AN INTEGRAL PART OF BOTANY1

American Journal of Botany 89(2): 369–374. 2002.

BOOK REVIEW

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INTEGRAL PART OF BOTANY1

NANCY G. DENGLER2 Department of Botany, University of Toronto, Toronto, Ontario, M5S 1A1 Canada

Plant anatomy, the study of the internal structure of plants, has been a source of fascination and a field of scientific inquiry since the time of the earliest microscopists. The subject matter of plant anatomy centers on aspects of structure that can be observed with the light microscope, specifically: (1) the spatial array of the dermal, ground, and vascular tissue systems within vegetative and reproductive organs; (2) the patterning of tissue and cell types within these three systems; and (3) the nature of individual specialized cell types. In a botanical hierarchy of levels of organization, plant anatomy sits between morphology and cell biology; however, the boundaries between them tend to be imprecise. Much of our understanding of the cell-specific properties of specialized cell types such as sieve tube or tracheary elements is based on analyses using transmission and scanning electron microscopy and other tools of cell biology. Plant anatomists also aim to place what is known about the internal structure of plants in the broader context of the plant’s external form, or morphology. Nevertheless, the science of plant anatomy focuses on plant structure at the light microscope level, with the major goals of understanding: (1) the fundamental principles of microscopic structure common to all vascular plants, (2) how internal structure facilitates or constrains physiological processes, (3) how individual taxa vary in the details of this organization, and (4) the developmental processes that yield mature anatomy. Plant anatomy, along with ‘‘whole plant’’ physiology and comparative plant morphology, has long formed the core of general botany courses. This is the subject matter at the heart of the study of plants at the organismal level, a focus that has been important since von Sachs’ Textbook of Botany (1875). In addition to its central role in the curriculum of general botany, recognition of plant anatomy’s central role in understanding how plants function was reflected in the early publication of Haberlandt’s Physiological Plant Anatomy (1914). Solereder’s treatise on comparative plant anatomy, Systematic Anatomy of the Dicotyledons (1908) appeared shortly after Haberlandt’s original German publication date. All three of these monographs were among the great achievements of early plant science, and their legacy was felt throughout the next century and into this one through subsequent translations, revisions by later workers, and assimilation into a range of other works. The most important contribution to general plant anatomy in the past century has been Esau’s Plant Anatomy (1965), a work that emphasized the developmental aspects of plant anatomy and the significance of understanding development for interpreting function. Both this work and the accompanying textbook, Anatomy of Seed Plants (1977) expanded the basic outline presented in Foster’s Practical Plant Anatomy (1949)

and continue to be widely cited today. In recent decades, only a handful of general plant anatomy books have been published, including those by Fahn (1977), Mauseth (1988), Buvat (1989), and Romberger, Hejnowics, and Hill (1993). At least 26 individual volumes (in German, French, and English) in the Encyclopedia of Plant Anatomy series have dealt with specific aspects of plant anatomy (e.g., Napp-Zinn, 1973, 1974). Additionally, the Anatomy of the Dicotyledons and Anatomy of the Monocotyledons series (e.g., Metcalfe and Chalk, 1979; Rudall, 1995) have treated the systematic anatomy of individual families. All of these have been useful as texts or references, but none have had the impact of Esau’s work on contemporary research and teaching. The dearth of current monographs on plant anatomy could be viewed as emblematic of the current state of the science. Plant anatomy can be regarded as 19th century science where the basic discoveries have all been made long ago. Worse, it can be seen as a strictly descriptive science, devoid of experimental manipulation, theoretical considerations, or the use of current and innovative techniques. Plant anatomy can also be thought to serve simply as a source of characters for classification and phylogeny reconstruction. I think that these perspectives are wrong, however. There is a continuing need to increase and refine our basic understanding of the internal structure of plants. Like any other branch of botany, plant anatomy is amenable to good experimental design, with clear hypotheses, controlled comparisons, sophisticated statistical analysis, and thoughtful interpretation. Technological advances make it possible to study old questions in new ways, but also affect the specific questions addressed. For instance, the combination of anatomical analyses with physiological measurements of hydraulic conductivity have identified features of tracheary element pits that now suggest that plants regulate flow in the xylem, rather than merely providing a system of inert pipes (Zwieniecki, Melcher, and Holbrook, 2001). Within the last decade, the tools of molecular biology and genetics have identified many genes that are required for anatomical development. For me, at least, the current interest and considerable activity in plant developmental biology is one of the strongest arguments for the need for a contemporary plant anatomy book. Although often not identified as such, the function of many developmentally important genes, as deduced from mutant phenotypes and gene expression patterns, is to regulate the spatial pattern of the tissue systems, tissue and cell pattern within tissues, and cell specialization (i.e., the core elements of a plant’s anatomy). Therefore William C. Dickison’s new plant anatomy book is a welcome new arrival. Perhaps any plant anatomy text would be, but this is a particularly attractive, well-illustrated, lucidly written one that incorporates a substantial amount of current literature. Integrative Plant Anatomy was written in

