Available online at www.sciencedirect.com
ScienceDirect
When biochemistry meets mechanics: a systems view
of growth control in plants
Massimiliano Sassi and Jan Traas
The emergence of complex shapes during the development of
plants is under the control of genetically determined molecular
networks. Such regulatory networks, comprising hormones
and transcription factors, regulate the collective behavior of cell
growth within a tissue. Because all the cells within a tissue are
linked together by the cell wall, their collective growth
generates a good amount of mechanical stress. In the last
few years a compelling amount of evidence has shown that
growth-generated mechanical stress can feed back on plant
developmental programs by modifying cell growth. This
involves primarily responses from the microtubules and
interaction with auxin transport and signaling. Here we discuss
the most recent advances in the understanding of mechanical
feedbacks in plant development.
Address
Laboratoire de Reproduction et Développement des Plantes, INRA,
CNRS, ENS, UCBL, 46 Allée d’Italie, 69364 Lyon Cedex 07, France
Corresponding authors: Sassi, Massimiliano
([email protected]) and Traas, Jan ([email protected])
Current Opinion in Plant Biology 2015, 28:137–143
This review comes from a themed issue on Cell biology
Edited by Hiroo Fukuda and Zhenbiao Yang
For a complete overview see the Issue and the Editorial
Available online 14th November 2015
http://dx.doi.org/10.1016/j.pbi.2015.10.005
1369-5266/# 2015 Elsevier Ltd. All rights reserved.
Introduction: mechanical forces and plant
development
Mechanical constraints play a central role in shaping the
plant. Because of their sessile habit, plants are forced to
endure and adapt to different mechanical stresses that can
come, for instance, from herbivore attack or adverse
weather conditions. However, the environment is not
the only source of mechanical constraints for the plants,
since a good amount comes from within [1,2]. Indeed, as
we will see, plant growth itself is capable of generating
strong mechanical stresses as a consequence of the way in
which tissue shapes are organized and plant cell expansion is achieved. The generation of mechanical stresses
due to differential growth rates between adjacent tissues
was first assumed in the 19th century, following the
observation that in excised sunflower stems the inner
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tissues kept on growing while the outer tissues shrank,
indicating that the epidermal layer is normally under
tension [3]. Over the years, this and other evidence led
to the idea that physical forces act as important players in
the regulation of plant morphogenesis [4,5]. Until recently, the issue was difficult to address, in particular because
the appropriate experimental tools were missing. Fortunately, the hypothesis of a biophysical regulation of plant
morphogenesis has gained renewed interest in the last few
years, in particular due to a number of interdisciplinary
studies that have shed new light on how growth-induced
mechanical forces can feed back on specific aspects of
plant development. These studies have also provided
insight in how mechanics interacts with biochemical regulation. As a consequence, a scenario emerges where
morphogenesis results from the constant interplay between biophysical and biochemical cues [6,7]. Here we
discuss the most recent advances in our understanding of
how the intertwined action of mechanical forces and
molecular regulation drives plant development.
Mechanics meets molecular regulation: a
central place for the cell wall
To understand the importance of mechanics in plant
development, a number of fundamental properties of
the plant cell have to be considered first. Plant cell
expansion results from the antagonistic interaction between the turgor pressure inside the cells and the rigid,
but deformable, plant walls by which the cells are surrounded. Turgor pressure, which can reach up to ten
times the value of atmospheric pressure, exerts a strong
mechanical stress on the cell wall, which is in turn
resisting, like a rigid but elastic box surrounding an
inflated balloon. The walls of most growing cells can
be seen as a fibre-reinforced gel composed of rigid cellulose microfibrils embedded and cross-linked into a viscous matrix composed of a dense network of pectins and
hemicelluloses [8]. Turgor pressure puts this gel under
tension, initially causing reversible (elastic) deformation.
Growth occurs when mechanical forces exceed a certain
threshold causing the matrix elements to break and the
wall to expand (plastic deformation). In the living cell this
is accompanied by a constants synthesis and insertion of
new wall material. Growth rates depend on the threshold
above which plastic deformation occurs and the dynamics
with which matrix elements break and are re-inserted
[9]. This so-called remodelling of the wall matrix is
subject to intense, molecular regulation by multiple
enzymes, encoded by large multigene families, which
are under the genetic control of several developmental
Current Opinion in Plant Biology 2015, 28:137–143
138 Cell biology
pathways. Intuitively, one might think that cellulose
synthesis also contributes to growth. Interestingly, however, its role is very different from the matrix polymers, as
the rigid cellulose fibres have mainly an inhibitory role:
the more cellulose fibres per cell wall unit, the slower the
cells will grow. Another important feature of the cellulose
fibres is that they can be deposited in highly ordered
arrays. The more fibres deposited in one direction, the
more the cell will tend to grow in the perpendicular
orientation. Therefore microfibril anisotropy is a major
determinant of growth directions [10]. The orientation of
newly deposited cellulose fibres is under control of the
cytoskeleton, and there is compelling evidence that
microtubules directly guide the cellulose synthesizing
complexes in the plasma membrane [11–13].
