Plant Body Plans

Annals of Botany 85: 411±438, 2000doi:10.1006/anbo.1999.1100, available online at http://www.idealibrary.com on

REVIEW

The Evolution of Plant Body PlansÐA Biomechanical Perspective

KARL J. NIKLAS*

Department of Plant Biology, Cornell University, Ithaca, New York 14853, USA

Received: 13 October 1999 Returned for revision: 11 November 1999 Accepted: 29 November 1999

of time.

Sheerin, 19

0305-7364/0

* Fax �1 6

De®ning `plants' inclusively as `photosynthetic eukaryotes', four basic body plans are identi®able among plantlineages (unicellular, siphonous, colonial and multicellular). All of these body plans occur in most plant lineages,but only the multicellular body plan was carried onto land by the embryophytes. Extensive morphological andanatomical homoplasy is evident among species with di�erent body plans. This is ascribed to the facts that theacquisition of nutrients and radiant energy is a�ected by plant body size, shape and geometry, and that, with theexception of the unicellular body plan, each of the other body plans involves an òpen and indeterminate' ontogenycapable of modifying body size, shape and geometry regardless of how organized growth is achieved. In terms ofunicellular species, the available data indicate that size-dependent variations in surface area, metabolic constituents(e.g. photosynthetic pigments), and reproductive rates limit maximum body size in nutrient poor habitats or thosethat change rapidly or unpredictably. This maximum size can be exceeded in more stable niches by either thecooperation of conspeci®c cells sharing a common extracellular matrix (i.e. the `colonial' body plan) or by repeatedmitotic cellular division associated with sustained cytoplasmic (symplastic) continuity (i.e. multicellularity). Thesiphonous plant body plan may have been evolutionarily derived from a unicellular or multicellular ancestral lifeform. Each of the plant body plans is reviewed in terms of its biomechanical advantages and disadvantages. Variantsof the multicellular body plan, especially those of the Chlorophyta, Charophyta, and Embryophyta, are given specialemphasis. # 2000 Annals of Botany Company

Key words: Algae, biomechanics, body plans, body size, embryophytes, evolution, multicellularity, plants.

. . . all organic beings have been formed on two great lawsÐUnity of Type and the Conditions of Existence. By unity of type ismeant that fundamental agreement in structure, which we see inorganic beings of the same class, and which is quite independent oftheir habits of life. The expression of conditions of existence . . . isfully embraced by the principle of natural selection [which] actsby either now adapting the varying parts of each being to its organicconditions of life; or by having adapted them in long-past periods

ÐCharles Darwin

INTRODUCTION

Much has been written about the initial appearance andsubsequent evolution of metazoan body plans, particularlyin terms of the great Cambrian èxplosion' and the attend-ing evolutionary debut of multicellular animal body plansduring a comparatively brief period of time (see Gould,1989; Valentine, Jablonski and Erwin, 1991; Lipps andSignor, 1992; Valentine, 1995; Ra�, 1996; Miller, 1997;Martindale and Henry, 1998; Knoll and Carroll, 1999). Incontrast, the evolution of body plans among plants, herede®ned as photosynthetic eukaryotes, has received com-paratively much less attention and has been discussedlargely in the context of the radiation of the early vascularland plants and their terrestrial non-vascular predecessorsduring early Paleozoic times (Banks, 1975; Chaloner and

79; Graham, 1993; Taylor and Taylor, 1993;

0/040411+28 $35.00/00

07-255-5407, e-mail [email protected]

Stewart and Rothwell, 1993; Niklas, 1997). This focus hassigni®cantly advanced our understanding of the evolutionof the embryophytes, but it has largely ignored a complexantecedent history during which di�erent body plansevolved within and among the genetically distinct butmorphologically homoplasic aquatic plant lineages, collect-ively called the àlgae' (Bold and Wynne, 1978; Grahamand Wilcox, 2000). This history involved evolutionarymodi®cations in a variety of body features that undoubt-edly pre®gured to some degree the highly stereotypedembryophyte body plan (see Graham, 1993). For thisreason, no synoptic discussion of plant body plan evolutionis possible without reference to those still representedamong the modern-day algal lineages that share the samegrade level of cytological and physiological organization.

Unlike those of the metazoans, the body plans ofplants are di�cult to categorize or de®ne. Setting asidethe similarities among unicellular (uni-nucleate) or colonialplant species, which are arguably trivial owing to theirtypically simple geometries and shapes, extensive morpho-logical and anatomical convergence is evident among meta-phytes, so much so that it is often impossible to distinguishbetween species drawn from diverse lineages on the basis oftheir general appearance, size, or internal structure (Bold,1967; Bierhorst, 1971; Bold and Wynne, 1978; Gi�ord andFoster, 1989; Niklas, 1997; Graham and Wilcox, 2000). Theperspective taken here is that plant BauplaÈne are far morepro®tably discussed in terms of how organized growth is
achieved and how di�erent tissue fabrics are used to
# 2000 Annals of Botany Company

to bias against some of the following.

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construct the plant body. Importantly, most of these bodyplans have an òpen and indeterminate' ontogenyÐoneinvolving multiple growing points and persistent cellulardivisions throughout the lifetime of the individual suchthat adult size, geometry and shape are not necessarilydevelopmentally pre®gured in the juvenile condition (Esau,1965). Arguably, this ontogeny permits morphological andanatomical convergence as well as divergence amongphyletically otherwise divergent plant lineages because itholds the potential to bypass many of the developmentalconstraints imposed on metazoans that often have a `closedand determinate' ontogeny.

Developmental `constraints' are important to body planevolution (Waddington, 1957; Gould, 1977; Wimsatt andSchank, 1988; see, however, Ra�, 1996). For plants, one ofthe most obvious of these is the phyletic legacy of a cell wall,which evolved independently many times among the variousplant lineages and whose mode of deposition and materialproperties profoundly in¯uence how cell size and shape arefree to change (Green, 1960; Mark, 1967; Preston, 1974;Cooke and Lu, 1992; Niklas, 1992). Perhaps more subtle arethe various developmental constraints that in¯uence therelationship between the body surface areas, volumes, andcytoplasmic machinery of cells. Nowhere are these moreclearly expressed than among plant species sharing theunicellular plant body plan, which is typically determinatein growth in size, geometry and shape (Bold and Wynne,1978). The data reviewed here show that physiological andreproductive rates fail to increase in pace with interspeci®cincreases in body (cell) size. This feature of the unicellularplant body plan may be legitimately considered a `develop-mental constraint' operating at the level of size-dependentvariations in the intracellular concentrations of importantcellular components (e.g. photosynthetic pigments). Indeed,allometric (size-dependent) variations suggest that an ùppersize limit' exists for the unicellular plant body. If so, thennatural selection probably favoured multiple independentorigins of other body plans that permitted an increase inoverall size by the addition of cells, each capable of optimalgrowth or reproductive rate.

If it is true that developmental constraints play animportant role in plant evolution, then it is equally true thatbiomechanical relationships have in¯uenced the evolutionof body plans at the cell, tissue, organ, and organismiclevels of organization (Wainwright et al., 1976; Speck andVogellehner, 1988; Cooke and Lu, 1992; Niklas, 1992, 1994,1997). Biomechanical limitations obviously exist for alltypes of organisms, since no life form can violate physicallaws or processes. For plants, which all perform essentiallythe same biological tasks to assure growth and repro-duction (light harvesting, nutrient acquisition and storage,etc.; see Nobel, 1983), these limitations are readily apparentin terms of quanti®able design considerations that emergewhen two or more tasks are performed simultaneously.These biomechanical `constraints' undoubtedly evokemorphological or anatomical reconciliations that scalewith respect to body size, geometry and shape rather thanwith how a particular body plan achieves its organizedgrowth. As a consequence, body plan diversi®cation within,

412 NiklasÐPlan

and convergence among, di�erent lineages become likely,

provided that development permits plants to assume a bodysize, geometry and shape convivial to survival in aparticular niche.

In the sections that follow, I brie¯y review the `body plan'concept in the context of the historical debate between `theunity of type' and the `conditions of existence'. This isfollowed by a brief discussion of the key features thatdistinguish the comparatively few basic plant body plans,which are de®ned on the basis of how organized growth isachieved and how, if present, di�erent tissue fabrics areused to construct the plant body. The remainder of thepaper is devoted to a discussion of each body plan in termsof its biomechanical advantages and `constraints'. Limitedspace allows for neither a detailed nor comprehensive treat-ment of each of these subjects, which can be only broadlyoutlined here.

Finally, in terms of phyletic a�liations, with the exceptionof our current understanding of the systematic relation-ships among the charophycean algae and their relationshipto the embryophytes (see Mattox and Stewart, 1984;Graham, 1993; Graham andWilcox, 2000), the phycologicaltaxonomy adopted throughout this paper is that of Bold andWynne (1978). This reference is based largely on morpho-logical rather than molecular information. Arguably, there-fore, it o�ers a conservative view of body plan di�erenceswithin each of the algal lineages (see Table 1), and thus tends

Body Plans

ÙNITY OF TYPE' VS . `CONDITIONSOF EXISTENCE'

The concept of the `body plan', layout, or Bauplan can betraced to the work of Georges Cuvier, Richard Owen, andother nineteenth-century comparative morphologists whoshowed that organisms can be classi®ed according to theirshared structural and anatomical traits, many or some ofwhich have no obvious connection to the ecological life-styles of the organisms sharing them (Mayr, 1982; see alsoWoodger, 1945; Brusca and Brusca, 1990). For example,trilobites and butter¯ies possess a bilaterally symmetrical,segmented body plan in which the ®rst few anteriorsegments are fused to form a head. These and other sharedtraits permit trilobites and butter¯ies to be groupedtogether along with other arthropods by virtue of a ùnityof type' that nevertheless achieves so great a diversity in its`conditions of existence' (e.g. aquatic, terrestrial, and aerialspecies) that many of the features characterizing arthropodscan be identi®ed in terms of their location and contributionto the body layout without compelling one to ascribe anadaptive role to each.

Although Cuvier, Owen, and others maintained thatthe `conditions of existence' were subordinate to the ùnityof type', Charles Darwin observed that many traits are aconsequence of descent from a last common ancestor thatare themselves the products of earlier, presumably adaptiveevolution. Darwin maintained that currently adaptive traitscan and do co-exist with highly conserved traits having noapparent adaptive purpose. He nonetheless maintained thatthe `conditions of existence' take priority over the ùnity of
type'. Darwin, like many others, was impressed by the

1995; Valentine and Hamilton, 1997).

TABLE 1. Distribution of body plans among the land plants (Embryophyta) and extant algal lineages (with the exceptionCharophyta, the systematics used here and throughout the text are based on Bold and Wynne, 1978)

MulticellularSiphonous Unicellular Colonial1 Filam. Pseudo. Parench.

Embryophyta ÿ ÿ ÿ �2 ÿ �3

Charophyta4 ÿ � � � � �Chlorophyta � � � � � �Chrysophyta � �5 � � � �Rhodophyta ÿ � � �6 �6 �6

Phaeophyta ÿ ÿ7 � � � �Pyrrhophyta ÿ � � ÿ ÿ ÿEuglenophyta ÿ � � ÿ ÿ ÿCryptophyta8 ÿ � � ÿ ÿ ÿ

Filam., ®lamentous (unbranched or branched); Pseudo., pseudoparenchymatous tissue construction; Parench., parenchymatous tissueconstruction.

1Aggregates of cells lacking cellular interconnections; excludes `volvocine algae' that have cellular interconnections early in development or thatmaintain them when mature (e.g. Pandorina and Volvox, respectively).

2Generally expressed in the gametophyte generation.3Expressed in the gametophyte and sporophyte generations of all species.4Sensu Mattox and Stewart (1984); includes Charales, Coleochaetales and Zygnematales.5Includes amoeboid (rhizopodial) types, and the Bacillariophyta.6In the form of secondary pit-connection formation.7Presumably either lost over the course of evolution or represented by a heterokont currently assigned to another phylum.8Molecular evidence indicates this is likely a polyphyletic group.

NiklasÐPlant Body Plans 413

remarkable `match' between body traits and the ecologicalconditions in which each particular organism lives andreproduces. Clearly, his theory of natural selection arguedin favour of the adaptive role of the majority rather than theminority of body traits.

It is undeniable that some shared ancestral traits havebeen conserved long after their initial adaptive signi®cancehas vanished. The coelom, which evolved more than once,may have been an adaptation for burrowing by soft-bodiedanimals, but its current function in the vertebrate bodyplan is radically di�erent from that of any of its presumedantecedent functions. Indeed, assertions that otherwisediverse organisms share a common ancestry are basedtypically on the presence of ancestral traits. The real issue isnot whether some body plan traits are conserved but whysome traits are lost, whereas others are not. Flightless birdshave reduced ®ght muscles and wings. Yet, all birds developfeathers and a beak. Parasitic angiosperms have reducedleaves, stems, or roots, or lack some of these organsentirely, but they all retain the capacity to produce ¯owersand vascular tissues.

