Cell Biology International 32 (2008) 178e187www.elsevier.com/locate/cellbi

Review

Demarcation of the cortical division zone in dividing plant cells

Daniel Van Damme a,b, Danny Geelen c,*

a Department of Plant Systems Biology, Flanders Institute for Biotechnology, Ghen University, B-9052 Ghent, Belgiumb Department of Molecular Genetics, Flanders Institute for Biotechnology, Ghent University, B-9052 Gent, Belgium

c Department Plant Production, University Ghent, Coupure links 653, B- 9000, Belgium

Received 9 May 2007; revised 6 July 2007; accepted 4 October 2007

Abstract

Somatic cytokinesis in higher plants involves, besides the actual construction of a new cell wall, also the determination of a division zone.Several proteins have been shown to play a part in the mechanism that somatic plant cells use to control the positioning of the new cell wall.Plant cells determine the division zone at an early stage of cell division and use a transient microtubular structure, the preprophase band (PPB),during this process. The PPB is formed at the division zone, leaving behind a mark that during cytokinesis is utilized by the phragmoplast toguide the expanding cell plate toward the correct cortical insertion site. This review discusses old and new observations with regard to mech-anisms implicated in the orientation of cell division and determination of a cortical division zone.� 2007 International Federation for Cell Biology. Published by Elsevier Ltd. All rights reserved.

Keywords: Cytokinesis; Division plane; Cytoskeleton; Preprophase band; Phragmoplast; Cell plate

1. Introduction

Orientation of the division plane and directed cell expan-sion determine the morphological and developmental diversityin plants. Controlled positioning of new cell walls also allowsthe organization of immobile plant cells in defined files andlayers (Lloyd, 1995; Smith et al., 1996). To ensure that eachdaughter cell contains a full set of chromosomes, the divisionplane has to be positioned to bisect the axis of chromosomalsegregation. This can be achieved in two ways: either the po-sition of the division zone is pre-determined before mitosisand the position of the spindle (and the forming cell plate inplants) is adjusted to match this location, or the divisionzone is specified by the position of the spindle.

Animal cells use the latter mechanism. The position of thedivision plane is not pre-determined before mitosis and it is

Abbreviations: BY-2, bright yellow tobacco cells; PPB, preprophase band;

GA, Golgi apparatus; ER, endoplasmic reticulum; GFP, green fluorescent

proteins.

* Corresponding author. Tel.: þ32 9264 6076; fax: þ32 9 264 6225.

E-mail address: danny.geelen@ugent.be (D. Geelen).

1065-6995/$ - see front matter � 2007 International Federation for Cell Biology.

doi:10.1016/j.cellbi.2007.10.010

the spindle that dictates where cleavage will occur (Rappaport,1996). This was nicely illustrated in experiments with Sanddollar eggs where shifting the mitotic spindle to new positionsinduced furrowing activity at the plasma membrane at the newspindle position (Rappaport and Ebstein, 1965). In mammaliancells, astral microtubules play a key role in positioning thespindle (Ahringer, 2003) and it is generally accepted that themicrotubules of the mitotic apparatus specify where the cleav-age furrow will form. However, there is no consensus on theexact mechanism of how these microtubules specify the divi-sion plane and the major models are discussed by Burgess andChang (2005).

Budding (S. cerevisiae) and fission (S. pombe) yeast clearlyuse the first mechanism. In budding yeast, the division site (thebud neck) is selected before mitosis and the position of the budneck is determined by the previous site of cell division (thebud scar). In G1 phase, a small GTPase signaling cascadedirects the formation of a filamentous ring of proteins, calledseptins, at the cortex near the previous bud site (Longtineet al., 1996) and positioning of the spindle at the bud site isaccomplished by a microtubule capture mechanism (Leeet al., 2000). Fission yeast cells are rod shaped and normally

Published by Elsevier Ltd. All rights reserved.

179D. Van Damme, D. Geelen / Cell Biology International 32 (2008) 178e187

divide by binary fission. Positioning of the nucleus in the cen-ter of the cell dictates where the cell will divide. Mutants thatexhibit abnormal nuclear positioning often divide off-center(Chang and Nurse, 1996). Recent experiments have elegantlyproven that the positioning of the G2 nucleus in fission yeast inthe middle of the cell occurs through a microtubule-basedpushing mechanism (Daga and Chang, 2005; Tolic-Norrelykkeet al., 2005). A key element involved in de- central positioningof the cytokinetic ring after nuclear movement in fission yeastis the MID1p protein (Paoletti and Chang, 2000). MID1p islocated in the nucleus during interphase and relocates to thesite of medial ring formation at mitosis, girdling the nucleus(Sohrmann et al., 1996).

