This Article Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via CrossRef Citing Articles via ISI Web of Science (23) Citing Articles via Google Scholar Google Scholar Articles by Wasteneys, G. O. Articles by Yang, Z. Search for Related Content PubMed PubMed Citation Articles by Wasteneys, G. O. Articles by Yang, Z. Agricola Articles by Wasteneys, G. O. Articles by Yang, Z.

UPDATE ON THE PLANT CYTOSKELETON

New Views on the Plant Cytoskeleton

Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4 (G.O.W.); and Center for Plant Cell Biology, Department of Botany and Plant Sciences, University of California, Riverside, California 92521–0124 (Z.Y.)

The advance of modern approaches in cell research, including genomics, proteomics, molecular genetics, and new and improved imaging technologies, is changing our views on the form, the function, and the regulation of the plant cytoskeleton. Ever since their discovery in plant cells in the 1960s and 1970s, the function of microtubules and actin microfilaments has been analyzed largely by pharmacological strategies. The use of cytoskeleton-disrupting drugs provided broad insights into the participation of microtubule or actin microfilament arrays in specific cell functions. The shift to a more integrative approach in the last few years has revolutionized the way we look at the plant cytoskeleton. Our initial view of static images has shifted to dramatic motion pictures of live, dynamic networks, and descriptive views have been replaced by mechanistic insights. Indeed, we are now attempting to understand how the organization and dynamics of the cytoskeleton are integrated into the regulatory networks underlying complex plant processes, from sexual reproduction to organ morphogenesis and cellular differentiation. Investigating the mechanisms underlying cytoskeletal organization and dynamics has also revealed previously unknown cytoskeletal functions. Integrating this new knowledge is reflected by a large volume of recent reviews (Kost and Chua, 2002; Mathur and Hulskamp, 2002; Wasteneys, 2002, 2004; Deeks and Hussey, 2003; Hashimoto, 2003; Smith, 2003; Wasteneys and Galway, 2003; Gu et al., 2004; Lloyd and Chan, 2004; Sedbrook, 2004), including several Update articles in this focus issue (Bisgrove et al., 2004; Lee and Liu 2004; Takemoto and Hardham, 2004). Most of these reviews deal with specific aspects of the latest advances in our understanding of the plant cytokeleton. In this Update article, we hope to provide an overarching but complementary view of this fast-growing field.

	NEW VIEWS ON FUNCTION

TOP NEW VIEWS ON FUNCTION LIVE VIEWS: ADVANTAGES AND... DYNAMIC VIEWS: CYTOSKELETAL... A FAR-REACHING VIEW: SIGNALS... LITERATURE CITED

 
Multifaceted approaches integrating mutational strategies, improved technologies for high-resolution imaging of cytoskeletal arrays, and identification of cytoskeleton-regulatory proteins are revealing new roles for the cytoskeleton in fundamental and plant-specific processes. The discovery of these previously unknown roles and an improved understanding of cytoskeletal remodeling are providing new ideas about how plant cells work.

A key example is the role of the cytoskeleton in cell shape determination. The predominant hypothesis that cortical microtubules modulate cell shape by directing cellulose synthase complex movement has always been marred because it neglected to explain how tip growth in pollen tubes and root hairs, or the complex shape of other diffusely expanding cells is achieved. In the past, these differences in form have generally been considered to be governed by fundamentally distinct mechanisms. In recognition of common cytoskeletal and wall-building mechanisms across the full range of plant cell morphologies, a concept has been put forward that positions tip growth and isotropic diffuse expansion at the extremes of a growth continuum, with other forms of growth, including anisotropic expansion, somewhere in between (Wasteneys and Galway, 2003). Recent studies that demonstrate a role for cortical microtubules in anisotropic growth that is independent of orienting cellulose microfibrils (Himmelspach et al., 2003; Sugimoto et al., 2003; Baskin et al., 2004; Wasteneys, 2004) provide an opportunity to rethink our ideas about how plant cells are formed. A clear way forward is to consider how the relative distribution and activity of actin microfilaments and microtubules control the mechanical properties of cell walls (Wasteneys and Galway, 2003). Consistent with the growth continuum concept, the cortical patches of actin microfilament networks in diffusely expanding cells may have a role in wall construction and modification that is analogous to the tip-localized actin filament networks of tip growing cells (Fu et al., 2001, 2002; Frank and Smith, 2002; Jones et al., 2002).

	LIVE VIEWS: ADVANTAGES AND LIMITATIONS OF GREEN FLUORESCENT PROTEIN-BASED PROBES

TOP NEW VIEWS ON FUNCTION LIVE VIEWS: ADVANTAGES AND... DYNAMIC VIEWS: CYTOSKELETAL... A FAR-REACHING VIEW: SIGNALS... LITERATURE CITED

 
Recognition that cytoskeletal polymers are not static has helped drive the quest for new technology that allows microtubules and actin filaments to be observed in living cells (Table I). Live probes usually utilize fluorescent protein-tagged monomers of the cytoskeletal polymers (e.g. green fluorescent protein [GFP]-tubulin; Ueda et al., 1999) or a protein domain that binds specifically to the cytoskeletal polymers (e.g. GFP-tagged actin-binding domain from mouse talin; Kost et al., 1998). They can be used to label all arrays, a specific array, or specific part of an array to provide novel insights into cytoskeletal dynamics and organization. Use of GFP-tubulin has uncovered a modified treadmilling mechanism for the dynamics of cortical microtubules in plant cells (Shaw et al., 2003), and the heterologous fusion protein YFP-CLIP170, which labels microtubule ends, revealed a difference in microtubule dynamics between interphase and preprophase cortical microtubules (Dhonukshe and Gadella, 2003). Similarly, use of GFP-EB1 (Chan et al., 2003; Mathur et al., 2003b) has provided support for the concept of dispersed microtubule organization centers in plant cells (Wasteneys, 2002). Live probes may also visualize the finer and more dynamic cytoskeletal arrays that are usually difficult to detect using conventional fixation-based methods. For example, GFP-mTalin has been used to label a dynamic form of F-actin in the tip of pollen tubes and root hairs and fine actin microfilaments in the cortex of Arabidopsis leaf pavement cells, which previously had not been visualized in fixed cells (Fu et al., 2001, 2002).

