Articulation Morphology of Plants and Plant Evo-Devo: A process-oriented, unified approach inspired by the theory of anaphytes (anaphytosis)
Abstract
According to the theory of anaphytes (anaphytosis), first proposed in 1843, in the open growth of plants, ramification is the key principle in plant morphology. It engenders articulation: the formation of articles, called anaphytes. While the original theory of anaphytes included tenets that are now considered outdated, Articulation Morphology, as proposed here as a modern version of the theory of anaphytes, focuses solely on ramification and articulation. According to articulation morphology, plants are articulated wholes: systems of articles formed through ramification. Articles are understood as process combinations according to process morphology. For practical purposes, they can also be seen as structures to which traditional names are given such as root, stem, leaf, or leaflet. However, articulation morphology does not require demarcating articles from one another. It relies only on the observation of ramifications and the resulting articulations. In this sense, it is strictly empirical. It supersedes questionable homologizations of controversial structures because, according to articulation morphology, these structures are simply uncommon patterns of ramification and articulation. Since this is a fundamentally different way of understanding plants, articulation morphology may be considered a new paradigm of plant morphology. From this perspective, by viewing plants as organisms that exhibit open growth through ramification and articulation, plant evo-devo becomes the investigation of the development and evolution of ramification and articulation.
The Theory of Anaphytes (Anaphytosis) and Articulation Morphology
Classical morphology remains predominant in mainstream plant morphology (Kaplan 2022, Sattler 2022), although it has been surpassed (e,g., Sattler 1994, Rutishauser 2020, Classen-Bockhoff 2024). According to classical morphology, plants such as flowering plants consist of three kinds of organs: root, stem (caulome), and leaf (phyllome) (Braun 1851, Troll 1954, Kaplan 2022). Thus, any organ we encounter must be either a root, a stem (caulome), or a leaf (phyllome). However, some structures deviate so much from the common pattern that they cannot be clearly assigned to any one of the three kinds of organs (Rutishauser 2016, 2020, Rutishauser et al. 2008, Sattler and Rutishauser 2023, Classen-Bockhoff 2024). As a result, endless debates have persisted and continue to arise about the assignment of controversial organs. These controversies remain unresolved because they appear to be pseudo-problems: attempts to categorize structures that do not fit the categories.
In the theory of anaphytes (anaphytosis), which was developed by C. H. Schultz, who is also known as Schultz-Schultzenstein, such problems or pseudo-problems do not arise (Schultz 1943, Schultz-Schultzenstein 1867). According to this theory, plant morphology is the result of two fundamental processes: ramification (branching) and articulation. These two processes are observable. We can observe that during the development of plants, ramification occurs, which leads to articles, called anaphytes, between successive ramifications or after a single ramification. For example, an internode is an article between successive ramifications and a simple leaf is an article after a single ramification that does not undergo further ramification. The process of the continued formation of anaphytes is called anaphytosis. Hence, Schultz-Schultzenstein named his theory anaphytosis. Like other authors, I refer to it more simply as the theory of anaphytes.
Organisms can be partitioned into different kinds of parts (Winther 2011). As I shall elaborate below, plants can be partitioned into organs, modules, or articles (anaphytes). Organs or modules are partitioned through boundaries or at least through a morphological theory, whereas articles are distinguished on the basis of processes that can be observed. According to articulation morphology - a modern version of the theory of anaphytes that I am proposing here - plants are articulated wholes: systems of articles that arise in succession or simultaneously.
The basis of articulation morphology is the open growth of plants (see, for example, Classen-Bockhoff 2024, Chapter 1). Open growth occurs through ramification, which leads to articulation: the formation of articles. Thus, ramification and articulation are intrinsic to the open growth of plants, which is the most basic process that distinguishes plants from most animals.
As mentioned already, one difference between the organs of mainstream morphology and the articles of articulation morphology is that the latter is based on the observable process of ramification, whereas the former is based on a morphological theory and often relies on demarcations that are questionable because there are no clear-cut boundaries between organs or modules, which are understood as morphological body parts (Minelli 2021). By drawing boundaries differently, five different models of plant construction have been created (see Rutishauser and Sattler 1985, pp. 420-424, Classsen-Bockhoff 2024, pp. 487-489, Fig. 8.2). While these models complement one another, they are all based on boundaries that do not exist in nature. However, Howard (1976) highlighted the stem-node-leaf continuum. This continuum is acknowledged in the model that subdivides the plant into phytomers, which are also called modules (White 1979, Classen-Bockhoff 2024, p. 352), but phytomers create a discontinuum in the stem from one internode to another. They consist of a node, the internode below, the leaf, the axillary bud and even roots if they are present. In contrast, the traditional root-stem-leaf model acknowledges the continuity of the stem but draws a boundary between the stem and the leaf. Other models of the shoot, while emphasizing a continuum in one way, have created demarcations in another way. In contrast, articulation morphology is not based on organs with disputed boundaries; it is based on articles - units that emerge through the observable process of ramification. We can observe that ramification occurs through the formation of a new growth centre (primordium) that develops into an article. We cannot delimit this growth center at its base since it is continuous with the underlying tissue of the article on which it is formed. As it develops into a new article it acquires distinct properties and through these properties – not through a non-existent boundary – it becomes distinguishable from the article on which it arises. Hence, the distinction of articles does not rely on boundaries: we can indeed distinguish articles without drawing boundaries. If the newly-formed article does not ramify, it remains a single article. If it does, the segment between successive ramifications constitutes an article. No boundary can be observed between articles - so why search for one? It is better to abandon the futile quest for non-existent boundaries. Even between organs no boundary can be observed. Yet in mainstream morphology a boundary is often assumed, but some mainstream morphologists acknowledge the non-existence of boundaries. Kaplan wrote: “The vagaries of defining the boundaries between stem and leaf components of the shoot underscore the fundamental developmental unity of these two elements and the artificiality of attempting to draw a rigid boundary between them” (Kaplan 2022, p. 5). Nonetheless, Kaplan insists that the shoot "consists of two major components: leaves and stem" (ibid., p. 4) and that "a flower is a reproductive short shoot bearing microsporophylls (stamens) … and megasporophylls (carpels) as its appendages or leaf homologues" (ibid., p. 1069). Even if the attempt to draw boundaries is given up, a crucial difference between organ-centred mainstream morphology and articulation morphology remains: organs are defined in terms of a morphological theory such as the root-stem-leaf model, whereas articulation morphology does not imply a morphological theory. It is solely based on the observable processes of ramification and articulation, independent of any morphological theory.