Plant cells also use a pre-determined division zone (Ota,1961). Centrifugal displacement of the mitotic apparatus inmetaphase or anaphase in Tradescantia stamen hair cells re-sulted in initial plate formation between the reforming daugh-ter nuclei at the new position, but during subsequent plateexpansion, the cell plate was guided to the position where itwould have inserted in the absence of centrifugal displace-ment. These experiments indicated that the division zone inplant cells is pre-determined before metaphase (Ota, 1961).

Fig. 1. Plant somatic cytokinesis model. Interphase plant cells have a parallel order

membrane. When the cell prepares for division, the nucleus moves to the center an

(Mineyuki et al., 1989) and actin (the latter not shown), the early preprophase band (

altered dynamicity of the microtubules in this area (Dhonukshe and Gadella, 2003

stage, microtubules and actin (the latter not shown) anchor the nucleus to the PPB (P

(Nebenfuhr et al., 2000). The position of the compact PPB corresponds to the future

PPB disappears before nuclear envelope breakdown, which led to the hypothesis th

telophase, the phragmoplast forms out of the remnants of the anaphase spindle. The

forming cell plate (gray) in the center. The cell plate is a newly formed membrane c

Polymerization of microtubules at the outside of the phragmoplast, together with d

a disc-like phragmoplast to a ring-like phragmoplast and leads to vesicle fusion at th

periphery. The cell plate is guided toward the pre-defined division zone by an unkno

filaments (Kakimoto and Shibaoka, 1987; Lloyd and Traas, 1988; Valster and Hep

vision zone. Eventually, the cell plate fuses with the plasma membrane and the callo

cells. After cytokinesis, the divided cells start to reform their cortical microtubula

New elements are emerging that support the formation of a pre-dictive cortical division zone that helps to define the positionof the cell plate attachment site during the final steps ofcytokinesis.

This review focuses on the establishment of a cortical divi-sion zone and discusses putative mechanisms to guide the cellplate to the pre-determined zone. The cell plate is formedthrough a vesicle trafficking and fusion process which occursbetween two sets of parallel ordered microtubules (Fig. 1).This plant specific cytokinetic structure is known as the phrag-moplast (recently reviewed by Jurgens, 2005a,b).

2. The position of the preprophase band coincides withthe future cortical division zone

Plant cells construct a plant-specific microtubular array, thepreprophase band (PPB) that encircles the nucleus before nu-clear membrane breakdown (Fig. 1). The PPB determines thedivision zone and the theory that the PPB functions in guidingthe growing cell plate to this zone was already proposed in1978 by Gunning et al. (1978). The term preprophase shouldnot be interpreted as a defined state in cell division occurring

ed cortical array of microtubules (black lines) located just beneath the plasma

d the cortical array of microtubules converts to a broad band of microtubules

early PPB), by de novo formation (Cleary et al., 1992; Panteris et al., 1995) and

; Vos et al., 2004). Later on, this broad PPB narrows down (late PPB). At this

anteris et al., 2006) and a belt of Golgi stacks forms at the position of the PPB

division zone (Gunning et al., 1978; Mineyuki et al., 1989; Smith, 2001). The

at a landmark is left behind to mark the division zone throughout mitosis. At

phragmoplast consists of two bundles of parallel microtubules separated by the

ompartment resulting from homotypic fusion of Golgi derived vesicles (green).

epolymerization of microtubules in the center results in the transformation of

e edges of the cell plate, which drives the expansion of the plate toward the cell

wn mechanism that likely involves microtubules (Muller et al., 2006) and actin

ler, 1997) that connect the phragmoplast and/or the daughter nuclei to the di-

se-rich cell plate is converted to a cellulose wall that separates the two daughter

r network (not shown).

180 D. Van Damme, D. Geelen / Cell Biology International 32 (2008) 178e187

between G2 and prophase, it rather points to a stage of a cell inwhich there is visible activity or organization related to the es-tablishment of the division zone (Mineyuki, 1999).

