Plant Motion

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V I E W
I N
C E
D V A
Vegetable Dynamicks:
The Role of Water in Plant
Movements
Jacques Dumais1 and Yoel Forterre2
1
Department of Organismic and Evolutionary Biology, Harvard University, Cambridge,
Massachusetts 02138; email: jdumais@oeb.harvard.edu
2
IUSTI, CNRS, Aix-Marseille Universite, 13453 Marseille cedex 13, France;
email: yoel.forterre@polytech.univ-mrs.fr
Annu. Rev. Fluid Mech. 2012. 44:45378
Keywords
The Annual Review of Fluid Mechanics is online at

fluid.annualreviews.org
plant biomechanics, osmotic pressure, growth, poroelasticity, instability,

surface tension, complex fluids
This articles doi:

10.1146/annurev-fluid-120710-101200
c 2012 by Annual Reviews.
Copyright !
All rights reserved
0066-4189/12/0115-0453$20.00
Abstract
Although they lack muscle, plants have evolved a remarkable range of mechanisms to create motion, from the slow growth of shoots to the rapid snapping
of carnivorous plants and the explosive rupture of seed pods. Here we review
the key fluid mechanics principles used by plants to achieve movements, summarizing current knowledge and recent discoveries. We begin with a brief
overview of water transport and material properties in plants and emphasize
that the poroelastic timescale of water diffusion through soft plant tissue
imposes constraints on the possible mechanisms for motion. We then discuss movements that rely only on the transport of water, from irreversible
growth to reversible swelling/shrinking due to osmotic or humidity gradients. We next show how plants use mechanical instabilitiessnap buckling,
cavitation, and fractureto speed up their movements beyond the limits imposed by simple hydraulic mechanisms. Finally, we briefly discuss alternative
schemes, involving capillarity or complex fluids.
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1. INTRODUCTION
Plants offer some of the most elegant applications of fluid mechanics principles found in nature.
Trees are little more than hydraulic systems that take water deep into the ground and elevate it
to the leaves. The branching of the shoots and roots, the anastomosing venation of leaves, and
the structural organization of plant tissues all speak to their transport function. Given this, it is
not surprising that plants have attracted attention in applied fluid mechanics (Canny 1977, Rand
1983). The first detailed study of the movement of water within plants is provided by Haless
(1727) Vegetable Staticks (Figure 1a). Hales (1727) not only described with great accuracy the
transpiration stream of plants, he also sought to interpret his observations in light of the fluid
mechanics of his time: The sap vessels are so curiously adapted by their exceeding fineness, to
raise the sap to great heights, in a reciprocal proportion to their very minute diameters.
Since the pioneering work of the Darwins (Darwin 1875, Darwin & Darwin 1880)
(Figure 1b), the question of how plants move in the absence of muscle has attracted the interest
of many scientists ( Jost & Gibson 1907, Ruhland 1959, Hart 1990). From a biological perspective, the physiology of plant movements is central to our understanding of plant development
and plants responses to environmental stimuli such as light and gravity (Gilroy & Masson 2008,
Moulia & Fournier 2009). In engineering and applied sciences, these nonmuscular movements
have provided inspiration for biomimetic design in the area of microfluidics and robotics (Taya
2003, Burgert & Fratzl 2009, Martone et al. 2010).
The goal of this review is to present some key fluid mechanics principles used by plants to
achieve movement, highlighting recent work performed at the frontier of mechanics and biology.
We do not address processes involving only water transport without organ motion, as seen, for
example, in the ascent of sap or the translocation of sugars in vascular systems. These topics
constitute a broad field of research and have already been the subject of many monographs and
reviews (Tyree & Zimmermann 2002, Holbrook & Zwieniecki 2005), including reviews in this
series (Canny 1977, Rand 1983).
Still the diversity of mechanisms that fit within the scope of this review is vast. From the slow
growth of shoots and roots to the opening and closing of the minute stomata at the leaf surface,
plants exhibit movements on a wide range of length scales. Most of these movements are slow,
but some compete in speed with those encountered in the animal kingdom and are used by plants
to trap prey or disperse their seeds (Sibaoka 1969, Hill & Findlay 1981).
Figure 1
Vegetable staticks and dynamicks. (a) Experimental setup used by Hales (1727) to collect the water
transpired by various plants. (b) A recording of leaf movement by Darwin & Darwin (1880).
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We begin with a brief overview of the plant cell and tissue structure and a discussion of the
various mechanical and hydraulic processes (e.g., osmosis, elasticity) enabling plants to move
(Section 2). Particular attention is given to how these processes set the timescales of the various
movements. In Section 3, we discuss hydraulic movements at the cell and tissue level, from
irreversible growth to reversible swelling/shrinking. In both cases, the driving force for motion
is the high differential water pressure supported by the plant cell wall. In Section 4, we show how
mechanical instabilitiessnap buckling, cavitation, and fracturecoupled with water transport
allow plants to overcome the poroelastic limit set by the diffusion of water through tissue. Finally,
in Section 5, we briefly discuss alternative strategies for movement broadly defined involving
capillarity and complex fluids.
2. FUNDAMENTALS
A bouquet of tulips left standing without water will gradually droop, the flaccid stems unable to
support the weight of the blossoms. If water is provided again, the stems will soon straighten, and
the bouquet will regain its former glory. Although the wilting of a flower may seem mundane,
it encapsulates the essence of the mechanism used by plants to achieve movement. To move,
plants drive water in and out of their cells by manipulating the osmotic gradients across their
semipermeable membranes. The local changes in cellular volume and tissue stiffness enable the
large-scale tissue deformations required for motion.
Therefore, plant motion is fundamentally a mechanical problem whose key features are rooted
in the structure and physiology of plant cells. Within the context of mechanics, the plant body
can be decomposed into two simple phases: a fluid phase representing as much as 75% of the total
mass of fresh tissue and a solid phase made largely of the cellulosic walls that surround every plant
cell. At this level, plants do not differ significantly from algae, fungi, and other organisms with
walled cells. We therefore have sampled freely between these groups to emphasize the generality
of the principles at work, but also to highlight the great ingenuity with which nature has sought
to endow these organisms with the power of movement.
2.1. Plant Cell and Tissue Structure

A fundamental difference between plants and animals is that plant cells are surrounded by a thin
but stiff cell wall made of highly organized cellulose microfibrils embedded in a pectin matrix
(Preston 1974, Taiz & Zeiger 2002, Baskin 2005) (Figure 2b). This structural difference prevents plant cells from using soft contractile proteins (such as the actomyosin system of muscle
fibers) to deform and generate movement. However, the stiff wall allows plant cells to sustain a
large internal hydrostatic pressure known as turgor. A turgor pressure of approximately 0.5 MPa
(5 bars) is common (Green et al. 1971, Zhu & Boyer 1992) (Figure 2a). Cells develop this pressure
by maintaining an osmotic gradient between their cytoplasm and the environment, thus allowing
water to move into the cell and put the wall under tension. As shown below, this high turgor
pressure provides the force for changing the cell volume and is thus the main motor for growth
and motion in plants.
With regard to plant tissues or entire organs, water can be found in two separate but interpenetrating compartments: the symplast and the apoplast (Figure 2b). The symplast is defined as
the volume contained within the plasma membrane of cells and thus under direct osmotic control
by the cells. The apoplast is the dual of the symplast and includes all the volume taken by cell
walls and intercellular spaces. Direct symplastic flow between cells is possible through intercellular
www.annualreviews.org The Role of Water in Plant Movements
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Guard cell
Plasma
membrane
Phloem
Typical plant cell
Cell wall
Muscle
Car tire
Blood pressure
Xylem tension
Fern leptosporangium
30
25 5
Pressure (MPa)
Figure 2
Water in plants. (a) The range of water pressures found in plants as compared with other familiar systems.
Plants are the only living organisms that use water in a state of high tension, as much as 300 bars in the case
of the fern leptosporangium. (b) The principal paths along which water flows. The cell-to-cell path !
comprises both the transmembrane path, where water moves across the semipermeable plasma membrane,
and the direct symplastic path through the plasmodesmata that does not cross the plasma membrane (double
blue line). In the apoplast path ", water moves through the relatively porous cell walls and intercellular
spaces without crossing any membranes. Finally, evaporative loss at the plant surface # plays an important
role in water relations and also drives many plant movements.
bridges known as plasmodesmata. Conversely, the porous nature of the cell walls that constitute
the apoplastic space provides an alternative path of high conductivity for water flow.
2.2. Water: The Prime Mover

