Kaplan’s Principles of

Plant Morphology
Kaplan’s Principles of
Plant Morphology
Donald R. Kaplan

Edited and Compiled by

Chelsea D. Specht
CRC Press
First edition published 2022
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Contents

Preface................................................................................................................................................................................................... vii
Acknowledgments....................................................................................................................................................................................ix
Authors.....................................................................................................................................................................................................xi

1. Introduction to the Science of Plant Morphology: Goals and Concepts...................................................................................1

2. The Cast of Characters: A Review of the Plant Kingdom and Its

Major Representatives.................................................................................................................................................................. 11

3. The Relationship between Morphology and Anatomy in Plants..............................................................................................43

4. Plant Embryogenesis: The Origin of Morphological Organization during Development.....................................................71

5. Early Plant Development: From Seed to Seedling to Established Plant............................................................................... 105

6. Divergent Patterns of Seedling Development and Their Significance for the Interpretation
of Plant Ontogeny and Evolution............................................................................................................................................... 133

7. Phyllotaxis.................................................................................................................................................................................... 159

8. The Concept of Differential Growth......................................................................................................................................... 183

9. The Effect of Internodal Elongation on Shoot Form............................................................................................................... 191

10. The Effect of Stem Thickening Growth on Shoot Form.......................................................................................................... 213

11. Shoot Lateral Symmetry............................................................................................................................................................243

12. Shoot Branching..........................................................................................................................................................................279

13. Developmental Expressions and Specializations of Shoot Branches.....................................................................................309

14. Leaf Morphology and Development.......................................................................................................................................... 335

15. Transectional Symmetry of Leaves...........................................................................................................................................367

16. Longitudinal Symmetry and Zonation of Leaves Part I: Leaf Zones...................................................................................387

17. Longitudinal Symmetry and Zonation of Leaves Part II: Blade Dissection......................................................................... 433

18. Specializations in Leaf Structure and Function......................................................................................................................503

19. Morphology of Reproductive Shoots I: Pteridophytes............................................................................................................585

20. Morphology of Reproductive Shoots II: Gymnosperms.........................................................................................................777

21. Morphology of Reproductive Shoots III: The Angiosperms

A. The Floral Shoot................................................................................................................................................................... 1067

v
vi Contents

22. Morphology of Reproductive Shoots III: The Angiosperms

B. The Floral Organs in Their Pre- and Post-Fertilization States....................................................................................... 1109

23. Morphology of Reproductive Shoots III: The Angiosperms

C. Inflorescence Morphology................................................................................................................................................... 1167

24. Principles of Root Morphology................................................................................................................................................ 1215

References.......................................................................................................................................................................................... 1253
Index................................................................................................................................................................................................... 1281
Preface

Kaplan’s Principles of Plant Morphology defines the field of plant morphology are being brought into studies of crop develop-
plant morphology, providing resources, examples, and theoretical ment, biodiversity, and adaptive responses to climate change, and
constructs that illuminate the foundations of plant morphology increasingly researchers are turning to historic texts to uncover
and clearly outline the importance of integrating a fundamen- research, data, and interpretations concerning plant morphology
tal understanding of plant morphology into modern research and the evolution and diversification of plant form and function;
in plant genetics, development, and physiology. As research on there is great need for a modern reference and textbook that high-
developmental genetics and plant evolution emerges, an under- lights past studies and provides the synthesis of data necessary
standing of plant morphology is essential to interpret develop- to drive our future research in plant morphological and develop-
mental, anatomical, and morphological data. The principles of mental evolution.

vii
Acknowledgments

While I can here recognize the many people who have made book a much more refined product while staying true to Don’s
the final stages of publication of this book possible, this does vision and voice, and I thank all the reviewers who contributed
not fully acknowledge those who supported and influenced Don their time and energy to this project. Among these, I especially
Kaplan during the writing of these chapters. I do know that Don thank Jim Seago for advice, critical feedback, and encourage-
would have thanked his students; all of them. Especially the ment; and Dennis Wm. Stevenson for providing substantial
students who sat in his classroom and experienced his lectures amounts of time, effort, and knowledge of all things plant mor-
delivered with lantern slides and/or slide carousels that were phology. In addition, Dennis was essential in helping me track
occasionally (and famously) dropped and scattered right before down figures, references, and citations, especially the most eso-
class began, for these students were the inspiration for this book. teric ones.
The text and extensive figures of this book served as the pri- The editing, revision, and publication of this book would
mary reading material for C107, Kaplan’s Principles of Plant not have been possible without the herculean efforts of Charles
Morphology at UC Berkeley, typically printed out in five vol- R. Crumly: Chuck’s enthusiasm for this project as well as his
umes from Odin Readers. I believe Don would have thanked the patience, persistence, ingenuity, flexibility, and expertise were all
staff at Odin for printing out copies, year after year, with annual tested time and time again, and each time he rose over barriers to
additions and modifications that were always geared toward build the momentum necessary to drive this project to comple-
making the text more instructive and valuable for his students. tion. This book is in your hands today because of his unwaver-
Don also would have thanked his graduate students and col- ing faith in and commitment to the final product. In addition,
leagues who are cited throughout the text for providing exam- Dorothy Kaplan provided resources, encouragement, and posi-
ples and exemplars of morphological patterns and processes so tive reinforcement every step of the way: And while this publica-
critical to his interpretations of fundamental principles. I also tion has taken much longer than planned, she’s never given up
know he would have thanked his wife, Dorothy, for her unwav- hope that her grandchildren will get to experience their grandfa-
ering support and his two sons, Andrew and Tim, for enriching ther’s work. I thank Chuck and Dorothy for everything they’ve
his life within and beyond academia. Don’s family has contin- done to keep this production on track, for trusting me with their
ued to foster his legacy between the time of his passing and the visions for this book, and for making me feel like part of their
publication of this book, supporting the establishment of the families in the process.
Donald R. Kaplan Memorial Lecture in Plant Morphology and Finally, I thank Ioana Anghel and Maria Pinilla Vargas who
fully endowing the Kaplan Dissertation Award in Comparative both helped extensively with references, figure captions, and edit-
Morphology, a major source of funding for independent gradu- ing; and I thank the entire production team at Taylor & Francis,
ate student research administered through the Botanical Society especially Becky Hainz-Baxter and Elizabeth King, who worked
of America. tirelessly in processing words, figures, legends, and references
For my part, I sincerely thank Raymund Chan and Michael and were always patient yet exacting in assisting me in complet-
L. Christianson who, as students and colleagues of Don Kaplan, ing this project.
provided inspiration and moral support early on to continue this This book is dedicated to the memory of Donald R. Kaplan,
project and honor Don’s legacy. They as well as the other schol- and to his sons and grandchildren who know and understand the
ars who reviewed and commented on various chapters made this weight of his work.

