PLANT BODY PLANS: UNITY OF TYPE OR CONDITIONS OF EXISTENCE?
Karl J. Niklas
Department of Plant Biology, Cornell University, Ithaca, NY
ABSTRACT
Eukaryotic photoautotrophs (‘plants’) have evolved
independently multiple times in Earth’s history. Most lineages
are ancient, strictly aquatic, and polyphyletic (collectively called
the ‘algae’), whereas the most recent lineage is largely terrestrial
and monophyletic (the embryophytes).
Yet, despite the
tremendous diversity in body size, shape, and internal structure
represented in these various lineages, only three basic body
plans exist (unicellular, colonial, and multicellular). Extensive
body plan convergence among and divergence within many of
the lineages has occurred. This aspect of plant life contrasts
with the ‘unity of body plan type’ evident in most animal
lineages and suggests that ‘conditions of existence’ have played
a greater role in plant than animal body plan evolution. This
hypothesis is here explored in terms of how each plant body
plan achieves its organized growth and how it can produce
different morphologies and anatomies adaptive to local
environmental conditions. Plant body plan size-dependent
(allometric) trends are also briefly reviewed. Some trends are
insensitive to phyletic affiliation or habitat suggesting that
deeply embedded biophysical phenomena have literally shaped
plant evolution.
INTRODUCTION
The goal of this paper is to broadly examine the
evolution of plant body plans.
A detailed and
comprehensive review of this topic is well beyond the
scope of any one paper. Therefore, the following is
presented as an admittedly incomplete survey of the topic
intended to highlight some of the main issues that beg
further attention.
Although much has been written about the evolution of
metazoan body plans, particularly in terms of the great
Cambrian ‘explosion’ (Gould, 1989; Valentine et al.,
1991; Knoll and Carroll, 1999), the evolution of plant
body plans has received comparatively little attention and
has been discussed largely in terms of the first appearance
and subsequent evolution of the land plants, the
monophyletic embryophytes (Banks, 1975; Chaloner and
Sheerin, 1979; Taylor and Taylor, 1993; Stewart and
Rothwell, 1993; Niklas, 1997; Hagemann, 1999; Sussex
and Kerk, 2001 a, b). Although it has contributed much
to our understanding of recent plant evolution, this
emphasis has largely ignored the complex antecedent
patterns of body plan evolution evident among the
polyphyletic aquatic plant lineages, collectively called the
algae (Graham, 1993; Graham and Wilcox, 2000). The
species within these algal lineages have both diversified
____________________
* Correspondence to: Karl J. Niklas
Department of Plant Biology, Cornell University
Ithaca, NY 14853 USA
Email: [email protected]
Phone: 607–255–8727; FAX: 607–255-5407
in and converged on body plan types by means of
developmental innovations some of which undoubtedly
prefigured the now highly stereotyped embryophytes.
The most obvious of these innovations is multicellularity
and discrete meristematic regions of cell production and
differentiation (Hagemann, 1999).
Therefore, no
discussion of plant body plans is sufficient without
reference to those found among modern-day algae
(Niklas, 2000).
Importantly, a survey of extant plants quickly shows
that their body plans cannot be adequately categorized or
defined solely on the basis of morphological or
anatomical criteria.
Cytological and biochemical
character states are required to taxonomically distinguish
among the various algal lineages, whereas genomic and
molecular techniques are required to resolve finer
taxonomic relations within each lineage (Gibbs, 1981;
Graham and Wilcox, 2000). Likewise, morphological,
anatomical, and growth habit convergence is evident
among the embryophytes. For example, the arborescent
growth habit has evolved independently at least six times
(sphenopsides, ferns, lycopods, dicots, monocots, and
gymnosperms), the rhizomatous growth habit appears in
each vascular plant group, and the vascular cambium
evolved independently at least three times (sphenopsides,
lycopods, and seed plants) (Niklas, 1997). Thus, whereas
metazoan lineages typically manifest a ‘unity of body
plan type,’ most plant lineages contain species with often
extremely divergent body plans.
The traditional explanation for the ‘unity of body plan
type’ is the operation of developmental constraints (see
Mayr, 1982). As a concept, ‘developmental constraints’
is useful but nonetheless ambiguous. It can mean
development is either ‘incapable’ of changing or that
developmental changes are so ‘maladaptive’ that virtually
all variants die or fail to reproduce. Thus, a lineage may
have a highly conservative body plan because dramatic
departures from a well defined developmental ‘norm’ are
either impossible or possible but quickly purged from
populations by draconian selection.
Under any
circumstances, any developmental modification requires
some sort of genomic alteration.
Therefore, any
‘constraint’ placed on body plan evolution is either the
result of the incapability or the ultimate inviability of
genomic change.
