BODY PLANS: UNITY OF TYPE OR CONDITIONS OF EXISTENCE? Karl J. Niklas Department of Plant , Cornell University, Ithaca, NY in and converged on types by means of ABSTRACT developmental innovations some of which undoubtedly prefigured the now highly stereotyped . Eukaryotic photoautotrophs (‘’) have evolved The most obvious of these innovations is multicellularity independently multiple times in Earth’s history. Most lineages and discrete meristematic regions of cell production and are ancient, strictly aquatic, and polyphyletic (collectively called differentiation (Hagemann, 1999). Therefore, no the ‘’), whereas the most recent lineage is largely terrestrial and monophyletic (the embryophytes). Yet, despite the discussion of plant body plans is sufficient without tremendous diversity in body size, shape, and internal structure reference to those found among modern-day algae represented in these various lineages, only three basic body (Niklas, 2000). plans exist (unicellular, colonial, and multicellular). Extensive Importantly, a survey of extant plants quickly shows body plan convergence among and divergence within many of that their body plans cannot be adequately categorized or the lineages has occurred. This aspect of plant contrasts defined solely on the basis of morphological or with the ‘unity of body plan type’ evident in most anatomical criteria. Cytological and biochemical lineages and suggests that ‘conditions of existence’ have played character states are required to taxonomically distinguish a greater role in plant than animal body plan . This hypothesis is here explored in terms of how each plant body among the various algal lineages, whereas genomic and plan achieves its organized growth and how it can produce molecular techniques are required to resolve finer different morphologies and adaptive to local taxonomic relations within each lineage (Gibbs, 1981; environmental conditions. Plant body plan size-dependent Graham and Wilcox, 2000). Likewise, morphological, (allometric) trends are also briefly reviewed. Some trends are anatomical, and growth convergence is evident insensitive to phyletic affiliation or suggesting that among the embryophytes. For example, the arborescent deeply embedded biophysical phenomena have literally shaped growth habit has evolved independently at least six times plant evolution. (sphenopsides, ferns, lycopods, dicots, monocots, and gymnosperms), the rhizomatous growth habit appears in each group, and the vascular cambium INTRODUCTION evolved independently at least three times (sphenopsides, lycopods, and seed plants) (Niklas, 1997). Thus, whereas The goal of this paper is to broadly examine the metazoan lineages typically manifest a ‘unity of body evolution of plant body plans. A detailed and plan type,’ most plant lineages contain species with often comprehensive review of this topic is well beyond the extremely divergent body plans. scope of any one paper. Therefore, the following is The traditional explanation for the ‘unity of body plan presented as an admittedly incomplete survey of the topic type’ is the operation of developmental constraints (see intended to highlight some of the main issues that beg Mayr, 1982). As a concept, ‘developmental constraints’ further attention. is useful but nonetheless ambiguous. It can mean Although much has been written about the evolution of development is either ‘incapable’ of changing or that metazoan body plans, particularly in terms of the great developmental changes are so ‘maladaptive’ that virtually ‘explosion’ (Gould, 1989; Valentine et al., all variants die or fail to reproduce. Thus, a lineage may 1991; Knoll and Carroll, 1999), the evolution of plant have a highly conservative body plan because dramatic body plans has received comparatively little attention and departures from a well defined developmental ‘norm’ are has been discussed largely in terms of the first appearance either impossible or possible but quickly purged from and subsequent evolution of the land plants, the populations by draconian selection. Under any monophyletic embryophytes (Banks, 1975; Chaloner and circumstances, any developmental modification requires Sheerin, 1979; Taylor and Taylor, 1993; Stewart and some sort of genomic alteration. Therefore, any Rothwell, 1993; Niklas, 1997; Hagemann, 1999; Sussex ‘constraint’ placed on body plan evolution is either the and Kerk, 2001 a, b). Although it has contributed much result of the incapability or the ultimate inviability of to our understanding of recent plant evolution, this genomic change. Logically, the corresponding emphasis has largely ignored the complex antecedent explanation for the absence of ‘unity of type’ is that patterns of body plan evolution evident among the genomic changes capable of evoking significant polyphyletic aquatic plant lineages, collectively called the developmental modifications to achieve new body plan algae (Graham, 1993; Graham and Wilcox, 2000). The types are either comparatively easily achieved species within these algal lineages have both diversified genomically or that they have a high probability of ______manifesting adaptive character states. Currently, there is no convincing evidence that plants * Correspondence to: Karl J. Niklas Department of Plant Biology, Cornell University have a greater intrinsic capacity for genomic restructuring Ithaca, NY 14853 USA than . Therefore, it is reasonable to conclude that Email: [email protected] selection on plant body plans is somehow more ‘relaxed’ Phone: 607–255–8727; FAX: 607–255-5407 than on animal body plans. This hypothesis cannot be

