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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). C 2007 Biochemical Society 149 150 Biochemical Society Transactions (2007) Volume 35, part 1 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 C 2007 Biochemical Society 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. References 1 Strutt, H. and Strutt, D. (2005) BioEssays 27, 1218–1227 2 Grebe, M. (2004) BioEssays 26, 19–29 3 Masucci, J.D. and Schiefelbein, J.W. (1994) Plant Physiol. 106, 1335–1346. 4 Grebe, M., Friml, J., Swarup, R., Ljung, K., Sandberg, G., Terlou, M., Palme, K., Bennett, M.J. and Scheres, B. (2002) Curr. Biol. 12, 329–334 5 Sabatini, S., Beis, D., Wolkenfelt, H., Murfett, J., Guilfoyle, T., Malamy, J., Benfey, P., Leyser, O., Bechtold, N., Weisbeek, P. and Scheres, B. (1999) Cell 99, 463–472 6 Swarup, R., Friml, J., Marchant, A., Ljung, K., Sandberg, G., Palme, K. and Bennett, M.J. (2001) Genes Dev. 15, 2648–2653 7 Rashotte, A.M., DeLong, A. and Muday, G.K. 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