Logically, the corresponding
explanation for the absence of ‘unity of type’ is that
genomic changes capable of evoking significant
developmental modifications to achieve new body plan
types are either comparatively easily achieved
genomically or that they have a high probability of
manifesting adaptive character states.
Currently, there is no convincing evidence that plants
have a greater intrinsic capacity for genomic restructuring
than animals. Therefore, it is reasonable to conclude that
selection on plant body plans is somehow more ‘relaxed’
than on animal body plans. This hypothesis cannot be
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K.J. Niklas – Plant Body Plan Evolution
examined directly, since the relative fitness of genomic
variants affecting plant development has not been
currently quantified for a sufficient number of species.
However, the hypothesis can be explored indirectly by,
first, categorizing the different plant body plans, and,
second, by examining quantitatively the relationship
among body plan forms, functional obligations, and the
environmental contexts in which they are performed. For
the majority of plants, only two broad environmental
contexts exist, the aquatic and aerial habitat. The hydric
and essentially weightless environment in which most
algae exist contrasts sharply with that of the dehydrating
and gravity/wind induced mechanical environment
occupied by most land plants.
The Three Plant Body Plans
As noted, it is strikingly evident that external
appearance, internal structure, size, or growth habit
cannot be used to distinguish among the various plant
lineages (see Bierhorst, 1971; Gifford and Foster, 1989;
Niklas, 1997; Graham and Wilcox, 2000). Within many
algal lineages, it is commonplace to find species with
filamentous, membranous, foliar, tubular, kelp-like, or
coralline life forms.
Some siphonous algae, like
Caulerpa, can attain body lengths in excess of 20 m and a
general morphology remarkably similar to that of some
rhizomatous vascular plants (Niklas, 1992; Peters et al.,
2000). Likewise, the external appearance of plants often
belies very different tissue constructions and thus
developmental patterns. The nonvascular blade-stipeholdfast construction of some marine brown algae (e.g.,
Macrocystis) is the result of intercalary meristematic
growth yet similar in general appearance to that of the
leaf-stem-root construction of vascular plants, whereas
the tree-sized growth habit of some monocot and fern
species (e.g., Cocos and Cyathea) that lack vascular
cambia is remarkably like that of some flowering and
gymnosperm species with cambia (e.g., Carica and
Cycas).
The view adopted here and elsewhere is that plant
body plans are best categorized in terms of how each
achieves its organized growth and, if present, tissue
construction (Niklas, 2000). This perspective recognizes
only three basic body plans –– the unicellular, colonial,
and multicellular body plan (Fig. 1). Each of these can be
distinguished on the basis of the operation of a limited
number of fundamental developmental features: (1) the
extent to which cytokinesis and karyokinesis are
coordinated dictates whether the body plan is uni- or
multi-nucleate, (2) the separation of cell division products
or their aggregation by means of a common extracellular
matrix or similar device determines whether a body plan
is unicellular or colonial, and (3) the establishment of
symplastic (cytoplasmic) continuity among adjoining cell
division
products
(by
cytoplasmic
‘bridges,’
plasmodesmata, etc.) distinguishes the multicellular body
plan from the other two (Niklas, 2000).
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Fig. 1. Basic plant body plans (unicellular, colonial, and
multicellular and the features defining how each achieves its
organized growth. The unicellular body plan is achieved by the
separation and non aggregation of cell division products (e.g.,
the chlorophyte Chlamydomonas). The colonial body plan
involves the aggregation of cell division products by a common
extracellular matrix (or loricas, etc.) (e.g., the chrysophyte
Synura and the chlorophyte Hydrodictyon).
Symplastic
continuity among some or all of the cell division products results
in the multicellular body plan (e.g., the phaeophyte Fucus and
the chlorophyte Ulva). Uninucelate or polynucleate variants
exist for each of the three basic body plans and is determined by
whether cyto- and karyokinesis are synchronized (uninucelateunicellular, e.g., the chlorophyte Chlamydomonous) or not
(polynucleate-unicellular, e.g., the chrysophyte Botrydiopsis).
The siphonous variant is obtained typically by indeterminate
growth in cell size and typically involves transient
multicellularity during reproduction (e.g., the chlorophyte
Caulerpa). Variants of the multicellular body plan result from
the manner in which cell division plans are oriented with respect
to the principal body axis and the location and duration of cell
division. Cell division in one or two planes gives rise to
unbranched and branched filaments, respectively (e.g., the
chlorophytes Ulothrix and Stigeoclonium); cell division in two
plans can also give rise to monotromatic or
pseudoparenchymatous tissue constructs (e.g., the chlorophyte
Volvox and the phaeophyte Leathesia). Cell division in all three
principal body planes gives rise to a parenchymatous tissue
construct (e.g., the moss Polytrichum and seed plant Quercus).
