Review

Research review
Blackwell Publishing Ltd

Waving and skewing: how gravity and

the surface of growth media affect root
development in Arabidopsis

Author for correspondence: Michele Oliva and Christophe Dunand

Christophe Dunand
Tel: +41 22 379 30 12 Laboratory of Plant Physiology, University of Geneva, Quai Ernest-Ansermet 30, CH-1211 Geneva 4,
Fax: +41 22 379 30 17 Switzerland
Email: Christophe.dunand@bioveg.unige.ch
Received: 11 April 2007
Accepted: 14 June 2007

Summary

Key words: cell file rotation, friction,
gravity, microtubules, root skewing and
waving.
Arabidopsis seedlings growing on inclined agar surfaces exhibit characteristic
root behaviours called ‘waving’ and ‘skewing’: the former consists of a series of
undulations, whereas the latter is a deviation from the direction of gravity. Even
though the precise basis of these growth patterns is not well understood, both
gravity and the contact between the medium and the root are considered to be the
major players that result in these processes. The influence of these forces on root
surface-dependent behaviours can be verified by growing seedlings at different gel
pitches: plants growing on vertical plates present roots with slight waving and skewing
when compared with seedlings grown on plates held at minor angles of < 90°.
However, other factors are thought to modulate root growth on agar; for instance,
it has been demonstrated that the presence and concentration of certain compounds
in the medium (such as sucrose) and of drugs able to modify the plant cell cytoskeleton
also affect skewing and waving. The recent discovery of an active role of ethylene
on surface-dependent root behaviour, and the finding of new mutants showing
anomalous growth, pave the way for a more detailed description of these phenomena.

New Phytologist (2007) 176: 37–43

© The Authors (2007). Journal compilation © New Phytologist (2007)

doi: 10.1111/j.1469-8137.2007.02184.x

whereas phototropism allows the root to escape light and

Introduction
Plant roots are very sophisticated sensors that are able to
perceive environmental cues and change their growth
accordingly: a correctly functioning root sensory feedback
mechanism, in fact, allows the plant to gain advantages and,
in some cases, to avoid death. For instance, hydrotropism
permits the root to orientate towards high water potentials,
appropriate for sustaining plant growth (Eapen et al., 2005),
permits the aerial part to follow the source of photons
(Kimura & Kagawa, 2006). However, the root response
studied in greatest detail is definitely gravitropism, a growth
re-orientation along the gravitational axis towards the earth
center (Blancaflor & Masson, 2003). The first studies on
gravitropism were almost only phenotypical descriptions
(Darwin & Darwin, 1880), but the rapid progress in plant
science research has led to a better comprehension of the