The typical explanation for the conservation of ancestralbody plan traits is the presence of pivotal developmentalprocesses whose mutation would be di�cult or imposs-ibleÐprocesses so basic to how an organism achieves itsorganized growth that any signi®cant deviation wouldresult in death or severe impairment. It is evident that`developmental constraints' exist and play an important rolein the conservation of some traits. The so-called spiraldeterminate cleavage of many planktotrophic spiralianspecies so rigidly casts the fate of each embryonic cellearly in the four- and eight-cell stage of embryo develop-ment that it is di�cult (although not impossible) to imagine
that mutations causing this embryology to deviate from the
norm would be anything but lethal. Among the diploblasticeumetazoa, the outer body wall, sensory and nervoustissues, and associated structures are derived from ecto-dermal cell lineages, whereas the archenteron and theorgans that develop along with it are derived fromendodermal cell lineages. Likewise, among all triplobasticanimals, a third germ layer, the mesoderm, develops fromeither ectodermal or endodermal cell precursors to give riseto muscles, muscular organs, gonadal tissues and otherinternal organs. Thus, developmental constraints arecommonly evoked to explain why some animals, likemolluscs, annelids, and arthropods, retain the same generalbody plan (characterized by the formation of a mouth fromthe blastopore and a coelom from splits in the mesoderm).Although `direct development' frequently occurs in avariety of animal lineages (see Ra�, 1996), the traditionalview of animal body plan evolution maintains that nearlyall are achieved as a result of well de®ned embryologiesthat give rise to a highly conserved set of body plans (theùnity of type'). Indeed, animal body plans are generally soconservative that many zoologists believe that all modern-day animal phyla trace their ancestry back to a last common(protist) ancestor (see Wainright et al., 1993; Valentine,

PLANT BODY PLANS

The evolution of plant body plans is far more complex thanthat of animals because the organisms called plants arepolyphyletic (Schlegel, 1994; Graham and Wilcox, 2000).Rather than constituting a single clade that can be tracedback to a single last common ancestor, plants (i.e. eukary-otic photoautotrophs) have multiple evolutionary origins
presumably as a consequence of primary endosymbiotic

FIG. 1. Convergent evolution among coralline red (A, B) and greenalgae (C, D). A, Corallina mediterranea. B, Bossiella sp. C, Penicillus

capitatus. D, Halimeda opuntia.

t Body Plans

events, giving rise to lineages like the Chlorophyta, or as aresult of secondary endosymbiotic events, giving rise toothers like the euglenids and chromists (Cavalier-Smith,1992; McFadden and Gilson, 1995; Wastl et al., 1999). Thisearly phase in plant evolution, which involved extensivelateral gene transfer among pro- and eukaryotic unicellularorganisms, was followed by one characterized by increasedgenetic isolation and divergence. By late Mesoproterozoicor early Neoproterozoic time, the major radiation eventsdistinguishing modern-day eukaryote lineages had alreadytaken place (Knoll, 1995; Porter and Knoll, 2000).

Plants can be thus classi®ed and sorted into di�erentlineages based on molecular, cellular, or ultrastructuralfeatures. These and other criteria support the generally heldview that each algal lineage traces its ancestry back to aunicellular ancestral organism, that colonial and multi-cellular life forms have evolved independently many times,that the land plants (embryophytes) and the charophyceanalgae share a last common ancestor, and that the embryo-phytes are a monophyletic group. However, it is strikinglyevident that the general appearance, size, or growth form ofplants cannot be used to distinguish the various lineages.Setting aside the obvious if somewhat trivial phenotypicsimilarities among the comparatively simple unicellular orcolonial species found in each of the major algal lineages,it is commonplace to ®nd plants with ®lamentous,membranous, foliar, tubular, kelp-like, and coralline lifeforms in each of the red, green, and brown algal clades(Fig. 1). Some acellular (siphonous) species, like those ofCaulerpa, can attain body lengths in excess of 20 m and ageneral morphology strikingly reminiscent of the rhizoma-tous growth habit of the vascular land plant without bene®tof multicellularity (Fig. 2). General appearance and sizealso belie very di�erent tissue constructions and develop-mental capacities. The non-vascular blade-stipe-holdfastarchitecture of some marine brown algae is constructedwith an intercalary meristem (e.g. Agarum and Macrocystis)and yet is remarkably similar to the leaf-stem-rootcon®guration of the vascular land plants. By the sametoken, the arborescent growth habit of many present-dayand extinct vascular plants which is achieved by virtue ofsecondary tissues produced by the vascular and corkcambia (e.g. Lepidodendron, Calamites and Pinus) ismimicked by monocot and fern species lacking cambia(e.g. Cocos nucifera and Cyathea medullaris).

Mindful of the extensive morphological and anatomicalhomoplasy among the various plant lineages, plant bodyplans are far more easily distinguished on the basis of howthey achieve their organized growth and, if present, theirbasic tissue constructions. This approach identi®es onlyfour basic body plansÐthe unicellular, colonial, siphonousand multicellular body plan. These can be distinguished onthe basis of a few basic developmental processes or events(Fig. 3): (1) the presence or absence of vegetative cytokinesisdetermines whether the plant body is based on a uni- ormulti-nucleate cellular plan (e.g. Chlamydomonas or Bryop-sis); (2) the separation of cell division products or theiraggregation by means of a common extracellular matrix, pitconnections, shared loricas, stalks, etc. determines whether

414 NiklasÐPlan

the body plan is unicellular or colonial (e.g. Calcidiscus or

Phaeocystis); (3) indeterminate growth of the multinucleatecell results in the siphonous body plan (e.g. Bryopsis andCaulerpa); and (4) symplastic continuity among cells duringand after cell division by means of `cytoplasmic bridges',plasmodesmata, etc. establishes the multicellular body plan(e.g. Volvox and Polytrichum).

The multicellular body plan has three basic variants thatcan be described morphologically, albeit not mechanisti-cally, in terms of the number of planes of cell division(Fig. 3): when restricted to one plane or orientation,unbranched ®laments can be formed (e.g. Spirogyra);when con®ned to two orientations, cell division can giverise to branched ®lamentous, monostromatic, or pseudo-parenchymatous tissue constructions (e.g. Stigeoclonium,Volvox and Ralfsia, respectively); and, when cell divisionoccurs in all three planes, a multicellular body layout ispossible, which can simultaneously manifest a ®lamentousand parenchymatous construction (e.g. Fritschiella). Sinceeach of these three multicellular variants can involvedi�use, trichothallic, intercalary, or apical cell divisions,or some combination of all four, a large number of multi-cellular body plan variants can be codi®ed (i.e. 3 celldivision planes � 5 meristematic locations � 15 variants deminimis), although the usefulness of doing so is question-able. Although a number of growing point (meristematic)
characteristics collectively in¯uence whether a variety of

FIG. 2. Representative morphologies of the siphonous green alga Caulerpa (A±D) and infrastructure of trabeculae in the symplast (E, F).A, C. chemnitzia. B, C. ¯oridana. C, C. racemosa var. clavifera. D, C. racemosa. E and F, Longitudinal and transverse views of trabeculae in

àssimilator' (vertical portions of plant body) and `rhizome', respectively.


morphological and anatomical features are achieved in aparticular body part or plan (e.g. the duration of activityand the number of cells involved at each location, as well asthe extent to which cells, tissues or organs di�erentiate ordi�er in symmetry, number, etc.; see Fig. 4), none of thesefeatures is considered here to be especially relevant to thefundamental distinctions that can be drawn among the fourbasic plant body plans.

This body plan classi®cation scheme draws sharpattention to the extent to which body plans have diversi®edwithin or converged among the various plant lineages andhow they have become con®ned in number in evolutionarily
more derived groups, such as the Charophyta and Embryo-
phyta (Table 1). For example, all four BauplaÈne occur in theChlorophyta and Chrysophyta, two of the most species-richplant phyla. The unicellular body plan, which is presum-ably the ancestral condition in each algal lineage, is absentonly in the Phaeophyta, whereas the colonial body plan isnot represented among embryophyte species. The multi-cellular body plan occurs in all but three algal lineages eachof which presumably evolved as a consequence of second-ary endosymbiotic events. Unlike the Charophyta, whichhave unicellular and colonial representative species (e.g.Stichococcus and Chlorokybus, respectively), all embryo-phytes are multicellular and have the capacity to fabricate
parenchymatous tissue by means of apical, intercalary, or

karyokinesis+ cytokinesis(uni-nucleate)

-cytokinesis(multi-nucleate)

determinategrowth

siphonous

indeterminategrowth

colonial

unicellular

multicellular

no

sym

plas

tic

con

tin

uit

y

no

aggr

egat

ion

aggr

egat

ion

sym

plas

tic

con

tin

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Location of growthdiffuse trichothallic intercalary apical

unbranched filaments

branched filaments, monostroma,pseudoparenchyma

parenchyma

Pla

ne

of

cell

div

isio

n

one

two

thre

e

FIG. 3. Basic plant body plans (unicellular, colonial, siphonous and multicellular), their de®ning features, and methods of achieving organizedgrowth. The unicellular body plan is generally considered the most ancient among all plant body plans and is characterized by the separationof cell division products after cytokinesis; uni- or multi-nucleate variants occur depending on whether cytokinesis keeps pace with karyokinesis(e.g. the uni-nucleate chlorophyte Chlamydomonas and the multi-nucleate chrysophyte Botrydiopsis, respectively). The colonial body plan is acollection of uni- or multi-nucleate cells aggregated together but lacking symplastic continuity among cells (e.g. the chrysophyte Synura and thechlorophyte Hydrodictyon, respectively). The unicellular and colonial body plans are determinate in cell size (shown in shaded area), although theoverall size of a colony may increase by the addition of cells. The siphonous and multicellular body plans are indeterminate in their growth in size(unshaded area). The siphonous body plan consists of a single multi-nucleate cell (e.g. Caulerpa). The multicellular body plan consists of uni- ormulti-nucleate cells that maintain symplastic continuity after cytokinesis (e.g. the unbranched ®lamentous chlorophytes Ulothrix and Urospora,respectively). The multicellular body plan can achieve organized growth by means of di�use, trichothallic, intercalary, or apical cell divisionsinvolving one, two, or three orthogonal planes of cell division. Cell division restricted to one plane produces unbranched ®laments; cell divisioncon®ned to two planes constructs branched ®laments, monostroma (sheets of cells or hollow structures one-cell thick), or pseudoparenchyma; cell

division in three orthogonal planes can be used to construct parenchymatous tissues.

416 NiklasÐPlant Body Plans

di�use meristematic activity. Among the land plants, the®lamentous variant of the multicellular body plan may beexpressed transiently in the sporophyte generation (e.g. the®lamentous embryo stage of seed plants), among free-living gametophytes (e.g. the mosses Buxbaumia and Poly-trichum), or not at all (e.g. the liverworts Scapania nemerosaand Conocephalum). Likewise, the siphonous body planis expressed brie¯y among embryophytes (e.g. the `free-cellular' condition of endosperm).

In this sense, the embryophyte body plan, especially thatof the sporophyte generation, evinces the greatest ùnity oftype' among all the plant lineages. This may re¯ect a`founder e�ect' when the last common ancestor of modern-
day embryophytes successfully invaded the terrestrial land-
scape presumably during Ordovician times. If so, then theland plants and the eumetazoa a�ord the best candidateswith which to study the broad e�ects of developmentalconstraints on body plan evolution. Alternatively, theembryophyte body plan may confer the highest relative®tness in terrestrial habitats, and thus may be the result ofextreme directional (canalizing) selection. It is noteworthythat the capacity to form parenchyma by means of a varietyof meristematic con®gurations and locations permits theconstruction of all multicellular tissue fabrics in the sameorganism, ranging from unbranched and branched ®la-ments to parenchymatous tissues (e.g. moss gametophyteprotonema and phyllids, respectively). Thus, the `conserva-
tive' nature of the embryophyte body plan may be more

A. Location of growth

B. Growing point characteristics

C. Differentiation of parts, e.g.

D. Body appearance, e.g.

branched filaments,pseudoparenchyma

parenchyma

Type:

Number:Duration:

intercalary apical

Div

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lan

e

thre

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o

unicellularprimary

onedeterminate

multicellularsecondary

> oneindeterminate

Cells:Tissues:Organs:

primary walls secondary wallsepidermis, storage, conducting

leaf, axis, attachment

symmetry:redundancy:correlation:form:

radial, or dorsiventralmany or few organs

allocation patterns; allometryrhizomatous, arborescent

FIG. 4. Examples of the multicellular body plan constructed from intercalary or apical meristematic activity involving two or three orthogonalplanes of cell division (A) and some developmental features in¯uencing the general appearance of the plant body (B±D). A, Two or threeorthogonal planes of cell division in intercalary or apical meristematic regions can be used to construct branched ®laments (or pseudo-parenchymatous tissues) and parenchymatous tissue, respectively. Some taxa are represented by species composed of branched ®laments(organized into pseudoparenchymatous tissues) or parenchyma (e.g. the chlorophyte Coleochaete); some taxa have both intercalary and apicalmeristems (e.g. the sporophyte of the moss Polytrichum). B, Growing point characteristics in¯uence cellular con®guration of meristems (meristemscomposed of one or many cells), whether new meristems develop later in ontogeny (primary vs. secondary meristems), and the number ofmeristems and their duration of growth. Some taxa have a single apical meristem composed of a single apical cell whose duration of growth isdeterminate (e.g. Polytrichum sporophyte). Other taxa have multiple apical meristems composed of many cells whose duration of activity isindeterminate (e.g. the phaeophyte Fucus). C and D, Patterns of cell, tissue, or organ di�erentiation and a variety of allometric phenomena

in¯uence in part the general appearance and internal structure of the multicellular plant body.


apparent than real. It undeniably imposes no barrier to thesuccessful exploitation of terrestrial habitats, as is evidentby the great morphological and anatomical diversity ofmodern embryophytes whose species number exceeds thatof all algal lineages combined.

