Botany 88:1215- 1217.

For a much more detailed discussion of Agnes Arber’s thinking in terms of degree (that is, fuzzy thinking – a term she did not use, as far as I know, because fuzzy logic was invented after her death) see the excellent article by Rutishauser, R. and Isler, B. (2001). Developmental genetics and morphological evolution of flowering plants, especially bladderworts (Utricularia): Fuzzy Arberian morphology complements classical morphology. Annals of Botany 88:1173-1202.

For a general discussion of fuzzy logic and its importance in practically all aspects of life see the excellent book by Bart Kosko. 1993. Fuzzy Thinking. The New Science of Fuzzy Logic. New York: Hyperion.

The words ‘fuzzy’ and ‘fuzziness’ appear distasteful for many people and especially for many scientists, I guess because these words are often equated with inexactness and vagueness, and science is supposed to be exact. However, fuzzy logic, as a quantitative approach, offers more exactness and precision than either/or logic. And continuum morphology, which reflects fuzzy logic, offers more precision than categorical classical morphology because instead of forcing the whole diversity of structures into mutually exclusive categories, it captures the whole range of structural variation. I guess if Zadeh, the inventor of fuzzy logic, would have called it ‘continuum logic,’ it would have been more palatable to many people; but Zadeh chose the name 'fuzzy logic.'

Although fuzzy logic appears compatible with modern research in plant evo-devo, as far as I know, it has not been sufficiently recognized explicitly.

Categorical thinking and essentialism appear closely related. I became aware of the pitfalls of essentialism early on in my morphological work and pointed them out in my paper “A new conception of the shoot of higher plants (1974, p. 369)” (see above in the section on Continuum Morphology). Later on in 1977, I elaborated on essentialism in a paper I presented at an international congress in Japan:

Sattler, R. 1977. Essentialism in plant morphology. Proceedings No. 3, XIVth International Congress of the History of Science. Tokyo & Kyoto, pp. 464-467.

More recently, I also discussed essentialism in my paper and website on Philosophy of Plant Morphology (see below).

Classical morphologists such as, for example, Kaplan (2022) tend to embrace essentialism consciously or more often subconsciously. When they encounter structures that do not fit the classical categories, they often insist that these “misfits” represent the essence of one of the categories. For example, for a structure that appears intermediate between a stem and a leaf they would argue that it is essentially a stem or a leaf. They might not agree which one it is, but they agree that it must be one or the other. Thus, the underlying belief or philosophy of essentialism that dates back to Plato and Aristotle is used - consciously or subconsciously – to force the whole diversity of structural variation into fixed categories or essences. To my mind, this implies a disregard of empirical findings in favour of the preconceived notion of categories or essences. Can we still call it science when misfits (intermediate structures) can no longer question the general validity of the categorical, essentialistic approach?

Evolutionary biologists generally reject essentialism. I have shown, however, that to some extent evolutionary plant morphology may also be trapped in essentialism because evolutionary plant morphologists often use mutually exclusive morphological categories and the use of such categories may imply essentialism.

I never denied that morphological categories have a limited usefulness because many, if not most structures fit more or less the categories. However, intermediate structures don’t fit, and therefore continuum morphology appears more encompassing than categorical morphology. Categorical morphology can be seen as a special case of continuum morphology that seems appropriate for the extremes in the continuum (see Lacroix et al. 2005).

As noted above, molecular genetics also supports the continuum view. For example, James (2009, p. 17) stated that "it is now widely accepted that... radiality [characteristic of most stems] and dorsiventrality [characteristic of typical leaves] are but extremes of a continuous spectrum. In fact, it is simply the timing of the KNOX gene expression!"

In contrast, when molecular geneticists discuss, for example, organ identity essentialism may be implied.

Sattler, R. 1978. ‘Fusion’ and ‘continuity’ in floral morphology. Notes from the Royal Botanic Gardens Edinburgh 36: 397-405.

In this paper I tried to elucidate the observable processes that underlie the so-called congenital fusions. In this way I recovered the empirical basis where it had been lost or obscured through classical plant morphology. And I pointed out the processes that change from one ontogeny to subsequent ontogenies during evolution, that is, the processes that are of concern to evo-devo research.