In summary, articulation morphology refers to the observable process of ramification and articulation: the formation of articles as the result of ramification. Both ramification and the resulting articulation are observable and therefore not dependent on morphological theories, but they presuppose the conceptualization of processes. Schultz included additional theoretical claims in his theory of anaphytes that now appear outdated. He regarded anaphytes as individuals that can form a whole plant. I do not endorse this claim and other theoretical components of his theory. I endorse only its factual basis of ramification and articulation. Morphology that is based on ramification could be called ramification morphology and morphology based on articulation, articulation morphology. I prefer the latter because it emphasizes more strongly the difference to mainstream morphology, which also addresses ramification but often in a more restrictive way concerning the formation of branches such as axillary branches. The process of ramification in articulation morphology refers to the formation of new primordia regardless of which articles they produce. Hence, in articulation morphology, ramification is used in a much broader and more fundamental sense than in mainstream morphology. This approach recognizes that structures such as compound leaves, stamens and carpels are also ramified.
Furthermore, in articulation morphology, the central and most basic concept is no longer morphological homology but transformation: the transformation of ramification and articulation. This changes the most basic questions we ask. Instead of asking questions about morphological homology, we ask how patterns of ramification and articulation have changed during development and evolution. For this reason, the new approach of articulation morphology may be considered a new paradigm of plant morphology. It changes fundamentally our way of thinking about morphology and consequently morphological investigation (for examples, see below).
Articulation morphology investigates transformation directly without the interference of morphological homology and the associated morphological categories. Different articles are not assigned to the morphological categories because categories such as those of classical morphology are not assumed in articulation morphology. Therefore, the problem or pseudo-problem of the assignment of controversial structures does not exist in articulation morphology. However, if one wants to make comparisons between articles it may be done using fuzzy set theory, where differences range from 0% toward 100%. 0% means no difference, hence sameness. If one does not or cannot quantify the difference, one can refer to “more or less different,” which equates to “more or less similar.” One could interpret the difference or similarity as the homology of articles, ranging from total to partial homology. However, as noted above, the primary aim of articulation morphology is not morphological homology but transformation. That said, other types of homology – beyond the morphological - play a role in the elucidation of evolution (Minelli 2018, Ochoterena et al. 2019).
How do we describe articles? I propose to describe articles as process combinations according to process morphology (Sattler 1990, 1992). This includes processes such as growth duration and growth distribution resulting in radial and dorsiventral growth. Articles may differ with regard to growth duration, and they may arise as radial or dorsiventral primordia. In the latter case, they may be oriented in the same plane as the article on which they are formed or in a transversal plane, that is, in a plane perpendicular to the plane of the article on which they are born. For example, teeth in serrated leaves arise in the plane of the leaf, whereas leaflets may be formed in a plane perpendicular to that of the leaf (Arber 1950, p. 116, Rutishauser and Sattler 1997).
For the convenience of communication, familiar terms may be used for the process combinations and new terms may be invented. For example, the process combinations that constitute what we call a simple leaf may be referred to as a simple leaf as long as we keep in mind that a leaf is not just a structure but a process combination. Other terms of mainstream morphology such as root and internode may also be used, and thus a limited continuity between mainstream morphology and articulation morphology is possible.
However, the difference between mainstream morphology and articulation morphology is much more fundamental than might initially seem. Whereas some articles correspond to organs of mainstream morphology, others do not. For example, a simple leaf, an internode, or a root is equivalent to an article as they result from just one ramification. However, a pinnate leaf, which is considered one organ according to mainstream morphology, is a system of articles. For flowers, the difference between mainstream morphology and articulation morphology is even more striking. Stamens are a system of articles as are carpels. They are not leaf homologues, since leaf homologues are not defined in terms of ramification and articulation. Classen-Bockhoff (2016, 2024) referred to them as sporangiophores. Sporangiophores are systems of ramification and articulation, which are processes that can be directly observed. Even a layperson can observe where a ramification occurs and the article that has been produced as a result of this ramification.
Articulation morphology, being based on open growth, includes the whole life cycle of plants. Regarding seed plants, the embryo differentiates into two poles: the root pole and the shoot pole. The root pole, through ramification and articulation, forms side roots. The first ramification in the shoot pole leads to one or two articles, the cotyledon(s). Subsequently, in the majority of seed plants, additional ramifications produce simple leaves, each of them corresponding to one article, or compound leaves, consisting of a system of articles (the leaflets). Side shoots result from axillary or extra-axillary ramification. As flowers are formed, ramifications first produce the members of the perianth, each of them corresponding to one article, and then the sporangiophores, consisting of a system of articles. As noted above, the primary aim of articulation morphology is not to enquire into the homology of the articles or systems of articles. The focus is on transformation as it occurs during the development of a single plant and how this development changed during evolution, that is, evo-devo (see below). Even the most extreme deviations from the common pattern pose no problem for articulation morphology; they are simply different patterns of ramification and articulation (see below).
