Evolution of Plant Body Plans

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R E V I E W

The Evolution of Plant Body PlansA Biomechanical Perspective

K A R L J . N I K L A S *

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

Dening `plants' inclusively as `photosynthetic eukaryotes', four basic body plans are identiable 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 dierent body plans. This is ascribed to the facts that theacquisition of nutrients and radiant energy is aected 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 of

unicellular 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 conspecic 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 lawsUnity 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 . . . is

fully 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 periodsof time.

Charles Darwin

IN T R O D U C T IO N

Much has been written about the initial appearance andsubsequent evolution of metazoan body plans, particularly

in 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, heredened 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 andSheerin, 1979; Graham, 1993; Taylor and Taylor, 1993;

Stewart and Rothwell, 1993; Niklas, 1997). This focus has

signicantly advanced our understanding of the evolutionof the embryophytes, but it has largely ignored a complexantecedent history during which dierent 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 evolutionarymodications in a variety of body features that undoubt-edly pregured 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 same

grade level of cytological and physiological organization.Unlike those of the metazoans, the body plans of

plants are dicult to categorize or dene. 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; Giord andFoster, 1989; Niklas, 1997; Graham and Wilcox, 2000). Theperspective taken here is that plant Bauplane are far more

protably discussed in terms of how organized growth isachieved and how dierent tissue fabrics are used to

Annals of Botany 85: 411438, 2000doi:10.1006/anbo.1999.1100, available online at http://www.idealibrary.com on

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* Fax 1 607-255-5407, e-mail [email protected]


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construct the plant body. Importantly, most of these bodyplans have an òpen and indeterminate' ontogenyoneinvolving multiple growing points and persistent cellulardivisions throughout the lifetime of the individual suchthat adult size, geometry and shape are not necessarilydevelopmentally pregured 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 inuence how cell size and shape are

free to change (Green, 1960; Mark, 1967; Preston, 1974;Cooke and Lu, 1992; Niklas, 1992). Perhaps more subtle arethe various developmental constraints that inuence 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 interspecicincreases 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-dependent

variations in the intracellular concentrations of importantcellular components (e.g. photosynthetic pigments). Indeed,allometric (size-dependent) variations suggest that an uppersize 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 inuenced the evolutionof body plans at the cell, tissue, organ, and organismiclevels of organization (Wainwright et al., 1976; Speck and

Vogellehner, 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 quantiable 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 organized

growth. As a consequence, body plan diversication within,and convergence among, dierent 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 briey review the `body plan'concept in the context of the historical debate between `theunity of type' and the `conditions of existence'. This is

followed by a brief discussion of the key features thatdistinguish the comparatively few basic plant body plans,which are dened on the basis of how organized growth isachieved and how, if present, dierent 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 aliations, with the exceptionof our current understanding of the systematic relation-ships among the charophycean algae and their relationship

to the embryophytes (see Mattox and Stewart, 1984;Graham, 1993; Graham and Wilcox, 2000), the phycologicaltaxonomy adopted throughout this paper is that ofBold andWynne (1978). This reference is based largely on morpho-logical rather than molecular information. Arguably, there-fore, it oers a conservative view of body plan dierenceswithin each of the algal lineages (see Table 1), and thus tendsto bias against some of the following.

` U N I T Y O F T Y P E ' V S. ` C O N D IT IO N SO F E X I S T E NC E '

The concept of the `body plan', layout, or Bauplan can be

traced to the work of Georges Cuvier, Richard Owen, andother nineteenth-century comparative morphologists whoshowed that organisms can be classied 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 butteries 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 butteries 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 identied 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 that

the `conditions of existence' take priority over the ùnity oftype'. Darwin, like many others, was impressed by the

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remarkable `match' between body traits and the ecological

conditions in which each particular organism lives and

reproduces. Clearly, his theory of natural selection argued

in favour of the adaptive role of the majority rather than the

minority of body traits.

It is undeniable that some shared ancestral traits have

been conserved long after their initial adaptive signicance

has vanished. The coelom, which evolved more than once,may have been an adaptation for burrowing by soft-bodied

animals, but its current function in the vertebrate body

plan is radically dierent from that of any of its presumed

antecedent functions. Indeed, assertions that otherwisediverse organisms share a common ancestry are based

typically on the presence of ancestral traits. The real issue is

not whether some body plan traits are conserved but why

some traits are lost, whereas others are not. Flightless birds

have reduced ght muscles and wings. Yet, all birds develop

feathers and a beak. Parasitic angiosperms have reduced

leaves, stems, or roots, or lack some of these organs

entirely, but they all retain the capacity to produce owersand vascular tissues.

