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First published online March 2, 2007; 10.1105/tpc.106.048579 The Plant Cell 19:877-889 (2007) © 2007 American Society of Plant Biologists Arabidopsis MICROTUBULE-ASSOCIATED PROTEIN18 Functions in Directional Cell Growth by Destabilizing Cortical Microtubules
a State Key Laboratory of Plant Physiology and Biochemistry, Department of Plant Sciences, College of Biological Sciences, China Agricultural University, Beijing 100094, China 2 To whom correspondence should be addressed. E-mail mingyuan{at}cau.edu.cn; fax 86-10-62733491.
Microtubule-associated proteins (MAPs) play important roles in the regulation of microtubule function in cells. We describe Arabidopsis thaliana MAP18, which binds to microtubules and inhibits tubulin polymerization in vitro and colocalizes along cortical microtubules as patches of dot-like structures. MAP18 is expressed mostly in the expanding cells. Cells overexpressing MAP18 in Arabidopsis exhibit various growth phenotypes with loss of polarity. Cortical microtubule arrays were significantly altered in cells either overexpressing MAP18 or where it had been downregulated by RNA interference (RNAi). The cortical microtubules were more sensitive to treatment with microtubule-disrupting drugs when MAP18 was overexpressed, but more resistant when MAP18 was eliminated in cells expressing MAP18 RNAi. Our study demonstrated that MAP18 may play a role in regulating directional cell growth and cortical microtubule organization by destabilizing microtubules.
Microtubule-associated proteins (MAPs) play critical roles in controlling microtubule (MT) dynamics and organization and hence are involved in the regulation of cell expansion (Lloyd and Chan, 2002  ; Hussey et al., 2002; Wasteneys and Galway, 2003; Mathur, 2004; Sedbrook, 2004; Smith and Oppenheimer, 2005). Mutations in proteins interacting with MTs result in abnormal plant development and plant cell morphogenesis due to disruption of MT organization. For instance, mutations in MOR1/GEM1, which stabilizes cortical MTs, result in organ twisting and isotropic cell expansion in roots as a result of defects in MT organization and cytokinesis (Twell et al., 2001; Whittington et al., 2001). Mutation of Arabidopsis thaliana SKU6/SPIRAL1, which encodes a plus end–localized MT-interacting protein, causes right-handed axial twisting in roots, etiolated hypocotyls, leaf petioles, and strongly right-skewed root growth on inclined agar media (Sedbrook et al., 2004). The radial expansion defect is also observed in katanin mutants (Burk and Ye, 2002; Webb et al., 2002). RIC1, a novel MT binding protein interacting with ROP GTPase, promotes the organization of cortical MTs locally to inhibit outgrowth of the Arabidopsis pavement cells (Fu et al., 2005). Also, mutations in ATMAP65-1 and ATMAP65-3/PLEIADE result in expanded short root phenotypes resulting from defective cytokinesis (Muller et al., 2004; Smertenko et al., 2004).
Several MT binding domains in interacting proteins have been described. One domain is the repetitive K-K-E-E and K-K-E-I/V motifs, which were first identified in a neural MT-associated protein, MAP1B from mouse. This has no structural relationship with the MT binding domains of kinesin, MAP2, or Tau (Noble et al., 1989
Here, we report the identification of a plant MAP, MAP18 from Arabidopsis, which was identified by an Arabidopsis genome BLAST search using the sequence of V-V-E-K-K-N/E-E. MAP18 destabilizes MTs and plays an important role in the regulation of MT organization to determine plant directional cell growth.
Identification of the MAP18 Gene and Purification of the Recombinant Protein A BLAST search of the Arabidopsis genome sequence identified a gene (At5g44610) located on chromosome 5, encoding a protein with unknown function and containing seven repeated motifs of V-E-E-K-K. The full-length cDNA sequence (CDS) encodes a predicted polypeptide of 168 amino acid residues, with an estimated molecular mass of 18.5 kD and a pI of 4.57. The gene has two exons (1 to 65 and 429 to 1104) and one intron (66 to 428) (www.arabidopsis.org). The coding region (445 to 951) is at the second exon (Figure 1).