In general, the body plan classi®cation scheme presentedhere does not drive a deep conceptual wedge among thevarious life-forms or `generations' that participate in thesexual life cycle of individual species. For example,although most ectocarpalian algae have an isomorphicalternation of generations, divergent gametophyte and
sporophyte morphologies are reported for some species
(e.g. Ectocarpus, Feldmannia, and Gi�ordia species). Yet,both generations in the life cycle of all ectocarpalian speciesshare a ®lamentous body plan. Likewise, despite thedramatic morphological disparities seen among the haploidand diploid generations in the triphasic life cycle of¯orideophycean algae (i.e. the diploid carposporophyteand tetrasporophyte, and the haploid gametophyte), all ofthese life forms share a branched ®lamentous body plan,just as the haploid gametophytes and diploid sporophytesof embryophytes share a multicellular body plan. There arenonetheless some exceptions to the uniformity in the body
plans of the di�erent life forms in the life cycles of some

t

species. Kelps have ®lamentous gametophytes andparenchymatous sporophytes, whereas some unicellularhaptophytes have a branched, ®lamentous Apistonema-stage in their life cycle (e.g. Pleurochrysis).

In general, however, the body plans seen in the sameplant life cycle are similar, paralleling what is typically seenamong the animals. Thus, insect juveniles often departmorphologically and anatomically from their correspond-ing adult forms, especially among holometabolic species,which undergo a profound metamorphic molt associatedwith quiescent pupation. However, like plants with lifecycles involving two generations di�ering in size, externalappearance, tissue construction, etc. all morphs in the insectlife cycle share the same general body plan (characterizedby bilateral symmetry, paired segmental coelomic bodycompartments, a contractile heart, and a nervous system

418 NiklasÐPlan

with a double nerve trunk and segmental ganglia).

`CONDITIONS OF EXISTENCE' AND PLANTONTOGENY

It is apparent that the disparity among BauplaÈne does notincrease dramatically as comparisons are drawn amonghigher taxonomic ranks, since all four plant body planshave evolved independently in many plant lineages(Table 1). This suggests that plant evolution is moreresponsive to the `conditions of existence' than con®nedby the ùnity of type', and, in turn, that `developmentalconstraints', which undoubtedly exist for all organisms,may be less prevalent in plant than in animal development.

This supposition is consistent with how the majority ofplants grow and develop. With the exception of unicellularuni-nucleate species, few plants are determinate in growthin size (e.g. Volvox and Arabidopsis) and this ontogenyappears to be a highly derived condition for the multi-cellular body plan. In contrast, most multicellular plantsachieve their organized growth by means of di�use, tricho-thallic, intercalary or apical cellular divisions at growingpoints that can remain active throughout the lifetime of theindividual. This òpen and indeterminate' ontogeny a�ordsan individual the opportunity to adaptively adjust its size,shape, or internal structure to its local environmentalconditions and to changes in these conditions as theindividual continues to grow during its lifetime. It alsoprovides each species with a heritable degree of phenotypic`plasticity' that allows conspeci®cs to assume di�erentmorphologies or anatomies depending on local environ-mental conditions.

The capacity to developmentally modify shape andinternal structure by virtue of òpen and indeterminate'growth is evident even among acellular species. Caulerpaspecies growing in wave-swept, high-energy environmentshave a `dwarfed' morphology and produce an internalsystem of cell wall extensions forming a mechanicallyresilient and strong beam-like infrastructure that is far moreextensively developed than that found in conspeci®cs withmore `luxuriant' morphologies growing in less mechanicallyenergetic habitats. In this sense, the morphology andanatomy of plants, regardless of whether they are acellular
or multicellular, are not pre®gured as uniformly or precisely
as they are for animals, the majority of which are charac-terized by the `closed and determinate' ontogeny.

The importance of the òpen and indeterminate' onto-geny of most plants takes on added signi®cance when weconsider how these organisms manufacture their livingsubstance and how this mode of life is largely dependent onform and appearance rather than on how the plant bodyachieves its organized growth. Unlike animals, whichcapture their prey or graze on plants in a variety ofdi�erent ways, all photosynthetic eukaryotes, regardless oftheir phyletic a�liation or particular ecology, requireessentially the same resources for growth and reproduction(i.e. light, water, atmospheric gases, minerals, and space).The acquisition of these resources is not intrinsicallydependent on the behaviour or characteristics of other lifeforms, and, perhaps for this reason, plant life is moredependent on and attuned to abiotic than biotic factors.Importantly, the ability to acquire the resources essentialfor growth depends on the external surface area of the plantbody, some of which is internalized to reduce tissuedehydration (e.g. aerenchyma). Water, minerals and atmo-spheric gases are absorbed from the external environmentthrough cell walls directly exposed to these substances.Irradiant energy is also intercepted and thus primarilyabsorbed by the body surface where chloroplasts aregenerally positioned. The body surface is also used todischarge a variety of metabolic products, particularly inthe aquatic environment. The magnitude of body surfacearea thus provides a reasonable morphometric measure ofthe capacity to absorb and exchange energy and mass withthe external environment.

Likewise, body volume provides a very indirect measureof metabolic capacity, nutrient demand, and the capacity(or need) to translocate materials. Here, `volume' refers tothe amount of the living substance in the plant body (i.e.the symplast). Clearly, there is certainly metabolism outsidethe protoplast membrane (e.g. enzymatic restructuring ofthe cell wall) as well as within vacuoles (Raven, 1997).However, the metabolic events in these compartments maybe viewed as qualitatively di�erent from those that occurwithin the symplast. A meaningful calculation of `volume',therefore, includes neither the cell wall infrastructure and¯uid-®lled spaces (i.e. vacuoles and the apoplast) normetabolically ìnert' internal or external materials (e.g.crystals and mucilage).

If body surface area to volume ratios are adopted ascrude surrogate measures of the plant body àcquisition anddemand ratio', then simple analytical geometry shows that aunicellular, ®lamentous, colonial, or any other plant bodyplan can achieve di�erent or identical ratios of surface areato volume, because these ratios are not intrinsicallydependent on body layout, mode of organized growth ortissue construction. The critical features in¯uencing surfacearea to volume ratios are body size, geometry and shape.This may account for body plan divergence in each algallineage, since very di�erent plant BauplaÈne can achieve thesame size, shape or geometry, and thus the same or verysimilar surface area to volume ratios. If true, then body plandivergence within some lineages may re¯ect `di�use

Body Plans

evolution' and not the intense operation of natural selection

10−2

10−3

10−4

Tim

e fo

r di

ffu

sion

(s)

t Body Plans 419

per se.Mutations altering how organized growth is achievedmay go largely unseen by the environment provided theyare not developmentally deleterious and do not lower thecapacity to adjust shape or geometry during ontogeny anddevelopment to maintain or increase body surface tovolume ratios as overall size increases. Likewise, thedependence of bodily functions on the surface to volumeratio, which is itself dependent on body size, shape andgeometry, helps to explain why species possessing verydi�erent body plans often converge on similar morpho-logies or anatomies. In these instances, the operation ofnatural selection rather than `di�use evolution' is the most

NiklasÐPlan

likely explanation.

Cell surface area (µm2)

106101 102 103 104 10510−5

FIG. 5. Estimated time for the passive di�usion of a substanceoriginally lacking in a cell to reach one-half the external concentrationin the cytoplasm of a unicellular plant plotted against cell surface area.Dashed line denotes the time required for the substance's passivedi�usion assuming that cell surface area scales as the 2/3-power of cellvolume; solid line is the ordinary least squares regression curve for thetime of di�usion calculated on the basis of empirically measured cellvolume. The lower slope of the regression curve indicates that surfacearea scales with respect to cell volume with a higher power than that of

2/3 (see Fig. 7).

THE UNICELLULAR BODY PLAN

Small body size confers numerous metabolic advantages, asis evident from a biomechanical examination of theunicellular Bauplan, which is the most ancient among allplant body plans. For example, all unicellular plants obtaincarbon dioxide, oxygen, and other non-electrolytic sub-stances dissolved in water from the external environmentoften by means of passive di�usion. Under these circum-stances, Fick's law shows that the time t required for theconcentration of a non-electrolyte j, initially absent from acell, to reach one-half the concentration of the externalconcentration of j is given by the formula

t � V

PjSln�co ÿ ci�t�0�co ÿ ci�t�0:5

� �

where V is cell volume, S is cell surface area, co is theexternal concentration of j, ci is the internal concentrationof j, Pj is the permeability coe�cient of j, (co ÿ ci)t�0 is theinitial di�erence in the external and internal concentrationsof j at time zero, and (co ÿ ci�t�0:5 is the di�erence in theexternal and internal concentration of j when ci � co/2.Since ln[(co ÿ ci�t�0/(co ÿ ci�t�0:5] � ln[(co ÿ 0)t�0/(co ÿ co/2�t�0:5] � ln 2 � 0.693, it follows that t � 0.693V/PjS (seeNobel, 1983; Niklas, 1994). This formula shows that, forany series of unicellular organisms di�ering in size butsharing the same geometry and shape, the time required toconcentrate nutrients within cells by means of passivedi�usion increases dramatically with increasing cell size(Fig. 5). Similar results are obtained when the e�ects ofboundary layers on the pool of substances around andabsorbed actively by cells are considered (see Niklas, 1994).Natural selection, therefore, would favour photosyntheticorganisms with small body (cell) sizes in the aquaticenvironment.

Light harvesting in water is also favoured by small bodysize, because equivalent amounts of pigments contained indiscrete `packages' or units (i.e. chloroplasts, cells, orcolonies of cells) are less e�ective at harvesting light as thesize of these units increases. For example, this `packagee�ect' is quantitatively expressed for spherical cells by theformula

I � Ioeÿ�k�nAa�d cosec b

where I is the downward ¯ux of light energy per unit areaon a horizontal plane at depth d, Io is the ¯ux of radiationon a horizontal plane just beneath the water surface, k is thetotal absorption coe�cient of water (and any dissolvedsubstances), n is the number of packages (cells) per cubicmetre, A is the average projected cell area in the suspension,a is the average proportion of total irradiant energy incidenton a cell, and b is the angle of incident light with respect tothe horizontal plane (e.g. when the direction of light isnormal to the horizontal, cosec b � 1.0) (see Kirk, 1975).Assuming that cells have equivalent amounts of chloro-phyll, this formula shows that the average light absorptionin a suspension of unicellular plants sharing a sphericalgeometry dramatically decreases as cell (body) size increases(Fig. 6; see Niklas, 1994 for details of simulation).

Finally, small cell size is favourable in terms of reducingthe rate at which a unicellular organism settles in acolumn of waterÐthe terminal settling velocity v of aquaticunicellular organisms lacking ¯agella or cilia is approxi-mated by Stokes' law, which states that v increases in pro-portion to the square of the radius r of a sphere (i.e. v / r2).Stokes' law also indicates that v is proportional to thedi�erence between the density of an organism and itssurrounding ¯uidÐa parameter that can be altered bymany unicellular plants by regulating vacuolar andcytoplasmic contents.

Despite the phenotypic plasticity evident among con-speci®cs of uni-nucleate and unicellular plant species, theevolution of this body plan was undoubtedly in¯uenced byits `closed and determinate' ontogeny, which pre®guresadult body (cell) size, shape and geometry. However, inter-
speci®c comparisons among unicellular species indicate that

Su

rfac

e ar

ea (

µm2)

Volume (µm3)

Size

Geom

etry

Sh

ape

α = 0.667

α = 0.699

simulation

plants (algae)

A

B

10111010108107100 106103102 104 105101

1011

1010

109

108

107

100

106

103

102

104

105

101

109

FIG. 7. Empirically determined relationship between cell surface area Sand volume V measured for 57 species of unicellular algae (shown bysolid regression curve with slope a � 0.699) (A) compared to therelationship between S and V for a series of spheres di�ering in size(volume) (shown by dashed line with a � 0.667) and a computersimulated series of di�erent geometries and shapes di�ering in size thatmaximizes S with respect to V as size increases (B). The smallest algalspecies in the data set have spheroidal geometries; the largest species inthe data set have cylindrical geometries. Within each class of geometry,shape changes (e.g. squat to slender cylinders). The computer-generated series of objects obtains the same slope for the relationshipbetween S and V as observed for the 57 alga species (a � 0.699). Theseries begins with small spheres and spheroids and ends with largeslender cylinders similar in appearance to unicellular plants (Adopted

from Niklas, 1994).

0.16

0.14

0.12

0.08

0.06

0.04

0.02

0.00

0.10

4 µm

8 µm

16 µm

64 µm

400 450 500 550 600 650 700 750

Wavelength of light (nm)

Ave

rage

abs

orpt

ion

(m

2 )

FIG. 6. Average absorption of light by a population of spherical cellsdi�ering in diameter (see insert) plotted as a function of the wavelengthof light (within the absorption range of chlorophyll a). The averageabsorption of cells in the population decreases as a function ofincreasing cell diameter for all wavelengths, but is particularlydiminished in the red and blue wavelengths critical for photosynthesis


cell geometry and shape, or both, change as a function ofan increase in body size. In fact, these changes allowunicellular organisms to `push to the limit' of cell size.Speci®cally, when representative unicellular species fromdiverse algal lineages are examined, the relationshipbetween body surface area S and volume V is anisometricsuch that an increase in surface area fails to keep pace withan increase in body volume (i.e. S / V 0:70) (Williams, 1964;Eppley and Sloan, 1965; Mullin, Sloan and Eppley, 1966;Niklas, 1994). However, the empirically observed size-dependent variation in body surface area and volume devi-ates signi®cantly from the `2/3-power rule' (i.e. S / V 0:67)(Fig. 7A) which describes the relationship expected betweenS and V for any series of objects di�ering in size but sharingexactly the same geometry and shape (Fig. 7A). Theviolation of the 2/3-power rule clearly indicates that eitherbody geometry or shape, or both change as size increases.Indeed, smaller unicellular species tend to have a sphericalor spheroidal (oblate or prolate) geometry, whereas largerspecies tend to have a cylindrical geometry, and, withineach class of cell geometry, larger species tend to be eithermore ¯at (spheroids) or more slender (cylinders) than theirsmaller counterparts. Therefore, the issue is not whether thegeometry or shape of the unicellular body plan changeswith increasing size, but whether the di�erences observedamong species evidence an àdaptive' trend.