The flow of water in living plant tissues shares many similarities with flow in porous media, with
the notable exception that osmotic gradients must be considered alongside the pressure gradients.
Depending on the length scale at which flow is considered, the permeability associated with the
pressure and osmotic gradients will vary slightly. Therefore, we consider in turn water flow at the
cellular level and at the tissue level.
2.2.1. Water transport across the cell membrane. At the cellular level, the water flux j (in
meters per second) across a perfect semipermeable membrane, and thus the rate of change in the
cell volume V, is driven by the change in the chemical potential of water, according to the relation
Water potential: the

chemical potential of
water per unit volume
relative to a reference
state
456
dV
= j A = A L p !" = A L p (!P + ! ),
(1)
dt
where A is the cell membrane area; Lp is the hydraulic conductivity of the cell membrane (in
meters per second per pascal); " = P is the water potential (in pascals); P is the hydrostatic
pressure minus the atmospheric pressure; = c RT is the osmotic component, with c the solute
concentration, R = 8.32 J mol1 K1 the gas constant, and T the temperature (in Kelvin); and
! stands for the difference between the inside and outside of the cell (Dainty 1976, Finkelstein
1987, Kramer & Boyer 1995, Nobel 1999). In the field of animal physiology, Equation 1 is known
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as the Starling equation and is used to quantify the rate of plasma filtration and resorption in
capillary beds. In the context of plant cells, Equation 1 states that changes in the volume of cells
are driven by modifications of the turgor pressure or solute concentration from their equilibrium
values. The rate of water flow depends on the membrane conductivity Lp , which is a crucial
quantity for water relations in plants. Values of the membrane conductivity span a wide range,
1013 L p 1011 m s1 Pa1 (Steudle 1989), and may be regulated by the opening or closing
of water pores, called aquaporins, which are under tight physiological and molecular regulation
(Maurel et al. 2008).
2.2.2. Water transport across plant tissue. The previous water relations at the cellular level
apply to the description of flow in tissues at the macroscopic level. For instance, the assumption
of only cell-to-cell transport across the cell membranes (path 1 in Figure 2b) yields a Darcy-like
relation between the water flux and the water-potential gradient, with a Darcy permeability (in
squared meters) L p R, where (in pascal seconds) is the water viscosity (Philip 1958). However, the situation in most tissues is more complex because water may also flow in the cell wall
continuum (apoplast pathway), whose permeability kwall depends on both the cell wall volume
fraction in the tissue and the cell wall permeability kwall (Figure 2b). In many cases (roots and
stems), both pathways are of similar conductivity, and one may define a single effective permeability k encompassing both the cell-to-cell and apoplast pathways, with typical values 1020 k
1019 m2 (Molz & Ikenberry 1974, Molz & Ferrier 1982, Steudle 1992). However, although osmotic and turgor gradients may drive water flow across the cell membrane, only pressure gradients
lead to significant bulk flow in the apoplast because the cell wall continuum is permeable to most
solutes (Steudle 1989, 1992). Thus both driving forces are not equivalent at the tissue level.
2.3. Material Properties of the Plant Cell Wall

The plant cell wall is a living material and as such must be approached mechanically with some
caution. For example, what may look like simple viscosity at the macroscopic level can in fact reflect
the addition of mass and a chemically mediated remodeling of wall material at the microscopic
level. The constitutive modeling of materials that add mass and remodel as they deform is an
active area of research (Ambrosi et al. 2011). Here we focus mostly on the macroscopic properties
of cell walls, as they suffice in explaining plant movements.
2.3.1. Elastic regime. The plant cell wall behaves elastically for a narrow range of strains (5%
or less), with the exception of a few specialized cells, such as the guard cells of the stomata (see
Section 3.2), in which higher wall strains can also be reversible. The Youngs modulus Ewall of the
cell wall of actively expanding cells is typically less than 1 GPa (Probine & Preston 1962), whereas
for wood fibers, it exceeds 25 GPa (Gibson & Ashby 1999). An alternative measure of elasticity
is the bulk modulus of the cell = V (dP/dV ) (Figure 3a). The bulk modulus characterizes how
changes in volume are related to changes in turgor pressure, and has a typical value between 1 and
50 MPa (Steudle et al. 1977, Cosgrove 1988). Although it is defined in the same way as the bulk
modulus of standard engineering materials, the interpretation of the cellular bulk modulus can be
challenging as it reflects not only the elasticity of the cell wall, but also the geometry of the cell
(Wu et al. 1985, Cosgrove 1988). The cellular bulk modulus is nonetheless a useful parameter as
it plays a pivotal role in setting the timescale of cellular responses to changes in osmotic balance.
At the tissue level, the relation between the macroscopic Youngs modulus of the tissue and
the cell properties (wall elasticity, cell size) can be approached from the standpoint of cellular materials (Gibson & Ashby 1999, Gibson et al. 2010). As long as the turgor pressure is
high and the cell walls stretched, the tissue Youngs modulus scales with the cell bulk modulus,
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b
P (MPa)
103
Cell length L (m)
Relative volume (%)
104
102
101
100
0
0.1 0.2 0.3 0.4 0.5 0.6 0.7
Cell pressure P (MPa)
900
0.60
0.55
0.50
0.45
800
Percent original dL/dt
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20
10
0
700
600
500
400
300
200
100
20
40
60
80
Time (min)
100
120
50
100
150
Percent original pressure
Figure 3
(a) Elastic and (b,c) plastic behavior of the cell wall as observed in Chara and Nitella internodal cells. (a) The pressure-volume curve is
shown for a single internodal cell in the elastic regime (Kamiya et al. 1963). Note the hysteretic response. (b) Increases or decreases in
turgor pressure lead to an abrupt (elastic) change in cell length followed by a gradual transition to a new elongation rate (Proseus et al.
2000). (c) The elongation rate depends strongly on the cells pressure and shows a marked yield pressure (approximately 50% of the
normal pressure) below which growth is not possible (Proseus et al. 2000).
E 10 MPa. However, E decreases sharply when the turgor pressure drops to zero because
the cell walls are no longer stretched and can bend easily (Nilsson et al. 1958, Warner et al. 2000).
Tropic response:
movement determined
by the direction of the
stimulus (gravity, light,
touch); examples
include phototropism,
gravitropism, and
thigmotropism
Nastic response:
movement that occurs
in a direction
independent of the
stimulus (e.g., the
folding of the Mimosa
pudica leaf and closing
of the Venus flytrap)
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2.3.2. Plastic regime and growth. Historically, the constitutive behavior of the growing cell wall
has been described as a Bingham fluid (Lockhart 1965, Green et al. 1971, Cosgrove 1985, Proseus
et al. 1999). Bingham fluids differ from ordinary viscous fluids in that they deform irreversibly
only for stresses that exceed a plastic yield stress y . For uniaxial deformation, the rate of plastic
deformation is written as ( = ( y ) for > y , where is the material extensibility (an
inverse viscosity). Lockhart (1965) was the first to apply this constitutive law to wall extension and
growth in plants, which was later extended to incorporate a viscoelastic behavior (Ortega 1985,
1990). Extensions of the simple uniaxial model to anisotropic materials under multiaxial stress are
now available (Dumais et al. 2006, Dyson & Jensen 2010).
The simple constitutive law adopted by Lockhart is well supported experimentally. A number of
investigators have demonstrated that the relative rate of cell expansion is not simply proportional
to the cell pressure (Green et al. 1971, Proseus et al. 1999). For example, small-step increases or
decreases in pressure (<10%) cause drastic changes in the rate of cell expansion (Figure 3b). Also,
with rare exceptions, cells show a clear yield pressure below which they cannot maintain growth
(Figure 3c).
2.4. Timescales of Plant Movements

