What makes plants different? Principles of extracellular matrix function in ‘soft’ plant tissues

Comparative Biochemistry and Physiology Part A 125 (2000) 151–167

Review

What makes plants different? Principles of extracellularmatrix function in ‘soft’ plant tissues�

Winfried S. Peters a,*, Wolfgang Hagemann b, A. Deri Tomos c

a AK Kinematische Zellforschung, Biozentrum der J.W.Goethe-Uni6ersitat, Marie-Curie-Str. 9, D-60439 Frankfurt, Germanyb Werderplatz 11a, D-69120 Heidelberg, Germany

c Ysgol Gwyddorau Biolegol, Prifysgol Cymru, Bangor, Gwynedd LL57 2UW, Cymru, UK

Received 15 June 1999; received in revised form 26 October 1999; accepted 4 November 1999

Abstract

An overview of the biomechanic and morphogenetic function of the plant extracellular matrix (ECM) in its primarystate is given. ECMs can play a pivotal role in cellular osmo- and volume-regulation, if they enclose the cell hermeticallyand constrain hydrostatic pressure evoked by osmotic gradients between the cell and its environment. From anengineering viewpoint, such cell walls turn cells into hydraulic machines, which establishes a crucial functional differencesbetween cell walls and other cellular surface structures. Examples of such hydraulic machineries are discussed. Thefunction of cell walls in the control of pressure, volume, and shape establishes constructional evolutionary constraints,which can explain aspects commonly considered typical of plants (sessility, autotrophy). In plants, ‘cell division’ byinsertion of a new cell wall is a process of internal cytoplasmic differentiation. As such it differs fundamentally from cellseparation during cytokinesis in animals, by leaving the coherence of the dividing protoplast basically intact. Theresulting symplastic coherence appears more important for plant morphogenesis than histological structure; similarmorphologies are realized on the basis of distinct tissue architectures in different plant taxa. The shape of a plant cellis determined by the shape its cell wall attains under multiaxial tensile stress. Consequently, the development of form inplants is achieved by a differential plastic deformation of the complex ECM in response to this multiaxial force(hydrostatic pressure). Current concepts of the regulation of these deformation processes are briefly evaluated. © 2000Elsevier Science Inc. All rights reserved.

Keywords: Plant cell wall; Plant extracellular matrix; Plant morphogenesis; Cell division (role in morphogenesis); Pressure/volumeregulation; Plant biomechanics; Cell theory

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1. Introduction

The introduction of the term ‘cell’ into biologywas intimately connected to the uniqueness of the

higher plants’ extracellular matrix (ECM), the cellwall. After the fine structure of biological materialbecame accessible due to the development of mi-croscopes in the 17th century, Robert Hookedescribed cork as consisting of numerous ‘cells’ ofan average length of about 20–30 mm (Hooke,1665). As we know today, Hooke had observedthe network of enduring cell walls of a deadtissue. The ease at which plant cells are identified,

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W.S. Peters et al. / Comparati6e Biochemistry and Physiology, Part A 125 (2000) 151–167152

because of the conspicuousness of their walls,contributed much to the acceptance of the celltheory, according to which higher organisms con-sist of elementary units (i.e. cells; Harris, 1998).Noteworthily, in the probably most influentialpaper on this topic the idea had not been devel-oped as a unifying biological concept, but as ahypothesis to explain the distinctiveness of theplant (cellular) from the animal (non-cellular)kingdom (Schleiden, 1838).

Today it is widely assumed that multicellularityis a common feature of higher organisms. Here weapproach the concept of multicellularity from acomparative viewpoint. We will argue that specificmechanical functions of the plant ECM duringcell division and morphogenesis establish con-structional constraints on plant evolution, whichare responsible for the apparent uniqueness ofplants in the living world. Our approach, whichunderlines the differences, is intended to provide aview which complements the unifying aspects ofmodern cell biology. The existence of such com-mon principles of ECM function is highlighted byrecent studies on embryo development in brownalgae of the genus Fucus. Cell fates were found tobe controlled by determinants in the cell wallduring certain developmental stages (Berger et al.,1994; Quatrano and Shaw, 1997). More generally,the spatial regulation of cellular morphogenesisseems to require the cooperation of cytoskeleton,ion channels, targeted exocytosis, and ECM(Goodner and Quatrano, 1993; Brownlee andBerger, 1995; Shaw and Quatrano, 1996; Fowlerand Quatrano, 1997; see also Lord and Sanders,1992). While it is trivial to zoologists (Yamadaand Akiyama, 1984; Ettinger and Doljanski, 1992;Bennett and Gilligan, 1993; Ingber et al., 1993),the idea that ECM interaction with the cytoplasmis of crucial importance for morphogenetic pro-cesses appears almost revolutionary to plant phys-iologists (Roberts, 1994).

