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Local auxin biosynthesis modulates gradient-directed planar polarity in Arabidopsis

Abstract

The coordination of cell polarity within the plane of a single tissue layer (planar polarity) is a crucial task during development of multicellular organisms. Mechanisms underlying establishment of planar polarity, however, differ substantially between plants and animals1,2,3. In Arabidopsis thaliana, planar polarity of root-hair positioning along epidermal cells is coordinated towards maximum concentration of an auxin gradient in the root tip3,4,5. This gradient has been hypothesized to be sink-driven6 and computational modelling suggests that auxin efflux carrier activity may be sufficient to generate the gradient in the absence of auxin biosynthesis in the root7. Here, we demonstrate that the Raf-like kinase CONSTITUTIVE TRIPLE RESPONSE1 (CTR1; Refs 8, 9) acts as a concentration-dependent repressor of a biosynthesis-dependent auxin gradient that modulates planar polarity in the root tip. We analysed auxin biosynthesis and concentration gradients in a variety of root-hair-position mutants affected in CTR1 activity, auxin biosynthesis and transport. Our results reveal that planar polarity relies on influx- and efflux-carrier-mediated auxin redistribution from a local biosynthesis maximum. Thus, a local source of auxin biosynthesis contributes to gradient homeostasis during long-range coordination of cellular morphogenesis.

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Figure 1: A genetic framework for btk action on planar polarity.
Figure 2: The btk mutation affects CTR1 Raf-like kinase activity in vitro.
Figure 3: Concentration-dependent effect of CTR1 Raf-like kinase on auxin gradient formation and Arabidopsis development.
Figure 4: CTR1 represses local auxin biosynthesis, which modulates planar polarity.
Figure 5: PIN2 acts on auxin gradient and planar polarity formation downstream of CTR1, AUX1 and GNOM.

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Acknowledgements

We gratefully acknowledge M. Bennett, J. Ecker, M. Estelle, J. Friml, G. Jürgens, K. Palme, B. Scheres, R. Swarup and J. Xu for sharing published research materials used in this study. We are grateful to R. Granbom for tissue preparation and technical assistance with auxin concentration and biosynthesis-rate measurements. We thank L. Bako for valuable advice on protein kinase assays, as well as C. Bellini, R. Bhalerao, Y. Boutté, A. Claes, S. Pietra, M. Rosa and B. Sundberg for helpful comments on the manuscript. This work was supported by grants from the Swedish Research Council (Vetenskapsrådet) and the Swedish Foundation for Strategic Research (SSF) to M.G., by an EU Marie-Curie International Incoming Postdoctoral Fellowship to Y.I, and by NSF grants (MCB 0519869, MCB 0315992) to J.M.A.

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M.G., Y.I. and K.L. conceived the project; Y.I., K.L. and M.G. designed, performed and analysed the experiments apart from PIN2 localization in gnom mutants, which were carried out by U.F., ROP localization, auxin-bead-application as well as YFP–AUX1 and PIN2–EGFP colocalization experiments, which were performed by S.M., analysed and interpreted by U.F., S.M., Y.I., and M.G.; A.N.S. and J.M.A. provided valuable experimental materials and advice; M.G. and Y.I. wrote the paper. All authors contributed to the interpretation of results and edited the manuscript.

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Correspondence to Markus Grebe.

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Ikeda, Y., Men, S., Fischer, U. et al. Local auxin biosynthesis modulates gradient-directed planar polarity in Arabidopsis. Nat Cell Biol 11, 731–738 (2009). https://doi.org/10.1038/ncb1879

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