Differences in the location and duration of sustained cell
division also results in multicellular variants. Adopted from
Niklas (2000).
Variants of each of the three body plans exist (Fig. 1).
For example, indeterminate growth in size attended by
nuclear division in the absence of sustained cytokinesis
K.J. Niklas – Plant Body Plan Evolution
gives rise to a siphonous life form, whereas a determinate
number of cell divisions whose products remain
aggregated but lack symplastic continuity obtains a
coenobial colonial condition. The most ‘versatile’ of the
three basic body plans is the multicellular body plan (Fig.
1). Different orientations of cell division with respect to
the principal body axis and differences in the location of
cell divisions in the body plan can result in seemingly
very different plant life forms.
Thus, cell division
products confined to one orientation give rise to
unbranched filaments (e.g., Spirogyra), division products
in two orientations give rise to branched filaments, or
monostromatic or pseudoparenchymatous structures (e.g.,
Stigeclonium, Volvox, and Ralfsia, respectively), and a
parenchymatous tissue construction results when cell
divisions occur in all three body planes (e.g., Fritschiella
and Quercus). The locations of cell division can also vary
in ways that fail to achieve discrete meristems (e.g.,
diffuse or trichothallic) and those that do (e.g., intercalary
or apical, or both).
Fig. 2. The siphonous and pseudoparenchymatous tissue
constructs as illustrated by the chlorophyte Codium (A– B) and
the phaeophyte Leathesia (C–D). Gross plant morphology (A
and C); representative sections through plant bodies (B and D).
It is sometimes profitable to distinguish among some
of these foregoing variants, but whether they are
sufficiently unique to warrant designation as a ‘body plan’
is debatable.
The siphonous body construct may
legitimately be viewed as sufficiently distinct as to rank
as a distinct body plan, just as the filamentous (branched
or
unbranched),
pseudoparenchymatous,
and
parenchymatous constructs of the multicellular body plan
may superficially appear intrinsically different (Fig. 2).
Likewise, the stereotypical leaf-stem-root vascular life
form has been traditionally recognized as a distinct body
plan (Kaplan, 2001). But it cannot escape attention that
the earliest known vascular plants lacked this
stereotypical construction such that yet another body plan
type would have to be added to a growing list of
designations (Taylor and Taylor, 1993). Indeed, the
tremendous diversity evident among extinct and extant
plants could be indefinitely subdivided to produce a
potentially cumbersome scheme for plant body plan types.
For example, some embryophyte vascular sporophytes
manifest secondary growth, whereas others do not. The
capacity to form wood is neither developmentally nor
evolutionarily trivial (Carlquist, 1975).
However, for the purpose of this article, all of the
foregoing variants can be adequately discussed in the
context of only three basic plant body plans.
Evidence for Divergence and Convergence
The classification scheme presented in Fig. 1 draws
into sharp focus the extent to which different plant
lineages have diversified and converged in terms of their
body plans. The extent of this diversification and
convergence is especially evident when the taxonomy of
the algal lineages is conservatively treated (Table 1),
since to do otherwise would only further emphasize body
plan convergence and divergence among these lineages.
For example, if the Phaeophyta and Chrysophyta are
grouped together taxonomically (as recent molecular and
cytological cladistic analyses strongly suggest they
should), the resulting new phylum (Ochrophyta) would
contain all known plant body plans (Graham and Wilcox,
2000). For this reason, the following discussion is based
on a modified version of the taxonomy proposed by Bold
and Wynne (1978).
All of the major body plans, including those with a
siphonous, filamentous, pseudoparenchymatous, and
parenchymatous cellular construction, occur in the
Chlorophyta and Chrysophyta (Table 1). This is not
surprising since these are two of the most species-rich
algal lineages. Likewise, the unicellular and colonial
body plans occur in all algal lineages with the exception
of the brown algae. The absence of the unicellular body
plan in the brown algae is somewhat surprising, since this
lineage undoubtedly had a unicellular ancestral condition.
Its absence in the brown algae suggests that it has
taxonomically escaped attention or that it has gone extinct
in terms of living representatives.
Only three algal
lineages lack living multicellular representatives. Each of
these lineages likely evolved as the result of secondary
rather than primary endosymbiotic events (Gibbs, 1992;
Douglas, 1991; McFadden et al., 1994). The likelihood
that each of these lineages is the result of a cytoplasmic
and genomic ‘plant-animal hybrid’ may account for the
absence of the multicellular body plan in each. Finally,
all extant embryophytes are exclusively multicellular and
none is known to have a pseudoparenchymatous tissue
construction. Filamentous and siphonous (coenocytic)
life forms may be expressed developmentally in some
embryophyte taxa. But, in each case, these forms are
ontogenetically transient (e.g., filamentous moss
protonema and the coenocytic ‘free cellular’ endosperm
and tetranucleate megaspore of some angiosperms).
