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Invited Special Paper |
Department of Plant and Microbial Biology, University of California, Berkeley, California 94720-3102 USA
Received for publication June 8, 2000. Accepted for publication March 29, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONTHE SCIENCE OF PLANT...HISTORICAL HERITAGE OF PLANT...THE PROBLEMATICAL STATUS OF...A REEVALUATION OF LEAF...A REEVALUATION OF SHOOT...GENERAL CONCLUSIONSLITERATURE CITED |
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Key Words: Goethe • Hofmeister • megaphyll • microphyll • plant morphology • primary thickening growth • Pteridophytes • systematics • Troll • von Goebel
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONTHE SCIENCE OF PLANT...HISTORICAL HERITAGE OF PLANT...THE PROBLEMATICAL STATUS OF...A REEVALUATION OF LEAF...A REEVALUATION OF SHOOT...GENERAL CONCLUSIONSLITERATURE CITED |
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In this article I attempt to clarify the concept of plant morphology as a discipline, review its historical heritage, and discuss how it relates to and differs from systematics. I show that plant morphology is a scientific discipline with its own principles, from which predictions can be made about the unknown. I illustrate some of these general principles and their application by evaluating them in a phyletically heterogeneous plant group, the pteridophytes, which previously had been interpreted largely by models from fossil rather than contemporary plants.
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THE SCIENCE OF PLANT MORPHOLOGY |
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TOPABSTRACTINTRODUCTIONTHE SCIENCE OF PLANT...HISTORICAL HERITAGE OF PLANT...THE PROBLEMATICAL STATUS OF...A REEVALUATION OF LEAF...A REEVALUATION OF SHOOT...GENERAL CONCLUSIONSLITERATURE CITED |
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), plant morphology in the United States was defined as the study of the anatomical and cytological features of the life histories of plants expressed in a taxonomic framework. Hence, the emphasis was on the microscopic details of vascular plant reproduction and systematic relationships with the focus of the German tradition relegated to brief accounts of the plant's habit.
In the context of our country's emphasis on tools and techniques rather than philosophy, this microscopical/life-history conception of plant morphology doubtless was seen as being more rigorous than the seemingly less precise study of form relationships based on external morphology, i.e., the German tradition. A series of influential textbooks exemplifying and promoting this Anglo-American conception of plant morphology developed through the years, including the most recent editions of Bold, Alexopoulos, and Delevoryas (1987)
; Gifford and Foster (1989)
; and Scagel et al. (1984)
. These works not only reinforced this life-history emphasis in research and pedagogy of vascular plants, but also resulted in a similar emphasis in the study of the bryophytes (Schofield, 1985
), algae (Bold and Wynne, 1985
), and fungi (Moore-Landecker, 1990
).
In contrast to this American conception of plant morphology, the German tradition can be characterized as the science of form relationships with the emphasis on the term relationships expressed at the whole plant and organ levels of organization. The contrast of plant morphology with systematics is illustrated in Fig. 1, where the field of plant morphology is illustrated as a central sphere that overlaps tangentially with systematics but is not equivalent to it. The arrows between the two fields indicate the mutual exchange of information and influence that occurs between them, as with the other disciplines shown. Despite this overlap, however, plant morphology and systematics are two different disciplines with different centers of gravity. In systematics, the emphasis is on the homologies in a phylogenetic sense, whereas in morphology, the emphasis is on the analogies or convergences in a phylogenetic sense. The principles of morphology transcend the systematic boundaries. Thus the two disciplines operate in opposite directions. Systematics uses morphological characteristics to carve diversity into its taxonomic subunits, whereas plant morphology uses diversity to deduce fundamental themes regardless of the systematic affinities. Hence, from first principles, systematics can be characterized as a dividing discipline, whereas plant morphology is a unifying discipline.
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Not only can plant morphology be delimited horizontally from other biological disciplines but it also can be vertically delimited from other levels of biological organization. The discipline of plant morphology encompasses the whole plant down to the organ level of organization (Fig. 2). While it occasionally uses the anatomical level of organization as morphological markers, it can only legitimately do so with histological characteristics that are correlated developmentally with morphogenesis or form generation. It has been demonstrated that the plant's morphology is an emergent property relative to its anatomy; i.e., the two levels of organization can be relatively independent and the anatomical level does not determine the morphological level (Kaplan and Hagemann, 1991
; Cooke and Lu, 1992
; Kaplan, 1992
). Similarly, the next higher level of organismal organization, growth habit, is an emergent property relative to the plant's morphology (Kaplan and Groff, 1995
). For example, members of the cactus family (Cactaceae) are characterized by an idiosyncratic shoot morphology (see Fig. 4). However, this distinctive shoot form does not limit the variety of growth habits cacti exhibit; one can find cacti growing as trees, shrubs, cushion plants, vines and even plagiotropic, rhizomatous forms (Rauh, 1979
).
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In order to more effectively characterize plant morphology I shall contrast it with what has been called "phytography" because there has been a tendency to confuse the two. Phytography refers to the naming of plants and/or plant parts. It is what has been termed "descriptive botany." For example, in the drawing of different leaf parts and types illustrated in Fig. 3 from Lawrence's introductory taxonomy book (Lawrence, 1955
), the application of the descriptive terms to each leaf or blade type is what comprises phytography. By contrast, plant morphology seeks to understand the common denominator that underlies or links these seemingly diverse and unrelated leaf forms. The plant morphologist comes to these conclusions of structural relationship by the comparative study of plant form between species and along the length of the metameric organism (serial homology or "homonomie") as well as by the study of organogenesis and experimentally induced variants, which supply additional, often cryptic clues about structural relationship. Thus, from the outset and at its very core, plant morphology is a comparative discipline concerned with the connectivity or linkages between characteristics, not their isolated expression. And while plant morphology is not obligately tied to phylogenetic formulations of form relationships, these linkages in character expression are, in my opinion, the most compelling evidence that the diversity of plant form we see on the earth today is the result of evolution.
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), making morphological connections easy to deduce. From these figures it can be deduced that the divergence of the shoot in species such as the barrel cactus from the more typical dicotyledonous shoot morphology involves a reduction in the degree of expression of the upper leaf (lamina–petiole) zone in favor of the development of the lower leaf zone as a decurrent leaf base or podarium accompanied by a marked increase in axis primary thickening (compare Fig. 4D with 4A–C). Hence, what might appear to be a radical departure in plant form can be shown to occur within a stereotypical organizational theme or "Bauplan" within the Cactaceae. That parallel changes in morphology have occurred in independent phyletic lines (e.g., Euphorbiaceae, Asclepiadaceae) reflects the basic morphological principles that are repeated in contemporary plants regardless of their systematic affinity. The characterization of these morphological themes and the principles they represent is the central goal of plant morphology as a basic science.
Finally, a corollary to a form relationship concept of plant morphology is that the concept of homology in this context refers simply to structural correspondences and not commonality of descent (Kaplan, 1984
). Such an agnostic outlook toward plant structural correspondences does not preclude their phylogentic application, but insures that structural correspondences will be more soundly determined because they have to be self-standing rather than resting on a phylogentic argument.
Because a science, just like an organism, is profoundly affected by its evolutionary history, in the next section I describe how the heritage of plant morphology has resulted in the development of its philosophical perspectives and analytical tools for evaluating plant form. Then I shall apply these perspectives and tools to the challenging problem of how to interpret shoot organization in different pteridophyte groups.
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HISTORICAL HERITAGE OF PLANT MORPHOLOGY |
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TOPABSTRACTINTRODUCTIONTHE SCIENCE OF PLANT...HISTORICAL HERITAGE OF PLANT...THE PROBLEMATICAL STATUS OF...A REEVALUATION OF LEAF...A REEVALUATION OF SHOOT...GENERAL CONCLUSIONSLITERATURE CITED |
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Despite its history of over two centuries, German plant morphology has had only four principal figures who were significant in its development: Johann Wolfgang von Goethe, Wilhelm Hofmeister, Karl von Goebel, and Wilhelm Troll. I now look at these gentlemen individually and collectively to have some sense of the path of development of plant morphology and the reasons it took the directions it did.