Since ramification is fundamental to articulation morphology we have to distinguish different modes of ramification: dichotomous, lateral, and axillary ramification. Dichotomous ramification is common in liverworts such as Marchantia and the earliest telomic fossils such as Rhynia and Cooksonia. Whereas the articles produced in liverworts are dorsiventral, the articles in the earliest telomic fossils are mostly of radial symmetry, but a continuum from radial to dorsiventral symmetry has been documented (Sattler 1998). In the telomic fossils it is most obvious that they consist of articles. An article that is the result of two successive ramifications is called a mesome, whereas an article after a single ramification that does not ramify further is called a telome. Both mesomes and telomes are telomes in the broadest sense. Thus, a telomic fossil is a telome truss that consists of telomes in the broadest sense. It consists only of telomes (articles), not organs. According to the telome theory (Zimmermann 1952, 1959, 1965), the diversity of vascular plants has evolved through five elementary processes. These processes produced different patterns of ramification and articulation. The elementary process of overtopping leads from dichotomous to lateral ramification. The elementary process of planation describes the change from three-dimensional to two-dimensional ramification. The elementary process of fusion has been implied in leaf formation, which has led to criticism (Stein and Boyer 2006, Beerling and Fleming 2007). However, Zimmermann himself (1959, p. 105, 1961) pointed out already that “fusion” should be understood as a basipetal shift of growth. In addition to the five elementary processes, intercalary meristems leading to zonal growth play an important role, especially in flowers. For example, inferior ovaries are formed through intercalary growth. Interprimordial growth leads to a common base of primordia (a “fusion”), for example, in the formation of a sympetalous corolla.
The telome theory is more limited than articulation morphology because it does not address plant structures such as enations, leaves of bryophytes and algae. Its applicability is further constrained because it is difficult or impossible to apply it to more highly evolved vascular plants such as seed plants in which individual telomes are usually no longer recognizable. Nevertheless, to the extent that the telome theory does explain the diversity of vascular plants, it corresponds to articulation morphology because telomes are articles, not organs.
Whereas dichotomous ramification is rare in vascular plants, lateral ramification is the most common type. Additionally, axillary ramification is characteristic of seed plants. Acknowledging this, Sachs (1882) proposed a schematic ground plan of seed plants, which was adopted by classical morphologists such as Troll (1954) and Kaplan (2022). It comprises a root system and a shoot system with a stem, leaves, and axillary buds. Hence it represents the trinity of the classical categories: root, stem (caulome), and leaf (phyllome). Although meant for all seed plants, it applies only to a limited extent in the vegetative region for plants with simple leaves, each of which corresponds to an article.
For a more complete description of ramifications, the spatial arrangement of articles has to be taken into account. If we refer to phyllotaxy in articulation morphology, this notion must be understood in a wider sense: not only as the formation of leaves on the shoot apical meristem (SAM) but as the formation of articles. These articles may arise sequentially (as in spiral phyllotaxy) or simultaneously (as in whorled and decussate phyllotaxy). Deviations from these patterns occur, especially in flowers.
There appears to be a continuum from leaves to leaflets, stipules, enations, and hairs (Rutishauser and Isler 2001, Fig. 39, Rutishauser and Sattler 1986, Arber 1950, p.141). Thus, articles comprise the whole continuum from organs to enations and hairs. Since hairs are often formed much later than organs, we may distinguish two phases of ramification: a first phase of organogenesis and a second phase of hair formation, but the two phases may overlap.
Any particular plant or group of plants may be described by its peculiar sequence of ramifications and the resulting articulations. Research in plant architecture complements articulation morphology, especially with regard to higher-level units such as branches and the plant as a whole (Hallé et al. 1978, Barthélémy, and Caraglio 2007). To a limited extent, classical mainstream morphology can also complement articulation morphology. For example, since a main and side root, a simple leaf and an internode represent one article, the terminology of mainstream morphology appears appropriate. For structures that deviate so much from the classical root-stem-leaf model that they cannot be fitted into its categories, articulation morphology is advantageous because it circumvents futile debates about whether these structures are homologous to a root, a stem, or a leaf. In mainstream morphology, it is often taken for granted that any structure must be homologous to one of the three basic categories. Thus, it implies Aristotelian either/or logic. However, nature does not always follow either/or logic but is often better understood through fuzzy logic; with regard to homology, this means partial or combinatorial homology (Sattler 1994, Minelli 2016, 2023).
Many structures that do not fit classical categories have been referred to as "misfits" (Minelli 2015, Rutishauser 2005, 2016, 2020, Rutishauser et al. 2008). "Misfits" are "misfits to a botanical discipline [such as classical morphology], not misfits for a successful existence (Bell 1991). One example of misfits is phylloclades such as the phylloclades of Semele of the Asparagaceae (Cooney-Sovetts and Sattler 1987). Their homology has been debated for centuries. According to articulation morphology, they represent dorsiventral articles. Thus, if we assume that the ancestors of plants with phylloclades bore axillary branches, during evolution, these branches (a system of articles) have been replaced by a single dorsiventral article (except in the fertile phylloclades where the article bears inflorescences - systems of articles) The question of homology arises no more in this context. We do not ask whether the single dorsiventral article is homologous with a leaf or a branch. We see it as a novel process combination that may be described as a dorsiventral article. What matters in this case in the evolution of development (evo-devo) is the transformation of a system of articles (an axillary branch) into a single dorsiventral article. Endless debates about the homology of these structures are not helpful and appear futile because they are based on a pseudo-question – the faulty premise that a structure that does not fit the categories must nonetheless be fitted.
Even common structures such as compound leaves remain controversial (Rutishauser and Sattler 1997, Lacroix et al. 2003). In terms of articulation morphology, the primary question is no longer whether they are homologous to simple leaves or partial shoots. Instead, we focus on the transformation of development (ontogeny) that occurred during evolution and find that compared to simple leaves, compound leaves acquired additional ramifications and articulations. In Chisocheton tenuis we find in addition to the first formed simple and pinnate leaves pinnate “leaves” with indeterminate growth that bear also inflorescences and vegetative shoots on their adaxial side (Fisher and Rutishauser 1990). Thus, the indeterminate “leaves” present an elaborate system of articles. In evo-devo we want to know how development changed during evolution. Debating homologies does not seem helpful in this respect, but examining how ramification and articulation changed is informative (see also below in the section on evo-devo).