www.newphytologist.org 37
38 Review Research review
molecular mechanisms at the basis of this movement. Even
though the Cholodny-Went theory (Muday, 2001) is, in
general, still accepted, new discoveries have highlighted the
importance of several players other than auxin: Ca2+ (Lee
et al., 1984), reactive oxygen species (ROS; Joo et al., 2005)
and ethylene (Buer et al., 2006; Edelmann & Roth, 2006)
seem to be involved in the differential cellular growth leading
to gravitropic curvature. Recently, the extensive use of in vitro
growth conditions has focused physiologists on particular
movements exerted by Arabidopsis on agar medium: seedlings
grown on vertical plates present roots with a characteristic
skewing from the vertical, which is also known as skewing or
slanting (Simmons et al., 1995), and a sinusoidal pattern
named waving (Okada & Shimura, 1990). At first a possible
combination of gravity and touch-induced root tip rotation
was proposed to influence these root growth patterns (Okada
& Shimura, 1990), but recent data underline also a direct
role of root–gel interaction (Thompson & Holbrook, 2004).
There is new compelling evidence that an exhaustive
description of the mechanisms leading to skewing and waving
should also include other factors, such as the availability of
determinate components (Buer et al., 2003). The correlation
of surface-dependent movements with different plant
research fields (for example root growth, cell cytoskeleton
arrangements and hormone action) make this topic extremely
complex and difficult to investigate, although these recent
discoveries have attracted the attention of more researchers.
This review will focus on the latest findings on Arabidopsis
root surface-dependent movements, including the discoveries
of new factors and proteins controlling waving and skewing.
(In the review, the names of the genes appear only as
abbreviations; the complete names and descriptions can be
found in Supplementary material Table S1).
Skewing and waving: facts and theories
Arabidopsis primary roots growing vertically on agar plates
show a tendency to deviate from a strict gravitational
direction (Simmons et al., 1995). It has been demonstrated
that the skewing in the ecotypes most commonly studied is
always to the left (if observed from the lid of the plate) but,
interestingly, the amplitude of the slanting angle differs
among the accessions: Columbia roots grow with a slight
skewing, whereas Landsberg and Wassilewskija have a larger
deviation (Rutherford & Masson, 1996). The magnitude of
the angle also seems to be related to the age of the seedlings
(Rutherford & Masson, 1996; Fig. 1). A direct involvement
of light in this process (Oyama et al., 1997) has been ruled out
and research focused on the known characteristic of roots to
rotate around their axes (twisting; Maher & Martindale,
1980). Indeed, it was observed that a rotation of the root
tip, manifested in the epidermal cell file rotation (CFR),
accompanied slanting (Yuen et al., 2005). This CFR, considered
left-handed in left-slanting roots by Hashimoto (2002), is
New Phytologist (2007) 176: 37–43 www.newphytologist.org © The Authors (2007). Journal compilation © New Phytologist (2007)
Fig. 1 Skewing process. (a) Arabidopsis ecotype Landsberg seedlings
grow on inclined agar surfaces by assuming a skewing pattern.
(b) The skewing angle is the most commonly used parameter to
measure the root slant.
enhanced in ecotypes showing a larger skewing-angle and is
weaker in Columbia. This hypothesis describes slanting as the
result of touch stimuli and twisting of Arabidopsis roots.
When the root tip hits the agar surface, it experiences a touch
stress and changes direction, then it hits the agar again and
changes direction, and so on. The intrinsic left-handedness of
the root would lead the tip to draw complete half-cycles to the
left and aborted cycles to the right: the total result would be a
skewing to the left (Migliaccio & Piconese, 2001). This
theory fits with the observation that mutants showing right-
handed growth also have a slanting towards the right, but this
seems to be in contrast with the recent discovery that CFR is
unnecessary for skewing (Buer et al., 2003).
When growing on vertical agar gels, Arabidopsis roots also
exhibit an oscillatory pattern called waving (Fig. 2a). As
shown in Fig. 2(b), this movement is characterized by two
components: frequency and amplitude. The former is the
distance between two contiguous peaks, whereas the latter is
the distance between a peak and the root axis. However, to
estimate waving compression, the angle formed by a tangent
traced on the root surface and an ideal root axis is also con-
sidered (Rutherford et al., 1998). Since its discovery, different
models have been proposed to explain this growth pattern.
The observation of wavy behaviour in plants growing on plates
angled at 45° led Okada & Shimura (1990) to hypothesize
that under these conditions roots undergo both a touch-
experience and a gravity influence. Thus, the root would grow
downwards owing to a positive gravitropic response and to a
negative phototropic response; the formation of turns would
be the result of repetitive touches between the tip and the
impenetrable agar. These touch stimulations would lead to a
re-orientation of root growth towards the opposite direction
and to a change in the handedness of twisting. The initial
discovery of mutants affected in both waving and auxin