While at the cellular level mechanical stress is generated
by turgor pressure, at the tissue level mechanical stress
arises as consequence of the collective cell behavior
during tissue growth [7,14]. Since the walls keep all
the cells within a tissue glued together, the different
expansion rates and/or directions of multiple neighbouring cells or of adjacent cell layers can generate high levels
of mechanical stress which can lead to tissue breakage or
organ growth arrest, if not accommodated by a local
coordination of cell growth [15,16].
In summary, the cell wall appears to play a central role in
the control of growth patterns, integrating both mechanical
and genetic control. In the following sections we will
discuss a number of recent studies that have provided a
first glance on how this might function. Most of them have
focused on the control of growth directions and wall
anisotropy whereas much less is known on the links between mechanical signals and the control of growth rates.
Determining growth directions: microtubules
and mechanical forces channel
morphogenesis
As seen above, microtubules play a relevant role in
growing cells, reinforcing the wall structure in particular
directions by guiding the deposition of cellulose microfibrils. In agreement with this, interphase microtubules,
often occur in ordered arrays at the plasma membrane,
oriented perpendicularly to the axis of cell expansion [10].
Since microtubules are dynamic polymeric structures
[17], one might wonder how the orientation of cortical
microtubule (CMT) arrays itself is regulated during
growth. Previous studies suggested that CMTs were
responding to strain rates, aligning themselves perpendicular to the main growth axis in fast-expanding cells,
and more variable in cells that have ceased the expansion
phase [18,19]. More recently, it has been proposed that
CMT orientation — at least in certain tissues — is determined at least in part by mechanical forces. There is
strong evidence that the outer cell layers of fast growing
tissues, such as the shoot apical meristem (SAM), are load
Current Opinion in Plant Biology 2015, 28:137–143
bearing [20]. In this scenario, the whole tissue can be seen
as a vessel under pressure. According to classical mechanics, the force patterns at the surface of such a vessel
depend on its geometry [21]. Interestingly the CMT
patterns at the surface of shoot apices follow the predicted
maximal stress orientations: circumferential at the periphery of the SAM, random or reorienting frequently at the
center of the shoot apex [21]. Relevantly, at the boundaries between organ and shoot apex, CMTs are oriented
along the direction of maximal stress but parallel to the
direction of maximal strain, further pointing at a stressbased ordering mechanism [22]. Evidence for stress-driven CMT alignment has also been observed at subcellular
scales as in developing cotyledon pavement cells, where
CMT alignment at the indenting regions of the cell
follows the pattern of geometrically driven mechanical
stress [23]. Dynamic responses of CMT reorientation
have also been recorded in response to different externally applied mechanical stresses such as compressions,
cell ablations or pharmacological treatments weakening
the cell wall [21,23,24–26,27,28].
Beyond CMTs and wall anisotropy, mechanical constraints have also been linked to the control of auxin
transport by affecting the subcellular localization of the
PIN-FORMED 1 (PIN1) auxin efflux carrier. PIN1
abundance, trafficking and density at the membrane were
shown to be affected by mechanical stresses [29]. This in
turn affects auxin distribution in shoot apices [29]. Relevantly, CMTs might be somehow associated with the
mechanical control of PIN1. A negative correlation between CMT organization and PIN localization has been
observed in several tissues. In both root and shoot apical
meristem cells, PIN1 localizes at plasma membranes
where CMT density is apparently reduced [24,30]. Moreover, externally applied mechanical stress at the SAM
triggers changes in PIN1 polarity that follows the same
kinetics as observed for CMTs reorientation. These
induced changes in PIN localization do not require
microtubules, however, indicating that a common upstream element might control both CMTs and PIN1
localization on the membranes [24]. This might involve
cellulose-based plasma membrane connections limiting
the lateral diffusion of PIN1 and other plasma membrane
proteins, or a ROP signaling pathway [31–33]. However,
direct relationships between microtubules and PIN recycling have been recently reported in root tips [34],
suggesting that the mechanisms linking the microtubular
cytoskeleton to PIN polarity might be more complex.
This interplay between wall anisotropy and auxin transport might be central to growth regulation. Reorganization of CMT is a mean to reinforce cell walls through
cellulose deposition in order to maintain physical stress at
a certain level and to orient growth directions. On the
other hand, the shifts in PIN1 polarity might sustain the
mechanical feedback by amplifying growth responses via
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When biochemistry meets mechanics Sassi and Traas 139
auxin redistribution (Figure 1). It must be noted that
responses to mechanical stress might occur preferentially
in undifferentiated tissues, which are more sensitive to
physical constraints [27].
Mechanosensing: feeling the stress
How do plant tissues perceive the mechanical stress?
Most of our current knowledge of plant mechano-sensing
and mechano-transduction comes from comparisons with
bacterial or other eukaryotic systems, where there is a
deeper understanding of how physical perturbations are
perceived [35]. Ca2+-fluxes in response to mechanical
signals are a common theme in both plants and animals
Figure 1
Mechanical
stress
Tissue
shape
FER?