An extreme example of a morphological misfit is Wolffia arhiza, the smallest vascular plant on Earth. Initially, it consists of a single flattened article, often referred to as a frond (Lemon and Posluszny 2000). It lacks roots. Homologization is difficult or impossible. However, without attempting homologization, we can understand how the development (ontogeny) of Wolffia has evolved. The first frond (article) evolved through a reduction (elimination) of ramification because the embryo appears to develop directly into the dorsiventral frond (article) without a shoot apical meristem (SAM). Subsequently, additional fronds (articles) are formed through budding, which entails ramification and articulation: the formation of new fronds (articles), again without the intervention of a shoot apical meristem. Understanding these processes does not depend on identifying homologies. What matters is the transformation of development during evolution, not morphological homology. As Wake (2007) pointed out, debates on homology, whether the frond is homologous to a stem or leaf, are irrelevant to the investigation of developmental transformation and consequently are a distraction from these central issues. Since the developmental transformation of Wolffia represents an enormous deviation from the usual pattern of flowering plants, Classen-Bockhoff (2024) included Wolffia in her list of exceptions to categorical classical morphology, and Minelli (2015) referred to it as a "misfit" that does not fit within the classical categories. However, from the perspective of articulation morphology, Wolffia is neither an exception nor a misfit; it is only an uncommon pattern of articulation. There are no exceptions or misfits in articulation morphology. Hence, it is more comprehensive and more fundamental than categorical organ-centred morphology. More specifically, what is gained by working with articles?
1. Ramification and articulation are intrinsic to open growth, the most fundamental process of plant morphology. In other words, open growth occurs through ramification and articulation - the formation of articles - is a direct consequence of ramification. As such, the formation of articles is fundamental. Although mainstream morphology acknowledges the importance of open growth, it has largely overlooked articles - the most fundamental morphological units – by skipping directly from open growth to organs.
2. Articles are defined by the fundamental process of ramification, whereas organs are often defined by imposing more or less artificial boundaries, although this is not necessary and is not always done.
3. Articles are continuous with one another. The continuity may be seen as a gradient. Like articles, organs are continuous with one another. However, even when this continuity is acknowledged, organs are still defined through a morphological theory such as the classical theory with its mutually exclusive categories.
4. Articles are directly observable by anyone, being defined by ramification, whereas organs imply a morphological theory such as the root-stem-leaf model.
5. There is general agreement on what constitutes an article because it is defined operationally through ramification. In contrast, the definition of organs remains contentious. For example, a leaf may be defined differently depending on whether one adopts the root-stem-leaf model, the leaf skin model, or the metameric model. If one surpasses these models, a leaf is still defined differently in terms of the classical theory or Arber’s partial-shoot theory of the leaf (Arber 1950).
6. Articulation morphology is more comprehensive than mainstream morphology. It accommodates all observed plant structures without exceptions or problematic cases. Structures that deviate from these patterns are not anomalies; they are simply uncommon ramifications and articulations. Changes in ramification and articulation are the explanation for these uncommon patterns.
7. Articles occur in thalli and the cormus, whereas organs are restricted to the cormus.
8.Articles comprise all levels of organization from organs such as leaves to leaflets, stipules, enations, and hairs, whereas organ-centred morphology is limited to the level of organs.
9. Articles are not confined to mutually exclusive categories, whereas organs are traditionally classified as belonging to either one category or another such as stem or leaf.
10. From the perspective of articulation morphology, the focus in plant evo-devo is on changes in ramification and articulation. Homology is no longer the most basic issue, but it may still play a role in the elucidation of evolution.
As articulation morphology is more fundamental and comprehensive than categorical organ-centred morphology, the latter, although more limited, can still be seen as complementary, especially for practical reasons. Furthermore, despite the differences between articulation morphology and categorical organ-centred morphology, the gulf between the two could be bridged to a significant extent through the following changes in categorical organ-centred morphology:
a. Recognizing that, like articles, organs cannot be demarcated by boundaries, as there is a continuum within a plant between organs such as the stem and leaf.
b. Acknowledging that some organs, like simple leaves, correspond to a single article, whereas others, such as compound leaves, represent a system of articles.
c. Accepting that mutually exclusive organ categories are too rigid to encompass the full diversity of plant forms, which means admitting, in addition to categorical total homology, also partial homology (Sattler 1994), factorial or combinatorial homology (Minelli 1998, 2016, 2018). Without this broader perspective, structures that do not fit the classical categories ("misfits") would either be forced into them or considered exceptions to classical mainstream morphology. However, besides articulation morphology, a comprehensive alternative is to redefine the leaf in a very broad sense that transcends the classical categories. In his botanical notes made during his Italian journey, Goethe hinted at this broader perspective with his hypothesis: "Alles ist Blatt” (All is leaf). This means the stem and the root are also leaves, albeit with radial symmetry. Schad (2005, p. 211) defined this broad notion of the leaf as "jedes potenzreiche Grundgewebe" (all ground tissue rich in potential). Consequently, all plant structures, including those of algae, can be understood as leaves in this broad sense (Schad, personal communication). By adopting this perspective, as in articulation morphology, questionable homologizations are avoided and there are no exceptions or misfits. To prevent confusion, it would be useful to introduce a new term for the leaf in the broad sense to distinguish it from the traditional notion of the leaf.
Nine Approaches to Plant Morphology
To place articulation morphology into a broader context, I will briefly outline nine approaches to plant morphology, and then, in the next section, I will compare it with the approaches most closely related to it.
1. Classical Morphology
Classical Morphology asserts that all structures, at least in seed plants, can be understood in terms of the root-stem-leaf model. This means that any organ we encounter must be a homologue of either a root, a stem, or a leaf - without exceptions. Classical morphology still tends to be predominant in mainstream morphology. A prime example of this approach is Kaplan’s “Principles of Plant Morphology” (2022). However, classical morphology faces two fundamental problems: 1. The delimitation of organs. Since there are no observable boundaries between organs, searching for them constitutes a pseudo-problem. 2. The other unresolvable problem is the categorization of atypical structures (Rutishauser 2020). Since they do not fit the categories, attempting to make them fit is also a pseudo-problem.