Johann Wolfgang von Goethe (1749–1832)
The celebrated German literary dramatist and poet Johann Wolfgang von Goethe also had strong interests in the sciences, having contributed not only to plant morphology, but also to the study of color, mineralogy, and animal skeletal morphology among many other fields (Fig. 5A) (Mann, Mollenhauer, and Peters, 1992
). Goethe originated the term "morphology," and more significantly, its methodology, i.e., comparative morphology or typology. His most significant contribution was the perspective that despite all the organographic diversity that flowering plants exhibit, one could deduce a fundamental organizational theme or "Bauplan" that linked this morphological variety. Moreover, Goethe theorized that knowing the fundamental "Bauplan" of an organism enabled one to predict plant forms that had not been discovered (Mueller and Engard, 1952
). Because these perspectives were originally published in 1790 in Goethe's book Versuch die Metamorphose der Pflanzen zu erklären ("An Attempt to Explain the Metamorphosis of Plants"; Goethe, 1790
) the origin of plant morphology as a discipline can be dated by the appearance of his pivotal publication.
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). Nevertheless, a significant range of research was carried out by idealistic morphologists, such as Alexander von Braun, who continued the Goethean tradition into the latter part of the 19th century. However, since Darwinian evolution simply supplied the explanation for the origin of many of the homologies determined by the Idealistic School, there actually was no conflict between these different points of view.
Wilhelm Hofmeister (1824–1877)
Undoubtedly the most notable figure in the history of plant morphology was Friederich Wilhelm Benedikt Hofmeister (Fig. 5B). Known principally as the discoverer of the alternation of generations and for his fundamental studies of plant embryology, Hofmeister is equally significant for having sired the most notable lineage of German plant morphologists. Since we have already devoted an extensive article to his life and contributions (Kaplan and Cooke, 1996
), I will summarize here his relevance to the science of plant morphology.
Hofmeister was an autodidact in botany and stands as one of the real geniuses in the history of botanical science. He had no university education, much less a Ph.D. degree, but ultimately was appointed Professor of Botany at Heidelberg at age 39. The fact that he was self-taught also explains the sharp separation between him and the idealistic morphological tradition that preceded him. Whereas the idealistic morphologists were concerned with the relationship of plant forms to one another, Hofmeister asked why plants exhibit these form relationships, i.e., what is the causal basis for this morphological diversity? To these questions he brought an impressive arsenal of tools and perspectives from physics and chemistry, all of which he also taught himself. As one of the earliest plant biophysicists, Hofmeister was so far ahead of his time that he was not understood by his contemporaries or many who followed him (Kaplan and Cooke, 1996
).
Hofmeister's principal contribution to the field of plant morphology was his book Allgemeine Morphologie der Gewächse ["General Morphology of (Plant) Growth," Hofmeister, 1868
], published as part of the series entitled the "Handbook of Physiological Botany" (Handbuch der Physiologischen Botanik) of which Hofmeister was the general editor. Even the title's emphasis on plant growth underscored its dynamic, developmental focus, representing a revolutionary break with the idealistic morphological tradition (Troll, 1937
). Hofmeister not only presented a fundamentally analytical view of the developmental basis underlying the diversity of plant form, but also biophysical interpretations of a range of phenomena including phyllotaxis and the effects of gravity and light on a plant's morphology. Although it was not an easy book to read or understand, it had a great influence on changing the outlooks of subsequent practitioners and was the first modern treatise on plant morphology, presaging the great tradition of plant morphogenesis that was to be expressed later in the 20th century.
Karl von Goebel (1855–1932)
Karl Ritter Eberhard von Goebel was a disciple of Hofmeister (Fig. 5C). Von Goebel, born in Billigheim in the state of Baden near Heilbronn, where his father owned a machine factory, would attend the University of Tübingen. Initially, following the wishes of his mother, he studied theology and philosophy. However, he switched to botany after coming under the influence of Hofmeister, who had come to Tübingen as Professor of Botany from Heidelberg in 1872. Had Hofmeister been in better health during his time at Tübingen, it is likely that von Goebel would have done his doctoral work with him. However, von Goebel moved in 1876 to Strasbourg, where he completed his doctorate with Heinrich Anton de Bary (Speta, 1997
). In spite of this brief exposure, Hofmeister would be a lasting influence on von Goebel's career and von Goebel would write extensively about Hofmeister (von Goebel, 1926
). It was his contact with Hofmeister that led von Goebel to develop his interest in morphology, especially its causal aspects, and in the study of cryptogamic plants. His knowledge of the algae, fungi, and plant anatomy was enhanced by his experience with DeBary.
Besides Hofmeister, the other significant influence on von Goebel's development was the great physiologist anatomist Julius von Sachs at Würzburg, whom von Goebel served as an assistant from 1878 through to his habilitation in 1880. Sachs' influence was expressed in von Goebel's experimental approaches to plant morphogenesis as well as his interest in physiological explanations of plant form. Sachs became a lifelong friend of von Goebel, and the two carried on an extensive correspondence until Sachs' death in 1897 (Bergdolt, 1942
).
Von Goebel occupied a succession of academic posts, proceeding from Strasbourg in 1881 to the University of Rostock from 1882 to 1886, and the University of Marburg from 1886 to 1891, when he received the call to Munich. At the University of Munich, von Goebel created the world famous Botanical Garden and Botanical Institute at Nymphenburg and established it as a center for the training of plant morphologists.
In contrast with Hofmeister, whose plant collecting activities were restricted largely to central Europe, von Goebel was an inveterate world traveler, traveling to India and Java in 1885–1886, to Australia and New Zealand in 1898–1899, to North America in 1905, and to Brazil in 1913. In 1925, at age 70, he made a second journey to Java (Speta, 1997
). During these trips von Goebel collected a tremendous diversity of plant species, greatly expanding the range of phenomena that had been accounted for in previous morphological treatises. Von Goebel had an eye for detail and a synthetic perspective that allowed him to place phenomenology in the context of whole-plant diversity. Not only did his knowledge cover vascular plant diversity worldwide, but also the cryptogams, especially the bryophytes. In fact, to this day, von Goebel's account of the bryophytes in his Organographie der Pflanzen (Organography of Plants) stands as the most comprehensive account of their comparative morphology (von Goebel, 1928–1933
).
Although he published numerous individual papers, Goebel's morphological legacy was his monumental treatise Organography of Plants, a three-volume work that appeared in three editions between 1898 and 1933 (von Goebel, 1898–1901, 1913–1923, 1928–1933
), including an English translation in 1900 (von Goebel, 1900–1905
). Because of its English translation, von Goebel's perspective and influence would be wider than that of either Hofmeister, who preceded him, or Wilhelm Troll, who followed him. Von Goebel purposely called his work "Organography" to underscore its causal orientation and hence avoid the stigma of "idealistic morphology." Furthermore, the goal of organography was to distinguish those features of plant form that could be understood as adaptations to environmental (external) conditions from those that were a result of inner, presumably genetic, bases. Reflecting his experience with Sachs, he emphasized the functional aspects of plant organs as well as their form relationships. In some of his deductions on the causal significance of a plant's morphology von Goebel would invoke rather vague physiological explanations, such as nutritional or hormonal (integrative) causes, and these, coupled with simple but naive experiments, represented the weaker elements of his legacy. However, the fact that he questioned why plants took the form they did ultimately made him the spiritual father figure of plant morphogenetic research in the 20th century.
By the time that von Goebel was a young Ph.D., Darwinian evolution had made its impact. Remarkably, in his own plant morphology treatise Hofmeister (1868)
had already fully assimilated Darwin's Origin of Species (Kaplan and Cooke, 1996
). Hence, in von Goebel's era, phylogenetic interpretations of plant morphology came to supersede those of idealistic morphology. Von Goebel nevertheless maintained a healthy skepticism toward such phylogenetic speculation. While he was inclined toward physiological explanations of the many variants in plant morphology, he also was highly critical of the simplistic adaptationist interpretations that were rampant in that era. Such skepticism toward phylogenetic theorizing and the adaptive mode of much of plant structure would be passed on to his disciples, resulting in an even sharper reaction from people such as Wilhelm Troll.
Wilhelm Troll (1897–1978)
Of the four major figures in German plant morphology, the most complicated and controversial was Wilhelm Julius Georg Hubert Troll, a doctoral student of von Goebel at Munich (Fig. 5D). Troll was the son of a psychiatrist-neurologist Theodor Julius Troll and was born in Munich but raised in the fore-alpine region south of Munich (in Gabersee, near Wasserburg/Inn) (Nickel, 1996
). In these natural areas and the Bavarian Alps Wilhelm and his younger brother Karl developed their intense interests in nature and in plants in particular. Karl Troll became one of the premier plant geographers, ultimately becoming more famous than his brother Wilhelm.