ix
Authors

Donald Robert Kaplan, PhD, w  as born in Chicago on January In addition to botany, Dr. Kaplan had many other interests,
17, 1938. He attended Northwestern University and graduated which he pursued with as much intensity and innovation as he
Phi Beta Kappa with a bachelor’s degree in biology in 1960. He did plant morphology. Among them were photography, railroads,
studied with Adriance Foster at UC Berkeley where he earned his classical music, and movies. He shared these passions with his
PhD in 1965. After completing a National Science Foundation- wife, Dorothy, and sons Andrew and Timothy.
sponsored postdoctoral fellowship at the Royal Botanic Gardens,
Kew, England, Dr. Kaplan became a founding member of the Chelsea Dvorak Specht, PhD,  was born in Wilmington,
newly established University of California, Irvine campus as an Delaware on September 13, 1971. She attended the University
assistant professor of organismic biology in 1965. He returned to of Delaware earning a BA. in biology magna cum laude and
UC Berkeley in 1968 as an associate professor in the Department Phi Beta Kappa in 1993. Initially planning on pursuing medi-
of Botany. Dr. Kaplan was promoted to professor in 1978, and cine, her undergraduate mentor Kenneth A. Campbell provided
moved to the Department of Plant and Microbial Biology during her first taste in academic research, changing her life forever.
reorganization of the biological sciences. He retired in 2004. Dr. Specht earned her MS in 1997 and PhD in 2004 from New
As a plant morphologist, Dr. Kaplan had a unique, European York University, during which time she was a Fulbright Fellow
perspective on plant form. Using key concepts and first princi- and worked for 2 years as a Program Officer and Ecoregional
ples, he approached his research in a strictly analytical way. He Coordinator for the World Wildlife Fund in Bolivia. Dr. Specht
was most interested in fundamental structural and developmental was part of an NSF-funded joint program between NYU and the
commonalities that underpin plant form across different major New York Botanical Garden and studied extensively with plant
taxa. Dr. Kaplan’s publications spanned the algae, bryophytes, morphologist and renowned botanist and cladist Dennis Wm.
ferns, gymnosperms, and angiosperms. Dr. Kaplan’s research Stevenson as her major advisor.
and theories on the relationship of cell and organism in vascular It was during her graduate training that Dr. Specht developed
plants have had a major impact on studies linking plant morphol- an appreciation for the principles of plant morphology combined
ogy with molecular biology/genetics, setting the stage for modern with a developmental genetic and phylogenetic perspective to
investigations on plant form and function. Dr. Kaplan was also investigate the mechanisms underlying the evolution and diver-
interested in the history of plant morphology, especially in those sification of plant form and function. Following a postdoctoral
who established the basic principles and concepts of the field as fellowship at the Smithsonian Institution’s National Museum
he practiced it, e.g. Goethe, Hofmeister, Goebel, and Troll. of Natural History, Dr. Specht became an Assistant Professor
Dr. Kaplan’s research accomplishments were well recognized and Plant Organismal Biologist in the Department of Plant and
by his peers and resulted in many awards. Among these were Microbial Biology at UC Berkeley and curator of Monocots for
the Alexander von Humboldt Distinguished Senior U.S. Scientist the University and Jepson Herbaria in 2005. At UC Berkeley
Award (1988-89), a Guggenheim Fellowship (1987–88), fellow of she taught Kaplan’s Plant Morphology course and used this
the California Academy of Sciences (1982), the Botanical Society book for many years in the form of five massive readers for the
Merit Award (1984), the Botanical Society of America’s Jeanette class. In 2017, she moved to Cornell University as the Barbara
Siron Pelton Award (1989) and Centennial Award (2006), and McClintock Professor in Plant Biology and is currently also
a Miller Research Professorship (1975–76). He was also recog- Associate Dean for Diversity and Inclusion for the College of
nized for his excellence in teaching with a Sigma Xi National Agriculture and Life Sciences. Dr. Specht is married to ento-
Lecturer Award (1995–97), the UC Berkeley Distinguished mologist Patrick O’Grady and shares her love of plants with their
Teaching Award (1976) and the Botanical Society of America’s daughter, Paceyn Julia.
Charles Edwin Bessey Award for excellence in botanical teach-
ing (2005).

xi
1
Introduction to the Science of Plant Morphology:
Goals and Concepts

CONTENTS
Examples of Higher Plant Structural Diversity and Life Forms...............................................................................................................1
Basic Organization of the Higher Plant Body...........................................................................................................................................4
The Shoot System................................................................................................................................................................................4
The Root System..................................................................................................................................................................................5
The Concept of Homology........................................................................................................................................................................5
Homology Criteria...............................................................................................................................................................................6
The Concepts of Analogy versus Homology.....................................................................................................................................10