1 Integrative plant anatomy. William C. Dickison. Harcourt/Academic Press. 2000. xvii 1 533 pp., ISBN 0-12-215170-4. 2 Phone: 416-978-3536; e-mail: [email protected].

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response to the question ‘‘What is the value of plant anatomy and how does it relate to other fields of study?’’ The stated goals of the book are to: (1) provide an overview of the fundamentals of the internal organization of plants, (2) to demonstrate the relations between anatomy and other botanical disciplines (such as ecology and systematics), and (3) to describe the contributions of the science of plant anatomy to other fields such as anthropology, forensics, and the arts. Integrative Plant Anatomy is divided into three sections. The first covers the foundations of plant anatomy; the second, evolutionary, physiological, and ecological plant anatomy; and the third, economic and applied plant anatomy. Each chapter within a section opens with a discussion of general principles of the subject matter (e.g., the goals of plant systematics and the utility of anatomical characters or the nature of plant adaptations to extreme environments). Chapters then expand on the general principles using well-chosen examples and illustrations. Within each chapter, a few of the major contributors to plant anatomy of recent decades are identified, and a wealth of detail and examples enrich the basic subject matter. Dickison has a lucid writing style and creates a logical flow of material. Technical terms related to plant anatomy are clearly defined in the context of the discussion, as well as (mostly) appearing in the glossary. Each chapter closes with a clear, detailed summary of the major points. Additional resources include a comprehensive list of general anatomical references and useful web sites at the back of the book. Although it is the integration of plant anatomy with other subject areas that is emphasized, a great strength of Dickison’s book is that the relationships between botanical subdisciplines are made explicit. Too often, other authors describe an anatomical feature and then mix in information about function, ecological adaptation, or systematic distribution (often with lists of families that may not be meaningful to today’s students). Thus, the relations between plant anatomy and other botanical disciplines is often left implicit and muddied, but Dickison clarifies this connection by highlighting each of these areas explicitly. THE AUTHOR AND HIS CONTRIBUTIONS The content of Integrative Plant Anatomy reflects Dickison’s own substantial contributions to systematic and ecological plant anatomy. Since the time of his own Ph.D. dissertation at Indiana University (1966) with James Canright, Dickison has been interested in the systematics of a number of eurosid families, particularly little-known families and monotypic genera of uncertain taxonomic affinity (e.g., Dickison, 1969, 1980, 1981, 1986, 1990; Dickison, Nowicke, and Skvarla, 1982; Rury and Dickison, 1984; Dickison and Phend, 1985, Dickison et al., 1994). In these and many other papers, Dickison characterized features such as nodal anatomy, wood anatomy, leaf venation and anatomy, floral anatomy, and pollen morphology with great precision and thoroughness. While his primary goal was systematic, Dickison never lost sight of the influences that geographical distribution and plant habitat superimposed on taxonomic patterns. Dickison not only provided a model for how systematic anatomy should be done, but also provided valuable overviews of the subject area (e.g., Radford et al., 1975). His contributions to plant anatomy as a whole included organizing and editing a symposium volume on Contemporary Problems in Plant Anatomy (White and Dickison, 1984).