Plant architecture (Hallé et al. 1978, Barthélémy and Caraglio 2007) may be seen as an extension of classical morphology. Since its focus is on higher-level units such as branches and the whole plant, it may encounter only rarely the problems or pseudo-problems of classical morphology.
2. Developmental Morphology
Developmental Morphology (according to Classen-Bockhoff 2024) explains the vast majority of plant structures according to classical morphology but recognizes, like Rutishauser (2005, 2016, 2020), that there are exceptions (misfits) that cannot be fitted into the classical categories. It also includes de novo structures not considered in classical morphology. In contrast to dogmatic classical morphology, this approach could be characterized as an open morphology.
Plant architecture is compatible with this approach.
3. Arber’s Partial-Shoot Theory
Arber’s Partial-Shoot Theory recognizes only one morphological category – the shoot (Arber 1950). According to this theory, leaves, leaflets, leaf lobes, even hairs to which leaf lobes may eventually be reduced, and roots are partial shoots ( ibid., 132-135, 140-142, 159). Since partiality is a matter of degree, Rutishauser and Isler (2001) referred to Arber’s Fuzzy Arberian Morphology (FAM) in contrast to categorical classical morphology (ClaM).
4. Continuum Morphology
Continuum Morphology (Sattler and Jeune 1992, Rutishauser 2020) has two aspects: 1. A continuum within any individual plant since there are no clear-cut boundaries between parts of a plant such as roots, stems, and leaves, and 2. A continuum between the structural categories of classical morphology. The exceptions (misfits) of Classen-Bockhoff’s morphology are absorbed within the continuum of structural categories and thus cease to be exceptions.
5. Process Morphology
Process morphology (Sattler 1992, Rutishauser 2020) envisages structures as process combinations. Τhese process combiantions form a continuum as in continuum morphology. For practical purposes, process combinations may be referred to as structures.
6. Articulation Morphology
As in Continuum and Process Morphology, there are no exceptions (misfits) in Articulation Morphology. Like other approaches, articulation morphology is based on open growth, the most fundamental process that distinguishes plants from most animals. However, contrary to mainstream morphology, articulation morphology recognizes that open growth implies ramification and articulation: the formation of articles, which have been overlooked in mainstream morphology. Articles are described in terms of process morphology as process combinations or, for practical purposes, as structures that correspond with process combinations. In articulation morphology, all morphological patterns are an expression of ramification and articulation. The most common patterns are those that are recognized by classical morphology. Those patterns that do not fit into the classical framework are simply unusual patterns of ramification and articulation. In contrast to the other approaches whose central concept is homology, in articulation morphology the focus is on transformation: transformation of ramification and articulation.
Plant Architecture complements articulation morphology to the extent that its focus is on whole plants and higher-level units such as branches.
7. Algorithmic Morphology
Algorithmic Plant Morphology involves modelling, simulation, and visualization of plant development using computer science. Various methods are employed such as computer graphics, formal language theory, and programming language design (Prusinkiewicz and Runions 2012, Runions et al. 2017, Di et al. 2021). As Minelli (2018, pp. 57-60) pointed out, this approach may involve “a view of the plant body very different from the traditional one, within which leaves, inflorescences, flowers, petals, stamens, etc. are ‘given’ - that is, represent (1) homologues … and (2) plant organs” (ibid., pp. 59-60). Instead, this approach focuses on “properties (e.g. ‘floweriness’ or ‘ ‘petalness’) with a specific …spatial distribution” (ibid., pp. 59-60). Algorithmic Morphology may contribute to the causal analysis of plant development. For example, phyllotaxis that plays a role in Algorithmic Morphology is also concerned with the causal mechanism underlying the various phyllotaxis patterns (Barabé and Lacroix 2020, Reinhardt and Gola 2022). Furthermore, algorithmic morphology has also an aesthetic appeal (Prusinkiewicz and Lindenmayer 1996).
8. Causal Morphology
Causal Morphology investigates the causation of plant development on the background of the descriptive and comparative frameworks of the preceding approaches. Nowadays, the predominant causal analysis is through developmental genetics. A considerable number of genes have been identified that influence the development of plant form. Epigenetic factors also affect gene expression. Even the experimenter may play a role in gene expression, which is known as the experimenter effect (Church 2018).
9. Functional Morphology
Functional morphology examines the functions of morphological traits. According to Bai (2017), the two major functions of plants are improvement of energy acquisition (photosynthesis) and adaptions to environmental stress.
Complementarity
Rutishauser and Sattler (1985) and Rutishauser (2020) emphasized the complementarity of different approaches. Classical morphology and developmental morphology are appropriate and useful for the majority of structures and offer convenient terminology. Classen-Bockhoff (2024), like Rutishauser (2020), recognizes exceptions (misfits) that in classical morphology are forced into categories where they don’t belong. Continuum and process morphology are more comprehensive than classical morphology and developmental morphology, incorporating the misfits within a continuum of structures or processes. Articulation morphology is also all-encompassing and, in addition, most fundamental and transformational. Algorithmic morphology uses computer modelling in contrast to the other conceptual approaches, and causal morphology analyzes the causation of the development of structures. Functional morphology is concerned with the functions of structures. Thus, each approach contributes differently to a better understanding of plant morphology. At least some of the nine approaches are not mutually exclusive but may overlap. Furthermore, the nine approaches are not exhaustive. Other approaches such as the metameric (phytomeric) and other models could be added, and Plant Architecture might be considered a separate approach.
Homology
Homology is widely considered the most basic and central concept of morphology. However, there is no agreement on how it should be defined (Hall 1994). Since Owen’s (1943) classic definition as the sameness of organs, many different definitions have proliferated (Hall 1994, Ochoterena et al. 2019). It is difficult to find a common denominator for this array of definitions, but maybe one could venture to suggest that they all revolve around the idea of correspondence and similarity or sameness with or without reference to common ancestry. Here and throughout this essay, “homology” refers specifically to morphological homology, even when not explicitly stated.