Another key issue is to evaluate the level of live probes that provides a faithful report of different cytoskeletal arrays. The adverse effects of GFP-mTalin (Ketelaar et al., 2004b) may be at least in part caused by high levels of expression. The usefulness of a specific live probe may also be tissue and cell specific. GFP-tubulin fusion proteins do not seem to incorporate into microtubules in roots, whereas GFP-MAP4 (and GFP-MBD) constructs (Granger and Cyr, 2001) work well in roots (Van Bruaene et al., 2004). There is no doubt that the use of live cytoskeleton probes has cast new views of the plant cytoskeleton arrays and their dynamics, yet we still need to fine-tune the existing probes and to generate new ones.

Important criteria to consider include:

(1) Are the expression levels of the fusion protein interfering with its normal function?

(2) If the fusion protein is being expressed in a heterologous system, is it competing with an endogenous protein for a tubulin- or actin-binding site?

(3) Is the positioning of the seedling or explanted organ in its microscope chamber generating pressure, wound, or gravity responses?

(4) How much repeated excitation with high-energy light can the cell or fusion protein tolerate without generating aberrant behavior?

(5) Is specimen drift through the z axis generating an illusion of movement of the microtubule or actin filament bundle?

The bottom line is that these experiments need to be scrutinized carefully and, where possible, results backed up by other experimental approaches.

	DYNAMIC VIEWS: CYTOSKELETAL ORGANIZATION AND DYNAMICS

TOP NEW VIEWS ON FUNCTION LIVE VIEWS: ADVANTAGES AND... DYNAMIC VIEWS: CYTOSKELETAL... A FAR-REACHING VIEW: SIGNALS... LITERATURE CITED

 

Actin and Its Regulatory Proteins

The existence of actin nucleation mechanisms allows the cell to modulate the timing, rate, and location of actin filament formation. Two types of conserved actin nucleation mechanisms have been characterized (Table II). In fungi and animals, the actin-related protein (Arp) 2/3 complex initiates the polymerization of branched actin filaments to form an actin network, whereas formin nucleates unbranched filaments that can cross-link to form actin bundles. Orthologs for all seven subunits of the Arp2/3 complex appear to be present in plants, but surprisingly, knocking out any of the seven Arabidopsis genes only alters trichome shape, leaf pavement cell, and root hair morphology (Deeks and Hussey, 2003; Le et al., 2003; Li et al., 2003; Mathur et al., 2003a, 2003c; El-Din El-Assal et al., 2004). Although the biochemical activity of the putative Arabidopsis Arp2/3 complex has not been studied, these observations suggest that another actin nucleation mechanism may play a predominant role in the regulation of actin assembly in plants. Perhaps this is consistent with the fact that 20 formin-homology genes are present in the Arabidopsis genome (Deeks et al., 2002). Indeed, overexpression in pollen suggests that formin may initiate the formation of bundled actin microfilaments (Cheung and Wu, 2004).

Actin microfilaments are most prominent in plant cells when bundled, and these so-called actin bundles serve as tracks for the myosin-mediated movement of organelles. Two classes of actin cross-linking proteins, villins and fimbrins, may be involved in the formation of actin bundles (Wasteneys and Galway, 2003). It will be interesting to see if different villins and fimbrins have distinct roles in organizing different populations of bundled actins, as appears to be the case for MAP65 involvement in microtubule bundling, which is discussed below.

Microtubule Dynamics and Organization

The lack of centriole-based microtubule organizing centers in plant cells presents considerable challenges for nucleating microtubules in the right place at the right time (Schmit, 2002; Wasteneys, 2002; Dixit and Cyr, 2004). -Tubulin, a critical factor in fungal and mammalian microtubule nucleation, has now been confirmed to be associated with putative sites of microtubule nucleation in plant cells (Drykova et al., 2003; Kumagai et al., 2003; Shimamura et al., 2004) and associated at these sites with the plant homolog of the SPC98 protein (Erhardt et al., 2002). -Tubulin's apparent distribution along the entire length of microtubules (Drykova et al., 2003; Kumagai et al., 2003) suggests either that additional functions for -tubulin exist, or that the dispersal of nucleation activity takes advantage of microtubule polymers as tracks (Wasteneys, 2002).

Organizing plant microtubules into functional arrays no doubt involves cross-linking mechanisms that substitute for the lack of centrosomes. The unique character and function of cortical microtubules in plant cells is to a large degree dictated by their close contact with the plasma membrane. Recent progress in understanding this relationship has come from the discovery that phospholipase D associates with microtubules (Marc et al., 1996; Gardiner et al., 2001) and that compounds activating phospholipase D result in microtubule detachment from the plasma membrane and loss of parallel order (Dhonukshe et al., 2003), inhibiting normal seedling development (Gardiner et al., 2003).

Cortical microtubule function depends on the presence of microtubule-associated proteins (MAPs) and their regulatory kinases and phosphatases (Sedbrook, 2004). The MOR1 homolog of the highly conserved MAP215 family (Gard et al., 2004) appears to be essential for microtubule function throughout plant development (Whittington et al., 2001; Twell et al., 2002; Wasteneys, 2002). This year, the identities of two proteins involved in the control of directional expansion and associated with microtubules were revealed. SPR1/SKU6 protein is a tiny (12-kD) protein originally identified from mutants that cause right-handed organ twisting (Nakajima et al., 2004; Sedbrook et al., 2004). Similar phenotypes are generated by mutations in the SPIRAL2/TORTIFOLIA1/CONVOLUTA gene, which encodes a 94-kD protein that colocalizes with microtubules (Buschmann et al., 2004; Shoji et al., 2004).

