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The mechanics behind cell division
Marion Louveaux1,2 and Olivier Hamant1,2
It is now well established that the orientation of the plane of cell compressive tensor in 3 out of 4 cells, the remaining
division highly depends on cell geometry in plants. However, quarter dividing perpendicularly to the compressive force
the related molecular mechanism remains largely unknown. [11]. Note that these experiments were performed with
Recent data in animal systems highlight the role of the different stress levels: experiments on tissues and
cytoskeleton response to mechanical stress in this process. explants [8 10] were performed with higher compression
Interestingly, these results are consistent with some data
force, corresponding to 2 10 times that of turgor pressure,
obtained in parallel in plants. Here we review and confront
while experiments on isolated cells embedded in agarose
these studies, across kingdoms, and we explore the possibility
were carried out with mechanical stress in the range of
that the intrinsic mechanical properties of the cytoskeleton play
turgor pressure [11].
a key role in the nexus between cell division and mechanical
stress. This opens many avenues for future research that are
In animal systems, new micromechanical and modeling
also discussed in this review.
approaches have been used recently to revisit this ques-
tion and have provided more clear-cut results. Alteration
Addresses
1
Laboratoire de Reproduction et Developpement des Plantes, INRA, of shapes of non-adherent single cells, either through
CNRS, ENS, UCB Lyon 1, 46 Allee d Italie, Lyon Cedex 07 69364, France
shear deformation [12] or by placing them in wells with
2
Laboratoire Joliot Curie, CNRS, ENS Lyon, Universite de Lyon, 46 Allee
defined geometries [13 ] can constrain the orientation of
d Italie, Lyon Cedex 07 69364, France
the new cell division plane. A difference of less than 15%
in aspect ratio is sufficient to provoke relocation of the
Corresponding authors: Hamant, Olivier ([e-mail])
nucleus [13 ] or the spindle [12]. In vivo, the extracellular
matrix is thought to transduce mechanical stress from the
Current Opinion in Plant Biology 2013, 16:774 779
environment to the cytoskeleton during interphase. This
This review comes from a themed issue on Cell biology
also occurs during cell division: adherent cells round up
Edited by David W Ehrhardt and Magdalena Bezanilla before mitosis but keep few points of anchorage to the
matrix, through actin-rich retracting fibres. Interestingly,
For a complete overview see the Issue and the Editorial
the transient round shape of mitotic cells has recently
Available online 6th November 2013
been shown to control spindle assembly, and this has
1369-5266/$  see front matter, # 2013 Elsevier Ltd. All rights
been related to microtubule length [14]. Mechanistically,
reserved.
it has been proposed that actin associated proteins that
http://dx.doi.org/10.1016/j.pbi.2013.10.011
accumulate at the end of the retracting fibres, also interact
with astral microtubules. In fact, when fibroblasts are
grown on asymmetric fibronectin patterns, the distri-
Evidence for a role of mechanical stress in bution of these proteins becomes heterogeneous. This
controlling the cell division plane across also alters the distribution of forces at the cell cortex and
kingdoms stabilizes the spindle in a position where all forces are
All living organisms experience mechanical stress, as balanced [15 17]. Mechanical stress can also change the
revealed, for instance by performing local cuts in tissues cell division plane orientation dynamically: when a fibro-
[1,2]. Conversely, the external application of mechanical nectin micropattern is stretched, a rotation of the spindle
deformation on tissues has been shown to affect growth is observed within a few minutes and cell division occurs
and morphogenesis, suggesting an instructing role of perpendicular to the stretch axis [17]. Could these find-
mechanical forces [3 7]. While these results imply that ings apply to plant cells?
cell division is a downstream target of mechanical stress,
this may be largely indirect. A contribution of mechanical stress behind
Errera s rule?