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The writing of Integrative Plant Anatomy took a circuitous path. Dickison initially planned to co-author and translate a volume in The Handbook of Plant Anatomy series with NappZinn, but Napp-Zinn died of a heart attack at the airport, on his way to North Carolina. This unfortunate circumstance led Dickison to resolve to write a book himself, one that gradually took shape as a plant anatomy book for a more general audience. Sadly, Dickison himself was diagnosed with cancer in 1992 and wrote the book with that knowledge and while undergoing chemotherapy in the last years of his life. Given the difficult circumstances, Integrative Plant Anatomy is a remarkable achievement. Although it may not be the book that Bill Dickison would have written in good health, it represents an original and important contribution to the literature of plant anatomy. THE FOUNDATIONS OF PLANT ANATOMY The first four chapters of Integrative Plant Anatomy provide an overview of the microscopic structure of plants. First, cellular organization is emphasized, with a straightforward account of primary and secondary wall structure, cell membranes, organelles, and vacuolar mineral deposition (Chapter 1). This chapter opens with an introduction to plant growth, meristems, and cell differentiation and also addresses developmental issues such as cell fate determinacy, cell pattern formation, and embryogenesis. Next, the origin and structure of the primary plant body, along with a description of the cells and tissues comprising the dermal, ground, and vascular tissue systems is covered (Chapter 2). Developmental topics such as apical meristems, leaf morphogenesis, and the development of vascular tissues, including the cytodifferentiation of tracheary elements, are highlighted. Chapter 3 deals with the internal organization of stems, leaves, and roots, as well as root hair patterning, formation of lateral roots, and formation of nitrogen-fixing nodules. The origin and structure of the secondary plant body, with an emphasis on the features of wood that are of value for wood identification and description, are covered in Chapter 4. There is much to praise in this relatively brief introductory section. Almost all the ‘‘essential core’’ of plant anatomy is present, although some topics that arguably should be included, such as trichome structure or secretory glands and ducts, are placed in later chapters. The material is presented clearly and in reasonable depth. In many general botany and anatomy texts, the same examples are used over and over, e.g., Ranunculus root, Syringa leaf, Cucurbita stem; refreshingly, none make an appearance here. Illustrations are derived from a wide range of sources, and many photographs are original with this work. Some of those from Dickison’s own collection and those made from the Bailey-Wetmore Wood Collection at Harvard University are truly outstanding. For instance, cross-sections of atypical secondary growth in the vines Clematis virginiana (fig. 4.5) and Macherium purpurascens (fig. 4.16) or the woody monocot Dracaena hawaiensis (fig. 4.38) are superb. (I only wish that they had been included in the handful of color plates!). Some line drawings are from classic papers such as Bailey’s (1919) report of cell division in the fusiform cambial initials of Pinus strobus, a beautiful piece of cell biology done without the advantages of today’s fluorescent probes for labeling the phragmoplast, cell plate, and daughter nuclei. Other photographs are taken from contemporary publications such as the Scheres et al. (1994) paper on the embryonic origin of

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root and shoot meristems, clearly portraying cell division patterns in Arabidopsis embryos. Another strength of this and other sections of Integrative Plant Anatomy is the inclusion of recent research work in the text and illustrations. Specific works are cited in the figure captions and listed at the end of each chapter, but not in the body of the text. Unfortunately, both of these strengths are balanced by weaknesses, and both limit the usefulness of Integrative Plant Anatomy as a textbook. First, there is often a curious lack of connection between the text and illustrations. Some subjects covered in the text are not illustrated at all (e.g., leaf blade formation and leaflet morphogenesis, Chapter 2). Although most topics are well illustrated, the editorial decision to omit figure references from the text leads to considerable frustration for the reader who has to search for the visual image to accompany a description. In a few cases, the illustrations are located far from the text description (e.g., intervessel and vessel-to-ray secondary wall pitting are described on page 183, but illustrated on pages 89 and 91). Additional frustration arises when terms used in the text and figures don’t jibe: the noncolumella cells of the root cap are called both peripheral cells (page 57) and lateral cells (fig. 2.5); the early formed secondary phloem is called both soft phloem (page 187) and soft bast (fig. 4.30); the smallest veins of grass leaves are called commissural veins (page 138) and transverse veins (fig. 3.15). Finally, reproduction of a few illustrations is poor; for example, the resolution of figures illustrating cell wall structure and the co-orientation of cortical microtubules and cellulose microfibrils (figs. 1.11, 1.12) is noticeably low. These may sound like trivial complaints, but plant anatomy is a visual subject, and primary data need to be represented graphically. No doubt poor health and budgetary contingency account for these problems, and the book was also intended for the general reader. Despite the general nature of Integrative Plant Anatomy, correction of these shortcomings would make it highly suitable as a text for short (one term or quarter) courses in plant anatomy. Although literature citations are omitted with the general reader in mind, the absence of citations further limits the usefulness of Integrative Plant Anatomy for plant anatomy and other advanced-level students. Many examples of specific research findings, controversies in the literature, and unresolved research questions are raised in the text, but readers have to hunt if they want to follow up on a specific topic. The pertinent references are present at the back of each chapter, but a naive reader would have to do a fair amount of guessing to match the content of the text to the original papers (e.g., phloem loading [Chapter 7] or ‘‘cell wall genes’’ [Chapter 9]). This problem is aggravated by the abbreviated treatment that many ideas receive. In writing a book with considerable breadth (not only the core material of plant anatomy, but also its contributions to a host of other fields), depth had to be sacrificed. One way to handle the breadth vs. depth dilemma is to provide a direct link to the primary literature, so that readers can follow up on points of interest. As the book stands now, readers have to jump a considerable hurdle to do this. EVOLUTIONARY, PHYSIOLOGICAL, AND ECOLOGICAL PLANT ANATOMY These four chapters demonstrate the contributions of plant anatomy to understanding plant evolution, physiology, and ecology. Chapter 5 opens with a discussion of the concept of