Transmission electron microscopy reveals just how common microtubule bundles are in plant cells, not just in preprophase bands but also apparent for many cortical microtubules. Bundles might generate stability but could also provide a means of bulking up proteins or other storage material on microtubule surfaces. Overlapping microtubules of opposite polarity, as occurs in some regions of the phragmoplast (Segui-Simarro et al., 2004), is also likely to involve many of the same mechanisms as more substantial bundles. Recent studies confirm that cortical microtubules also exist in arrays of mixed polarity. It has been suggested that the MOR1 protein may cross-link microtubules. The tobacco (Nicotiana tabacum) homolog of MOR1, TMBP200, was reported to have in vitro microtubule-bundling activity (Yasuhara et al., 2002), and an antibody raised against a C-terminal MOR1 fragment labeled the zone of microtubule overlap in phragmoplast arrays in Arabidopsis protoplasts (Twell et al., 2002). A study just published, however, concludes that the tobacco MAP200 homolog of MOR1 has no bundling activity, and the authors attribute the previously reported property to contamination by a MAP65 fraction (Hamada et al., 2004). Both in vitro biochemical assays and protein localization studies have implicated the MAP65 family proteins in microtubule bundling (Chan et al., 2003; Muller et al., 2004; Wicker-Planquart et al., 2004). In Arabidopsis, MAP61-1 is localized to a subpopulation of the interphase cortical microtubules, the center of the preprophase band, and to antiparallel overlapping regions of spindle and phragmoplast microtubules. MAP65-3/PLE knockout mutants show a specific defect in cytokinesis (Muller et al., 2004). In tobacco BY-2 cells, GFP-tagged MAP65-1 and MAP65-5 are localized to different subpopulations of cortical microtubules, whereas GFP-MAP65-4 is localized to a specific array of microtubules that rearranged to form spindles (Van Damme et al., 2004). These observations raise the possibility that different members of the MAP65 family may have distinct functions in cross-linking specific subpopulations of microtubules.

	A FAR-REACHING VIEW: SIGNALS AND PATHWAYS REGULATING THE CYTOSKELETON

TOP NEW VIEWS ON FUNCTION LIVE VIEWS: ADVANTAGES AND... DYNAMIC VIEWS: CYTOSKELETAL... A FAR-REACHING VIEW: SIGNALS... LITERATURE CITED

 
Given the wide range of processes modulated by the cytoskeleton, it is not surprising that a variety of intracellular, extracellular, hormonal, and environmental signals are known to regulate the dynamics and organization of both microtubules and actin microfilaments. A specific cytoskeletal array itself (e.g. the preprophase band) might act as a signal to regulate other types of arrays. Identification of specific signals and dissection of signaling networks interfacing with cytoskeletal organization and dynamics are the ultimate goal of integrating the cytoskeleton with plant growth, development, and physiological responses.

One of the better-characterized signal-cytoskeleton response systems is the modulation of changes in the actin cytoskeleton in poppy pollen tube self-incompatibility (SI) responses by SI protein (Staiger and Franklin-Tong, 2003). An SI protein produced by self-pistil triggers rapid growth arrest and subsequent cell death of pollen tubes (Thomas and Franklin-Tong, 2004). These responses include rapid reorganization of actin microfilaments in the tip and subsequent massive depolymerization of the whole actin cytoskeleton system in pollen tubes (Snowman et al., 2002). Changes to the actin cytoskeleton seem to be regulated by calcium signaling (Huang et al., 2004). The most rapid SI response in poppy pollen detected so far is the disappearance of tip-focused calcium gradients followed by a massive influx of calcium in the shank (Franklin-Tong et al., 2002). Calcium-sensitive profilin and gelsolins appear to be involved in SI-induced changes to the actin cytoskeleton (Huang et al., 2004).

In any signal-cytoskeleton response system, the final signaling targets are most likely cytoskeleton-associated proteins that control organization and dynamics. How a specific extracellular or intracellular signal regulates MAPs or ABPs is a question beginning to attract significant attention. ROP/Rac family GTPases have emerged as a key signaling switch in the regulation of the cytoskeleton in plants (Fu and Yang, 2001; Fu et al., 2002; Jones et al., 2002; Yang, 2002; Gu et al., 2004). ROPs (Rho-related GTPases from plants) have been shown to control tip growth in pollen tubes and root hairs and polar cell expansion in different cell types (Kost et al., 1999; Li et al., 1999; Fu et al., 2001, 2002; Molendijk et al., 2001; Jones et al., 2002; Yang, 2002). A common theme linking ROPs to polar growth in different cells is that localized ROP promotes localized organization of fine actin filaments (Yang, 2002), although ROPs appear to coordinate the actin-promoting pathway with distinct pathways in different forms of polar growth (Gu et al., 2004). ROPs are most likely activated by polarity signals in these cases, but the nature of polarity signals in plants and the mechanism by which polarity signals activate ROPs remain elusive. The SPK1 gene, originally identified in screens for trichome morphology mutants, encodes a putative guanine nucleotide exchange factor for ROPs and thus could be involved in signaling to ROPs (Qiu et al., 2002).