Gravitational and Space Biology Bulletin 17(2) June 2004 133

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 remarkably similar to that of some rhizomatous vascular plants (Niklas, 1992; Peters et al., Fig. 1. Basic plant body plans (unicellular, colonial, and 2000). Likewise, the external appearance of plants often multicellular and the features defining how each achieves its organized growth. The unicellular body plan is achieved by the belies very different tissue constructions and thus separation and non aggregation of cell division products (e.g., developmental patterns. The nonvascular blade-stipe- the chlorophyte Chlamydomonas). The colonial body plan holdfast construction of some marine brown algae (e.g., involves the aggregation of cell division products by a common Macrocystis) is the result of intercalary meristematic extracellular matrix (or loricas, etc.) (e.g., the chrysophyte growth yet similar in general appearance to that of the Synura and the chlorophyte Hydrodictyon). Symplastic leaf-stem-root construction of vascular plants, whereas continuity among some or all of the cell division products results the tree-sized growth habit of some monocot and fern in the multicellular body plan (e.g., the phaeophyte Fucus and species (e.g., Cocos and Cyathea) that lack vascular the chlorophyte Ulva). Uninucelate or polynucleate variants exist for each of the three basic body plans and is determined by cambia is remarkably like that of some flowering and whether cyto- and karyokinesis are synchronized (uninucelate- gymnosperm species with cambia (e.g., Carica and unicellular, e.g., the chlorophyte Chlamydomonous) or not Cycas). (polynucleate-unicellular, e.g., the chrysophyte Botrydiopsis). The view adopted here and elsewhere is that plant The siphonous variant is obtained typically by indeterminate body plans are best categorized in terms of how each growth in cell size and typically involves transient achieves its organized growth and, if present, tissue multicellularity during reproduction (e.g., the chlorophyte construction (Niklas, 2000). This perspective recognizes Caulerpa). Variants of the multicellular body plan result from only three basic body plans –– the unicellular, colonial, the manner in which cell division plans are oriented with respect and multicellular body plan (Fig. 1). Each of these can be to the principal body axis and the location and duration of cell division. Cell division in one or two planes gives rise to distinguished on the basis of the operation of a limited unbranched and branched filaments, respectively (e.g., the number of fundamental developmental features: (1) the chlorophytes Ulothrix and Stigeoclonium); cell division in two extent to which cytokinesis and karyokinesis are plans can also give rise to monotromatic or coordinated dictates whether the body plan is uni- or pseudoparenchymatous tissue constructs (e.g., the chlorophyte multi-nucleate, (2) the separation of cell division products Volvox and the phaeophyte Leathesia). Cell division in all three or their aggregation by means of a common extracellular principal body planes gives rise to a parenchymatous tissue matrix or similar device determines whether a body plan construct (e.g., the moss Polytrichum and seed plant Quercus). is unicellular or colonial, and (3) the establishment of Differences in the location and duration of sustained cell symplastic (cytoplasmic) continuity among adjoining cell division also results in multicellular variants. Adopted from Niklas (2000). division products (by cytoplasmic ‘bridges,’

plasmodesmata, etc.) distinguishes the multicellular body Variants of each of the three body plans exist (Fig. 1). plan from the other two (Niklas, 2000). For example, indeterminate growth in size attended by