As we have seen, plants mostly rely on water and their cellulosic wall to move. Given this, the
diversity of movements and timescales observed in plants is quite remarkable. Comparing the slow
growth of shoots (days to hours) with the explosive motion of seeds and spores (<0.1 ms), one
sees that the characteristic times of plant motions span almost 10 orders of magnitude. Biologists
usually classify these movements depending on their reversible or irreversible character, on their
active (physiological) or passive origin, or on the relation between the nature of the stimulus and the
response (tropic or nastic response to light, touch, gravity, etc.) (Hill & Findlay 1981, Hart 1990,
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b
1
Pressure probe
0.63
Change in tissue length (%)
Cell turgor pressure P (MPa)
0.64
Giant algal cell (Chara)
0.62
0.61
0.60
0.59
20
25
Time (s)
30
35
40
1mM KCl
0
1
2
1
10
15
20
Time (min)
Desiccation
in dry air
25
0
1
2
Salt solution/
fresh water
3
4
15
25mM KCl
Stop air flow
Water bath
0
Time (min)
Figure 4
Swelling/shrinking timescales in plant cells and tissues. (a) Single-cell relaxation in a giant algal cell (Chara corallina internode)
measured by a cell pressure probe (Steudle 1993) (data from Ye et al. 2006). A pressure step is applied by suddenly injecting a small
volume of water in the cell. In this system, V/A = 200 m and = 30 MPa. The cell relaxation time is cell = 3.5 s, which gives a
cell membrane conductivity L p 2 1012 m s1 Pa1 . (b) Reversible swelling and shrinking of a plant tissue (pealed pea epicotyl 1 cm
in length) suddenly immersed in baths of different solute concentrations (upper panel ) or in a fresh solution after desiccation in air
(lower panel ). The measured tissue relaxation time (poroelastic time) is p = 4080 s. In this radial water transport geometry,
p = 0.022 L2 /D (Philip 1958), where L = 1.6 mm is the segment diameter, which gives a coefficient of diffusion D 109 m2 s1 .
Data taken from Cosgrove & Steudle (1981).
Braam 2005), with no clear reference to the underlying physical mechanism. A key suggestion made
recently by Skotheim & Mahadevan (2005) is that the timescale for water transport constrains
the maximal speed of hydraulic movements in these soft nonmuscular systems, thus providing
a physical basis for the classification of motion in plants and other walled organisms such as
fungi.
2.4.1. Cell relaxation time. We first address this question at the cellular level. A cell perturbed
from equilibrium by a small sudden change in the osmotic potential or turgor pressure relaxes
exponentially with a timescale given by
cell =
V
R
,
A( + ! )L p
L p
(2)
where R = V/A is the typical cell radius, and $ ! , as is the case for most turgid cells
(Dainty 1976). Typical measurements in giant algal cells of R = 200 m, = 30 MPa, and
L p = 2 1012 m s1 Pa1 give cell = 3.5 s (Figure 4a).
The cell relaxation time (Equation 2) may be interpreted as the shortest response time of a plant
cell to small water-potential perturbations and thus provides a bound for hydraulic movements
at the cellular level. Figure 5a plots the timescale of motion as a function of the typical cell
size R for a wide range of unicellular movements in plants and fungi, together with the boundary
given by Equation 2. Systems with > cell can rely on water transport to swell or shrink, whereas
systems with < cell must use other mechanisms, as shown in Sections 4 and 5. The dependence
of cell on the cell size R shows that water transport may be fast if a cell is sufficiently small, as in
the case of the rapid swelling of nematode-trapping fungi (see Section 3.1).
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Fastest cell swelling cell

Fastest cell growth Lockhart
Nitella
Pollen tube
Sporangium (opening)
Oedogonium
Stomata
Chara (relaxation)
Arthrobotrys brochopaga (fungus)
Zoophagus insidians (fungus)
A. dactyloides (fungus)
Dactylaria brochopaga (fungus)
Utricularia (trapdoor)
Pilobolus
Sporangium (closing)
Ballistospore
106
105
104
103
102
Timescale (s)
Timescale (s)
16:48
101
100
Fastest tissue swelling p

Fastest elastic motion el
105
103
102
101
100
101
102
102
103
103
105
107
105
Mechanical
instability
(buckling/cracks)
104
Ballistospores
(surface tension)
106
Hydraulic movements
(swelling/growth)
104
101
104
Lonicera japonica
L. sempervirens
Pinguicula vulgaris
Ipomoea nil
Pharbitis nil
Arabidopsis thaliana
Oryza sativa
Desmodium gyrans
Mimosa pudica
Dionaea
Stylidium crossocephalum
S. graminifolium
S. piliferum
Utricularia (trapdoor)
Aldrovanda
Catasetum
Lepidium campestre
Ruellia brittoniana
Ecballium elaterium
Hura crepitans
Arceuthobium
106
104
103
102
105
106
105
104
Cell radius R (m)
103
102
101
100
Tissue size L (m)
Figure 5
Classification of (a) unicellular and (b) multicellular movements in plants and fungi, based on the timescale of water transport (from an
original idea of Skotheim & Mahadevan 2005). The plots give the duration of movement as function of (a) the cell radius R and (b) the
tissue size L, defined as the smallest macroscopic moving part. The order of the labels in the figure key coincides with their order in the
figure from top to bottom. In panel a, the solid blue line gives the cell relaxation time (the fastest cell swelling) cell = R/(L p ), with
= 30 MPa and L p = 2 1012 m s1 Pa1 , and the dashed blue line gives the Lockhart time (the fastest cell growth not limited by
water transport) Lockhart = R/(! L p ), with ! = 0.5 MPa. In panel b, the solid blue line gives the poroelastic time (the fastest tissue
swelling) p = 0.022 (L2 /D), with D = 109 m2 s1 . The solid red line gives the timescale for elastic wave propagation (the fastest
elastic motion) el = L /E, with = 1,000 kg m3 and E = 10 MPa.
2.4.2. Poroelastic time. The previous relation (Equation 2) holds at the cellular level. However,
the swelling or shrinking of a tissue requires not only a local change in cell volumes, but also the
transport of water from one part of the tissue to another. The flow of water in a soft porous media
such as plant tissue is a diffusive process, whose timescale over a tissue of size L, known as the
poroelastic time p , is given by
p
L2
L2
,
D
kE
(3)
where D = kE/ is a diffusive coefficient that depends on the Darcy permeability of the porous
tissue k, the (undrained) Youngs modulus of the tissue E, and the water viscosity (Biot 1941,
Wang 2000). Philip (1958) was the first to derive a diffusion-like equation for water transport
through plant tissues assuming cell-to-cell transport only. This model was further extended to
incorporate both the cell-to-cell and the apoplast pathway (Molz & Ikenberry 1974, Molz &
Ferrier 1982, Steudle 1992). Typical values for plant tissues (k = 1020 /1019 m2 , E = 10 MPa,
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and = 103 Pa s) give D = 1010 /109 m2 , compatible with swelling experiments of tissues
(Figure 4b) (Molz & Boyer 1978, Cosgrove & Steudle 1981, Steudle 1989).
The poroelastic time p (Equation 3) may be interpreted as the fastest possible water-driven
movement at the tissue and organ levels (Skotheim & Mahadevan 2005). Its strong size dependence
( L2 ) shows that hydraulic movements are increasingly less efficient in terms of speed as the system
size increases. Figure 5b presents the duration of plant movement as a function of the typical
distance L through which the fluid is transported for a wide range of movements and timescales.
The boundary = p naturally separates two categories of movements dominated either by
swelling/growth or by mechanical instabilities.
In the following, we present some specific examples of plant movement mechanisms in light
of this classification. We first address slow hydraulic movements (irreversible growth, reversible
swelling/shrinking). We then shift to rapid movements that cross the poroelastic boundary, in
particular those using a mechanical instability to amplify their speed.
3. HYDRAULIC MOVEMENTS IN PLANTS