In plant tissues which are still able to grow, cellwalls have not yet undergone secondary changes.Such secondary modifications (e.g. lignification)can, in a sense, be considered biomechanicallyanalogous to the process of cartilage calcificationin the vertebrate ECM. Since in tissues with sec-ondary cell wall modifications the primary ECMfunction is obscured, we here will focus on ‘soft’tissues. The reader interested in the biomechanicsof ‘hard’ plant tissue is referred to the pertinentliterature (e.g. Mosbrugger, 1990; Mattheck, 1991;

Niklas, 1992). We will also refrain from consider-ing the molecular structure of primary cell walls,although in recent years substantial progress hasbeen made in the field (Preston, 1979; Labavitch,1981; McNeil et al., 1984; Brett and Hillman,1985; Fry, 1986; Cassab and Varner, 1988; Mc-Cann and Roberts, 1991; Bolwell, 1993; Carpitaand Gibeaut, 1993; Cosgrove, 1997). Many bio-chemically distinct types of cell wall exist (Percivaland McDowell, 1967; Dodge, 1973; Mackie andPreston, 1974; Kandler, 1982; Carpita andGibeaut, 1993), and yet most of them ‘respond tothe same cues and perform the same physicalfunctions during growth, but they do so with verydifferent kinds of molecules’ (Carpita andGibeaut, 1993). Thus principles of ECM functionin plants will not emerge from molecular analyses,but rather must be sought on the cellular, organ,and organismic level.

2. The primary function of cell walls and itsconsequences

A decisive step in the origin of life was thedevelopment of a border, by which ‘living’ unitsbecame separated from their environment (Mo-rowitz et al., 1988; Fleischaker, 1990; Morowitz,1992). This interface likely was a layer of am-phiphilic molecules, similar to the lipid mem-branes found in living organisms (Deamer, 1986;Israelachvili et al., 1977; Hargreaves and Deamer,1978). Lipid membranes are permeable to waterand small uncharged molecules, but less so for bigor charged ones. Every living cell, be it evolution-arily primitive or modern, has to solve the prob-lems caused by differential membranepermeability to maintain its chemical compositiondifferent from that of the outer solution. Theintracellular presence of macromolecules, forwhich the membrane is practically impermeable,turns cells into Donnan-systems. Osmotic gradi-ents result, providing the driving force for waterfluxes. As a consequence cells are in permanentdanger of ‘death-by-flooding’ (for a readable re-view see Stein, 1995). Two solutions to this prob-lem have been realized in evolution (Fig. 1).First,active ion transport may build up chemicalgradients, and work continuously against theirdissipation. A well-understood example is theNa+–K+-ATPase common in animal cells, which

W.S. Peters et al. / Comparati6e Biochemistry and Physiology, Part A 125 (2000) 151–167 153

in effect immobilizes sodium extracellularly, sothat the osmotic impact of non-permeating intra-cellular macromolecules is compensated for(Stein, 1995; see also Sarkadi and Parker, 1991;Hoffmann and Dunham, 1995). Second, cells maylive in a hermetically sealed ECM, strong enoughto mechanically counteract the hydrostatic pres-

sure (turgor) that builds up intracellularly as aconsequence of osmotically driven water influx.This type of construction, which is relatively in-sensitive to changes in internal hydrostatic pres-sure, dominates among procaryotes, fungi, andplants. It is a telling detail that in plants plasmamembrane transport is energized by the protonelectrochemical gradient created by H+-ATPases(Sze et al., 1999). Concentrations of protons pluscorresponding hydroxyl in biologically relevantfluids are far to low to contribute significantly tothe osmotic balance between cytoplasm and extra-cellular space. Thus, membrane energization iscybernetically uncoupled from osmoregulation inplants, but not in unwalled animal cells.

Our cell-mechanic approach includes a func-tional characterization of the term ‘cell wall’: wehere define cell walls as specialized types of ECM,which are able to restrain intracellular hydrostaticpressure. It is clear that some structures usuallyreferred to as ‘cell walls’, such as the perforated,composite shells or scales that occur among uni-cellular algae (Dodge, 1973; Preisig et al., 1994),do not comply with this functional definition; theyrather are biomechanic analogues of the shellsfound in radiolarians, foraminifers, or heliozoa.The distinction between walls and shells is crucialfrom a functional viewpoint. To avoid ambiguity,we here use the term ‘plant’ only when referringto organisms possessing a functional wall.

The existence of two different strategies of es-cape from the ‘death-by-flooding’ threat does ofcourse not exclude intermediate solutions. Gener-ally, bacteria and plants possess membrane trans-

Fig. 1.

Fig. 1. Cartoon showing fundamental differences betweenplant and animal cells. (A) In animals, the plasma membrane(green) is not covered by a cell wall, and cells may be motile.Osmotic stability is achieved by active solute transport, exem-plified here by the Na+–K+-pump (arrows). Complete sepa-ration of daughter cells during cytokinesis is brought about bythe activity of the cytoskeleton (red). (B) In plant cells theplasma membrane (green) is pressed against a rigid cell wall(black), which counteracts internal hydrostatic pressure whilepreventing motility. The primary electrogenic pump in plantplasma membranes translocates protons (arrows), which isosmotically irrelevant. During cell division, Golgi-derived vesi-cles (violet) containing cell wall material are guided by thecytoskeleton (red) to form the cell plate, which develops intothe new wall. During the process, protoplasts are not sepa-rated: cytoplasmic connections (plasmodesmata), throughwhich strands of ER extend, remain. N, nucleus; blue struc-tures, endomembranes other than Golgi. Adapted fromLackie, 1986; Hagemann, 1991.