nuclear division in the absence of sustained cytokinesis

134 Gravitational and Space Biology Bulletin 17(2) June 2004

K.J. Niklas – Plant Body Plan Evolution gives rise to a siphonous life form, whereas a determinate plan (Kaplan, 2001). But it cannot escape attention that number of cell divisions whose products remain the earliest known vascular plants lacked this aggregated but lack symplastic continuity obtains a stereotypical construction such that yet another body plan coenobial colonial condition. The most ‘versatile’ of the type would have to be added to a growing list of three basic body plans is the multicellular body plan (Fig. designations (Taylor and Taylor, 1993). Indeed, the 1). Different orientations of cell division with respect to tremendous diversity evident among extinct and extant the principal body axis and differences in the location of plants could be indefinitely subdivided to produce a cell divisions in the body plan can result in seemingly potentially cumbersome scheme for plant body plan types. very different plant life forms. Thus, cell division For example, some vascular sporophytes products confined to one orientation give rise to manifest secondary growth, whereas others do not. The unbranched filaments (e.g., Spirogyra), division products capacity to form wood is neither developmentally nor in two orientations give rise to branched filaments, or evolutionarily trivial (Carlquist, 1975). monostromatic or pseudoparenchymatous structures (e.g., However, for the purpose of this article, all of the Stigeclonium, Volvox, and Ralfsia, respectively), and a foregoing variants can be adequately discussed in the parenchymatous tissue construction results when cell context of only three basic plant body plans. divisions occur in all three body planes (e.g., Fritschiella and Quercus). The locations of cell division can also vary Evidence for Divergence and Convergence in ways that fail to achieve discrete meristems (e.g., The classification scheme presented in Fig. 1 draws diffuse or trichothallic) and those that do (e.g., intercalary into sharp focus the extent to which different plant or apical, or both). 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 (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 Fig. 2. The siphonous and pseudoparenchymatous tissue in terms of living representatives. Only three algal constructs as illustrated by the chlorophyte Codium (A– B) and lineages lack living multicellular representatives. Each of the phaeophyte Leathesia (C–D). Gross (A these lineages likely evolved as the result of secondary and C); representative sections through plant bodies (B and D). rather than primary endosymbiotic events (Gibbs, 1992; Douglas, 1991; McFadden et al., 1994). The likelihood It is sometimes profitable to distinguish among some that each of these lineages is the result of a cytoplasmic of these foregoing variants, but whether they are and genomic ‘plant-animal hybrid’ may account for the sufficiently unique to warrant designation as a ‘body plan’ absence of the multicellular body plan in each. Finally, is debatable. The siphonous body construct may all extant embryophytes are exclusively multicellular and legitimately be viewed as sufficiently distinct as to rank none is known to have a pseudoparenchymatous tissue as a distinct body plan, just as the filamentous (branched construction. Filamentous and siphonous (coenocytic) or unbranched), pseudoparenchymatous, and life forms may be expressed developmentally in some parenchymatous constructs of the multicellular body plan embryophyte taxa. But, in each case, these forms are may superficially appear intrinsically different (Fig. 2). ontogenetically transient (e.g., filamentous moss Likewise, the stereotypical leaf-stem-root vascular life protonema and the coenocytic ‘free cellular’ endosperm form has been traditionally recognized as a distinct body and tetranucleate megaspore of some angiosperms). Gravitational and Space Biology Bulletin 17(2) June 2004 135 K.J. Niklas – Plant Body Plan Evolution