3.1. Growth and Growth Movements
The most ubiquitous but also least obvious movements in plants are associated with growth. It
took the patient eye of Charles Darwin (Darwin & Darwin 1880) to finally draw greater attention
to them. The elongation of stems is a slow but vital race toward the sun. Plants left behind are
bound to spend their lives in the shadow of their taller neighbors. Given the selective pressure for
rapid growth in many environments, one may ask what limits the rate of plant growth. Lockhart
(1965) provided the first model to address this question at the cellular level. For a cell to expand,
two processes must occur concomitantly: The cell wall must increase its surface area, and water
must enter the cell to increase its volume. Lockharts model for a cylindrical cell of radius R and
wall thickness h predicts the following governing equation for the relative rate of volume increase:
( =
(R! h y )
1 dV
= Lp
.
V dt
h L p + R2
(4)
If typical values for cell geometry, hydraulic conductivity, and wall extensibility are considered, it
is seen that h L p $ R2 . Lockharts equation thus simplifies to
"
!
R!
(5)
y .
( limited =
h
This limit is known as the extensibility-limited regime for cell expansion. In other words, the
characteristic strain rate of growing plant cells is set by how fast the cell can extend its wall and not
by its ability to take up water through the plasma membrane. Given that the extensibility is set by
the rate at which the wall is synthesized and assembled by the cell, the extensibility-limited regime
is really a statement about the cells maximal metabolic rate. In that context, it is a remarkable
observation that some cells can achieve local strain rates as high as 0.25 min1 (Rojas et al. 2011)
(an equivalent wall viscosity 1/ 10 GPa s, assuming typical values R/h 100 and !
0.5 MPa).
An elegant example of growth-mediated movement is seen in the phototropic response of the
Phycomyces sporangiophore, a cell of gigantic size (as much as 10 cm) that raises the sporangium
and its spores above the boundary layer for dispersal (Figure 6a). The zone of elongation is
confined to a 3-mm region just below the terminal sporangium. Within this region, strain rates
can reach values as high as 0.05 min1 . The high strain rates and relatively narrow sporangiophore
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b
1 cm
1 mm
0h
3h
5h
10 h
16 h
19 h
Figure 6
Growth movements at the cellular and tissue scales. (a) Phototropic bending of the Phycomyces
sporangiophore in response to unilateral light coming from the right. Images were taken at 5-min intervals
(Shropshire 1963). (b) Bending movement induced by differential growth of a cyclamen flower stalk
(MacDonald et al. 1987). The numbers indicate the times (in hours) at which the pictures were taken. The
coiling proceeds over several days until the terminal seed pod is buried into the ground.
stalk allow for rapid bending (3 7 min1 ) in response to unidirectional light (Figure 6a) (Castle
1962). Similar bending responses, albeit slower, are also seen in stems and roots (Figure 6b).
In some special cases, cells can increase in volume at a relative rate that is nearly equal to
the maximum rate the membrane conductivity will allow (Equation 1). This regime is known as
conductivity-limited growth (h L p ' R2 ). In this limit, the Lockhart equation takes the form
(R! h y )
.
R2
Figure 5a shows the Lockhart timescale, defined as
( Lp limited = L p
Lockhart =
1
R
.
( Lp limited
L p !
(6)
(7)
The Lockhart timescale may be interpreted as the fastest possible cell growth not limited by water
diffusion across the membrane. It is usually much larger than the cell relaxation time ( $ ! ),
except in cells in which the turgor pressure is very high and the wall is soft like stomata.
One way cells reach the conductivity limit (Equations 67) is by assembling the wall surface
necessary to increase cell volume before expansion. The algal cell Oedogonium offers a clear example
(Figure 7a). Cell expansion in these algae is coupled to cell division and begins with the formation
of an internal flap of wall material at one end of the cell. Because of its position within the external
load-bearing wall, this flap can develop without having to support the turgor pressure of the cell.
When the cell is ready to divide and expand, a fracture develops in the outer wall, thus transferring
the load to the unstretched wall flap. Consequently, the initial phase of expansion is mainly limited
by the rate at which water can enter the cell. Actively growing cultures of Oedogonium are described
as twitching, providing some indication of the bursting nature of cell expansion following the
release of the old wall. One observes in Figure 5a that Oedogoniums growth rate is indeed close
to the Lockhart limit.
A similar mechanism has been put to good use in nematode-trapping fungi. These soil fungi
have evolved a simple noose that they use to capture the nematodes with whom they share their
environment (Figure 7c). Although the capture mechanism has not been fully elucidated, it is
believed that a load-bearing wall layer loses its mechanical integrity upon stimulation of the noose
cells by a passing worm. The ensuing sharp decline in turgor pressure puts the cell out of osmotic
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b
Growth
scar
Wall
ring
Slit
10 m
t=0s
5 m
t = 0.12 s
t = 0.18 s
10 m
Figure 7
Conductivity-limited growth. (a) Expanding inner wall ring in Oedogonium (Pickett-Heaps 1975). (b) Wallring development and early phase of expansion (Pickett-Heaps 1975). The wall ring develops inside the cell
at the level of a slit in the load-bearing wall. Fracture of the outer wall along the slit puts the inner wall ring
under tension, allowing for rapid cell elongation. (c) Constricting ring of the nematode-trapping fungus
Arthrobotrys brochopaga. (d ) A trapped nematode. Panels c and d taken from Nordbring-Hertz et al. (2006).
equilibrium, thus allowing water to rush in. The rapid swelling of the cells closes the noose, leaving
the snared prey to be slowly invaded by fungal hyphae and digested.
For cells bathed in water, the conductivity of the cell membrane is such that water uptake
rarely limits growth. However, in multicellular tissues, cells have access to water only through
neighboring cells. One may ask whether, in that context, water flow may not limit the rate of growth
(Molz & Boyer 1978, Boyer & Silk 2004). Simple scaling arguments may be used to address this
question. For uniform growth to occur in a plant tissue, this tissue must maintain a constant water
flux given by the Darcy law (k/)!P/L, where L is the typical size of the growing organ and
!P is the pressure difference. This flux is related to the growth rate ( by volume conservation
One may assume that the process is not conductivity limited as long as the
(k/)!P/L L(.
pressure drop is small compared with the typical cell turgor P, yielding ( ' k P/L2 . The inverse
of this maximal growth rate sets the tissue Lockhart timescale:
L2
.
(8)
kP
This timescale is the analog at the tissue level of the Lockhart timescale for the cell (Equation 7).
It may be interpreted as the fastest possible uniform tissue growth not limited by water transport.
For a while, there has been quite a debate in the plant physiology community on whether these
growth-induced gradients of pressure could play an important role in plant growth (Steudle 1989).
For rapidly growing tissues (coleoptile, roots), they might not be negligible and may play a role
in the regulation of growth movements (gravitropism, phototropism, thigmotropism).
Lockhart tissue
3.2. Actuation Driven by Osmotic Gradients