The typical explanation for the conservation of ancestral

body plan traits is the presence of pivotal developmental

processes whose mutation would be dicult or imposs-

ibleprocesses so basic to how an organism achieves its

organized growth that any signicant deviation would

result in death or severe impairment. It is evident that

`developmental constraints' exist and play an important role

in the conservation of some traits. The so-called spiraldeterminate cleavage of many planktotrophic spiralian

species so rigidly casts the fate of each embryonic cell

early in the four- and eight-cell stage of embryo develop-

ment that it is dicult (although not impossible) to imaginethat 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 from

either 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 dened embryologiesthat give rise to a highly conserved set of body plans (the`unity of type'). Indeed, animal body plans are generally so

conservative 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,1995; Valentine and Hamilton, 1997).

PL A N T B O D Y PL A N S

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 originspresumably as a consequence of primary endosymbiotic

TA B L E 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 2 3

Charophyta4 Chlorophyta Chrysophyta 5 Rhodophyta 6 6 6

Phaeophyta 7 Pyrrhophyta Euglenophyta Cryptophyta8

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.4

Sensu 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.

NiklasPlant Body Plans 413


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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 unicellular

organisms, 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 classied and sorted into dierentlineages 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 benet

of multicellularity (Fig. 2). General appearance and sizealso belie very dierent 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-rootconguration 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 identies onlyfour basic body plansthe 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, pit

connections, shared loricas, stalks, etc. determines whetherthe body plan is unicellular or colonial (e.g. Calcidiscus or

Phaeocystis); (3) indeterminate growth of the multinucleate

cell results in the siphonous body plan (e.g. Bryopsis and

Caulerpa); and (4) symplastic continuity among cells during

and 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 that

can 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 conned to two orientations, cell division can give

rise to branched lamentous, monostromatic, or pseudo-

parenchymatous tissue constructions (e.g. Stigeoclonium,

Volvox and Ralfsia, respectively); and, when cell division

occurs in all three planes, a multicellular body layout is

possible, which can simultaneously manifest a lamentous

and parenchymatous construction (e.g. Fritschiella). Since

each of these three multicellular variants can involve

diuse, trichothallic, intercalary, or apical cell divisions,

or some combination of all four, a large number of multi-

cellular body plan variants can be codied (i.e. 3 cell

division planes 5 meristematic locations 15 variants de

minimis), although the usefulness of doing so is question-

able. Although a number of growing point (meristematic)characteristics collectively inuence whether a variety of

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

capitatus. D, Halimeda opuntia.



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morphological and anatomical features are achieved in aparticular body part or plan (e.g. the duration of activity

and the number of cells involved at each location, as well asthe extent to which cells, tissues or organs dierentiate ordier 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 four

basic plant body plans.

This body plan classication scheme draws sharpattention to the extent to which body plans have diversiedwithin or converged among the various plant lineages and

how they have become conned in number in evolutionarilymore derived groups, such as the Charophyta and Embryo-

phyta (Table 1). For example, all four Bauplane occur in theChlorophyta and Chrysophyta, two of the most species-rich

plant 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 is

not 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 fabricateparenchymatous tissue by means of apical, intercalary, or

FIG . 2. Representative morphologies of the siphonous green alga Caulerpa (AD) 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

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



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diuse meristematic activity. Among the land plants, thelamentous variant of the multicellular body plan may beexpressed transiently in the sporophyte generation (e.g. thelamentous 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 briey 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 `unity oftype' among all the plant lineages. This may reect a

`founder eect' 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 aord the best candidateswith which to study the broad eects of developmentalconstraints on body plan evolution. Alternatively, theembryophyte body plan may confer the highest relativetness 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 congurations 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 gametophyte

protonema and phyllids, respectively). Thus, the `conserva-tive' nature of the embryophyte body plan may be more

karyokinesis

+ cytokinesis(uni-nucleate)

-cytokinesis(multi-nucleate)

determinategrowth

siphonous

indeterminategrowth

colonial

unicellular

multicellular

nosymplastic

continuity

no

aggregation

aggregation

symplastic

continuity

Location of growthdiffuse trichothallic intercalary apical

unbranched filaments

branched filaments, monostroma,pseudoparenchyma

parenchyma

Planeofcelldivision

one

two

three

F IG . 3. Basic plant body plans (unicellular, colonial, siphonous and multicellular), their dening 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 diuse, 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 divisionconned 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.



