Download Planar polarity of root hair positioning in Arabidopsis

Intercellular Signalling in Plants
Planar polarity of root hair positioning
in Arabidopsis
U. Fischer, Y. Ikeda and M. Grebe1
Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-90183 Umeå, Sweden
Abstract
The co-ordinated polarity of cells within the plane of a single tissue layer (planar polarity) is intensively
studied in animal epithelia but has only recently been systematically analysed in plants. The polar positioning
of hairs in the root epidermis of Arabidopsis thaliana provides an easily accessible system for the functional
dissection of a plant-specific planar polarity. Recently, mutants originally isolated in genetic screens for
defects in root hair morphogenesis and changes in the sensitivity to or the production of the plant hormones
auxin and ethylene have identified players that contribute to polar root hair placement. Here, we summarize
and discuss recent progress in research on polar root hair positioning from studies in Arabidopsis.
Introduction
The co-ordination of cell polarity within the plane of a single
tissue layer is commonly observed in animal epithelia, where
the term planar polarity is frequently used to describe this
phenomenon [1]. For example, the co-ordinate positioning of
wing hairs in Drosophila melanogaster has been successfully
used to genetically dissect the mechanisms underlying planar
polarity formation [1]. Similarly, root hair positioning in the
flowering plant Arabidopsis thaliana provides a system to
study cell polarity and its co-ordination within the plane of
the root epidermal layer [2], where hairs emerge close to the
basal (root tip-oriented) ends of hair-forming cells (trichoblasts) [3,4]. Masucci and Schiefelbein [3] originally noted
that root hair positioning in Arabidopsis is a co-ordinated
event and described mutants, pharmacological and hormonal
treatments affecting this process.
Co-ordinate root hair positioning can be
modulated by auxin and ethylene
In the rhd6 (root hair defective 6) mutant, hairs often emerge
from a more apical position along the trichoblast than in the
wild-type and some trichoblasts initiate more than one hair
from different positions (Figure 1) [3]. These defects can be
partially restored by application of the plant hormone auxin
or ACC (1-aminocyclopropane-1-carboxylic acid), a precursor of the hormone ethylene. In the wild-type, exogenous
application of auxin or ACC induces root hair formation
from a basal-most position. In contrast, a reduction of the responsiveness to auxin in the dominant axr2-1 (auxin resistant
2-1) mutant, or reduced ethylene perception in the dominant
ethylene receptor mutant etr1-1 (ethylene resistant 1-1) causes
the opposite effect, namely an apical shift of root hair position
Key words: Arabidopsis, auxin, co-ordinate polarity, ethylene, planar polarity, root hair.
Abbreviations used: ACC, 1-aminocyclopropane-1-carboxylic acid; aux1, auxin resistant 1; axr21, auxin resistant 2-1; PIN, pin-formed; PGP, P-glycoprotein; TRH1, TINY ROOT HAIR 1; ROP,
Rho-of-plant; scn1, supercentipede 1.
To whom correspondence should be addressed (email [email protected]).
1
and formation of more than one hair per trichoblast (Figure 1)
[3]. Circumstantial evidence that endogenous auxin may contribute to polar hair positioning has been provided by studies
showing that root hair placement is oriented towards an
auxin concentration maximum in the root tip [4,5] and that
pharmacological interference with auxin transport disturbs
root hair position along the trichoblast [3–5].
Auxin influx is required for co-ordinate
root hair positioning
Genetic studies identified the auxin influx carrier AUX1 as
one component of the auxin transport machinery contributing to planar polarity of hair positioning. aux1 loss-of-function mutants display weak apical shifts of hair position and
occasional formation of two hairs per trichoblast (Figure 1)
[4]. Auxin levels are reduced in the root tips of aux1 mutants
[6], which show impaired basipetal auxin transport [7] likely
to involve reduced AUX1-dependent influx from the tip region to elongating epidermal cells [8]. These findings indicate
that auxin influx from the auxin concentration maximum
to elongating epidermal cells contributes to planar polarity
of root hair positioning. However, the subtle defects of aux1
single mutants suggest that additional components are
involved.
The auxin efflux modulator TRH1 (TINY
ROOT HAIR 1) restricts root hair positioning
Considering the contribution of AUX1 to the co-ordination
of planar epidermal polarity, it is tempting to speculate that
additional auxin efflux components may be required for this
process. Members of the PIN (pin-formed) and PGP (P-glycoprotein) protein families have recently been demonstrated to
directly confer cellular auxin efflux properties [9,10]. However, neither pin2 single [4] nor pgp1;pgp19 double mutants,
defective in two PGPs required for root gravitropism, show
significant defects in apical–basal polarity of single hair
positioning (M. Grebe, unpublished work).