Fig. 2 Waving process. Arabidopsis ecotype Columbia seedlings grow
on inclined plates with a waving pattern (a). (b) Parameters describing
waving: a, amplitude; b, wave frequency; c, wave tangent line (WTL).
transport suggested a prominent role for this hormone in the
establishment of waving. The subsequent findings of other
mutants also indicated a possible involvement of circumnuta-
tion (Simmons et al., 1995), light (Oyama et al., 1997) and
humidity gradients (Takahashi et al., 2002) on this growth
pattern. A recent idea considers the formation of waves as the
result of both gravity and root–gel interaction (Thompson &
Holbrook, 2004): the root would grow laterally because it was
unable to penetrate the agar and gravity would correct this
trajectory by pushing it to the other direction. This model is
consistent with the finding that Arabidopsis seedlings grow
almost vertically in plates kept at 90° (in this case the root tip
does not push against the agar) and present a more marked
wavy behaviour in plates held at angles of less than 90° (the
tip tries in vain to penetrate the medium) (Mullen et al.,
1998). Another possibility is that the wave turns are the result
of an anisotropic cellular growth, rather than the consequence
of a change of root twisting: a circadian clock would control
the formation of waves (Buer et al., 2003).
An open debate exists regarding any correlation between
skewing and waving: a hypothesis that tries to combine the
two behaviours in an unifying model (Migliaccio & Piconese,
2001) clashes with the opinion that slanting and waving are
two uncoupled processes, even though both depend on twisting
and/or on anisotropic cell growth (Buer et al., 2003). The
existence of mutations affecting skewing, but not waving
(and vice versa) (Supplementary material Table S1), led us to
consider that different processes regulate the two behaviours.
Another root growth aspect to highlight is that roots growing
on horizontal plates lose their slanting and waving patterns
and acquire a clockwise coiling-behaviour; an explanation of
this phenomenon was correlated to the intrinsic left-handed
twisting in Arabidopsis roots (Hashimoto, 2002).
© The Authors (2007). Journal compilation © New Phytologist (2007) www.newphytologist.org
Research review Review 39
Nutrients and cytoskeleton-affecting drugs modulate
skewing and waving
Since their discovery, it was clear that surface-dependent
behaviours were heavily affected also by slight changes in the
properties of the medium. For instance, not only the slope,
but also the hardness of the agar medium, is thought to
influence the skewing (Rutherford & Masson, 1996): roots
growing on 0.8 or 1.5% agar bend more than roots growing
on a harder medium (3%). Conversely, softer media cause the
slanting angle to decrease: in this case, the surface probably
exerts a minor resistance to tip penetration. Root growth is
also affected by the concentration of some nutrients in the
medium. Sucrose (Suc), for example, reduces waving when
seedlings are grown on medium lacking nutrients, but it has
no effect on root growth on Murashige and Skoog nutrients
(Murashige & Skoog, 1962). On the other hand, skewing is
enhanced in the presence of Suc, but decreased in its absence.
Ethylene also affects root growth, reducing skewing and
promoting waving at low Suc concentrations (Buer et al.,
2003). The way that Suc and ethylene affect growth patterns
is not well understood, but the discovery that root responses
to Suc concentration are ethylene dependent suggests that the
situation is very complex. In addition, nitrogen and the gel
polymer composition are also thought to influence root
behaviour (Buer et al., 2000).
Another aspect to consider is the effect of some cytoskeleton-
affecting drugs on waving and skewing; indeed, as mentioned
before, root-surface movements are probably closely correlated
to epidermal cell elongation (the basis of CFR) and thus to
the organization of the cytoskeleton. It is known that the
orientation of microtubules (MTs) in the cytoplasm influences
the deposition of cellulose microfibrils in the cell wall. In
particular, cellulose microfibrils co-align with MTs and
establish the direction of cell elongation: if the microfibrils
are all deposed in the same orientation, the cell will expand
along an axis perpendicular to the cellulose direction (Baskin,
2001). MT-depolymerizing molecules, such as propyzamide
and oryzalin, or MT-stabilizing compounds (e.g. taxol),
provoke pronounced skewing angles (Furutani et al., 2000;
Yuen et al ., 2005). These compounds seem to distort
epidermal cells and thus create a strong left-handed helical
growth because of their ability to re-orient MTs to right-
handed helices. However, the utilization of these drugs
sometimes produces strange or unwanted effects; for taxol it
has been reported that there can be a reduction of root
growth, whereas high concentrations of the pesticide oryzalin
can suppress both waving and skewing (Sedbrook et al.,
2004).
Genes implicated in skewing and waving
In the last decade, several genes affecting root behaviour on
the surface of growth medium have been discovered. The
New Phytologist (2007) 176: 37–43
40 Review Research review
screening of collections of transgenic lines germinated on
inclined plates has been the approach most often used to
identify seedlings with particular root features. However, in
some cases, mutants with aberrant root growth patterns were
discovered as secondary phenotypes by researchers focused on
the development of other plant organs. This occurrence is not
so surprising, given that the majority of mutants with strange
waving and skewing also present other anomalous traits
(Supplementary material Table S1). Mutants affected in root
slanting can be grouped into three classes. The first class