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characters in systematics and surveys the utility of anatomical characters such as vessel element size, shape, perforation type and pitting type, nodal anatomy, stomatal and trichome types, and crystalline inclusions for classification and phylogeny reconstruction. Dickison emphasizes that accurate scoring of anatomical character states requires precise character description and relies on understanding the range and source of character variation within individual plants. Although diverse characters are covered in the chapter, the contributions of wood anatomy are emphasized. Major trends in vessel element specialization are identified and well-illustrated. Important correlations among character states such as perforation type, intervessel pitting, ray heterogeneity and distribution of axial parenchyma are indicated in a series of tables. Chapter 6, ‘‘Macromorphology,’’ deals primarily with floral anatomy and its contributions in establishing homology relationships of floral appendages. Here, Dickison is also cautious in making claims for the uncritical use of vascular anatomy in the interpretation of floral morphology. With this caveat in mind, the chapter reviews some of the contributions of Eames and other floral anatomists and provides examples where floral vascular pattern has proved useful in the interpretation of pseudomonomerous gynoecia, inferior ovaries, or derivation of nectaries. The functional significance of anatomical features is addressed in Chapter 7. Because of my own research interests in Kranz anatomy, I was delighted that Dickison refers to Haberlandt’s (1914) prediction that the structural differences between the bundle sheath and mesophyll chlorenchyma cells surrounding the leaf veins in certain grasses and sedges represent a division of labor. Dickison nicely summarizes these anatomical differences and what is now known about their biochemical and physiological significance. Dickison selects other examples for which anatomical data have defined the constraints on a physical process. For instance, the frequency of secondary plasmodesmata between sieve tube element– companion cell complexes and surrounding parenchymatous cells provides an important source of primary data for determining whether loading is apoplastic or symplastic (Haritatos, Medville, and Turgeon, 2000). Chapter 8 deals with ecological plant anatomy. The chapter opens with a general discussion of plant adaptation and then focuses on anatomical adaptations that are thought to contribute to plant survival in extreme conditions of intense sun or shade, cold or heat, wetness or dryness, and soil mineral nutrient deficiencies. The fact that we simply don’t understand the functional significance of many structures is recognized, but within these limitations, the chapter provides many detailed examples of the strong correlations between structure and habitat. Many of these examples are drawn from leaf anatomy, including the absorptive trichomes of epiphytic bromeliads, the chambered air channels of many floating aquatics, and the ‘‘accordion-pleated’’ vascular bundles of the Namibian resurrection plant Chamaegigas intrepidus (Scrophulariaceae) (Schiller, Wolf, and Hartung, 1999). Other examples of strong correspondence between wood anatomy, leaf anatomy, and habitat include Dickison’s own work on the genus Hibbertia (Rury and Dickinson, 1984). Some of the case studies covered, however, would be better grouped under the heading of ‘‘phenotypic plasticity’’ (such as sun-shade leaf dimorphism and heterophyllous leaf shape in semiaquatic species). The effects on plant structure of acid rain, ozone, ionizing radiation, ultraviolet B radiation, herbicides, and insecticides are briefly