To characterize the activity of this protein on MTs, we cloned the full-length CDS into the pGEX-4T vector and transformed the plasmid into Escherichia coli. The expressed recombinant protein was then purified with a glutathione sepharose 4B resin column and analyzed using SDS-PAGE (Figure 2
). The results indicate that purified recombinant protein was obtained. Although the predicated molecular mass of this protein is
MAP18 Binds to MTs in Vitro and Colocalizes with Cortical MTs in Vivo To address the question whether this protein is a MAP or not, we assessed the binding activity of the recombinant protein to taxol-stabilized MTs using cosedimentation experiments. Preformed taxol-MTs (5 µM) were incubated with various concentrations (0, 0.5, 1, 2, 4, and 6 µM) of the recombinant protein (glutathione S-transferase [GST] removed) and centrifuged after incubation. SDS-PAGE analysis of the pellets showed that the protein bound to and cosedimented with MTs (Figure 3A ). Scanning of the SDS-PAGE gel showed that the mass of recombinant protein in the pellets increased as higher concentrations of recombinant protein were added, before reaching saturation (Figure 3B). The molar binding ratio of the recombinant protein to the tubulin dimer was estimated to be  0.4:1 at the saturation level. To further confirm that this protein binds to MTs, we raised its antibody and performed in vitro immunofluorescence labeling. Preformed rhodamine-labeled MTs stabilized with taxol were incubated with the recombinant protein. Samples were stained with the antibody and secondary antibody and observed on a CCD camera. The observations showed that the protein formed dot-like structures along MTs (Figures 3C to 3E), while no such structures were observed when the protein was denatured by boiling (Figures 3F to 3H) or stained with secondary antibody alone (Figures 3I to 3K). Thus, we conclude that this protein is capable of binding to MTs in vitro, and it was named MAP18.
To further investigate the localization of MAP18 in cells, we conducted double immunofluorescence microscopy to visualize both MAP18 and MTs in cells. Confocal microscopy observations showed that MAP18 formed dot-like structures both in the cytoplasm and the cortex of root epidermal cells. Close observation showed that such dot-like structures of MAP18 were colocalized with cortical MTs (Figures 3L to 3N). Staining of MAP18 with preimmune serum showed no MAP18 signal detected when MTs were double stained (Figures 3O and 3P). A linear-dotted pattern could still be seen in cells stained with anti-MAP18 antibody without MT labeling (Figure 3Q). Our observations demonstrated that MAP18 binds to MTs not only in vitro but also in vivo.
MAP18 Inhibits Tubulin Polymerization
To further confirm this result, MTs were polymerized from rhodamine-labeled tubulin in the presence and absence of MAP18. The observation showed that fewer MTs formed in the presence of 10 µM GST-MAP18 (Figure 4C) compared with MTs in the absence of MAP18 (Figure 4B). GST (10 µM), used as a control, had no effect on MT formation (Figure 4D). This observation is consistent with the results from the turbidimetrical analysis. Therefore, we conclude that MAP18 has an inhibitory effect on tubulin polymerization. In addition, our observations of MTs at various concentrations of MAP18 indicated that MTs were always present as single-filament patterns, and no MT bundles were observed (Figure 4C).
The Expression Pattern of MAP18
Furthermore, we transformed Arabidopsis with a MAP18 promoter:ß-glucuronidase (GUS) gene fusion construct to determine the expression pattern of MAP18 in tissues and organs. Thirty-five transgenic lines were analyzed. GUS activity was detected in root (Figures 5C and 5G), flower (Figure 5D), cotyledon (Figures 5C and 5E), hypocotyls (Figure 5C), trichome stalks (Figure 5F), root hairs (Figure 5H), and lateral root (Figure 5I) but not in root tip and mature leaves (Figures 5C, 5G, and 5I). Our GUS experiment results were not fully consistent with the data of gene chip analysis in the Genevestigator database. GUS activity was detected both in elongation tissues and some mature tissues, suggesting that MAP18 may function during and after cell growth. To analyze the in vivo function of MAP18 in Arabidopsis, both RNA interference (RNAi) and overexpressing transgenic plants were generated. Fifty-two lines of MAP18 RNAi and 12 lines of MAP18-overexpressing Arabidopsis were obtained. The MAP18 RNAi lines having cotyledon pavement cells with fewer extension lobes and shorter cell length, and MAP18-overexpressing lines with a root skewing phenotype were selected for further study. Nineteen lines of MAP18 RNAi Arabidopsis and six homozygous lines of MAP18-overexpressing Arabidopsis showing such phenotypes were selected and analyzed. Line 2 of MAP18-overexpressing Arabidopsis (OE2) and line 18 of MAP18 RNAi transgenic Arabidopsis (R18) were selected for cell and MT analysis. The transcription level of MAP18 was determined by RNA gel blots and RT-PCR analysis (Figure 6 ). The results indicated that MAP18 expression was considerably enhanced in the overexpressing lines and inhibited in the RNAi lines.