How do the nine approaches relate to homology, if at all? In classical morphology and developmental morphology (according to Classen-Bockhoff), homology is usually defined as sameness or essential similarity. Thus, if two organs belong to the same morphological category, such as stem or leaf, they are homologous. This kind of homology is based on either/or logic: an organ either belongs to a category or not. A problem – or rather a pseudo-problem - arises if an organ does not fit any of the categories, for example, if it is intermediate between two categories. In such cases, endless debates have resulted into which of the two categories the organ should be forced. To end such futile debates, Classen-Bockhoff (2024) acknowledges that there are exceptions (misfits) such as Wolffia that do not fit the categories and therefore they cannot and should not be homologized. This highlights the limitations of the classical homology concept. If, however, we accept the concept of partial, factorial or combinatorial homology (Sattler 1994, Minelli 2018), then the misfits can be accommodated as structures that are partially homologous to one or more than one category. For example, the phylloclade of Ruscus aculeatus can be seen as partially homologous to an axillary shoot and a leaf (Cooney-Sovetts and Sattler 1987). The concept of partial, factorial or combinatorial homology has been implied in continuum and process morphology (Sattler 1994). Furthermore, it has been recognized in causal morphology. For example, it was shown that during the development of the phylloclade of Ruscus aculeatus genes are expressed that are normally expressed in the shoot apex and leaves (Hirayama et al. 2007). Therefore, these authors concluded that “the phylloclade is not homologous to either the shoot or the leaf, but that it has a double identity” (ibid.). This represents a shift from either/or logic to both/and logic (Sattler 2018), thus offering a more inclusive understanding of homology.
Arber’s Partial Shoot Theory does not explicitly rely on homology. Homology is not listed in the index of The Natural Philosophy of Plant Form (Arber 1950) and I could not find any reference to homology in this encompassing book. Since, according to her theory, all structures are a partial shoot, the question of whether they are homologous to this or that category does not arise. There is only one fundamental category: the shoot. As such, her theory is a unifying framework like Goethe’s and Schad’s leaf theory (see above).
Functional morphology is not concerned with homology and the algorithmic approach also does not rely on homology. Its primary aim is to generate the widest possible range of morphological patterns. However, once these patterns have been generated, they could be compared in terms of total and partial homology. The situation in articulation morphology is similar.
Articulation morphology, like algorithmic morphology, does not aim at establishing homologies. Its primary aim is to generate the widest possible array of morphological patterns. That does not involve homology. It means seeing the development of a plant or group of plants as a succession of ramifications and their resulting articulations: the formation of articles. How does this work? We begin with the succession of ramifications and articulations and then investigate how this has evolved in other plants or groups of plants. For example, in Wolffia arhiza, in the formation of articles (fronds), the number of ramifications has been greatly reduced. In contrast, in plants with compound leaves, the number of ramifications has increased: starting with a succession of single ramifications that produce simple leaves, the formation of additional ramifications led to compound leaves. Thus, the evolution of compound leaves is explained as a transformation of the pattern of ramification and articulation, producing novel articles (the leaflets). A critic might argue that there is no difference between articulation morphology and organ-centred mainstream morphology, since the latter also acknowledges changes in ramification and articulation. There is, however, a significant difference. Mainstream morphology attempts to homologize structures such as the fronds of Wolffia and compound leaves by fitting them into classical categories. When this is difficult or impossible for structures such as the fronds of Wolffia, they are considered exceptions or misfits. This shows that the categorical framework of mainstream morphology is insufficient to accommodate all structures. In contrast, for articulation morphology there are no exceptions or misfits. It includes all structures - even highly deviant ones like the fronds of Wolffia - simply as unusual patterns of ramification and articulation. Thus, articulation morphology surpasses mainstream morphology because it is all-encompassing. Another reason why articulation morphology differs significantly from mainstream morphology is that the latter involves homologization based on a morphological theory such as the root-stem-leaf model, whereas articulation is based on the observable processes of ramification and articulation. To understand evolution as changes in ramification and articulation we do not need to enquire about homology: we do not need to ask whether compound leaves are homologous with simple leaves or partial-shoots. What matters is tracing the transformation of ramification and articulation. However, if we wish to consider questions of homology, we may still do so, though the primary aim of articulation morphology is not the search for homology, but the exploration of transformation: the transformation of ramification and articulation.
To sum up, although there is still a widely held belief that homology is and must be the most basic and central concept of morphology, this is not the case for all approaches to plant morphology. In developmental morphology (according to Classen-Bockhoff 2024), homology does not apply to exceptional forms and not to sporangiophores of flowers, which are considered de novo structures. Arber (1950) makes no explicit reference to homology. Neither algorithmic morphology nor functional morphology nor articulation morphology have homologization as their primary goal. Causal morphology may or may not address questions of homology, depending on the specific context. While continuum and process morphology have been framed in terms of total and partial homology, they can also be conceived independently of the notion of homology and morphological categories. This warrants further clarification, especially with regard to articulation morphology.
Articulation Morphology, Continuum and Process Morphology
Articulation Morphology is related to both continuum and process morphology (Sattler 1992, Sattler and Jeune 1992, Rutishauser 2020). Like these frameworks, articulation morphology is comprehensive, leaving no misfits. However, articulation morphology also differs significantly from continuum morphology. While continuum morphology relies on the classical categories as a reference system and demonstrates a continuum between them (Sattler and Jeune 1992), articulation morphology operates independently of these classical categories. It can, however, retrospectively reveal that common patterns of ramification and articulation correspond with classical categories. Furthermore, it may be possible to devise a continuum morphology that does not rely on the classical categories as a reference system.
Process morphology can be understood in at least two different ways:
1. As in continuum morphology, the categories of classical morphology are used as a reference system but they are understood as process combinations. They are linked through a continuum of process combinations, which leads to a dynamic continuum (Jeune and Sattler 1992).
2. Alternatively, process morphology and process combinations can also be understood independently of the reference system of classical morphology. In this broader context, articulation morphology can be seen as a uniquely dynamic approach based on the fundamental process of open growth that implies the equally fundamental processes of ramification and articulation. Ramification provides an observational (empirical) basis for the distinction of articles that are conceived as process combinations.