port capacities, which control intracellular solutecomposition and perform osmoregulation (e.g.Anthony, 1988; Kornberg and Henderson, 1990;Logan et al., 1997; Sanders and Tester, 1997).Under certain conditions some bacteria loosetheir cell walls and establish so-called ‘stable pro-toplast type L-forms’. In some cases these wereshown to acquire a limited ability for osmo- andvolume regulation during the course of manygenerations (Gumpert and Taubeneck, 1983).Switching between walled and unwalled statesoccurs frequently among algae (e.g. Kniep, 1928).These organisms combine the advantages of thewalled (low energetic costs for volume control andstabilization of form) and unwalled (motility; abil-ity to perform phagocytosis; ability for cells tomerge and thus for sexual reproduction) types ofconstruction. Noteworthily, switches betweenwalled and unwalled stages occur only in unicellu-lar species, or in unicellular stages in the life cycleof multicellular ones (spores or gametes). On thecontrary, multicellular plants as such are notknown to switch to an animal-type mode of vol-ume regulation. At least two reasons are conceiv-able. First, if a multicellular plant abandons itscell walls, a number of disjointed subunits resultinstead of a multicellular wall-less organism. Thisprocess occurs in the laboratory, when protoplastsare produced from plant tissue with the help ofwall-digesting enzymes. Second, wall-less cells de-pend on the cytoskeleton for shape control andlocomotion. Plant cells possess a fully functionalcytoskeleton, which plays an important role in thespatial organization of the cytoplasm. However,no cytoskeletal continuity exists between cells in amulticellular plant. Therefore the required coher-ent organization of the mechanically active ele-ments within the organism is guaranteed duringthe transition from the walled to the unwalledstage in single cells, but not in multicellular units.

A number of implications relevant for cell func-tion and evolution follow from the above con-structional considerations (Sussex, 1974; Petersand Felle, 1992). First, in walled cells a step-gradi-ent of hydrostatic pressure occurs across theplasma membrane, which can be in excess of 2MPa (e.g. Wiencke et al., 1992; Franks et al.,1998). This pressure may be utilized to mechani-cally stabilize the plant body, or to perform me-chanic work. Because lipid membranes cannotsustain significant mechanic forces, similar pres-sure gradients across plasma membranes do not

exist in organisms without functional cell walls.Even the most extreme values postulated for someunwalled cell-types (about 0.1 MPa; Bereiter-Hahn and Strohmeier, 1987) are only a fraction offigures commonly measured in plants. Second, forcells that either have lost or never had acquiredmembrane transport capabilities efficient enoughto perform pressure regulation by ion pumping,the possession of a functional wall is a construc-tional constraint: any mutant impaired in wallsynthesis will be eliminated from the evolutionaryprocess. Third, walled cells are incapable of re-peated fast movements. Thus plants must be ses-sile, if their size exceeds the limit forflagella-driven locomotion. Fourth, multicellularplants will depend on types of nutrition and en-ergy, which can penetrate their hermetically sealedECM by diffusion, or as radiation. This leavesonly two options: plants may be saprophytic (asmost fungi), or autotrophic (as all green plants),or a mixture of both. Fifth, the position of a cellrelative to its neighbors is fixed in a tissue consist-ing of walled cells. Thus regulation and mecha-nisms of morphogenesis in multicellular plantsmust be expected to radically differ from thesituation in animals, where cell migration is animportant factor (Thiery et al., 1985). The trans-fer of zoological models of morphogenetic mecha-nisms to plants therefore appears problematic(Trewavas, 1981, 1982; Hathway, 1990).

3. The nature of cell divisions and multicellularityin plants

The development of the concept of multicellu-larity was triggered by the conspicuous compart-mentation of the plant ECM. In a historical view,the modern concept of the cell as a plasma mem-brane bound protoplast, forming the ‘elementaryunit of life’, is a secondary achievement (Harris,1998). In this context it appears worthwhile toreconsider the nature of cell division in plants andanimals.

Typically, animal cell mitosis ends with theisolation of two daughter cells from each other bya cleavage furrow (White and Borisy, 1983; Rap-paport, 1986). In higher plants the situation isdifferent (Fig. 1). Here the cell plate, i.e. the newcross-wall, builds up within the cell between thedaughter nuclei in a centrifugal manner. New wallmaterial is delivered by Golgi-derived vesicles.