Observation of the MT arrays of cells in the root tips showed that the mitotic index was not significantly affected in MAP18-overexpressing and RNAi Arabidopsis (Table 1 ), suggesting that MAP18 function is not required for cell division.
MAP18 Transgenic Arabidopsis Lines Show Abnormal Root Growth and Defects of Directional Cell Growth Examination of the transgenic Arabidopsis lines showed that overexpression of MAP18 gave rise to several abnormalities in root growth and cell directional expansion (Figure 7 ). The roots of MAP18-overexpressing Arabidopsis lines showed a left-handed skewing pattern when grown on the surface of Murashige and Skoog (MS) medium containing 1% agar (Figure 7B). The files of the root epidermal cells also exhibited a left-handed twist in these lines (Figure 7E). However, roots and root epidermal cell files showed no left-skewing and twisting growth in both wild-type and MAP18 RNAi lines (Figures 7A, 7C, 7D, and 7F).
Abnormal cell shapes were also observed in cells exhibiting anisotropic growth, such as hypocotyl cells and cotyledon pavement cells. Measurements of 7-d-old seedlings showed that MAP18 overexpression resulted in shorter hypocotyls, but there was no difference between MAP18 RNAi and wild-type plants in hypocotyl length (Figures 7G to 7I, Table 2 ). The observation of hypocotyls by scanning electron microscopy revealed that the epidermal cells of hypocotyls overexpressing MAP18 were spindle-shaped and formed a jagged surface (Figure 7K). On the other hand, the hypocotyl epidermal cells of MAP18 RNAi Arabidopsis showed a shorter and laterally expanded pattern (Figure 7L) compared with wild-type cells (Figure 7J). Further observation of the hypocotyl cells by cross and longitudinal section microscopy revealed an overall swelling pattern, and the cell layers were obviously disordered in MAP18-overexpressing Arabidopsis (Figures 7M to 7R). Measurements of hypocotyl epidermal cells showed that the cells of MAP18-overexpressing hypocotyls were shorter in length and wider (Table 2). Besides the epidermal cells, the cortex cells of MAP18-overexpressing hypocotyls were much fatter and in many cases had oblique end walls between them instead of vertical end walls in wild-type cells (Figures 7N and 7Q). Measurements also showed that cortex cells of MAP18-overexpressing line hypocotyls were also shorter in length and wider compared with the wild type (Table 2). However, the cortex cells of MAP18 RNAi hypocotyls showed no abnormality (Figures 7O and 7R), compared with the wild type (Figures 7M and 7P, Table 2).
Mature pavement cells of Arabidopsis cotyledons usually have a jigsaw puzzle shape at their periphery. They have lobes intercalated with the neck of adjacent cells and thus display various sizes of radial diameter (Figure 7S). However, cotyledon pavement cells of Arabidopsis overexpressing MAP18 were longer in cell length and narrower at their necks than that of wild-type pavement cells (Table 2). The lobes of the cell were dramatically eliminated, resulting in nearly rectangular or spindle-like cells with straight-sided walls (Figure 7T, Table 2). In MAP18 RNAi transgenic Arabidopsis, the pavement cells of cotyledons also showed certain abnormalities. The lobes of the cell had much less extension, although the number of lobes remained almost the same, and the length of cells was much shorter compared with the wild type (Figure 7U, Table 2). Microscopy of cotyledon sections showed that cell shapes of not only epidermal but also cortex cells changed both in MAP18-overexpressing and MAP18 RNAi transgenic Arabidopsis, exhibiting a rounded pattern, with obviously disordered cell layers (Figures 7V to 7X). The cotyledons of MAP18-overexpressing Arabidopsis usually had a curved growth pattern (Figure 7H), while those of MAP18 RNAi transgenic Arabidopsis showed no abnormalities (Figure 7I) compared with the wild type (Figure 7G).