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K.J. Niklas – Plant Body Plan Evolution
Thus, when viewed broadly, the embryophytes are the
only plant lineage to manifest a ‘unity of body plan type’
(multicellular). This may reflect a ‘founder effect’ or
severe selection pressure.
The embryophytes are
monophyletic and believed to have evolved from algal
ancestors similar in many ways to modern-day
multicellular charophycean algae (Graham, 1993; Graham
and Wilcox, 2000). Although unicellular and colonial
species also occur in the Charophyta, cladistic analyses
consistently identify multicellular charophycean taxa,
such as Coleochaete, as the closest living relatives of the
embryophytes.
In turn, this suggests that the
embryophytes had a multicellular phyletic legacy that
dictated their evolution on land. However, the unity of
type evident for the embryophytes may also be the result
of directional (canalizing) selection. Any truly terrestrial
plant cannot survive, grow, or successfully reproduce in
an aerial environment without biophysical and
physiological features that arguably necessitate a
multicellular body plan. The view taken here is that the
‘unity of type’ evident among embryophytes is the result
of selection acting on ‘the conditions of existence’ and
not the result of developmental (genomic) ‘constraints’
sensu stricto.
Conditions of Existence: Water versus Air
Any explanation for the body plan convergence among
and divergence within the various plant lineages is
problematic. But it is fair to say that each plant lineage
reflects an independent ‘experiment’ in terms of how
plant life evolutionarily adapted to its environment. Since
convergent evolution provides some of the strongest
circumstantial evidence for adaptation and since
divergence provides equally convincing evidence for
diversifying selection, it is reasonable to suppose that
body plan convergent evolution reflects adaptations to the
conditions of plant existence and that these conditions are
manifold and complex.
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In terms of selection on plant form, it is important to
note that all photosynthetic eukaryotes (plants) must
perform the same four basic tasks to survive, grow, and
perpetuate their kind. Each must harvest sunlight,
exchange mass in the form of gases and minerals between
its living substance and the fluid in which it lives, each
must cope with externally applied mechanical forces, and
each must successfully reproduce, either asexually or
sexually (Niklas, 1992, 1994). The performance of none
of these tasks intrinsically requires a particular body plan,
since unicellular, colonial, and multicellular organisms
are each theoretically capable of performing all of these
tasks equally well. However, the physical environment in
which these tasks are performed has a profound effect on
the relation between plant form and function such that the
‘conditions of existence’ limit the body plan options for
any plant. Remarkably, support for these claims comes
from simple geometry, physics, and chemistry.
Theory and practice show that the most efficient light
harvesting and nutrient absorbing plants are very small
unicellular algae (Kirk, 1975; Niklas, 1994), because
small objects have very large surface areas relative to
their volumes and since their populations have very high
absorption cross sections (Fig. 3). Likewise, provided
that a plant is very small (or very large but composed of
flexible yet elastic materials), large surface areas can
impose very small drag forces, since a unicellular plant
can move with the flow, while a very large plant can bend
and twist to reduce its projected surface area toward
oncoming water (Niklas, 1994). Thus, since dehydration
is unlikely in an aquatic environment, the amplification of
surface areas with respect to body volume evokes no
intense selection.
Indeed, allometric analyses of unicellular algae reveal
that cell surface area scales approximately as the 3/4power of cell volume (Fig. 3). Noting that the scaling
exponent for surface area to volume is 2/3 for any series
of objects sharing the same geometry and shape (which
K.J. Niklas – Plant Body Plan Evolution
are not the same thing) but that differ in overall size
(volume), it is obvious that algal conspecifics differing in
size or species differing in phyletic affiliation have
different cell geometries and shapes and that either
geometry or shape changes as a function of absolute cell
size.
Fig. 3. Effect of changes in cell surface area and cell volume
on the capacity to absorb nutrients from the surrounding
medium and to capture sunlight. A. Cell surface area plotted
against cell volume for a variety of algal species drawn from
diverse lineages shows a log-log linear trend with a slope less
than unity (i.e., surface area decreases with respect to cell
volume with increasing size. B. Quotient of cell surface area
and volume plotted against cell volume for algal taxa in A. This
quotient is highest for the smallest cells and decreases in a loglog linear manner with increasing cell size (volume). C.
Absorption cross section (reflects the capacity of cells to harvest
sunlight) for spherical cells differing in diameter (see insert)
plotted against the wavelengths of visible (and
photosynthetically useable) light. The light harvesting capacity
for spherical cells decreases with increasing cell diameter.
Adopted from Niklas (1994).
Significantly, computer models reveal that the 3/4
scaling exponent typically observed for different
unicellular algal species is the maximum that can be
expected for the range of cell size, shape, and geometry
represented among these species (Niklas, 1994). This
higher than expected scaling exponent provides strong
circumstantial evidence that surface area has been
maximized with respect to cell volume over the long
course of algal evolution.