Wilhelm Troll completed his doctorate with von Goebel in Plant Morphology at the University of Munich in 1921. He then served as an assistant to von Goebel in the Botanical Institute, becoming habilitated in 1925. From 1928 to 1930 he participated in the Sunda Expedition to Malaysia, principally studying root structure and function in mangrove vegetation. In 1932, he was appointed Ordinarius Professor and Director of the Botanical Garden at the Martin Luther University in Halle and served in that capacity until 1945, near the end of World War II. Because Halle ultimately came to be located in the DDR (East Germany), Troll and a whole host of East German intellectuals were moved by the U.S. forces to the west zone just in advance of the Russian occupation in July 1945. From July 1945 to January 1946 Troll obtained an interim teaching position at the Gymnasium school in Kircheimbolanden/Pfalz. Finally, in May 1946, he was appointed Ordinarius Professor and Director of the Botanical Institute and Botanical Garden of the newly reconstructed University of Mainz in West Germany. He retired in March 1966 and worked as an emeritus Professor until his death on 28 December 1978 at age 81 (Nickel, 1996
). Thus, Troll's life and career spanned the most tumultuous era in German history, including the two World Wars, and the nature of his career and perspectives must be evaluated against that background.
Prior to his full-time entry into the University of Munich, Wilhelm Troll served in the German Army as a lieutenant on the Western Front in World War I, from 1916 to 1918. Like many Germans, this experience had a devastating affect on him that no doubt influenced many of the scientific perspectives he would develop. He withdrew from his native Catholicism and, like many in this postwar period, developed a reaction against industrial materialism, mechanism in science, and the tendencies of contemporary science to focus on narrowly circumscribed, mathematically based problems (Nickel, 1996
). This disillusionment engendered a desire to return to a more romantic era of Germany's past, to holism and the idealistic morphology of Goethe.
Von Goebel was fond of saying that only those phenomena could be called morphological that could not yet be explained physiologically ("morphologisch das sei, was sich physiologisch noch nicht erklären lasse"; cited in Nickel, 1996
). Troll, however, did not feel that one could deal with morphology causally. He believed that one could only deal with description and presentation ("Darstellung"), but that morphological relationships or typologies were not susceptible to explanation or causal analysis. Troll, like Goethe, saw the central goal of morphology as the analysis of diversity and the deduction of types. This typological approach was basically an intuitive process that would be evident to the investigator once he or she had analyzed the spectrum of form variants. Like Goethe, Troll believed that the types were real, not just abstractions, and that they stood behind the diversity that one saw in the physical world. In many ways, Troll held a platonic view of the biological world.
Troll felt that the pinnacle of morphology would be knowing the diversity of forms so well that one could predict morphologies that had not yet been discovered or described (Troll, 1928
). The best analogy for Troll's goal of plant morphology is the development of the equivalent of the Periodic Table in chemistry. According to such a perspective, the range of variants could be derived from the type by quantitative variations in growth distribution, a point of view represented by Goethe's principle of variable proportions (Troll, 1949
). In fact, Troll's idealistic morphological accounts of the variations in plant form in his treatises (Troll, 1937–1943
) are very reminiscent of D'Arcy Thompson's theoretical derivations of differences in animal morphology (Thompson, 1917
). Many of Troll's constructs were purely hypothetical and not tested by actual developmental studies. In a few cases, they turned out to be wrong because they were based on the false assumption that all developmental changes were strictly quantitative in nature, when in fact qualitative changes in development can also be significant (Kaplan, 1980
). Thus, while Troll's idealistic morphological theorizing can be useful pedagogically, in other instances it can be misleading. Nevertheless, because he used variations in development as an underpinning of his typological deductions, Troll's treatises and papers are a useful resource for information on comparative plant development.
Troll's typological approach became especially murky with reference to questions of phylogeny. From von Goebel he inherited a skepticism toward the more simplistic phylogenetic deductions of the time. He had also developed his own skepticism about relying on fossil plants for a definitive picture of plant evolution; he saw the fossil record as being too fragmentary and lacunate to be able draw any valid phylogenetic conclusions from it. Such views put Troll at loggerheads with the noted German paleobotanist/phylogenist Walter Zimmermann, the author of the telome theory (Zimmermann, 1965
). The two carried on a polemical debate in the literature (Zimmermann, 1930, 1937, 1953, 1959, 1968
; Troll, 1937–1943
) without resolution because of its partisan nature.
In reality, Troll's views on Darwinian evolution were complex. Looking at his typological philosophy superficially, with its quasi-religious overtones, it would be easy to paint him as anti-evolutionary, and there are some who have done so (Eyde, 1975
). However, in reality, Troll conceded that evolution was the best explanation we have of the succession of forms found in the earth's history (Nickel, 1996
). Darwin's recognition of the basic unity of type in different groups served as a point of harmony between Troll and Darwin (Troll, 1925
). They differed, however, in their views about what this unity of type represented. Darwin felt it reflected the commonality of descent, whereas Troll considered it to be a form principle that was more fundamental than geneology. Because he saw his typologies as fundamental natural expressions, Troll felt that classification systems could be built upon them. Furthermore, since they involved a consideration of entire organisms and the integration of their form relationships, Troll believed the typologies were more significant than the individual, isolated characteristics upon which systematists tended to base their conclusions.
While Troll conceded that natural selection did play a role in the origin of some characteristics of organisms, he did not believe that it could explain all of the variations in form. Certainly, modern views of structural evolution would incorporate the idea that the organizational theme or "Bauplan" of the organismal group in question have to be taken into account in any consideration of plant evolution (Kaplan and Groff, 1995
). Thus, Troll inveighed against a strictly random conception of the evolutionary process.
Interestingly, Troll postulated that major jumps in the evolution of forms could occur, as opposed to the gradualism represented in Darwin's views. Eldredge and Gould's theory of "punctutated equilibrium" (Eldredge and Gould, 1972
; Gould and Eldredge, 1977
) would have found some resonance with Troll, even though their philosophies were very different. Despite starting from altogether different first principles and being colored by an element of skepticism about the simplistic features of phylogenetic thinking and Darwinian dogmatism, Troll's views of plant phylogeny are not as extreme as they might seem.
Like von Goebel and Hofmeister, the central point of Troll's contributions and perspectives were contained in his major, multivolume treatise entitled Vergleichende Morphologie der höheren Pflanzen, (Troll, 1937–1943
) ("Comparative Morphology of Higher Plants"). Whereas von Goebel tried to distance his own work from its idealistic morphology predecessors by calling it "organography," Troll's naming of his treatise "comparative morphology" was intended to express his return to that idealistic tradition. If von Goebel's treatise was impressive for its time in terms of the breadth and depth of its coverage, Troll's was even more so. Troll's work was more complete and comprehensive than von Goebel's and also better organized and more clearly written. Whatever questions one might have about Troll's scientific philosophy, one could never fault him as a didactor and empiricist. The quality and clarity of his artwork and photography set new standards. These same high standards of description and illustration would characterize Troll's work for his entire career. A testimonial to their high quality is the great number of modern, non-German texts that have drawn upon Troll's figures long after his works were out of print (e.g., Gifford and Foster, 1989
).
Troll's comparative morphology treatise, an amalgamation of his own research and the work of others, was the most comprehensive to date. The formal work was intended to be a programmatic presentation of the complete range of vascular plant morphology, both vegetative and reproductive. Only the first three volumes dealing with vegetative morphology were published. Volume I dealt with vegetative shoot morphology, Volume II dealt with vegetative leaf morphology, and Volume III with the morphology of roots and root systems. The original intention was to follow with volumes on reproductive shoots ending with seed and seedling morphology. Unfortunately, World War II interrupted the work.
Troll's principal activity in his postwar position in Mainz was the continuation of this programmatic work, beginning with inflorescence morphology. Unfortunately, Troll's contributions in this area became so excessive in detail and quantity (he is reputed to have studied literally thousands of species in >300 families; Troll, 1969
) that he never completed the remainder of the program. Not even his most active disciple, Focko Weberling, was able to complete the inflorescence program, so massive and extensive was this undertaking. Fortunately, Troll did publish a more compact overview in his companion volumes entitled Praktische Einführung in die Pflanzenmorphologie ("Practical Introduction to the Morphology of Plants"), which appeared as a two volume work (Troll, 1954, 1957
) and covered the more general aspects of flower, fruit, and inflorescence morphology in economic plants (Troll, 1957
).