Have you ever wondered as you stroll through a forest how the the range of their morphological expression. Once you have
many varieties of plants are related to one another? How does a acquired the ability to analyze plant morphology, we will apply
herb differ from a tree or what gives a vine its distinctive climb- these principles to plants that grow in particular kinds of habitats
ing characteristics? Are they radically different kinds of plants to see how form relates to function.
or do they share some common features? Questions such as these Before we delve into the specifics of how plants are con-
are addressed by the science of plant morphology. structed, let’s look at some biologically interesting examples of
The science of plant morphology deals with the external form the kinds of plants we are going to learn to analyze. While at first
of plants. The word morphology comes from the Greek words glance these species may seem simply weird and unrelated to
morphos meaning shape and logos meaning discourse. Since your experience, by the time we come to consider them as indi-
plant morphology is concerned principally with the structure and vidual vegetation types, you will see how even the most extreme
variation of the major plant organs (leaf, stem, and root), another representatives are related structurally to more conventional
term for its study is organography. In terms of the equivalent plant species that you are familiar with.
level of study of animals, plant morphology is comparable to
animal anatomy, whereas plant anatomy, which is concerned
with the cell to tissue levels of organization, is equivalent to ani-
mal histology. In this book our emphasis will be on the mac- Examples of Higher Plant Structural
roscopic aspects of plant structure, or what we can see largely
Diversity and Life Forms
with the unaided eye. We will make occasional excursions into
the microscopic structure of plants, but only to analyze the ori- Among the most distinctive plant types are epiphytes, plants that
gin and development of organs and organ components and where grow on the surfaces of other plants (the term epiphyte comes from
histology can tell us something about the status and function of Greek root words epi meaning upon and phyte meaning plant).
a particular organ type. True epiphytes spend their entire lives up away from the earth’s
All vascular plants (also known as tracheophytes) appear to be surface typically on one of the aerial branches of a forest tree or
built on the same fundamental organizational theme or ground on the surfaces of some other elevated plant. In Figure 1.1, we see
plan. Thus the vast majority of structural variants that we find two epiphytic species which are members of the pineapple fam-
occupying the many different habitats on earth today are simply ily, Bromeliaceae. Interestingly, taxonomically, they are both in
variations on this basic theme. A fundamental goal of the sci- the genus Tillandsia L. Tillandsia fasciculata Sw. has an upright
ence of plant morphology is to deduce this basic organizational shoot system, whereas, T. usneoides L., the well-known Spanish
theme from broad, comparative studies and to determine how moss, has a highly branched shoot system that hangs down, form-
variants come about through differences in plant growth and ing an intertwining reticulum in the air. For both these epiphytes
development. the particular environment in which they grow is a harsh one com-
The principal goals of this text are: 1) to teach the reader how pared to life on the ground below. While they may be in an advan-
to analyze the basic structural features of plants that are altered tageous position with regard to incident light in the forest, such
to produce the major variations in plant form and 2) to determine an aerial growth site is very poor in water and minerals. Plants of
the significance of these morphological variants in the environ- this type must exhibit structural and physiological specializations
ments in which the plants grow. To these ends this book will first that permit them to scavenge the maximum available nutrients
acquaint you with the science of plant morphology and the basic and water. The shoot surfaces of these two Tillandsia species are
organ components of the plant body, how they originate during covered with specialized epidermal scales that take up water and
plant development, and what parameters are varied to produce minerals from the surrounding air (Benzing, 1970).

1
2 Kaplan’s Principles of Plant Morphology

leaves which grow erectly and are heavily ribbed for reinforce-
ment (ML, Figure 1.2). The mantle-type leaves catch water and
debris from the trees above. In essence, the plant forms its own
flowerpot, and its roots grow into the accumulated soil and water
which are sources of nutrients in this otherwise nutrient-poor
environment. We will see numerous other examples of particular
plant groups that exhibit distinctly different but equally effective
morphological solutions to similar environmental problems.
It is an easy step to go from plants that live on the surfaces
of other plants (epiphytes) but do not penetrate the tissues of
their support plant and are nutritionally self-sufficient, to plants
that actually penetrate the tissues of their host and are parasitic.
Figure 1.3 shows an example of a parasitic flowering plant grow-
ing on a branch of a spruce tree, Picea spp. The parasite is the
dwarf mistletoe Arceuthobium microcarpum (Engelm) Hawksw.
& Wiens. While the aerial flowering shoots arising from the host
surface may look conventional, in reality they are only the repro-
ductive phase of this species. The vegetative or feeding phase
consists of simplified strands that permeate the body of the host
and draw water and nutrients from it. At the time of reproduc-
tive dispersal from the old host to a new one, the Arceuthobium
initiates flowering shoots from the internal absorptive system.
These flowering shoots break through the bark of the host to
produce seeds, which are essential for dispersal of the parasite
(Figure 1.3). Given Arceuthobium’s nutritional dependence on

FIGURE 1.1 Two epiphytic species of Tillandsia growing on a tree branch

in a Cypress swamp in southern Florida. Tillandsia fasciculata is the erect
growing rosette shoot and T. usneoides, “Spanish moss,” is the much-
branched, net-like species hanging below it.