How ROP GTPases regulate cytoskeletal organization and dynamics is also becoming a topic of intense scrutiny. A potential link between ROPs and the putative Arp2/3 complex is hinted at by several recent studies showing that knocking out homologs of subunits of the WAVE complex produces phenotypes similar to those of the Arp2/3 complex mutants (Basu et al., 2004; Brembu et al., 2004; Deeks et al., 2004; El-Assal et al., 2004). In mammalian cells, Rac GTPases modulate the WAVE complex, which in turn affects either the activity or localization of the Arp2/3 complex (Bompard and Caron, 2004). In addition to the WAVE complex, Rac/Cdc42 can activate another class of Arp2/3 complex-activating proteins, such as WASP, which are apparently absent from the Arabidopsis genome (Yang, 2002). However, disrupting the function of ROPs results in a much more dramatic defect on both fine cortical actin microfilaments and polar cell growth than knocking out subunits of the putative Arabidopsis Arp2/3 complex (Li et al., 1999, 2003; Fu et al., 2001, 2002). These observations support the notion that ROPs may use a mechanism for the regulation of the actin cytoskeleton that is independent of the conserved Arp2/3 complex. This notion is consistent with the existence of a class of plant-specific ROP-interacting proteins, known as RICs, that appear to act as ROP-signaling targets (Wu et al., 2001). ROP inactivation of ADF appears to be another means by which these GTPases modulate actin remodeling (Chen et al., 2003).

Another potentially important cytoskeletal signaling mechanism is the MAP kinase (MAPK) cascade. One such MAPK cascade in tobacco has been shown to be required for cytokinesis (Nishihama et al., 2002; Soyano et al., 2003). Signaling targets of this kinase have not been clearly identified but could be microtubule-associated proteins that regulate the dynamics of phragmoplast microtubules. Interestingly, the MAPK cascade is activated by a kinesin-like protein that is also localized to the phragmoplast, implicating microtubules as signals for feedback regulation of phragmoplast microtubules (Soyano et al., 2003). The idea that a MAPK cascade mediates microtubule organization is further supported by demonstrating the involvement of a MAPK phosphatase in the control of cortical microtubule organization (Naoi and Hashimoto, 2004).

The study of cytoskeletal signaling in plants is still in its infancy, but linking signals and pathways to the regulation of MAPs and ABPs is expected to be a major future thrust in the field of the plant cytoskeleton.

Received November 10, 2004; returned for revision November 18, 2004; accepted November 19, 2004.

	FOOTNOTES

 
www.plantphysiol.org/cgi/doi/10.1104/pp.104.900133.

^* Corresponding authors; e-mail geoffwas{at}interchange.ubc.ca, zhenbiao.yang{at}ucr.edu; fax 604–822–6089, 951–827–4437.

	LITERATURE CITED

TOP NEW VIEWS ON FUNCTION LIVE VIEWS: ADVANTAGES AND... DYNAMIC VIEWS: CYTOSKELETAL... A FAR-REACHING VIEW: SIGNALS... LITERATURE CITED

 
Baskin TI, Beemster GT, Judy-March JE, Marga F (2004) Disorganization of cortical microtubules stimulates tangential expansion and reduces the uniformity of cellulose microfibril alignment among cells in the root of Arabidopsis. Plant Physiol 135: 2279–2290[Abstract/Free Full Text]

Basu D, El-Assal Sel-D, Le J, Mallery EL, Szymanski DB (2004) Interchangeable functions of Arabidopsis PIROGI and the human WAVE complex subunit SRA1 during leaf epidermal development. Development 131: 4345–4355[Abstract/Free Full Text]

Bisgrove SR, Hable WE, Kropf DL (2004) +TIPs and microtubule regulation. The beginning of the plus end in plants. Plant Physiol 136: 3855–3863[Free Full Text]

Bompard G, Caron E (2004) Regulation of WASP/WAVE proteins: making a long story short. J Cell Biol 166: 957–962[Abstract/Free Full Text]

Bouquin T, Mattsson O, Naested H, Foster R, Mundy J (2003) The Arabidopsis lue1 mutant defines a katanin p60 ortholog involved in hormonal control of microtubule orientation during cell growth. J Cell Sci 116: 791–801[Abstract/Free Full Text]

Brembu T, Winge P, Seem M, Bones AM (2004) NAPP and PIRP encode subunits of a putative wave regulatory protein complex involved in plant cell morphogenesis. Plant Cell 16: 2335–2349[Abstract/Free Full Text]

Buschmann H, Fabri CO, Hauptmann M, Hutzler P, Laux T, Lloyd CW, Schaffner AR (2004) Helical growth of the Arabidopsis mutant tortifolia1 reveals a plant-specific microtubule-associated protein. Curr Biol 14: 1515–1521[CrossRef][ISI][Medline]

Chan J, Calder GM, Doonan JH, Lloyd CW (2003) EB1 reveals mobile microtubule nucleation sites in Arabidopsis. Nat Cell Biol 5: 967–971[CrossRef][ISI][Medline]

Chan J, Mao G, Smertenko A, Hussey PJ, Naldrett M, Bottrill A, Lloyd CW (2003) Identification of a MAP65 isoform involved in directional expansion of plant cells. FEBS Lett 534: 161–163[CrossRef][Medline]

Chen CY, Cheung AY, Wu HM (2003) Actin-depolymerizing factor mediates Rac/Rop GTPase-regulated pollen tube growth. Plant Cell 15: 237–249[Abstract/Free Full Text]

Cheung AY, Wu HM (2004) Overexpression of an Arabidopsis formin stimulates supernumerary actin cable formation from pollen tube cell membrane. Plant Cell 16: 257–269[Abstract/Free Full Text]

Deeks MJ, Hussey PJ (2003) Arp2/3 and ‘the shape of things to come’. Curr Opin Plant Biol 6: 561–567[CrossRef][ISI][Medline]

Deeks MJ, Hussey PJ, Davies B (2002) Formins: intermediates in signal-transduction cascades that affect cytoskeletal reorganization. Trends Plant Sci 7: 492–498[CrossRef][Medline]

Deeks MJ, Kaloriti D, Davies B, Malho R, Hussey PJ (2004) Arabidopsis NAP1 is essential for Arp2/3-dependent trichome morphogenesis. Curr Biol 14: 1410–1414[CrossRef][ISI][Medline]