In plants, mechanical perturbations have various and Attempts to predict the position of division planes for
sometimes contradictory effects on the orientation of cell symmetric cell divisions were pioneered by plant biol-
division planes. Bending Helianthus tuberosus explants ogists in the 19th century and they emphasized the role of
randomizes the orientation of division planes [8]. Com- cell geometry in this process [11,20]. Sachs observed that
pressing Coleus internodes or Nicotiana tabacum new cell walls form an angle of 908 with existing walls in
explants induce a preferential orientation of cell division symmetric divisions. Hofmeiser proposed that cells
planes perpendicular to the axis of compression [9,10]. divide perpendicular to the cell s main growth axis. Errera
Compressing protoplasts or single cells from tobacco roots proposed that a new cell wall minimizes its surface area
orient the new cell division plane parallel to the applied and behaves like a soap film [11,20]. While these rules
Current Opinion in Plant Biology 2013, 16:774 779 www.sciencedirect.com
Mechanical stress and cell division Louveaux and Hamant 775
Figure 1
Geometry
sensing
PPB formation Spindle Phragmoplast
CLASP, TON complex TON complex
CLASP, MAP65 POK TPLATE
MAP65, Katanin TAN, RanGAP
Global pattern Center of mass: Segregation:
of stress Balance of forces Pulling forces
Current Opinion in Plant Biology
Integrating mechanical stress in the kinetics of cell division. In addition to the spindle, cell division in plants involves the formation of the preprophase
band (PPB), which predicts the future cell division plane orientation, before cell division and the formation of the phragmoplast, after cell division
(snapshots of an epidermal cell from a shoot apical meristem expressing the GFP-MBD microtubule marker have been taken every 20 min). The
presence of the nucleus at the center of mass of the cell (via a balance of forces that depend on cell geometry) could promote microtubule nucleation,
and arguably PPB formation, at the equator of the cell, while the global pattern of stress would prescribe a direction to the microtubules at interphase,
and thus to the PPB. Several microtubule regulators are involved in these different processes, and the ones potentially involved in the response to
mechanical stress have been highlighted in blue here. The contribution of mechanical stress in cell division plane orientation is multiscale and can be
revealed at supracellular level (e.g. global pattern of stress controlling microtubule and PPB orientation across several cell files), at cell level (e.g. cell
geometry constraining the balance of forces inside the cell and positioning the nucleus at the center of mass) and at molecular level (e.g. pulling forces
controlling chromosome segregation).
provide realistic outcomes in computer simulations of it was proposed that PPB formation relies on remodeling
growing tissues [18] and can even recapitulate the whole of the microtubule network by motor proteins, changes
development of simple organisms like Coleochaete [19], in microtubules dynamics, and/or new events of micro-
cells with similar shape can divide along several possible tubule nucleation from the nuclear envelope or the cell
planes [20 ]. A thorough analysis of cell division planes in cortex [21,22]. The recent functional characterization of
leaves and meristems revealed that the different division the TONNEAU complex, which is absolutely required
planes are associated with several surface area minima for PPB formation, is certainly an essential step to
that are prescribed by cell shape before division, thus further explore this question [23 25,26 ]. Strikingly
generalizing Errera s rule to a probabilistic rule [20 ]. the PPB predicts the position of the next division plane
What is the molecular basis behind these geometrical orientation. As the PPB highly depends on the orien-
relations? tation of cortical microtubules before division, this
suggests that the impact of mechanical stress on cell
Geometry sensing, that is, the selection of the shortest division plane orientation in plants could be a con-
path within the plant cell, has been proposed to depend sequence of the response of microtubules to mechanical
on the behavior of microtubules and cytoplasmic strands signals.