The Organization of Cortical MTs Is Affected in MAP18 Transgenic Arabidopsis Cells
In mature cotyledon pavement cells of wild-type Arabidopsis, the cortical MTs usually formed a randomly oriented array and sometimes localized densely around the neck region (Figure 8A , left panel). However, in MAP18-overexpressing cotyledon pavement cells the cortical MTs were mostly organized into an array of parallel MTs orientated transversely against the long axis, a pattern often present in the earlier stages of pavement cell development (Figure 8A, middle panel). In cotyledon pavement cells of MAP18 RNAi Arabidopsis, the cortical MTs also exhibited an array of parallel MTs, although mostly along the long growth axis of the cell (Figure 8A, right panel).
In wild-type hypocotyl epidermal cells, cortical MTs were usually organized into a parallel array, transversely oriented to the longitudinal growth axis (Figure 8B, left panel). However, only a small proportion of cells in MAP18-overexpressing and RNAi Arabidopsis hypocotyls had transversely parallel arrays of MTs (Table 3). Cortical MTs in hypocotyl epidermal cells of MAP18-overexpressing Arabidopsis (Figure 8B, middle panel) and MAP18 RNAi Arabidopsis (Figure 8B, right panel) showed a parallel array that was mostly oblique to the long expansion axis of the cell. Because it was difficult to observe the MTs in root cells with GFP-tubulin Arabidopsis, we used immunofluorescence microscopy to visualize cortical MTs in root epidermal cells. The root epidermal cells of wild-type Arabidopsis also had transverse cortical MTs (Figure 8C, left panel). However, the cortical MTs in root epidermal cells overexpressing MAP18 were mostly organized into oblique or longitudinal arrays (Figure 8C, middle panel). On the other hand, cortical MTs in root epidermal cells of the MAP18 RNAi Arabidopsis were generally transverse, similar to wild-type cells (Figure 8C, right panel). Our observations indicated that either the overexpression or the elimination of MAP18 results in the abnormal organization of cortical MTs and, as a consequence, abnormalities in cell morphogenesis.
MAP18-Overexpressing Arabidopsis Lines Are Hypersensitive to MT-Disrupting Drugs
To further confirm this, we compared MTs in cells of wild-type, MAP18-overexpressing, and MAP18 RNAi Arabidopsis hypocotyls after treatment with oryzalin, another MT-disrupting drug. Observations showed that MTs were disrupted in hypocotyl epidermal cells in MAP18-overexpressing lines, while MTs in cells of wild-type and MAP18 RNAi Arabidopsis hypocotyls remained almost normal after the treatment of 5 µM oryzalin for 15 min (Figure 10A ). Increasing oryzalin concentration or treatment time resulted in the disruption of cortical MTs in cells of both wild-type and MAP18-overexpressing Arabidopsis hypocotyls; however, the cortical MTs were almost normal in cells of MAP18 RNAi Arabidopsis hypocotyls (Figures 10B and 10C). Furthermore, when oryzalin was washed off after the treatments, the cortical MTs were mostly recovered in the cells of wild-type and MAP18 RNAi Arabidopsis hypocotyls. However, most of the cortical MTs remained disrupted in cells of MAP18-overexpressing Arabidopsis hypocotyls (Figure 10D). Therefore, we conclude that MAP18 exerts a destabilizing effect on MTs.