The PPB is a unique array of cortical microtubules sur-rounding the nucleus and positioned just underneath theplasma membrane (Hardham and Gunning, 1978). Most differ-entiated and expanded cells have a cortical array of parallelbundled microtubules oriented perpendicular to the longestaxis of the cell (Fig. 1). Prior to division, this cortical arrayis replaced by the preprophase band consisting of microtubulesand aligned actin filaments (Cleary, 1995; Kakimoto andShibaoka, 1987; Palevitz, 1987; Pickett-Heaps and Northcote,1966; Traas et al., 1987). When somatic cells start to divide,this PPB at first covers about 2/3rd of the peripheral areaand gradually becomes more densely packed as the cell ap-proaches the mitotic phase of the cell cycle (Fig. 1). Actin fil-aments may help to narrow the PPB (Eleftheriou and Palevitz,1992). Genetic evidence links the organization of the corticalarray of microtubules to PPB formation. Tonneau mutants ofArabidopsis (ton1 and ton2/fass) specifically fail to organizeand orient their cortical microtubular array and subsequentlyfail to form a PPB (Camilleri et al., 2002; McClinton andSung, 1997; Torres-Ruiz and Jurgens, 1994; Traas et al.,1995).

Much attention has been given to the development of thispreprophase band. Incorporation of fluorescent tubulin in thePPB, together with the observation that the microtubule stabi-lizing drug taxol inhibited PPB formation led to the conclu-sion that PPB microtubules form de novo (Cleary et al.,1992; Panteris et al., 1995). PPB microtubules are built byrecuperating tubulin from the degraded cortical microtubulesindependent from protein synthesis (Mineyuki et al., 1994).The condensation of cortical microtubules at the circumfer-ence of the nucleus is a result of altered dynamicity and spa-tial stabilization of microtubules (Hush et al., 1994; Shawet al., 2003; Dhonukshe and Gadella, 2003; Vos et al.,2004). Microtubule binding proteins like MOR1 (Whittingtonet al., 2001) and the MAP65 protein family (Smertenko et al.,2000, 2004; Van Damme et al., 2004a,b) also play a role instabilizing the PPB microtubules. MOR1 is the TMBP200/XMAP215 homolog of Arabidopsis and mor1-1 mutantsshow defects in PPB formation in Arabidopsis roots(Kawamura et al., 2006). The localization of the AtMAP65-3/ PLEIADE protein to the PPB could also point to a rolein stabilizing the PPB microtubules (Muller et al., 2004).PPB stabilization is however not common to all AtMAP65proteins, since AtMAP65-4-GFP, regardless of constitutiveover-expression, did not localize to the preprophase band inBY-2 cells, although it clearly labeled the prophase spindlemicrotubules occurring at the same time as the PPB (VanDamme et al., 2004b).

3. The role of the nucleus in division plane determination

One of the important issues unsolved is what mechanismcontrols the positioning of the PPB. Evidence has been accu-mulating that, in plant somatic cytokinesis, PPB and

consequent division zone positioning correlate to some extentwith the position of the nucleus, analogous to what is knownfor the actomyosin ring in fission yeast. Early experimentson Adiantum protonema cells (consisting of a single elongatedcell) where the nucleus was displaced prior to preprophaseband formation showed that a PPB formed at the new positionof the nucleus. Centrifugation of nuclei in cells that alreadyformed a PPB resulted in the formation of a second PPB atthe nuclear position (Murata and Wada, 1991). During divi-sions of vacuolated cells, the nucleus moves from the periph-ery to the center of the cell before PPB formation (Fig. 1).Asymmetric cell divisions that form the subsidiary stomatalcells in the leaf epidermis (Gallagher and Smith, 1999; Geisleret al., 2003) or the asymmetric division of the pericycle cellsthat produce side-root primordia (Casimiro et al., 2003) bothinvolve nuclear movement toward the cell periphery and sub-sequent formation of a PPB at that position. Movement of thenucleus to the cell center is not inhibited by the DNA polymer-ase blocker aphidicolin, which arrests cells in S-phase andsuppresses PPB formation (Katsuta et al., 1990). This indi-cates that the migration of the nucleus to the cell centermust be independent of PPB formation. Nuclear movementcan be an actin- or a microtubule-dependent process (Chyti-lova et al., 2000; Ketelaar et al., 2002; Van Bruaene et al.,2003). To date, it is not entirely clear how nuclear migrationoccurs and whether it depends on actin, microtubules or (prob-ably) both. However, the observation that BY-2 cells withslightly off-centered PPBs can adjust the position of the nu-cleus so that it becomes centered inside the PPB (Grangerand Cyr, 2001) shows that nuclear positioning and PPB forma-tion to some extent cross-communicate.