[20 ,21]. Laser ablation experiments [21] show that
cytoplasmic strands, which contain microtubules, are The behavior of the cytoskeleton is affected
under tension; they position the nucleus at the center by mechanical stress
of mass of the cell before division. This is somewhat The cytoskeleton can be viewed as an integrator of the
similar to what is observed in animal cells [13 ]. The different cues that impact cell division. Note that while
strands then coalesce into a plane named the phragmo- the emphasis is often put on microtubules in plant cell
some, and cortical microtubules form a ring at the equator division, actin is also present in the PPB and the phrag-
of the cell, also called the preprophase band (PPB, moplast. The position of the future division plane is
Figure 1). This process remains ill understood although actually marked by transient absence of actin [27 ] and
www.sciencedirect.com Current Opinion in Plant Biology 2013, 16:774 779
776 Cell biology
disruption of the actin network leads to spindle misor- associated with F-actin buckling, demonstrating the
ientation and oblique cell plates [28,29]. There is now existence of a coupling between compression and actin
accumulating evidence that mechanical stress affects the turnover [42]. Finally, the rate of actin polymerization by
behavior of the cytoskeleton both in plants and animals. the formin Bni1p in yeast was shown to be regulated by
the antagonistic actions of physical forces and profilin
In animal cells, the actomyosin cytoskeleton is comple- [43]. Beyond actin buckling, severing and polymerization,
tely reorganized in presence of a directional mechanical the low intrinsic stiffness of actin (1000-fold less rigid
stress, whether it is induced by an hydrodynamic flow than microtubules) has been proposed to be a key factor
[30], adhesion to fibronectin micropatterns [16], or for the dynamic reorganization of the actin network in
morphogenetic movements [31]. Microtubules also cells under myosin-generated compressive forces [44].
respond to mechanical stress; they notably buckle follow-
ing compression with a glass needle applied on plasma Despite the high intrinsic stiffness of microtubules, which
membrane or when compressed by the inner contraction compares to plexiglas [45], microtubules should buckle
of the actomyosin network in cardiac cells [32]. In plant under loads of the order of 1 pN [32], which is of the same
cells, mechanical stress affects the cortical microtubule order of magnitude as the force generated by molecular
network, whether mechanical perturbations are induced motors (ca. 5 pN, as measured in vitro for kinesins and
by stretching or compressing tissues [33 35], centrifu- dyneins [32,46 48]. However, in animal cells microtu-
gation [36], or wounding [35]. More specifically, there is bules were found to bear higher compressive loads, and
evidence that microtubules align along the maximal buckle at smaller wavelength than in vitro, thus revealing
tensile stress direction [33,35]. Note that actin also reori- the role of the cytoskeletal network topology and associ-
ents after wounding in plants [37]. While actin and ated proteins in the modulation of the intrinsic mechan-
microtubules seem to display consistent and dynamic ical properties of microtubules [32]. A very elegant study
interactions in plant cells [38], their final organization recently confirmed this prediction: when grown in vitro
in the presence of mechanical stress may rely on different under an hydrodynamical flow, microtubules bend; add-
responses to mechanical forces: local deformation with a ing the bundling protein MAP65/Ase1 to the mix
microindenter actually showed that microtubules depo- increases bending by reducing the flexural stiffness of
lymerize under compression, while actin bundles in microtubules [49 ]. Tension was also shown to promote
similar conditions [39]. In fact, microtubules may have microtubule polymerization [67].
opposite responses to compression and tension: micro-
tubules have the appearance of being more bundled in Altogether, this suggests a novel biological role for cytos-
cells under greater tension [35]. The mechanical asym- keleton regulators: the modulation of the response of the
metry of microtubules could partly explain why micro- cytoskeletal network to mechanical stress. In the follow-
tubules orient along maximal tensile stress in plant tissues ing, we select a number of candidates, which have an
[40]. established regulatory role for the cytoskeleton, and may
also have a role in regulating the response to mechanical
While these data support a role for the cytoskeleton in stress, and thus cell division.