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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 classication 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 isomorphic

alternation of generations, divergent gametophyte andsporophyte morphologies are reported for some species

(e.g. Ectocarpus, Feldmannia, and Giordia 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 oforideophycean 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 are

nonetheless some exceptions to the uniformity in the bodyplans of the dierent life forms in the life cycles of some

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

Divis

ionplane

three

two

unicellular

primary

one

determinate

multicellular

secondary

> one

indeterminate

Cells:

Tissues:

Organs:

primary walls secondary walls

epidermis, storage, conducting

leaf, axis, attachment

symmetry:

redundancy:

correlation:

form:

radial, or dorsiventral

many or few organs

allocation patterns; allometry

rhizomatous, 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 inuencing the general appearance of the plant body (BD). 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 inuence cellular conguration 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 is

indeterminate (e.g. the phaeophyte Fucus). C and D, Patterns of cell, tissue, or organ dierentiation and a variety of allometric phenomenainuence in part the general appearance and internal structure of the multicellular plant body.



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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 seen

among 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 diering 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 systemwith a double nerve trunk and segmental ganglia).

` C O N DI T I O N S O F E X I S T E N CE ' A N D P L A N T

O N T O G E N Y

It is apparent that the disparity among Bauplane 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 connedby 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 unicellular

uni-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 diuse, tricho-thallic, intercalary or apical cellular divisions at growingpoints that can remain active throughout the lifetime of theindividual. This òpen and indeterminate' ontogeny aordsan 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 conspecics to assume dierentmorphologies 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 conspecics withmore `luxuriant' morphologies growing in less mechanicallyenergetic habitats. In this sense, the morphology and

anatomy of plants, regardless of whether they are acellularor multicellular, are not pregured 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 signicance when weconsider how these organisms manufacture their livingsubstance and how this mode of life is largely dependent on

form and appearance rather than on how the plant bodyachieves its organized growth. Unlike animals, whichcapture their prey or graze on plants in a variety ofdierent ways, all photosynthetic eukaryotes, regardless oftheir phyletic aliation 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 plant

body, 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 measure

of 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 dierent from those that occurwithin the symplast. A meaningful calculation of `volume',therefore, includes neither the cell wall infrastructure anduid-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 dierent 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 inuencing surfacearea to volume ratios are body size, geometry and shape.This may account for body plan divergence in each algallineage, since very dierent plant Bauplane can achieve thesame size, shape or geometry, and thus the same or verysimilar surface area to volume ratios. If true, then body plan

divergence within some lineages may re ect `diuseevolution' and not the intense operation of natural selection



9/28

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, the

dependence of bodily functions on the surface to volumeratio, which is itself dependent on body size, shape andgeometry, helps to explain why species possessing verydierent body plans often converge on similar morpho-logies or anatomies. In these instances, the operation ofnatural selection rather than `diuse evolution' is the mostlikely explanation.

T H E U N IC E L L U L A R B O D Y PL A N

Small body size confers numerous metabolic advantages, asis evident from a biomechanical examination of theunicellular Bauplan, which is the most ancient among all

plant 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 diusion. 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 cit0co cit0X5

!

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 coecient of j, (co ci)t0 is theinitial dierence in the external and internal concentrationsof j at time zero, and (co cit0X5 is the dierence in theexternal and internal concentration of j when ci co/2.Since ln[(co cit0/(co cit0X5] ln[(co 0)t0/(co co/2t0X5] ln 2 0.693, it follows that t 0.693V/PjS (seeNobel, 1983; Niklas, 1994). This formula shows that, forany series of unicellular organisms diering in size butsharing the same geometry and shape, the time required toconcentrate nutrients within cells by means of passivediusion increases dramatically with increasing cell size(Fig.5). Similar results are obtained when the eects 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 eective at harvesting light as thesize of these units increases. For example, this `packageeect' is quantitatively expressed for spherical cells by theformula

I IoeknAad 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 coecient of water (and any dissolved

substances), 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 a

column of waterthe 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 G r2).Stokes' law also indicates that v is proportional to thedierence between the density of an organism and itssurrounding uid a parameter that can be altered bymany unicellular plants by regulating vacuolar andcytoplasmic contents.