In this respect, the plant colonial body plan may be
viewed as a biophysical extension of the unicellular body
plan adaptive ‘experiment.’ Each aggregated cell can
retain its small size (and thus large surface area and light
harvesting capability), yet benefit from aggregation in a
variety of ways (Kirk, 1998). Some cells in the colony
can reproduce, serve to adhere the colony to a substrate,
provide flexible extensions (thereby elevating the colony
above nearby obstructions of light), etc. Likewise, the
cell aggregate can increase in size and change its overall
shape and geometry (without changing cell size, shape, or
geometry), thereby favorably influencing the microhydrodynamic environment in terms of either the
availability or the rate of absorption of dissolved nutrients
at the level of individual cells (Niklas, 2000). Aggregated
cells may also benefit by contributing to a common
chemical defense system.
It also cannot escape attention that flexible filamentous
growth forms, either unbranched or branched, can
maintain large surface areas with respect to their body
volumes yet grow indefinitely in size. Simple geometry
shows that the surface area to volume ratio of a cylinder
composed of cells equals the reciprocal of cell diameter.
Thus, a filamentous alga can grow indefinitely in length
yet not experience a reduction in surface area provided
cell diameter remains constant. By the same token, the
interweaving of siphonous cell components (or filaments,
which obtains a pseudoparenchymatous tissue
construction) can benefit from this geometric ‘rule’ (see
Fig. 2). Provided that the fluid medium can penetrate and
refresh the inner meshwork of cell walls with nutrients
and provided that light can penetrate to illuminate all or
much of the cytoplasm, the siphonous or the multicellular
(pseudoparenchymatous or parenchymatous) body plan is
as effective physiologically or biomechanically as the
unicellular or colonial body plan.
Body size and shape, therefore, are not intrinsically
limited in the aquatic environment provided that
organized growth achieves morphologies that abide by
some very simple biophysical and geometric rules. Since
the unicellular, colonial, and multicellular body plans are
each capable of developmentally adjusting surface area
with respect to body volume, it is not surprising that these
body plans are represented by numerous species in
virtually every major algal lineage.
However, in the absence of mitigating features (e.g.,
cuticles, roots, and stomata) most of which necessitate a
multicellular body plan, large surface areas with respect
to volumes are detrimental for a terrestrial (or more
properly speaking, an aerial) plant (Nobel, 1983). As
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K.J. Niklas – Plant Body Plan Evolution
body parts are increasingly elevated above ground, they
become more susceptible to dehydration, first, because
the distance (and thus the transport time) between a
hydrated substrate and evaporative body parts increases,
and, second, because wind speeds tend to increase
exponentially from the ground surface to the ambient
wind speed limit (Vogel, 1981; Nobel, 1983). Plants that
‘hug’ their substrates or grow in tight clumps as do many
bryophytes can reduce their individual rates of water loss
and they can alter their micro-aerodynamic environments
favorably in much the same manner as do aquatic colonial
or multicellular plants. But it is nonetheless generally
true that a truly aerial plant requires a multicellular body
plan, whereas an aquatic plant is largely free of this
‘constraint.’
Living in the Air
An aerial existence imposes many demands on plant
life. Yet, it also confers many advantages. An aquatic
plant typically has free access to water over all of its
exposed surfaces. Likewise, it is neutrally or negatively
buoyant (virtually all plant cells and tissues are as dense
or less dense than water). Water also provides a filter for
UV radiation. In contrast, an aerial plant always risks
dehydration and it must support its own weight against
gravity as well as wind induced pressure (drag) forces.
The successful colonization of land by plants, therefore,
required adaptations to wind and gravity. Nonetheless,
access to carbon dioxide and oxygen is much greater in
air than in water, and air is optically transparent in
contrast to water (which absorbs all wavelengths of
visible light and preferentially absorbs the blue and red
wavelengths most useful for photosynthesis) (Nobel,
1983). For these reasons, many aquatic plants ‘hug’ the
air-water interface where atmospheric gases are more
readily dissolved and available in water and where light is
less attenuated in intensity or filtered preferentially in the
red and blue wavelengths. Indeed, this interface may
have been the cradle for land plant evolution.
Fluctuations in the levels of freshwater ponds, lakes, or
stream banks would have periodically exposed the ancient
algal ancestors of the embryophytes to air, thereby
selecting those species that could cope with brief periods
of exposure. The inverse relation between body size and
mutation rates suggests that the survivors were probably
comparatively small, short-lived, and genomically
mutable.
Indeed, the oldest known land plant sporophytes were
small, anatomically simple, and produced cutinized spores
capable of surviving exposure to the air (Banks, 1975;
Chaloner and Sheerin, 1979; Taylor and Taylor, 1993).