MAP18 Is Involved in the Regulation of Cell-Polarized Expansion by Controlling the Organization of Cortical MTs Several kinds of abnormality in plant growth and cell expansion are often observed in mutants where cortical MTs are affected. First, root growth is often shown to exhibit a left- or right-skewing pattern and a left- or right-twist cell file rotation. For example, the lefty mutants with tubulin mutations cause unstable MTs and result in a left-handed twist in Arabidopsis organs (Thitamadee et al., 2002 ). Mutation of SKU6/SPIRAL1 causes right-handed axial twisting in roots, etiolated hypocotyls, leaf petioles, and strongly right-skewed root growth on inclined agar media (Sedbrook, 2004). Seedlings overexpressing WVD2, which may directly or indirectly interact with MTs, exhibit constitutive right-handed helical growth in both roots and etiolated hypocotyls and left-handed twisting in the petioles of rosette leaves (Yuen et al., 2003). Second, the anisotropic cell growth is often reduced, and the radial expansion of the cell is often enhanced. For instance, mutations of Arabidopsis SPR1 or SPR2 reduce anisotropic growth of endodermal and cortical cells in roots and etiolated hypocotyls (Furutani et al., 2000). Mutation of MOR1/GEM1 also results in radially expanding roots (Whittington et al., 2001; Twell et al., 2002). The radial expansion defect is also observed in katanin mutants (Burk and Ye, 2002; Webb et al., 2002). The Arabidopsis TON2 mutants also show reduced anisotropic growth of hypocotyl cells, along with aberrant orientation of cortical MTs (Camilleri et al., 2002). Third, aberrant pavement cells are often formed. For example, the shape of pavement cells is significantly altered in mutants of the plant Rho-related protein family ROPs, which control both the organization of actin filaments and cortical MTs (Fu et al., 2002, 2005). All these abnormalities in root growth and cell expansion are observed in MAP18-overexpressing lines. When MAP18 is overexpressed, the root skews at a left angle, and the cell files have a left-handed twist. Hypocotyl cells exhibit an overall swelling pattern and disordered cell layers. The lobes of cotyledon pavement cells were dramatically eliminated, causing nearly rectangular or spindle-like cells. Further investigation of the cortical MTs in cells overexpressing MAP18 revealed that the organization of cortical MTs is significantly altered. Cortical MTs in hypocotyl epidermal cells form a parallel array, mostly oblique to the long expansion axis of the cell, instead of perpendicular to the long expansion axis in wild-type hypocotyl epidermal cells. By contrast, in cotyledon pavement cells, the cortical MTs are organized into an array of parallel MTs oriented transversely to the long growth axis, a pattern often present in elongating cells. These observations suggest that MAP18 is involved in determination of cell morphology. The observed nontransverse arrays may be the result of altered growth properties in the transgenic plants. Our data on MAP18 promoter-directed GUS activity showed that MAP18 is expressed mainly in cells under expansion but not in dividing cells. Therefore, MAP18 may function during cell expansion and exert its regulatory effect on the determination of plant growth and cell morphology.
MAP18 Is Involved in Controlling MT Organization by Destabilizing Cortical MTs
Treatments of MT-interacting drugs often cause phenotypes similar to mutants of MT-interacting proteins. Long-term treatment with the MT-stabilizing drug taxol often causes left-skewing of root growth (Furutani et al., 2000
How is such MT destabilization involved in MT organization, and in turn, how does this determine cell shape? In Arabidopsis, cortical MTs exhibit dynamics at both ends: polymerization-biased dynamic instability at one end and slow depolymerization at the other end. As a result, sustained cortical MTs migrate by a hybrid treadmilling mechanism and are organized into different cortical MT arrays (Shaw et al., 2003
Three stages are suggested for the development of Arabidopsis pavement cells (Fu et al., 2002 However, overexpressing MAP18 may result in different cortical MT organization in different cell types. In hypocotyl epidermal cells, where cortical MTs usually take a global transverse orientation in wild-type plants, cortical MTs are mostly oblique to the long expansion axis of the cell when MAP18 is overexpressed. As a consequence, the expansion of cells along the longitudinal growth axis was found to be significantly reduced. Again, such abnormal MT organization may also result from the destabilization of cortical MTs. In conclusion, we have demonstrated that MAP18 has a destabilizing effect on cortical MTs. Therefore, overexpression of MAP18 restrains the stabilization of cortical MTs and results in abnormal cell growth.
Plants Arabidopsis thaliana ecotype Columbia was used for the study. Transgenic Arabidopsis expressing GFP-tagged  -tubulin was crossed with MAP18 overexpression and RNAi lines for the observation of cortical MTs.