The process is controlled by the phragmoplast, aspecialized cytoskeletal structure (Gunning andWick, 1985; Samuels et al., 1995; Staehelin andHepler, 1996). Notably, a cell plate does notseparate the daughter cells: numerous strands ofER cross the plane of cell plate development, andat these locations pores remain (Lucas et al., 1993;Kragler et al., 1998). These so-called plasmodes-mata allow for intercellular movement of macro-molecules (McLean et al., 1997) or even nucleiand plastids (Zhang et al., 1990), and electricalcoupling (Overall and Gunning, 1982; Racusen,1976). A cell plate becomes part of the ECM aftermaking contact with the walls of the mother cell.From this stage on its composition and moleculararchitecture is modified and controlled mainly byexocytosis (Battey and Blackbourn, 1993), and thepeculiar mechanism of cellulose synthesis, bywhich cellulose microfibrils are synthesized duringthe process of glucose extrusion into the extracel-lular space (Delmer and Amor, 1995). These pro-cesses resemble the excretion of ECM material inanimal cells. However, so-called cell division inplants is not analogous to cytokinesis in animals,which leads to the separation of daughter cells.Rather it is a process of internal cytoplasmicdifferentiation, which leaves the coherence of thesymplast, i.e. the entirety of the cytoplasm, funda-mentally unaffected. Symplastic continuity seemsindispensible for plant development and function(Lucas et al., 1993), as indicated by the frequentdevelopment of secondary plasmodesmata inwalls of mature cells in algae and higher plants(even between cells of different species, as ingrafts; Kollmann and Glockmann, 1985). The factthat guard cells, a highly specialized cell type,acquire symplastic isolation during cellular mor-phogenesis (Wille and Lucas, 1984; Palevitz andHepler, 1985), does not question the generalconclusion.

Most contemporary text-books of cell biologyask students to conclude ‘that the planes of celldivision, together with cell enlargement, determineplant form’ (Alberts et al., 1989). However, it hasbeen argued that the notion of a regulatory func-tion of cell divisions in plant morphogenesis isbased on interpretations implied by the cell-theoryrather than on empirical facts (Kaplan, 1992). Asan alternative, an organismal theory was pro-posed (Kaplan and Hagemann, 1991; Hagemann,1992, 1999), which is related to arguments raisedagainst the cell-theory in the last century

(Hofmeister, 1867). One of its tenets is thatgrowth and morphogenesis in plants is controlledby mechanisms acting on the organ or wholeplant level. Vegetative cell divisions, interpreted asinternal differentiations of an enlarging symplast,are viewed as a consequence of growth ratherthan its cause. Thus morphogenesis should bebasically independent of histological features inplants. Considerable evidence supporting thisview has accumulated over the years. For exam-ple, cell division was shown to be nonessential forleaf morphogenesis in wheat (Haber et al., 1961;Haber, 1962). In maize leaves the orientation ofdivision planes appears to lack morphogeneticimportance (Smith et al., 1996; Cleary and Smith,1998). The fate of plant cells during developmentappears generally not limited by cell lineage, butis determined by cell position (Poethig, 1989); itwas concluded that organ shape is ‘self-correctingand not simply the sum of the constituent celldivisions’ (Dawe and Freeling, 1991; see alsoHemerly et al., 1995). Contrary to text-bookknowledge, initiation of organ primordia can oc-cur without cell division (Foard et al., 1965;Foard, 1971). The view that supracellular biome-chanics rather than mitotic activity controls mor-phogenesis in shoot apical meristems (Selker etal., 1992; Green, 1994; Green et al., 1996) appearssupported by reports of epidermal bulges reminis-cent of leaf primordia being induced by localizedtreatment with expansion (Fleming et al., 1997;Reinhardt et al., 1998; but see Green, 1997), anextracellular enzyme which increases cell wall ex-tensibility (Cosgrove, 1997, 1998). Comparativestudies in higher plants imply that neither theestablishment of the embryonic axis nor earlyembryonic development correlate with the geome-try of cell divisions in a regular way (Johri, 1984;Kaplan and Cooke, 1997). In Thale Cress (Ara-bidopsis thaliana) embryos, basic morphogenesisremains unaffected in a mutant with abnormalplanes of cell division (Torres-Ruiz and Jurgens,1994). In embryos of brown algae the plane of celldivision depends on morphogenetic polarity, andnot vice versa (Shaw and Quatrano, 1996; Qua-trano and Shaw, 1997). Moreover, it is demon-strated by numerous examples from unrelatedtaxa that similar morphological structures candevelop on the basis of distinct types of histologi-cal organization (Kaplan and Hagemann, 1991;Cooke and Lu, 1992). But the most stunning casesarguing against a dependence of complex mor-


phogeneses on cell divisions are found among thesiphonous green algae of the genus Caulerpa(Kaplan and Hagemann, 1991; Hagemann, 1992).The bodies of these plants are differentiated intocomposite phylloids (leaf-like structures), cauloids(stem-like structures), and rhizoids (root-like struc-tures; Fig. 2). However, these organisms achievetheir complex morphology in the absence of celldivision; they are multinucleate, but lack internalcell walls. The outer shape is stabilized by trabec-ulae, threads of wall material which act like brac-ing wires on the outer walls. Trabeculae thus servethe same mechanical function as the network ofinternal cell walls in multicellular plants (Niklasand Kaplan, 1991).