Once the nucleus is centered in the middle of the PPB, itsposition is stabilized (Fig. 1). A strong connection between thenucleus and the PPB must exist because the nucleus and thePPB remain associated when cells are broken (Tiwari et al.,1984; Wick and Duniec, 1983, 1984). Drug studies have sug-gested a microtubule dependent mechanism to be responsiblefor this premitotic nuclear anchoring (Mineyuki and Furuya,1986). This is also the case for polar anchoring of the nucleusduring asymmetric cell divisions of subsidiary mother cells.Here, connecting microtubules between the monopolar spindleand the PPB fix the position of the nucleus to a polar site nearthe inducing guard cell (Panteris et al., 2006).

4. The PPB as an adaptation of cell division ina cellular context

Other nuclear positioning is however not the only mecha-nism that dictates where the PPB will form. Experiments usingonion cotyledon cells pointed out that the nucleus, when dis-placed by centrifugation before PPB formation, has the capac-ity to form a PPB at an ectopic location but a PPB also formsat the original site, independent of the nucleus (Mineyukiet al., 1991a). This led to the conclusion that both intercellularstimuli and nuclear position play a role in determining the po-sition where the PPB will form. An interesting observation inline with this is that prolonged incubation of BY-2 cells with

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the polarity inhibitor NPA causes the formation of abnormalpreprophase bands and oblique cell plates (Dhonukshe et al.,2005). The role of intercellular stimuli for division zone spec-ification is in agreement with the hypothesis that divisionevents that involve a PPB appear to be an adaptation for cellsthat are part of a complex multicellular architecture (Pickett-Heaps et al., 1999). PPBs are not characteristic for algae andthey do not occur in gametophytic cells or in the syncytialtype of cytokinesis in the endosperm. In line with the ideathat the PPB correlates with divisions in a tissue context, itwas noticed before that some suspension-cultured cells dividewithout the need for a PPB (Mineyuki, 1999; Chan et al.,2005) and that suspension culture cells frequently produce ab-normal PPBs, but still manage to divide (Granger and Cyr,2001; Hasezawa et al., 1994). The observation that Arabidop-sis ton/fass mutants that no longer produce a PPB are still ca-pable of dividing (Camilleri et al., 2002; Torres-Ruiz andJurgens, 1994; Traas et al., 1995) also proves that PPB forma-tion per se is not essential for division. But it does matter whenit concerns plate positioning.

The interplay between nuclear and intercellular signals indetermining PPB positioning becomes even more complex inthe case of binucleated cells, formed by disturbing cytokinesisby caffeine in onion meristems (Gimenez-Abian et al., 1998).These binucleated cells could form two PPBs around each nu-cleus, one PPB around the nucleus located most distantly fromthe cell tips or one PPB located in the middle of both nuclei.These observations are in line with a diffusible factor emerg-ing from the nucleus like MID1 to establish a gradient be-tween the nucleus and the cell periphery. The axis of thisgradient is instrumental to define the cell cortex that is closestto the nucleus.

Vacuolated cells usually contain a cortical array of MTsthat is positioned perpendicular to the longest axis of thecell and thus already parallel to the future division plane.However, guard mother cells have to switch the orientationof their division plane perpendicular to the previous division.This occurs through a randomization of the cortical microtu-bules and the first indication of the new orientation of the cor-tical microtubules is the emergence of a broad PPB (Mineyukiet al., 1989). The broad PPB fixes the axis of division planeorientation and subsequent narrowing of the PPB determinesthe exact division zone with micrometer accuracy (Mineyukiet al., 1989).

5. Functional properties of the PPB

This theory has recently been challenged by Marcus et al.(2005) who state that narrowing of the PPB is not necessaryfor division plane determination. They show that the cell platecan still insert at the proper site in BY-2 cells in which the PPBmicrotubules have been depolymerized. Their data do not sup-port a role for the narrowing of the PPB microtubules in focus-ing the signal that is used to guide the cell plate. Instead theystate that the PPB is required for spindle positioning, whichsets the growth trajectory of the phragmoplast. A functionfor the PPB in spindle positioning was also concluded from