Dhonukshe P, Gadella TW Jr (2003) Alteration of microtubule dynamic instability during preprophase band formation revealed by yellow fluorescent protein-CLIP170 microtubule plus-end labeling. Plant Cell 15: 597–611[Abstract/Free Full Text]

Dhonukshe P, Laxalt AM, Goedhart J, Gadella TW, Munnik T (2003) Phospholipase D activation correlates with microtubule reorganization in living plant cells. Plant Cell 15: 2666–2679[Abstract/Free Full Text]

Dixit R, Cyr R (2004) The cortical microtubule array: from dynamics to organization. Plant Cell 16: 2546–2552[Free Full Text]

Drykova D, Cenklova V, Sulimenko V, Volc J, Draber P, Binarova P (2003) Plant gamma-tubulin interacts with alphabeta-tubulin dimers and forms membrane-associated complexes. Plant Cell 15: 465–480[Abstract/Free Full Text]

El-Assal Sel-D, Le J, Basu D, Mallery EL, Szymanski DB (2004) Arabidopsis GNARLED encodes a NAP125 homolog that positively regulates ARP2/3. Curr Biol 14: 1405–1409[CrossRef][ISI][Medline]

El-Din El-Assal S, Le J, Basu D, Mallery EL, Szymanski DB (2004) DISTORTED2 encodes an ARPC2 subunit of the putative Arabidopsis ARP2/3 complex. Plant J 38: 526–538[CrossRef][ISI][Medline]

Erhardt M, Stoppin-Mellet V, Campagne S, Canaday J, Mutterer J, Fabian T, Sauter M, Muller T, Peter C, Lambert AM, et al (2002) The plant Spc98p homologue colocalizes with gamma-tubulin at microtubule nucleation sites and is required for microtubule nucleation. J Cell Sci 115: 2423–2431[Abstract/Free Full Text]

Frank MJ, Smith LG (2002) A small, novel protein highly conserved in plants and animals promotes the polarized growth and division of maize leaf epidermal cells. Curr Biol 12: 849–853[CrossRef][ISI][Medline]

Franklin-Tong VE, Holdaway-Clarke TL, Straatman KR, Kunkel JG, Hepler PK (2002) Involvement of extracellular calcium influx in the self-incompatibility response of Papaver rhoeas. Plant J 29: 333–345[CrossRef][ISI][Medline]

Fu Y, Li H, Yang ZB (2002) The ROP2 GTPase controls the formation of cortical fine F-actin and the early phase of directional cell expansion during Arabidopsis organogenesis. Plant Cell 14: 777–794[Abstract/Free Full Text]

Fu Y, Wu G, Yang ZB (2001) Rop GTPase-dependent dynamics of tip-localized F-actin controls tip growth in pollen tubes. J Cell Biol 152: 1019–1032[Abstract/Free Full Text]

Fu Y, Yang Z (2001) Rop GTPase: a master switch of cell polarity development in plants. Trends Plant Sci 6: 545–547[CrossRef][ISI][Medline]

Gard DL, Becker BE, Josh Romney S (2004) MAPping the eukaryotic tree of life: structure, function, and evolution of the MAP215/Dis1 family of microtubule-associated proteins. Int Rev Cytol 239: 179–272[ISI][Medline]

Gardiner J, Collings DA, Harper JD, Marc J (2003) The effects of the phospholipase D-antagonist 1-butanol on seedling development and microtubule organisation in Arabidopsis. Plant Cell Physiol 44: 687–696[Abstract/Free Full Text]

Gardiner JC, Harper JD, Weerakoon ND, Collings DA, Ritchie S, Gilroy S, Cyr RJ, Marc J (2001) A 90-kD phospholipase D from tobacco binds to microtubules and the plasma membrane. Plant Cell 13: 2143–2158[Abstract/Free Full Text]

Gibbon BC, Zonia LE, Kovar DR, Hussey PJ, Staiger CJ (1998) Pollen profilin function depends on interaction with proline-rich motifs. Plant Cell 10: 981–993[Abstract/Free Full Text]

Granger CL, Cyr RJ (2001) Spatiotemporal relationships between growth and microtubule orientation as revealed in living root cells of Arabidopsis thaliana transformed with green-fluorescent-protein gene construct GFP-MBD. Protoplasma 216: 201–214[ISI][Medline]

Gu Y, Wang Z, Yang Z (2004) ROP/RAC GTPase: an old new master regulator for plant signaling. Curr Opin Plant Biol 7: 527–536[CrossRef][ISI][Medline]

Hamada T, Igarashi H, Itoh TJ, Shimmen T, Sonobe S (2004) Characterization of a 200 kDa microtubule-associated protein of tobacco BY-2 cells, a member of the XMAP215/MOR1 family. Plant Cell Physiol 45: 1233–1242[Abstract/Free Full Text]

Hashimoto T (2003) Dynamics and regulation of plant interphase microtubules: a comparative view. Curr Opin Plant Biol 6: 568–576[CrossRef][ISI][Medline]

Himmelspach R, Williamson RE, Wasteneys GO (2003) Cellulose microfibril alignment recovers from DCB-induced disruption despite microtubule disorganization. Plant J 36: 565–575[CrossRef][ISI][Medline]

Huang S, Blanchoin L, Chaudhry F, Franklin-Tong VE, Staiger CJ (2004) A gelsolin-like protein from Papaver rhoeas pollen (PrABP80) stimulates calcium-regulated severing and depolymerization of actin filaments. J Biol Chem 279: 23364–23375[Abstract/Free Full Text]

Huang S, Blanchoin L, Kovar DR, Staiger CJ (2003) Arabidopsis capping protein (AtCP) is a heterodimer that regulates assembly at the barbed ends of actin filaments. J Biol Chem 278: 44832–44842[Abstract/Free Full Text]