Another epiphyte which exhibits quite different morphologi-

cal specializations to cope with the rigors of this environment
is the staghorn fern in the genus Platycerium (Figure 1.2).
Platycerium climbs along its support plant, using its roots for
attachment. It produces at least two different leaf types: large,
elaborate pendant fronds which are the photosynthetic and spore-
bearing organs of the shoot (FL, Figure 1.2) and mantle-type

FIGURE 1.3 The dwarf mistletoe Arceuthobium microcarpum growing as

FIGURE 1.2 The staghorn fern in the genus Platycerium grows as an epi- a parasite on a branch of a species of Spruce (Picea). The mistletoe shoots
phyte along the trunk of a tropical forest tree. This species exhibits two types seen protruding from the surface of the host are actually the flowering por-
of leaves, the large branched and pendant foliage leaves (FL) which photo- tions of the parasite and are formed from the absorptive system inside the
synthesize and bear the spores, and the mantle leaves (ML) that persist and host tissues and secondarily break out onto its surface for pollination and
impound debris as a source of nutrients for the roots of this fern to grow into. seed dispersal. (From Hawksworth and Wiens, 1972.)
Introduction to the Science of Plant Morphology 3

its host, it is not necessary to have an elaborate vegetative struc-

ture differentiated into leaf and stem because this organism is
no longer autotrophic. Such examples show us how closely plant
structure and function can be linked in species with very special-
ized life modes.
Certainly one of the most fascinating plant types are the so-
called insectivorous or carnivorous plants. The thought that
there can be such things as man (and woman)-eating plants has
stirred the imaginations of science fiction writers since time
immemorial. In reality, these plants are adapted to grow in areas
that are deficient in certain mineral elements, especially nitrogen.
Their plant bodies are specialized for the attraction, capture, and
digestion of animals (mostly insects) as sources of nitrogen and
other nutrients. An example is the shoot system of the California
pitcher plant, Darlingtonia californica. This species has a
rosette-type shoot with large, elaborately colored, tubular leaves
that serve as traps and sites of digestion of the insects that nour-
ish the plant. Despite the seemingly bizarre and unique functions
that the leaves of this carnivore perform, their leaf morphology
has been shown to be related to that of other, more conventional
plants. Once we learn how to analyze plant form and understand
the basis for its variation, such modified or functionally special-
ized organs will not seem quite so out of the ordinary.
One of the truly distinctive types of vegetation on the earth
today are the mangroves. Mangroves are trees that grow along
seacoasts and coral reefs in the tropical to subtropical latitudes.
They are salt tolerant and are able to grow on relatively unstable
substrates that can be covered by seawater during high tides.
Because of the distinctive soil environment in which mangroves
grow, it is their roots and root systems that exhibit specialization.
Figure 1.4A shows an individual tree of the black mangrove,
Avicennia germinans L. growing on the southwest coast of the
Florida peninsula. If you observe this species at low tide, you
will notice at the base of the trunk horizontally growing, cable- FIGURE 1.4 A. Black mangrove tree Avicennia germinans growing on the
like roots that spread over the sandy substrate. Growing upward south coast of Florida showing vertically growing root branches or pneu-
from these cable roots are erect, finger-like branches called pneu- matophores exposed at low tide. B. Closeup view of pneumatophores grow-
ing upward from laterally extending strand roots. P, pneumatophore.
matophores (Figure 1.4B). When the rest of the root system is
covered by saltwater at high tide, the pneumatophores protrude
above the water and aerate the submerged roots. If you were to
examine the structure of the pneumatophores microscopically
you would see that they really are roots modified to function in
this distinctive habitat.
While we tend to think of plants as self-supporting struc-
tures whose shoots grow toward the light, vines and twining
plants climb the surfaces of other plants to reach sufficient light.
In contrast to epiphytes, vining plants begin their lives on the
ground and only secondarily ascend their support plants. Many
climbing plants have specialized branches or leaves that exhibit
a particular physiological response called thigmotropism.
Thigmotropism is a growth movement induced by the con-
tact of a plant organ with some surface, usually the surface of
another plant. Plant organs that exhibit a thigmotropic response
are called tendrils. The most typical thigmotropic response of
tendrils is a coiling growth, whereby the tendril organ wraps
around whatever structure it contacts. In most vines, the tendril
FIGURE 1.5 Aerial shoots of the leguminous shrub Bauhinia vahlii exhib-
is a free structure that will strike a potential support surface or
iting watch-spring tendrils (T) developed as lateral branches in the axils of
plant as it swings through the air and respond by grabbing that leaves. In this vine, the support plant grows through the tendril and then the
structure. However, in the leguminous shrub Bauhinia vahlii tendril exhibits a thigmotropic response by coiling tightly around support
(Figure 1.5), the converse occurs: the support plant grows plant axis.
4 Kaplan’s Principles of Plant Morphology

through the already coiled Bauhinia tendril securing support for

the Bauhinia. Tendrils in Bauhinia are modified shoot branches
with tips that coil spontaneously in a single plane, like a watch
spring. If a shoot of some other plant grows through the coil of
one of these tendrils, the tendril will tighten around it. When we
study the morphology and biology of climbing plants in Chapter
24 we will explore the variety of attachment mechanisms that
vines exhibit.