ROPs?
KATANIN
Tissue
growth
Microtubule
reorientation
Cell
expansion &
proliferation
Cellulose
deposition
Auxin
signaling
Auxin
distribution
PIN localization
and abundance
at the PM
Current Opinion in Plant Biology
Mechanical feedbacks in plant development. The image illustrates the
possible mechanical feedbacks inferred from recent literature.
Mechanical stresses, arising from tissue growth and shape, modifie
through the action of KATANIN the organization of CMTs in a pathway
that might require FERONIA (FER) and/or ROP signaling. CMT
reorganization strengthens the cell wall by redirecting cellulose
deposition as a mean to reinforce the cell wall and to endure the
stress (orange arrow). CMT reorientation can also play a role in
redistributing auxin by affecting PIN localization at the plasma
membrane, either by involving cellulose-based connections that limit
PIN diffusion on the plasma membrane, or by other cell wallindependent means (purple arrow). The effect of mechanical stress on
PIN localization and abundance at the PM will, in turn, promote cell
growth to generate tissue shapes, further sustaining the mechanical
feedback. Additional shortcuts to the main feedback loop: mechanical
stress can directly alter cell expansion and proliferation regardless of
the pre-existing effects of auxin signaling (blue arrow) as observed in
lateral root development; changes in auxin distribution, affect CMT
organization via ROP6/KTN mediated signaling (red arrow) as
observed in the shoot apex. Notice that the arrows used in the figure
only define the direction of the feedbacks and have no regulatory
meaning.
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[35,36,37]. In plants, mechanically induced Ca2+ fluxes
can be promoted by stretch-activated ion channels that
react to changes in membrane tension and/or cell wall
elasticity by allowing the passage of ion fluxes across the
membranes [35,36]. On the other hand, receptor-like
kinases of the CrRLK1L family, which are deputed to
monitor the integrity of the cell wall, have also been
linked to the activation of Ca2+ fluxes downstream
mechanical stimuli [35,38]. In particular, FERONIA
(FER) a prominent member of the CrLRK1L family,
has been recently shown to be required for the Ca2+dependent transduction of mechanical signals in
Arabidopsis thaliana roots [39].
Ca2+ fluxes further induce other downstream signaling
pathways including reactive oxygen species (ROS) production, mitogen-activated protein (MAP) kinase activation, transcriptional responses and cytoskeleton
remodelling [35,36,37]. In animal systems, mechanically
induced cytoskeleton remodelling also requires the Rho
GTPase-mediated pathway [37,40]. Rho GTPases of
plants (ROPs) might also play a role in mechanical stress
transduction as they act downstream of FER in ROS
production [41]. Relevantly, ROPs are involved in the
regulation of several developmental responses among
which cytoskeleton reorganization and PIN polarity
[33,42,43,44,45]. In particular, there is evidence that
ROP6 is involved in the regulation of CMT organization
through a signaling cascade involving RIC1 and KATANIN1 (KTN1) [42]. KTN1 localizes at microtubule
crossovers where its severing activity promotes CMT
bundling leading to ordered CMT arrays [42,46,47].
Compelling evidence indicates that CMT responses to
mechanical stress require KATANIN1 (KTN1) microtubule-ordering function [23,25]. As a consequence,
knock-out KNT1 mutants, such as botero alleles, are
unable to maintain ordered CMT arrays displaying severe
growth defects and a complete loss of CMT reorientation
[23,25,48]. Relevantly, KTN1 has also been implicated
in CMT responses to environmental and hormonal
stimuli further confirming that it plays a broad role in
microtubule organization [43,44,47]. Therefore, it is
tempting to speculate that the KTN-ROP complex could
represent a hub on which multiple signals impinge to
modulate plant growth via CMT reorientation..
Emerging scenarios for mechano-chemical
feedback loops in shoot and root
development
More and more precise scenarios start to emerge on the
way mechanics and molecular regulations are integrated
during development. Clear examples of mechano-chemical feedbacks have been observed during SAM morphogenesis and in lateral root formation.
At the SAM, auxin maxima generated by transport promote organ formation [49,50]. Recent findings point at a
Current Opinion in Plant Biology 2015, 28:137–143
140 Cell biology
dual role of auxin in doing so. First the hormone locally
changes the mechanical properties of the cell wall by
modifying wall elasticity [20,43,51,52]. This could involve at least in part the de-methyl-esterification of the
pectic matrix [51,52]. In parallel, auxin also affects the
cytoskeleton [43]. When no auxin accumulation
occurs — for example when auxin transport is impaired–a naked stem forms. This shape largely depends
on the highly anisotropic microtubule arrangements,
which correlate with the stress patterns at the naked
shoot apex [21]. Interestingly, auxin accumulation
removes the anisotropic constraint by promoting the
disorganization of ordered CMT arrays at the SAM periphery, that is by uncoupling CMT organization from the
stress patterns [43]. Computational modelling has shown
that cell wall loosening and isotropy could synergistically
act to promote growth rates at the bulging primordium
[43]. The mechanical forces generated by such boostedup growth might, in turn, affect PIN1 polarity and its
abundance on the plasma membrane, thus enhancing
auxin accumulation in organ primordia [29]. In agreement
with this, impairing auxin-mediated cell wall loosening
via biochemical modification of the pectic matrix, results
in disrupted PIN1 polarity and halts SAM organogenesis
[52]. Taken together, evidence strongly suggests the
existence of a feedback loop between growth, the cytoskeleton, auxin transport and mechanical stress that
guarantees robust morphogenesis at the SAM [53].