These sporophytes had cylindrical bifurcating axes that
may have had a cuticle capable of reducing the rate of
water loss from exposed surfaces. Nothing is currently
known about their corresponding gametophytes, but these
were likely prostrate or short multicellular life forms,
since one of the shared ancestral conditions of all extant
embryophytes is a diplobiontic life cycle (an alternation
between a multicellular diploid sporophyte and a
multicellular haploid gametophyte generation) involving
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Gravitational and Space Biology Bulletin 17(2) June 2004
an archegonium (a specialized multicellular eggproducing structure) (Graham, 1993). Since cladistic
analyses currently identify multicellular charophycean
algae as the sister group to the land plants and since all of
these algae lack a multicellular diploid (‘sporophyte’)
generation, it is reasonable to suppose that the
embryophyte sporophyte may represent an evolutionary
innovation that appeared during or very shortly after plant
life made it onto land. The benefits of a multicellular
diploid phase are nonetheless clear –– it amplifies the
number of cells that can undergo meiosis and thus
increases the number of haploid individuals that a
fertilization event can produce.
Fig. 4. Morphological and anatomical differences between the
gametophyte (A–C) and sporophyte (D–E) of the moss
Polytrichum commune. A. Gametangiophore (reproductive
axis of gametophyte, g) bearing sporophyte with a single
sporangial capsule (c) elevated by a hair-like seta (s). B.
Phyllid (leaf-like lateral appendage) of gametophyte with ribbed
adaxial surface (r) and ‘mid-rib’ of conducting tissues (m). C.
Portion of cross section through ‘leafy’ gametangiophore
showing complex tissue differentiation reminiscent of vascular
stem anatomy (hydrome, h; leptome, l). D. Longitudinal cross
section through sporophyte capsule showing central chamber of
sporogenous tissue (st) surrounding the central columella (c)
enclosed apically by the operculum (o) . E. Distal view of
sporangium lacking the operculum and revealing the peristome
(p).
But, from a body plan perspective, the embryophyte
life cycle is schizophrenic –– the reproductive roles
played by the gametophyte and sporophyte generations
are very different and require different body plan features
K.J. Niklas – Plant Body Plan Evolution
(Niklas, 1997, 2000). The reproductive tasks of the
gametophyte are to produce gametes and to retain,
nourish, and protect the developing sporophyte, which
develops from a fertilized egg retained within an
archegonium. The tasks of the sporophyte are to produce
and disperse spores. Free-living gametophytes, such as
those of modern-day bryophytes and pteridophytes,
require free-standing water for sperm dispersal and
syngamy. For this reason, most free-living gametophytes
are prostrate or vertically challenged. Curiously, their
sporophytes are not terrestrial sensu stricto, since they are
attached directly to an organic rather than an inorganic
substrate, the gametophyte, which provides water and soil
nutrients (Fig. 4). These sporophytes typically elevate
their spores above the boundary layer produced by and
around their gametophytes, thereby capitalizing on
rapidly moving and turbulent air currents to disperse
spores. From an engineering perspective, the optimal
‘design’ for spore elevation is a cylinder. This geometry
can grow in length (and height) and yet retain the same
surface area relative to volume with increasing overall
size. It also provides an excellent geometry for dealing
with bending and twisting forces (Niklas, 1992). Not
surprisingly, therefore, the basic geometric unit of the
embryophyte sporophyte is a terete cylinder.
Viewed from the perspective of form, function, and
environmental context, the morphology and anatomy of
the gametophyte and sporophyte generation of land plant
species have been evolutionarily driven down separate
and often highly divergent pathways. Yet another wedge
between the two is that only one of the two multicellular
generations in the embryophyte life cycle can be
reasonably expected to manifest indeterminate growth in
size, since both are physically attached and inexorably
physiologically interdependent such that continued
growth of one will have negative effects on the other
(Niklas, 1997). Among extant nonvascular embryophytes
(mosses, liverworts, and hornworts), the gametophyte
generation is typically long-lived and indeterminate in
growth, whereas the sporophyte generation is short-lived
and determinate in growth (Bold, 1967). The reverse is
true for most vascular plant species. Indeed, among the
seed plants, the gametophyte generation has been reduced
to microscopic size (e.g., angiosperm pollen grains and
megagametophytes).
The ‘wedge’ between the size and continued growth in
size of the gametophyte and sporophyte generations of
embryophytes has had a profound effect on anatomy as
well. Continued growth in size attended by the vertical
elevation of body parts biophysically requires the bulk
transport of water and thus increasingly specialized tissue
systems, since rates of nutrient passive diffusion are too
slow to accommodate the metabolic needs of large plants
(Nobel, 1983). The hydrome and leptome of some
mosses are functionally analogous and oft times
morphologically strikingly similar to xylem and phloem
tissues of vascular plants (see Fig. 4 C). By the same
token the ‘trumpet cells’ of some large marine brown
algae, which supply nutrients to light-starved cells well
below the water-air interface, are functionally analogous
to phloem tissue for much the same reasons (Bold and
Wynne, 1978).