translating a pattern of mechanical stress into a pattern of
subcellular organization that could be used to set up Integrating the cytoskeleton regulators in the
division plane orientation, it still remains unclear how response to mechanical stress
exactly mechanical stress is transduced to the cytoskele- In the wild type, the application of mechanical pertur-
ton, to modify its behavior. Here we propose to explore bations on Arabidopsis shoot apical meristems promotes
the possibility that the cytoskeleton itself acts as a apparent microtubule bundling, and the cells with the
mechanosensor. In this framework, the intrinsic geometry most unstable microtubule orientations are the most
and mechanics of the cytoskeleton should play a key role. competent to reorient their microtubules along maximal
A few pioneering studies have opened the way. stress orientation in this tissue [35]. This suggests that
high microtubule dynamics is promoting the microtubule
How the mechanics of the cytoskeleton may response to stress. Interestingly, mutants impaired in the
guide the response to mechanical stress microtubule severing protein Katanin exhibit reduced
In an elegant in vitro approach, actin was found to branch microtubule dynamics leading to isotropic microtubule
preferentially on the convex side of curved actin and organizations and arguably reduced bundling [50]. Con-
relevant computer models demonstrated that such a bias versely, when katanin is overexpressed, microtubules
would reinforce the actin network against compressive exhibit a transient hyperbundling attributed to increased
forces [41 ]. Furthermore, on the basis of in vitro recon- rate of collisions and increased microtubule dynamics
stituted actin cortex on a lipid bilayer, the contraction of [51]. When mechanical perturbations were performed on
the actomyosin network was shown to depend almost katanin mutant meristems, the microtubule response to
entirely on F-actin buckling induced by myosin-gener- stress was reduced suggesting that microtubule severing
ated stresses. Interestingly, increased severing was also provides a competence to the microtubules to respond to
Current Opinion in Plant Biology 2013, 16:774 779 www.sciencedirect.com
Mechanical stress and cell division Louveaux and Hamant 777
mechanical stress. Intriguingly, the katanin mutant also include cell cycle regulators, as compression was shown to
exhibits altered cell division plane orientations in the decrease cell division rate in animal cells [62,63].
shoot meristem, which may be consistent with a relation
between stress, microtubule dynamics and cell division To conclude, as we gain better understanding of the
planes [52 ]. mechanics of the cytoskeleton, we can begin to investi-
gate the role of mechanical stress in cell division with
Because of its essential role in the formation of the more compelling findings. Beyond the mechanistic
preprophase band, the TONNEAU complex, which insight, this research may have far reaching implications
bears similarity to centrosomal proteins, is a likely candi- on development. For instance, because dividing cells
date in the nexus between physical forces and cell transiently modify their mechanical properties, cell
division plane orientation [23,26 ]. Interestingly, the division itself may generate mechanical stress and this
function of TONNEAU seems conserved in the green may contribute to the coordination of cell divisions be-
lineage [25]. Furthermore, the different partners (TON1- tween neighboring cells [64]. In the Drosophila imaginal
TRM-PP2A) of the complex have now been identified disk, a higher rate of division was associated with
and found to exhibit synergistic functions [24,26 ]. The increased compression of the tissue, and compression
analysis of the corresponding mutants in the presence of in turn inhibited proliferation, placing division rate and
mechanical stress may help us understand whether these compression in a feedback loop [65]. The choice of the
proteins play a role in integrating mechanical forces as division plane orientation may also have a regulatory role
part of their biological function. in development with recent modeling work proposing
that division plane orientation may impact local growth
Other potential candidates, whose role in cell division is heterogeneity [66 ]. Many other exciting questions are
well established include AURORA kinase [53], POK emerging in this rejuvenated field and we hope that this
kinesins [54] and EB1 [55]. Last, cell geometry sensing review will contribute to further stimulating discussions.
may involve microtubule regulators, like AIR9, which
marks the preprophase band position before the for- Acknowledgement
This work was supported by a PhD grant from ARC3 Environnement,
mation of the phragmoplast [56] and CLASP which pre-
Région Rhône-Alpes.
ferentially localizes to cell edges in the PPB and was
proposed to promote microtubule bending in cell corners,
References and recommended reading
thus potentially enabling or acting as part of a cell
Papers of particular interest, published within the period of review,
geometry sensor [57 ]. have been highlighted as:
of special interest
A more general role of mechanical stress in
of outstanding interest
cell division?
As suggested by studies in animal systems, mechanical stress
1. Landsberg KP, Farhadifar R, Ranft J, Umetsu D, Widmann TJ,
has other impacts on cell division, beyond plane orientation.
Bittig T, Said A, Jülicher F, Dahmann C: Increased cell bond
In particular, chromosome segregation heavily relies on
tension governs cell sorting at the Drosophila anteroposterior
forces within the spindle. The forces required to move compartment boundary. Curr Biol 2009, 19:1950-1955.
one chromosome were measured directly in vitro [58] and
2. Dumais J, Steele CR: New evidence for the role of mechanical
forces in the shoot apical meristem. J Plant Growth Regul 2000,
indirectly estimated in vivo [59] and ranged between 10 and
19:7-18.