The second main class of water-driven movements in plants is associated with small reversible
changes in the cell volume within the elastic range of cell wall deformation. These modifications
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Stomatal half-aperture (m)
1.0 MPa
2.0 MPa
3.0 MPa
4.0 MPa
4
2
0
Guard cell turgor pressure P (MPa)
200
150
Fast
Slow
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Upper pulvinus
50
Lower pulvinus
0
200
400
600
800
1,000
Time (s)
Figure 8
Actuation in plants driven by osmotic gradients. (a) Relationship between the stomata aperture and the
turgor pressure inside the guard cells, measured by confocal microscopy. Figure adapted from Franks et al.
(2001). The left panel shows the stomata on the surface of a broad-bean leaf (Vicia faba). (b) The slow
recovery of the main pulvinus of Mimosa pudica imaged by nuclear magnetic resonance, showing a
displacement of water from the upper to the lower half. The plot gives the distribution of water as function
of time, together with the petiole to stem angle. Figure adapted from Tamiya et al. (1988).
may be driven by an active transport of solutes (ions) across the cell membrane by specialized
pumps. Although the variations in volume involved are usually small, the resulting change in turgor
pressure may be very large as the cell wall is stiff (large bulk modulus). The additional coupling
with the geometry and structural properties of the cell, tissue, or organ allows the amplifying
mechanism to convert small reversible changes in volume into large movements.
The opening and closing of stomata are probably among the most important and therefore
best-studied reversible movements in plants (Meidner & Mansfield 1968) (Figure 8a). Stomata
are small pores on the surface of the leaves that control the leaf transpiration and gas exchange
with the atmosphere, on a timescale ranging from a day (diurnal rhythm) to a few minutes (shortterm response to environmental change) (Woods & Turner 1971, Buckley 2005, Kaiser & Grams
2006). In most plants, the stomatal complex consists of two kidney-shaped guard cells that flank
a central pore (Taiz & Zeiger 2002). When the turgor pressure inside the guard cells increases
owing to accumulation of solute (up to P 5 MPa), the cells swell reversibly (by 20%40% in
volume) and become more curved in shape, pushing apart the surrounding cells and opening the
pore (Figure 8a). When the turgor pressure decreases, the two guard cells are pressed together
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by the surrounding cells, and the pore closes. The relationship between the stomatal aperture and
the turgor pressure of the guard cells and the surrounding epidermal cells has been studied both
experimentally and theoretically (Aylor et al. 1973, de Michelle et al. 1973, Cooke et al. 1976,
Franks et al. 2001, Franks 2003, Buckley 2005) (Figure 8a). The bending of the guard cells as
they swell comes from the large asymmetry in wall thickness and the mechanical anisotropy of the
cellulosic network.
Other classic examples of actuation in plants are the circadian and light-induced leaf movements
of several plants due to a specialized multicellular motor organ, called the pulvinus, located at the
base of the leaf petiole (i.e., where the leaf comes in contact with the stem). These movements
are usually under slow diurnal rhythms but can be as fast as seconds in the case of the leaves of
the sensitive plant Mimosa pudica. The current paradigm attributes all pulvinus movements to a
differential osmotic swelling/shrinking on opposite sides of the pulvinus, whose location at the
base of the leaf acts as a lever to amplify the leaf s angular motion (Hill & Findlay 1981, Moran
1990) (Figure 8b). The rapid closing of M. pudica seems to have attained the fastest possible
hydraulic motion (Figure 5b) according to the size of its pulvinus [pulvinus diameter L 200 m
(Weintraub 1952), poroelastic time b 1 s]. However, to our knowledge, no direct evidence for
rapid water flow in this system exists.
3.3. Passive Actuation Driven by Humidity Gradients

Osmotic gradients are not the only mechanisms for water exchange between cells and their surroundings. When cells are exposed to a dry atmosphere with a low partial water pressure, evaporation causes the volume to change as well. Many passive motions in plants are driven by these
humidity (water-potential) gradients between the cell and the ambient air. The water potential
of air is a function of the water-vapor partial pressure Pvap through the classical vant Hoff relation "vap = (RT /V w ) ln[Pvap /Psat (T )], where V w 18 cm3 mol1 is the partial molar volume
of liquid water and Psat (T ) the saturation water pressure (Atkins & de Paula 2002). For a relative humidity 100 Pvap /Psat (T ) = 50%, the water potential in air is very low (approximately
94 MPa) and, together with water cohesion properties, may lead to large negative pressure in
cells with stiff walls (see Section 4.2) and force other cells to crumple tightly to accommodate the
lost volume.
Pollen grains are routinely exposed to harsh osmotic environments and have therefore evolved
a coping mechanism. The surface of pollen grains comprises two regions: the porous apertures
and the water-impermeable interapertural areas (Figure 9a,b). The permeability of the apertures
is necessary to allow communication and exchange of water with the receptive surfaces of flowers.
The same permeability, however, threatens the survival of the minute pollen grains while in transit
from one flower to another. The solution found by pollen grains is to design their apertures such
that they fold inwardly when the pollen loses water, thus effectively preventing further evaporation
(Figure 9a,b) (Katifori et al. 2010). Unlike crumpling, the regular folding of pollen grains is fully
reversible when water becomes available again.
3.4. Hygroscopic Movements

Humidity-driven movements also occur in dead cells at the tissue level (sclerenchymal tissue) ( Jost
& Gibson 1907). Sclerenchymal tissue typically consists of fiber cells with walls comprising several
layers of oriented cellulose fibrils. When absorbing/expelling water in response to changes in air
humidity, the tissue expands/shrinks anisotropically, perpendicular to the fibrils orientation (Fahn
& Werker 1972, Burgert & Fratzl 2009). Asymmetry in the orientation of the fibrils at the organ
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6
7
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1,200
50
40
30
20
10
0
100
t (s)
200
300
400
500
t (min)
Figure 9
Passive movements driven by changes in humidity in (a,b) living cells and (cf ) dead tissues. The folding
(self-sealing) response of (a) lily and (b) Euphorbia pollen grains. (c,e) The drilling motion of the awn of
Erodium (Evangelista et al. 2011). (e) Number of turns of the awn as a function of time for wetting and drying
transients. The wetting time constant is = 330 s, and the drying time constant is = 400 s. (d,f ) The
opening motion of conifer cones, showing much longer time constants in accordance with the larger system
(Reyssat & Mahadevan 2009).
level then converts this local swelling/shrinking to a global bending movement, which can drive,
for example, the opening and closing of a pine cone (Dawson et al. 1997, Reyssat & Mahadevan
2009) (Figure 9d, f ), the penetration of seeds into soil (Elbaum et al. 2007, Evangelista et al. 2011)
(Figure 9c,e), and the opening of seed pods (Armon et al. 2011). The difference between these
actuation mechanisms and those seen previously with living cells is that, in dead tissues, there are
no longer cell membranes to maintain an osmotic gradient. Still, in some cases, a turgor gradient
may be maintained at equilibrium with the atmosphere with the cell wall acting as a semipermeable
membrane between the vapor and liquid phase (Wheeler & Stroock 2008). We note that a related
mechanism of anisotropic swelling/shrinking driven by the cell wall architecture applies in the
control of branch movements in woody organs (reaction wood), although on a different timescale
and length scale (Niklas 1992).
4. BEYOND WATER DIFFUSION: INSTABILITY

AND FLUID-SOLID COUPLING
The hydraulic movements discussed above are constrained in terms of speed by the timescale of
water diffusion p = L2 /kE (poroelastic time), especially so as the system size increases (see
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Section 2). Yet, from carnivorous plants to seed dispersal, many plant motions cross this hydraulic
boundary to generate some of the fastest motions ever recorded in living systems (Figure 5).
The strategy to reach these speeds is based on a simple principle: mechanical instability. A water
flowdriven either by osmotic or humidity gradientsfirst slowly stores elastic energy in the cell
walls, which is prevented from being released by some energy barrier. Above a critical threshold,
the barrier is overcome, and the elastic stress is suddenly released. In this section, we discuss these
champions of the plant kingdom, in light of recent discoveries made possible by the use of highspeed video. We note that the speed of these elastic movements is expected to be limited, ultimately,
by the speed of elastic waves (Skotheim & Mahadevan 2005). The timescale el = L /E for
elastic waves to travel a distance L, where is the tissue density, is given in Figure 5b. No plant
movements are found below this limit.
4.1. Snap-Buckling Instabilities