It would be naive, though, to take the statementthat ‘cell divisions are a consequence of growth’literally (Jacobs, 1997). The fact that zones ofmitotic activity and high growth rates are more orless separated in plant organs (Green, 1976) ex-cludes such a simplified view. Patterns of cell walldevelopment are evolutionarily adapted to createstructures that serve a multitude of functions, notonly during the course of tissue development, butalso in the adult organs (Barlow, 1994). The com-parative approach shows that more than one solu-tion to this problem exist, and not all of theminclude ‘multicellularity’. Thus studies on cell divi-sion patterns cannot be expected to yield insights

into morphogenetic principles. Neither does a cell-focussed approach promise to elucidate ECMfunction in plant tissues. In studying the role of thecell wall in plant development and function weshould focus on functional domains within theECM rather than on single cells. Such domainsmight be either larger or smaller than the visiblecells. For example, it is long known that in growingshoot organs the peripheral cell walls, and inparticular the outer epidermal wall, bear parts ofthe stresses exerted by the turgor pressure gener-ated in the symplast as a whole (Pfeffer, 1904). Ithas been concluded that in these organs the outerepidermal wall should be regarded as a ‘supracellu-lar organ wall’, which controls organ growth byrestricting turgor-driven expansion (Kutschera,1992, 1995). On the other hand, it follows fromgeometric considerations alone that growth ratesof different portions of the wall surrounding asingle cell differ (Roberts, 1994), and that thereforeinfracellular regulative mechanisms must exist.This is obvious in the tip growth of fungal hyphae,algal rhizoids, pollen tubes, or root hairs (Chen,1973; Green, 1984; Heath, 1990; Wessels,1993;Bartnicki-Garcia et al., 1995; Derksen et al., 1995),or in unicellular algae with complex outer shape(Pickett-Heaps and Tippit, 1974; Mandoli, 1998;Serikawa and Mandoli, 1998). However,

Fig. 2. The green alga Caulerpa taxifolia. (A) Habitus. The unicellular plant consists of a creeping cauloid, from which compositeleaf-like phylloids extend into the free water, and rhizoids grow downward into the substrate. The length of the cauloid shown isapproximately 7 cm. (B) Optical longitudinal cross-section through the growing tip of a phylloid. Internal structures are trabeculae,which connect the outer cell walls and stabilize them mechanically when stretched. In this section plane stretched trabeculae are seenspanning the insertions of the phylloid leaflets (between arrowheads). Width of photograph 380 mm.


Fig. 3. Aerenchyma from the Hard Rush, Juncus inflexus. (A)Cross section through the aerenchyma of an adult stem. Cellsform complex three-dimensional networks with wide air-filledintercellular spaces. Width of photograph 290 mm. (B) Sche-matic representation of the development of aerenchyma fromcompact parenchymous tissue by surface growth of the cellwall portions surrounding the intercellular spaces (modifiedafter Troll, 1959). This growth pattern requires regulation ofdifferential cell wall growth on the subcellular level as well assupracellular coordination.

(cellulose fibrils). The existence of a rigid, three-dimensional ECM counteracting hydrostatic pres-sure prevented the evolutionary development ofcoherent, supracellular cytoskeletal structures inplants. In the context of a mechanic architecturebased on walled cells, reversible movements ofcells or organs can only be achieved by the regula-tion of turgor. Following an engineering approachto plant soft tissue biomechanics, we have to viewcells and tissues as hydraulic machines.

Guard cells have become the paradigm of sucha hydraulic machine. Pairs of guard cells form thefunctional core of stomata, pores in the epidermisof leaves and stems which control transpirationand gas exchange (Hetherington et al., 1998 con-tains a useful collection of papers on variousaspects of stomatal biology). The walls of guardcells are highly anisotropic: at high turgor pres-sure the two cells bulge outwards, increasing thesize of the pore between them (Raschke, 1979).When turgor drops, the cells relax and the porecloses. While the physiological mechanisms of thecontrol of stomatal aperture are still elusive, it isclear that turgor changes in guard cells depend onthe accumulation of various osmolytes (Raschkeet al., 1988). Fluxes of potassium and chloride,which ultimately are energized by the plasmamembrane H+-ATPase, and the intracellular pro-duction of malate seem to play major roles (Ass-mann, 1993; MacRobbie, 1997). Experiments,which focussed on processes occurring in intactleaves during the complete light phase of a dayrather than on short-term reactions of isolatedcells, implicated sucrose as an additional impor-tant factor in guard cell osmo- and pressure regu-lation (Talbott and Zeiger, 1996, 1998). A recentpatch-clamp study on the regulation of potassiumconductivities in guard cell protoplasts demon-strated a positive feedback loop between gradientsin osmotic pressure and the activity of inwardlyand outwardly rectifying channels (Liu and Luan,1998): in the presence of osmotic forces drivingwater flux into or out of the cell, patterns ofpotassium channel activity tended to cause anenhancement of the osmotic gradients. These re-actions would be disastrous in wall-less cells(Lang, 1998), which underlines the fundamentalbiomechanical distinctiveness of plant and animalcells.

The best-studied cases of multicellular motororgans in plants are the pulvini, specialized tissuesat the bases of petioles and laminae, which are

differential wall growth is common also in multi-cellular plants (Sinnott and Block, 1939; an exam-ple is given in Fig. 3).