65 pN. Consistently, the kinetochore is able to resist 10 pN
3. Farge E: Mechanical induction of twist in the drosophila
[60 ], an intensity which is up to 6 times above the force a
foregut/stomodeal primordium. Curr Biol 2003, 13:1365-1377.
kinetochore can bear when dragged by a microtubule.
4. Engler AJ, Sen S, Sweeney HL, Discher DE: Matrix elasticity
directs stem cell lineage specification. Cell 2006, 126:677-689.
This also implies that external forces may interfere with
5. Hernandez LF, Green PB: Transductions for the expression of
chromosome segregation. Application of compressive
structural pattern: analysis in sunflower. Plant Cell Online 1993,
impulses of 10 nN on HeLa cells actually modulate 5:1725-1738.
mitosis progression [61 ]: when compression is applied
6. Green PB: Expression of pattern in plants: combining
molecular and calculus-based biophysical paradigms. Am J
parallel to the spindle, spindle length is reduced and
Bot 1999, 86:1059-1076.
spindle width is increased, tension within the spindle
7. Fleming AJ, McQueen-Mason S, Mandel T, Kuhlemeier C:
is thus decreased and the transition between metaphase
Induction of leaf primordia by the cell wall protein expansion.
and anaphase is delayed. On the contrary, when com-
Science 1997, 276:1415-1418.
pression is perpendicular to the spindle, tension is
8. Yeoman MM, Brown R: Effects of mechanical stress on the
increased and anaphase is accelerated [61 ]. The exact plane of cell division in developing callus cultures. Ann Bot
1971, 35:1102-1112.
mechanotransduction mechanism remains to be investi-
gated but, because the spindle is conserved across Eukar- 9. Lintilhac PM, Vesecky TB: Mechanical stress and cell wall
orientation in plants. II. The application of controlled
yotes, these findings are likely to apply to plant cells too.
directional stress to growing plants; with a discussion on the
Last, the targets of mechanical stress in plants may also nature of the wound reaction. Am J Bot 1981, 68:1222-1230.
www.sciencedirect.com Current Opinion in Plant Biology 2013, 16:774 779
778 Cell biology
10. Lintilhac PM, Vesecky TB: Stress-induced alignment of division A detailed review of the molecular actors involved in the orientation of
plane in plant tissues grown in vitro. Nature 1984, 307:363-364. division plane.
11. Lynch TM, Lintilhac PM: Mechanical signals in plant 28. Lloyd CW, Traas JA: The role of F-actin in determining the
development: a new method for single cell studies. Dev Biol division plane of carrot suspension cells. Drug studies.
1997, 181:246-256. Development 1988, 102:211-221.
12. Fernandez P, Maier M, Lindauer M, Kuffer C, Storchova Z, 29. Kojo KH, Higaki T, Kutsuna N, Yoshida Y, Yasuhara H,
Hasezawa S: Roles of cortical actin microfilament patterning in
Bausch AR: Mitotic spindle orients perpendicular to the forces
imposed by dynamic shear. PloS One 2011, 6:e28965. division plane orientation in plants. Plant Cell Physiol 2013
http://dx.doi.org/10.1093/pcp/pct093.
13. Minc N, Burgess D, Chang F: Influence of cell geometry on
30. Dalous J, Burghardt E, Müller-Taubenberger A, Bruckert F,
division-plane positioning. Cell 2011, 144:414-426.
Gerisch G, Bretschneider T: Reversal of cell polarity and actin
By constraining sea urchin eggs in wells of various shapes before division,
myosin cytoskeleton reorganization under mechanical and
the authors demonstrate a direct influence of cell shape on nucleus
chemical stimulation. Biophys J 2008, 94:1063-1074.
position and spindle orientation.
14. Lancaster OM, Le Berre M, Dimitracopoulos A, Bonazzi D, Zlotek- 31. Lecuit T, Lenne P-F: Cell surface mechanics and the control of
cell shape, tissue patterns and morphogenesis. Nat Rev Mol
Zlotkiewicz E, Picone R, Duke T, Piel M, Baum B: Mitotic rounding
Cell Biol 2007, 8:633-644.
alters cell geometry to ensure efficient bipolar spindle
formation. Dev Cell 2013, 25:270-283.