Bacterial Expression of MAP18
MT Binding and Polymerization Assays
In vitro immunofluorescence labeling experiments were also performed to investigate the binding of MAP18 to MTs. NHS-rhodamine tubulin was prepared according to Keating and White (1998) For the MT polymerization assay, various concentrations of GST-MAP18 were added to 40 µM tubulin solution in PEM buffer supplemented with 1 mM GTP. The time course of MT polymerization was monitored turbidimetrically by the absorbance at 350 nm, and 10 µM GST was used as a control. To further examine the effect of MAP18 on tubulin polymerization, 15 µM NHS-rhodamine–labeled tubulin was incubated with 10 µM GST-MAP18 at 37°C for 30 min. Glutaraldehyde (1% [v/v]) was added into the system to terminate the reaction before observation with the confocal microscopy, and 10 µM GST was used as a control.
Antibodies and Protein Gel Blots The protein extracts were prepared from root, stem, leaf, and flower tissues of 30-d-old Arabidopsis plants. The protein sample was separated on 10% SDS-PAGE gels and transferred to nitrocellulose membrane. Blots were probed with purified anti-MAP18 antibody at the dilution of 1:500 with TBST (50 mM Tris, 150 mM NaCl, and 0.05% Tween 20, pH 7.5) and the secondary antibody of alkaline phosphatase-conjugated goat anti-rabbit IgG antibody (Sigma-Aldrich) at the dilution of 1:10,000.
Analysis of MAP18 Promoter:GUS Activity GUS staining was performed in a solution containing 1 mM 5-bromo-4-chloro-3-indolyl-ß-D-glucuronide, 10 mM phosphate buffer, pH 7.0, 0.05 mM potassium ferrocyanide, 0.05 mM potassium ferricyanide, 2 mM EDTA, and 0.1% (v/v) Triton X-100. Plants were incubated in staining solution at 37°C for 12 h in dark and then cleared with a solution of ethanol:acetic acid at 3:1 (v/v) several times before observation. Samples were examined on an Olympus microscope equipped with a color CCD camera (Sutter Instrument; LAMBDA 10-2).
MAP18 Overexpression and RNAi Arabidopsis
RNA Gel Blot and RT-PCR Analysis M-MLV reverse transcriptase (Promega) was used for RT-PCR. The following primers were used for detection of MAP18 expression: 5'-CGAAGGTTGTTCCAAGG-3' and 5'-AAGAGTGCGTACCACGTC-3'. EF4A was used as control. EF4A was used as control, using the primers 5'-TTGGCGGCACCCTTAGCTGGATCA-3' and 5'-ATGCCCCAGGACATCGTGATTTCAT-3'.
Microscopy Scanning electron microscopy images of 7-d-old Arabidopsis were obtained with a XL30 ESEM scanning electron microscope (Philips). For the observation of cell morphology, 7-d-old seedlings were fixed with 2% (w/v) paraformaldehyde and 1% glutaraldehyde, followed by 1% (v/v) OsO4. Samples were dehydrated in an ethanol series and embedded in Spurr's embedding medium (SPI-Chem; low viscosity kit). Sections (1.5 µm thick) were stained in 0.1% toluidine blue and observed on an Olympus BX51 microscope equipped with a color CCD camera (Olympus DP70).
Drug Treatments
Upper hypocotyls of 7-d-old seedlings of transgenic Arabidopsis expressing GFP-tagged
Accession Numbers
We thank Patrick J. Hussey (University of Durham, UK) for critical reading and comments to the manuscript. Zhenbiao Yang (University of California, Riverside) and Bo Liu (University of California, Davis) generously provided the seeds of Arabidopsis-expressed GFP-tubulin. This research was supported by the National Key Basic Research Project of China (2006CB100101) and National Natural Science Foundation of China (30421002, 30370707, and 30570925).
1 These authors contributed equally to this work.  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) is: Ming Yuan (mingyuan{at}cau.edu.cn). www.plantcell.org/cgi/doi/10.1105/tpc.106.048579 Received October 30, 2006; Revision received January 31, 2007. accepted February 8, 2007.
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INTRODUCTION