4. Cell wall function during changes of form andshape

4.1. Re6ersible changes: turgor-dri6en mo6ements

While all elements of the cytoskeleton knownfrom animal cells are present in walled plant cells(Lloyd, 1991; Nick, 1999), their sole function inplants is the spatial organization of the proto-plast, which includes highly dynamic processessuch as protoplasmic streaming. Cytoskeletal con-trol of morphogenesis occurs indirectly, i.e. not bydirectly shaping the cell, but by regulating theorientation of newly synthesized wall elements


responsible for leaf movements in various species.Pulvini adjust the position of a leaf or leaflet byantagonistic changes in turgor of the upper andlower portions of its parenchymous cortex tissue(Fig. 4; Satter et al., 1990). There is agreementthat the mechanisms of cell swelling and shrink-age are similar in guard cells and pulvinus cortexcells (Cote, 1995; Mayer and Hampp, 1995).However, while turgor changes are correlatedwith substantial changes in solute concentrationsin guard cells (e.g. Humble and Raschke, 1971;Talbott and Zeiger, 1998), single cell sampling ofbean pulvinus cells showed that intracellular os-motic pressure remained practically constant de-spite significant changes in turgor (Irving et al.,1997). The apparent contradiction is resolved if

one takes tissue architecture into account. In par-enchymal plant tissue the contribution of the cellwall to overall tissue volume is in the range of 5%(Winter et al., 1993, 1994). Due to the high vol-ume ratio between symplast and cell wall, solutefluxes over the plasma membrane will cause nota-ble changes in the osmolarity of the cell wallsolution before detectable changes in the osmoticpressure of the protoplast occur (changes of cellwall potassium concentration related to leafmovement have been measured directly; Starrachand Mayer, 1989). Since turgor depends on thegradient of osmotic pressure across the plasmamembrane, the apparent constancy of cellular os-motic pressure during significant changes of tur-gor in pulvinus cortex cells (Irving et al., 1997) isnot surprising. In guard cells the situation isdifferent. Here, the hydraulically active cells aremore or less isolated; they are embedded, as itwere, in a huge volume of passive cells (epidermisand parenchyma), which seem to act as an ionos-tat for extracellular ions (e.g. Blatt, 1985). If leafcell wall osmolarity is more or less constant,guard cell turgor changes must be associated withnotable shifts in intracellular osmotic pressure.

4.2. Irre6ersible changes: cell walls and expansi6egrowth

The shape of cells in which a cell wall counter-acts internal hydrostatic pressure is determined bythe shape the wall attains under multiaxial tensilestress. Due to the isotropic nature of hydrostaticpressure any change in shape, be it plastic orelastic, will be controlled by differential cell wallmechanics. One consequence might be called the‘paradigm of plant cell growth’: while turgor pro-vides the driving force for plastic deformation, thegeneration of a particular form is achieved by thedifferential regulation of cell wall mechanicalcharacters.

This paradigmatic statement requires some ex-plication. Pickett-Heaps and Klein recently haveprovided conclusive evidence that cellular mor-phogenesis in diatoms can occur in the absence ofturgor pressure, and concluded that thereby theparadigm was refuted (Pickett-Heaps and Klein,1998). However, the paradigm as formulated hereis derived from a defined biomechanic premise,namely the presence of a functional cell wall. Theso-called ‘walls’ of the diatoms consist of separatevalves, which usually are perforated by numerous

Fig. 4. Changes of turgor pressure in the upper (adaxial) andlower (abaxial) cortex cells of the pulvinus of terminal leafletsof kidney bean (Phaseolus 6ulgaris) leaves, resulting in move-ment of the leaflet. (A) Experimental setting. Turgor is mea-sured by means of an intracellular pressure-probe in theadaxial or abaxial cortex of the pulvinus, while the relativeposition of the leaflet (laminar elevation) is altered by chang-ing illumination conditions. (B) Turgor pressure in the adaxialand abaxial pulvinus cortex in dependence of laminar eleva-tion. Original data from Irving et al., 1997.


Fig. 5. Schematic representation of currently discussed con-cepts in the regulation of plant cell growth. (A) Cartoonshowing the primarily transverse orientation of cellulose mi-crofibrils (black stripes) in the wall of an elongating cell. Thesemicrofibrils strongly resist any increase in cell diameter (hoopreinforcement), while elongation is restrained mainly by non-cellulose polymers of the wall matrix, which interconnect thetransverse cellulose strands. (B) Two cellulose microfibrils(thick lines) connected by xyloglucan tethers (thin lines) areshown. The cell wall enzyme xyloglucan endotransglycosylase(XET) is thought to cut xyloglucan chains that are strained(arrow-heads), while connecting free ends of currently un-strained chains (arrows), thus enabling the transverse cellulosemicrofibrils to move apart. (C) The cell wall enzyme expansinpromotes elongation in a pH-dependent manner, probably bybinding to regions where xyloglucan chains and cellulosemicrofibrils interact (asterisks), which results in loosening ofthe serial hydrogen bonds between the two types of polymers.

