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Vol. 19, Issue 11, 4730-4737, November 2008
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The University of British Columbia, Vancouver, BC V6T 1Z4, Canada
Submitted July 1, 2008;
Revised August 4, 2008;
Accepted August 7, 2008
Monitoring Editor: David G. Drubin
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). In contrast, in the acentrosomal cells of higher plants, the majority of interphase MTs are nucleated in a dispersed manner throughout the cell cortex and typically remain cortically anchored along their lengths for the duration of their lifespan (Hardham and Gunning, 1978; Wasteneys, 2002; Chan et al., 2003; Shaw et al., 2003; Ehrhardt and Shaw, 2006).
Despite the ubiquitous association of microtubules with the cell cortex in plant cells, little is known of the molecular components responsible for this linkage. Cross-bridges between MTs and the plasma membrane have been detected by transmission electron microscopy, but their identity remains unknown (Hardham and Gunning, 1978). The biochemical identification of a 90-kDa phospholipase D (PLD) from MT fractions led to a proposed role for PLD in membrane anchoring (Gardiner et al., 2001). Consistent with this, treatment with the PLD drug n-butanol has been shown to disorganize cortical MTs (Gardiner et al., 2003) or to detach them from the cell cortex (Dhonukshe et al., 2003) when MTs are labeled by overexpression of the green fluorescent protein (GFP)-MBD MT reporter protein. Other studies, however, show a MT-destabilizing effect of n-butanol at higher concentrations (Hirase et al., 2006). More recently n-butanol has been demonstrated to enhance the developmental reorientation of MTs from transverse to longitudinal in leek cells (Sainsbury et al., 2008). The drug morlin has also been shown to induce detachment of cortical MTs from the membrane in combination with the overexpression of the GFP-MBD reporter protein, although the putative target(s) of this drug are unknown (DeBolt et al., 2007).
We report here that the Arabidopsis CLASP protein is involved in mediating MT-cortex attachment. CLASP/Orbit/MAST proteins are important players in stabilizing subsets of MT plus ends in specific regions of the cell cortex (Akhmanova et al., 2001; Lansbergen et al., 2006). In response to cellular and morphogenetic cues, CLASPs localize preferentially to MT plus ends in the leading edge of migrating cells, where they form a complex with the cortex-associated proteins LL5β and ELKs, which, by forming a link between MT plus ends and the cortex, facilitates normal cytoskeletal polarization and cell migration (Drabek et al., 2006; Lansbergen et al., 2006). In migrating PtK1 epithelial cells, CLASP localization on MTs is also differentially regulated, exhibiting plus-end tracking in the cell body and MT sidewall association upon entry into the leading edge lamella (Wittmann and Waterman-Storer, 2005). In both cell types, the differential localization of CLASP is mediated by an important regulator of cell polarity, GSK3β, which reduces MT lattice-binding affinity in the cell body (Akhmanova et al., 2001; Wittmann and Waterman-Storer, 2005).
The recently discovered CLASP homologue in higher plants has been shown to localize in several differentiated cell types along the full length of cortical MTs, with only a weak enrichment at MT plus ends (Ambrose et al., 2007; Kirik et al., 2007). This distribution is reminiscent of the MT sidewall distribution of GFP-CLASP seen in the leading edge lamellae of migrating PtK1 epithelial cells (Wittmann and Waterman-Storer, 2005), suggesting it is a functionally conserved regulatory mode of CLASP. Interestingly, the MT sidewall decoration of CLASP upon entry of MTs into the lamella appears to be accompanied by a drastic reduction in lateral MT mobility, presumably because of anchoring of the MTs along their length to the plasma membrane. On the basis of these observations, we hypothesized that the constitutive MT sidewall binding of CLASP in plant cells may play a role in the lateral association of MTs with the cell cortex and may represent a universal mechanism of linking MTs to the cortex.