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covered, and features of plant anatomy associated with resistance (stomatal distribution, trichome frequency, etc.) to some of these pollutants are identified. ECONOMIC AND APPLIED PLANT ANATOMY These eight chapters of Integrative Plant Anatomy consider applications of plant anatomy to a wide range of fields (plant pathology, plant breeding, wood technology, etc.), as well as the importance of the identification of microscopic plant remains for forensics, archaeology, and dating of historical antiquities. This section is a wonderful source of material for teaching and is packed with stories that illustrate why knowledge of basic plant anatomy is relevant in today’s society. The section opens with a discussion of genetics and plant breeding (Chapter 9). Tree breeding programs have selected for desirable qualities such as the improved tear resistance of papers, hardness of furniture woods, and stiffness of construction lumber, properties that are all related to cell size and wall characteristics in woody tissues. This discussion builds nicely on earlier chapters on wood properties such as the discussions on the links between wood structure and function in Chapter 7 and on ecological wood anatomy in Chapter 8. However, the second part of this chapter, addressing the genetic basis of anatomical traits, seems to be an awkward fit with the first. Since it touches on some of the genes regulating, for example, initiation of the shoot apical meristem during embryogenesis, stomatal patterning, and trichome initiation, the material fits best with Section II of Integrative Plant Anatomy, the integration with other subdisciplines of basic botanical science. I felt that this placement and abbreviated treatment represented a missed opportunity to highlight some of the ‘‘big stories’’ in plant anatomy of the last decade and to emphasize issues raised earlier in the text. For instance, a number of genes required for morphogenetic and histogenetic functions of the shoot apical meristem have been identified (e.g., reviewed in Bowman and Eshed, 2000; Schoof et al., 2000). This work is at a stage where the region-specific expression patterns are known, interactions between several genes have been demonstrated through analysis of double mutants, and well-supported predictions of gene function have been made. This would have been a great opportunity to relate ‘‘classical’’ zonation patterns (as covered in Chapter 2) to those indicated by more recent work. Chapter 10 combines a discussion of the nature of plant defenses with the responses of plants to wounding and invasion by microorganisms. Some vivid examples are illustrated, such as the impalement of leafhopper nymphs on the hooked trichomes of bean leaves. Intraspecific variation in resistance to Dutch elm disease and the influence of developmental stage on determining susceptibility are discussed in detail and are useful for testing the reader’s understanding of the three-dimensional architecture of woody tissues. Important contemporary topics such as the long distance movement of viruses within the phloem are also addressed in this chapter. Chapter 11 describes the basic kinds of secretory structures—external structures such as glandular trichomes, nectaries, and hydathodes and internal structures such as laticifers, secretory cavities, and ducts—and how plants use the chemical products of many of these structures as defense against harmful insects and other herbivores. The chapter also addresses how humans have used these chemicals as condiments, medicines, fragrances, dyes, and ornaments and emphasizes the

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pharmacognosy of herb, spice, and drug plants. This is a fascinating chapter and one that provides plenty of interesting examples for teachers and students of botany. Chapter 12 relates the physical properties of plant fibers (defined as any cell that is long, durable, and has a high tensile strength) to their use in the manufacture of paper and other wood products and as forage fiber. Aspects of wood anatomy appear in 9 of 16 chapters, an organizational decision that leads to some repetition and difficulty in locating certain topics. The special features of compression and tension wood and their effects on the quality of paper and wood products seem appropriately located in this chapter, however. Chapter 13, on forensic science and animal food habits, is one of the most interesting in the book and is sure to provide valuable source material for many teachers. Dickison highlights the Lindbergh kidnapping case and the role that wood identification skills and knowledge of tree growth patterns played as expert testimony in the court case (Graham, 1997). The chapter provides a general discussion of features to look for when examining microscopic plant remains as forensic evidence, although none in as satisfying detail as the Lindbergh example! The discussion of the identification of microscopic plant remains is extended to the reconstruction of herbivore diets. A few anatomical correlates of feeding behavior also are identified, and questions such as ‘‘why do African elephants prefer the bark of Acacia albida to that of Combretum imberbe?’’ (Malan and van Wyk, 1993) are answered. Chapters 14, 15, and 16 apply a knowledge of the microscopic structure of plants, as well as the more macroscopic aspects of wood, to the identification of plant materials used by ancient and not-so-ancient peoples. The principles of dendrochronology are nicely illustrated by line drawings from Stokes and Smiley (1968). Several case studies of applications of dendrochronology are given, including its role in ‘‘solving’’ the mystery of the disappearance of the Roanoke Colony from Virginia in 1587 (Stahle et al., 1988). Chapter 15 relates the physical and mechanical properties of wood to its microscopic structure, and Chapter 16 returns to the application of plant anatomy to the identification and dating of wood used in art objects and various other artifacts. This final chapter contains some great stories for teaching, for instance: What is the relationship between the bordered pits of softwood tracheids and the sound of a Guarneri violin? How can you tell that an alledged van Eyck painting is actually a forgery? What do the relative proportions of sclerenchymatous bundle sheath and xylem elements have to do with the sound of a clarinet? CONCLUSIONS As a whole, Integrative Plant Anatomy provides a novel perspective on the microscopic structure of plants. The introductory section provides an overview of the fundamentals of plant anatomy in sufficient detail so that the book could stand alone without reference to other works. The contributions of plant anatomy to other botanical subdisciplines and the applications of plant anatomy are discussed with copious, wellillustrated examples in the second and third sections, respectively. Dickison’s approach emphasizes the integration of plant anatomy with other fields, but the major strength of the book as I see it is that the contributions and applications of plant anatomy are presented separately from the treatment of the fundamental core of knowledge of plant anatomy. The relations between the core and other aspects of botanical science