includes seedlings with an exacerbated skewing to the left
(compared with the control); the second group includes
mutants that grow straight; and the third category comprises
seedlings that slant towards the right. Among the first
discovered slanting mutants, sku1 and sku2 (Rutherford &
Masson, 1996) presented a marked bend to the left on tilted
plates; even though more than 10 yr have elapsed since they
were discovered, the proteins encoded by the SKU1 and
SKU2 genes still have an unknown function. Other genes
showing some implications in root skewing and waving
processes have been characterized and seem to perform very
different functions (Supplementary material Table S1). For
example, the mutation in a gene encoding a basic leucine
zipper transcription factor (HY5) leads to exaggeration of the
left-slant (Oyama et al., 1997). Although the participation of
this protein in auxin signalling could indicate its involvement
in gravity sensing, its function in the red-light-guided
morphogenesis (Molas et al., 2006) could also suggest an
interesting connection between light perception pathways
and the control of root growth on media. Recently, attention
has been mainly directed to genes coding for proteins
correlated to cytoskeleton stability; in fact, cytoskeleton
re-arrangements could be important processes for the
establishment of CFR and twisting. Lefty1 and lefty2 are two
mutants showing a marked root skewing to the left; more
attentive analyses showed that the mutations in these loci also
cause a right-handed organization of cortical MTs in the
epidermal cells of the root elongation zone (Thitamadee et al.,
2002). Interestingly, both LEFTY loci encode α-tubulin
isoforms: α-tubulin 6 (TUA6) and α-tubulin 4 (TUA4) for
lefty1 and lefty2, respectively. The lefty root phenotype is very
similar to that caused by cytoskeleton-affecting drugs and is
probably the result of a different conformation of MT
filament assembly (Abe et al., 2004). This hypothesis explains
the severe impact of these mutations on whole plant growth;
lefty mutants are shorter than controls and exhibit left-handed
growth in hypocotyls and flower petals. In addition, the double
mutant lefty1/lefty2, showing completely disordered MT
arrays, also has aberrant trichome growth (Abe et al., 2004).
Amazingly, mutations in SPR1 and SPR2, two other genes
related to cytoskeleton assembly, provoke right skewing. Under
standard growth conditions, spr1 exhibits a very marked
slanting, if compared with wildtype (WT), and a pronounced
right-handed helical growth of the epidermal cells. On the
New Phytologist (2007) 176: 37–43 www.newphytologist.org © The Authors (2007). Journal compilation © New Phytologist (2007)
other hand, spr2 shows only a slight right-skewing (Furutani
et al., 2000). Recent studies established that SPR1 is a small
protein (12 kDa) with a rod-forming repeat sequence,
typical of some proteins able to interact with actin. Although
its function is not yet known, SPR1 localization at the plus
ends of cortical MTs suggests a role in protein recruitment
to this site (Sedbrook et al., 2004). Mutations affecting
waving are more difficult to classify because there are
several parameters to analyze. Even so, mutants with a lack
of waving or with aberrant waving can be found. In the
latter case, seedlings show roots with anomalous amplitude
and/or wavelength of waving. Compared with skewing, the
proteins affected in waving mutants seem to have very
different functions. The first mutants discovered were
almost all affected in the gravitropic response (Okada &
Shimura, 1990); among these, the nonwaving mutant pin2
is not susceptible to gravity. Interestingly, it has been
demonstrated that PIN2 is a gene that encodes an auxin
efflux carrier. It is localized at the base of cortical cells and
on the upper part of epidermal and lateral root cap cells
(Mullen et al., 1998). As the Cholodny-Went hypothesis
explains, auxin localization plays a fundamental role in the
root gravitropic response: the presence of a nonfunctional
auxin transporter could provoke alteration of the hormone
flux and, as a consequence, an anomalous response to gravity
leading to a reduced waving phenomenon. In addition,
recent data report an AUX1-dependent formation of lateral
roots on the external part of waving curves (De Smet et al.,
2007). As AUX1 encodes an auxin influx carrier whose
mutation leads to waving suppression (Okada & Shimura,
1990), it is likely that gravitropism, waving and lateral root
formation are closely related processes. The correlation
between auxin and waving has been confirmed by treating
growing seedlings with naphtylphthalamic acid (NPA), an
auxin transport inhibitor that suppresses waving (Rashotte
et al., 2000). Furthermore, several genes not involved in
gravity responses have been found. For instance, WAV2
encodes a protein belonging to the BUD EMERGENCE 46
family and possesses an α/β-hydrolase domain (Mochizuki
et al., 2005); and the mutant wav2-1 shows a compressed
wavy behaviour on a tilted agar surface. The localization of
the expressed protein at the membrane suggests a possible
role in the modulation of morphogenic determinants
(such as GDP exchange factors (GEFs)), even though the
involvement of the gene in root rotation supports the idea
of an interaction with MTs. WAG1 and WAG2, the genes
discovered most recently to affect waving, encode protein
kinases (Santner & Watson, 2006). Surprisingly, the phenotype
of the double mutant wag1/wag2 exhibits compressed waves
– loss of WAG1 affects mainly wavelength whereas lack of
WAG2 affects wave amplitude. The function of these genes
in waving formation is not known; however, different
experiments indicate a role in auxin transport, probably
related to gravity sensing.
 Research review Review 41