Basic Organization of the Higher Plant Body

Early in this chapter we stated that the vast majority of special-
izations exhibited by higher plants represent structural varia-
tions on a basic theme or organizational ground plan. Now that
we have looked at several examples of these specializations, we
would like to characterize the ground plan that links these seem-
ingly disparate and distinctive species and indicate how we char-
acterize the major plant organs and organ systems.
Figure 1.6 is a general, idealized drawing of the major organs
of the higher plant and their structural relationships. The basic
body of the higher plant can be resolved into two major organ
systems: the shoot and the root. In many plant groups the shoot
and root components are spatially separate, and we can speak
of distinct shoot and root systems. In others there is no spatially
distinct root system and roots arise exclusively from the shoot.
One usually thinks of the shoot as the aerial component of the
plant and the roots the subterranean portion, but as we will see,
one can find plants with subterranean shoots and others with
aerial roots.
Both roots and shoots have regions of continued embryonic
activity at their tips, the apical meristems, where organ forma-
tion, or organogenesis, continues during much of the life of the
plant (Figure 1.6A). Because of the existence of these embry-
onic centers at the extremities of each plant axis, both shoots FIGURE 1.6 A. General ground plan of the body of a dicotyledon-
and roots exhibit gradients of differentiation along their lengths, ous flowering plant, showing differentiation into a proximal root system
with the most embryonic or primordial tissues and organs and a distal shoot system. B. Dicotyledonous embryo after cotyledon ini-
tiation. C. Mature embryo showing shoot pole, root pole, and hypocotyl.
located at the distal end and the most mature at the proximal end
D. Transection of a root showing tissue distribution. E. Transection of a stem
(Figure 1.6A). showing tissue distribution. B, axillary bud; C, cortex; Ca, vascular cam-
bium; Co, cotyledon; E, endodermis; In, internode; L, foliage leaf; LR, LR’,
lateral roots of successive orders; N, node; Pe pericycle; Ph, phloem; Pi, pith;
The Shoot System PR, primary root; RAM, root apical meristem; RC, root cap; SAM, shoot
The shoot system of the plant consists of two major compo- apical meristem; X, xylem. Horizontally shaded areas represent embry-
onic or growing regions. Hatched areas xylem; open phloem and/or mature
nents, leaves and stem. The leaves are the lateral appendages
tissues. (Redrawn from Troll, 1937)
and comprise its major photosynthetic surface (L, Figure 1.6A).
Typically, leaves are dorsiventrally flattened organs of deter-
minate size and shape and can be differentiated regionally into embryonic leaves with protection from desiccation by the sur-
a flattened distal blade region, a petiole or stalk, and the leaf rounding older, more mature leaves. If stem internodes of a bud
base, where they are inserted onto the shoot axis or stem (L, will eventually be extended, elongation usually takes place some
Figure 1.6A). The point of leaf insertion on the stem is called the distance below the shoot tip and results in the separation of the
node and the section of stem between two nodes the internode points of leaf insertion from one another (Figure 1.6A). In so-
(N, IN, Figure 1.6A). called rosette shoots, the internodes do not become extended
The shoot apical meristem is the site of origin of leaves and and the leaves retain the tightly congested pattern characteristic
new stem increments whose continued initiation and expansion of the terminal bud but with the leaves expanded to their full,
are responsible for the extension of the shoot in space (SAM, mature size.
Figure 1.6A). At the shoot apical meristem, the rate of leaf The position of insertion of leaves on the shoot axis is not ran-
inception exceeds that of stem elongation, hence the leaves dom but occurs in a precise geometric pattern that can be charac-
become packed together forming a terminal bud (Figure 1.6A). teristic for a given species. Such patterns of leaf arrangement are
The terminal bud configuration provides the youngest, most called the phyllotaxis (from the Greek words phyllo, meaning
Introduction to the Science of Plant Morphology 5

leaf, and taxis, meaning arrangement) and they influence the cortex before emerging to the exterior. The structure and meri-
overall appearance of the shoot of an individual plant. For exam- stem characteristics of the lateral roots are similar to those of the
ple, because the lateral branches of the shoots of most seed plants parent root.
(gymnosperms and angiosperms) are borne at the positions In the same way that there are distinctive geometric patterns
where leaves are inserted, i.e., the leaf axil (B, Figure 1.6A), the for the positioning of leaves in the shoot (the phyllotaxis), there
spatial distribution of branches will reflect the phyllotactic pat- are distinctive geometric patterns to the arrangement of lateral
tern of the shoot. Thus the phyllotaxis is a fundamental expres- roots on the parent root. One therefore can speak of rhizotaxis
sion of the symmetry and overall morphology of a shoot. (from the Greek words rhizo-, meaning root and taxis, meaning
Because leaves have a limited life span and usually abscise arrangement) and, like phyllotactic patterns, rhizotaxes can be
or fall from the shoot after they die, they leave the stem as a characterized in precise mathematical terms.
relatively naked axis and give the impression that the stem itself One of the most distinctive features of the root is the nature
is the basic component of a plant’s morphology and that the of its meristem. In contrast to that of the shoot, the root apex
leaves are only secondary as though they have been attached produces no lateral appendages from its periphery. In addition,
onto the stem as an afterthought. In fact, from a developmental- the root apex is covered by a cellular product of the meristem, the
morphological perspective, the converse is true. Leaves are the root cap (RC, Figure 1.6A). Cells of the cap are produced con-
primary structures laid down at the shoot apex. In seed plants, tinuously by the root apical meristem so that the youngest, most
at least, they dominate the growth and development of the shoot embryonic cap cells are those adjacent to the body of the root and
and significantly influence the differentiation patterns of tissues, the oldest, most mature cells are at the cap’s periphery. As cap
e.g., the vascular tissues (Esau, l965). If the internodes elongate, cells mature peripherally, they slough off and secrete mucilagi-
they do so after the leaves have been initiated and have influ- nous material. Thus the cap serves not only as a protective buffer
enced the fundamental transectional symmetry (Chapter 10) for the subjacent meristem as the root tip grows through the soil,
of the shoot. In some plants, in fact, the leaf bases extend with but also serves as a lubricant for root growth. Recent research has
the internodes so the stem really looks as though it is made shown that the root cap also is significant in regulating the geo-
up of the extended basal portion of the leaves (decurrent leaf tropic responses of roots or the direction of their growth relative
bases) rather than being an independent structure. The vagaries to the earth’s surface (Feldman, 1985).
of defining the boundaries between stem and leaf components Shoots and roots also differ from each other in the arrange-
of the shoot underscore the fundamental developmental unity of ment of their tissues. Figure 1.6D,E shows transections through
these two elements and the artificiality of attempting to draw a a representative root and stem of a higher plant. Just inside the
rigid boundary between them. peripheral band of cortical tissue of the stem is a cylinder of vas-
As we shall see when we examine in more detail the develop- cular bundles (Figure 1.6E). Of the two vascular tissue types
mental potentials and parameters of the shoot system, the indi- comprising each bundle—the xylem and phloem—the xylem is
vidual axillary buds along the length of a shoot axis can exhibit oriented toward the central pith region and the phloem toward
a range of developmental fates, producing, on the one hand, the outside of the stem or cortex, and both conducting tissues lie
branches that simply replicate the morphology of the parent axis on the same radius (Figure 1.6E). By contrast, in roots the xylem
from which they were derived, and on the other, lateral shoots and phloem are arranged on alternating radii (Figure 1.6D) and
specialized for a range of biological functions. In the shoots of there may or may not be a well-defined pith region. The presence
higher plants, it is the leaf and branch components that play spe- or absence of a pith in roots seems to depend on the diameter of
cial roles. the root’s primary body: Those roots with large diameters usu-
ally have some pith region in their centers whereas those with a
smaller diameter typically do not.
The Root System
Located at the opposite pole of the plant body, or 180 degrees
from the shoot, is the root system (Figure 1.6A). Like the
The Concept of Homology
shoot system, the root system consists of a main axis or pri-
mary root from which branches are produced laterally. Where Now that we have characterized the fundamental organization
a spatially separated root system is developed, this bipolarity of of higher plants, let’s see how it can vary in order to produce the
the plant body is forecast by the bipolarity of the plant embryo great diversity of plant form that we see on earth today.
(Figure 1.6B,C). In order to conclude that the diversity of plant morphology
Roots differ from shoots in that roots lack lateral appendages, represents variations on a basic organizational theme, we must
or the equivalents of leaves. What may look like leaf structures assume that the structural specializations observed represent
emerging from roots (Figure 1.6A) are actually branch roots modifications of the same basic organ systems. This idea is
extending in a lateral orientation from the body of the parent expressed by the concept of homology.
root. In contrast to shoot branches, which originate exogenously We will use the term homology in a strictly comparative con-
from superficial (surface) tissues, root branches arise endog- text to mean morphological correspondence to one of the major
enously from within the body of the parent root and only sec- organ categories, i.e., leaf, stem, or root. You may have heard
ondarily grow out into the substratum (Chapter 24). Typically, the term homology defined as structural correspondence due
their point of origin is from the meristematic pericycle layer at to a commonality of evolutionary descent. However, where we
the periphery of the root’s vascular cylinder (Pe, Figure 1.6A). are concerned with the principles of structural change in plants,
Hence, branch roots must burrow through the surrounding root such phylogenetic definitions of homology are far too restrictive.
6 Kaplan’s Principles of Plant Morphology