Thus, when viewed broadly, the embryophytes are the In terms of selection on plant form, it is important to only plant lineage to manifest a ‘unity of body plan type’ note that all photosynthetic (plants) must (multicellular). This may reflect a ‘founder effect’ or perform the same four basic tasks to survive, grow, and severe selection pressure. The embryophytes are perpetuate their kind. Each must harvest sunlight, monophyletic and believed to have evolved from algal exchange mass in the form of gases and minerals between ancestors similar in many ways to modern-day its living substance and the fluid in which it , each multicellular charophycean algae (Graham, 1993; Graham must cope with externally applied mechanical forces, and and Wilcox, 2000). Although unicellular and colonial each must successfully reproduce, either asexually or species also occur in the Charophyta, cladistic analyses sexually (Niklas, 1992, 1994). The performance of none consistently identify multicellular charophycean taxa, of these tasks intrinsically requires a particular body plan, such as Coleochaete, as the closest living relatives of the since unicellular, colonial, and multicellular organisms embryophytes. In turn, this suggests that the are each theoretically capable of performing all of these embryophytes had a multicellular phyletic legacy that tasks equally well. However, the physical environment in dictated their evolution on land. However, the unity of which these tasks are performed has a profound effect on type evident for the embryophytes may also be the result the relation between plant form and function such that the of directional (canalizing) selection. Any truly terrestrial ‘conditions of existence’ limit the body plan options for plant cannot survive, grow, or successfully reproduce in any plant. Remarkably, support for these claims comes an aerial environment without biophysical and from simple geometry, physics, and chemistry. physiological features that arguably necessitate a Theory and practice show that the most efficient light multicellular body plan. The view taken here is that the harvesting and nutrient absorbing plants are very small ‘unity of type’ evident among embryophytes is the result unicellular algae (Kirk, 1975; Niklas, 1994), because of selection acting on ‘the conditions of existence’ and small objects have very large surface areas relative to not the result of developmental (genomic) ‘constraints’ their volumes and since their populations have very high sensu stricto. absorption cross sections (Fig. 3). Likewise, provided that a plant is very small (or very large but composed of Conditions of Existence: Water versus Air flexible yet elastic materials), large surface areas can Any explanation for the body plan convergence among impose very small drag forces, since a unicellular plant and divergence within the various plant lineages is can move with the flow, while a very large plant can bend problematic. But it is fair to say that each plant lineage and twist to reduce its projected surface area toward reflects an independent ‘experiment’ in terms of how oncoming water (Niklas, 1994). Thus, since dehydration plant life evolutionarily adapted to its environment. Since is unlikely in an aquatic environment, the amplification of provides some of the strongest surface areas with respect to body volume evokes no circumstantial evidence for and since intense selection. divergence provides equally convincing evidence for Indeed, allometric analyses of unicellular algae reveal diversifying selection, it is reasonable to suppose that that cell surface area scales approximately as the 3/4- body plan convergent evolution reflects to the power of cell volume (Fig. 3). Noting that the scaling conditions of plant existence and that these conditions are exponent for surface area to volume is 2/3 for any series manifold and complex. of objects sharing the same geometry and shape (which 136 Gravitational and Space Biology Bulletin 17(2) June 2004

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 Significantly, computer models reveal that the 3/4 size or species differing in phyletic affiliation have scaling exponent typically observed for different different cell geometries and shapes and that either unicellular algal species is the maximum that can be geometry or shape changes as a function of absolute cell expected for the range of cell size, shape, and geometry size. 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 micro- hydrodynamic 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