In search of a pathway
To date, a satisfying scenario describing the molecular and
cellular processes that generate skewing and waving has not
been produced. Probably the main reason for this resides in
the fact that the major discoveries in this field are related to the
finding of single genes; thus, we are unsure of the temporal
succession in which these genes are expressed and least of
all about the eventual interactions between such proteins.
However, in general, two working models can be outlined for
waving and skewing (Fig. 3). Our opinion suggests that
several steps follow the perception of the stimulus (gravity or
touch): re-arrangement of the cytoskeleton (CSK) and the cell
wall (CW) in the root would cause a change of CFR
handedness or an asymmetrical flank growth (Fig. 3a). The
root growth would follow the new direction until another
physical stimulus was received. If we consider Thompson
and Holbrook’s theory for waving as valid (Thompson &
Holbrook, 2004), the proteins involved in this process should
belong to two different complex machineries: the first is
related to the perception of gravity, and the second responds
to this gravitational sensing leading to the formation of turns;
genes such as PIN2 could encode proteins of the first group,
whereas WAG1 and WAV2 could be important players in the
signalling, culminating in MT re-arrangements in epidermal
cells. In turn, these cytoskeleton modifications would
lead to the often-seen change of CFR (as an alternative to
asymmetrical growth) on the wave curves. Ethylene could
also modulate waving by affecting the extent of the
curvature. In fact, strong data suggest a role for ethylene,
both in formation of hooks in the shoot apex (Lehman et al.,
1996) and in the establishment of nutations on hypocotyls
(Binder et al., 2006). In the alternative hypothesis describing
waving (Simmons et al., 1995), touching is the driving
force that creates turns: in this case we would expect the
involvement of a ‘touch perception apparatus’ and of a
mechanism that converts the ‘touch input’ to a change in the
cell cytoskeleton.
The generation of skewing is basically thought to depend
both on touch stimulus and on the implicit tendency of the Fig. 3 Models describing the cellular steps leading to the
establishment of waving and skewing. (a) In the Simmons model for
Arabidopsis root tip to grow following helices (always left-
waving, the turn would form after the contact between the root tip
handed in the wild type) (Migliaccio & Piconese, 2001; and the medium (cross-hatched box; Simmons et al., 1995) whereas
Fig. 3b). This complex model is the result of two components: in the recent Thompson & Holbrook hypothesis the main force that
the Simmons pathway for waving and a genetic program to pushes root growth on the opposite direction is gravity (grey box)
determine cell cytoskeleton and wall modifications able to (Thompson & Holbrook, 2004). (b) Migliaccio & Piconese combine
waving and skewing in a unifying vision (Migliaccio & Piconese,
fix a precise handedness in roots. Thus, slanting could be
2001). Ethylene and molecules that affect the cytoskeleton would
included, at least in part, in the vast and complex dimension interfere in one or more steps.
of plant chirality; the establishment of asymmetry in both
plant and animals has always been a cutting-edge topic for
developmental biologists, but a solid theory explaining this
phenomenon is still far from being elucidated. At the molecular
level, genes affecting skewing are mainly involved in the
arrangement of cytoskeleton structure in epidermal cells
(LEFTY1, LEFTY2, SPR1, SPR2 and probably WVD2 are all