Despite the phenotypic plasticity evident among con-specics of uni-nucleate and unicellular plant species, theevolution of this body plan was undoubtedly inuenced byits `closed and determinate' ontogeny, which pregures

adult body (cell) size, shape and geometry. However, inter-specic comparisons among unicellular species indicate that

Cell surface area (m2)

10101 102 103 104 105

102

103

104

105

Timefordiffus

ion(s)

FI G . 5. Estimated time for the passive diusion 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 passivediusion 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 diusion 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).



10/28

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.Specically, 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. SG V0

X70) (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 signicantly from the `2/3-power rule' (i.e. S G V0

X67)(Fig. 7A) which describes the relationship expected betweenSand Vfor any series of objects diering 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 either

more 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 dierences observedamong species evidence an `adaptive' trend.

In this regard, computer simulations indicate thatinterspecic dierences 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 diering in cell size (Fig. 7B). These

simulations provide evidence, albeit circumstantial that thesize-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 the

presence of vacuoles or intracellular crystals dieringin size) fails to keep pace with increasing body volume

Surfacearea(m2

)

Volume (m3)

Size

Geom

etry

Shape

= 0.667

= 0.699

simulation

plants (algae)

A

B

10111010108107100 106103102 104 105101

1011

1010

109

108

107

100

106

103

102

104

105

101

109

FI G . 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 diering in size(volume) (shown by dashed line with a 0.667) and a computersimulated series of dierent geometries and shapes diering 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). The

series begins with small spheres and spheroids and ends with largeslender cylinders similar in appearance to unicellular plants (Adoptedfrom Niklas, 1994).

0.16

0.14

0.12

0.08

0.06

0.04

0.02

0.00

0.10

4 m

8 m

16 m

64 m

400 450 500 550 600 650 700 750

Wavelength of light (nm)

Averageabsorp

tion(m2)

F IG . 6. Average absorption of light by a population of spherical cellsdiering 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

(Adopted from Niklas, 1994).



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(i.e. M G V0X81) (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 G M0

X32) 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 interspecic 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 G M0

X79) such that the concentration of chlorophyll perunit cell mass decreases (Fig. 9A). Likewise, phosphorus

and nitrogen subsistence quotas fail to keep pace withincreasing 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 body

plan is conned to a comparatively small size, and why theorganisms possessing this body plan are generally conned

A

B

104

103

102

101

100

103

Body mass (pg C)

Volume (m3)

102

101

100

103

101

101 100 101 102 103 104

101 102 103 104 105 107 108

y = 0.008 x0.99

r2 = 0.99

y = 0.92 x0.25

r2 = 0.90

y = 0.08 x0.32

r2 = 0.45

Bodymass(pgC)

102

105

101 109100 1010

106 107

Growthrate(h1)

unicellular

metazoans

metaphytes

unicellular

algae

bacteria

y = 0.003 x0.81

r2 = 0.96

101

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

101

Body mass (pg C)

Volume (m3)

Chlorophylla(p

gC)

Subsistencequotas

phosphorus

nitrogen

104

103

102

101

100

101

105

106

101 100 101 102 103 104 105

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

FI G . 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).



12/28

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 to

metabolize 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 environmentalconditions.

T H E C O L O N IA L A N D SIPH O N O U SB O D Y PL A N S

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 uidow patterns can be modied and used to remove sub-stances or concentrate anti-microbial or toxic substances to

deter 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 lowuid-ow speeds, nearly stagnant physiological conditionscan prevail. In this environment, the ability of a cell toexchange mass with its surrounding uid can be crudely

gauged by the equivalent external conductance t for anobject of similar size, shape and geometry (Niklas, 1994). Inelectrostatics, t equals the quotient of the capacitance andthe permittivity of the medium, and, for a single sphere (cell)with radius r, t1 4pr $ 12X6rY whereas, for two touchingspheres (cells) withequivalentradii r,t2 8p (ln 2)r $ 17

.4r.Since [(t2/t1) 1] 100% 38%, the analogy betweenmass exchange and conductance suggests that two adjoiningcells may physiologically benet 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 diusion.

Also, adjoining cells will compete for the same resources (butby 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 other

substances. 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 modifyinguid ow patterns, thereby assisting in the circulation ofinorganic nutrients around cell clusters. A matrix issimilarly benecial 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. Some

individuals 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 `adult' assumes the role of a`gamete' (Fig. 10). It is not surprising, therefore, thatcolonial life forms have evolved independently manytimes among the dierent algal lineages (Table 1).