Fig. 3. Effect of changes in cell surface area and cell volume unicellular or colonial body plan. on the capacity to absorb nutrients from the surrounding Body size and shape, therefore, are not intrinsically medium and to capture sunlight. A. Cell surface area plotted limited in the aquatic environment provided that against cell volume for a variety of algal species drawn from organized growth achieves morphologies that abide by diverse lineages shows a log-log linear trend with a slope less some very simple biophysical and geometric rules. Since than unity (i.e., surface area decreases with respect to cell the unicellular, colonial, and multicellular body plans are volume with increasing size. B. Quotient of cell surface area each capable of developmentally adjusting surface area and volume plotted against cell volume for algal taxa in A. This with respect to body volume, it is not surprising that these quotient is highest for the smallest cells and decreases in a log- body plans are represented by numerous species in log linear manner with increasing cell size (volume). C. Absorption cross section (reflects the capacity of cells to harvest virtually every major algal lineage. sunlight) for spherical cells differing in diameter (see insert) However, in the absence of mitigating features (e.g., plotted against the wavelengths of visible (and cuticles, roots, and stomata) most of which necessitate a photosynthetically useable) light. The light harvesting capacity multicellular body plan, large surface areas with respect for spherical cells decreases with increasing cell diameter. to volumes are detrimental for a terrestrial (or more Adopted from Niklas (1994). properly speaking, an aerial) plant (Nobel, 1983). As Gravitational and Space Biology Bulletin 17(2) June 2004 137 K.J. Niklas – Plant Body Plan Evolution body parts are increasingly elevated above ground, they an archegonium (a specialized multicellular - become more susceptible to dehydration, first, because producing structure) (Graham, 1993). Since cladistic the distance (and thus the transport time) between a analyses currently identify multicellular charophycean hydrated substrate and evaporative body parts increases, algae as the sister group to the land plants and since all of and, second, because wind speeds tend to increase these algae lack a multicellular diploid (‘sporophyte’) exponentially from the ground surface to the ambient generation, it is reasonable to suppose that the wind speed limit (Vogel, 1981; Nobel, 1983). Plants that embryophyte sporophyte may represent an evolutionary ‘hug’ their substrates or grow in tight clumps as do many innovation that appeared during or very shortly after plant bryophytes can reduce their individual rates of water loss life made it onto land. The benefits of a multicellular and they can alter their micro-aerodynamic environments diploid phase are nonetheless clear –– it amplifies the favorably in much the same manner as do aquatic colonial number of cells that can undergo meiosis and thus or multicellular plants. But it is nonetheless generally increases the number of haploid individuals that a true that a truly aerial plant requires a multicellular body fertilization event can produce. 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 ) (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 Fig. 4. Morphological and anatomical differences between the selecting those species that could cope with brief periods gametophyte (A–C) and sporophyte (D–E) of the moss of exposure. The inverse relation between body size and Polytrichum commune. A. Gametangiophore (reproductive rates suggests that the survivors were probably axis of gametophyte, g) bearing sporophyte with a single comparatively small, short-lived, and genomically sporangial capsule (c) elevated by a -like seta (s). B. mutable. Phyllid (leaf-like lateral appendage) of gametophyte with ribbed Indeed, the oldest known land plant sporophytes were adaxial surface (r) and ‘mid-rib’ of conducting tissues (m). C. small, anatomically simple, and produced cutinized spores Portion of cross section through ‘leafy’ gametangiophore showing complex tissue differentiation reminiscent of vascular capable of surviving exposure to the air (Banks, 1975; stem (hydrome, h; leptome, l). D. Longitudinal cross Chaloner and Sheerin, 1979; Taylor and Taylor, 1993). section through sporophyte capsule showing central chamber of These sporophytes had cylindrical bifurcating axes that sporogenous tissue (st) surrounding the central columella (c) may have had a cuticle capable of reducing the rate of enclosed apically by the operculum (o) . E. Distal view of water loss from exposed surfaces. Nothing is currently sporangium lacking the operculum and revealing the peristome known about their corresponding gametophytes, but these (p). were likely prostrate or short multicellular life forms, since one of the shared ancestral conditions of all extant But, from a body plan perspective, the embryophyte embryophytes is a diplobiontic life cycle (an alternation life cycle is schizophrenic –– the reproductive roles between a multicellular diploid sporophyte and a played by the gametophyte and sporophyte generations multicellular haploid gametophyte generation) involving are very different and require different body plan features 138 Gravitational and Space Biology Bulletin 17(2) June 2004