Using live imaging of Arabidopsis epidermal cells we show here that MTs in plants lacking CLASP display frequent and prolonged cortical detachments. Detached MTs exhibit large deformations and changes in orientation in response to the prevailing cytoplasmic stream. This enhanced lateral mobility of MTs in the absence of CLASP increases the frequency of interactions between MTs that result in bundle formation, and correlates with increased parallel ordering of MTs in leaf epidermal cells. These data reveal a new self-organizational mechanism for cortical MT arrays, wherein modulation of MT-cortex anchoring directs the outcome of MT–MT interactions.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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) were obtained as a gift from Dr T. Hashimoto (Nara Institute of Science and Technology, Japan) and crossed to clasp-1 plants (SALK accession no. salk_120061).
Tissue Preparation and Microscopy
Images were acquired on a Zeiss Axiovert (Zeiss, Göttingen, Germany) microscope equipped with an axiocam HRmCCD camera, driven by Axiovision software (Zeiss). Bandpass filters for GFP were 460–480-nm excitation and 505–530-nm emission. Typical light exposure regimens were 1–1.5-s exposures at 30% arc lamp intensity (Zeiss FluoArc), at 5-s intervals. Photobleaching was negligible under these conditions. Individual cells were observed for no more than 5 min, because MT detachment activity was sensitive to photodamage. Confocal imaging was performed with a 40x plan-apochromatic water immersion objective mounted on a Zeiss Pascal, using the 488-nm line from an argon laser. Typical scan times were 4 s, using a line averaging of two. Slice thickness was 1.5 µm. For latrunculin B treatments, a 20 µM solution in 1% DMSO was prepared from a 2 mM stock in 10% DMSO. Cessation of streaming was typically observed at 5–10 min after application. DMSO, 1%, alone had no obvious effect on detachment activity or MT organization.
Image Analysis and Statistical Analysis
Image analysis was performed using ImageJ software (http://rsb.info.nih.gov/ij/). Figures were assembled in Corel Draw (www.Corel.com; Corel Systems, Ottawa, ON, Canada). Statistical analysis was performed using Microsoft Excel (Microsoft, Redmond, WA).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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; Kirik et al., 2007). In agreement with our previous immunofluorescence data reported for roots (Ambrose et al., 2007), as well as for GFP-tubulin in hypocotyl cells (Kirik et al., 2007), MTs in most clasp-1 cells were well organized into parallel arrays. Analysis of MT orientation in living cells expressing GFP-tubulin (GFP-TUB6) revealed that in cotyledon and leaf epidermal cells, clasp-1 MTs exhibited a greater degree of parallel order than those of wild type (Figure 1). In contrast to the varied MT orientations present within individual wild-type cells, clasp-1 cells typically possessed one predominant MT orientation throughout the cell (Figure 1, A and B). Quantification of MT angles in individual cells showed a narrowing of the angular distribution in clasp-1 compared with wild type (Figure 1B). Consistent with the increased MT parallelism, a higher proportion of MT plus ends were found to be growing along preexisting MT tracks in clasp-1. From time-lapse image series obtained with a high-resolution CCD camera, we determined that clasp-1 mutants have an approximate threefold increase in the ratio of MT plus ends growing along other MT tracks compared with those growing freely (Figure 1C).
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Cortex detachments were occasionally observed in wild-type cells, albeit much less frequently, and involving less extensive stretches of MTs than those observed in clasp-1 cells (Figure 2, C–E). Specifically, MT detachments in clasp-1 were 3.2 times more frequent, were 1.6 times longer in duration, and the detached lengths were twice as long compared with those observed in wild-type cells (Figure 2, C–E; Table 1). The observed cortical detachments in wild type suggest that the clasp-1 phenotype is an exacerbation of a normal behavior.
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Partial Cortical MT Detachment Enables Interactions between MTs and Bundle Formation
Partially detached MTs in clasp-1 often waved in the cytoplasmic stream until encountering another partially detached or a cortex-associated MT, resulting in the two MTs associating laterally to form a bundle (Figure 3, A and B; see also Figure 2A).