Fig. 5. Allometric (size-dependent) relations for plant
growth rates and body mass (A) and for light harvesting
capacity (B) across unicellular and multicellular plants. A.
Annual average plant growth rates plotted against body mass is
described by a log-log linear curve with a slope ~ 3/4. B.
Annual average plant growth plotted against light harvesting
capacity (gauged by algal cell pigment concentration or
standing leaf biomass per plant) is described by two log-log
linear curves, each of which has a slope ~ 1. Adopted from
Niklas and Enquist (2001).
The Allometry of Body Plans
Morphological and anatomical changes occur as most
organisms continue to grow in size.
Likewise,
evolutionary increases in the adult size of related species
are typically attended by changes in anatomy and body
geometry or shape.
Curiously, broad interspecific
comparisons among phyletically highly diverse organisms
reveal strikingly similar patterns of adjustment. Indeed,
some of these patterns are ‘invariant’ for plants and
animals. One of the better known of these ‘invariant’
patterns is the scaling of overall growth rates with respect
to body mass (Niklas and Enquist, 2001). Across
unicellular and multicellular animals and plants, annual
growth rate scales, on average, as the 3/4–power of body
mass (Fig. 5 A). Perhaps less well known is the scaling of
plant growth rates with respect to the capacity of the
individual to harvest light. Across algae and aquatic as
well as terrestrial vascular plants, this relationship is
isometric, that is growth rates scale as the 1–power of
light harvesting capacity measured as algal cell pigment
concentration or standing leaf biomass per individual
tracheophyte (Fig. 5 B). Remarkably consistent scaling
relations are also observed for seed plant leaf, stem, and
root biomass (Enquist and Niklas, in press). Across a
broad spectrum of spermatophytes, leaf biomass per
individual scales as the 3/4–power of stem (or root)
Gravitational and Space Biology Bulletin 17(2) June 2004
139
K.J. Niklas – Plant Body Plan Evolution
biomass such that stem and root biomass evince an
isometric relationship (Fig. 6 A).
Anatomical allometric trends are also evident. For
example, the relationship between plant height and stem
diameter is curvilinear even when the data are logtransformed. Thus, across all species, no unique scaling
exponent exists for this relationship (Fig. 6 B). Yet,
biomechanical calculations show that the density-specific
stiffness of the tissues providing the bulk of stem
mechanical support has significantly increased among the
largest of the living representatives of each major land
plant reproductive grade (i.e., bryophytes, pteridophytes,
and seed plants) (Niklas, 1994). Likewise, the fossil
record as well as comparative studies among extant
species highlights a number of important allometric trends
in plant anatomy relating to the capacity to resist windthrow.
Fig. 6. Allometric (size-dependent) relations among leaves,
stems and roots of tree species differing in size (A) and plant
height and stem (or moss sporophyte) diameter (B). A. Leaf
biomass plotted against stem biomass is described by a log-log
linear curve with a slope ~ 3/4; root biomass plotted against
stem biomass is described by a log-log linear curve with a slope
~ 1. B. Plant height plotted against stem diameter is log-log
nonlinear and ‘convex’ (indicating plant height decreases with
respect to interspecific increases in stem diameter). Solid lines
denote hypothetical maximum plant height provided that each
plant stem is composed exclusively of a single tissue (P =
parenchyma, X = primary vascular tissues, S = sclerenchyma;
W = wood). Interspecific increases in plant height are attended
by anatomical differences codified by the evolutionary adoption
140
Gravitational and Space Biology Bulletin 17(2) June 2004
of stiffer and proportionally less dense plant tissues for the
principal stem stiffening agent. Adopted from Niklas (1992).
Theories abound to explain these and other allometric
trends, but none has escaped well reasoned criticism.
Most of these theories emphasize the scaling relationship
between total body surface area and volume. Plant
surface area (whether that of a unicellular or multicellular
plant) is a reasonable surrogate measure of the ability of
the individual organism to exchange mass and energy
with its external environment; body volume is a
reasonable measure of the metabolic demands of the
organism. Since the density of plant materials is nearly
constant across materials and organisms, body volume is
a comparatively good measure of body mass. In this
crude sense, the relationship between surface area and
body volume crudely reflects the rates of energy/nutrient
influx and metabolic demand, respectively. Growth is a
measure of the net gain in body volume (hence mass), and
so the allometry of growth to body mass is expected on
theoretical grounds to reflect the allometry of surface area
to volume (mass). As noted, the expected scaling
exponent for surface area with respect to body volume is
2/3, but only provided that neither body shape nor
geometry changes with respect to body size. Yet, we
have strong evidence that each of the three basic plant
body plans (unicellular, colonial, and multicellular) can
and does change shape and geometry with increasing
body size. Thus, the scaling exponent for body surface
area with respect to body volume is nearly 3/4 across even
unicellular plant species.
