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Cell Biology: Cytoskeleton Network one dominant mechanism: cutting where they cross each Topology Feeds Back on Its other. 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 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 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 MicrotubuleM 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 activity could be analyzed own properties. In the next paragraph, in this new light. For instance, the I rapidly review these features and References Rho effector RIC1 has recently explore whether they could be 1. Zhang, Q., Fishel, E., Bertroche, T., and Dixit, R. been shown to promote severing associated with crossover recognition. (2013). Microtubule severing at crossover by directly binding to katanin [12]. Like all biological objects, sites by katanin generates ordered cortical microtubule arrays in Arabidopsis. Curr. Biol. This effect could be re-examined to microtubules are never perfectly 23, 2191–2195. investigate, for instance, whether built — they contain defects in their 2. Wightman, R., Chomicki, G., Kumar, M., Carr, P., and Turner, S.R. (2013). SPIRAL2 the presence of crossovers modulates lattice (e.g. 14 subunits instead of determines plant microtubule organization by binding affinity. Phosphorylation 13 at the microtubule perimeter). modulating microtubule severing. Curr. Biol. of katanin has been shown to Interestingly, these errors have been 23, 1902–1907. 3. Paredez, A.R., Somerville, C.R., and decrease its severing activity, shown to act as spatial signals Ehrhardt, D.W. (2006). Visualization of and this regulation has been shown promoting severing both theoretically cellulose synthase demonstrates functional association with microtubules. Science 312, to control spindle length in different [16] and experimentally [17]. In the 1491–1495. species [13,14]. Again, the link light of the two recent publications 4. Baskin, T.I. (2005). Anisotropic expansion of between phosphorylation and the presented above, one could wonder the plant cell wall. Annu. Rev. Cell Dev. Biol. 21, 203–222. presence of crossovers could whether microtubule crossovers 5. Corson, F., Hamant, O., Bohn, S., Traas, J., be analyzed. Finally, crosstalks promote such errors, and whether Boudaoud, A., and Couder, Y. (2009). Turning a plant tissue into a living cell froth through between katanin and the microtubule SPR2 is somewhat sensitive to these isotropic growth. Proc. Natl. Acad. Sci. USA nucleating complex have been errors. In that scenario, the proposed 106, 8453–8458. Dispatch R965

6. Bichet, A., Desnos, T., Turner, S., to microtubule alignment in cortical arrays. Drosophila katanin-60 depolymerizes Grandjean, O., and Hofte, H. (2001). Plant J. 52, 742–751. and severs at microtubule defects. Biophys. J. BOTERO1 is required for normal orientation 12. Lin, D., Cao, L., Zhou, Z., Zhu, L., Ehrhardt, D., 100, 2440–2449. of cortical microtubules and anisotropic Yang, Z., and Fu, Y. (2013). Rho GTPase 18. Sudo, H., and Baas, P.W. (2010). Acetylation cell expansion in Arabidopsis. Plant J. 25, signaling activates microtubule severing to of microtubules influences their sensitivity to 137–148. promote microtubule ordering in Arabidopsis. severing by katanin in neurons and fibroblasts. 7. Roll-Mecak, A., and McNally, F.J. (2010). Curr. Biol. 23, 290–297. J. Neurosci. 30, 7215–7226. Microtubule-severing enzymes. Curr. Opin. 13. Loughlin, R., Wilbur, J.D., McNally, F.J., 19. Portran, D., Zoccoler, M., Gaillard, J., Cell Biol. 22, 96–103. Nedelec, F.J., and Heald, R. (2011). Stoppin-Mellet, V., Neumann, E., Arnal, I., 8. Qiang, L., Yu, W., Liu, M., Solowska, J.M., Katanin contributes to interspecies Martiel, J.L., and Vantard, M. (2013). and Baas, P.W. (2010). Basic fibroblast spindle length scaling in Xenopus. Cell 147, MAP65/Ase1 promote microtubule flexibility. growth factor elicits formation of interstitial 1397–1407. Mol. Biol. Cell 24, 1964–1973. axonal branches via enhanced severing of 14. Whitehead, E., Heald, R., and Wilbur, J.D. 20. Odde, D.J., Ma, L., Briggs, A.H., DeMarco, A., microtubules. Mol. Biol. Cell 21, 334–344. (2013). N-terminal phosphorylation of p60 and Kirschner, M.W. (1999). Microtubule 9. Zhang, D., Grode, K.D., Stewman, S.F., katanin directly regulates microtubule severing. bending and breaking in living fibroblast cells. Diaz-Valencia, J.D., Liebling, E., Rath, U., J. Mol. Biol. 425, 214–221. J. Cell Sci. 112, 3283–3288. Riera, T., Currie, J.D., Buster, D.W., 15. Nakamura, M., Ehrhardt, D.W., and Asenjo, A.B., et al. (2011). Drosophila Hashimoto, T. (2010). Microtubule and katanin is a microtubule depolymerase katanin-dependent dynamics of microtubule Laboratoire de Reproduction et that regulates cortical-microtubule plus-end nucleation complexes in the acentrosomal De´ veloppement des Plantes, INRA, interactions and cell migration. Nat. Cell Biol. Arabidopsis cortical array. Nat. Cell Biol. 12, CNRS, ENS, UCB Lyon 1, France and 13, 361–370. 