Cell Biology: Cytoskeleton Network One Dominant Mechanism: Cutting Microtubules Where They Cross Each Topology Feeds Back on Its Other

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Microtubule severing had previously been shown to occur Regulation preferentially at microtubule crossovers in a seminal article [11]. The work by Zhang et al. thus narrows Many cell functions rely on microtubule dynamics and ordering. Two recent down the molecular mechanism to studies show that microtubule severing by katanin plays an overbearing role only one predominant factor — katanin. in this process and is primarily regulated at microtubule crossovers. In particular, they show that this enzyme localizes to microtubule Olivier Hamant one of the main controlling factors. crossovers and that in a katanin In fact, one of the katanin alleles mutant, severing at crossovers is By showing how microtubule in Arabidopsis is called botero, completely absent (Figure 1). crossovers are at a central position referencing the artist’s work reflecting Interestingly, a quantitative analysis of in the control of cytoskeleton ordering, the rather obese and thus isotropic the corresponding kinetics highlights and by providing a regulatory geometry of the corresponding mutant that longer-lived crossovers are more mechanism underlying this control, phenotype [6]. prone to severing than early ones, the work by Zhang et al. [1] in this issue Katanin was originally purified in demonstrating that microtubule and Wightman et al. [2] published extracts from sea urchin eggs. Since crossovers act both as a spatial recently in Current Biology illustrates then, this AAA ATPase has been found and temporal regulator of severing [1]. how plant research provides important in all eukaryotes and acts as an This provides a feedback loop in new findings that are relevant to heterodimer, with the 60 kDa katanin which microtubule severing by katanin cell biology in all kingdoms, with subunit displaying the catalytic activity, promotes the organization of the implications in development and and the 80 kDa WD40-repeat microtubule network, which in turn, biomedical research, too. counterpart displaying a regulatory through the amount, position and Understanding the regulation of role [7]. Importantly, while the function age of crossovers, regulates katanin microtubule dynamics is crucial to of katanin was initially associated with activity. many biological processes. This is centrosomal microtubules, there Because of their prevailing role in probably most obvious in plants — in is now evidence that this role is also controlling microtubule organization, this kingdom, growth is driven by relevant to non-centrosomal crossovers in the microtubule network turgor pressure, and the mechanical microtubules. This is not only emerge as a central regulatory point properties of the cell wall constrain illustrated by the work conducted in in plant cell biology. The work by its rate and direction. Because plants — katanin is also involved in the Wightman, et al. [2] illustrates this idea microtubules control the deposition of control of axonal growth [8] and cell by providing a new regulatory module cellulose [3], and thus the mechanical migration [9]. Katanin has also been that relies on microtubule crossovers. anisotropy of cell walls, any defect proposed to increase the number of The authors notably show that the in microtubule behavior is translated short microtubule fragments near presence of highly aligned microtubule into an abnormal macroscopic cell meiotic chromatin to compensate for bundles in the spiral2 mutant is and tissue shape [4]. Most remarkably, their rather inefficient nucleation in this due to the inhibition of severing by when microtubules are depolymerized, context [10]. Therefore, the work that SPR2, a previously identified aerial plant organs become spherical is highlighted here [1,2] consolidates microtubule-associated protein (MAP). and cells resemble soap bubbles [5]. some ideas and provides a number of More strikingly, they found that Mutants with disorganized predictions that may change the way SPR2 accumulates at microtubule microtubules also exhibit isotropic we understand microtubule ordering crossovers, where it prevents severing growth, and among the known in all eukaryotes. locally (Figure 1). Interestingly, this regulators, the microtubule severing Briefly, Zhang et al. [1] show that activity is also modulated in different protein katanin has emerged as katanin activity is triggered through cell types — the increased severing Current Biology Vol 23 No 21 R964 Other regulators surveillance role of katanin could be (e.g. RIC1) extended to a more general mechanism MMicrotubule for the control of microtubule bending ordering. Post-translational modifications have also been shown Kinase to modulate severing activity in ? animal systems. In particular, ? microtubule acetylation promotes severing by katanin [18]. Surprisingly, Microtubule the contribution of post-translational KataninKata crossover modification of microtubules remains poorly studied in plants, and thus its relation to severing or crossover recognition is unknown. Finally, the intrinsic mechanical properties of the cytoskeleton are also regulated. SPR22 For instance, using an elegant in vitro approach, it has been shown Current Biology recently that microtubule bending (i.e. flexural rigidity) depends on the Figure 1. Katanin is recruited and regulated at microtubule crossover to sever microtubules. recruitment of MAP65 in plants [19]. Left panel: microtubule pattern in pavement cells from Arabidopsis cotyledons (image size: Interestingly, microtubule bending has 60 x 60 mm). Right panel: the role of SPR2 in regulating severing activity at crossovers is been proposed to promote breaking, illustrated, together with other putative contributors. too [20]. Crossover recognition may thus also depend on the mechanics of microtubules. activity in petiole cells can be identified in the past [15], and Altogether, microtubules, which are correlated to unstable SPR2 spatial the identification of the biochemical classically seen as dynamic threads localization, while relatively low function of SPR2 may provide some under the regulation of external severing levels in pavement cells novel insights into the regulation of factors, now become the regulators is correlated to stabilized SPR2 nucleation. themselves — they use their chemistry, localization at crossovers [2]. As the The work by Zhang et al. [1] and geometry and mechanics to control amount of protein is roughly similar Wightman et al. [2] provide an the recruitment of MAPs and other in both cell types, this illustrates the unprecedented focus on a central microtubule regulators. The work by role of the spatial dynamics of MAPs regulatory role of the microtubule Zhang et al. [1] and Wightman et al. [2] in controlling the microtubule network network topology but the exact deserve the spotlight because they topology. mechanism behind microtubule provide a simple katanin-based One may predict that many other crossover recognition is still unknown. mechanism in which microtubule MAPs may mediate their action In the spirit of these rather encounter acts as a central regulatory specifically through modulation of parsimonious feedback loops, one process of microtubule ordering. severing by katanin at crossovers. may argue that the intrinsic features This will surely stimulate further The analysis of severing in other of the cytoskeleton are involved. work to better understand the role mutants should be conducted to There is indeed accumulating evidence of the microtubule network topology explore this hypothesis further. suggesting that the microtubule in its own regulation in the future, and in Conversely, the known regulators of network topology emerges from its other systems. katanin

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