In the final analysis, despite having a number of notable disciples, Troll's idiosyncratic philosophy was not practiced or promoted actively by his students. His students tended to represent much more conventional perspectives and made syntheses with other areas of interest. The only long-term benefit of Troll's typological orientation was his belief that only way to deduce types was through the rigorous and accurate characterization of nature. Thus, Troll's lasting contributions were his exceptionally detailed, lucidly presented comparative studies of plant morphology and his effective organization of the subject. While it was good to have such an extensive subject represented by a single, uniform perspective, the negative side has been that such an exhaustive treatment gives the impression that everything has been studied and therefore the subject of plant morphology is closed. Nothing could be further from the truth. No matter how extensively a given discipline may be studied by an individual, the work of that person is restricted to a particular time in history. With the advent of new technologies and accompanying new perspectives, every discipline, regardless of its age, is subject to revision. No matter how empirically based they may have been, Troll's contributions contain uncertainties that need to be revisited if for no other reason because they were colored by his distinct philosophical biases.
Today most of the tradition of plant morphology has died out in Germany, with only a handful of Troll's former students, such as Focko Weberling, Albrecht Siegert, Wolfgang Hagemann, Hans Froebe, and Weberling's student Thomas Stützel, carrying on any semblance of this heritage.
Historical conclusions
Having reviewed the major figures in the history of German plant morphology and their contributions to the development of the field, I now want to return to the original question of why the field became eclipsed. Given the fundamental nature of the contributions of these notable figures, why hasn't this science made a greater impact on contemporary plant biology?
Clearly there are a variety of reasons, some obvious and others subtle. One of the most obvious reasons is the language barrier. Even if investigators do have some facility with German, their tendencies will be to focus on a particular set of facts or descriptions in these large treatises and to shy away from the broader, more philosophical expositions in them. This is due in part to the fact that the historical and/or philosophical presentations are more difficult to read and involve grammatical and interpretive nuances that can be beyond the German reading ability of the average Anglo-American morphologist. As a result, many of the broader interpretive issues or frameworks from this German heritage tend not to receive any consideration in this country. This situation is further exacerbated by the recent declines and almost complete disappearance of requirements for foreign language skills in Ph.D. programs in the United States. Therefore, is it any wonder that there is no critical assessment or understanding of Troll's philosophical perspectives among contemporary non-German botanists?
Another obvious barrier to the penetration of this German conception into our U.S. scientific culture is the aforementioned emphasis on tools and technology here, in contrast to the philosophically grounded approaches of Europe. Moreover, with the advent of molecular techniques in this decade, this gulf has become even wider because plant morphology as a discipline is grounded in organismal biology and the latter has virtually disappeared from view. Once we have sequenced all of the relevant plant genomes and have come to realize that such sequence data leaves many questions in organismal biology unanswered, we may finally appreciate that organisms are valid and fundamental biological units worthy of our attention. Then morphology may finally be appreciated and respected as a key to the understanding of plant organismal biology.
The broad historical trends of plant morphology, have followed the general path of any science: description of phenomena, classification of those phenomena, and the investigation of the causal linkages between phenomena. These developments have received different degrees of emphasis in the respective practitioners. For example, both Goethe and Troll were concerned more with the classification and integration of morphological phenomenology and Goebel and Hofmeister more with the causal aspects. During the development and progressive refinement of the subject, however, all of its past practitioners have contributed to both the causal and descriptive areas of the science.
With the current emphasis on genetics in biology, plant morphology today focuses more on the causal aspects of plant form. Even though the mode today is to focus on selected "model systems" because of their greater ease of experimental manipulation, in fact, you cannot derive general principles from such model systems. Such principles can only be derived from the type of broad, comparative investigations plant morphology traditionally has provided. Instead of seeing exhaustive treatises like Troll's as the endpoint in the development of the subject, they should be seen as starting points in the development of a more integrated view of plants as organisms.
And while today plant morphology may play a less fundamental role in mapping out phylogenies than it has in the past, it can play a significant role in evolutionary biology in general. Not only can it help elucidate the developmental basis for the evolution of form in the respective plant groups (Kuzoff, Hufford, and Soltis, 2001
), but it also can be significant in giving evolutionary biologists a clearer picture of "developmental constraints" (Smith et al., 1985
) and their role in the evolution of morphology and its adaptive significance.
Similarly, the great record of plant morphology can be of significance to the paleobotanists in their characterization of the evolution of plant form. While it is true that the interpretation of ancient extinct vascular plants should not be biased by the study of contemporary representatives alone, neither should fossil plants be studied without a full understanding of the morphological principles underlying the diversity of contemporary plants. Since the study of fossils has tended to be biased toward anatomical data, the context of contemporary plant morphology has not been used sufficiently to determine the actual morphological status these extinct groups show. In the next section I illustrate the problems with the latter approach and the insights from the study of contemporary plants that plant morphology can provide for the study and interpretation of the broad patterns of structural evolution in vascular plants.
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THE PROBLEMATICAL STATUS OF PTERIDOPHYTE MORPHOLOGY |
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TOPABSTRACTINTRODUCTIONTHE SCIENCE OF PLANT...HISTORICAL HERITAGE OF PLANT...THE PROBLEMATICAL STATUS OF...A REEVALUATION OF LEAF...A REEVALUATION OF SHOOT...GENERAL CONCLUSIONSLITERATURE CITED |
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Pteridophytes are linked only by a common life-history pattern: a heteromorphic alternation of generations, between a dominant, free-sporing sporophyte and a free-living but highly reduced gametophyte (Gifford and Foster, 1989
). Because the pteridophytes are not a natural group, the morphological correspondences they exhibit are indicative of fundamental principles and thus provide a good illustration of the goals of plant morphology as a discipline. All members of this group (Psilopsida, Lycopsida, Sphenopsida, and Filicopsida) have a more extensive representation in the fossil record than among contemporary plants, and interpretation of their morphology has been based largely on fossil rather than contemporary plant models. However, despite their ancient phyletic lineages and phylogenetic heterogeneity, we now want to ask whether contemporary pteridophytes exhibit the same basic shoot organizational principles as those exhibited by seed plants or whether they exhibit ancient morphological properties that are not to be found in any other contemporary plants.
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A REEVALUATION OF LEAF MORPHOLOGY IN THE PTERIDOPHYTES |
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TOPABSTRACTINTRODUCTIONTHE SCIENCE OF PLANT...HISTORICAL HERITAGE OF PLANT...THE PROBLEMATICAL STATUS OF...A REEVALUATION OF LEAF...A REEVALUATION OF SHOOT...GENERAL CONCLUSIONSLITERATURE CITED |
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).
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By contrast, megaphylls have been considered to have originated by a process of cladification (derivation from branch systems) from isotomous, dichotomizing, rhyniophyte ancestors (Fig. 6F), including processes of anisotomy or "overtopping" (Fig. 6G), followed by planation (Fig. 6H) and webbing to form laminate leaves (Fig. 6I). This interpretation, which was formalized as the Telome Theory by Walter Zimmermann (1930)
, has been the prevailing view of the evolutionary origin of megaphyllous organs. The complex venation of the megaphyll leaf product was thus seen as an evolutionary fusion and planation product of a number of protostelic axes (Fig. 6F–I). The appeal of Zimmermann's theory was that it explained the origin of both the morphological and anatomical features of megaphyllous leaves.
Regardless of how firmly entrenched the concepts of microphyll and megaphyll may be in the literature, there are numerous contradictions and inconsistencies that make these concepts questionable and indefensible from the viewpoint of comparative morphology. In the first place, as concepts, they are anatomically, not morphologically based. Given that it is the vascular tissue, particularly the xylem, which tends to be best preserved in fossil plants, it is understandable that the practicing paleobotanist would focus on the vascular strands in defining organ natures and morphology. Anatomical perspectives tend to imply that the vascular system determines the organ's morphogenesis. However, contemporary studies of the relationship of histogenesis (tissue differentiation) to morphogenesis have demonstrated either the independence of these processes or that the morphogenesis is the primary process with histogenesis following form development (Hagemann, 1967
; Kaplan and Hagemann, 1991, 1992
; Cooke and Lu, 1992
; Kaplan, 1992
; Kaplan and Cooke, 1997
). Thus, while anatomical characters may be the only source of organ definition in many fossil specimens, they can no longer be seen as more basic than the morphology. Whether an organ is or is not a leaf is defined not by its vasculature, but by other, subtler, more fundamental morphological relationships, i.e., basic dorsiventrality of the leaf organ and its distinctive meristem distribution in relation to this symmetry pattern (Kaplan and Groff, 1995
).