Geometric frustration is among the most elegant ways for a plant to accumulate elastic energy to
power motion. It is based on the idea that a thin shell, under a specific mode of loading, can be
locked in a configuration that represents a local energy minimum rather than the global energy
minimum. The transition between the two configurations often involves extensive stretching of
the shella costly mode of deformation in term of elastic energy (Landau & Lifshitz 1986).
However, the accumulation of elastic energy with increasing load can allow the shell to cross the
energy barrier. It then snaps into the configuration of lowest energy, releasing the stored elastic
energy. In this section, we give two examples of rapid movements in carnivorous plants that use a
snap-buckling instability to catch prey.
4.1.1. Venus flytrap. The rapid closure of the Venus flytrap (Dionaea muscipula) is one of the
best-known rapid motions in the plant kingdom and led Darwin (1875) to describe the plant as
one of the most wonderful in the world (Lloyd 1942, Juniper et al. 1989) (Figure 10a). Closure
of the trap is initiated by the mechanical stimulation of one of the trigger hairs [usually twice
within 20 s (Brown 1916)], which elicits an electrical action potential that spreads over the leaf in
less than 1 s (Burdon-Sanderson 1882, Stuhlman & Darder 1950, Sibaoka 1969, Hodick & Sievers
1989, Volkov et al. 2007). The trap then shuts in a few tenths of second, which seems too fast to
be accounted for by pure water transport across the 0.5-mm leaf thickness (Figure 5b).
A recent study suggests that the mechanism of closure of the Venus flytrap involves a snapbuckling instability, analog to the buckling of an elastic shell (Forterre et al. 2005). The two lobes
of the trap are curved outward in the open state and curved inward in the closed state (Figure 10b).
Upon triggering, the lobes actively change their natural curvature in the direction perpendicular
to the midrib. However, because of the geometric constraint of the doubly curved lobe, this active
bending causes the trap to accumulate stretching energy, until the stored elastic energy becomes
so large that the trap snaps shut rapidly (Figure 10c). Although the lobes behave like curved shells,
the closing dynamics is much slower and damped than what one would expect for a purely inertial
snapping of an elastic shell. It has been proposed that, within the hydrated soft porous tissue
of the leaf, passive flow induced by bending provides viscous resistance that balances the elastic
energy, in agreement with a poroelastic shell dynamics model (Figure 10c) (Forterre et al. 2005).
Biomimics of this mechanism have been applied in the context of microfluidics (soft actuators)
(Kim & Beebe 2007), robotics (Lee et al. 2010), and smart surfaces (Holmes & Crosby 2007).
Whereas the role of elastic instability in the trapping mechanism seems to be supported at
a macroscopic level, the mechanisms by which the plant actively changes its natural curvature
and bend are still a matter of debate (von Guttenberg 1925, Lloyd 1942, Hill & Findlay 1981,
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1.0
0.5
t (s)
0.02
0.5
0.3 0.5 0.7 0.9 1.1
0.04
0.1
0.1
Local mean
1
curvature m (mm )
t = 0.04 s
0.3
0.5
0.7
t (s)
0.9
1.1
e
Trapdoor
Bladder
Trapdoor
0.5 mm
Threshold
Slow
deflation
0.5 mm
f
Fast
suction
Figure 10
Snap buckling in carnivorous plants: (ac) Venus flytrap and (df ) bladderworts. (a) Venus flytrap in the (right panel ) open and (left
panel ) closed state. (b) Dynamic sequence of the leaf closure measured using three-dimensional reconstruction. (c) The spatially
averaged mean curvature m (blue) and the spatially averaged Gaussian curvature g (red ) as a function of time (the trap was triggered at
t = 0). The solid line corresponds to the poroelastic theoretical model. (d ) Sketch of a bladderworts bladder (side view) and top view
of Utricularia inflata in the deflated ready-to-catch state and just after triggering. (e) Inversion of the trapdoor and buckling of the
median door axis visualized by light sheet fluorescence microscopy. ( f ) Numerical simulation of the trapdoor opening. Panels ac taken
from Forterre et al. (2005) and panels df from Vincent et al. (2011).
Williams & Bennett 1982, Hodick & Sievers 1989, Volkov et al. 2008). Direct measurements of
the cell turgor pressure using pressure-probe techniques could provide a powerful tool to test the
hypotheses put forward (Colombani & Forterre 2011).
Cell pressure probe:
measures the turgor
pressure in single plant
cells by means of a
microcapillary
connected to a
pressure gauge
468
4.1.2. Bladderworts. Another nice example of plant movement involving the snapping of an
elastic shell is provided by the bladderworts (Utricularia).The bladderworts represent a large and
widely distributed genus of rootless semi-aquatic plants that circumvent nutrient shortages by
catching tiny creatures (microorganisms, small arthropods) in water or on swampy ground (Lloyd
1942, Juniper et al. 1989) (Figure 10d ). The traps consist of small (0.55-mm) bladders filled
with water and closed by a trapdoor. Capture is based on a suction mechanism (Figure 10d ).
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During a slow initial phase, water is pumped outside the bladder so that elastic energy is stored
in the trap body as it flattens and curves inward, which results in a decrease of water pressure in
the trap (pressure difference !P = 1015 kPa) (Sydenham & Findlay 1973, Sasago & Sibaoka
1985, Singh et al. 2011). When the prey stimulates the trigger hairs located at the base of the
trapdoor, the trapdoor suddenly opens inward, and the stored elastic energy in the bladder is
rapidly converted into kinetic energy as water is sucked inside the bladder together with the prey.
The whole trapping sequence lasts approximately 3 ms, with a suction phase of only 0.5 ms (Singh
et al. 2011, Vincent et al. 2011). This timescale may be understood using a simple spring/mass
argument, in which the spring stiffness is related to the trap body elasticity and the mass is given
by the volume of displaced water (Vincent et al. 2011).
The opening mechanism of the trapdoor itself has been partly unveiled in a recent study
(Vincent et al. 2011) (Figure 10e, f ). In the set condition, the trapdoor has a is a shallow dome
whose convex face is facing outward, thereby resisting the pressure difference across it much like
a stone arch. Triggering induces a buckling transition in the trapdoor, which rapidly reverses its
curvature from convex to concave. In this new configuration, the door is no longer able to sustain
the pressure difference and rapidly swings inward. As for the Venus flytrap, the mechanism by
which the buckling onset is reached is not fully elucidated. However, it is interesting to note
that, without any prey, the trap fires and resets periodically, which could be the signature of a
spontaneous buckling once the pressure drop reaches a critical threshold (Vincent et al. 2011).
4.2. Cavitation Catapults and Squirt Guns