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These conspicuous MT interactions in clasp-1 prompted us to quantify MT bundle formation, which we define here as the annealing of two or more MTs into a single linear filament. To avoid erroneous inclusion of instances where MTs coincidentally grew in overlapping trajectories, bundling was only considered to have occurred when alignment was accompanied by a clear change in growth trajectory or position of one or both of the aligning MTs.
Our analysis identified a strong correlation between the frequency of MT detachment and MT bundle formation. Bundle formation events were roughly three times more frequent in clasp-1 than in wild type (Figure 4A), which correlates closely with the 3.2-fold increase in detachment frequency (Figure 2C). Of these bundling events, 85% in clasp-1 were associated with a detachment of one or both of the aligning MTs, compared with 52.5% for wild type (Figure 4B). In the absence of CLASP, detached portions of MTs were also far more likely to reattach to the cortex via MT bundling rather than to reassociate freely with the cortex. In clasp-1, over three quarters of cortex reattachment events resulted in bundling upon reattachment, compared with roughly half in wild type (Figure 4C). Increased bundle formation in clasp-1 is further supported by the observation that freely growing MTs, regardless of their cortical attachment status, spent less time before coaligning with other MTs in clasp-1 compared with wild type (73.1 ± 4.1 s vs. 85.8 ± 4.4 s, p = 0.018, t test).
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First, we drew a correlation between degree of detachment and bundle formation on a cell-to-cell basis. Wild-type cells that showed the highest degree of detachment activity also exhibited the highest frequency of bundling. The proportion of bundle formation events associated with MT detachment rose to as high as 80–90% in cells with the greatest degrees of detachment activity, compared with the above-noted wild-type average of 52.5%. Conversely, this proportion dropped to 10–20% in cells with the lowest detachment activity. Second, we were also able to draw a positive correlation between the degree of MT detachment and coalignment activity on an individual MT basis in wild-type cells. As shown in Figure 4D, longer MT detachment lengths are more likely to bundle with other MTs upon reattachment. Specifically, MTs that detached and bundled with other MTs were detached over a 31% greater MT length compared with those that did not bundle with other MTs upon cortex reassociation (Figure 4D).
Taken together, our data suggest an indirect role for CLASP in modulating MT–MT interactions, whereby maintaining MTs in close association along their entire lengths with the cell cortex reduces their exploratory capacity. When CLASP's function is reduced, larger partial MT detachment lengths allow exploration of larger swaths of cortical cytoplasm, thereby increasing the probability of finding and freely coaligning with other MTs.
CLASP Restricts the Angle of Incidence of MT Coalignment
On the basis of the findings that interactions between MTs may contribute to the self organization of noncentrosomal cortical MTs in plants and animals (Dixit and Cyr, 2004a; Reilein et al., 2005) and the observations here of increased bundle formation in clasp-1, we next sought to determine whether the outcomes of MT–MT interactions are affected in clasp-1 cells. As documented by others (Shaw et al., 2003; Dixit and Cyr, 2004b), we also observed that growing MTs encountering an obstacle MT at small angles (<40°) frequently coalign to form a bundle. To distinguish this coalignment behavior from other types of bundling events, we define coalignment here specifically as the interaction and coalignment of a growing MT plus end with the obstacle MT it encounters. In wild-type cells this was the predominant mechanism of bundle formation, whereas in clasp-1, it was accompanied by the numerous detachment-associated mechanisms of bundle formation described above. Quantifying MT coalignments at first proved difficult in the steady-state arrays of clasp-1 because many MTs were parallel to one another, thereby making collisions between freely growing plus ends and other MTs relatively infrequent. To achieve a situation wherein clasp-1 was comparable with wild type, we rapidly depolymerized MTs with cold (–20°C, 4 min) and then observed their repolymerization upon return to room temperature (24°C). Immediately after cold treatment, MTs in clasp-1 and wild type were completely depolymerized or retained a few short remnants of MT bundles (where bundles resided before chilling; Figure 5A; see Supplemental Movie S9). On return to room temperature, cells exhibited normal, rapid cytoplasmic streaming and MT behavior and returned to full polymer status within <10 min, indicating the treatments were not detrimental to the cells (Figure 5A; see Supplementary Movie S9). At larger encounter angles, clasp-1 MTs were more capable of coaligning than wild-type MTs (Figure 5B). MT coalignments in clasp-1 occurred at up to 105° initial encounter angles, with a significantly higher mean coalignment angle of 35.2° for clasp-1 and 23.8° for wild type (Figure 5B). Notably, large-angle MT coalignment events were also typically accompanied by partial detachment of the coaligning MT, consistent with our observations in non–cold-treated cells that MT detachment facilitates more promiscuous bundling activity.