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are made explicit and given a conceptual framework by placing them in separate chapters. While Integrative Plant Anatomy meets the goals set out in the preface, it contains several weaknesses that will limit its usefulness as a textbook. These limitations undoubtedly are the result of contingency and the fact that Dickinson did not set out to write a textbook, but a treatment of how plant anatomy is applied to other subjects. Integrative Plant Anatomy represents a fine achievement, given that the final stages of writing, editing, and illustrating were accomplished while coping with ill health. A second edition could easily rectify current problems with the text, and I hope that the publishers will consider a revision in the near future. In its present version, Integrative Plant Anatomy is still a wonderful source of fascinating examples and good stories about plants and their internal structure. I would strongly recommend the book to anyone who is involved in teaching general biology, general botany, plant anatomy, or any other advanced course dealing with the organismal level of plant biology. For those of you who may not teach in these areas, but have to answer your neighbor’s and nonbotanical colleague’s questions about ‘‘what is the value of botany?,’’ this book is full of anecdotes about applications of basic botanical knowledge. While not functioning perfectly as a textbook, Integrative Plant Anatomy still represents a major contribution to the science of plant anatomy. Dickison’s unique approach drives home the point that knowledge of the microscopic structure of plants is fundamental to understanding how plants grow and function as organisms; it is, indeed, an integral part of organismal botany. LITERATURE CITED BAILEY, I. W. 1919. Phenomena of cell division in the cambium of arborescent gymnosperms and their cytological significance. Proceedings of the National Academy of Sciences (USA) 5: 283–285. BOWMAN, J. L., AND Y. ESHED. 2000. Formation and maintenance of the shoot apical meristem. Trends in Plant Science 5: 110–115. BUVAT, R. 1989. Ontogeny, cell differentiation and structure of vascular plants. Springer-Verlag, Berlin, Germany. DICKISON, W. C. 1967. Comparative morphological studies of the Dilleniaceae. I. Wood anatomy. Journal of the Arnold Arboretum 48: 1–29. DICKINSON, W. C. 1980. Diverse nodal anatomy of the Cunoniaceae. American Journal of Botany 67: 975–981. DICKINSON, W. C. 1981. Contributions to the morphology and anatomy of Strasburgeria and a discussion of the taxonomic position of the Strasburgeriaceae. Brittonia 33: 564–580. DICKINSON, W. C. 1986. Wood anatomy and affinities of the Alseuosmiaceae. Systematic Botany 11: 214–221. DICKINSON, W. C. 1990. The morphology and relationships of Medusagyne (Medusagynaceae). Plant Systematics and Evolution 171: 27–56. DICKINSON, W. C., M. S. HILS, T. W. LUCANSKY, AND W. L. STERN. 1994. Comparative anatomy of systematics of woody Saxifragaceae Endl. Botanical Journal of the Linnean Society 114: 167–182. DICKINSON, W. C., J. W. NOWICKE, AND J. J. SKVARLA. 1982. Pollen morphology of the Dilleniaceae and Actinidiaceae. American Journal Botany 69: 1055–1073.