growing root. Here, cell divisions occur mainly inthe very tip, whereas elongation growth is mostpronounced in a restricted zone slightly above theroot apex (Green, 1976). In such a setting, ele-ments of the root tip (cells, or any other geometri-cally defined units) move along a gradient ofgrowth intensity, which can be described basicallyindependent of the nature of the elements consid-ered (Erickson and Sax, 1956; Silk and Erickson,1979; Peters and Bernstein, 1997). By this processthe elongate, cylindrical shape of the root is con-stantly re-created from new tissue elements. Thisbecomes obvious if the shape of single cells isfollowed along the growing root tip: the ratiobetween length and diameter (perpendicular to thelongitudinal axis) increases many-fold along thegrowing zone (Baluska et al., 1990). The perma-nent morphogenetic process is controlled by adominance of the longitudinal cell wall extensibil-ity over the radial one. This is thought to bebrought about by a predominantly transverse ori-entation of cellulose microfibrils within the wall(‘hoop reinforcement’, Fig. 5; Taiz, 1984; Lyndon,1990; Green, 1994).

Beyond their paramount importance in the gen-eration of form, cell walls are frequently consid-ered ‘growth-controlling’ in a quite differentsense. Turgor pressure values between 0.2 and 1MPa have been reported from growing plant tis-sue; given that the cross-sectional area of the cellwall is in the range of some few percent of thewhole cell, this implies tensile wall stresses of upto 100 MPa (Cosgrove, 1993). Walls of growingcells yield to such stresses, leading to stress relax-ation (Fig. 6; Cosgrove, 1986, 1987a; Matyssek etal., 1988). The biochemical mechanism of wallyielding and stress relaxation is obscure still; theinvolvement of cell wall pH (Hager et al., 1971;Rayle and Cleland, 1992; Peters et al., 1998) andof cell wall enzymes such as xyloglucan endo-transglycosylase (XET; Fry et al., 1992; Nishitaniand Tominaga, 1992; Fry, 1993; Pritchard et al.,1993) or expansin (Cosgrove, 1998; Li et al., 1993;McQueen-Mason et al., 1992; Fig. 5) is currentlydiscussed. In any case, wall stress is the counter-force of turgor pressure, and wall stress relaxationinevitably leads to a decrease in turgor and cellwater potential. If growth is to continue, turgorhas to be maintained by water uptake and soluteaccumulation in the cells, to increase wall stressagain (Fig. 6; Taiz, 1984; Cosgrove, 1987b; Ray,1987). An important question regarding mecha-

pores. Moreover, diatom protoplasts regularlyleave their ‘walls’ during cell division and sexualrecombination (Pickett-Heaps et al., 1990). Thusit appears that the diatom ‘wall’ is mechanicallyanalogous to the shells found in other protisttaxa, which traditionally are included in the ani-mal kingdom. From the strictly functional view-point advocated here, data by Pickett-Heaps andKlein, (1998) elegantly demonstrate that diatomsare animal-like as far as their biomechanics areconcerned (compare Schmid, 1987). If so, cellgrowth in the absence of turgor in diatoms bearslittle on our concepts of plant cell morphogenesis.

To further analyze the role of cell walls inirreversible changes of size and form, consider a


nisms of endogenous growth control is whetherturgor-maintaining (water uptake and solute ac-cumulation) or turgor-reducing processes (wallstress relaxation) are rate-limiting (Lockhart,1965; Cosgrove, 1981; Tomos, 1985; Ray, 1987;Frensch, 1997). Findings that growth rates rapidlyrecover to control values after experimentalchanges of turgor (Green et al., 1971; Shackel etal., 1987; Passioura and Fry, 1992), and thatturgor is uniform along growth rate gradients inelongation zones of roots and leaves (Pritchard,1994; Tomos and Pritchard, 1994) support theview that growth rates are regulated by cell wallmechanics (for alternative interpretations seeFrensch and Hsiao, 1994; Fricke and Flowers,1998). On the other hand it has been stressed thatin the living plant significant gradients of waterpotential and turgor can develop across layers ofgrowing tissues, particularly under transpiringconditions (Matyssek et al., 1988; Nonami andBoyer, 1989; Meshcheryakov et al., 1992; Rygol etal., 1993; Nonami et al., 1997). Such gradients areoften absent from excised organ segments in theartificial situations established during experimen-tal studies on growth regulation. The intact plant,however, functions as a coherent hydraulic sys-tem, in which water supply and the efficacy ofwater transport might become growth limiting(Boyer, 1987, 1988).