32. Brangwynne CP, MacKintosh FC, Kumar S, Geisse NA, Talbot J,
Mahadevan L, Parker KK, Ingber DE, Weitz DA: Microtubules can
15. Théry M, Bornens M: Cell shape and cell division. Curr Opin Cell
bear enhanced compressive loads in living cells because of
Biol 2006, 18:648-657.
lateral reinforcement. J Cell Biol 2006, 173:733-741.
16. Théry M, Jiménez-Dalmaroni A, Racine V, Bornens M, Jülicher F:
33. Hejnowicz Z, Rusin A, Rusin T: Tensile tissue stress affects the
Experimental and theoretical study of mitotic spindle
orientation of cortical microtubules in the epidermis of
orientation. Nature 2007, 447:493-496.
sunflower hypocotyl. J Plant Growth Regul 2000, 19:31-44.
17. Fink J, Carpi N, Betz T, Bétard A, Chebah M, Azioune A,
34. Fischer DD, Cyr RJ: Mechanical forces in plant growth and
Bornens M, Sykes C, Fetler L, Cuvelier D et al.: External forces
development. Gravitational Space Biol Bull 2000, 13:67-73.
control mitotic spindle positioning. Nat Cell Biol 2011, 13:771-
778.
35. Hamant O, Heisler MG, Jönsson H, Krupinski P, Uyttewaal M,
Bokov P, Corson F, Sahlin P, Boudaoud A, Meyerowitz EM et al.:
18. Sahlin P, Söderberg B, Jönsson H: Regulated transport as a
Developmental patterning by mechanical signals in
mechanism for pattern generation: capabilities for phyllotaxis
Arabidopsis. Science 2008, 322:1650-1655.
and beyond. J Theor Biol 2009, 258:60-70.
36. Wymer CL, Wymer SA, Cosgrove DJ, Cyr RJ: Plant cell growth
19. Dupuy L, Mackenzie J, Haseloff J: Coordination of plant cell
responds to external forces and the response requires intact
division and expansion in a simple morphogenetic system.
microtubules. Plant Physiol 1996, 110:425-430.
Proc Natl Acad Sci USA 2010, 107:2711-2716.
37. Goodbody KC, Lloyd CW: Actin filaments line up across
20. Besson S, Dumais J: Universal rule for the symmetric division of
Tradescantia epidermal cells, anticipating wound-induced
plant cells. PNAS 2011, 108:6294-6299.
division planes. Protoplasma 1990, 157:92-101.
Errera s rule states that cell divide along the shortest path. The authors
propose a generalization of this rule, accounting for the fact that cells of
38. Sampathkumar A, Lindeboom JJ, Debolt S, Gutierrez R,
identical shapes can divide along more than one plane.
Ehrhardt DW, Ketelaar T, Persson S: Live cell imaging reveals
structural associations between the actin and microtubule
21. Flanders DJ, Rawlins DJ, Shaw PJ, Lloyd CW: Nucleus-
cytoskeleton in Arabidopsis. Plant Cell 2011, 23:2302-2313.
associated microtubules help determine the division plane of
plant epidermal cells: avoidance of four-way junctions and the
39. Hardham AR, Takemoto D, White RG: Rapid and dynamic
role of cell geometry. J Cell Biol 1990, 110:1111-1122.
subcellular reorganization following mechanical stimulation
of Arabidopsis epidermal cells mimics responses to fungal
22. Vos JW, Dogterom M, Emons AMC: Microtubules become more
and oomycete attack. BMC Plant Biol 2008, 8:63.
dynamic but not shorter during preprophase band formation: a
possible   search-and-capture  mechanism for microtubule
40. Landrein B, Lathe R, Bringmann M, Vouillot C, Ivakov A,
translocation. Cell Motil Cytoskeleton 2004, 57:246-258.
Boudaoud A, Persson S, Hamant O: Impaired cellulose synthase
guidance leads to stem torsion and twists phyllotactic
23. Traas J, Bellini C, Nacry P, Kronenberger J, Bouchez D,
patterns in Arabidopsis. Curr Biol 2013, 23:895-900.
