Abstract
The coordination of cell polarity within the plane of the tissue layer (planar polarity) is crucial for the development of diverse multicellular organisms. Small Rac/Rho-family GTPases and the actin cytoskeleton contribute to planar polarity formation at sites of polarity establishment in animals and plants. Yet, upstream pathways coordinating planar polarity differ strikingly between kingdoms. In the root of Arabidopsis thaliana, a concentration gradient of the phytohormone auxin coordinates polar recruitment of Rho-of-plant (ROP) to sites of polar epidermal hair initiation. However, little is known about cytoskeletal components and interactions that contribute to this planar polarity or about their relation to the patterning machinery. Here, we show that ACTIN7 (ACT7) represents a main actin isoform required for planar polarity of root hair positioning, interacting with the negative modulator ACTIN-INTERACTING PROTEIN1-2 (AIP1-2). ACT7, AIP1-2 and their genetic interaction are required for coordinated planar polarity of ROP downstream of ethylene signalling. Strikingly, AIP1-2 displays hair cell file-enriched expression, restricted by WEREWOLF (WER)-dependent patterning and modified by ethylene and auxin action. Hence, our findings reveal AIP1-2, expressed under control of the WER-dependent patterning machinery and the ethylene signalling pathway, as a modulator of actin-mediated planar polarity.
Highlights
Development of multicellular organisms relies on formation and maintenance of structural asymmetries at the single-cell level as well as their coordination within the tissue context
We found that root hair position shifted slightly apically in act2-3 when compared with wild type (WT) (Fig. 1A,B,G)
Defects in polar hair positioning were significantly stronger in act7 compared with the act2 allele (Fig. 1B,C,G; supplementary material Fig. S1A,B) and much more pronounced in the act2-3; act7-6 double mutant when compared with the single mutants (Fig. 1B-D,H), suggesting that ACT7 contributes more strongly to planar polarity than ACT2, but that both synergistically act on polar root hair positioning
Summary
Development of multicellular organisms relies on formation and maintenance of structural asymmetries at the single-cell level as well as their coordination within the tissue context. In contrast to Drosophila, in which the long-range polarising cue instructing the Frizzled planar cell polarity pathway is provided by Wingless and its homologue dWnt (Wu et al, 2013), vectorial information for planar polarity in Arabidopsis is provided by a concentration gradient of the phytohormone auxin (Fischer et al, 2006; Ikeda et al, 2009) Formation of this gradient depends on local auxin biosynthesis in the root tip, where auxin concentration reaches its maximum, and on the basipetal (shootward) transport of auxin in the root epidermis (Ikeda et al, 2009). In Drosophila, the single actin-depolymerizing factor (ADF) Twinstar (Tsr) interacts with the single actin-interacting protein 1 (AIP1) Flare (Flr) during epithelial morphogenesis (Chu et al, 2012) Both negatively regulate actin filament organisation required for planar cell polarity downstream of the Frizzled pathway (Blair et al, 2006; Ren et al, 2007). AIP1 homologues from several systems, such as Aip1p from yeast and AIP1-1 from Arabidopsis, have been shown to enhance the F-actin depolymerizing activity of ADF (named Cofilin in yeast) in vitro
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