In this regard, computer simulations indicate thatinterspeci®c di�erences in body geometry and shape achievethe theoretically greatest increase in cell surface area withrespect to an increase in cell volume. Simulations identify aseries of geometries and shapes, beginning with very smallspheres and ending with large and very slender cylinders,that are virtually indistinguishable from those observedamong algal species di�ering in cell size (Fig. 7B). Thesesimulations provide evidence, albeit circumstantial that the

(Adopted from Niklas, 1994).

size-dependent relationship between cell surface area and

volume has played an important role in the evolution of theunicellular body plan.

An upper limit to unicellular Bauplan size may exist, butit is not a simple consequence of size-dependent variationsin surface area. Size-dependent variations in the `metabolicmachinery' packaged in the unicellular body also exist.Comparisons among unicellular eukaryotic species showthat an increase in body mass M (measured in picograms ofcarbon per cell to avoid any ambiguity resulting from thepresence of vacuoles or intracellular crystals di�ering
in size) fails to keep pace with increasing body volume

A

B

104

103

102

101

100

10−3

Body mass (pg C)

Volume (µm3)

10−2

101

100

10−3

10−1

10−1 100 101 102 103 104

101 102 103 104 105 107 108

y = 0.008 x0.99

r2 = 0.99

y = 0.92 x−0.25

r2 = 0.90

y = 0.08 x−0.32

r2 = 0.45

Bod

y m

ass

(pg

C)

10−2

105

10−1 109100 1010

106 107

Gro

wth

rat

e (h

−1)

unicellularmetazoans

metaphytes

unicellularalgae

bacteria

y = 0.003 x0.81

r2 = 0.96

10−1

105 108

106

FIG. 8. Allometric relationships among the body mass (measured aspicograms of carbon per cell), body volume and maximum reportedgrowth rate for bacteria, unicellular plants (algae), animals andmulticellular plants. A, Body mass plotted as a function of cell volumefor bacteria and unicellular algal species. B, Maximum growth rate(picrograms of carbon produced per cell body mass per hour) plottedagainst body mass for algae, metazoans and metaphytes (i.e. Lemnaand Azolla). Solid lines denote reduced major axis regression curves for

data (see regression formulae) (Data taken from Niklas, 1994).

A

B

104

103

102

101

100

10−1

Body mass (pg C)

Volume (µm3)

Ch

loro

phyl

l a (

pg C

)S

ubs

iste

nce

qu

otas

phosphorusnitrogen

104

103

102

101

100

10−1

105

106

10−1 100 101 102 103 104 105

101 102 103 104 105 107 108

y = 1.12 x0.79

r2 = 0.94

y = 0.06 x0.72

r2 = 0.96

y = 0.06 x0.84

r2 = 0.69

106

FIG. 9. Allometric relationships among chlorophyll a concentration,body mass (measured as picrograms of carbon per cell), cell volume,and phosphorus and nitrogen subsistence quotas reported forunicellular plants (algae) drawn from diverse lineages. A, Chlorophylla concentration plotted as a function of cell (body) mass. B,Subsistence quotas plotted as a function of cell (body) volume. Solidlines denote reduced major axis regression curves for data (see

regression formulae) (Data taken from Niklas, 1994).


(i.e. M / V 0:81) (Fig. 8A). Likewise, the growth rate G(measured as the maximum rate of cell division for culturesgrown under optimal growth conditions) decreases withincreasing body mass M (i.e. G /Mÿ0:32) in much the sameway it decreases among metaphytes and metazoans(Fig. 8B) (see Fenchel, 1974; Banse, 1976; Peters, 1983;Reiss, 1989; Niklas, 1994). The available data indicate thatthe cellular concentrations of many important constituentsdecrease relative to an interspeci®c increase in body size.For example, the amount of chlorophyll a per cell C doesnot increase proportionally with respect to cell mass M (i.e.C / M0:79) such that the concentration of chlorophyll perunit cell mass decreases (Fig. 9A). Likewise, phosphorusand nitrogen subsistence quotas fail to keep pace with
increasing body volume (Fig. 9B). These and many other
size-dependent relationships indicate that, even thoughlarger cells contain higher concentrations of photosyntheticpigments and require larger amounts of metabolicallyimportant substances, the metabolic `machinery' of theunicellular body plan becomes progressively `diluted' asbody size increases (measured either in terms of cell mass orvolume). Together with the size-dependent decrease in cellsurface area, this phenomenon may be directly or indirectlyresponsible for the decline in the growth rate as theunicellular body plan increases in size across species.

Regardless of their proximate cause(s), from an eco-logical perspective, size-dependent variations in metabolismand growth rates help to explain why the unicellular bodyplan is con®ned to a comparatively small size, and why the
organisms possessing this body plan are generally con®ned

t

to low nutrient concentrations or habitats characterized byrapid environmental changes. Regardless of shape orgeometry, a small body size confers a large surface arearelative to body volume containing a proportionally more`condensed' metabolic machine. Smaller organisms canthus obtain nutrients more rapidly, are better equipped tometabolize these nutrients, and can grow in size andreproduce faster than their larger unicellular counterparts.All of these features confer the ability to take advantage ofbrief or intermittent `windows of environmental opport-unity' to complete the life cycle. It is also reasonable tosuppose that small unicellular organisms are capable ofrapid physiological dormancy, and are thus able to adapt toand `weather out' inclement but transient environmental

422 NiklasÐPlan

conditions.

times among the di�erent algal lineages (Table 1).

Multicellular Unicellular

Number of generations

Nu

mbe

r of

indi

vidu

als

0 2 4 6 8 10

104

103

102

101

100

multicellular

unicellular

FIG. 10. Hypothetical increase in the number of sexually reproductiveindividuals in a population of a multicellular plant (life cycle shown inupper left) and a unicellular plant (life cycle shown in upper right)plotted as a function of number of generations (reproductive cycles).Each population starts with one individual; each individual producesone `gamete' (the adult plant body in the unicellular organism). Eachindividual is assumed to survive across all generations (Adopted from

THE COLONIAL AND SIPHONOUSBODY PLANS

Some of the advantages conferred by a small body (cell)size are retained when individual cells become looselyaggregated together. Each cell is free to capitalize on itscapacity for rapid growth and reproduction, and, providedthat cells are spaced some distance apart in a pattern thatreduces self-shading, the attenuation of light by neighbour-ing cells can be minimized. Indeed, there are some advan-tages to clumping cells. Metabolites can be exchangedamong neighbours and used as lines of chemical communi-cation to coordinate metabolic activities, patterns ofvegetative cell division, or sexual reproduction. Local ¯uid¯ow patterns can be modi®ed and used to remove sub-stances or concentrate anti-microbial or toxic substances todeter pathogens or predators in the immediate vicinity.Clumped cells can also reduce the rate at which each loseswater during dry periods.

Some of the advantages of clumping cells together can beillustrated by drawing on the very loose physical analogybetween mass transport in a very low Reynolds numberenvironment where viscous forces dominate and the electro-static problem of a charged conductor in a charge-freehomogeneous dialectric medium. For small unicellularorganisms existing in an environment dominated by low¯uid-¯ow speeds, nearly stagnant physiological conditionscan prevail. In this environment, the ability of a cell toexchange mass with its surrounding ¯uid can be crudelygauged by the equivalent external conductance J for anobject of similar size, shape and geometry (Niklas, 1994). Inelectrostatics, J equals the quotient of the capacitance andthe permittivity of the medium, and, for a single sphere (cell)with radius r, J1 � 4pr � 12:6r; whereas, for two touchingspheres (cells) with equivalent radii r,J2 � 8p (ln 2)r � 17.4r.Since [(J2/J1) ÿ 1] � 100% � 38%, the analogy betweenmass exchange and conductance suggests that two adjoiningcells may physiologically bene®t from each other's presencein terms of respiration or photosynthesis. Naturally, thisanalogy erroneously suggests that mass exchange willincrease as a function of cell radius, which is not likely tobe the case for real cells depending on passive di�usion.Also, adjoining cells will compete for the same resources (but
by doing so they are likely to accentuate gradients of
materials dissolved in their immediate ¯uid environment,thereby enhancing their collective access to nutrients).

Mass exchange and other density-dependent phenomenacan be facilitated if neighbouring cells are bound togetherby a common extracellular matrix that is both permeable toand can retain water, metabolites, hormones, and othersubstances. Such a matrix can be also used to anchor non-motile cells to a substrate to prevent the collective frombeing washed away, elevate cells above a potentiallystagnant boundary layer, or construct comparatively largenon-cellular surfaces capable of physically modifying¯uid ¯ow patterns, thereby assisting in the circulation ofinorganic nutrients around cell clusters. A matrix issimilarly bene®cial to cells with ¯agella or cilia whosecollective activities are capable of stirring the boundarylayer near the matrix surface and thus contribute to themetabolism as well as the locomotion of the whole (Knight-Jones, 1954; Blake and Sleigh, 1974; Niklas, 1994). Thespecialization of some cells is likewise made possible. Someindividuals can retain ¯agella or cilia and thus providewater circulation or locomotion, whereas others can devotetheir existence to reproduction (Kirk, 1998). Yet anotherpotential advantage of operating as a loose confederacy isthat the ecological `presence' of the aggregate is retainedeven if some cells die or reproduce, whereas the unicellular(uni-nucleate) organism ceases to exist when it enters itssexual life cycle, since each àdult' assumes the role of a`gamete' (Fig. 10). It is not surprising, therefore, thatcolonial life forms have evolved independently many

Body Plans

Niklas, 1997).

FIG. 11. Unicellular (uni-nucleate) (A) and colonial body plans (B±E). A, Chlamydomonas sp. (Chlorophyta). B, Synura splendida (Chrysophyta).C, Dinobryon sertularia (Chrysophyta). D, Gonium sacculiferum (Chlorophyta). E, Pandorina morum (Chlorophyta).


However, a sharp biological distinction must be drawnbetween the colonial body plan and the colonial growthform. The latter is sometimes adopted temporarily by avariety of unicellular and multicellular species in responseto nutrient depletion, desiccation, low light intensity, orsome other type of environmental stress. For example,Chlamydomonas (Fig. 11A) and many unicellular organismsin the Chlamydomonadaceae (Chlorophyta) can lose¯agella, form `colonial' aggregates on a substrate, andenter a period of metabolic or reproductive dormancy untilenvironmental conditions return to normal (Bold andWynne, 1978). The cells in the ®lamentous body plan ofthe chrysophycean alga Phaeothamnion confervicola candissociate and form a mucilaginous `colony' when physio-logically stressed (Bold and Wynne, 1978). Conversely, itmust be noted that some cellular prokaryotes and non-photosynthetic eukaryotes aggregate to form morpho-
logically complex colonies when starved of nutrients or
otherwise stressed (e.g. Chrondromyces crocatus and Dictyo-stelium discoidium, respectively), leading some to speculateon the transition from the unicellular to the multicellularbody plan in distantly related groups of organisms (seeKaiser, 1993 and references therein). Regardless of theinferences that can be drawn from these organisms, manyexamples su�ce to show that the `colonial' (palmelloid)growth habit is adopted by species with a variety ofdi�erent body plans in response to inclement environmentalconditions. Conceptually and biologically this contrastswith the colonial body plan that is adopted as a con-sequence of normal growth and development (e.g. Synurasplendida and Dinobryon sertularia in the Chrysophyta, andGonium sacculiferum and Pandorina morum in the Chloro-phyta) (Fig. 11B±E).

Yet, even among bona ®de colonial species, a furtherdistinction must be drawn between colonies with an òpen
and indeterminate' ontogeny involving the mitotic division

multi-nucleate unicellular organisms.

t

of cells that remain physically attached but cytoplasmicallydisconnected from one another (e.g. S. splendida) vs.colonies with a `closed and determinate' (coenobial)ontogeny that produces a multicellular body plan with apre®gured number of cells. In some cases, the multicellularbody plan is retained in the adult condition (e.g. Volvox)(Starr, 1968), whereas in other cases the multicellular bodyplan is adopted early in development but is subsequentlylost with the dissolution of cytoplasmic connections amongadjoining cells before the adult condition is reached(e.g. G. sacculiferum) (Kirk, 1988, 1998). Thus, the colonialbody plan may have evolved either from a unicellularorganism that biologically bene®ted from the presence ofconspeci®cs, or from an inherited developmental `demo-lition' of a multicellular body plan. Attempts to use certainplant groups, such as the volvocine green algae, asexemplars of how multicellularity may have evolved froma presumed antecedent loose confederacy of cells are thushighly problematic (Buss, 1987), especially since, amongthe volvocine algae, the available information indicatesthat the colonial body plan is most probably the derivedrather than the ancestral condition. Under any circum-stances, based on molecular data, some of the `genera'in the volvocine `lineage' are undoubtedly polyphyletic(e.g. Chlamydomonas, Eudorina and Volvox), making itdi�cult or impossible to adduce a `linear sequence' ofevolutionary transformations (Adair et al., 1987; Larson,Kirk and Kirk, 1992).