Regardless of these fundamental considerations of organ determination, within the examples of microphyllous and megaphyllous leaves, each of the criteria are either conflicted or contradicted in each of the major plant groups to the point that it is difficult to distinguish microphylls from megaphylls among contemporary vascular plants. For example, Wagner, Beitel, and Wagner (1982)
have described species of Selaginella (S. adunca and S. schaffneri) as having complex dichotomous to reticulate venation patterns in what otherwise have been considered to be classic microphyllous leaves.
Conversely, ferns in the genera Lygodium, Gleichenia, and all of the filmy ferns (Hymenophyllaceae) have large, dissected fronds with complicated venation, but their stems are protostelic without leaf gaps. Hence, on the basis of their vascular supply, they would not qualify as megaphylls even though other features of their morphology and anatomy make them classical examples of megaphyllous appendages. And while the univeined appendages of Equisetum suggest that they are microphyllous leaves, its fossil representatives, such as species of Sphenophyllum, have more elaborated leaves with dichotomous venation (Taylor and Taylor, 1993
). These species illustrate the lack of correlation between anatomical and morphological features of an organ and underscore that the anatomical features cannot be substituted for morphological characteristics in drawing morphological conclusions.
One could, with equal justification, ask why the linear, univeined leaves in many conifers are not microphylls. The principal reason is that morphologists know that species of Araucaria, Agathis, and Podocarpus have larger leaves with elaborate dichotomous venation and hence assume that the simple, univeined conifer needle has been derived by reduction.
Even the concept of leaf gap in so-called megaphyllous plants (ferns and seed plants) is conflicted and difficult to define. For example, Beck, Schmid, and Rothwell (1982), in a thorough review of stelar structure, have shown that the primary vascular system in the majority of seed plants consists of a longitudinal system of leaf trace sympodia, the leaf traces of which are impossible to distinguish from their sympodial continuations because every axial component ultimately supplies a leaf and itself can be considered a leaf trace. Furthermore, it is largely in those closed sympodial systems with lateral interconnections between adjacent sympodia that a parenchymatic gap is circumscribed above the point of departure of the leaf trace. Such parenchymatic regions appear even more gaplike in those shoots that form secondary vascular tissues from cambial activity. Nevertheless, it is clear from the review of Beck, Schmid, and Rothwell (1982) that the basic configuration of the primary vascular systems of microphyllous and megaphyllous plants do not differ fundamentally from one another, hence the supposed presence or absence of leaf gaps is not a basic distinction between these leaf types.
Even present views of the phylogeny of microphylls and megaphylls are conflicted. While most contemporary texts in morphology and paleobotany accept the difference in derivation (Fig. 6A–D, F–I), Zimmermann (1930)
proposed that microphylls were derived from megaphylls by a process of evolutionary reduction rather than by two different phylogenetic origins (enation vs. cladification). Since he was the author of the telome theory, it would be expected that Zimmermann would see the megaphyll as the fundamental leaf type. However, given the lack of a valid distinction between these leaf types, if any phylogenetic interpretation has any validity, Zimmermann's derivation of microphyllous from megaphyllous leaves would seem more credible than their derivation from enations.
The problem with both the enation and the telome theories is that they are gap-filling theories, or hypotheses. There is gap between levels of plant organization, that of the leafless rhyniophyte like plant body and that of leafy shoots. Both the enation and telome theories attempt to bridge this gap by inventing a set of intermediates between these two character states (Fig. 6B, C and Fig. 6G, H). The problem is that the fossil plants discovered after this theoretical derivation are then slotted into the theory rather than being used to test and challenge it. Because these two theories have a phylogenetic slant, in contrast to the typologies of idealistic morphology, they have been taken more seriously than Troll's models because they have been viewed as having been based in a more concrete reality (Zimmermann, 1931, 1953). In fact, Zimmermann's theory is as hypothetical and as much a case of idealistic morphology as Troll's typologies based on contemporary plants. It is just that Zimmermann pushed his type back earlier in time and based it on the morphology of a particular, seemingly concrete fossil form. Given their fundamental similarities, it is ironic that Troll and Zimmermann should have become such arch antagonists.
Finally, Wardlaw (1957)
demonstrated that so-called "microphyllous" leaves in pteridophytes are initiated in the same phyllotactic patterns as shoots of their megaphyllous counterparts and that the details of their initiation from their shoot apical meristems are indistinguishable from those of megaphyllous leaves in ferns and seed plants. Thus, there is little legitimate basis for distinguishing microphylls from megaphylls among any contemporary plants in terms of their position or developmental pattern.
Regardless of the phylogenetic theories that have been in vogue, when members of so-called microphyllous and megaphyllous contemporary vascular plants groups are compared morphologically, they are nearly impossible to distinguish morphologically. They are simply "leaves," whether they represent evolutionary homologies or analogies between their respective groups. Because both microphylls and megaphylls are inseparable components of their shoots, the evolution of leaf morphology must be evaluated in the context of the shoot as a whole and not as isolated organ types. Because the phylogenetic basis for their recognition is so tenuous and theoretical, I think it is best that this distinction between leaf types in vascular plants be abandoned until we have more convincing evidence of a true distinction between them.
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A REEVALUATION OF SHOOT MORPHOLOGY IN THE PTERIDOPHYTES |
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TOPABSTRACTINTRODUCTIONTHE SCIENCE OF PLANT...HISTORICAL HERITAGE OF PLANT...THE PROBLEMATICAL STATUS OF...A REEVALUATION OF LEAF...A REEVALUATION OF SHOOT...GENERAL CONCLUSIONSLITERATURE CITED |
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Principle I: Relationship of leaf to stem
The shoots of higher plants are typically characterized as being differentiated into nodes and internodes. The nodes, by definition, are the sites of leaf insertion, whereas the internodes are considered to be the stem units that typically elongate between the points of leaf insertion. The model for such a clear delineation between node and internode is illustrated in Fig. 7A. However, a more accurate model of leaf–stem relationships is illustrated in Fig. 7B. Here, leaf insertion is not localized at the node. Each internode is not just stem, but a compound structure consisting of decurrent leaf bases, that run along the length of the internode below it (Fig. 7B). These decurrent leaf bases corticate the shoot axis, and the photosynthetic tissue one sees at the periphery of a stem transection is actually leaf tissue that is adnate with the shoot axis.
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) seems even more insightful.
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Leaf insertions extend along the length of an internode because the leaves are initiated from the periphery of the shoot apex before there is any significant extension of the internodes. Since the incipient internode is such a short region (only a couple of cell diameters high), a part of the leaf base is inevitably included with shoot elongation (shaded areas in Fig. 7F, G). Thus the shoot axis, represented in its purest form by the central pith region, is always corticated by surrounding leaf tissues (Fig. 7G).
In passing, it should be noted that these deductions on leaf–stem relationship can only be observed in the region of the shoot where the primary body is retained unchanged. If secondary growth occurs, then the contribution of leaves to the transection of the shoot axis will either be obscured or lost. This is not a problem with the contemporary pteridophytes we characterize below because none of them exhibit any secondary growth.
Principle II: Rhythms of primary thickening growth ("Erstarkungswachstum")
A second principle in the growth of the shoots of seed plants is an ontogenetic rhythm in shoot primary thickening that has been termed "Erstarkungswachstum" or "strengthening growth" by the Germans (Troll and Rauh, 1950
). The German word "Erstarkungswachstum" actually refers both to the ontogenetic increase in stem diameter and to the decrease in the distal, flowering region of a shoot, especially in herbaceous annual plants (Fig. 9A) (Troll and Rauh, 1950
). In this regard, Tomlinson and Zimmermann's (1966)
use of the term "establishment growth" for "Erstarkungswachstum" seems even less appropriate because of the functional, adaptational connotations of the term "establishment." In fact, the obconical shape of young shoot regions, by itself, is not a mechanically sound construction. Without an augmentation of mechanical support, either in the form of shoot-borne prop roots or secondary growth, such an inverted cone axis would not be stable. Thus, it is more accurate to use a neutral, purely descriptive term, such as "Erstarkungswachstum" or primary thickening rhythm for this aspect of shoot development.