© The Authors (2007). Journal compilation © New Phytologist (2007) www.newphytologist.org New Phytologist (2007) 176: 37–43
42 Review Research review
correlated to the formation of MT arrays). This re-arrangement
would lead to the CFR necessary for the formation of the
implicit left-handed pattern. However, some genes seem to
belong to intracellular pathways: perhaps the most exciting
recent finding is cle40, a mutant with enhanced waving and
whose gene is phylogenetically related to the CLE family
(Hobe et al., 2003). CLE40 encodes a secreted protein similar
to CLV3, a ligand that binds the CLV1/CLV2 receptor
complex, an earlier player in the signalling pathway leading
to the down-regulation of WUSCHEL (a gene that fixes the
fate of shoot stem cells; Doerner, 2003). The severely affected
root phenotypes caused by CLE40 misexpression implies
that this protein can influence a number of cell processes in
roots by modulating root stem cell differentiation. This scenario
becomes more complex if we consider the data confirming
a role of light and moisture gradient on modulating waving
and skewing: Takahashi discovered that some mutants affected
in waving and slanting also exhibit a greater response to
humidity (Takahashi et al., 2002), and Oyama found a mutant
affected both in light response and surface movements
(Oyama et al., 1997). Recent work show that plant tropisms
are closely related and could even share parts of their signalling
pathways: hydrotropism is thought to counteract gravitational
responses by degrading the gravity-sensing amyloplasts in
columella cells, whereas light could regulate plant tropisms
both in a positive and a negative way (Iino, 2006). Taken
together, we can interpret that light and moisture gradients
probably do not have a direct role on shaping root growth
patterns, but they can modulate them indirectly by affecting
the response to gravity. In conclusion, even though many
questions about the generation of skewing and waving are still
unanswered, the new exciting progresses in high-throughput
mutant screens – in vivo visualizations of hormone levels
and systems biology analyses – could help the scientific
community to clarify the molecular mechanisms leading to
the establishment of root-surface movements.
Glossary
Differential growth: the process that provokes the formation
of curvatures in hypocotyls or roots after the application of
stimuli (e.g. light, gravity, touch). It is based on the different
growth rate of cells localized in the turn.
Cholodny-Went model (1927): a theory describing root
bending as a result of gravistimulation. In a root placed
horizontally, auxin would localize in the lower side, promot-
ing inhibition of cell growth in the elongation zone. On the
other hand, the low concentration of auxin in the upper side
of the root would provoke extension of the cells.
Acknowledgements
We would like to thank William Broughton for helpful
suggestions and critical reading of the review. This work was
New Phytologist (2007) 176: 37–43 www.newphytologist.org © The Authors (2007). Journal compilation © New Phytologist (2007)
supported by the Swiss National Science Foundation (grant
3100A0-109325).
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Supplementary Material
The following supplementary material is available for this
article online:
Table S1 List of the mutants related to root skewing and
waving
This material is available as part of the online article from:
http://www.blackwell-synergy.com/doi/abs/10.1111/
j.1469-8137.2007.02184.x
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Please note: Blackwell Publishing are not responsible for the
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© The Authors (2007). Journal compilation © New Phytologist (2007) www.newphytologist.org New Phytologist (2007) 176: 37–43