In addition, if morphological data is to be used as evidence of have lateral appendages but roots do not, if you found nodes or
phylogenetic relationships, the question of structural equiva- leaf scars along its axis and its branches were not endogenous in
lence must first be determined independent of phylogenetic sta- origin, you would predict you had a modified stem. On the other
tus. Thus, we will determine homologies on the basis of their hand, if the structure had no signs of appendages but had a cap
structural equivalence using strictly morphological criteria. over its meristem with branches that were endogenous in origin,
Evolutionary biologists often develop hypotheses to test whether then most likely it would be a modified root.
such structural correspondences are a result of evolutionary Further discrimination could be provided by analyzing tissue
convergence (either parallel or convergent evolution) and there- arrangements. Since vascular tissues in stems tend to be aligned
fore represent what Lankester (1870) has called a homoplasy or on the same radii (Figure 1.6E), whereas those in roots are on
whether they reflect a commonality of ancestry or in Lankester’s alternate radii (Figure 1.6D), it is possible to determine whether
terminology, a homogeny (Lankester, 1870). Such phylogenetic an unknown axis is a root or a shoot. This is another example of
interpretation requires integration of our morphological data the application of the special quality criterion for determining
with information from all other aspects of the plant’s biology in organ homologies.
order to reach valid conclusions concerning evolutionary rela- The third criterion, the existence of intermediates between
tionships. Thus the determination of structural relationships on two seemingly different structures, is dependent on the first two
the basis of comparative morphology should not be viewed as an criteria but can nevertheless be a useful tool in determining mor-
end in itself, but merely the first step in a long and complicated phological relationships. Since plants are metameric organisms
process of systematic evaluation. whose bodies consist of repeating subunits (e.g., leaves, nodes,
How do we actually determine the homologies of a problem- and internodes in the shoot; Figure 1.6A) and the characteris-
atic plant organ with one of the fundamental units of the plant tics of those metamers can change gradually along the length
body? In other words, what criteria do we apply to determine of the plant, one can see transitions in structure along a shoot
whether a given plant structure is a modified leaf, stem or root? axis. Where intermediates exhibited by positionally homologous
organs occur along the length of a given plant axis, the phenom-
enon is termed serial homology.
Homology Criteria An example of serial homology can be observed in young
plants of the barberry, Berberis wilsonae (Figure 1.7). After
The German morphologist-systematist Remane (l952) has sug- the first leaves or cotyledons, the shoot produces a number of
gested three criteria that can be used to decide homologies of an broadly laminate, green foliage leaves. At the more distal nodes,
organ or organ system. These are: however, the shoot produces non-photosynthetic spine-like
leaves that consist of three to five spine branches. Instead of the
1. Equivalent positions within the general ground plan or main axis bearing the photosynthetic leaf surfaces, short shoots
organization (positional criterion). borne in the axils of the spines (those with little to no internodal
2. Equivalent special quality (quality criterion). elongation) bear the laminate green leaves. The spiniferous
3. Connection of differing structures by intermediates appendages borne on the main axis do not seem at first glance to
(transitions criterion). be homologues of leaves, much less structurally related to more
conventional foliar organs. Yet if we analyze the properties of
The positional criterion is certainly one of the most fundamen- these spines, particularly their structural relationships to other
tal and a feature that influences many of the properties of the leaves of that shoot, their morphological relationships become
organs of the plant body. For example, the leaf component of more apparent.
the shoot always occupies a set position as a lateral outgrowth The spiniferous organs occupy the same position in the shoot
from the stem (Figure 1.6A). In seed plants, this position tends as the earlier-formed leaves and, like these leaves, bear shoot
to be demarcated by the location of a lateral branch or branch branches in their axils (Figure 1.8A). Hence they are position-
primordium in the axil of the leaf. Thus, if you were to observe ally homologous with leaves. Furthermore, by their spiniferous
an axis bearing leaf-like appendages along its length, you could nature it is clear that, like other leaves, they are determinate
determine whether it was (a) homologous with an individual organs. But more significantly, at the nodes between those bear-
leaf whose blade was cut into subunits or leaflets or (b) a lat- ing the basal laminate appendages and those bearing the spines
eral branch bearing its own leaves by determining the location are leaves that are intermediate in morphology between green
of axillary buds. If it were an individual leaf whose blade was and spiniferous leaves and support the homology of spines with
cut into leaflets, there would be a bud in the axil of the entire leaves (Figure 1.8A,B).
structure and no buds in the axils of the leaflets (Figure 1.6A). The intermediate leaves have blades that are cleaved into lobes
If it was a branch bearing its own leaves, it would be subtended but the lobes end in distinct spines (P, Figure 1.8B, II,III).
by a leaf or a leaf scar and each of the leaves would have buds in There is a short step from these intermediates that are spinif-
their axils (Figure 1.6B). erous but still produce a broad, green, photosynthetic surface
The special quality criterion refers to characteristics of an to leaves where each blade segment or leaflet is entirely spine-
organ which are distinctive and whose expression is not neces- like (Tr, Figure 1.8A,B, II–IV). Thus by studying transitional
sarily dependent upon the position of the structure in the plant forms that combine the characteristics of the two extremes we
body. If you were given a plant axis separated from the rest of are able to see a structural relationship, or homology, between
the plant and were asked to decide whether it was a stem or a two structures which, if considered in isolation, would seem to
root, this criterion would be useful. For example, since shoots bear little to no relation to one another.
Introduction to the Science of Plant Morphology 7