1064–1070. Laboratoire Joliot Curie, CNRS, ENS Lyon, 10. Srayko, M., O’Toole, E.T., Hyman, A.A., and 16. Davis, L.J., Odde, D.J., Block, S.M., and Universite´ de Lyon, 46 Alle´ e d’Italie, Muller-Reichert, T. (2006). Katanin disrupts Gross, S.P. (2002). The importance of the microtubule lattice and increases polymer lattice defects in katanin-mediated 69364 Lyon Cedex 07, France. number in C. elegans meiosis. Curr. Biol. 16, microtubule severing in vitro. Biophys. J. 82, E-mail: [email protected] 1944–1949. 2916–2927. 11. Wightman, R., and Turner, S.R. (2007). Severing 17. Diaz-Valencia, J.D., Morelli, M.M., Bailey, M., at sites of microtubule crossover contributes Zhang, D., Sharp, D.J., and Ross, J.L. (2011). http://dx.doi.org/10.1016/j.cub.2013.09.051

Development: Lights, Camera, many dead embryos are pieced Drosophila together to get a sense of temporal Action — The Embryo dynamics. With the publication of two studies in this issue of Current Goes Live! Biology, by Garcia et al. [4] and Lucas et al. [5], this static view has given way to real-time dynamics of Live imaging of developmental gene expression in Drosophila embryos opens gene activation in living embryos. up exciting new prospects for understanding gene regulation during With the advent of new technologies development. comes the opportunity for new discoveries, and the dividends Jacques Bothma and Michael Levine* numerous insights into the spatial provided by live imaging are immediate control of gene expression, such as the and exciting. For the past 30 years, the early modular organization of enhancer Both papers investigate one of the Drosophila melanogaster embryo has DNAs, the importance of localized classical paradigms of gene regulation been used as a model to visualize repressors in delineating restricted in development: the activation of the differential gene activity in patterns of gene expression, and the gap gene Hunchback by the gradient development [1]. It is ideally suited for regulation of enhancer–promoter of the Bicoid protein [6,7]. This such studies due to its rapid interactions [1,2]. Recently developed gradient is distributed across the development, ease of collection, and quantitative methods allow exact anterior–posterior axis of the embryo, the simple arrangement of nuclei in the measurements of the numbers of with the highest levels present at the syncitial blastoderm stage. During the mRNAs and proteins encoded by anterior pole. Both high and maternal–zygotic transition, which critical patterning genes such as intermediate levels are sufficient to marks the onset of transcription from Bicoid, and highlight the remarkable activate Hunchback expression in the the embryo’s genome, there are two precision in the regulation of gene anterior half of the embryo, synchronous mitotic divisions, expression during the corresponding to the future head and followed by an extended maternal–zygotic transition, when anterior thorax of the embryo. Low period when the embryo is composed broad maternal gradients give way to levels of Bicoid appear to be of w6,000 nuclei arranged as a sharp on/off patterns of gene insufficient to activate Hunchback monolayer at the cortex of the syncitial expression [3]. Despite the extensive expression in the posterior thorax and blastoderm. These nuclei display fast information on the spatial control of abdomen. The formation of the sharp and furious expression of key gene expression, we know little about Hunchback border within the patterning genes during a period of less temporal dynamics. Time is a more presumptive thorax has been the than one hour, resulting in localized abstract concept than space and much subject of extensive experimental and stripes and bands of gene expression trickier to control experimentally. Most theoretical studies [8]. that establish the basic blueprint of the of our insights into gene regulation Both studies [4,5] examined the adult fly. The visualization of gene stem from the use of fixed dynamic activation of gene expression expression in this system has provided preparations, whereby snapshots of by the proximal Hunchback enhancer