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have shown that such an ontogenetic cycle in primary thickening is characteristic of ferns and all seed plants, whether they undergo secondary thickening or not. The obconic shape of the base of the shoot axis is most evident in the shoots of pteridophytes and monocotyledonous angiosperms because they lack the secondary growth that masks this inverted cone form at the base of shoots of gymnosperms and dicotyledons. However, Troll and Rauh (1950)
have illustrated the occurrence of obconic young axes in aquatic dicotyledons such as Oenanthe aquatica and Sium latifolium (Apiaceae) because they also show so little secondary xylem formation (Fig. 9A–D). Even in dicotyledons, such as Helianthus annuus (Asteraceae), which has a substantial amount of secondary xylem at the base of its shoot, the obconical shape of its primary axis is preserved in the shape of its pith (Troll and Rauh, 1950
) (Fig. 9G, H).
While the obconic axis shape is characteristic of the earliest phases of shoot ontogeny, sooner or later this primary thickening impulse reaches a maximum and is followed by a decrease in axis diameter, usually coinciding with the onset of the reproductive phase (Fig. 9A). Correlated with these changes in axis diameter are corresponding increases and decreases in the maximal diameter of the shoot apex (Troll and Rauh, 1950
). Although it has been traditional to interpret the changes in the diameter of the shoot apex as the cause of changes in dimensions of the subjacent axis (Steeves and Sussex, 1989
), it is virtually impossible to distinguish cause and effect between the shoot apex and axis in the intact plant. For these reasons, their relationship is best left as a correlation.
Other characteristics that also change in correlation with the primary thickening rhythm are leaf and lateral bud size and complexity. For example, in the leaf series in Sium latifolium shown in Fig. 9E, the primary leaves that follow the simple spatulate cotyledons (Fig. 9EI) have palmately dissected and ternate blades and are inserted at the narrowest shoot nodes (Fig. 9EII,III). As shoot axis diameter increases, leaves inserted at the wider nodes become correspondingly longer, with a greater number of pinnae in their blade sectors (Fig. 9B, EIV), reaching their maximum length and pinna number in the widest part of the shoot (Fig. 9EV). Conversely, as the axis becomes narrower in the distal, reproductive region, the structure of the leaves, expressed as floral bracts, become reduced and simpler, but not necessarily in a way identical to the simplified primary leaves in the juvenile region of the shoot (see Figs. 11, 12).
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) have demonstrated such a correlation between lateral bud size and stem diameter in the rhizomatous shoots of Acorus calamus (Acoraceae). I showed that all the buds, regardless of size, contain the same number of leaves and leaf primordia (about ten). The differences in bud size reflect differences in sizes of the axillary meristems and their leaf products. Thus, the entire shoot system shows an integration of all of its components in this thickening process.
If a given species initiates roots from its shoot axis, the number of roots initiated will also show a correlation with this primary thickening rhythm; shoots with narrow diameter axes will have a smaller circumference and will form fewer roots per node than those with a larger stem diameter (Troll and Rauh, 1950
) (Fig. 9F and C, respectively).
Collectively, all of these changes in shoot morphology, including the "Erstarkungswachstum" of the axis, are an expression of the heteroblastic development of the shoot as a whole (Allsopp, 1967
). Heteroblastic development usually has been described in terms of differences in leaf morphology because it is the most obvious expression of change in shoot form. But the evidence of a spectrum of integrated events (leaf and axis development as well as differences in bud and root development) underscore that this heteroblastic change is a whole-organism phenomenon and not restricted to an individual organ component of the shoot (Troll and Rauh, 1950
; Allsopp, 1967
).
Principle III: Developmental segmentation of leaf primordia and their relationship to heteroblastic changes in mature leaf morphology
Eichler (1861)
recognized that the earliest differentiation of a leaf primordium after its initiation from the shoot apex is into a broader, axis-encircling proximal region that he called the lower leaf zone ("Unterblatt") and a distal, typically narrower and freely projecting region that he called the upper leaf zone ("Oberblatt") (Fig. 10C, D). Typically, the upper leaf zone differentiates into the lamina and petiole regions of the leaf (Fig. 10D, E, and A respectively), whereas the lower leaf zone differentiates into the leaf base and its appendages (the stipules), if these are developed (Fig. 10D, E, A, and B respectively). The extent to which the upper and lower leaf zones are differentiated from each other may vary between species. Where upper and lower leaf zones are clearly distinguishable, one can see in the heteroblastic leaf series a developmental articulation between these two different leaf zones where successive leaves show differing degrees of upper and lower leaf development.
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Psilopsida
Because of the seemingly simple, inconspicuous nature of its leaves, the isotomous nature of its aerial shoot branching and lack of roots, and its isomorphic alternation of generations, Psilotum has been seen by many paleobotanists and plant morphologists as a living "rhyniophyte" (Rouffa, 1971, 1978
; Stewart and Rothwell, 1993
). Certainly, at a superficial level Psilotum would seem to simulate those ancient fossil plants (Fig. 13A). However, a more critical analysis of its morphology and shoot organization reveals that despite its seeming simplicity, Psilotum exhibits the same level of organization as that of seed plants. Had the more elaborated morphology of its related genus Tmesipteris been studied thoroughly before that of Psilotum, the latter would have been more accurately interpreted because Tmesipteris would have provided the appropriate context. Because species of Tmesipteris are more exotic than those of Psilotum, and because many investigators saw Psilotum as a rhyniophyte, Psilotum has been the focus, rather than its more elaborated relative. However, the critical and comprehensive studies of Albrecht Siegert on Psilotum (Siegert, 1964, 1965, 1967, 1969, 1970, 1973
) provide fundamental information on the morphology and development of Psilotum nudum that decisively refutes this rhyniophyte bias.
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) (Fig. 13A). The typically subterranean cryptophilic axes are devoid of leaves, but bear rhizoids, whereas the photophilic shoots bear reduced, scale-type leaves (Fig. 13A). The cryptophilic zone also differs in the irregularity of its branching, as contrasted with the regular, cruciate dichotomy in the distal region of the photophilic zone (Fig. 13A). Siegert (1964)
has noted that sporophylls in Psilotum tend to be restricted to the ultimate branches of the photophilic shoot (Fig. 13A). However, he has also shown examples where sporophylls occur distal to the final branching point.
In contrast with the leafless cryptophilic zone, P. nudum's photophilic shoots bear leaves along their length, even though they may be inconspicuous (Fig. 13A, B). Figure 14 (A, B) shows the details of the simple scale leaves borne at the base of the photophilic shoot (Fig. 14A) and a sporophyll from the distal, fertile region (Fig. 14B). The sterile leaf typically is awl-shaped and trough-like at its point of insertion (Fig. 14A). By contrast, the fertile leaf has two lobes, each of which resembles the reduced blade of the sterile leaf, but bearing a trisporangiate synangium on its adaxial surface (Fig. 14B). Like the shoots of seed plants, both sterile and fertile appendages have decurrent leaf bases along the length of the shoot axis below the point of blade insertion (Figs. 13B, 14A, B). Using Eichler's (1861)
terminology, the freely projecting region of a sterile leaf would correspond to its upper leaf zone, whereas the decurrent ridge would correspond to its lower leaf zone.
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has shown that the shoots of P. nudum exhibit a distinct primary thickening rhythm or "Erstarkungswachstum," which we have described for the shoots of seed plants. Furthermore, correlated with this cycle of axis thickening are changes in size and degrees of elaboration of the appendages borne on those shoot regions. The region of maximal thickening typically occurs in the transition between the cryptophilic and photophilic zones at the site where the stem undergoes its change from a plagiotropic to orthotropic growth (Fig. 13A). From that point to the distal extremity of the photophilic zone, the diameter of the shoot typically declines (Fig. 13A, B). This distal narrowing of the shoot axis is expressed in the changes in phyllotaxis along its length. For example, the basal region of the photophilic shoot will bear six to nine ribs or phyllotactic orthostichies (Fig. 14A). As these axes narrow distally, the phyllotactic fraction becomes reduced to the one third or tristichous pattern characteristic of the fertile region of the shoot (Fig. 14B). Hence, as one proceeds distally in this primary thickening cycle, the greatest proportion of aerial shoot diameter is made up of the decurrent leaf ridges instead of the central stem region of the axis. This decrease in stem diameter is thus a consequence not only of branching, but also of the size of the leaf primordium relative to the volume of the shoot apex (Fig. 14D, F). In the maximal phase of shoot development, leaf primordium size is small relative to apical volume (Fig. 14C, D), whereas in the distal fertile region, the relationship is the opposite (Fig. 14E, F).