Stress relaxation in the walls of growing cellsimplies changes in the architecture of the wall,which on a phenomenological level are equivalentto tensile plastic deformation. Such deformationmight occur without being immediately evident,as classical experiments demonstrate. Growing or-gans or tissues are fixed in an experimental device(such as a coat of plaster of Paris; Pfeffer, 1893)which allows metabolic activities to proceed, butprevents any expansion. If turgor is abolished byplasmolysis after different periods of incubation,the unstressed, i.e. plasmolized length of the or-gan is found to have increased with time. In otherwords, turgor-induced elastic cell wall strain,which can be calculated from the amount ofshrinkage under plasmolysis, decreases; the elasticextension of the wall is gradually turned intoirreversible extension by cell-controlled biochemi-cal processes. It has long been known (Pfeffer,1893; Kolkwitz, 1897) that under such circum-stances turgor-dependent stress is transferredfrom the cell walls to the holding device. By thismechanism plants exert substantial forces on ex-ternal obstacles. Seedlings pushing their waythrough thick layers of asphalt are a proverbialexample. Likewise, if differential rates of stressrelaxation occur between tissues in a growingorgan, stress will be transferred from cells withrapidly relaxing walls to cells with slowly relaxing

Fig. 6. Elementary mechanical processes, into which plant cell growth can be analytically dissected. (A; from top to bottom) Internalhydrostatic pressure (P) induces tensile stress in the cell wall. When the wall yields to this force, wall stress relaxes and turgor drops.As a consequence, cellular water potential decreases. The resulting water influx (arrows marked W) allows turgor and wall stress torecover, while cell volume increases. (B) Changes in cell wall mechanics during cell growth modeled by connected plastic (PL) and elastic(EL) elements (from top to bottom). Plastic deformation (yielding to tensile stress) of the cell wall results in a relaxation of elasticallystrained elements (stress relaxation). If water uptake restores the tensile force, strain recovers (creep). The overall increase in length ofthe model equals the length increase due to plastic deformation. Adapted from Cosgrove, 1987a,b, 1993 modified.


Fig. 7. The phenomenon of tissue tension. (A) Preparation ofa sunflower hypocotyl. In this particular experiment, a medianlamella is isolated from a hypocotyl segment by removing theouter parts. The lamella is then divided into four columns bylongitudinal cuts. (B) After 10 min in tap water, the tissuecolumns have bent outside. Obviously, the curvature of theinner two columns cannot have been brought about by me-chanic interaction between peripheral and central tissues. Itrather indicates that tissue tension phenomena are due tocontinuous radial gradients of the mechanic behavior of thetissues, which is not explained by the simplistic ‘spring-in-a-tube’-model (see text for details).

and strongly so if immersed in water (Fig. 7). Theeffect is due to the partial leveling of the gradientin tensile wall stress, which is induced by theabolishment of organ symmetry (Sachs, 1875). Itshould be noted that in this classical interpreta-tion cell walls of all tissues in the growing organare thought to be under tensile stress. This is atrivial conclusion from simple plasmolysis experi-ments, in which tissues are found to shrink uponremoval of turgor pressure. However, an alterna-tive model has been proposed in the second halfof our century, which has gained significant influ-ence on the thinking of modern plant physiolo-gists. This model likens the growing stem to a‘weak spiral spring’ coupled to ‘rubber tube ofsimilar length. Neither is capable of supportingitself when erect; if, however, the spring is slippedinto the rubber tube and the former slightly com-pressed, … the two combined form a structure ofconsiderable rigidity. Here, just as in the stem, theinner part is in a state of compression while theouter is extended’ (cited from Fritsch and Salis-bury, 1953). The model is put in other wordswhen growing stems are described as mechanicalanalogues of single cells, the inner tissues beingequivalent to the protoplast, and the outer ones tothe cell wall Kutschera, 1995. Unfortunately, the‘spring-in-a-tube’ model ignores the principle roleof cell walls as a three-dimensional network oftensile elements. In a growing stem the wholesymplast is under compression, whereas the ECMas a whole is in a state of tension (though gradi-ents in stress intensity may exist). The fashionablenotion of a particular tissue as such being in a‘state of compression’ within a growing stem isclearly inadequate biomechanically (Vincent andJeronimidis, 1992; Peters and Tomos, 1996a,b).

5. Concluding remark

In a mechanical sense ‘soft’ plant tissues aresystems of connected compression chambers,which rely critically on their ECM’s ability toconstrain significant hydrostatic pressure. Thethree-dimensional structure of this ECM is theproduct of an internal differentiation of a coher-ent symplast, which as such is pressurized. Conse-quently, the development of a particular shapeduring morphogenesis is achieved by differentialyielding of the ECM to a multiaxial force. On theother hand, cells in animal tissues are practically

ones (Tomos et al., 1989). The phenomena arisingfrom the resulting gradients in tensile stress havebeen studied by the older botanists and subsumedunder the term ‘tissue tension’ (Sachs, 1865; for ahistorical review see Peters and Tomos, 1996a).Tissue tension is particularly obvious in growingstems: if a growing internode is excised and cutlengthwise, the segments will curve outwardly,


in hydrostatic equilibrium, and free to move.Forces involved in animal morphogenesis aremainly directed ones, exerted by cytoskeletal ele-ments on each other or on the ECM. How theapparently so similar molecular events withinplant and animal cells are translated into thedistinct forces that actually shape plants and ani-mals, remains a challenge.

Acknowledgements

Views expressed in this review were shaped incontinuing discussions with numerous colleagues,particularly Hubert Felle, Wieland Fricke, BerndHerkner, Hartwig Luthen, Dieter Mollenhauer,and Gerhard Thiel. We are indebted to Uwe GertSchlosser and David G. Robinson for advice onrelevant literature.

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What makes plants different? Principles of extracellular matrix function in ‘soft’ plant tissues

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