K.J. Niklas – Plant Body Plan Evolution (Niklas, 1997, 2000). The reproductive tasks of the to phloem tissue for much the same reasons (Bold and gametophyte are to produce gametes and to retain, Wynne, 1978). 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. Fig. 5. Allometric (size-dependent) relations for plant Viewed from the perspective of form, function, and growth rates and body mass (A) and for light harvesting capacity (B) across unicellular and multicellular plants. A. environmental context, the morphology and anatomy of Annual average plant growth rates plotted against body mass is the gametophyte and sporophyte generation of land plant described by a log-log linear curve with a slope ~ 3/4. B. species have been evolutionarily driven down separate Annual average plant growth plotted against light harvesting and often highly divergent pathways. Yet another wedge capacity (gauged by algal cell pigment concentration or between the two is that only one of the two multicellular standing leaf per plant) is described by two log-log generations in the embryophyte life cycle can be linear curves, each of which has a slope ~ 1. Adopted from reasonably expected to manifest indeterminate growth in Niklas and Enquist (2001). size, since both are physically attached and inexorably physiologically interdependent such that continued The of Body Plans growth of one will have negative effects on the other Morphological and anatomical changes occur as most (Niklas, 1997). Among extant nonvascular embryophytes organisms continue to grow in size. Likewise, (mosses, liverworts, and hornworts), the gametophyte evolutionary increases in the adult size of related species generation is typically long-lived and indeterminate in are typically attended by changes in anatomy and body growth, whereas the sporophyte generation is short-lived geometry or shape. Curiously, broad interspecific and determinate in growth (Bold, 1967). The reverse is comparisons among phyletically highly diverse organisms true for most vascular plant species. Indeed, among the reveal strikingly similar patterns of adjustment. Indeed, seed plants, the gametophyte generation has been reduced some of these patterns are ‘invariant’ for plants and to microscopic size (e.g., angiosperm pollen grains and animals. One of the better known of these ‘invariant’ megagametophytes). patterns is the scaling of overall growth rates with respect The ‘wedge’ between the size and continued growth in to body mass (Niklas and Enquist, 2001). Across size of the gametophyte and sporophyte generations of unicellular and multicellular animals and plants, annual embryophytes has had a profound effect on anatomy as growth rate scales, on average, as the 3/4–power of body well. Continued growth in size attended by the vertical mass (Fig. 5 A). Perhaps less well known is the scaling of elevation of body parts biophysically requires the bulk plant growth rates with respect to the capacity of the transport of water and thus increasingly specialized tissue individual to harvest light. Across algae and aquatic as systems, since rates of nutrient passive diffusion are too well as terrestrial vascular plants, this relationship is slow to accommodate the metabolic needs of large plants isometric, that is growth rates scale as the 1–power of (Nobel, 1983). The hydrome and leptome of some light harvesting capacity measured as algal cell pigment mosses are functionally analogous and oft times concentration or standing leaf biomass per individual morphologically strikingly similar to xylem and phloem tracheophyte (Fig. 5 B). Remarkably consistent scaling tissues of vascular plants (see Fig. 4 C). By the same relations are also observed for seed plant leaf, stem, and token the ‘trumpet cells’ of some large marine brown root biomass (Enquist and Niklas, in press). Across a algae, which supply nutrients to light-starved cells well broad spectrum of spermatophytes, leaf biomass per below the water-air interface, are functionally analogous 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 of stiffer and proportionally less dense plant tissues for the isometric relationship (Fig. 6 A). principal stem stiffening agent. Adopted from Niklas (1992). Anatomical allometric trends are also evident. For example, the relationship between plant height and stem Theories abound to explain these and other allometric diameter is curvilinear even when the data are log- trends, but none has escaped well reasoned criticism. transformed. Thus, across all species, no unique scaling Most of these theories emphasize the scaling relationship exponent exists for this relationship (Fig. 6 B). Yet, between total body surface area and volume. Plant biomechanical calculations show that the density-specific surface area (whether that of a unicellular or multicellular stiffness of the tissues providing the bulk of stem plant) is a reasonable surrogate measure of the ability of mechanical support has significantly increased among the the individual organism to exchange mass and energy largest of the living representatives of each major land with its external environment; body volume is a plant reproductive grade (i.e., bryophytes, pteridophytes, reasonable measure of the metabolic demands of the and seed plants) (Niklas, 1994). Likewise, the fossil organism. Since the density of plant materials is nearly record as well as comparative studies among extant constant across materials and organisms, body volume is species highlights a number of important allometric trends a comparatively good measure of body mass. In this in relating to the capacity to resist wind- crude sense, the relationship between surface area and throw. 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 Fig. 6. Allometric (size-dependent) relations among leaves, the vast majority of plant species shares the same basic stems and roots of tree species differing in size (A) and plant height and stem (or moss sporophyte) diameter (B). A. Leaf physiological requirements for survival, growth, and biomass plotted against stem biomass is described by a log-log successful reproduction. linear curve with a slope ~ 3/4; root biomass plotted against stem biomass is described by a log-log linear curve with a slope Concluding Remarks ~ 1. B. Plant height plotted against stem diameter is log-log We know comparatively little about the early nonlinear and ‘convex’ (indicating plant height decreases with evolutionary history of most plant lineages, in part respect to interspecific increases in stem diameter). Solid lines because the fossil record is highly fragmentary and denote hypothetical maximum plant height provided that each because the assignment of many fossils is problematic plant stem is composed exclusively of a single tissue (P = owing to extensive morphological and anatomical parenchyma, X = primary vascular tissues, S = sclerenchyma; W = wood). Interspecific increases in plant height are attended convergence. Detailed developmental studies of many by anatomical differences codified by the evolutionary adoption important taxa are also lacking. Algal molecular taxonomy and are still in their 140 Gravitational and Space Biology Bulletin 17(2) June 2004

K.J. Niklas – Plant Body Plan Evolution infancy Likewise, with all the emphasis on vascular land as the establishment of symplastic continuity among plant evolution and biology, especially that of seed plants, neighboring cells, has evolved in the cyanobacteria, we are still also remarkably ignorant about the details of which are believed to be the modern-day descendants of non-vascular and relictual vascular non-seed plants (the the prokaryotes from which the first chloroplasts evolved bryophytes and pteridophytes). For all these reasons, this (Margulis, 1992; Maddock, 1984; Gober and Margues, treatment of the evolution of plant body plans is 1995). This possibility suggests that the genetic and unavoidably speculative and incomplete. 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