Normally, determination of each ultimate photophilic branch is associated with this progressive dwindling of the diameter of the shoot apex. However, quite often the shoot tip will proliferate, producing an axis that is markedly thickened compared with the region that preceded it. For example, the specimen shown in Fig. 13C exhibits a shoot segment with the typical reduction of axis diameter associated with the end of the fertile region of a photophilic branch. However, instead of terminating growth, its meristem has reverted to vegetative development, forming scale leaves in a distichous rather than the tristichous pattern that preceded it. More significantly, however, this proliferated shoot segment shows a progressive increase in axis diameter, regaining the maximum diameter characteristic of the more proximal fertile shoot regions (Fig. 13C).
Siegert (1964, 1969, 1970, 1973)
has shown that such reversions to vegetative growth, but without the aforementioned marked change in phyllotaxis and symmetry of the example in Fig. 13C, is quite common in photophilic shoots of P. nudum. In these instances, there can be two to three tiers of fertile shoot segments, separated by one or more unitipped sterile appendages that Siegert has called "onset" leaves ("Anlaufblätter") (Siegert, 1964
). Each successive tier is characterized by an increase in axis diameter, followed by its narrowing (Fig. 15). Correlated with these changes in axis diameter are corresponding changes in the size and degree of elaboration of the sporophylls borne on these shoot segments. For example, the first fertile tier exhibits the narrowest axis diameter (Fig. 15A). Following a short zone of normal sporophyll formation, there is a zone of moderate to weak development of sporophylls ending in very reduced or what Siegert terms "hypoplasious" sporophylls (Fig. 15A).
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The regular occurrence of sporophylls bearing two and even three synangia on their adaxial surface refutes previous suggestions that the synangium in Psilotum actually terminates a lateral branch and that the two lobes of the sporophyll are homologous with individual sterile leaves (e.g., Bierhorst, 1956
). In addition to evidence from these variant sporophyll morphologies, Siegert (1967)
noted that branch and leaf primordia in Psilotum are not only distinctive from inception but also occupy different positions in the shoot.
Siegert (1967)
also pointed out that adaxial insertion of synangia in Psilotaceae is even more convincingly demonstrated in Tmesipteris. The blade surfaces in both the sterile and fertile leaves in Tmesipteris differ from those of Psilotum because of their distinctive vertical planation or flattening in the median rather than the usual transverse plane (Fig. 16A, B). The bisporangiate synangium of Tmesipteris is inserted on the adaxial surface of the sporophyll, not its apex (Fig. 16B). Siegert (1967)
indicated that if each of the leaflet lobes of the sporophyll of Tmesipteris were the homologue of an individual sterile leaf, with their median flattening, they would exhibit the orientation shown in Fig. 16C. Instead, they show the orientation shown in Fig. 16D, which is the same as that of the sterile, vegetative leaf (compare Fig. 16B with A).
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An example of previous attempts to squeeze the morphology of Psilotum into a rhyniophyte model is the paper by Rouffa (1971)
on what he termed an "appendageless" variant of P. nudum. According to Rouffa, this form seemed to bear no appendages and its synangia were clustered at the tips of its branches, reminiscent of an ancient, Rhynia-type morphology.
Rouffa's deductions seem to have been made without a knowledge or understanding of Siegert's previous investigations. Critical examination of Rouffa's figures demonstrates that while superficially this form may seem appendageless, it is not leafless. All of its shoots have decurrent leaf bases of wild-type Psilotum and these leaf bases fall into the same phyllotactic pattern as wild-type P. nudum. Since these decurrent bases are developmental expressions of the lower leaf zone, it is the upper leaf zone or lamina region that is reduced. In fact in some of Rouffa's specimens, a reduced, stublike upper leaf zone is evident at the summit of each decurrent base. Because he accepted Bierhorst's (1956)
branch homology of the synangium, Rouffa (1971)
referred to these reduced laminae as "branch stubs" on the assumption that they represented variously arrested branch outgrowths. Since Siegert (1967)
convincingly demonstrated that shoot branches and leaves in Psilotum occupy different positions in its shoot system, it is clear that these "branch stubs" are not branch, but leaf homologues.
There are a host of xeromorphic species (e.g., Rhipsalis in Cactaceae) in which the upper leaf zone is reduced or even absent and only the leaf base region is expressed. Given the marked degree of phenotypic plasticity exhibited by species of Psilotum, such an "appendageless" variant is not surprising. Since its synangia are normally borne on the lamina surface, if the lamina is reduced, the synangia will not be developed on the elongated axes. The terminal region is thus the only zone where synangia are developed in this variety, comparable to the normally occurring sporophyll aggregation that Siegert (1973)
has characterized (Fig. 15D).
Thus, despite the predominance of previous interpretations suggesting Psilotum is a living rhyniophyte, critical modern studies on the organization and developmental patterns of its shoot indicate that both genera of Psilotaceae exhibit a shoot organization like that of seed plants. Not only is the leaf component an integrated element of the shoot as indicated by its decurrent leaf bases, but also its regular changes in size and complexity correlate with the cycles of primary thickening growth, as in all vascular plants (Troll and Rauh, 1950
). Regardless of what its phyletic history may have been, the organizational level of Psilotum is comparable to that of other vascular plants of a wide range of affinities. Moreover, the simplified nature of its leaves is suggestive of an evolutionary reduction rather than an enation homology.
Lycopsida
The clubmosses in the genera Huperzia, Lycopodiella, Lycopodium, Phylloglossum, Selaginella, Isoëtes, and Stylites differ from the Psilopsida in their development of roots and larger and more elaborate leaves. Like the whisk ferns (Psilopsida), Lycopsida traditionally have been viewed as being primitively microphyllous. Despite this traditional characterization, like members of Psilotaceae, they exhibit features of shoot and leaf morphology that contradict these views.
All members of the homosporous Lycopodiaceae have decurrent leaf bases just as we have described for seed plants and Psilotum. Figure 17A, for example, shows a portion of a longitudinal section of the shoot of a species of Lycopodium (most likely L. complanatum). Its decurrent leaf bases are evident and exhibit the same histology as their freely projecting blades (Fig. 17A). The transection of a so-called "internode" of L. complanatum gives a similar image; it is impossible to distinguish the cortex of this axis from the leaf base region of the appendages because they are one and the same (Fig. 17B). Given that the so-called leaf cushions that persisted on the trunks of fossil arborescent lycopods such as Lepidodendron and Sigillaria (Stewart and Rothwell, 1993
) are also decurrent leaf bases, the expression of the same characteristic in living lycopods suggests that this organizational feature may have had its origin early in lycopod evolution.
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Evidence for the validity of the delineation of upper leaf and lower leaf zones in the mature leaves of species in Isoëtaceae described above comes from the study of the youngest stages of leaf morphogenesis, when these two regions are defined. Figure 20A–D shows the developmental stages of young, whole leaves of Isoëtes andina (Kubitzki and Borchert, 1964
). At the earliest stage of development, enlargement of the lower leaf zone is more extensive than the upper leaf zone (Fig. 20A). Not only is the lower leaf zone significantly longer and wider than the upper leaf rudiment projecting from it distally, but the upper leaf is completely covered by the ligule, which is significantly longer at this stage (Fig. 20A). In its precocious rate of extension, the ligule is reminiscent of stipules in angiosperm leaves (Troll, 1937–1943
). Once the ligule has reached its final length, the upper leaf zone continues to elongate (Fig. 20B, C) and ultimately extends beyond its ligule (Fig. 20D), dwarfing it in the mature leaf (Fig. 19B).