experiments on Arabidopsis cell cultures where the majorityof the cells did not produce a PPB. Cells in this culture thatdivided without a PPB formed bipolar spindles after nuclearenvelope breakdown and showed variable spindle orientationsand phragmoplast mobility. On the other hand, cells that didproduce a PPB established a bipolar cap-like organization ofthe prophase spindle microtubules perpendicular to the planeof division before nuclear envelope breakdown. These obser-vations suggest that the PPB is involved in polarization eventsto promote spindle pole morphogenesis and positional stabilityduring cell division. The Arabidopsis Aurora kinases are pos-sible candidates to translate the positional information of thePPB to the formation of the bipolar cap-like organization ofthe prophase spindle microtubules. In mammalian cells, AU-RORA B and C are part of the chromosomal passenger com-plex and their functions overlap during cytokinesis (Adamset al., 2001; Terada, 2001; Yan et al., 2005). Chromosomalpassenger proteins act in a complex that is involved in coordi-nating the chromosomal and cytoskeletal events of mitosis, in-cluding bipolar spindle formation and cytokinesis (Carmenaand Earnshaw, 2003; Vagnarelli and Earnshaw, 2004).AtAURORA1 and 2 display characteristics of these chromo-somal passenger proteins (Demidov et al., 2005). The AtAUR-ORA1 protein localizes to the PPB in Barley and in BY-2cells, to the prophase spindle microtubules of BY-2 cells dur-ing the bipolar cap formation and eventually, it ends up in theforming cell plate (Demidov et al., 2005; Geelen and Inze,2006; Kawabe et al., 2005). Moreover, the AtAURORA3 pro-tein localizes to the metaphase plate in BY-2 cells (Demidovet al., 2005; Kawabe et al., 2005) and over-expression ofAtAURORA3 in BY-2 cells caused an alteration of the orien-tation of cell division, together with a disorganization of thespindle microtubules (Kawabe et al., 2005).

A role of the PPB in spindle orientation also comes fromexperiments using BY-2 cells that form double PPBs (Yonedaet al., 2005). Double PPBs can be induced by synchronizationof elongated BY-2 cells (Hasezawa et al., 1994). Yoneda andco-workers have observed that most cells with double prepro-phase bands formed multipolar spindles at prophase, in con-trast to cells that only had a single PPB, where alwaysnormal bipolar spindles were formed. However, by metaphaseonly bipolar spindles were found in cells that had developeddouble preprophase bands, indicating that there are two stagesin bipolar spindle formation, one that is controlled by the PPBand that of a correctional mechanism at prometaphase (Yonedaet al., 2005).

6. The phragmoplast is guided to the zone previouslyoccupied by the PPB

Regardless whether it is the narrowing of the PPB itself orsome other factor that determines the future division zone, a re-current observation is that the position of the mature and nar-row PPB corresponds to the division plane and the positionwhere the cell plate inserts into the mother wall (Smith,2001). The PPB is dismantled at the beginning of prophase(Fig. 1). Surprisingly, in centrifuged cells of Adiantum and

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Allium (Mineyuki et al., 1991a; Murata and Wada, 1991), onlythe PPB that encircles the nucleus is degraded as the cells pro-cess through mitosis, suggesting that factors surrounding orshuttling from the nucleus are involved in PPB degradation.The use of general kinase inhibitors like staurosporine andK252a have led to the conclusion that a kinase is directly in-volved in PPB degradation (Katsuta and Shibaoka, 1992; No-gami and Mineyuki, 1999) and this kinase was identified as theCDKA/cyclinB kinase complex (Hush et al., 1996). Immuno-localization and live cell imaging using a GFP-tagged CDKAshowed that this kinase associates with the narrow PPB justbefore breakdown (Colasanti et al., 1993; Weingartner et al.,2001). The localization of AtAURORA1 kinase at the PPB(Demidov et al., 2005; Geelen and Inze, 2006) could also pointto a function for this kinase in PPB dynamics.

The separation in time between the destruction of the PPBand the insertion of the cell plate led to the idea that the PPBleaves behind a landmark that will guide the expanding phrag-moplast to the site where the PPB was positioned. Mineyukiand Gunning (1990) proposed that the division zone is estab-lished by: ‘‘(1) localized deposition of insertion and matura-tion factors in a latent form; and (2) provision of meansthat, later on, will guide the leading edge of the centrifugallyextending phragmoplast to the site. Once the new wall has at-tached, the factors are activated and utilized to insert, anchorand integrate the new wall .. The PPBs raison d’etre is to. provide the necessary spatial guidance . for the localizeddeposition of the(se) factors.’’. This theory was based on theobservation that cell plates that are forced to insert at an ec-topic location do not mature to a flat and stiff wall (Mineyukiand Gunning, 1990).

So far, a factor that positively marks the division zone hasnot been identified. The positional landmark after PPB de-struction resists the centrifugation of the nucleus (Ota,1961), but is disrupted by making minute wounds in the divi-sion zone of mitotic cells with a micro needle (Gunning andWick, 1985). Using a GFP-tagged soybean mannosidase, itwas shown that a number of Golgi stacks aggregate in a‘‘Golgi belt ‘‘ in dividing BY-2 cells and that this belt accu-rately predicts the future division zone after disassembly ofthe PPB (Nebenfuhr et al., 2000) (Fig. 1), suggesting thatGolgi secretion may be required for marking the divisionzone. However, inhibition of Golgi secretion in BY-2 cellsby Brefeldin A still allowed plate insertion at the propersite, indicating that Golgi secretion is not involved in estab-lishing the landmark and does not play an active role in divi-sion zone determination (Dixit and Cyr, 2002).