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; Dixit and Cyr, 2004b). We observed that in both wild type and clasp-1, MT coalignments are often associated with varying degrees of cortical detachment. In both wild type and clasp-1, encounter of a growing plus end with an obstacle MT is frequently followed by a brief dissociation from the cortex of the leading end of the growing MT. Importantly, for shallow angle encounters, this obstacle-associated detachment often results in coalignment, as the detached portion rapidly pivots into alignment with the obstacle MT (Figure 6A). Similarly, upon obstacle-based detachment, the MT may simply reassociate with the cortex and continue growth in the original trajectory or undergo reorientation during detachment and reassociate in a new growth path (Figure 6B). This was more typical of steep angle collisions, which have previously been shown to result in crossover of the obstacle MT (Dixit and Cyr, 2004b; Wightman and Turner, 2007).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). Here we provide compelling molecular-genetic evidence for the role of a microtubule-associated protein in MT-cortex attachment. On the basis of our findings, we present a hypothetical model for CLASP function in the spatial organization of cortical arrays (Figure 7). By modulating CLASP activity, plant cells can achieve varying degrees of MT-cortex lateral attachment. MTs attached along their full lengths grow in linear trajectories and thus can only "find" MTs in their one-dimensional growth path, as indicated by the yellow highlight. When CLASP's activity is reduced or absent, partial MT detachment allows the freed MT portions to explore a larger volume (yellow) of the cortical cytoplasm, thereby increasing the frequency of MT–MT encounters in orientations that can lead to bundling. Moreover, partial detachment allows MTs to anneal with other MTs at any point along the detached segment of the MT lattice (blue outline), whereas full-length anchoring restricts the anneal-able region to only the plus end. Thus partial detachment also greatly increases the "sticky" surface area of the searching MT, increasing the likelihood of encounters that favor bundle formation (i.e., shallow plus-end encounters or lateral encounters). Ultimately, MT searching capacity is defined by the combination of two factors: the search volume, and the MT surface area available for bundle formation. Furthermore, lateral uncoupling from the cell cortex also allows initial MT–MT contact points to propagate as MTs zipper together via polymerization-independent bundling (Figure 7, bottom).
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; DeBolt et al., 2007). The apparent contradiction of increased MT order in clasp-1 cells is reconciled by the fact that cortex detachment is only partial in clasp-1, with MTs remaining bound along one or more regions, leaving the unattached regions free to explore the cortical cytoplasm in a restricted space. In contrast, complete dissociation of a MT from the cortex would result in internalization to the interior cytoplasm, which is sparsely populated with MTs. Furthermore, one cannot rule out possible nonspecific effects of these drugs, because the target(s) of morlin are unknown, and n-butanol likely affects many cellular processes.
Lower concentrations of n-butanol (0.2%) were recently shown to enhance the developmental reorientation of MTs from transverse to longitudinal in leek epidermal cells (Sainsbury et al., 2008). Perhaps this concentration induces a clasp-1-like partial detachment of MTs. Interestingly, this MT reorientation in leek cells was shown to require the actomyosin-driven forces of cytoplasmic streaming, suggesting that detached MT sections may be prone to flow realignment, as in Nitella cells (Foissner and Wasteneys, 1999).