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DICKINSON, W. C. AND K. D. PHEND. 1985. Wood anatomy of the Styracaceae: evolutionary and ecological considerations. IAWA Journal 6: 3–22. ESAU, K. 1965. Plant anatomy, 2nd ed. John Wiley & Sons, New York, New York, USA. ESAU, K. 1977. Anatomy of seed plants, 2nd ed. John Wiley & Sons, New York, New York, USA. FAHN, A. 1990. Plant anatomy, 4th ed. Pergamon Press, New York, New York, USA. FOSTER, A. S. 1949. Practical plant anatomy, 2nd ed. Van Nostrand, New York, New York, USA. GRAHAM, A. 1997. Anatomy of the Lindbergh kidnapping. Journal of Forensic Science 42: 368–377. HABERLANDT, G. 1914. Physiological plant anatomy. (English translation, M. Drummond).Macmillan, New York, New York, USA. HARITATOS, E., R. MEDVILLE, AND R. TURGEON. 2000. Minor vein structure and sugar transport in Arabidopsis thaliana. Planta 211: 105–111. MALAN, J. W., AND A. E. VAN WYK. 1993. Bark structure and preferential bark utilization by the African elephant. IAWA Journal 14: 173–185. MAUSETH, J. D. 1988. Plant anatomy. Benjamin/Cummings, Menlo Park, California, USA. METCALFE, C. R., AND L. CHALK. 1979. Anatomy of the dicotyledons. Clarendon Press, Oxford, UK. NAPP-ZINN, K. 1973. Anatomie des Blattes. II. Blattanatomie der Angiospermen. In W. Zimmerman, S. Carlquist, P. Ozenda, and H. D. Wulff [eds.], Encyclopedia of plant anatomy, 1–764, band VIII, teil 2, vol. 1. Gebruder Borntraeger, Berlin, Germany. NAPP-ZINN, K. 1974. Anatomie des Blattes. II. Blattanatomie der Angiospermen. In W. Zimmerman, S. Carlquist, P. Ozenda, and H. D. Wulff [eds.], Encyclopedia of plant anatomy, 765–1424, band VIII, teil 2, vol. 2. Gebruder Borntraeger, Berlin, Germany. RADFORD, A. E., W. C. DICKISON, J. R. MASSEY, AND C. R. BELL. 1975. Vascular plant systematics. Harper and Row, New York, New York, USA. ROMBERGER, J. A., Z. HEJNOWICS, AND J. F. HILL. 1993. Plant structure: function and development. Springer-Verlag, Berlin, Germany. RUDALL, P. 1995. Anatomy of the monocotyledons. VIII. Iridaceae. Clarendon Press, Oxford, UK. RURY, P. M., AND W. C. DICKISON. 1984. Structural correlations among wood, leaves and plant habit. In R. A. White and W. C. Dickison [eds.], Contemporary problems in plant anatomy, 495–540. Academic Press, San Diego, California, USA. SCHERES, B., H. WOLKENFELT, V. WILLEMSEN, M. TERLOUW, E. LAWSON, C. DEAN, AND P. WEISBECK. 1994. Embryonic origin of the Arabidopsis primary root and root meristem initials. Development 120: 2475–2487. SCHILLER, P., R. WOLF, AND W. HARTUNG. 1999. A scanning electron microscopical study of hydrated and desiccated submerged leaves of the aquatic resurrection plant Chamaegigas intrepidus. Flora 194: 97–102. SCHOOF, H., M. LENHARD, A. HAECKER, K. F. X. MAYER, G. J. RGENS, AND T. LAUX. 2000. The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100: 635–644. SOLEREDER, H. 1906. Systematic anatomy of the dicotyledons. Clarendon Press, Oxford, UK. STAHLE, D. W., M. K. CLEAVELAND, D. B. BLANTON, M. D. THERRELL, AND D. A. GAY. 1988. The lost colony and Jamestown droughts. Science 289: 564–567. STOKES, M. A., AND T. L. SMILEY. 1968. An introduction to tree-ring dating. University of Chicago Press, Chicago, Illinois, USA. VON SACHS, J. 1875. Textbook of botany. Clarendon Press, Oxford, UK. WHITE, R. A., AND W. C. DICKISON. 1984. Contemporary problems in plant anatomy. Academic Press, San Diego, California, USA. ZWIENIECKI, M. A., P. J. MELCHER, AND M. N. HOLBROOK. 2001. Hydrogel control of xylem hydraulic resistance in plants. Science 291: 1059–1062.