Mechano-chemical feedbacks have also been observed in
the development of the root system, in particular during
the emergence of lateral roots. Here, mechanical stress
generates because lateral root primordia (LRP) derive
from an inner cell layer, the pericycle, buried deep within
the primary root. In order to emerge LRP have to overcome the mechanical constraint imposed by the overlying
cell layers. This is accompanied by cell rearrangement
and cell wall remodelling in the overlying layers that allow
the growing LRP to break through the root [16,54]. As
soon as the LRP founder cells in the pericycle start
proliferating, the cells in the facing endodermal tissue
undergo severe shrinking, as a result of vacuole fragmentation and plasma membrane fusion, to create a gap that
allows the passage of LRP through the endodermis [16].
Both pericycle proliferation and endodermis rearrangement are regulated by auxin although through different
transcriptional modules [55]. If the rearrangement of the
endodermis is disrupted, auxin-mediated transcriptional
responses in the pericycle are inhibited, and cell proliferation in the LRP is halted [16]. The mechanical feedback from the overlying layers is not limited to the first
stages of LRP initiation but contributes to the shaping of
the LRP throughout its emergence. Developing LRPs
display highly stereotypical shapes due to the mechanical
constraint of the overlying tissues [56]. The shaping of a
LRP involves a stereotypical shift from bilateral to radial
symmetry that is required to pass through the gap in the
Current Opinion in Plant Biology 2015, 28:137–143
endodermis [56]. The origin of this symmetry shift is not
clear. Interestingly, CMT-transduced mechanical signals
could also be involved here. In developing adventitious
roots, CMTs align circumferentially to the surface of the
emerging root [57]. Disruption of CMT alignment or of
cellulose deposition, leads root primordia to transform
into callus-like structures characterized by uncontrolled
cell proliferation and arrested cell differentiation [57].
Furthermore, the disruption of CMT organization also
leads to a complete loss of the stereotypical PIN1 polarity
patterns in LRP [58] resulting in altered auxin accumulation in callus-like primordia [57]. These results suggest
that the cross-talk between CMT organization and auxin
transport could be of major relevance for responses to
mechanical inputs in developing lateral roots [57]. Interestingly, previous studies showed that LRP initiation
can be induced by manual bending of the primary root,
pointing at a central role for mechanical stress in lateral
root morphogenesis [59–61].
Concluding remarks
As discussed above, growth-generated mechanical inputs
have the capacity to feed back on developmental pathways
of plants, providing a sophisticated mechanism to constantly survey the growth status of tissues and to fine tune
morphogenesis. It is relevant to point out that our understanding of the influence of mechanics on plant development has been relying for a large part on theoretical studies
and modelling approaches, due to a lack of technologies
aimed to measure mechanical forces in planta. New quantitative imaging approaches to measure cell growth and
micro-indentation techniques to probe cell wall elasticity
(Atomic and Cellular Force Microscopy) [62–65], represent a major implements in the studies of mechanics
applied to plant development. So far, auxin-regulated
pathways have emerged as the preferential targets of
mechanical feedbacks. It remains to be established
whether mechanics can also interact with other growth
regulators such as gibberellins and brassinosteroids, which
have been previously linked to the cytoskeleton, to the
cell wall and to putative mechano-sensors [66–69].
Understanding, the molecular basis underlying the integration of mechanical inputs into regulatory networks will
be a major leap forward for plant developmental biology.
Acknowledgements
We would like to apologize to all colleagues whose works could not be cited
for space constraint. MS and JT were supported by an ERC advanced grant
(MORPHODYNAMICS).
References and recommended reading
Papers of particular interest, published within the period of review,
have been highlighted as:
of special interest
of outstanding interest
1.
Hamant O: Widespread mechanosensing controls the
structure behind the architecture in plants. Curr Opin Plant Biol
2013, 16:654-660.
www.sciencedirect.com
When biochemistry meets mechanics Sassi and Traas 141
2.
Fisher DD, Cyr RJ: Mechanical forces in plant growth and
development. Gravit Space Biol Bull 2000, 13:67-73.
3.
Kutschera U, Niklas KJ: The epidermal-growth-control theory
of stem elongation: an old and a new perspective. J Plant
Physiol 2007, 164:1395-1409.
4.
Selker JM, Steucek GL, Green PB: Biophysical mechanisms for
morphogenetic progressions at the shoot apex. Dev Biol 1992,
153:29-43.
5.
Boudaoud A: An introduction to the mechanics of
morphogenesis for plant biologists. Trends Plant Sci 2010,
15:353-360.