Hussey PJ, Allwood EG, Smertenko AP (2002) Actin-binding proteins in the Arabidopsis genome database: properties of functionally distinct plant actin-depolymerizing factors/cofilins. Philos Trans R Soc Lond B Biol Sci 357: 791–798[CrossRef][ISI][Medline]

Jones MA, Shen JJ, Fu Y, Li H, Yang ZB, Grierson CS (2002) The Arabidopsis Rop2 GTPase is a positive regulator of both root hair initiation and tip growth. Plant Cell 14: 763–776[Abstract/Free Full Text]

Ketelaar T, Allwood EG, Anthony R, Voigt B, Menzel D, Hussey PJ (2004a) The actin-interacting protein AIP1 is essential for actin organization and plant development. Curr Biol 14: 145–149[CrossRef][ISI][Medline]

Ketelaar T, Anthony RG, Hussey PJ (2004b) Green fluorescent protein-mTalin causes defects in actin organization and cell expansion in Arabidopsis and inhibits actin depolymerizing factor's actin depolymerizing activity in vitro. Plant Physiol 136: 3990–3998[Abstract/Free Full Text]

Klahre U, Friederich E, Kost B, Louvard D, Chua NH (2000) Villin-like actin-binding proteins are expressed ubiquitously in Arabidopsis. Plant Physiol 122: 35–47[Abstract/Free Full Text]

Kost B, Lemichez E, Spielhofer P, Hong Y, Tolias K, Carpenter C, Chua NH (1999) Rac homologues and compartmentalized phosphatidylinositol 4, 5-bisphosphate act in a common pathway to regulate polar pollen tube growth. J Cell Biol 145: 317–330[Abstract/Free Full Text]

Kost B, Spielhofer P, Chua NH (1998) A GFP-mouse talin fusion protein labels plant actin filaments in vivo and visualizes the actin cytoskeleton in growing pollen tubes. Plant J 16: 393–401[CrossRef][ISI][Medline]

Kost B, Chua NH (2002) The plant cytoskeleton: vacuoles and cell walls make the difference. Cell 108: 9–12[CrossRef][ISI][Medline]

Kovar DR, Drobak BK, Staiger CJ (2000) Maize profilin isoforms are functionally distinct. Plant Cell 12: 583–598[Abstract/Free Full Text]

Kumagai F, Nagata T, Yahara N, Moriyama Y, Horio T, Naoi K, Hashimoto T, Murata T, Hasezawa S (2003) Gamma-tubulin distribution during cortical microtubule reorganization at the M/G1 interface in tobacco BY-2 cells. Eur J Cell Biol 82: 43–51[CrossRef][ISI][Medline]

Le J, El-Assal Sel D, Basu D, Saad ME, Szymanski DB (2003) Requirements for Arabidopsis ATARP2 and ATARP3 during epidermal development. Curr Biol 13: 1341–1347[CrossRef][ISI][Medline]

Lee Y-RJ, Liu B (2004) Cytoskeletal motors in Arabidopsis. Sixty-one kinesins and seventeen myosins. Plant Physiol 136: 3877–3883[Free Full Text]

Li H, Lin Y, Heath RM, Zhu MX, Yang Z (1999) Control of pollen tube tip growth by a Rop GTPase-dependent pathway that leads to tip-localized calcium influx. Plant Cell 11: 1731–1742[Abstract/Free Full Text]

Li S, Blanchoin L, Yang Z, Lord EM (2003) The putative Arabidopsis arp2/3 complex controls leaf cell morphogenesis. Plant Physiol 132: 2034–2044[Abstract/Free Full Text]

Lloyd C, Chan J (2004) Microtubules and the shape of plants to come. Nat Rev Mol Cell Biol 5: 13–22[CrossRef][ISI][Medline]

Marc J, Sharkey DE, Durso NA, Zhang M, Cyr RJ (1996) Isolation of a 90-kD microtubule-associated protein from tobacco membranes. Plant Cell 8: 2127–2138[Abstract]

Mathur J, Hulskamp M (2002) Microtubules and microfilaments in cell morphogenesis in higher plants. Curr Biol 12: R669–R676[CrossRef][ISI][Medline]

Mathur J, Mathur N, Kernebeck B, Hulskamp M (2003a) Mutations in actin-related proteins 2 and 3 affect cell shape development in Arabidopsis. Plant Cell 15: 1632–1645[Abstract/Free Full Text]

Mathur J, Mathur N, Kernebeck B, Srinivas BP, Hulskamp M (2003b) A novel localization pattern for an EB1-like protein links microtubule dynamics to endomembrane organization. Curr Biol 13: 1991–1997[CrossRef][ISI][Medline]

Mathur J, Mathur N, Kirik V, Kernebeck B, Srinivas BP, Hulskamp M (2003c) Arabidopsis CROOKED encodes for the smallest subunit of the ARP2/3 complex and controls cell shape by region specific fine F-actin formation. Development 130: 3137–3146[Abstract/Free Full Text]

McCurdy DW, Kovar DR, Staiger CJ (2001) Actin and actin-binding proteins in higher plants. Protoplasma 215: 89–104[CrossRef][ISI][Medline]

McKenna ST, Vidali L, Hepler PK (2004) Profilin inhibits pollen tube growth through actin-binding, but not poly-L-proline-binding. Planta 218: 906–915[CrossRef][ISI][Medline]

McKinney EC, Kandasamy MK, Meagher RB (2001) Small changes in the regulation of one Arabidopsis profilin isovariant, PRF1, alter seedling development. Plant Cell 13: 1179–1191[Abstract/Free Full Text]

Molendijk AJ, Bischoff F, Rajendrakumar CS, Friml J, Braun M, Gilroy S, Palme K (2001) Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growth. EMBO J 20: 2779–2788[CrossRef][ISI][Medline]