The evolutionary origins of the siphonous (unicellularmulti-nucleate) body plan are equally unclear. Althoughrare (Table 1), the siphonous body plan has an òpen andindeterminate' ontogeny that arguably confers someadvantages over the `closed and determinate' ontogenytypical of the unicellular (uni-nucleate) body plan, sincesiphonous plants can (and typically do) conserve orelaborate their body surface area with respect to volumeby adopting a cylindrical geometry as the iterative unit oftheir body construction. Simple analytical geometry showsthat the cylinder is one of the few geometries that caninde®nitely increase in volume (size) without decreasing itsratio of surface area to volume (i.e. since S � 2prl andV � pr2l, where r is radius and l is length, it follows thatS=V � 2=r; indicating that the ratio of S to V is propor-tional to the radius of a cylindrical body plan and isindependent of body length). The delicate, feather-like`fronds' of many chlorophycean siphonous species, such asthose of Bryopsis (which generally attain a length of 10 cmbut which can reach 40 cm in length in the case ofB. maxima) and Caulerpa sertularioides and C. ¯orida(which exceed 15 cm in length), are all constructed out ofvery slender tubular elements that have very large surfaceareas with respect their volume. Likewise, the coenocyticvegetative axes of many xanthophycean species, such asVaucheria and Ophiocytium, have a cylindrical geometry.Additionally, large body size in the siphonous body plancan be achieved by appressing the majority of organellesagainst the cell wall by a large vacuole. This cytologicalcon®guration minimizes the transport distance (and thusthe transport time) for the passive di�usion of nutrients or

424 NiklasÐPlan

wastes across the cell membrane and wall.

The comparative rarity of the siphonous body plan maybe related to the fact that microbial or viral infections aredi�cult or impossible to localize and thus can becomesystemic in the absence of the compartmentalization of theprotoplast by cell walls. Mechanical perforation of thesingle cell wall also can result in the evacuation of asubstantial amount of protoplasm before the damaged wallcan be repaired. These and other features may explain whythis body plan is found among a comparatively smallnumber of species. In terms of the origin of the siphonousbody plan, either the unicellular or multicellular ancestralcondition is theoretically possible. It must be noted,however, that all siphonous species are capable of partition-ing their protoplasts by means of cell walls during theformation of reproductive structures (Bold and Wynne,1978) and that some multicellular taxa are multinucleate(e.g. Urospora and Cladophora). These features suggest thatsome siphonous algae are evolutionarily derived frommulticellular organisms by the modi®cation of the relation-ship between cyto- and karyokinesis, whereas othersiphonous algae evolved from unicellular multi-nucleateorganisms that attained the capacity for indeterminategrowth in cell size.

Unfortunately, our current understanding of the cellularmechanics and genetics responsible for disparity betweenkaryo- and cytokinesis, and thus the distinction between theuni- and multi-nucleate cellular condition is incomplete.It has long been known that the volume of the nucleuswith respect to that of the cytoplasm is fairly constantacross unicellular and siphonous plants (Sharp, 1926; Sitte,1992). `Super-cell' organisms, like Caulerpa, Valonia,Bryopsis and Vaucheria, contain nuclei whose collectivevolume is proportional to the volume of the cytoplasmenveloped by their single cell wall. This phenomenology isconsistent with the ènergid' concept of Sachs (1892), whichpostulates that each nucleus in a cell `dominates' a certainvolume of the cytoplasm. In the parlance of this theory,unicellular organisms are `monoenergidic', whereas sipho-nous organisms are `polyenergidic'. Yet, the mechanism(s)responsible for the disparity between cyto- and karyokinesisremain(s) poorly understood. Among bacteria, cytokinesisby cleavage is mediated by a set of proteins, principallyFtsZ (Bramhill, 1997), which has sequence similarities toeukaryotic tubulins (Erickson, 1997). Although it has yet tobe proven, cleavage among eukaryotic plants appears to bepredicated on an actin-based phenomenon. Spatial appor-tionment of the cytoplasm and control over cytokinesis inmulticellular plants are dependent on nuclear-based radialsystems of microtubules that de®ne what have been callednuclear-cytoplasmic domains (see Brown and Lemmon,1992). Genetic alterations of these systems arguably mayaccount for evolutionary transitions between uni- and

Body Plans

FILAMENTOUS MULTICELLULAR BODYPLAN VARIANTS

The evolution of the multicellular body plan was a majorevolutionary achievement that required precise control over
the plane of cell division and the establishment of

FIG. 12. General morphology of representative cyanobacteria withunbranched and branched ®lamentous (A and B) and parenchyma-tous-like (pluriserate) constructions in which symplastic continuitymay be maintained among adjoining cells (C). A, Cylindrospermum sp.

FIG. 13. Hypothetical derivation of a multicellular (simple ®lamen-tous) body plan (centre) from a unicellular (A), colonial (B), and

siphonous (C) body plan. See text for further details.


cytoplasmic (symplastic) continuity among adjoining cells.Interestingly, the capacity to regulate cell division planes,di�erentiate cell types, and fabricate unbranched ®laments,branched ®laments, and cellular con®gurations similar ingeneral appearance to parenchyma (i.e. pluriserate ®la-ments) is evident among the cyanobacteria (e.g. Cylindros-permum,Hapalosiphon andFischerella, respectively; Fig. 12),many of which can also establish symplastic continuityamong neighbouring cells in the form of delicate (`micro')plasmodesmata that cross the transverse walls of adjoiningcells (Bold and Wynne, 1978; Westermann et al., 1994).Whether these structures are primary or secondary, andwhether they provide robust avenues for metabolic transportor communication as plasmodesmata do among eukaryoticphotoautotrophs remain conjectural. However, it cannotescape attention that many chloroplast genes currentlyreside in the nuclear genomes of plants and that chloroplastsare presumed to have evolved from ancient forms of blue-green bacteria. It is conceivable, therefore, that some ofthe genetic material encoding for cyanophycean multi-cellularity may have been transmitted to `host' cell genomesshortly after the primary endosymbiotic events occurringin the Precambrian. In this sense, some of the featuresof eukaryotic multicellularity may have been pre®gured

B, Hapalosiphon sp. C, Fischerella sp.

during the early evolution of many of the ancient algal

lineages. Under any circumstances, the basic elements of themulticellular body plan evidently predate the eukaryoticcondition.

Although the genetic mechanisms required for multi-cellularity are undoubtedly complex, on strictly morpho-logical grounds, the multicellular body plan may haveevolved directly from a unicellular, colonial, or siphonousBauplan (Fig. 13). It is currently impossible to say which, ifany of these was the antecedent condition for the mostancient multicellular organisms in any particular plantlineage. The view taken here, however, is that the unicellularbody plan is the most plausible morphological antecedentcondition to multicellularity in the majority of the algallineages and that the unbranched ®lament is the mostancient variant of the multicellular body plan (seeFig. 13A). Cell division in one plane followed by cytokinesisand the retention of cytoplasmic `bridges' or the formationof plasmodesmata between derivative cells immediatelyestablish the unbranched ®lamentous multicellular bodyplan. Di�use cellular division would increase body size andproduce a cylindrical body geometry. As noted, thisgeometry is one of the few that can increase in size withoutreducing the ratio of body surface area to volume.Filaments of cells can increase in size by the addition ofnew cells anywhere along their length, and each individualcell can increase in length, thereby allowing the surface areato volume ratio of constituent cells as well as the entireplant body to either remain constant or increase dependingon metabolic demands. The derivation of an unbranched®lamentous multicellular body plan from a unicellular
organism is consistent with the widely held view that the

t

latter is the most ancient body plan in each algal lineage. Itis also consistent with the ontogeny of many ®lamentousspecies, which begin their vegetative existence as ¯agellatedzoospores, lose their ¯agella, and subsequently undergo anindeterminate number of mitotic cellular divisions to forman unbranched ®lament (e.g. Stichococcus chloranthus andUlothrix zonata).

The ability to form simple unbranched ®laments requiresa cell division mechanism sensitive to the orientation ofcell growth with respect to adjoining cells such that theplane of cell division is consistently con®ned to theperpendicular direction with respect to the body axis.Subsequent evolutionary modi®cations were required toalter this mechanism such that two or more orthogonalplanes of cell division become possible to form branched®laments and parenchymatous tissues (see Fig. 3). A varietyof mechanisms responsible for the orientation of celldivision has been proposed. The preprophase band isconsidered pivotal by some workers, especially in terms ofthe evolution of the embryophytes (see Brown andLemmon, 1990), since the developmental switch from thetip growth in the ®lamentous (protonemal) stage of mossgametophyte growth to gametangiophore bud formation iscorrelated with the appearance of preprophase bands in thelatter stage (Doonan, 1991). Nonetheless, preprophasebands are absent among many organisms that manifestprecise control over their planes of cell division and thusproduce ®lamentous or parenchymatous growth (e.g.Coleochaete and Chara). For this reason, other workershave emphasized the importance of mechanical stressesgenerated during cell division, draw attention to plastidorientation, or implicate the role of cytoskeletal elements ofthe phragmosome as factors in¯uencing the site of futurecell wall formation (e.g. Lintilhac, 1974; Brown andLemmon, 1984; Green, 1987; Lloyd, 1991; Cooke and Lu,1992; Oates and Cole, 1992).

Perhaps the most far-reaching mechanism for celldivision orientation thus far is the `tensegrity' concept ofPickett-Heaps et al. (1999; see also Ingber, 1993), whichproposes that each cell is organized by an integratedcytoskeleton of tension elements (actin ®bres) extended overa compression resistant domain composed of microtubules.If so, then mechanical as well as chemical cues are requiredfor the orientation of the cell division plane. Although all ofthese explanations are plausible mechanistically, consider-able variation in mitosis and cytokinesis occurs acrossplant lineages (see Pickett-Heaps, 1972) and most explana-tions cannot be applied universally across all of the pro-and eukaryotic lineages in which multicellularity isexpressed, indicating that our understanding of themechanism(s) responsible for the planes of cell division isincomplete.

From a functional perspective, even the most morpho-logically simple variants of the multicellular body plan (e.g.unbranched and branched ®laments) confer similar advan-tages to that of the colonial body planÐbody size canincrease by the addition of cells that metabolically orreproductively bene®t by virtue of their comparatively smallsize and large surface area to volume ratios, and the

426 NiklasÐPlan

organism as a whole can devote some cells to sexual

reproduction without sacri®cing its ecological persistence ina population (see Fig. 10). Unlike the colonial body plan,cells in a multicellular organism remain symplasticallyinterconnected by means of cytoplasmic bridges, plasmo-desmata, etc. that establish a large continuous internalplasmalemma system that can be used for chemicalexchange and intercellular communication. The numberand distribution of these cytoplasmic bridges between cellscan also be developmentally adjusted to create preferredroutes of intercellular transport for nutrients and growthhormones (Ding, Itaya and Woo, 1999). Cell-to-celltra�cking of macromolecules can be used to generatechemical gradients to regulate cell, tissue, and body planpolarity, help de®ne where and how long meristematicactivity occurs, and that can isolate reproductive cells by thedissolution of symplastic continuity (Kwiatkowska, 1988).

Patterns of cellular di�erentiation become possible aswell, since plasmodesmata are known to preferentiallytra�c di�erent hormones (Drake and Carr, 1978, 1979) andsince each cell in the multicellular organism is no longerentirely responsible for its own metabolic requirements andsurvival (e.g. non-photosynthetic cells can be metabolicallysustained by photosynthetic cells or tissues; some cells canbe developmentally programmed to die after they deposittheir cell walls whose lumens can be used to transport waterand growth hormones). Since body shape and geometrycan be speci®ed by cell-to-cell coordinated e�orts, multi-cellularity confers numerous advantages in terms ofacquiring nutrients, intercepting sunlight, occupyingspace, and thus competing with other species for the sameor similar resources.

The ®lamentous body plan confers a number ofmechanical as well as physiological advantages, especiallywhen anchored by a specialized basal cell to a substrateunder water. For example, the net hydrodynamic force FNexerted on any plant body is the vector resultant of twoorthogonally opposed forcesÐthe lift force FL , whichoperates perpendicular to the direction of ¯uid ¯ow, andthe two horizontal force components, which are thepressure (drag) force FD and the acceleration force FA.When ¯uid-¯ow is accelerating, the two horizontal forces actin the same direction; when the ¯uid decelerates, these twoforces act in opposing directions (Fig. 14). Mathematically,these three force components are given by the formulae

FL � 0:5ru2SplanCL

FD � 0:5ru2SpCD

FA � rCmVa;

where 0.5ru2 is the dynamic pressure, Splan is the `planformarea' (the area of the plant body projected perpendicular tothe direction of ¯ow), CL is the lift coe�cient, Sp is thesurface area of the plant body projected against thedirection of ¯uid ¯ow, CD is the pressure (drag) coe�cient,Cm is the inertia coe�cient, V is plant body volume, and a isthe ¯uid acceleration (Denny, 1988; Niklas, 1994). In anenvironment with rapid and steady ¯uid-¯ow, the planform

Body Plans

area and the projected area of a ¯exible ®lamentous body

organisms living in high-energy, wave-swept habitats.

u FL

FN

FD FA

Splan = πr2

FIG. 14. Diagram of hydrodynamic force components exerted on amulticellular (simple ®lamentous) body plan attached to a substratesubjected to a ¯uid-¯ow with velocity u. The net hydrodynamic forceFN equals the vector sum of the vertical lift force FL and two horizontalforce components, the pressure (drag) force FD and the accelerationforce FA. The planform surface area projected toward the directionof ¯uid-¯ow, which in¯uences the magnitude of FL and FD (seetext for formulae), is independent of body length and depends on

cell radius r.