Multicellular Unicellular

Number of generations

Numbero

f

individuals

0 2 4 6 8 10

104

103

102

101

100

multicellular

unicellular

FI G . 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). Each

individual is assumed to survive across all generations (Adopted fromNiklas, 1997).



13/28

However, a sharp biological distinction must be drawnbetween the colonial body plan and the colonial growthform. The latter is sometimes adopted temporarily by a

variety 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 loseagella, 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 multicellular

body plan in distantly related groups of organisms (seeKaiser, 1993 and references therein). Regardless of theinferences that can be drawn from these organisms, manyexamples suce to show that the `colonial' ( palmelloid)growth habit is adopted by species with a variety ofdierent 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. 11BE).

Yet, even among bona de colonial species, a further

distinction must be drawn between colonies with an `openand indeterminate' ontogeny involving the mitotic division

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



14/28

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 apregured 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 beneted from the presence ofconspecics, 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, among

the 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 itdicult 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 `open andindeterminate' ontogeny that arguably confers some

advantages 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 canindenitely 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 thatSaV 2arY 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 cytologicalconguration minimizes the transport distance (and thus

the transport time) for the passive diusion of nutrients orwastes across the cell membrane and wall.

The comparative rarity of the siphonous body plan maybe related to the fact that microbial or viral infections aredicult 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 a

substantial 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 modication 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 collective

volume is proportional to the volume of the cytoplasmenveloped by their single cell wall. This phenomenology isconsistent with the `energid' 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 be

predicated 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 dene what have been callednuclear-cytoplasmic domains (see Brown and Lemmon,1992). Genetic alterations of these systems arguably mayaccount for evolutionary transitions between uni- andmulti-nucleate unicellular organisms.

F IL A ME N T O U S MU L T IC E L L U L A R B O D YPL A N VA R IA N T S

The evolution of the multicellular body plan was a major

evolutionary achievement that required precise control overthe plane of cell division and the establishment of



15/28

cytoplasmic (symplastic) continuity among adjoining cells.Interestingly, the capacity to regulate cell division planes,dierentiate cell types, and fabricate unbranched laments,branched laments, and cellular congurations similar ingeneral appearance to parenchyma (i.e. pluriserate la-ments) is evident among the cyanobacteria (e.g. Cylindros-

permum, Hapalosiphon and Fischerella, 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 adjoining

cells (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 features

of eukaryotic multicellularity may have been preguredduring 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 cytokinesis

and the retention of cytoplasmic `bridges' or the formationof plasmodesmata between derivative cells immediatelyestablish the unbranched lamentous multicellular bodyplan. Diuse 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 unicellularorganism is consistent with the widely held view that the

FIG . 12. General morphology of representative cyanobacteria withunbranched and branched lamentous (A and B) and parenchyma-tous-like ( pluriserate) constructions in which symplastic continuity

may be maintained among adjoining cells (C). A, Cylindrospermum sp.B, Hapalosiphon sp. C, Fischerella sp.

FI G . 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.



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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 and

Ulothrix 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 conned to theperpendicular direction with respect to the body axis.Subsequent evolutionary modications were required toalter this mechanism such that two or more orthogonalplanes of cell division become possible to form branchedlaments 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 of

the 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 of

the phragmosome as factors inuencing 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 plan body size canincrease by the addition of cells that metabolically orreproductively benet by virtue of their comparatively small

size and large surface area to volume ratios, and theorganism as a whole can devote some cells to sexual

reproduction without sacricing 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 chemical

exchange 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-celltracking of macromolecules can be used to generatechemical gradients to regulate cell, tissue, and body planpolarity, help dene where and how long meristematicactivity occurs, and that can isolate reproductive cells by thedissolution of symplastic continuity (Kwiatkowska, 1988).

Patterns of cellular dierentiation become possible aswell, since plasmodesmata are known to preferentiallytrac dierent hormones (Drake and Carr, 1978, 1979) and

since 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 specied by cell-to-cell coordinated eorts, 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 of

mechanical 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 forcesthe 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 0X5ru2SplanCL

FD 0X5ru2SpCD

FA rCmVaY

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 coecient, Sp is thesurface area of the plant body projected against thedirection of uid ow, CD is the pressure (drag) coecient,Cm is the inertia coecient, Vis plant body volume, and a isthe uid acceleration (Denny, 1988; Niklas, 1994). In an

environment with rapid and steady uid-ow, the planformarea and the projected area of a exible lamentous body



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plan roughly equal the cross-sectional area of an averagecell in the lament, and thus the lift and drag forces on alament 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 coecients for a cylinder are independent of thelength of a cylindrical lament, whereas the inertiacoecient ranges from 1.62 to 2.0 for a cylinder withlength to diameter ratios of 1.2 and innity, respectively.Consequently, the principal variables inuencing the net

hydrodynamic 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 indenite increase in body volume canengender large acceleration forces, provided the organismgets big enough to experience turbulent ow regimes, thelamentous body plan, whether branched or unbranched,can metabolically benet, 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 exchange

between the plant body and its surrounding water andthus higher respiration and photosynthetic rates (see Parodiand Ca ceres, 1991).