Leaflets or pinnate

Stem

Compound leaf
Axillary bud
Petiole
Leaf base

Terminal bud

Axillary buds

FIGURE 1.8 A. Seedling of Berberis wilsonae exhibiting serial (sequen-

tial) changes in leaf morphology along the length of its shoot axis. After the
cotyledons, this plant forms primary leaves that are green and broadly lami-
nate but whose lamina lobes bear spines. In the more distal portion of the
shoot, foliage leaves are strictly spiniferous and bear axillary short shoots
with broad green blades. B. Transitions in leaf morphology between broadly
laminate primary leaves (l) and spiniferous, non-photosynthetic leaves (IV)
Axillary lateral and the intermediates between them (II, III). AS, axillary short shoot; Co,
branch cotyledon; L, lamina; P, primary leaf; Pet, petiole; St, stipule; T, thorn leaf;
Tr, transition leaf. (From Troll, 1939.)

in their axils, one would be hard pressed to think of this spe-

cies as a member of the cactus family (Figure 1.9A). In Opuntia
Subtending or Axillant leaf subulata (Figure 1.9B) the blade has been reduced significantly
B compared to that of the leaves of Pereskia. Instead of having a
broad, dorsiventral blade, the lamina of Opuntia is more linear
FIGURE 1.7 Comparison and contrast between (A) a compound leaf bear- and cylindrical and has considerably less surface area when com-
ing lateral leaflets and (B) a lateral branch bearing leaves. pared with that of Pereskia (compare Figure 1.9A with B). As a
correlative development, the leaf base in O. subulata is expanded
Such transitional forms can be observed not only along the into a prominent, cushion-like outgrowth which students of cacti
length of an individual plant but also between different individ- have termed a podarium (LB, Figure 1.9B). In O. cylindrica,
uals or species of plants. For example, members of the cactus the lamina is even shorter and less conspicuous than that in
family (Cactaceae) are said to be leafless, stem-succulent plants. O. subulata (compare Figure 1.9C with B). Moreover, because
The stem is swollen as an organ of water storage and the leaf the blade of O. cylindrica abscises relatively early in ontogeny,
component so reduced that it seems absent altogether. In reality, it is evident only on the youngest leaves at the distal end of the
the leaf component is present in all members of Cactaceae as we shoot (Figure 1.9C). As the leaves mature and their blades fall
shall see when we take a closer look at members of this family off, the more mature, proximal region of the stem is left clothed
later in this book. The interesting thing about the cactus family is simply by the expanded podaria. In more derived species of cac-
that its evolutionary diversification must have occurred relatively tus, such as those placed in the genus Mammilaria, the leaf blade
quickly because all the intermediates have been preserved. For is so reduced that it is microscopic and seemingly absent in the
example, one can find cacti that bear large, laminate leaves that mature leaf. All that remains of the leaf is the base, which has a
look like those of other dicotyledonous flowering plants all the conspicuously tuberculate form (LB, Figure 1.9D).
way to cacti whose leaves are reduced and even inconspicuous. In this comparison of intermediates in leaf morphology
Four cactus species (Figure 1.9) illustrate transitions in leaf between so-called leafy and leafless cacti it can be seen that all
reduction in this family and provide some insight into how the species bear leaves and that it is only a portion of the leaf,
it has taken place. In a “leaf-bearing” cactus, Pereskia spp., the lamina, which has been reduced. It is the subjacent leaf base
(Figure 1.9A), the leaves are broadly laminate with a very short or the point of attachment of the leaf on the stem that becomes
petiole or leaf stalk. If it were not for the spine-bearing short shoot expanded as the major photosynthetic surface of the shoot. As we
8 Kaplan’s Principles of Plant Morphology