Caboche M: Normal differentiation patterns in plants lacking
microtubular preprophase bands. Nature 1995, 375:676-677.
41. Risca VI, Wang EB, Chaudhuri O, Chia JJ, Geissler PL,
Fletcher DA: Actin filament curvature biases branching
24. Drevensek S, Goussot M, Duroc Y, Christodoulidou A, Steyaert S,
direction. Proc Natl Acad Sci USA 2012, 109:2913-2918.
Schaefer E, Duvernois E, Grandjean O, Vantard M, Bouchez D et al.:
On the basis of an in vitro and modelling approach, the authors propose
The Arabidopsis TRM1 TON1 interaction reveals a recruitment
that actin geometry may serve as a mechanosensor.
network common to plant cortical microtubule arrays and
eukaryotic centrosomes. Plant Cell 2012, 24:178-191.
42. Murrell MP, Gardel ML: F-actin buckling coordinates
contractility and severing in a biomimetic actomyosin cortex.
25. Spinner L, Pastuglia M, Belcram K, Pegoraro M, Goussot M,
Proc Natl Acad Sci USA 2012, 109:20820-20825.
Bouchez D, Schaefer DG: The function of TONNEAU1 in moss
reveals ancient mechanisms of division plane specification
43. Courtemanche N, Lee JY, Pollard TD, Greene EC: Tension
and cell elongation in land plants. Development 2010, 137:2733-
modulates actin filament polymerization mediated by formin
2742.
and profilin. Proc Natl Acad Sci USA 2013, 110:9752-9757.
26. Spinner L, Gadeyne A, Belcram K, Goussot M, Moison M, Duroc Y,
44. Silva EMS, Depken M, Stuhrmann B, Korsten M, MacKintosh FC,
Eeckhout D, De Winne N, Schaefer E, Van De Slijke E et al.: A
Koenderink GH: Active multistage coarsening of actin
protein phosphatase 2A complex spatially controls plant cell
networks driven by myosin motors. Proc Natl Acad Sci USA
division. Nat Commun 2013, 4:1863.
2011, 108:9408-9413.
This article describes the physical interactions and functional synergy
among the different members of the TON complex, which is absolutely 45. Gittes F, Mickey B, Nettleton J, Howard J: Flexural rigidity of
required for PPB formation. Interestingly, these members share homol- microtubules and actin filaments measured from thermal
ogy with centrosomal proteins. fluctuations in shape. J Cell Biol 1993, 120:923-934.
27. Rasmussen CG, Wright AJ, Müller S: The role of the cytoskeleton 46. Gennerich A, Carter AP, Reck-Peterson SL, Vale RD: Force-
and associated proteins in determination of the plant cell induced bidirectional stepping of cytoplasmic dynein. Cell
division plane. Plant J 2013, 75:258-269. 2007, 131:952-965.
Current Opinion in Plant Biology 2013, 16:774 779 www.sciencedirect.com
Mechanical stress and cell division Louveaux and Hamant 779
47. Toba S, Watanabe TM, Yamaguchi-Okimoto L, Toyoshima YY, cortical microtubule organization in Arabidopsis. Nat Commun
Higuchi H: Overlapping hand-over-hand mechanism of single 2011, 2:430.
molecular motility of cytoplasmic dynein. Proc Natl Acad Sci In this article, the authors propose a CLASP-based mechanism for cell
USA 2006, 103:5741-5745. geometry sensing.
48. Visscher K, Schnitzer MJ, Block SM: Single kinesin molecules
58. Grishchuk EL, Molodtsov MI, Ataullakhanov FI, McIntosh JR:
studied with a molecular force clamp. Nature 1999, 400:181-184.
Force production by disassembling microtubules. Nature 2005,
438:384-388.
49. Portran D, Zoccoler M, Gaillard J, Stoppin-Mellet V, Neumann E,
Arnal I, Martiel JL, Vantard M: MAP65/Ase1 promote
59. Nicklas RB: The forces that move chromosomes in mitosis.
microtubule flexibility. Mol Biol Cell 2013, 24:1964-1973.