Another intriguing observation in cells with double PPBs isthat oblique cell plates form when both PPBs contribute to theselected insertion sites (Dhonukshe et al., 2005; Granger andCyr, 2001). It is well established that the forming cell platecan readjust its expansion toward the division zone (Clearyand Smith, 1998; Ota, 1961; Palevitz, 1986; Smith, 1999; Van-straelen et al., 2006). In these cases, the formation of obliquecell plates can not be attributed to oblique spindle orientations.It has been proposed that the mechanism to select the insertionsite depends on the fact that the cell plate preferentially

attaches to the cortical zone where the largest amount ofPPB microtubules had been present (Dhonukshe et al.,2005). This implies that the presumed landmark is not a ringbut a single or a few spots along the cortical division zone.The formation of oblique cell plates therefore argues againstthe necessity of a landmark being positioned along the lengthof the division zone. Cell plate formation in vacuolated cells istypically polarized to one side of the cell and the strongest sig-nal on the opposite side can guide further plate expansion(Cutler and Ehrhardt, 2002). The idea of discrete landmarkscould explain the formation of the oblique cell plates seen incells with double PPBs.

7. The actin depleted zone marks the division zone uponPPB degradation

The actin network does not disappear throughout the pe-ripheral space like the cortical microtubules (Cleary et al.,1992; Liu and Palevitz, 1992; Mineyuki and Palevitz, 1990;Traas et al., 1987). Upon breakdown of the PPB a region de-void of actin is formed termed the actin depleted zone (ADZ)(Cleary, 1995; Cleary et al., 1992; Liu and Palevitz, 1992). Be-cause the position of the ADZ corresponds to that of the PPB,it too marks the division zone. Importantly, this ‘‘negative tem-plate’’ remains throughout metaphase and anaphase suggestingit transmits the spatial requirements for phragmoplast guid-ance. However, actin drug treatments resort defects in divisionplane positioning when applied during preprophase but notwhen applied during later phases (Hoshino et al., 2003; Van-straelen et al., 2006). These observations point to a role forthe ADZ in establishing a landmark rather than a function inphragmoplast guidance.

Recently, the dynamics of the actin cytoskeleton have beenmonitored in live cells during cell-cycle progression in BY-2cells transformed with the fimbrin actin-binding domain 2fused to GFP (GFP-ABD2), (Sano et al., 2005; Yu et al.,2006). Time-lapse studies of these BY-2 cells revealed thatthe cortical actin network in G2 phase is not homogenouslydistributed over the cell cortex as assumed by Mineyuki(1999), but is centered in the middle of the cell overlyingthe nucleus and the PPB. This band separates upon PPB break-down into two bands with high fluorescence intensity anda zone of weak fluorescence, corresponding to the ADZ, inthe middle. This structure was termed ‘‘Twin Peaks’’. The ex-panding cell plate was subsequently guided to the middle ofthe valley between the two bands of actin filaments. How thesebands of actin filaments and the ADZ guide of the expandingcell plate toward the insertion site remains unknown.

8. Implications of the plasma membrane in theestablishment of the division zone

The prime activity of the microtubule and actin cytoskele-ton during cytokinesis is to provide the spatial infrastructure toposition and guide new cell wall formation. When the new cellplate emerges there is at first no connection with the existingplasma membrane, a feature that is unique to plant cell

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division. To allow fusion the plasma membrane needs to beprimed with appropriate SNARE factors and perhaps addi-tional vesicle fusion proteins. Ideally these vesicle fusionprimers reside in the division zone to favor attachment at thecorrect site. Earlier work on Adiantum protonema cells showedthat in the presence of lipid solvents (2% DMSO or 1% meth-anol), there is an increase in the occurrence of oblique cellplates, underscoring the importance of plasma membrane in-tegrity for conserving positional information (Mineyukiet al., 1991b).