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Figure 1 Effects of mutations and treatments on root hair cell
polarity
Genotypes are in italic, and treatments are in roman. NPA (1-naphthyl-
Figure 2 Planar polarity in Arabidopsis roots
The epidermal cell layer is highlighted in black. A median longitudinal
section is shown.
phthalamic acid) and BFA (Brefeldin A) interfere with auxin transport
[7,19]. D, dominant mutation; OE, overexpression.
Evidence for an involvement of auxin efflux in root hair
positioning comes from analysis of the Arabidopsis trh1
mutant, which forms multiple hairs from single trichoblasts
(Figure 1) [11]. TRH1 encodes a potassium carrier that enhances auxin efflux when expressed in yeast cells [11,12].
Consistent with TRH1 function of an auxin efflux modulator,
segments of trh1 mutant roots accumulate and retain radioactively labelled auxin and display restricted long-range auxin
transport [12]. The expression of TRH1 in roots appears to
be restricted to the tip (Figure 2) [12], suggesting that the
formation of multiple hairs from trh1 trichoblasts may result
from non-cell autonomous effects. Accordingly, VicenteAgullo et al. [12] speculate that auxin transport from the
auxin concentration maximum in the root tip is impaired in
trh1 and that the phenotypic effects observed are caused by
decreased auxin levels. It will be interesting to see whether
trh1 mutations also affect positioning of single root hairs, as
it is not yet clear whether hair positioning along the apical–
basal trichoblast axis and restriction of hair formation to a
single site rely on exactly the same regulatory mechanisms.
Similarly, it remains open whether a certain auxin level in the
trichoblast is required to restrict the number of hair initiation
sites per cell, if auxin provides directional information for
basal hair positioning or enhances polarity predetermined by
other factors.
Potential downstream factors required for
root hair positioning in target cells
How exactly the action of auxin or ethylene, which are likely
to act upstream in polar root hair positioning, is linked to
the later morphological events of hair formation at a certain
position remains unclear at present. In analogy to planar
polarity of Drosophila wing hair positioning, the actin cytoskeleton may be expected to play a role in root hair placement. Indeed, ACTIN2 is required for root hair positioning
in Arabidopsis, because deformed root hair 1/actin 2 mutants
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display apical shifts of hair position and double hair formation
from single cells [13]. Small GTPases of the ROP (Rhoof-plant) gene family, such as ROP2, may provide the link
between intracellular auxin or ethylene signalling and actin
organization during hair initiation. ROPs already localize
to the hair initiation site during trichoblast elongation, prior
to morphological onset of hair bulging when actin becomes
recruited to the site of hair formation [14–17]. However,
studies examining whether ROP can be functionally placed
downstream of hormone action during root hair positioning
have not been conducted. Nevertheless, ROP2 overexpression induces the formation of multiple hairs per trichoblast
[15], similar to the loss-of-function phenotypes reported for
scn1 (supercentipede 1) mutants, which are defective in a
Rho-GDP dissociation inhibitor that can directly interact
with ROP2 [18]. While ROPs modulate actin organization
during root hair tip growth [14], functional evidence for
ROP action on actin assembly at the root hair initiation site
is lacking. Together, ROP2 overexpression and scn1 lossof-function suggest that balanced ROP activity regulates
the number of hair initiation sites per cell [15,18]. Whether
ROPs also regulate where a single hair is positioned along
the apical–basal trichoblast axis and how ROP localization
to the hair initiation site is co-ordinated by potential upstream factors remain interesting open questions for future
studies.
Conclusions and perspectives
Similar to the situation in animal systems, Rho-type small
GTPases and the actin cytoskeleton appear to act as downstream components in Arabidopsis planar polarity of root
hair positioning. However, the potential upstream factors
may turn out to be quite different. Genes homologous with
components of the frizzled pathway, a core complex of planar
polarity signalling in animals [1], do not exist in Arabidopsis
Intercellular Signalling in Plants
(M. Grebe, unpublished work). By contrast, the plant-specific
hormones auxin and ethylene contribute to the co-ordination
of root hair positioning. Genetic studies have identified a
number of mutants defective in hormone production, transport and response and potential downstream components
such as Rho-GDIs (guanine nucleotide dissociation inhibitor), ROP proteins and the actin cytoskeleton which are
affected in planar root hair positioning. Studies analysing
the functional hierarchy of action and interaction between
these components, as well as their cell-autonomous or nonautonomous contributions to polar hair positioning, should
aid the understanding of how single-cell polarity becomes
co-ordinated in plants. A new study on planar root hair
positioning from our laboratory has recently been published
[20].
We thank Alan Marchant for comments on this paper. Work on coordinate root hair positioning in our laboratory is supported by grants
from the Swedish Research Council (Vetenskapsrådet) to M.G., the
SSF (Swedish Foundation for Strategic Research) to Göran Sandberg
and a European UnionMarie-Curie Incoming Postdoctoral Fellowship
to Y.I.
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Received 20 September 2006
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