FIGURE 1.9 Members of family Cactaceae illustrating progressive stages of leaf blade reduction in selected genera and species. A. Broadly laminate
foliage leaves in Pereskia aculeata. B. Reduced, cylindrical blades in Opuntia subulata. Note that a cushion-like leaf base has developed in this species. C.
Opuntia cylindrica; only the youngest leaves bear a lamina (L) and the blade abscises later leaving only the cushion like leaf base (LB) or podarium clothing
the stem. D. Shoot of Mammillaria elephantidens showing enlarged tuberculate leaf bases and no sign of a lamina evident. (A–C from Troll, 1939; D from
Goebel, 1932.)

shall see, the comparison of intermediate morphological forms is ways of determining which units can be compared in order to
a useful approach in deducing the structural relationships in what understand the patterns and processes of plant evolution. As we
may seem to be divergent structures. make homology statements, it is important to consider that the
It should be emphasized that these homology criteria should plants themselves do not know that they are being subdivided
not be viewed as rules that are applied rigidly and dogmatically into component parts any more than you think of yourself as
to the evaluation of the diversity of plant morphology. Depending being segmented into arms, legs, and head as you go about your
on the characteristics of the plant organ in question, certain cri- daily activities. We make these subdivisions so that we can com-
teria may be more useful than others. It is always important to pare plants and see how they vary from one another, not because
keep in mind that homology is a hypothesis, and the criteria are we think the subdivisions have any independent reality.
Introduction to the Science of Plant Morphology 9

FIGURE 1.10 Illustrations of spine root morphology and positions on the shoot system of the palm Crysophila guagara. A. Young plant. B. Crown spines
emerging from the tops of leaf sheaths. C. Detail of short trunk spines. D. Detail of prop roots at base of trunk. E. Morphology of individual root types.
1. Trunk roots and apical spine conversion. 2. Large prop roots with unmodified apices. 3. Crown root morphology. (From McArthur and Steeves, 1969.)

Let’s look at one more example of a problematic plant struc- homology to roots, but also provides an example of how devel-
ture, the spine-like outgrowths along the trunk of the Central opmental stages represent the application of the third criterion
American palm Crysophila guagara (Figure 1.10A–D) and (the transitions) to the elucidation of structural relationships.
apply the three criteria to elucidate its homology. McArthur and Figure 1.11 shows the developmental stages of root spine
Steeves (1969) have shown that the spines along the trunk of this formation in C. gaugara. In its early stages the spine has the
palm originate endogenously from stem tissue just like the prop- form of a typical root apex with a well-defined body and cap
type feeding roots at the base of its trunk that penetrate the soil (Figure 1.11A). During subsequent development, it progres-
(Figure 1.10D). Thus there is a serial homology and gradient sively loses the characteristics of a typical root meristem, by
of developmental expression of roots initiated along the length shedding its cap (Figure 1.11B,C) and its apex becomes scleri-
of the shoot with indeterminate, feeding roots initiated close to fied into a thorn (Figure 1.11D,E). The cell lineage patterns
the soil (Figure 1.10D) and determinate, spine-like roots initi- characteristic of root meristems are no longer evident. Thus
ated along the trunk (Figure 1.10B,C). These spine roots have while the root spine may look quite unlike a conventional root
lateral branches that, like lateral roots (Figure 1.10E, 1 and 2), at maturity, it does look like a root in its early development.
arise endogenously from the internal tissues of the parent root. The comparison of developmental stages of the root spine to
Because the tissue arrangement of the spines is characteristic of a conventional root has the same value in determining the
roots rather than shoots (Figure 1.11A–E), the special quality organ’s homology as does comparing morphological interme-
criterion also supports the root homology of these spines. diates using serial homology within an individual or transi-
Finally, the developmental stages of the transformation tions of organs between species.
of a root primordium into a spine reinforces not only their
10 Kaplan’s Principles of Plant Morphology

FIGURE 1.11 Median longitudinal sections of the lateral trunk roots of the palm Crysophila guagara showing the developmental transitions from a con-
ventional root apex to that of a spine root. A. Unmodified root apex. B. Later stage showing acropetal extension of elongation and differentiation resulting in
attenuation of the apex. C. Sloughing off of the root cap. D. Differentiation of elongated sclerenchyma cells in cortical and vascular regions. E. Mature spine
tip. All ×60. (From McArthur and Steeves, 1969.)

The Concepts of Analogy versus Homology shoot-borne roots. In all three we are characterizing structures
that have identical functions (grasping and twining) but are not
If the term homology deals with the structural relationships of homologous: they are analogous.
plant organs regardless of their particular functions, the term As we proceed through this text, we will see numerous exam-
analogy refers to different plant organs that perform the same ples of structural analogies, especially in plants that belong to
function. For example, tendrils are plant structures that exhibit different taxonomic or evolutionary groups but live in the same
a contact-induced growth response or thigmotropism. However, habitat. Behaviorally they all will be similar, but in many cases
tendrils can be modified shoots (branches), leaves, or roots. In will represent differing or analogous solutions to the same envi-
the grapevine relative Cissus spp., tendrils are modified shoots, ronmental stimuli. One of the principal goals of the practicing
equivalent morphologically to sterilized inflorescence branches plant morphologist is to be able to discriminate homologies from
that have acquired thigmotropic behavior associated with flo- analogies. This is accomplished by applying the homology crite-
ral reduction. By contrast, in the sweet pea, Lathyrus spp., ria that we have described in this chapter.
the tendrils are modified subunits of the leaf (leaflets or pin-
nae), whereas in the orchid Vanilla spp., tendrils are modified,
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Ontogeny and Evolution
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