6.
Newell AC, Shipman PD, Sun Z: Phyllotaxis as an example of the
symbiosis of mechanical forces and biochemical processes in
living tissue. Plant Signal Behav 2008, 3:586-589.
7.
Traas J, Sassi M: Plant development: from biochemistry to
biophysics and back. Curr Biol 2014, 24:R237-R238.
8.
Cosgrove DJ: Re-constructing our models of cellulose
and primary cell wall assembly. Curr Opin Plant Biol 2014,
22:122-131.
9. Ali O, Mirabet V, Godin C, Traas J: Physical models of plant
development. Annu Rev Cell Dev Biol 2014, 30:59-78.
In this review the authors discuss the physical aspects of plant morphogenesis with a particular emphasis on the role of the cell wall.
10. Chan J: Microtubule and cellulose microfibril orientation
during plant cell and organ growth. J Microsc 2012, 247:23-32.
11. Paredez AR, Somerville CR, Ehrhardt DW: Visualization of
cellulose synthase demonstrates functional association with
microtubules. Science 2006, 312:1491-1495.
12. Gutierrez R, Lindeboom JJ, Paredez AR, Emons AMC,
Ehrhardt DW: Arabidopsis cortical microtubules position
cellulose synthase delivery to the plasma membrane and
interact with cellulose synthase trafficking compartments. Nat
Cell Biol 2009, 11:797-806.
13. Crowell EF, Bischoff V, Desprez T, Rolland A, Stierhof Y-D,
Schumacher K, Gonneau M, Höfte H, Vernhettes S: Pausing of
Golgi bodies on microtubules regulates secretion of cellulose
synthase complexes in Arabidopsis. Plant Cell 2009, 21:11411154.
14. Sampathkumar A, Yan A, Krupinski P, Meyerowitz EM: Physical
forces regulate plant development and morphogenesis. Curr
Biol 2014, 24:R475-R483.
15. Maeda S, Gunji S, Hanai K, Hirano T, Kazama Y, Ohbayashi I,
Abe T, Sawa S, Tsukaya H, Ferjani A: The conflict between cell
proliferation and expansion primarily affects stem
organogenesis in Arabidopsis. Plant Cell Physiol 2014, 55:
1994-2007.
This paper shows that growth coordination between different tissues is
crucial for proper development of plants. The authors show how the
mechanical stress that generates from uncoupled cell proliferation and
cell expansion in the stem of det3 clv3 mutants causes the disruption of
epidermal tissues.
16. Vermeer JEM, von Wangenheim D, Barberon M, Lee Y,
Stelzer EHK, Maizel A, Geldner N: A spatial accommodation by
neighboring cells is required for organ initiation in
Arabidopsis. Science 2014, 343:178-183.
This paper describe another clear example of growth coordination
between adjacent tissues. The authors show the existence of an
auxin-mediated accommodation mechanism based on the localized
disruption of the endodermis that allows the emergence of lateral roots.
The mechanical stress caused by an unaccommodating endodermis is
able to halt lateral root emergence by feeding back on primordium
proliferation.
19. Granger CL, Cyr RJ: Spatiotemporal relationships between
growth and microtubule orientation as revealed in living root
cells of Arabidopsis thaliana transformed with greenfluorescent-protein gene construct GFP-MBD. Protoplasma
2001, 216:201-214.
20. Kierzkowski D, Nakayama N, Routier-Kierzkowska A-L, Weber A,
Bayer E, Schorderet M, Reinhardt D, Kuhlemeier C, Smith RS:
Elastic domains regulate growth and organogenesis in the
plant shoot apical meristem. Science 2012, 335:1096-1099.
21. Hamant O, Heisler MG, Jönsson H, Krupinski P, Uyttewaal M,
Bokov P, Corson F, Sahlin P, Boudaoud A, Meyerowitz EM et al.:
Developmental patterning by mechanical signals in
Arabidopsis. Science 2008, 322:1650-1655.
22. Burian A, Ludynia M, Uyttewaal M, Traas J, Boudaoud A,
Hamant O, Kwiatkowska D: A correlative microscopy approach
relates microtubule behaviour, local organ geometry, and cell
growth at the Arabidopsis shoot apical meristem. J Exp Bot
2013, 64:5753-5767.
23. Sampathkumar A, Krupinski P, Wightman R, Milani P, Berquand A,
Boudaoud A, Hamant O, Jönsson H, Meyerowitz EM: Subcellular
and supracellular mechanical stress prescribes cytoskeleton
behavior in Arabidopsis cotyledon pavement cells. Elife 2014,
3:e01967.
This paper shows how geometric features of cotyledon pavement cells
generate mechanical stresses that regulate the organization of cortical
microtubules at a subcellular scale. These subcellular forces can be
overridden by external supracellular forces, suggesting the existence
of a competition between mechanical cues from different scales.
24. Heisler MG, Hamant O, Krupinski P, Uyttewaal M, Ohno C,
Jönsson H, Traas J, Meyerowitz EM: Alignment between PIN1
polarity and microtubule orientation in the shoot apical
meristem reveals a tight coupling between morphogenesis
and auxin transport. PLoS Biol 2010, 8:e1000516.