Muller S, Smertenko A, Wagner V, Heinrich M, Hussey PJ, Hauser MT (2004) The plant microtubule-associated protein AtMAP65-3/PLE is essential for cytokinetic phragmoplast function. Curr Biol 14: 412–417[CrossRef][ISI][Medline]

Nakajima K, Furutani I, Tachimoto H, Matsubara H, Hashimoto T (2004) SPIRAL1 encodes a plant-specific microtubule-localized protein required for directional control of rapidly expanding Arabidopsis cells. Plant Cell 16: 1178–1190[Abstract/Free Full Text]

Nakamura M, Naoi K, Shoji T, Hashimoto T (2004) Low concentrations of propyzamide and oryzalin alter microtubule dynamics in Arabidopsis epidermal cells. Plant Cell Physiol 45: 1330–1334[Abstract/Free Full Text]

Naoi K, Hashimoto T (2004) A semidominant mutation in an Arabidopsis mitogen-activated protein kinase phosphatase-like gene compromises cortical microtubule organization. Plant Cell 16: 1841–1853[Abstract/Free Full Text]

Nishihama R, Soyano T, Ishikawa M, Araki S, Tanaka H, Asada T, Irie K, Ito M, Terada M, Banno H, et al (2002) Expansion of the cell plate in plant cytokinesis requires a kinesin-like protein/MAPKKK complex. Cell 109: 87–99[CrossRef][ISI][Medline]

Qiu JL, Jilk R, Marks MD, Szymanski DB (2002) The Arabidopsis SPIKE1 gene is required for normal cell shape control and tissue development. Plant Cell 14: 101–118[Abstract/Free Full Text]

Ramachandran S, Christensen HEM, Ishimaru Y, Dong CH, Chao-Ming W, Cleary AL, Chua NH (2000) Profilin plays a role in cell elongation, cell shape maintenance, and flowering in arabidopsis. Plant Physiol 124: 1637–1647[Abstract/Free Full Text]

Romero S, Le Clainche C, Didry D, Egile C, Pantaloni D, Carlier MF (2004) Formin is a processive motor that requires profilin to accelerate actin assembly and associated ATP hydrolysis. Cell 119: 419–429[CrossRef][ISI][Medline]

Schmit AC (2002) Acentrosomal microtubule nucleation in higher plants. Int Rev Cytol 220: 257–289[ISI][Medline]

Sedbrook JC (2004) MAPs in plant cells: delineating microtubule growth dynamics and organization. Curr Opin Plant Biol 7: 632–640[CrossRef][ISI][Medline]

Sedbrook JC, Ehrhardt DW, Fisher SE, Scheible WR, Somerville CR (2004) The Arabidopsis sku6/spiral1 gene encodes a plus end-localized microtubule-interacting protein involved in directional cell expansion. Plant Cell 16: 1506–1520[Abstract/Free Full Text]

Segui-Simarro JM, Austin JR II, White EA, Staehelin LA (2004) Electron tomographic analysis of somatic cell plate formation in meristematic cells of Arabidopsis preserved by high-pressure freezing. Plant Cell 16: 836–856[Abstract/Free Full Text]

Shaw SL, Kamyar R, Ehrhardt DW (2003) Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science 300: 1715–1718[Abstract/Free Full Text]

Sheahan MB, Staiger CJ, Rose RJ, McCurdy DW (2004) A green fluorescent protein fusion to actin-binding domain 2 of Arabidopsis fimbrin highlights new features of a dynamic actin cytoskeleton in live plant cells. Plant Physiol 136: 3968–3978[Abstract/Free Full Text]

Shimamura M, Brown RC, Lemmon BE, Akashi T, Mizuno K, Nishihara N, Tomizawa K, Yoshimoto K, Deguchi H, Hosoya H, et al (2004) Gamma-tubulin in basal land plants: characterization, localization, and implication in the evolution of acentriolar microtubule organizing centers. Plant Cell 16: 45–59[Abstract/Free Full Text]

Shoji T, Narita NN, Hayashi K, Asada J, Hamada T, Sonobe S, Nakajima K, Hashimoto T (2004) Plant-specific microtubule-associated protein SPIRAL2 is required for anisotropic growth in Arabidopsis. Plant Physiol 136: 3933–3944[Abstract/Free Full Text]

Smith LG (2003) Cytoskeletal control of plant cell shape: getting the fine points. Curr Opin Plant Biol 6: 63–73[CrossRef][ISI][Medline]

Snowman BN, Kovar DR, Shevchenko G, Franklin-Tong VE, Staiger CJ (2002) Signal-mediated depolymerization of actin in pollen during the self-incompatibility response. Plant Cell 14: 2613–2626[Abstract/Free Full Text]

Soyano T, Nishihama R, Morikiyo K, Ishikawa M, Machida Y (2003) NQK1/NtMEK1 is a MAPKK that acts in the NPK1 MAPKKK-mediated MAPK cascade and is required for plant cytokinesis. Genes Dev 17: 1055–1067[Abstract/Free Full Text]

Staiger CJ, Franklin-Tong VE (2003) The actin cytoskeleton is a target of the self-incompatibility response in Papaver rhoeas. J Exp Bot 54: 103–113[Abstract/Free Full Text]

Stoppin-Mellet V, Gaillard J, Vantard M (2002) Functional evidence for in vitro microtubule severing by the plant katanin homologue. Biochem J 365: 337–342[CrossRef][ISI][Medline]

Sugimoto K, Himmelspach R, Williamson RE, Wasteneys GO (2003) Mutation or drug-dependent microtubule disruption causes radial swelling without altering parallel cellulose microfibril deposition in Arabidopsis root cells. Plant Cell 15: 1414–1429[Abstract/Free Full Text]

Thomas SG, Franklin-Tong VE (2004) Self-incompatibility triggers programmed cell death in Papaver pollen. Nature 429: 305–309[CrossRef][Medline]