Clearly, process morphology can have different aims and foci. On one hand, it supports a dynamic continuum of process combinations – a process-based interpretation of continuum morphology (Jeune and Sattler 1992). On the other hand, focusing on the fundamental process of open growth and its associated processes of ramification and articulation, it leads to articulation morphology, which, in terms of these processes, traces the development of the whole plant from embryogenesis to the vegetative and reproductive phase. Thus, the dynamic continuum of process combinations and articulation morphology can be seen as two aspects of process morphology, which is an expression of process philosophy (Nicholson and Dupré 2018).
Homology - both total and partial – has been implied in continuum and process morphology (Sattler 1994). In continuum morphology structures are totally or partially homologous (Sattler and Jeune 1992), whereas in the dynamic continuum, it is the process combinations that show total and partial homology (Sattler 1994). However, it may be possible to conceive of a continuum and process morphology that does not imply homology. In articulation morphology, transformation, not homology, is the most basic concept: transformation of patterns of ramification and articulations. A posteriori these patterns can be compared in terms of total and partial homology, which provides a link between articulation morphology and the dynamic continuum – the dynamic interpretation of continuum morphology.
Shared Background of the Morphological Approaches
The morphological approaches, different as they are, nonetheless share a common background. This background is often taken for granted and many morphologists may not even be aware of it. It is relevant to the way we understand facts. For naïve realists, facts exist independently of us, but to critical observers, facts constitute a consensus that is due to a common background. This common background is not easily elucidated. Some of its facets include:
1. Morphology deals with the physical aspect of plant form. The physical form is perceived through vision and interpreted intellectually. Therefore, Arber (1950, p.211, 1954) understood morphology as a synthesis of the eye and the intellect or mind. Materialists maintain that only the physical realm exists. The mind is an epiphenomenon of the brain, hence, fundamentally also physical. However, there is much evidence for a reality beyond the material that has been referred to by different names such as spirit (e.g., Ravindra 1991) or consciousness (e.g., Greene 2009, Hoffman 2019). Although morphology is restricted to physicality, it is important to realize that physical form, the subject of morphology emerges out of a more encompassing reality. Contemplating forms in nature - such as a flower - may lead us to an awareness of this deeper reality.
2. The physical aspect of plant form is described and analyzed in terms of the categories of space and time, which do not exist independently of us but are our common way of perceiving reality. Mystics and some poets have long recognized that space and time do not constitute ultimate reality. In Siddhartha, Hermann Hesse (1951) wrote: “Time is not real…And if time is not real, then the dividing line that seems to lie between this world and eternity…is also an illusion.” Similarly, William Blake concluded:
To see the world in a grain of sand,
And a heaven in a wild flower,
Hold infinity in the palm of your hand,
And eternity in an hour
Plant morphologists, then, may realize that the common experience of plant form in terms of space and time emerges from a deeper reality of infinity and eternity.
3. Morphologists rely on language to describe and analyze plant form. However, words and concepts cannot fully capture reality as it is; they are an abstraction from reality. Abstracting means selecting some features while omitting others. Therefore, Korzybski (1933) concluded that whatever you say about reality is not reality. Language functions like a map: useful for navigation, but ultimately not the territory it represents.
How does all this relate to articulation morphology? I emphasized that, in contrast to organs that are based on a morphological theory, articles are factual. However, this does not mean that they represent ultimate reality. They represent a consensus of morphologists that is based on a widely shared background – however, a consensus that captures only an aspect of the reality of plants. An awareness of these limitations can lead to a deeper understanding of plants, from which morphology emerges. Contemplating a leaf or a flower, then, can become a door to a more profound reality.
Articulation morphology may be seen as an expression of the profound wisdom of the Heart Sutra, which, in Tanahashi’s (2014) translation, states:
Form is boundlessness;
boundlessness is form.
Articles are boundless, giving rise to the wholeness of the plant. Yet, this very wholeness – this boundlessness - manifests itself through the form of articles. In short: the form of articles is boundlessness, and boundlessness assumes the form of articles. There is no contradiction between the boundlessness and the articulation, which is indicated by saying that the plant is an articulated whole.
Evo-Devo and Articulation Morphology
According to evo-devo, the evolution of plants is the evolution of plant development (Minelli 2018, Rutishauser 2020). Morpho evo-devo emphasizes the morphological aspects of evo-devo (Wanninger 2015, Petrone-Mendoza et al. 2023). Articulation morphology investigates morphological changes in ramification and articulation. The evolution of land plants involved a change from dichotomous to lateral ramification and eventually also to axillary branching. Laterally formed articles, in many instances, gave rise to additional articles, for example, in compound leaves. Whereas in mainstream morphology simple and compound leaves are homologous, in articulation morphology they are not because simple leaves are due to one ramification and compound leaves to another set or sets of ramifications. What counts are ramifications and the resulting articulation. The challenge in evo-devo is to explain the change in ramification and articulation. Instead of asking how organs such as stamens and carpels changed, the more fundamental question is now how and why ramification and articulation changed, how and why one system of articles became transformed into another one.
Although a change in ramification and articulation is of central importance in evolution, we have to recognize also the prevalent repetition of ramification and articulation in both development and evolution. For example, the same articles such as a particular leaf type may be produced repeatedly along the stem of a plant. Also, much repetition occurs during evolution. Only some patterns of ramification and articulation change, whereas many others are retained over long periods.
Switching from an organ-centred approach to one centred on ramification and articulation can change the questions we ask and the insights we obtain. It can eliminate futile questions and pseudo-questions that result from looking for demarcations that cannot be found because they don’t exist.