It is evident from the numerous instances of detached MT segments zippering and rapidly snapping into alignment with other MTs that MTs have an affinity for one another, presumably mediated by cross-linking MAPs of the MAP65 class (Chan et al., 1999; Hussey et al., 2002; Van Damme et al., 2004; Wicker-Planquart et al., 2004). Our data do not indicate a direct role for CLASP in MT cross-linking; however, a recent report demonstrates that CLASP plays a role in stabilizing overlapping MTs in fission yeast and that this function requires the MAP65 orthologue Ase1 (Bratman and Chang, 2007). MT bundles formed by overexpression of CLASP likely result from hyper-stabilization of MTs by CLASP, not via direct cross-linking of the MTs by CLASP (Maiato et al., 2003; Ambrose et al., 2007; Kirik et al., 2007). The seemingly paradoxical finding reported herein of increased interactions between MTs in the absence of CLASP further supports this notion. Specifically, the fact that MTs retain their bundling capacity in the absence of CLASP is indicative of independent cross-linking by other factors. In the absence of CLASP protein, enhanced bundling is promoted not via hyper-stabilization, but rather by increasing the search capacity of MTs. We propose that by modulating the degree of MT-cortex anchoring in plant cells it is possible to achieve a wide range of organizational states ranging from net-like for wild type (strong attachment) to parallel in clasp-1 (partial detachment) to complete disorganization of previously organized arrays (complete detachment). In this sense, keeping one part of the MT anchored while the rest probes for other cortical MTs is analogous to the search-and-capture behavior observed during spindle formation, wherein MTs nucleated and tethered to centrosomes dynamically probe the cytoplasm with their growing plus ends to interact with chromosomal kinetochores or MTs from the opposite pole.
Function of CLASP Sidewall Binding versus Plus-End Tracking
CLASP's role in cortex attachment may be conserved across eukaryotic taxa. Centrosome-dependent MT organization is typical in proliferating cells but many differentiated animal cell types have extensive noncentrosomal MTs as well as MTs that associate along their length with the cortex (Keating and Borisy, 1999; Bartolini and Gundersen, 2006). Interactions between MTs are important in the MT arrays found in association with the basal cortex of epithelial cells (Reilein and Nelson, 2005; Reilein et al., 2005). Interestingly, in these cells the plus-end tracker EB1 also associates along the length of MTs, in contrast to its characteristic plus-end binding (Reilein and Nelson, 2005). In this manner, the regulation of MT plus-end versus sidewall binding of MAPs such as EB1 and CLASP represents a way to modulate cortical association of MTs (i.e., end-on attachment vs. lengthwise attachment).
The binding of CLASP to the full length of MTs in plants is informative as to the general role of CLASPs in eukaryotic cell MT-cortex association. The observation that the lattice binding of CLASP is differentially regulated in animal epithelial cells suggests that it may be an important determinant in regulating cortical association of MTs. In a simplistic model, sidewall labeling of CLASP (and other proteins such as EB1) results in lateral cortex association (as in higher plants and possibly in migrating cell leading-edge lamellae), whereas restricting CLASP to the plus ends favors the end-on MT-cortex association found in many animal cell types. Although we and others observed a slight enrichment of CLASP at MT plus ends (Ambrose et al., 2007; Kirik et al., 2007), it remains to be seen whether this localization can be modulated in plants as well, perhaps in different cell types or stages of the cell cycle. One situation where one may predict a stronger plus-end association of CLASP in higher plants is after cell division, when MTs are nucleated on the nuclear envelope and grow radially through the cytoplasm toward the cortex.
In animal cells, CLASPs interact with two membrane bound proteins, LL5β and ELKS (Lansbergen et al., 2006). BLAST searches indicate an absence of clear orthologues for these in the Arabidopsis genome. Identifying additional molecular components involved in plant cortical MT association will be of interest in the future.
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ACKNOWLEDGMENTS |
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Footnotes |
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Address correspondence to: Geoffrey O. Wasteneys (geoffwas{at}interchange.ubc.ca)
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