25. Uyttewaal M, Burian A, Alim K, Landrein B, Borowska-Wykre˛t D,
Dedieu A, Peaucelle A, Ludynia M, Traas J, Boudaoud A et al.:
Mechanical stress acts via katanin to amplify differences in
growth rate between adjacent cells in Arabidopsis. Cell 2012,
149:439-451.
26. Creff A, Brocard L, Ingram G: A mechanically sensitive cell layer
regulates the physical properties of the Arabidopsis seed coat.
Nat Commun 2015, 6:6382.
27. Jacques E, Verbelen J-P, Vissenberg K: Mechanical stress in
Arabidopsis leaves orients microtubules in a ‘‘continuous’’
supracellular pattern. BMC Plant Biol 2013, 13:163.
Similarly to Ref. [23], this paper shows the responses of cortical microtubules to mechanical stress in leaf pavement cells. However, the authors
also show that younger cells display more pronounced responses to
mechanical stress compared to the older ones.
28. Hush JM, Overall RL: Electrical and mechanical fields orient
cortical microtubules in higher plant tissues. Cell Biol Int Rep
1991, 15:551-560.
29. Nakayama N, Smith RS, Mandel T, Robinson S, Kimura S,
Boudaoud A, Kuhlemeier C: Mechanical regulation of auxinmediated growth. Curr Biol 2012, 22:1468-1476.
30. Boutté Y, Crosnier M-T, Carraro N, Traas J, Satiat-Jeunemaitre B:
The plasma membrane recycling pathway and cell polarity in
plants: studies on PIN proteins. J Cell Sci 2006, 119:1255-1265.
31. Feraru E, Feraru MI, Kleine-Vehn J, Martinière A, Mouille G,
Vanneste S, Vernhettes S, Runions J, Friml J: PIN polarity
maintenance by the cell wall in Arabidopsis. Curr Biol 2011,
21:338-343.
17. Hashimoto T: Microtubules in Plants. The Arabidopsis
Book2015, 3:e0179.
An interesting review discussing several aspects of plant microtubule
biology.
32. Martiniere A, Lavagi I, Nageswaran G, Rolfe DJ, Maneta-Peyret L,
Luu D-T, Botchway SW, Webb SED, Mongrand S, Maurel C et al.:
Cell wall constrains lateral diffusion of plant plasmamembrane proteins. Proc Natl Acad Sci U S A 2012, 109:
12805-12810.
18. Sugimoto K, Williamson RE, Wasteneys GO: New techniques
enable comparative analysis of microtubule orientation, wall
texture, and growth rate in intact roots of Arabidopsis. Plant
Physiol 2000, 124:1493-1506.
33. Xu T, Wen M, Nagawa S, Fu Y, Chen J-G, Wu M-J, PerrotRechenmann C, Friml J, Jones AM, Yang Z: Cell surface- and rho
GTPase-based auxin signaling controls cellular interdigitation
in Arabidopsis. Cell 2010, 143:99-110.
www.sciencedirect.com
Current Opinion in Plant Biology 2015, 28:137–143
142 Cell biology
34. Ambrose C, Ruan Y, Gardiner J, Tamblyn LM, Catching A, Kirik V,
Marc J, Overall R, Wasteneys GO: CLASP interacts with sorting
Nexin 1 to link microtubules and auxin transport via PIN2
recycling in Arabidopsis thaliana. Dev Cell 2013, 24:649-659.
This paper shows the link between auxin transport and microtubules in
Arabidopsis roots. The authors demonstrate that the microtubule-associated protein CLASP interacts with the retromer component SNX1,
which is in turn required for the recycling of the PIN2 auxin efflux carrier.
Consistently, clasp-1 mutants display several auxin-related defects.
35. Monshausen GB, Haswell ES: A force of nature: molecular
mechanisms of mechanoperception in plants. J Exp Bot 2013,
64:4663-4680.
Very exhaustive review on plant mechanosensing and mechanotransduction.
47. Lindeboom JJ, Nakamura M, Hibbel A, Shundyak K, Gutierrez R,
Ketelaar T, Emons AMC, Mulder BM, Kirik V, Ehrhardt DW: A
mechanism for reorientation of cortical microtubule arrays
driven by microtubule severing. Science 2013, 342:1245533.
Here the authors address the mechanisms of microtubule reorientation
during blue light induced phototropic responses in the arabidopsis
hypocotyl. In agreement with Ref. [46], the reorientation of microtubule
arrays in phototropic responses requires KTN1 severing at crossovers.
Accordingly, ktn1 mutant displays reduced hypocotyl bending in
response to blue light.
48. Bichet A, Desnos T, Turner S, Grandjean O, Höfte H: BOTERO1
is required for normal orientation of cortical microtubules
and anisotropic cell expansion in Arabidopsis. Plant J 2001,
25:137-148.