Therefore, on theoretical
grounds, most of the ‘invariant’ scaling exponents that
have been identified for plant allometric relationships are
expected to equal or approximate 3/4 (or some multiple
thereof). Similarly, growth rates across diverse plants is
expected to scale in a nearly isometric way with respect to
the capacity to harvest sunlight.
Nonetheless, all that can be said with certainty is that
some seemingly invariant trends exist, that some of these
trends hold true for animal as well as plant life, and that
they point to some deep seated biophysical phenomena
that have literally shaped much of organic evolution.
More detailed studies are required to both confirm the
existence of ‘invariant’ allometric trends and to identify
precisely their proximate and ultimate physical and
biological causes. In many respects, plants provide the
best experimental venue for this research agenda, since
the vast majority of plant species shares the same basic
physiological requirements for survival, growth, and
successful reproduction.
Concluding Remarks
We know comparatively little about the early
evolutionary history of most plant lineages, in part
because the fossil record is highly fragmentary and
because the assignment of many fossils is problematic
owing to extensive morphological and anatomical
convergence. Detailed developmental studies of many
important taxa are also lacking.
Algal molecular
taxonomy and developmental biology are still in their
K.J. Niklas – Plant Body Plan Evolution
infancy Likewise, with all the emphasis on vascular land
plant evolution and biology, especially that of seed plants,
we are still also remarkably ignorant about the details of
non-vascular and relictual vascular non-seed plants (the
bryophytes and pteridophytes). For all these reasons, this
treatment of the evolution of plant body plans is
unavoidably speculative and incomplete. Yet, this area of
research is vital to our understanding of life on Earth,
since all but a few ecosystems are dependent on plant life
as the primary producers and since animal evolution
cannot be truly understood without at least passing
reference to plant biology.
Certainly the role of homeotic genes needs to explored
for plants. As is well known, these genes encode for
transcription factors similar to bacterial repressor proteins
and thus appear to be taxonomically ubiquitous and thus
very ancient (Sommer et al., 1990; Davies and SchwarzSommer, 1994; Gerhart and Kirschner, 1997). Among
arthropods, vertebrates, and flowering plants, these
transcription factors can serve as molecular markers for
the position of cells along the body axis (Carroll, 1995;
Akam, 1998 a, b). And, in both plants and animals, the
activation of individual homeotic genes at different
positions in meristematic/embryonic regions is associated
with patterns of differentiation that can be maintained
throughout ontogeny. Since the differential expression of
homeotic genes is associated with the appearance of
different developmental fates in different regions of the
body plan axis and since mutations at these loci can shunt
developmental patterns along normal or atypical
pathways, the potential capacity for homeotic gene
mutations to change the course of plant body plan
evolution is obvious.
However, homology at the molecular level of base-pair
comparisons is not equivalent to homology at the level of
macro-phenotypic comparisons. Organic diversity is
largely the result of combinatorial genomic variation
rather than an unlimited capacity for genomic innovation
(Theissen et al., 1996). Each gene and its product(s)
operate in the context of extensive gene and product
networks and the products of a single gene or gene
network can operate developmentally or physiologically
in different ways depending on their location within the
same organism (e.g., IAA in the vascular plant body).
Thus, while homeotic genes are undoubtedly important,
their ability to potentially define or transform one body
plan type into another must be understood in the broader
context of complex genomic and epigenetic phenomena,
about which we are currently just beginning to
understand.
Finally, the evolution of multicellular life forms in all
of the algal lineages believed to trace their ancestry back
to primary endosymbiotic events in Earth’s ancient
history (e.g., chlorophytes and phaeophytes) and the
absence of multicellularity in those algal lineages
believed to have evolved as the result of secondary
endosymbiotic
events
(e.g.,
euglenoids
and
cryptomonads) raises the tantalizing possibility that
multicellularity evolved in part as the result of lateral
gene transfers during primary endosymbiotic events
(Niklas, 2000). Certainly, multicellularity, here defined
as the establishment of symplastic continuity among
neighboring cells, has evolved in the cyanobacteria,
which are believed to be the modern-day descendants of
the prokaryotes from which the first chloroplasts evolved
(Margulis, 1992; Maddock, 1984; Gober and Margues,
1995). This possibility suggests that the genetic and
epigenetic phenomena associated with prokaryotic
multicellularity may be fertile ground for research into the
evolution of plant multicellularity.
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