NiklasÐPlant

plan roughly equal the cross-sectional area of an averagecell in the ®lament, and thus the lift and drag forces on a®lament aligned in the direction of ¯ow are largelyinsensitive to the number of cells along the length of theplant body (Fig. 14). By the same token, the drag andinertia coe�cients for a cylinder are independent of thelength of a cylindrical ®lament, whereas the inertiacoe�cient ranges from 1.62 to 2.0 for a cylinder withlength to diameter ratios of 1.2 and in®nity, respectively.Consequently, the principal variables in¯uencing the nethydrodynamic force on an unbranched ®lamentous bodyplan are ¯uid-¯ow speed u and acceleration a, which cannotbe controlled by the plant, and body volume V, which isdetermined by an organism's ontogeny and life-expectancy.Although an inde®nite increase in body volume canengender large acceleration forces, provided the organismgets big enough to experience turbulent ¯ow regimes, the®lamentous body plan, whether branched or unbranched,can metabolically bene®t, in terms of mass exchange, fromforced convection. Indeed, for some ®lamentous algae (e.g.Cladophora), the frequency of branching increases (to alimit) in proportion to water speed, presumably becausehigh ¯ow regimes favour more rapid mass exchangebetween the plant body and its surrounding water andthus higher respiration and photosynthetic rates (see Parodiand CaÂ ceres, 1991).

It is worth noting that cell division in two orthogonaldirections is required to construct branched ®laments. Thisalso a�ords the opportunity to construct monostromaticthalli that have large surface areas with respect to theirvolumes, since cells are exposed on both sides to water anddissolved atmospheric gases and nutrients. Provided cellwalls are ¯exible, cylindrical and plate-like plant bodiesanchored to a substrate are capable of streamlining andreducing drag in rapid ¯uid-¯ow environments by de¯ectingand/or folding upon themselves downstream. Extensiblehollow tubes can also sustain very large recoverable elastic
longitudinal deformations by circumferential contraction.
Multicellular plants composed of a pseudoparenchyma-tous tissue can be viewed as having a modi®ed ®lamentousbody layout when di�use, trichothallic, or apical celldivisions are not developmentally coordinated to producea species speci®c body shape or geometry. Variants ofthis kind are especially well represented by species currentlyassigned to the Leathesiaceae in the Phaeophyta(e.g. Leathesia di�ormis). In contrast, a bona ®de pseudo-parenchymatous body plan is achieved when branched orunbranched ®laments are formed and regulated by speci®cmeristematic regions whose activities are coordinated toproduce species speci®c adult morphologies and anatomies,as is seen in many plant lineages such as the Rhodophyta.In either case, a pseudoparenchymatous tissue fabric can beused to construct comparatively large and potentiallymorphologically complex organisms containing a largenon-symplastic volume fraction that is ìnternal' withrespect to the outer surface of cells but that is topologicallyexternal with respect to the organism and the ¯uidsurrounding it. This extracellular but ìnner body compart-ment' can be used to concentrate metabolites, retain water,or serve as an extracellular system for the transport ofsubstances from one part of the organism to another (seeRaven, 1997; Kirk, 1998). Developmental control of theorientation of ®lamentous and pseudoparenchymatoustissues by specialized meristematic regions can also providefor a mechanically anisotropic plant body, one that candeform or resist externally applied mechanical forcesdi�erently depending on the direction these forces areapplied with respect to the three principal body axes. Tissuemechanical anisotropy may be especially important to

Body Plans 427

THE PARENCHYMATOUS PLANT BODY

Arguably, the most evolutionarily derived variants of themulticellular plant body plan are constructed out ofparenchymatous tissues produced by spatially discretemeristematic regions rather than di�use cell division. Thecapacity to establish or sever protoplasmic interconnectionsamong all the surfaces of adjoining cells a�ords the opport-unity to develop complex lines of lateral and longitudinalchemical communication in the plant body by means ofcytoplasmic `domains', the construction of specializedtissues and tissue systems, and the coordination of thephysiological e�orts of vegetative and reproductive organs.In essence, the multicellular parenchymatous plant body iscomposed of a single functional symplast incompletelypartitioned by an infrastructure of cell walls, very like thesiphonous plant body plan but with all the mechanical andphysiological bene®ts conferred by a cellular condition.

These features of the parenchymatous body plan must beconceptually linked to the spatial and temporal coordina-tion of cellular division and the evolution of meristematicregions. Without exception, all contemporary parenchyma-tous species possess well de®ned meristems that are eitherintercalary or apical in location. Unfortunately, the fossilrecord does not provide su�cient information about howthis body plan con®guration evolved in each of the plant
lineages in which it occurs. It is nonetheless tempting to

FIG. 15. Scenarios for the evolution of a parenchymatous tissue fabricconstructed by means of a marginal (peripheral) zone of meristematiccells (A±D) and the evolution of an apical meristem consisting of onecell (capable of dichotomization) from a marginal (peripheral) zone ofmeristematic cells (E±I). Among species of the charophycean algaColeochaete, a discoid thallus (A) can be constructed out of branchedabutting ®laments (pseudoparenchymatous tissue) characterized by Y-shaped cell walls (sector of cells diagrammed in B corresponding tocells outlined in A). An intermediate condition between branched®laments and parenchymatous clusters of cells is reported for somespecies (sector of cells with Y-shaped and bisecting cell walls shown inC). Species with purportedly parenchymatous thalli have radial andcircumferential cell divisions that form bisecting cell walls (D). Thetransition from a parenchymatous organism, like the brown algaPadina (E) whose marginal apical meristem consists of many cells (F)to a parenchymatous organism, like that of the brown alga Dictyota(G), may have been accomplished by reducing the number ofmeristematic cells at di�erent points in the plant body to individualapical cells (H), each capable of bisecting to produce `branches' (I).

t Body Plans

derive the parenchymatous plant body and its specializedmeristematic regions from either a ®lamentous or pseudo-parenchymatous precursor in which meristematic activitywas con®ned to developmentally speci®ed locations, pre-sumably as a consequence of chemical and physical con-trolling mechanisms relying on plasmodesmata tra�cking.

Some evidence supports this point of view. Among thecharophycean algae, which probably share the same lastcommon ancestor with the embryophytes, meristematicgrowth is typically con®ned to the apices of ®laments,whereas, among parenchymatous charophycean species,meristematic growth is con®ned to the margins of thalli.The juxtaposition of these contemporary species may shedlight on how the parenchymatous body plan with apicalmeristems evolved in these algae and was carried forth intothe land plants (see Graham, 1993). Speci®cally, the discoidthallus of some Coleochaete species is composed of laterallyadjoining ®laments that grow in length at their tips by meansof transverse (circumferential) cell divisions and that branch(radially) at their tips to create a pseudoparenchymatoustissue system as evidenced by the appearance of Y-shapedcells (e.g. C. nitellarum) (Fig. 15A, B). Other species in thisgenus construct discoid purportedly parenchymatous thalliby means of a marginal apical meristem that producescoherent cell lineages derived by circumferential andbisecting (radial) divisions (e.g. C. orbicularis) (Fig. 15D).Species in which Y-shaped and radially bisected cells arelocated at the perimeter of thalli may represent the inter-mediate condition between a ®lamentous and parenchy-matous organism (e.g. C. soluta) (Fig. 15C).

Likewise, recent studies of cytokinesis in Chara speciesindicate that this ®lamentous organism establishes plasmo-desmata among all nodal cells that thus assume the role ofdiscrete lateral meristematic regions (Franceschei, Ding andLucas, 1994; Cook, Graham and Lavin, 1998), suggestinghow the parenchymatous plant body evolved from anancestral branched (pseudoparenchymatous) ®lamentousone. By the same token, the transition from a marginalmeristem composed of many initials to an apical meristemcomposed of one or a few initials can be represented by thejuxtaposition of some parenchymatous phaeophyceangenera, among which some have a marginal zone of manyapical meristematic cells (e.g. Padina) similar to that ofparenchymatous Coleochaete species and others have ameristem composed of a single apical cell (e.g. Dictyota)similar to that of Chara and many non-vascular land plants(Fig. 15E±I).

Scenarios such as these, however, are highly speculativesince the sequence of Coleochaete species purported to showthe evolution of parenchymatous tissue from branched®laments (Fig. 15B, C) can be read in the oppositedirection; the charophycean and phaeophycean algae donot share the same last common ancestor; and manyparenchymatous phaeophycean algae possess intercalaryrather than apical meristems (e.g. Laminaria and Macro-cystis). Alternative and equally plausible evolutionaryscenarios also exist. It is possible to derive a parenchymat-ous plant body with apical meristems from a ®lamentousbody layout similar to that of Chara. In the absence of

428 NiklasÐPlan

additional data, therefore, the origins of parenchymatous

plants with well de®ned meristems, apical or otherwise,remain conjectural.

Regardless of its evolutionary origins, a parenchymatousplant body with meristematic activity con®ned largely toone or more apical cells or cell clusters is advantageous in anumber of respects. Body size can be increased inde®nitelyby the exogenous addition of new body parts at growingtips without interrupting the bulk ¯ow or the activetransport of metabolites by specialized tissues that developand mature in older portions of the plant. Reiteration of thebody layout is made possible by repeated bifurcation ofgrowing points to produce a rami®ed (branched) morpho-logy. Multiple apical meristems provide a margin of safetyfor the continued existence of the organism, since the life ofthe individual is not cut short by the decapitation or death
of one or more of its distal parts. Some meristems can be

t Body Plans 429

devoted to the formation of specialized vegetative orreproductive organs that are determinate in size, shape andgeometry (e.g. leaf-like functional analogues and sporangia,respectively), whereas other meristems can continue togrow inde®nitely. Many of these features are di�cult orimpossible to achieve with intercalary meristematic growingregions, although it cannot escape attention that some ofthe largest marine plant species have a parenchymatousbody plan that employs intercalary meristems to achieve itsorganized growth, presumably as a failsafe against the highprobability of distal mechanical failure by shearing water

NiklasÐPlan

currents (e.g. Macrocystis).

FIG. 16. Mechanical behaviour of a thin walled cell in a hydrostatictissue. A, The protoplast of the cell is appressed to its cell wall (shadedarea) by an internal positive (turgor) pressure Pi placing the cell wall inuniform tensile stress s� . Any externally applied tensile or compressiveforce magni®es tensile stresses in wall (not shown). B, A reduction inturgor pressure reducing the volume of the protoplast and thus theforce it exerts on the cell wall which deforms and is subjected to tensileand compressive bending stresses (s� and s± , respectively) (Adopted

from Niklas, 1992).

EMBRYOPHYTE BODY PLAN VARIANTS

Embryophytes and charophycean algae share a commonancestor that probably had (1) cell walls containingcellulose micro®brils that a�orded mechanical supportwhen placed in tension but that deformed easily undercompression, (2) a parenchymatous body plan lacking awaxy cuticle with a high surface area with respect to bodyvolume, (3) a life cycle involving only one multicellular lifeform that functioned as the gametophyte (i.e. a haplobion-tic haploid life cycle), and (4) motile sperm requiring liquidwater to fertilize eggs (Graham, 1993; Niklas, 1997). Eachof these traits is poorly suited for survival on land whereaccess to water may be limited. For example, like those ofmany algae, charophycean cells and tissues mechanicallyfunction as hydrostatsÐ¯uid-®lled devices whose sti�nessis proportional to their inner positive (turgor) pressure(Fig. 16). When fully turgid, the living protoplast in eachcell is compressed against its wall where the resultingcircumferential tension is mechanically sustained by cellu-losic micro®brils (Niklas, 1989). For its density, cellulose isthe strongest known biopolymer measured in tension.However, like all long-chained biopolymers, it provideslittle mechanical support when compressed along the back-bone of its molecular structure, and so, when cell turgorpressure is lost, algal protoplasts de¯ate, their cellulosic cellwalls lose their rigidity, and cells or tissues collapse undertheir own weight when exposed to air.

In water, hydrostatic devices are mechanically reliable,and, since they are nearly neutrally buoyant, they exert littleor no weight on adjoining cells. On land, however, hydro-static tissues are approximately 1000 times more dense thanair and thus generate compressive forces within themselves.This mechanical force can be resisted by turgid cells andtissues, since it is transmitted to cell walls in the form oftensile forces that are mechanically sustained by cellulosemicro®brils. However, when protoplasts are deprived ofwater, compressive bending stresses develop in cell wallsthat are better equipped to cope with tensile stresses(Niklas, 1989). One solution is to produce tissues composedof small cells with thick walls, since the hydrostatic stressesin a cell wall s generated by any internal hydrostaticpressure P are directly proportional to cell radius r andinversely proportional to cell wall thickness t (e.g. for anisodiametric cell, s � rP=2t; see Niklas, 1992).