To illustrate the difference between an organ-centred approach and articulation morphology let us consider carpels. In mainstream morphology, a carpel is interpreted as a closed megasporophyll, that is, a leaf homologue. According to articulation morphology, ramification at the floral apex produces a carpel primordium that develops into an article, the carpel, which I prefer to call a gynoecial appendage (Sattler 2024). As the gynoecial appendage develops, ramification leads to the formation of ovules: first the nucelli, then the integument(s). Hence, the formation of a carpel (a gynoecial appendage with ovules) involves three or four ramifications resulting in four kinds of articles: the gynoecial appendage, the nucellus, and one or two integuments. Contrary to the organ-centred approach of mainstream morphology, the question in articulation morphology is no longer whether the carpel is a leaf homologue. The question is how have ramification and articulation changed. This provides a new direction for evo-devo research: instead of analyzing the carpel as a whole, we have to ask questions about the ramifications and the resulting articulations: where is the placenta, which is an article, formed? How does it ramify, and what articles result from the ramification? Since these questions concern morphology, the fundamental importance of morphology in evo-devo research becomes evident. Before proceeding to analyses of developmental genetics, which are important in evo-devo, the initial questions are framed in morphological terms, and here we have the choice between categorical terms of mainstream morphology, loaded with questionable assumptions of homology, or terms of articulation morphology that refer to directly observable processes. Thus, articulation morphology can redirect analyses of developmental genetics to articles, the fundamental units of plant morphology.
It is interesting that without reference to the theory of anaphytes, which has been largely forgotten, some researchers have already moved toward it in its modern version that I call Articulation Morphology. From the perspective of developmental genetics that plays a major role in evo-devo, Mathews and Kramer (2012) concluded “that the carpel is a complex organ consisting of a foliaceous appendage and the placenta,” hence two articles: the foliaceous appendage and the placenta. On morphological grounds, Sattler (2024) came to the same conclusion. The complexity results from ramification and articulation.
Articulation morphology offers a framework for the investigation of developmental genetics in evo-devo. Focusing on the analysis of articles, can reveal aspects that have been missed in evo-devo based on organ-centred morphology and thus may open up new avenues for evo-devo research.
Conclusions
In contrast to most animals, plants exhibit open growth, which may continue throughout their life. Open growth occurs through ramification and ramification results in articulation: the formation of articles between successive ramifications and after single ramifications. Thus, as open growth, ramification and articulation are the fundamental processes in the development and evolution of morphological diversity. In contrast to mainstream morphology, whose fundamental units are organs, in articulation morphology the fundamental units are articles. They are understood as process combinations according to process morphology (Sattler 1990, 1992). To some extent, process combinations correspond with structures of mainstream morphology such as roots, internodes, and simple leaves. This allows for a limited continuity between articulation morphology and mainstream morphology. Despite this limitation, mainstream morphology remains useful and complementary to articulation morphology, but it cannot accommodate deviant structures that do not fit into its categorical framework. In contrast, articulation morphology is all-encompassing. Even the most deviant structures can be understood as deviant patterns of ramification and articulation. Thus, articulation morphology provides a more comprehensive framework for evo-devo research. Instead of being confined to organs, it can direct analyses of developmental genetics to articles, the non-controversial factual fundamental units of plant morphology, and thus open new avenues for developmental genetic research and evo-devo.
According to articulation morphology, a plant is an articulated whole: a system of interconnected articles resulting from ramification. Articles arise as growth centres (primordia) in continuity with preceding articles. They are directly observable. Anyone can see that. They are not controversial. They do not involve a morphological theory. Hence, they provide an empirical foundation for evo-devo.
Although articulation morphology is based on articles instead of organs, the connection to organs can be made. If an article does not ramify further, it corresponds to an organ. Thus, for example, a simple leaf is an article and an organ. If, however, the leaf forms leaflets, it corresponds to a system of articles. Articles that are formed between ramifications such as internodes do not correspond to an organ.
If one wants to make comparisons between articles it may be through fuzzy set theory, according to which differences range from 0% toward 100%, which means more or less different in ordinary language. One might interpret the difference, translated into similarity, as the homology of articles, ranging from total to partial homology, with total homology being 0% difference (sameness). However, in articulation morphology, the central and most basic concept is no longer morphological homology but transformation: the transformation of ramification and articulation. This changes the most basic questions we ask. Instead of asking questions about morphological homology, we ask how ramification and articulation have changed during development and evolution. This changes fundamentally our way of thinking about morphology and consequently morphological investigation. Articulation morphology investigates transformation directly without the interference of morphological homology, whereas mainstream morphology uses morphological homology as its most basic and central concept and infers the transformation of development during evolution within the framework of morphological homology.
Ramification can also be understood as an expression of differential growth. If one can see differential growth as leading to articulation, it approaches articulation morphology. The development of articles can be seen as a process of differentiation. Using the concepts of differential growth and differentiation, which are well accepted in mainstream morphology, would create a connection between articulation morphology and mainstream morphology. Since articulation morphology emphasizes transformation, prioritizing the transformation of differential growth and differentiation over homologizaton would further strengthen this connection.
Throughout the history of plant morphology, many different approaches have been developed (Cusset 1982). Proponents of different schools have often been more or less hostile to each other. However, at least some morphologists have become more tolerant, viewing different approaches as complementary (Rutishauser and Sattler 1985, Classen-Bockhoff 2024). Articulation morphology has the potential to go even beyond complementarity - without dismissing it – by offering a non-controversial, factual foundation based on ramification and articulation that can be shared by all morphologists, regardless of their theoretical preferences.
Briefly, the significance of articulation morphology is two-fold: first, to move beyond the pseudo-problems of classical morphology; and second, to offer a unified, process-oriented approach: unified because it includes all exceptions (misfits) so that they cease to be exceptions, and process-oriented because it is based on the fundamental processes of open growth, ramification and articulation: the formation of articles, whose existence has been largely overlooked. This essay seeks to reintroduce them and underscore their fundamental significance for plant morphology and plant evo-devo.
Acknowledgements: I am very grateful to Regine Classen-Bockhoff, Daniel Faccini, Bruce Kirchoff, Alessandro Minelli, and Rolf Rutishauser for their critical evaluations of the first versions of this essay, which contributed to its refinement and expansion.
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Latest update on May 22, 2025.