Takemoto D, Hardham AR (2004) The cytoskeleton as a regulator and target of biotic interactions in plants. Plant Physiol 136: 3864–3876[Free Full Text]

Twell D, Park SK, Hawkins TJ, Schubert D, Schmidt R, Smertenko A, Hussey PJ (2002) MOR1/GEM1 has an essential role in the plant-specific cytokinetic phragmoplast. Nat Cell Biol 4: 711–714[CrossRef][ISI][Medline]

Ueda K, Matsuyama T, Hashimoto T (1999) Visualization of microtubules in living cells of transgenic Arabidopsis thaliana. Protoplasma 206: 201–206[CrossRef]

Van Bruaene N, Joss G, Van Oostveldt P (2004) Reorganization and in vivo dynamics of microtubules during Arabidopsis root hair development. Plant Physiol 136: 3905–3919[Abstract/Free Full Text]

Van Damme D, Van Poucke K, Boutant E, Ritzenthaler C, Inzé D, Geelen D (2004) In vivo dynamics and differential microtubule-binding activities of MAP65 proteins. Plant Physiol 136: 3956–3967[Abstract/Free Full Text]

Wang YS, Motes CM, Mohamalawari DR, Blancaflor EB (2004) Green fluorescent protein fusions to Arabidopsis fimbrin 1 for spatio-temporal imaging of F-actin dynamics in roots. Cell Motil Cytoskeleton 59: 79–93[CrossRef][ISI][Medline]

Wasteneys GO (2002) Microtubule organization in the green kingdom: chaos or self-order? J Cell Sci 115: 1345–1354[Abstract/Free Full Text]

Wasteneys GO (2004) Progress in understanding the role of microtubules in plant cells. Curr Opin Plant Biol 7: 651–660[CrossRef][ISI][Medline]

Wasteneys GO, Galway ME (2003) Remodeling the cytoskeleton for growth and form: an overview with some new views. Annu Rev Plant Biol 54: 691–722[CrossRef][Medline]

Whittington AT, Vugrek O, Wei KJ, Hasenbein NG, Sugimoto K, Rashbrooke MC, Wasteneys GO (2001) MOR1 is essential for organizing cortical microtubules in plants. Nature 411: 610–613[CrossRef][Medline]

Wicker-Planquart C, Stoppin-Mellet V, Blanchoin L, Vantard M (2004) Interactions of tobacco microtubule-associated protein MAP65-1b with microtubules. Plant J 39: 126–134[CrossRef][ISI][Medline]

Wu G, Gu Y, Li S, Yang Z (2001) A genome-wide analysis of Arabidopsis Rop-interactive CRIB motif-containing proteins that act as Rop GTPase targets. Plant Cell 13: 2841–2856[Abstract/Free Full Text]

Yang Z (2002) Small GTPases: versatile signaling switches in plants. Plant Cell (Suppl) 14: S375–S388

Yasuhara H, Muraoka M, Shogaki H, Mori H, Sonobe S (2002) TMBP200, a microtubule bundling polypeptide isolated from telophase tobacco BY-2 cells is a MOR1 homologue. Plant Cell Physiol 43: 595–603[Abstract/Free Full Text]

This article has been cited by other articles:

				E. Kawamura and G. O. Wasteneys MOR1, the Arabidopsis thaliana homologue of Xenopus MAP215, promotes rapid growth and shrinkage, and suppresses the pausing of microtubules in vivo J. Cell Sci., December 15, 2008; 121(24): 4114 - 4123. [Abstract] [Full Text] [PDF]

				S. Wang, G.-H. Zhao, Y.-H. Jia, and X.-M. Du Cloning and Characterization of a CAP Gene Expressed in Gossypium arboreum Fuzzless Mutant Crop Sci., November 24, 2008; 48(6): 2314 - 2320. [Abstract] [Full Text] [PDF]

				A. S. Rajangam, M. Kumar, H. Aspeborg, G. Guerriero, L. Arvestad, P. Pansri, C. J.-L. Brown, S. Hober, K. Blomqvist, C. Divne, et al. MAP20, a Microtubule-Associated Protein in the Secondary Cell Walls of Hybrid Aspen, Is a Target of the Cellulose Synthesis Inhibitor 2,6-Dichlorobenzonitrile Plant Physiology, November 1, 2008; 148(3): 1283 - 1294. [Abstract] [Full Text] [PDF]

				T. Nakayama, T. Ishii, T. Hotta, and K. Mizuno Radial Microtubule Organization by Histone H1 on Nuclei of Cultured Tobacco BY-2 Cells J. Biol. Chem., June 13, 2008; 283(24): 16632 - 16640. [Abstract] [Full Text] [PDF]

				M. Iwano, H. Shiba, K. Matoba, T. Miwa, M. Funato, T. Entani, P. Nakayama, H. Shimosato, A. Takaoka, A. Isogai, et al. Actin Dynamics in Papilla Cells of Brassica rapa during Self- and Cross-Pollination Plant Physiology, May 1, 2007; 144(1): 72 - 81. [Abstract] [Full Text] [PDF]

				S. D.X. Chuong, V. R. Franceschi, and G. E. Edwards The Cytoskeleton Maintains Organelle Partitioning Required for Single-Cell C4 Photosynthesis in Chenopodiaceae Species PLANT CELL, September 1, 2006; 18(9): 2207 - 2223. [Abstract] [Full Text] [PDF]

				N. Kanzawa, Y. Hoshino, M. Chiba, D. Hoshino, H. Kobayashi, N. Kamasawa, Y. Kishi, M. Osumi, M. Sameshima, and T. Tsuchiya Change in the Actin Cytoskeleton during Seismonastic Movement of Mimosa pudica Plant Cell Physiol., April 1, 2006; 47(4): 531 - 539. [Abstract] [Full Text] [PDF]