Another solution is to insert a chemical `bulking agent' in
the cell wall matrix that can buttress cellulose micro®brils
against lateral ¯exure. Lignin provides this service, and,since dehydrated cellulose is sti�er than wet cellulose, ligninhas the additional advantage of being a hydrophobicmaterial. Likewise, lignin can provide some protectionagainst high intensity ultraviolet light and microbialdegradation of cell walls. Resistant polyphenolic com-pounds occur in Coleochaete and various bryophyte species(Delwiche, Graham and Thomson, 1989), and lignins havebeen reported for hornwort species (Takeda, Hasegawa andShinozaki, 1990). However, larger phenolic polymers thatcan be unambiguously assigned to lignin have not beendemonstrated for any species other than tracheophytes [see,however, Gunnison and Alexander (1975) who report`lignin' in the walls of Staurastrum]. However, extensivebiochemical surveys of the algae have not been conducted,and so the distribution of biosynthetic pathways underlying
the formation of lignin is uncertain.

15

10

5

00 2 4 6 8 10 12

Wind speed (cm s−1)

5 cm s−1 10 cm s−1

Hei

ght

abov

e gr

oun

d

FIG. 17. Wind speeds at di�erent locations with respect to heightabove ground within a moss gametophyte `cushion' measured in a windtunnel at two di�erent ambient wind speeds (5 and 10 cm sÿ1). Shadedregion indicates vertical shape of cushion; archegoniophore withsporophyte denotes location of anemometer used to measure windspeeds in cushion. Sporangium is elevated above the region ofattenuated wind speeds created by cushion. Gametophyte locatedin region of comparatively low wind speeds and thus within a

boundary layer.

430 NiklasÐPlant

The ampli®cation of body surface area with respect tovolume is bene®cial in terms of mass and energy exchangeand can proceed inde®nitely in an aquatic environmentwhere desiccation is unlikely. On land, however, water mustbe conserved within the plant body as well as absorbedfrom a substrate. In the absence of a cuticle perforated withpores or stomata, or some physiological means to toleratedry conditions or suspend metabolic activity, a morpho-logical dilemma ensues for a land plantÐlarge surfaceareas are required to absorb water and minerals fromsubstrates, but large surface areas can lose water rapidly.Under these circumstances, growth and survival on land islargely con®ned to dependably moist microhabitats.

Hugging a moist substrate and growing within itsboundary layer by means of a dorsiventral thallus, orgenerating a boundary layer around an elevated plant bodyby appressing vertical but short wick-like body parts closelytogether are reasonable morphological solutions for waterconservation on land (Fig. 17). These body plan symmetriesare reminiscent of the multicellular gametophyte generationof charophycean algae, such as Coleochaete and Chara, andresurface on land over and over again in the form of thethalloid or `leafy' morphologies assumed by the gameto-phyte generation of bryophytes (see Bold, 1967). Whencombined with short stature, these layouts can retain a thinlayer of water over their surfaces and are thus well suited forthe survival and transit of ¯agellated sperm cells.

Additionally, all modern-day land plant groups, includ-ing the bryophytes, appear to possess the capacity toproduce extracellular lipids and cutin, and thus all have theability to form an extracellular `cuticle' that impedes water
loss from the plant body surface to some degree. In
contrast, cuticles like those chemically identi®ed for theland plants have not been demonstrated for any extantaquatic species, although epidermal cutin- and waxy-likechemical moieties are known to occur on the submergedleaf surfaces of some marine and freshwater macrophytes(Holloway, 1982) and on the thalli of some Coleochaetespecies (Cook and Graham, 1998; Graham and Wilcox,2000). Since the land plant cuticle is more resistant to thepassive di�usion of water than to either carbon dioxide,oxygen or other substances (e.g. the permeability coe�-cients of the Citrus cuticle for H2O, CO2 and O2 are inthe order of 10ÿ9, 10ÿ8 and 10ÿ7 m sÿ1, respectively; seeLendzian, 1984), a cuticle-like precursor is not antithetic toan aquatic existence, especially since a polyesteri®edsur®cial layer has the capacity to retard microbes, absorbultraviolet light, and, when con®ned to the surfaces of anaquatic plant body that are predictably exposed to the air,can impede water loss. It is not unreasonable to assume,therefore, that cuticle-like materials may have beenproduced by the last common ancestors of the embryo-phytes and the charophycean algae.

A land plant cuticle sensu stricto must be perforated topermit e�cient gas exchange between the plant body andair. Among modern-day embryophytes, perforations takethe form of epidermal pores or stomata that open intotopologically external but spatially internalized surfacesforming chambers or labyrinthine spaces within the plantbody. Although not widely appreciated, this con®gurationfosters very di�erent gradients of water vapour and carbondioxide at the plant/air interface. Since the air within ahypodermal chamber is saturated with water vapour and islost from a small pore into a potentially moist boundarylayer, a shallow water vapour di�usion gradient can becreated. In contrast, since carbon dioxide is absorbed bymoist cell surfaces everywhere along the surface of thechamber, a steep gradient of carbon dioxide can be estab-lished at the pore opening. In this way, the rate at whichwater vapour is lost to the air can be reduced relative to therate at which carbon dioxide is gained by photosynthetictissues (Cooke and Rand, 1980; Rand and Cooke, 1980).Clearly, the evolution of guard cells that can regulate porediameter and thus control the rate of water vapour loss wasa signi®cant event in the history of plant life. But, even intheir absence, the physics of passive and active di�usionindicates that the ìnternal' surface areas of terrestrial plantsare highly adaptive.

If it is reasonable to assume that the gametophytegeneration of the ®rst land plants retained some of thephyletic legacy of its ancestral charophycean-like alga, it isnot unreasonable to suppose that the land plant sporophytegeneration represents a life cycle innovation that evolvedprimarily or exclusively on land. All extant multicellularmembers of the Charophyta have a haplobiontic haploidlife cycle in which only the gametophyte expresses multi-cellularity. This is a poor `design', since a unicellular diploidphase is poorly equipped to disperse meiospores into theair. Thus, the issue of how the embryophyte sporophytegeneration evolved is an important one.

Traditionally, the origin of the embryophyte sporophyte

Body Plans

is described in terms of `delayed zygotic meiosis', that is, the

t

intercalation of a multicellular diploid generation as theresult of one or more mitotic cell divisions of the zygote.However, the phrase `delayed zygotic meiosis', conveys littlewith regard to the mechanisms responsible for the evolutionof the sporophyte generation of embryophytes, which couldhave made its evolutionary debut in a haplobiontic haploidlife cycle as a result of either the inhibition of zygoticmeiosis or the stimulation of zygotic mitosis. Likewise,delayed zygotic meiosis implies neither the existence of amulticellular sporophyte nor an archegonium, both ofwhich are hallmarks of the embryophytes.

In terms of mechanisms, it must be borne in mind that alarge number of genetic and physiological factors in¯uencethe onset and successful completion of meiosis and mitosis.These factors establish extremely complex and extensivenetworks that control the cell cycle. For example, in manyeukaryotes, cdc2/cylin B mitosis-inducing kinase is acti-vated when the tyrosine-14 or -15 residue in its ATP-binding region is dephosphorylated by cdc25 phosphatase-10-15. In these organisms, cdc2/cylin B kinase is inhibitedwhen the tyrosine residues are phosphorylated by Wee 1tyrosine kinase-4-9, which, in turn, is inhibited by Nim-1kinase (i.e. Nim1 promotes the onset of mitosis byinhibiting Wee 1; see Wu and Russell, 1993). Geneticmodi®cation of these or other kinases can alter when andwhere mitosis occurs. Studies also show that dividing cellscan be induced to undergo mitotic cell division during, aswell as after, their ®rst meiotic cell division by eitherchanges in the physical environment (e.g. high temperature)or genetic mutation, indicating that the `commitment tomeiosis' does not involve an irreversible inhibition ofmitosis as previously thought (see Honigberg and Esposito,1994). Thus, the modi®cation of any one of a number ofphysical or genetic factors attending the evolution of thearchegonium may have been responsible for the evolution-ary origin of the embryophyte sporophyte by `delayedzygotic meiosis'.

As noted, `delayed zygotic meiosis' per se does notimply the existence of an archegonium or a multicellularsporophyte. Theoretically, zygotic mitosis may result in apopulation of cytoplasmically disconnected diploid cells inwhich each cell may function as a zygote. This caveat isimportant in light of the fossil record, which indicates thatconsiderable life cycle èxperimentation' may have occurredduring the early Paleozoic when the embryophyteswere becoming ®rmly established on land. Some of thisexperimentation is illustrated by the charophycean-like algaParka decipiens, which ranged from the Upper Silurian tothe Lower Devonian. The discoid thalli of this enigmaticalga were large (0.5 to 7.5 cm in diameter), pseudopar-enchymatous, monostromatic, and attached to their sub-strate by a centrally located ventral holdfast-like structure(Fig. 18A, B). Scanning electron microscopy and math-ematical simulations indicate that Parka grew by means ofboth anticlinal and periclinal cell divisions along themargins of its outwardly radiating branched ®laments in amanner very similar to that of some modern-day species ofColeochaete (Niklas, 1976). Little is known about the lifecycle of Parka other than that multicellular structures on

NiklasÐPlan

the dorsal surface of thalli contained numerous small cells

(25±45 mm in diameter) (Niklas, 1976). These cells hadsporopollenin-rich walls but lacked haptotypic markings(Fig. 18C). Nonetheless, their cell walls are reported to besimilar to those of the spores of some modern-daybryophytes (Hemsley, 1990).

If an analogy is drawn between Parka and Coleochaete,as suggested by the similarities in their general morphologyand mode of growth, then it is not unreasonable to supposethat Parka had an haplobiontic haploid life cycle. If so,then Parka's multicellular structures may have developedaround fertilized egg cells that divided meiotically toproduce haploid cells much like Coleochaete. However,the presence of a large number of spore-like cells in Parka'sreproductive structures suggests a number of scenarios. Forexample, Parka's zygotes may have divided meiotically ®rst,then divided mitotically to produce a large population ofcells that later developed sporopollenin containing walls(Fig. 18D). Under these circumstances, the gametophytegeneration of Parka would have begun its existence as adormant spore-like entity, albeit lacking haptotypic mark-ings rather than as a zoospore as in the case of modern-dayColeochaete. Alternatively, the zygotes of Parka may havedivided mitotically to produce a coterie of diploid cells thatdeveloped thick walls (also lacking haptotypic markings).These cells may have remained dormant for a time, only todivide meiotically to produce zoospores after being releasedfrom the gametophyte. In either case, the bene®ts ofpotentially rare egg fertilization events would have beenampli®ed. Both of these scenarios are admittedly highlyspeculative, but the latter is advanced here simply to showthat `delayed zygotic meiosis' does not logically require amulticellular sporophyte.

Regardless of its evolutionary origins, the land plantsporophyte typically takes the form of an unbranched orbranched cylinder in contrast to the diversity in body shapeobserved for the gametophyte generation of charophyceanalgae and embryophytes, which can be either axial(cylindrical) or thalloid (dorsiventral) in symmetry.Arguably, the ùnity of type' characterizing the land plantsporophyte re¯ects the unity of the `condition of existence'and the reproductive role played by this ìntercalated'generation (i.e. to produce, elevate, and disperse spores intothe air above the substrate), whereas the diversity in charo-phycean or embryophyte gametophyte symmetry mayre¯ect greater latitude in aquatic or semi-aquatic habitatsin terms of the successful fertilization of eggs by motilesperm and the survival of zygotes. In this sense, the landplant sporophyte generation may be viewed as an adap-tation to the aerial environment, whereas its correspondinggametophyte generation retains the àquatic' legacy of itsalgal ancestors.

Under any circumstances, the cylindrical geometryachieved by the apical and intercalary meristematic growthof the land plant sporophyte confers numerous physiologi-cal, mechanical, and reproductive advantages. As noted, acylinder can continue to elongate without sustaining areduction in surface area with respect to volume. Likewise,a vertical cylinder incurs little or no bending moment and isone of the few geometries that can grow in length without

Body Plans 431

sustaining a signi®cant reduction in its ability to harvest

FIG. 18. Morphology (A±C) and hypothetical reproductive biology (D and E) of the charophycean-like fossil alga Parka decipiens. A and B,Ventral and dorsal views of a Parka thallus. A, Ventral view of discoid pseudoparenchymatous thallus with a holdfast. B, Dorsal view of thallusshowing reproductive structures containing cells with thick walls containing sporopollenin and lacking haptotypic markings. C, Dorsal view of aportion of thallus showing three reproductive structures one of which is cut open to show thick-walled cells. D and E, Two scenarios for theformation of cells with thick walls (indicated by bold outlines) lacking haptotypic markings. D, Within reproductive structures, zygotes dividemeiotically and then mitotically to produce a number of haploid cells that subsequently form cell walls. E, Within reproductive structures, zygotesdivide mitotically to produce a population of diploid cells with cell walls; diploid cells subsequently divide meiotically after their release fromreproductive structures. In this scenario, `delayed zygotic meiosis' does not establish a multicellular sporophyte generation. See text for further

details (Fig. A±C adopted from Niklas, 1976).


light (Niklas and Kerchner, 1984). And, because the axialand torsional second moments of area of a circular crosssection are equivalent regardless of how the cross section isbisected (Wainwright et al., 1976; Niklas, 1992), a teretecylinder is especially well suited to resist externally appliedbending or twisting forces. Finally, in moderate to highwinds, a cylinder generates a thicker boundary layer and aconcomitant reduction in the rate of water loss than either asphere or ¯at plate (`leaf-like' shape) of comparablediameter or length (Nobel, 1983; Niklas, 1994). Since a
cylindrical morphology is simultaneously physiologically
and mechanically adroit and can elongate and elevatesporangia above ground where spores can be released intothe wind for long-distance dispersal, it is not surprising thatthis geometry serves as the basic building block for the mostancient land plant sporophytes.