Some of the fastest movements on record involve a relatively slow storage of elastic energy within
cell walls and the rapid release of this energy by some sort of fracture. The squirt gun of the
fungus Pilobolus is one elegant example (Figure 11) (Yafetto et al. 2008). Morphologically, Pilobolus resembles Phycomyces discussed in Section 3.1. As in Phycomyces, the long sporangiophore
supports a terminal sporangium that must be dispersed (Figure 11a). The distal end of the stalk
is swollen, and its wall is endowed with great elasticity. While the terminal sporangium matures,
the stalk cell below starts swelling and building elastic energy. Although the pressure of 0.55 MPa
Sporangium
t=0
t = 40 s
t = 80 s
t = 120 s
t = 160 s
t = 200 s
1 mm
Annulus
Spore
Stalk
cell
100 m
Figure 11
Squirt guns and water cohesion catapults for the dispersal of spores. (a) The Pilobolus sporangiophore comprises a terminal sporangium
filled with spores (black) and is supported by a large stalk cell that stores elastic energy in its wall (blue). (b) The first 200 s of the
ejection. Note the collapse and recoil of the stalk cell as it squirts out its cytoplasmic content. (c) Spore ejection in the fern
leptosporangium. A row of specialized cells known as the annulus is the motor of the catapult. Water loss by the annulus forces the
lateral walls of the annular cells to approach each other, leading to an inversion of the sporangium. The water tension that builds in the
annular cells is formidable (as much as 30 MPa) and will ultimately lead to cavitation of one cell, setting a chain reaction across the
annulus. At this point, the sporangium shuts back into its closed position, releasing the spores in the process.
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(Yafetto et al. 2008) is not exceptionally high, the stresses it generates in the wall are (>5.5 MPa
or 55 bars). The concomitant increase in wall stresses and the weakening of the contact region
between the stalk and sporangium lead to the fracture of the wall and the explosive release of the
sporangium in approximately 0.05 ms. Here the characteristic time for the ejection is likely set by
the inertial time required to accelerate the water contained in the stalk (Figure 11b).
One of the most elegant trigger mechanisms for this class of fast motions relies on the cohesive
property of water (Koller & Scheckler 1986). The tensile strength of a water column at room
temperature exceeds 26 MPa (Briggs 1950), providing ample room for energy storage and release
once cavitation occurs. A number of organisms use the coupling of water volume changes and
elastic storage to achieve motion (King 1944, Hovenkamp et al. 2009). The best-studied example
is the fern leptosporangium (Figure 11c). The slow opening of the sporangium that contains the
spores comes from the bending of the annulus, a ring-shaped organ made of a single row of cuboid
cells (King 1944). Upon exposure to a dry environment, these cells lose water and thus decrease
their volume. Volume reduction is converted into bending energy because the cells walls have
a unique U-shape, thin on one side and thick on the other (Figure 11c). This slow backward
bending builds elastic strain within the annulus walls that is balanced by a high negative pressure
within the annulus cells. At a critical pressure of approximately 35 MPa (Renner 1915, Ursprung
1915), cavitation occurs in the cells, causing a rapid closure of the sporangium that launches the
spores into the air.
Other examples abound, in particular the wide range of explosive seed pods that store elastic
energy as they dry until a fracture propagates along a predetermined path, thus catapulting the
seeds (Swaine & Beer 1977). Many of these systems have minimal water content when triggered
and come closest to the ultimate physical limit for fast motion, that set by the speed of elastic
waves within solids (see Figure 5b) (Skotheim & Mahadevan 2005).
5. RELATED FLUID MECHANICS PHENOMENA

5.1. Surface TensionDriven Movements: Propulsion of Fungal Spores
The Basidiomycetes, a large class of fungi that includes the generic white mushroom found in
supermarkets, have evolved what may be the most economical mechanism to generate movement.
These mushrooms actively disperse their spores using the surface tension of water as their only
source of energy (Buller 1909, Ingold 1939, Turner & Webster 1991). The spores, known as ballistospores, are borne by the gills of mushroom caps and must be ejected from the gill surface before
being picked up by air currents (Figure 12a). The ejection process begins with the condensation
of a water drop, known as Bullers drop, at the proximal end of the spore and the growth of a thin
film of water on the spore (Figure 12b,c). When the drop reaches a critical size, it touches the
water film on the spore surface. At this point, the surface tension quickly pulls the drop onto the
spore, thus creating the necessary momentum to detach the spore from the supporting sterigma
and to set it in motion.
The energy available to eject the spore comes from the difference in surface energy before and
after the fusion of Bullers drop: !E p = 4 R2D (1 R D /R*D ), where is the energy associated
with the liquid-vapor interface, and RD and R*D are the radii of the drop before and after fusion,
respectively (Noblin et al. 2009). Assuming that all the freed energy serves to accelerate the drop
and using the conservation of momentum between the drop and spore, we predict a spore velocity
of 1.2 m s1 , whereas the observed velocity is 0.8 m s1 . The predicted velocity is surprisingly
accurate given that energy loss has not been taken into account in the model. Finally, it is possible
to compute the time required for ejection by considering the magnitude of the capillary force
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1 cm
Gill
Spore
Basidium
1 cm
10 m
1 cm
0 s
c
Spore
4 s
Drop
growth
Early
coalescence
8 s
12 s
Late
coalescence
Ejection
R'D
Film
+
R
+D
+
+
Capture rate (%)
f 100
80
60
40
20
0
Flies
Ants
0.1
1.0
10.0
Deborah number, De = /
Drop
Figure 12
(ac) Surface-tension propulsion of fungal spores. (df ) Viscoelastic trap in pitcher plants. (a) Section of a typical mushroom cap
showing the gills and the location of the spore-bearing basidia (insert). The approximate trajectory of the spore is shown as a dotted
line. (b) Early stages of spore discharge in Auricularia auricula [250,000 frames per second (fps) and 1-s exposure]. (c) Four stages of
ballistospore ejection, from drop growth and coalescence to ejection. The radius of the drop before (RD ) and after (R* D ) coalescence is
indicated. The circle-and-cross symbol indicates the position of the spores center of mass during the ejection process. (d ) Pitcher of
Nepenthes rafflesiana (Brunei). (e) Dynamical sequence of a fly (Calliphora vomitoria) after falling into the digestive fluid, showing a
viscoelastic liquid filament attached to its leg (arrows). Time between frames is 80 ms. ( f ) Capture rate of insects as a function of the
Deborah number, defined as the ratio of the fluid elastic relaxation time to the typical half-period of the swimming stroke of insects in
the fluid . Panels ac taken from Noblin et al. (2009) and panels df from Gaume & Forterre (2007).
R D , the inertia of the droplet, and the distance L the droplet must travel:
c a p =
L3
"1/2
(9)
where L 2R D , and is the droplet density. We find that the ejection takes less than 1 s,
making this movement the fastest to be completed.
5.2. Viscoelastic Trap in Carnivorous Pitcher Plants