36. Kurusu T, Kuchitsu K, Nakano M, Nakayama Y, Iida H: Plant
mechanosensing and Ca2+ transport. Trends Plant Sci 2013,
18:227-233.
49. Sassi M, Vernoux T: Auxin and self-organization at the shoot
apical meristem. J Exp Bot 2013, 64:2579-2592.
37. Benavides Damm T, Egli M: Calcium’s role in
mechanotransduction during muscle development. Cell
Physiol Biochem 2014, 33:249-272.
50. Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA,
Meyerowitz EM: Patterns of auxin transport and gene
expression during primordium development revealed by live
imaging of the Arabidopsis inflorescence meristem. Curr Biol
2005, 15:1899-1911.
38. Cheung AY, Wu H-M: THESEUS 1, FERONIA and relatives: a
family of cell wall-sensing receptor kinases? Curr Opin Plant
Biol 2011, 14:632-641.
39. Shih H-W, Miller ND, Dai C, Spalding EP, Monshausen GB: The
receptor-like kinase FERONIA is required for mechanical
signal transduction in Arabidopsis seedlings. Curr Biol 2014,
24:1887-1892.
This paper demonstrate that fer mutants display dramatic alteration of
2+
Ca signaling and growth responses to mechanical stress. On this basis,
the authors propose that the receptor-like kinase FER is a key regulator of
mechanosensing in Arabidopsis.
40. Janmey PA, Wells RG, Assoian RK, McCulloch CA: From tissue
mechanics to transcription factors. Differentiation 2013, 86:112120.
41. Duan Q, Kita D, Li C, Cheung AY, Wu H-M: FERONIA receptorlike kinase regulates RHO GTPase signaling of root hair
development. Proc Natl Acad Sci U S A 2010, 107:17821-17826.
42. Lin D, Cao L, Zhou Z, Zhu L, Ehrhardt D, Yang Z, Fu Y:
Rho GTPase signaling activates microtubule severing to
promote microtubule ordering in Arabidopsis. Curr Biol 2013,
23:290-297.
This article shows that ROP GTPase-dependent signaling regulates
microtubule organization via KTN1. The authors demonstrate that
RIC1, effector of ROP6 GTPase, physically interacts with KTN1 and
promotes its microtubule severing actvity.
43. Sassi M, Ali O, Boudon F, Cloarec G, Abad U, Cellier C, Chen X,
Gilles B, Milani P, Friml J et al.: An auxin-mediated shift toward
growth isotropy promotes organ formation at the shoot
meristem in Arabidopsis. Curr Biol 2014, 24:2335-2342.
This report describes the role of cortical microtubules in organ formation
at the shoot apex. The authors demonstrate that auxin promotes the
disorganization of microtubules at the meristem periphery to promote
organ initiation.
44. Chen X, Grandont L, Li H, Hauschild R, Paque S, Abuzeineh A,
Rakusová H, Benkova E, Perrot-Rechenmann C, Friml J:
Inhibition of cell expansion by rapid ABP1-mediated auxin
effect on microtubules. Nature 2014, 516:90-93.
This paper shows how a rapid, auxin-mediated rearrangement of microtubule organization inhibits cell elongation in roots and hypocotyls. It is
further shown that auxin action on microtubule organization is regulated
by ABP1 through a ROP6-mediated signalling cascade that affects KTN1
severing activity.
45. Chen X, Naramoto S, Robert S, Tejos R, Löfke C, Lin D, Yang Z,
Friml J: ABP1 and ROP6 GTPase signaling regulate clathrinmediated endocytosis in Arabidopsis roots. Curr Biol 2012,
22:1326-1332.
46. Zhang Q, Fishel E, Bertroche T, Dixit R: Microtubule severing at
crossover sites by katanin generates ordered cortical
microtubule arrays in Arabidopsis. Curr Biol 2013, 23:21912195.
This paper illustrates the microtubule-ordering mechanism of KTN1. With
live-cell imaging, Zhang and colleagues demonstrates that KTN1 localizes to microtubule crossovers where it exerts its severing activity.
Current Opinion in Plant Biology 2015, 28:137–143
51. Peaucelle A, Braybrook SA, Le Guillou L, Bron E, Kuhlemeier C,
Höfte H: Pectin-induced changes in cell wall mechanics
underlie organ initiation in Arabidopsis. Curr Biol 2011, 21:
1720-1726.
52. Braybrook SA, Peaucelle A: Mechano-chemical aspects of
organ formation in Arabidopsis thaliana: the relationship
between auxin and pectin. PLOS One 2013, 8:e57813.
In this paper, the authors investigate the relationship between auxin and
the mechanical properties of the cell wall at the shoot apex. By using
atomic force microscopy the authors demonstrate that auxin promotes a
decrease in cell wall rigidity before organ formation through modification
of the pectin matrix. Conversely, chemical modifications of the pectin
matrix aimed to rigidify the cell wall alter the polarity of PIN1, suggesting
the existence of a feedback loop between pectin biochemistry and auxin
transport during organogenesis.