Annu Rev Biophys Biophys Chem 1988, 17:431-449.
Using an elegant in vitro approach, the authors show how MAP65
modulates microtubules flexibility. 60. Rago F, Cheeseman IM: The functions and consequences of
force at kinetochores. J Cell Biol 2013, 200:557-565.
50. Burk DH, Zheng-Hua Y: Alteration of oriented deposition of
A detailed review of the forces involved in chromosome segregation.
cellulose microfibrils by mutation of a katanin-like
microtubule-severing protein. Plant Cell 2002, 14:2145-2160.
61. Itabashi T, Terada Y, Kuwana K, Kan T, Shimoyama I, Ishiwata S:
Mechanical impulses can control metaphase progression in a
51. Stoppin-Mellet V, Gaillard J, Vantard M: Katanin s severing
mammalian cell. PNAS 2012, 109:7320-7325.
activity favors bundling of cortical microtubules in plants.
By applying mechanical impulses on HeLa cells, inducing either com-
Plant J 2006, 46:1009-1017.
pression or extension of the spindle, the authors show a direct effect of
mechanical stress on mitosis progression.
52. Uyttewaal M, Burian A, Alim K, Landrein B, Borowska-Wykret D,
Dedieu A, Peaucelle A, Ludynia M, Traas J, Boudaoud A et al.:
62. Cheng G, Tse J, Jain RK, Munn LL: Micro-environmental
Mechanical stress acts via katanin to amplify differences in
mechanical stress controls tumor spheroid size and
growth rate between adjacent cells in Arabidopsis. Cell 2012,
morphology by suppressing proliferation and inducing
149:439-451.
Apoptosis in cancer cells. PLoS ONE 2009:4.
This article shows how katanin can modulate the microtubule response to
mechanical stress, with implications for growth heterogeneity, and poten-
63. Montel F, Delarue M, Elgeti J, Malaquin L, Basan M, Risler T,
tially cell division.
Cabane B, Vignjevic D, Prost J, Cappello G et al.: Stress clamp
experiments on multicellular tumor spheroids. Phys Rev Lett
53. Van Damme D, De Rybel B, Gudesblat G, Demidov D,
2011:107.
Grunewald W, De Smet I, Houben A, Beeckman T, Russinova E:
Arabidopsis aurora kinases function in formative cell division
64. Gibson WT, Veldhuis JH, Rubinstein B, Cartwright HN, Perrimon N,
plane orientation. Plant Cell 2011, 23:4013-4024.
Brodland GW, Nagpal R, Gibson MC: Control of the mitotic
cleavage plane by local epithelial topology. Cell 2011, 144:
54. Müller S, Han S, Smith LG: Two kinesins are involved in the
427-438.
spatial control of cytokinesis in Arabidopsis thaliana. Curr Biol
2006, 16:888-894.
65. Shraiman BI: Mechanical feedback as a possible regulator of
tissue growth. Proc Natl Acad Sci USA 2005, 102:
55. Chan J, Calder G, Fox S, Lloyd C: Localization of the
3318-3323.
microtubule end binding protein EB1 reveals alternative
pathways of spindle development in Arabidopsis suspension
66. Alim K, Hamant O, Boudaoud A: Regulatory role of cell division
cells. Plant Cell 2005, 17:1737-1748.
rules on tissue growth heterogeneity. Front Plant Sci 2012:3.
Modelling the impact of the cell division plane orientation on growth
56. Buschmann H, Chan J, Sanchez-Pulido L, Andrade-Navarro MA,
reveals a potential regulatory role of cell division on growth heterogeneity.
Doonan JH, Lloyd CW: Microtubule-associated AIR9
recognizes the cortical division site at preprophase and cell-
67. Trushko A, Schaffer E, Howard J: The growth speed of
plate insertion. Curr Biol 2006, 16:1938-1943.
microtubules with XMP215-coated beads coupled to their
57. Ambrose C, Allard JF, Cytrynbaum EN, Wasteneys GO: A CLASP- ends is increased by tensile force. PNAS 2013, 110:14670-
modulated cell edge barrier mechanism drives cell-wide 14675.
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