It is worth noting that cell division in two orthogonaldirections is required to construct branched laments. Thisalso aords 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 deectingand/or folding upon themselves downstream. Extensible

hollow tubes can also sustain very large recoverable elasticlongitudinal deformations by circumferential contraction.

Multicellular plants composed of a pseudoparenchyma-tous tissue can be viewed as having a modied lamentousbody layout when diuse, trichothallic, or apical celldivisions are not developmentally coordinated to producea species specic body shape or geometry. Variants ofthis kind are especially well represented by species currently

assigned to the Leathesiaceae in the Phaeophyta(e.g. Leathesia diormis). In contrast, a bona de pseudo-parenchymatous body plan is achieved when branched orunbranched laments are formed and regulated by specicmeristematic regions whose activities are coordinated toproduce species specic 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 `internal' withrespect to the outer surface of cells but that is topologicallyexternal with respect to the organism and the uid

surrounding it. This extracellular but `inner 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 forcesdierently depending on the direction these forces areapplied with respect to the three principal body axes. Tissuemechanical anisotropy may be especially important toorganisms living in high-energy, wave-swept habitats.

T H E PA R E N C H Y MA T O U S PL A N T B O D Y

Arguably, the most evolutionarily derived variants of themulticellular plant body plan are constructed out ofparenchymatous tissues produced by spatially discretemeristematic regions rather than diuse cell division. Thecapacity to establish or sever protoplasmic interconnectionsamong all the surfaces of adjoining cells aords 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 the

physiological eorts 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 benets 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 dened meristems that are eitherintercalary or apical in location. Unfortunately, the fossilrecord does not provide sucient information about how

this body plan conguration evolved in each of the plantlineages in which it occurs. It is nonetheless tempting to

u FL

FN

FD FA

Splan =r2

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 inuences the magnitude of FL and FD (seetext for formulae), is independent of body length and depends on

cell radius r.



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derive the parenchymatous plant body and its specializedmeristematic regions from either a lamentous or pseudo-parenchymatous precursor in which meristematic activitywas conned to developmentally specied locations, pre-sumably as a consequence of chemical and physical con-trolling mechanisms relying on plasmodesmata tracking.

Some evidence supports this point of view. Among thecharophycean algae, which probably share the same lastcommon ancestor with the embryophytes, meristematicgrowth is typically conned to the apices of laments,whereas, among parenchymatous charophycean species,meristematic growth is conned 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). Specically, 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 the juxtaposition 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. 15EI).

Scenarios such as these, however, are highly speculativesince the sequence ofColeochaete species purported to showthe evolution of parenchymatous tissue from branchedlaments (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 lamentous

body layout similar to that of Chara. In the absence ofadditional data, therefore, the origins of parenchymatous

plants with well dened meristems, apical or otherwise,

remain conjectural.Regardless of its evolutionary origins, a parenchymatous

plant body with meristematic activity conned largely to

one or more apical cells or cell clusters is advantageous in a

number of respects. Body size can be increased indenitely

by the exogenous addition of new body parts at growing

tips without interrupting the bulk ow or the active

transport of metabolites by specialized tissues that develop

and mature in older portions of the plant. Reiteration of the

body layout is made possible by repeated bifurcation of

growing points to produce a ramied (branched) morpho-

logy. Multiple apical meristems provide a margin of safety

for the continued existence of the organism, since the life of

the individual is not cut short by the decapitation or deathof one or more of its distal parts. Some meristems can be

FI G . 15. Scenarios for the evolution of a parenchymatous tissue fabricconstructed by means of a marginal (peripheral) zone of meristematiccells (AD) and the evolution of an apical meristem consisting of onecell (capable of dichotomization) from a marginal (peripheral) zone ofmeristematic cells (EI). 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 to

cells outlined in A). An intermediate condition between branchedlaments 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

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Evolution of Plant Body Plans