53. Tameshige T, Hirakawa Y, Torii KU, Uchida N: Cell walls as a
stage for intercellular communication regulating shoot
meristem development. Front Plant Sci 2015, 6:324.
54. Swarup K, Benková E, Swarup R, Casimiro I, Péret B, Yang Y,
Parry G, Nielsen E, De Smet I, Vanneste S et al.: The auxin influx
carrier LAX3 promotes lateral root emergence. Nat Cell Biol
2008, 10:946-954.
55. Vermeer JEM, Geldner N: Lateral root initiation in Arabidopsis
thaliana: a force awakens. F1000Prime Rep 2015, 7:32.
56. Lucas M, Kenobi K, von Wangenheim D, Vob U, Swarup K, De
Smet I, Van Damme D, Lawrence T, Péret B, Moscardi E et al.:
Lateral root morphogenesis is dependent on the mechanical
properties of the overlaying tissues. Proc Natl Acad Sci U S A
2013, 110:5229-5234.
In this paper, the authors study the contribution of the outer layers of the
primary root to the formation of lateral root primordia. By using live-cell
imaging and 3D/4D image analysis, the author show how the overlying
cell layer determine the stereotypical shape of lateral root primordia
despite highly variable cell proliferation patterns.
57. Abu-Abied M, Rogovoy (Stelmakh) O, Mordehaev I, Grumberg M,
Elbaum R, Wasteneys GO, Sadot E: Dissecting the contribution
of microtubule behaviour in adventitious root induction. J Exp
Bot 2015, 66:2813-2824.
Here the authors study the contribution of microtubule to the formation of
adventitious roots. They show that the shape of the root primordium and
its differentiation status are determined by the organization of the microtubules. They also show that microtubule organization determines the
polarity of PIN1 and the distribution of auxin in the emerging primordium.
58. Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D,
Jürgens G, Friml J: Local, efflux-dependent auxin gradients as
a common module for plant organ formation. Cell 2003,
115:591-602.
59. Ditengou FA, Teale WD, Kochersperger P, Flittner KA, Kneuper I,
van der Graaff E, Nziengui H, Pinosa F, Li X, Nitschke R et al.:
Mechanical induction of lateral root initiation in Arabidopsis
thaliana. Proc Natl Acad Sci U S A 2008, 105:18818-18823.
www.sciencedirect.com
When biochemistry meets mechanics Sassi and Traas 143
60. Laskowski M, Grieneisen VA, Hofhuis H, Ten Hove CA,
Hogeweg P, Marée AFM, Scheres B: Root system architecture
from coupling cell shape to auxin transport. PLoS Biol 2008,
6:e307.
61. Richter GL, Monshausen GB, Krol A, Gilroy S: Mechanical stimuli
modulate lateral root organogenesis. Plant Physiol 2009,
151:1855-1866.
62. Barbier de Reuille P, Routier-Kierzkowska A-L, Kierzkowski D,
Bassel GW, Schüpbach T, Tauriello G, Bajpai N, Strauss S,
Weber A, Kiss A et al.: MorphoGraphX: a platform for
quantifying morphogenesis in 4D. Elife 2015, 4:05864.
This paper presents the MorphoGraphX software, a powerful tool that
allows a wide range of analysis such as cell segmentation, lineage
tracking and fluorescence signal quantification operating directly on
the curved surfaces of 3D images.
63. Weber A, Braybrook S, Huflejt M, Mosca G, RoutierKierzkowska A-L, Smith RS: Measuring the mechanical
properties of plant cells by combining micro-indentation with
osmotic treatments. J Exp Bot 2015, 66:3229-3241.
64. Milani P, Gholamirad M, Traas J, Arnéodo A, Boudaoud A,
Argoul F, Hamant O: In vivo analysis of local wall stiffness at the
www.sciencedirect.com
shoot apical meristem in Arabidopsis using atomic force
microscopy. Plant J 2011, 67:1116-1123.
65. Fernandez R, Das P, Mirabet V, Moscardi E, Traas J, Verdeil J,
Malandain G, Godin C: Imaging plant growth in 4D: robust
tissue reconstruction and lineaging at cell resolution. Nat
Methods 2010, 7:547-553.
66. Guo H, Li L, Ye H, Yu X, Algreen A, Yin Y: Three related receptorlike kinases are required for optimal cell elongation in
Arabidopsis thaliana. Proc Natl Acad Sci U S A 2009, 106:76487653.
67. Locascio A, Blázquez MA, Alabadı́ D: Dynamic regulation of
cortical microtubule organization through Prefoldin–DELLA
interaction. Curr Biol 2013, 23:804-809.
68. Wang X, Zhang J, Yuan M, Mao T: Arabidopsis microtubule
destabilizing protein40 is involved in brassinosteroid
regulation of hypocotyl elongation. Plant Cell 2012, 24:
4012-4025.
69. Wolf S, Mravec J, Greiner S, Mouille G, Höfte H: Plant cell wall
homeostasis is mediated by brassinosteroid feedback
signaling. Curr Biol 2012, 22:1732-1737.
Current Opinion in Plant Biology 2015, 28:137–143