Recent studies identified a distinct plasma membrane areathat is formed at the onset of mitosis and lasts until the endof cytokinesis. The plasma membrane domain is defined bythe localization of two proteins: a kinesin-like protein,KCA1, that is specifically excluded from the division zonethroughout cytokinesis (Vanstraelen et al., 2006) and a plant-specific protein, TPLATE, that accumulates at the divisionzone just prior cell plate plasma membrane fusion (VanDamme et al., 2006). KCA interacts in a yeast-two-hybridscreen with CDKA;1 and accumulates at the plasma mem-brane in cells entering mitosis (Vanstraelen et al., 2004,2006). GFP-KCA1 does not accumulate at the area near the di-vision plane and generates a KCA depleted zone or KDZ co-incident with the position of the PPB and ADZ. Time-lapsestudies and drug analysis showed that the KDZ depends onPPB formation and double KDZs were formed in cells thatproduced double PPBs. Once established, the KDZ does nolonger require an intact microtubule or actin cytoskeletonand persists throughout cytokinesis (Vanstraelen et al., 2006).

Vesicle trafficking may have next to a role in generatinga cell plate also function in division plane determination. In-creases in the cellular concentration of 1-naphthalene aceticacid (NAA) in BY-2 cells caused aberrant division orientationin cells that resumed dividing (Petrasek et al., 2002). Auxin isalso identified as an inhibitor of endocytosis and could there-fore have an impact on plasma membrane composition(Paciorek et al., 2005). Localized modification of the plasmamembrane is an appealing hypothesis since yeast and animalscells form division plane associated lipid rafts enriched in ste-rol content (Rajagopalan et al., 2003; Takeda et al., 2004;Wachtler et al., 2003). Plasma membrane modifications couldhelp exclude GFP-KCA1 from the cortical division zone and/or specifically target TPLATE-GFP. Plasmolysis experimentson Tradescantia (Cleary, 2001) and BY-2 cells (Vanstraelenet al., 2006) revealed plasma membraneecell wall connectionsat the division zone, suggesting that plasma membranee cellwall linker proteins may function to maintain the KDZ andkeep the division zone at its predefined position, underliningthe putative role of the plasma membrane in division zonedetermination.

9. Guidance of the phragmoplast: actin, microtubulesor both?

Following the establishment of the division zone by thePPB, the ADZ and the KDZ, a mechanism must exist thatguides the expanding cell plate toward the pre-determined

division zone. The exact mechanism remains unresolved andconflicting evidence on the role of the actin and microtubulecytoskeleton has been generated. Evidence for a role of the ac-tin cytoskeleton in guidance of the phragmoplast comes fromthe observation that in some cells, actin-containing cytoplas-mic strands have been seen to link the edges of the phragmo-plast to the cortical division zone (Kakimoto and Shibaoka,1987; Lloyd and Traas, 1988; Valster and Hepler, 1997). Arole for actin in guidance is also suggested from drug studies:cytochalasin inhibit actin polymerization and do not interferewith cell plate formation, but cause misorientation of cellplates (Wick, 1991). Inhibition of myosin function in Trades-cantia by butanedione monoxime (BDM) resulted in tilting ofthe cytokinetic apparatus (Molchan et al., 2002). LatrunculinB treatment frequently causes abnormal plate insertion, sug-gesting a role for actin in guidance of the phragmoplast(Granger and Cyr, 2001). Disrupting actin microfilaments byBistheonellide A in BY-2 cells with double PPBs resulted ina decrease in the number of oblique cell plates (Yonedaet al., 2005).

Other studies report that the actin cytoskeleton plays a rolein consolidation of the cell plate rather than guidance (Gun-ning and Wick, 1985) and no major role for actin in guidancewas found in meristematic cells (Cleary, 1995). CytochalasinD or bistheonellide A treatment of BY-2 cells during ADZ for-mation resulted in distorted cell plate formation, while treat-ment of cells at later time points reduced the frequency ofaberrant cell divisions, supporting a role in division plane es-tablishment but not plate guidance (Hoshino et al., 2003; Sanoet al., 2005). It cannot however be ruled out that the incubationtime required or drug specificity is insufficient to disrupt theactin cytoskeleton and thus affect the guidance mechanism.

So far, there is no genetic evidence that supports a role foractin filaments in somatic cytokinesis. Arabidopsis encodeseight functional actin genes and highly conserved variantsare expressed in the same tissue, hampering the analysis ofloss-of-function mutations. Analysis of a dominant negativeform of actin (ACT2-2D) that disturbs actin polymerization re-vealed no effect on cell division patterns in the root meristem(Nishimura et al., 2003). Discordia mutant dcd1 is disrupted inan actin-dependent process required for the guidance of thephragmoplast in the formation of guard cells, where a strongdisplacement of the spindle is required (Gallagher and Smith,1999). Genetic evidence supports a role for microtubules incell plate guidance. The tangled-1 mutation (tan-1) of maizewas found to affect cell division orientation, resulting in theformation of oblique cell walls in diverse tissue layers andat a wide range of developmental stages. Preprophase bandsand actin depleted zones formed normally in tan-1 mutantsand division planes appeared to be established normally, al-though they formed mostly in transverse rather than in longi-tudinal orientations. The TAN1 gene is expressed in dividingcells and encodes a highly basic protein that binds to the mi-crotubules of the PPB, spindle and phragmoplast (Cleary andSmith, 1998; Smith et al., 1996, 2001). These observationspoint to a microtubule dependant mechanism, involving theTANGLED1 protein, in cell plate guidance. Recently two