One phenomenon that has been lost or obscured through the concept of congenital fusion is heterotopy, which implies a change in the position of structures. Together with my students and collaborators, I provided empiriral evidence for heterotopy in several publications such as, for example:

Dickinson, T.A. and Sattler, R. 1974. Development of the epiphyllous inflorescence of Phyllonoma integerrima (Turcz.) Loes.: implications for comparative morphology. Bot. J. Linn. Soc. 69: 1-13.

I discussed the significance and implications of heterotopy, especially for homologization and evo-devo in plant biology (see, for example, the above paper on "A new conception of the shoot of higher plants," 1974).

Instead of using the term heterotopy, molecular geneticists refer to ectopic gene expression when genes are expressed in different locations.

Heterotopy may occur anywhere in the plant body. However, it is especially important in the gynoecium of flowers, where it has often been obscured through the application of the concept of congenital fusion. In 1974, I published a paper in which I introduced a gynoecial morphology that does not rely on unobservable congenital fusions and elucidates developmental changes during evolution:

Sattler, R. 1974. A new approach to gynoecial morphology. Phytomorphology 24:22-34.

In retrospect, I would prefer the title “An empirical approach to gynoecial morphology” because this title would underline that this approach is based on observable data. As a result of these data, the floral concept of classical morphology had to be revised in a rather fundamental way. My students and I provided much empirical evidence for this revision (see my book Organogenesis of Flowers (1973), Macdonald and Sattler (1973), Posluszny and Sattler (1976), Pauzé and Sattler (1979), Sattler and Perlin (1982), and Sattler and Lacroix (1988), quoted in Morphological Development of Flowers).

Sattler and Perlin (1982) and Sattler and Lacroix (1988) rescued the carpel concept to some extent by a redefinition. Traditionally a carpel is defined as a folded megasporophyll, that is, an appendage that bears and encloses ovule(s). Consequently, gynoecia whose ovules are not born on the gynoecial appendages are acarpellate (without carpels). But they may also be considered carpellate (having carpels), if we redefine the carpel as an appendage that encloses ovule(s) and that may or may not bear the ovule(s). Thus, cauline ovules (that are born on the floral axis) can be recognized and it is not necessary to postulate in principle unobservable congenital fusions. Hence, this redefinition renders gynoecial morphology more empirical.

However, some gynoecia such as those of Stylidium (Sattler 1974) remain acarpellate (without carpels) even according to the redefined carpel concept. Therefore, we have to conclude that the flowers of angiosperms may be carpellate or acarpellate, although the majority are carpellate according to the redefined carpel concept.

As far as I know, the diversity of gynoecial construction, especially acarpellate gynoecia, have not been sufficiently explored in evo-devo research that tends to imply the classical carpel concept (in the sense of a folded megasporophyll), and therefore evo-devo has not caught up sufficiently with the redefinition of the carpel as I proposed it and as it has been endorsed by Greyson (1994), Leins and Erbar (2010) and others.

My most recent article on the gynoecium supersedes even the distinction of carpellate and acarpellate gynoecia through a topographic approach:

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

In most textbooks and research publications the classical concept of the flower is taken for granted. According to this concept, a flower is a modified monaxial shoot that consists of sterile and fertile appendages (leaf homologues). The sterile appendages, if present, are tepals or sepals and petals, whereas the fertile appendages are stamens and carpels.

Investigations of the diversity and complexity of floral development have shown that the classical concept of the flower often is not supported by empirical evidence (see my publications and my book Organogenesis of Flowers). Therefore, alternative concepts have been proposed. These concepts that are often ignored have been summarized and applied to the flowers of Myrica gale by

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.

We discussed these concepts with regard to Myrica gale because the female flowers of this species are not easily understood in classical terms. Other floral concepts, especially that of Leon Croizat, provide interesting perspectives. I am not aware of any other publication that applies all of these floral concepts to any other species of angiosperms.

Sattler and Jeune (1992), cited above, found that the continuum model of the shoot also applies to flowers, which means that floral organs cannot always be clearly assigned to mutually exclusive categories. Especially stamens turned out to be often more or less intermediate between typical phyllomes and caulomes or shoots (Sattler 1988, see below).

As in the vegetative region, the continuum in the reproductive region is a dynamic continuum, that is, a continuum of process combinations. This view, which I called process morphology, I first proposed for floral morphology and then extended it to plant morphology in general (see below under Towards a Process Morphology of Plants).

I seems that plant evo-devo research could benefit from more awareness of different floral concepts.