By the same token, the methods by which land plantsporophytes organize their growth confer obvious bene®ts.An intercalary meristem can contribute to growth in bodylength (and thus elevate the plant apex further aboveground) even after its apical meristem begins to di�erentiate
into a sporangium (Fig. 19A). Among modern-day

FIG. 19. Hypothetical transformation of a monosporangiate sporophyte with a `closed and determinate' ontogeny into a branched poly-sporangiate sporophyte with an òpen and indeterminate' ontogeny (A) similar to an early vascular land plant (B). A, A series starting with auniaxial sporophyte elongating by means of intercalary (ic) and apical meristems. Intercalary meristem elevates sporangium after apical meristemdi�erentiates into a sporangium (sp). Bisporangiate sporophyte results from bifurcation of apical meristem before sporangium formation andcontinues to grow in length by means of intercalary meristems. Polysporangiate plant with indeterminate growth in body size resulting from apicalmeristematic growth. B, Reconstruction of branched sporophyte of Aglaophyton (Rhynia) major bearing terminal sporangia on aerial axes with

centrally located strands of conducting tissues (after Edwards, 1986).


bryophytes, this mode of growth is generally associatedwith a `closed and determinate' ontogeny that results in amorphologically simple and short-lived sporophyte with a®nal àdult' size and limited reproductive output. Amongthe most ancient vascular land plants, larger sporophyteswith greater reproductive potential were achieved by thebifurcation of apical meristems to produce a population ofapical growing points some of which could reiterate thebifurcation process, whereas others di�erentiated intosporangia. This òpen and indeterminate' ontogeny, whichwas passed on to each of the major tracheophyte lineages,can inde®nitely magnify the bene®ts of potentially rarefertilization events among terrestrial plants whose spermrequire water for survival (Fig. 19A). Manifold meristemsalso open the door for the specialization of body parts formechanical support, photosynthesis and anchorage (the
stem, leaf and root embryophyte organization).
An inde®nite increase in the land plant body plan,however, requires tissues specialized for the bulk transportof nutrients, since aerial portions became progressivelydistanced from the substrate that supplies water and othernutrients. Tissues specialized for mechanical support arealso required to cope with the bending moments generatedin the plant body by gravity and wind pressure. Thevascular tissues of tracheophytes are clear adaptations forrapid nutrient transport. They also provide avenues forhormonal transport, which can be used to control vegeta-tive and reproductive growth patterns. Among the mostancient vascular land plants, vascular tissues were centrallylocated in cylindrical axes where they were least likely toexperience high tensile, compression or torsional shearstresses, but where they were least e�ective in sti�ening orstrengthening organs (Fig. 19B). For these plants, the
epidermis probably served as a high strength `skin' that

t

rigidi®ed the plant body when it was placed in tension bythe hydrostatically in¯atable inner core of thin walledparenchymatous tissue it enveloped (see Niklas andPaolillo, 1997).

Since the sti�ness of any hydrostatic device is a functionof its water content, and at best is low in comparison to itsweight per unit volume, land plants relying on hydrostaticmechanical support are typically con®ned to hydrichabitats and have a comparatively short stature. In contrast,tissues with ligni®ed and thick cell walls are mechanicallyless dependent on water content and are far sti�er andstronger. When placed at or near the perimeter of the crosssection of a vertical or cantilevered stem, such a tissue canresist elastic deformation and provide protection againstherbivory or microbial attack. In this location, however,ligni®ed and thick walled tissues also attenuate the intensityof sunlight, especially in the blue and red wavelengths usedby photosynthetic tissues. Indeed, in the absence ofsecondary growth, the ideal location for structural andphotosynthetic tissues is much the same, which may, inpart, explain why the functional analogues to the foliar leafand the mechanically supportive stem evolved early in landplant history (Chaloner and Sheerin, 1979; Taylor and

434 NiklasÐPlan

Taylor, 1993).

HOMEOTIC GENES AND CLOSINGREMARKS

Currently, we know comparatively little about the evolutionof the various plant body plans. The early history of thevarious algal lineages remains obscure, in part because wellpreserved fossils of the vegetative structure of theseorganisms are infrequently found, and because the assign-ment of these fossils to speci®c lineages becomes highlyproblematic in light of the extensive morphological andanatomical convergent evolution evident among modern-day species. Algal LaÈ gerstatten are known, but these are toostratigraphically scattered to build a su�ciently detailedpicture of algal evolution to adduce plant body plantransformations even in comparatively well known lineages(see Knoll, 1995 and references therein). Likewise, cladisticphylogenetic hypotheses for algae are still in their formativestages of development and those that are currently availableare often based wholly or partly on molecular or cytologicalfeatures whose preservation in the fossil record is unlikelyand which by themselves shed little light on morphologicalevolution (Martin, Somerville and Loiseaux, 1992; Schlegel,1994; Graham and Wilcox, 2000). Detailed developmentalstudies for many important taxa are currently lacking yetbadly needed, especially since this avenue of research holdsparticular promise in shedding light on the mechanismsresponsible for body plan transformations among modern-day algal species. With all the emphasis placed on embryo-phyte growth and development, we are still remarkablyignorant about the developmental details of many import-ant non-vascular and relictual vascular taxa, whicharguably are more re¯ective of the early stages in theevolution of the land plant body plans than those of themore derived seed plants. For all these reasons, any
treatment of the various plant bodies and their evolution
is unavoidably and undeniably highly speculative andidiosyncratic. Yet, this topic is pivotal to our understandingof the history of life, since all but a very few ecosystems aredependent on photoautotrophs as primary producers andsince much of animal evolution cannot be understoodwithout at least passing reference to plant biology.

Clearly, the role of homeotic genes in the evolution ofbody plans needs to be explored. These genes encode fortranscription factors similar to bacterial repressor proteinsand thus appear to be taxonomically ubiquitous and veryancient (Sommer et al., 1990; Davies and Schwarz-Sommer,1994; Gerhart and Kirschner, 1997; Knoll and Carroll,1999). In arthropods, vertebrates and ¯owering plants,these transcription factors can serve as molecular markersfor the position of cells along an organ or body axis(Carroll, 1995; Akam, 1998a,b), and, in both plants andanimals, the activation of individual homeotic genes atdi�erent positions in meristematic or embryonic regions isassociated with patterns of di�erentiation that are main-tained throughout ontogeny. Since the di�erential expres-sion of homeotic genes is correlated with the adoption ofdi�erent developmental fates in di�erent regions of theplant or animal body axis by cells that appear otherwiseequivalent and since mutations at these loci shunt thedevelopment of meristematic or embryonic cell clustersfrom normal to typically dysfunctional developmentalfates, homeotic genes shared by otherwise diverse organ-isms may shed light on why some body plans are highlyconservative and why others are not.

It is now clear that the family of homeotic genesdiversi®ed early in the radiation of the metazoa andpossibly metaphytes. Within some lineages, these genescan be used to establish phylogenetic relationships amongdi�erent groups. Thus, patterns of expression of homeoticgenes can provide markers to relate body plan variants, as isthe case for the head segmentation patterns of chelicerateand mandibulate arthropods. Comparisons of gene expres-sion between more distantly related taxa are far moredi�cult to interpret, however, since we currently neitherunderstand how homeotic gene regulation in¯uences thepathways available for cell and tissue di�erentiation norhow changes in the roles of these genes occurred evenamong closely related groups (see Wray and Abouheif,1998).

Homeotic genes will undoubtedly continue to ®gureprominently in speculation about the evolution of animaland plant body plans. However, homology at the molecularlevel of DNA base-pair sequences does not imply that thedevelopmental or structural features they in¯uence arehomologous. Genes for transcription factors are undoubt-edly very ancient, as attested to by the fact that homeoticgene analogues occur in bacteria, and these factors haveundoubtedly been shuttled within eukaryotic genomes forhundreds of millions of years. Importantly, no gene acts inisolation. Each is part of a variety of complex genetic anddevelopmental cascades such that the product a geneencodes may perform very di�erently depending on themolecular, physiological, or developmental context. Indeed,organisms di�er largely because of combinatorial variations

Body Plans

of genes rather than as a result of an unlimited capacity to

while parsimonious, may be misleading.

Botanical Society of Japan.

Akam M. 1998b. Hox genes: from master genes to micromanagers.

t

endlessly add new ones to those that came before (e.g.Theissen, Kim and Saedler, 1996). Homeotic genes areundoubtedly important to our understanding of the evolu-tion of plant and animal body plans, but their ability topotentially de®ne or transform body plans is expressedwithin a complex genetic and epigenetic milieu of which weare currently incompletely aware.

What is clear is that di�erent body plans in very di�erentplant lineages are capable of extensive morphological andanatomical homoplasy and that this convergence on similarstructural solutions using di�erent ways of achievingorganized growth re¯ects the nearly identical functionalrequirements for plant growth and survival regardless ofphyletic legacy. In turn, these structural solutions areexplicable, or at least quanti®able in terms of the relation-ship between the surface area of the plant body throughwhich plants acquire nutrients and energy, and the livingbody volume (� symplast), which dictates metabolicdemand and the capacity for nutrient utilization. Theopen and indeterminate ontogeny, which characterizes allbut the unicellular (uni-nucleate) plant body plan, permitsthe ampli®cation of body surface area with respect tovolume as overall size increases. The capacity to exchangemass and energy between the plant body and its externalenvironment is thus largely uncon®ned developmentallysuch that very di�erent body plans can converge on thesame or very similar morphologies and anatomies.

The advent of multicellularity characterized by cyto-plasmic (symplastic) continuity permitted the establishmentof di�erent physiological domains within the plant bodythat could serve as a basis for cell, tissue and organdi�erentiation. Although perhaps not overly emphasizedin this review, some of the features characterizing themulticellular plant body, such as cellular di�erentiation,plasmodesmata-like structures, control mechanisms for theorientation of cell cleavage, and cellular di�erentiation, areevident among extant and presumably very ancientcyanobacteria, indicating that the rudiments of multi-cellularity existed well before the advent of the eukaryoticcondition (see Maddock, 1994; Gober and Marques, 1995).This draws attention to the tantalizing possibility thatmulticellularity among the various plant lineages evolved inpart as the result of lateral gene transfer occurring during orshortly after primary endosymbiotic events in the verydistant past. The curious absence of multicellularity inplant lineages believed to have evolved as a result ofsecondary endosymbiotic events presumably involvingunicellular eukaryotes (e.g. euglenoids and cryptomonads)is consistent with this conjecture. The view taken here isthat the genetic and epigenetic phenomena in¯uencing cellcleavage, di�erentiation and morphogenesis are buried deepin evolutionary time and that the expression of thesephenomena among contemporary prokaryotes will providefertile grounds for future research in the evolution of plantbody plans.

Finally, little has been said here regarding the charophy-cean-embryophyte `connection', in large part because theevolutionary relationships between these two plant lineagesare extensively and well reviewed elsewhere (see Graham,

NiklasÐPlan

1993), although in a taxonomic format that rarely addresses

the adaptive relationship between form and function (seeKenrick and Crane, 1997). Among the various plantlineages, the embryophytes, particularly the sporophytegeneration of tracheophytes, are the most conservative interms of their body plan, being largely con®ned to theparenchymatous multicellular variant predicated on acylindrical morphology fabricated by means of intercalaryand apical meristematic regions. In contrast, the charo-phytes manifest a variety of body plans that achieve theirorganized growth di�erently, perhaps re¯ecting the many`degrees of freedom' permitted in an aquatic habitat incontrast to the adaptive versatility of the parenchymatoustissue fabric of embryophytes, which clearly permitted thefull exploitation of the terrestrial landscape. The evolution-ary derivation of the embryophyte body plan from one (ormore) of the multicellular variants seen among extantcharophycean algae remains conjectural, but it cannotescape attention that the latter includes ®lamentous andparenchymatous tissue fabrics constructed from di�use,intercalary, or apical meristematic regions, nor that axial(cylindrical) and dorsiventral body symmetries mimickingthose of bryophyte gametophytes are represented amongmodern-day charophyte species. This suggests that theancestral algal plexus from which extant charophytes andembryophytes evolved and subsequently diverged fromcontained a developmentally rich repertoire. If so, then astrictly `linear' scenario for the transformation of acharophyte-like body plan to the embryophyte body plan,

Body Plans 435

ACKNOWLEDGEMENTS

The author thanks Linda E. Graham (University ofWisconsin) for providing some of the information used toconstruct Table 1 and for her special insights into algalphylogeny and taxonomy; Andrew H. Knoll (HarvardUniversity) for providing information about the ®rstoccurrences of eukaryotic lineages in the fossil record;Michael L. Christianson (Kansas University), DominickJ. Paolillo Jr (Cornell University), Tom L. Phillips(University of Illinois) and James W. Valentine (Universityof California, Berkeley) for their helpful suggestions toimprove an early manuscript; and John A. Raven (Univer-sity of Dundee) and Ichiro Terashima (Osaka University)who, acting as reviewers, provided many helpful suggest-ions. The author is especially grateful to Ichiro Terashimaand Tadaki Hirose (Tohoku University) who generouslyhosted his visit to Japan as a participant in a symposium onplant biomechanics and evolution sponsored by the

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