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Histological sections of early stages of leaf development in I. lacustris and I. melanopoda further substantiate this early differentiation of these primordial leaf zones in sporophyll development. For example, Fig. 21A–D shows median longisections of successive stages of early development of the sporophylls of I. lacustris. From the earliest stage shown, the point of ligule insertion occurs below the boundary between upper and lower leaf zones (Fig. 20A). Characteristically, at this early stage, precocious elongation of the ligule has caused it to be swept back over the leaf apex, covering it almost completely (as seen in the leaf dissections, compare Fig. 21A with Fig. 20A). However, at this early stage, the upper leaf zone is already characterized by the greater thickening growth that sets it off from its leaf-base region (Fig. 21A) and that becomes more accentuated in later stages of development (Fig. 21B–D). The thickening growth of the upper leaf zone is both adaxial and abaxial, associated with radially oriented cell lineages derived from the protoderm on both sides of the leaf (Fig. 21B–D). In this marked radial growth, the young leaf stages of Isoëtes resemble unifacial leaves in the monocotyledons, which have upper leaf regions that undergo growth predominantly in volume, in contrast with the surface growth of their sheathing bases (lower leaf zones) (Kaplan, 1975
). However, the lower leaf zone of Isoëtes lacustris only undergoes thickening growth when it initiates its massive sporangium from the adaxial surface of its basal sheath (compare Fig. 21C, D with B). Once the apex of the upper leaf zone becomes attenuated, the basipetal wave of leaf maturation sets in and the meristematic activity of the leaf becomes displaced basally, in a classic case of basiplastic leaf differentiation, with the proximal sheath being the last zone of the leaf to reach its full length (Fig. 21D).
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Given that the leaves of Isoëtes and Stylites exhibit morphogenetic processes that resemble those in unifacial leaves in seed plants and also show a range of variation as a result of differential extension between upper and lower leaf zones, it is difficult to see these organs in Isoëtes as being microphyllous or enation homologues. The application of the microphyll vs. megaphyll dichotomy to the interpretation of their morphology seems inappropriate, whether they have a single vein or not. Because certain species of Isoëtes can exhibit large leaves with an equivalent degree of regional differentiation and developmental complexity, they demonstrate how such rigid, phylogenetic conceptions can be a limitation rather than an aid in assessing the evolutionary status of the morphology of these organisms.
Sphenopsida
This is another pteridophytic group whose representation in the fossil record is more extensive than among contemporary plants (Taylor and Taylor, 1993
). Today it is represented only by the genus Equisetum, comprising some 15 species worldwide (Mabberley, 1997
).
Among the diagnostic features of vegetative shoot morphology in Equisetum are its clear differentiation into nodes and internodes and its leaves, arranged in a whorled phyllotaxis and united into a common sheath. The only indication of the number of leaves comprising a vegetative whorl is the number of teeth at the summit of its leaf sheaths (Fig. 23A). Although the sporophylls in the strobilus region of a shoot are free from one another, they also occur in a whorled phyllotaxis. The shoot system consists of subterranean, plagiotropic, rhizomatous axes bearing orthotropic, aboveground aerial branches that ultimately bear the cones. Roots typically are confined to the rhizomatous portion and are initiated only from the lateral branch primordia, not from its main axes (de Janczewski, 1876–1877). Thus, its roots are not only shoot-borne but, more precisely, lateral shoot-borne.
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The organization of its shoot can be seen in the median longisection of the shoot of E. arvense in Fig. 23B. The portion of each leaf whorl that projects from the axis is the leaf sheath with its summital teeth (cf. Fig. 23B with 23A). However, below their point of insertion is a cushionlike protrusion corresponding to the decurrent leaf base. As the so-called internode elongates, this leaf base region extends with it, differentiating into the chlorenchyma, which corticates the axis (Fig. 23B). Hence, like all of the other species we have characterized in this article, what has been described as cortical tissue of the stem of Equisetum is actually leaf tissue adnate to its central axis.
From a traditional phylogenetic viewpoint, because of their simple, univeined nature (Fig. 23A), leaves in the vegetative region of the shoot of Equisetum have been considered microphyllous. However, the peltate sporophylls in the strobilus region of its shoot have been considered to be megaphyllous. Cone appendages in Equisetum traditionally have been called sporangiophores rather than sporophylls because they have been interpreted as originating from fertile telome systems, which, in the course of evolution, became recurved and reduced to form their characteristic peltate configuration (Stewart and Rothwell, 1993
). The problem with such theories is that serial appendages along the length of an individual shoot would then have two different phylogenetic origins. Such a contradiction lies either in the spurious distinction between microphylls and megaphylls or in a misunderstanding of the morphological relationships between sterile and fertile appendages in Equisetum, or both. By demonstrating the regular occurrence of intermediates between sporophylls and vegetative leaves in Equisetum, it can be shown that these contradictions in appendage morphology and evolution result from misinterpretations of appendage homology in Equisetum.
Page (1972)
has noted that within a clone of Equisetum, aerial shoots exhibit approximately the same number of nodes, regardless of whether the shoot is strictly vegetative or has both sterile and fertile (cone-bearing) regions. Appendages in both fertile and sterile regions occur in clear whorls. Since the internodes are short in the strobilus, a fertile shoot has a greater number of nodes in its cone region than in the subjacent vegetative region. Conversely, the strictly vegetative shoots are longer because their internodes are elongated, even though their node number is the same. This concept is illustrated in Fig. 24. All three shoots diagrammed have 29 nodes. In shoot A, 22 nodes are fertile and seven are vegetative (including the annulus or basal node of the cone) (Fig. 24A). In shoot B, ten nodes are fertile and 19 are sterile (Fig. 24B), whereas in shoot C, all 29 are sterile (Fig. 24C). Such equivalences in numbers along a given aerial shoot suggest a serial homology between the vegetative and reproductive appendages of an aerial shoot.
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This leaf series also shows that the first sporangia to be differentiated are the basalmost pair and that as the sporangia-forming blade region of the sporophyll is expanded laterally and distally, additional sporangia arise laterally and distally (Fig. 25J–N). The degree of distinction of the sporophyll petiole from the sporangia-bearing blade is increased by the hypopeltate (abaxial) expansion of the blade, seemingly eliminating the continuity between the blade and base that would indicate the homology of the stalk in the fully differentiated sporophyll (Fig. 25K–N).
It can be concluded that each sporophyll in Equisetum is homologous with an entire individual vegetative leaf, not just a portion of it. The sporophyll blade that bears the sporangia is comparable positionally to the distal portion of a vegetative leaf, and its petiole corresponds to the basal portion of the vegetative leaf or that part that is united into the sheath. Other than bearing sporangia, the principal divergence of the sporophyll from its trophophyll homologue is that it develops a hypopeltate (abaxial) blade extension that serves to seal the cone and protect the developing sporangia from desiccation until they are ripe and ready to release their spores.
Hence, Equisetum serves as effective a challenge to the concepts of microphyll vs. megaphyll as any of the pteridophytes we have noted. If intermediates occur between organs that have been classified into each of these categories, then the categories are no longer valid. Such examples emphasize what the study of contemporary plants can contribute to the study of organ phylogenies that may not be obtainable from fossils.
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GENERAL CONCLUSIONS |
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TOPABSTRACTINTRODUCTIONTHE SCIENCE OF PLANT...HISTORICAL HERITAGE OF PLANT...THE PROBLEMATICAL STATUS OF...A REEVALUATION OF LEAF...A REEVALUATION OF SHOOT...GENERAL CONCLUSIONSLITERATURE CITED |
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The seeming generality of this high degree of shoot organization in contemporary Pteridophytes suggests that this type of shoot organization could have had its inception much earlier in vascular plant evolution than currently thought. While our usual thinking is to hypothesize a number of steps between one character state and the next (as in the telome and enation theories; Fig. 6), the evolution from leafless rhyniophyte axes to those of a typical leafy shoot organization might have been a relatively simple, one-step organizational change, not involving a series of intermediates. As a result of biophysical/biomechanical constraints, once land plants developed certain degrees of stature and self-standing orthotropic growth, then present leaf–stem relationships and leaf elaboration could have been correlated with this basic change in habit. Such perspectives would then be in harmony with our view that evolutionary changes in plant morphology are expressed in the organism as a whole rather than in individual organs one at a time, as has been thought traditionally.
This survey of shoot morphology in pteridophytes illustrates the kind of unique perspectives that the principles of plant morphology, which cut across phylogenetic lines, bring to the understanding the major features of plant evolution. Such perspectives have the potential to complement the current emphasis on plant phylogeny and further illuminate our understanding of plant structural change.
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FOOTNOTES |
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2 Author for reprints (e-mail: kaplandr{at}nature.berkeley.edu
).
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LITERATURE CITED |
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100 µm long. (B) Leaf 