As shown above, moving fast is an increasingly difficult challenge in plants as the system size
increases, and unsurprisingly the fastest motions have been found within the smallest systems.
However, there are plenty of other strategies for the smart plant to cope with a mobile world. One
strategy is the use of complex fluids, as recently discovered in some carnivorous plants.
The tropical pitcher plants of the genus Nepenthes (Figure 12d ) are among the most successful
carnivorous plants in terms of prey spectra and the amount of insects trapped ( Juniper et al.
1989). They have long been thought to function as simple pitfall traps relying on slippery surfaces
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that decrease insect adhesion (Gaume et al. 2004, Gorb et al. 2005) and wettable surfaces that
cause insect aquaplaning (Bohn & Federle 2004). Recently, the digestive liquid contained inside
the pitcher has been shown to play a crucial role in the trapping mechanism as well (Gaume &
Forterre 2007, Bonhomme et al. 2011). High-speed videos of flies thrown on the free surface of
the digestive liquid reveal that they are unable to escape from the fluid, their legs being tethered
by sticky viscoelastic filaments typical of biological fluids composed of long-chain polymers such
as mucus or saliva (Figure 12e). Remarkably, the trapping efficiency of the digestive liquid remain
high even when the fluid is highly diluted by water, a property of great adaptive significance for
these tropical plants, which are often subjected to heavy rainfalls.
Measurements of the thinning dynamics of the liquid filaments [capillary break-up rheometry
(Rodd et al. 2005)] show that this unique trapping property comes from the high viscoelasticity
and apparent elongational viscosity of the digestive liquid, which may be more than 105 that of
water. The capture/escape transition is actually controlled by the Deborah number De, defined as
the ratio between the elastic relaxation time of the liquid and the typical period of insect swimming
in the pool (Figure 12f ). Capture occurs for De > 1, when the elastic forces created by insect
movements have no time to relax (Gaume & Forterre 2007). This study shows how the use of
complex fluids provides an alternative to motion in some cases. The same strategy is likely applied
at a smaller scale in other carnivorous plants such as Drosera (sundews) or Pinguicula (butterworts),
which have sticky leaves to immobilize their prey, before engulfing them slowly.
6. CONCLUSION
Motility in plants is made possible by a few broad mechanisms that are variations on a common
themethe interaction of water with a solid phase made of the cell walls. Although water-driven
movements may lack the rapid temporal control of muscular movements, they offer some clear
advantages. A comparison with the peak force generated by animal tissue is illuminating. Tissues
specialized for force generation such as muscle will at best produce a tensile stress of 0.3 MPa
(Bray 2001). These stress levels are reached at the cost of filling muscle cells with cytoskeletal
proteins and motors. In contrast, plants can achieve a much wider range of stresses (Figure 2a),
both tensile and compressive, without the need for extensive cellular specialization beyond the
presence of the cell wall. Therefore, in terms of versatility and design potential, the plants strategy
to generate movement is certainly appealing. Finally, the sole reliance on water and cellulose, the
most abundant biopolymer on Earth, offers a clear and cheap path for biomimetic designs.
In this review, we mostly focus on the physical mechanisms behind plant motion and only
skim over the physiology and molecular signaling associated with these processes. Much remains
to be done to fill the gap between the physical and biological approaches. Future efforts should
combine tools and concepts from both mechanics and modern biology to provide a comprehensive
description of these nonmuscular machines.
SUMMARY POINTS
1. From the slow growth of shoots and roots to the rapid snapping of carnivorous plants and
the explosive rupture of seed pods, the characteristic times of plant motion span almost
10 orders of magnitude.
2. Plants and other walled organisms such as fungi are hydraulic machines that rely on
the high differential hydrostatic pressure supported by their thin and stiff cell walls to
produce movements.
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3. At the cellular level, hydraulic movements (reversible swelling/shrinking, irreversible

growth) are driven by osmotic or humidity gradients. The material properties of cell walls
(elasticity, plasticity, and anisotropy) and cell geometry set the timescale and amplitude
of motion.
4. Growth (irreversible) movements are mainly controlled by the rheological properties of
the cell wall, which is a complex yield-stress fluid under tight molecular and physiological
control.
5. The poroelastic timescale of water diffusion at the cellular and tissue level constrains
the maximal speed of purely hydraulic movements and provides a physical basis for the
classification of motion in plants and other walled organisms.
6. To overcome the poroelastic limit and generate faster movements, plants couple passive
or active water transport (osmosis, evaporation) to mechanical instabilities (snap buckling,
cavitation, fracture).
7. At the micrometer scale, the surface tension of water can serve as an energy store and
trigger mechanism, without the need of an elastic solid phase. This mechanism is perhaps
the purest strategy to power locomotion and allows basidiomycete fungi to disperse
millions of spores cheaply.
8. Complex viscoelastic fluids that can ensnare insects offer an alternative to motion in
carnivorous plants.
FUTURE ISSUES
1. Plant movements result from the interplay between water transport and cell wall deformation and thus offer a wealth of opportunities for studies of fluid-structure interactions.
An investigation of poroelasticity in complex materials mimicking plant tissues (porous
cellular materials, slender geometries) would help us better understand the dynamics and
constraints on plant movements. Coupling with other processes such as elasto-capillarity,
cavitation, and evaporation should be investigated as well.
2. An additional feature of living systems is growth. The constitutive modeling of complex
fluids that add mass and remodel as they deform is an active area of research. Better
understanding the mechanical coupling between growth, osmotic pressure, and water
transport in cellular tissues is a great challenge.
3. Although the kinematics and dynamics of plant motion are well understood at a macroscopic level, the associated mechanical processes have been much less explored at the
cellular and tissue level. There is a need for quantitative physics and mechanics measurements in cells and tissues (noninvasive flow visualization, cell force and pressure
measurements) to better understand the link between the biological signals (osmotic
gradients, action potential) and the mechanical responses (change in turgor pressure, cell
wall softening) in plant motion.
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4. Finally, movements in plants at the molecular level are poorly understood. Future studies
should tackle the constraints brought by these movements on the timescale of important
physiological processes such as flow in water channels and rapid ion transport across cell
membranes. In particular, it is still not clear whether the contractile properties of the
actin and microtubule cytoskeleton have to be ruled out completely for plant movements
(Morillon et al. 2001, Kanzawa et al. 2006).
DISCLOSURE STATEMENT
The authors are not aware of any biases that might be perceived as affecting the objectivity of this
review.
ACKNOWLEDGMENTS
We thank J. Skotheim and P. Marmottant for supplying figures and data. Y.F. thanks the Agence
Nationale pour la Recherche for financial support. J.D. thanks the Harvard Center for Nanoscale
Systems for use of their microscope facility and the Materials Research Science and Engineering
Center for financial support.
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RELATED RESOURCES
Web sites on plant motion: http://plantsinmotion.bio.indiana.edu, http://www.snv.jussieu.
fr/bmedia/mouvements/index.htm (in French)
DVD on plant motion: Attenborough D. 1995. The Private Life of Plants. London: BBC. 390 min.
Peters Savage Garden: http://www.exploratorium.edu/gardening/feed/peter_savage_
garden/
Charles Darwins The Power of Movement in Plants: http://darwin-online.org.uk/
EditorialIntroductions/Freeman_ThePowerofMovementinPlants.html
Movie of nematode-trapping fungi: http://archive.microbelibrary.org/ASMOnly/Details.asp?
ID=1769
Movie of bladderworts (Utricularia): http://www.youtube.com/watch?v=Zb_SLZFsMyQ
Movie of the fungus Pilobolus: http://www.plantpath.cornell.edu/PhotoLab/TimeLapse2/
Pilobolus1_crop1_FC.html
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FL44CH19-Forterre

Annu. Rev. Fluid Mech. 2012. 44:45378

The Annual Review of Fluid Mechanics is online at

plant biomechanics, osmotic pressure, growth, poroelasticity, instability,

This articles doi:

2.1. Plant Cell and Tissue Structure

2.2. Water: The Prime Mover

Water potential: the

2.3. Material Properties of the Plant Cell Wall

Cell length L (m)

Relative volume (%)

0.1 0.2 0.3 0.4 0.5 0.6 0.7

Cell pressure P (MPa)

Percent original dL/dt

Percent original pressure

2.4. Timescales of Plant Movements

Change in tissue length (%)

Cell turgor pressure P (MPa)

Giant algal cell (Chara)

Stop air flow

Fastest cell swelling cell

Fastest tissue swelling p

Cell radius R (m)

Tissue size L (m)

elastic motion) el = L /E, with = 1,000 kg m3 and E = 10 MPa.

3. HYDRAULIC MOVEMENTS IN PLANTS

3.2. Actuation Driven by Osmotic Gradients

Stomatal half-aperture (m)

Guard cell turgor pressure P (MPa)

Proton signal (a.u.)

3.3. Passive Actuation Driven by Humidity Gradients

3.4. Hygroscopic Movements

4. BEYOND WATER DIFFUSION: INSTABILITY

4.1. Snap-Buckling Instabilities

4.2. Cavitation Catapults and Squirt Guns

5. RELATED FLUID MECHANICS PHENOMENA

Capture rate (%)

5.2. Viscoelastic Trap in Carnivorous Pitcher Plants

3. At the cellular level, hydraulic movements (reversible swelling/shrinking, irreversible

www.annualreviews.org The Role of Water in Plant Movements

Wiss. Bot. 56:61767

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