184 D. Van Damme, D. Geelen / Cell Biology International 32 (2008) 178e187

homologous kinesins were identified through a yeast two hy-brid screen using the maize TAN1 (Muller et al., 2006). Dou-ble knock-out mutations of the corresponding orthologs inArabidopsis lead to the development of a root cell division pat-tern phenotype resembling weak alleles of tonneau 2. At thecellular level multiple misoriented cell walls are observed inembryos and in root tips, suggesting that the two kinesinsPok 1 and 2 cooperate with ATN, the TAN1 counterpart inArabidopsis, to control phragmoplast guidance (Muller et al.,2006). Another gene that could be important for guidance isair9 that was identified through a proteomic screen for micro-tubule binding proteins. AIR9 GFP fusion protein indiscrimin-ately binds microtubule structures and concentrates at thecortical division site where the cell plate merges with themother wall. The localization of AIR9 is in line with the em-bryo lethal phenotype of an insertion mutant and suggests anessential role in cell division (Buschmann et al., 2006).

The function of microtubules in guidance of the cell plate isalso supported by microtubule stabilizing drug treatments.Fig. 2 illustrates some of our own observations using taxolto interfere with microtubule dynamics in BY-2 cells over-expressing RFP-tubulin and TPLATE-GFP (D. Van Damme ,unpublished results). These cells allow the simultaneous visu-alization of the microtubular cytoskeleton and the forming cellplate throughout cytokinesis. During the early phragmoplaststage astral microtubules emanating from the nuclear surface

Fig. 2. Microtubule based cell plate guidance. Time lapse of a BY-2 cell co-expres

presence of 40 m M taxol to stabilize the microtubules. Astral microtubules emanati

taxol, ectopic microtubule asters are formed that connect with ectopic sites and dev

connect with the cell cortex. Taxol treatment causes the emer-gence of new microtubule asters that connect with an ectopicposition at the cortex outside the predicted division zone. Inthis particular cell, the cell plate inserted at a ‘‘newly formed’’cortical division site with the mother wall. It illustrates thatmicrotubule are determinative in the guidance process.

10. To be or not to be guided

It is important to keep in mind that the mechanism of cellplate guidance may not be that essential when consideringsmall cells or cells that are not part of an organized tissue. Itis easy to conceive that small cells that divide along the short-est axis have a very narrow window for error compared tolarge and longitudinally dividing cells. A stunning exampleof longitudinal division, for instance, occurs in cambial initialsof pine where the cell plate is several millimeters long and re-quires about a day to complete (Bednarek and Falbel, 2002).Small Tradescantia cells did not show tilting of the cell platewhen myosin function was inhibited, presumably because oflittle room for rotation. However, tilting occurred in largercells (Molchan et al., 2002). In tangled1 mutants of maize,transverse cell divisions in all tissue layers, at a wide rangeof developmental stages occur at normal frequencies com-pared to wild-type, but longitudinal divisions are largelysubstituted by a variety of aberrantly oriented divisions (Smith

sing RFP-tubulin (red) and the cell plate marker TPLATE-GFP (green) in the

ng from the nucleus connect with the cortical division zone. In the presence of

iate cell plate expansion away from the predicted position. Scale bar is 10 m m.

185D. Van Damme, D. Geelen / Cell Biology International 32 (2008) 178e187

et al., 1996). The longitudinal division obviously requires aneffective guidance mechanism to reduce the chance that theplate ends inserts at ectopic positions.

On the contrary, small cells have a tight association be-tween the nucleus and the phragmoplast, and nuclear or spin-dle positioning is by itself sufficient to guide the plate (Asadaand Shibaoka, 1994). The attachment of phragmoplasts todaughter nuclei might be particularly important for asymmet-rical divisions where one of the daughter nuclei, associatedwith the actin patch, serves as a scaffold for the expandingphragmoplast (Cleary, 1995). Therefore, plant cells mayhave developed different guidance mechanisms and selecta strategy that is best suited according to their size and shape.

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