PIN-FORMED (PIN) transporters mediate directional, intercellular movement of the phytohormone auxin in land plants. To elucidate the evolutionary origins of this developmentally crucial mechanism, we analysed the single PIN homologue of a simple green alga Klebsormidium flaccidum. KfPIN functions as a plasma membrane-localized auxin exporter in land plants and heterologous models. While its role in algae remains unclear, PIN-driven auxin export is probably an ancient and conserved trait within streptophytes.

CEITEC Masaryk University Mendel Centre for Genomics and Proteomics of Plants Systems Brno Czech Republic

Department of Chemical Biology and Genetics Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science Palacký University Olomouc Czech Republic

Department of Experimental Plant Biology Faculty of Science Charles University Prague Czech Republic

Department of Forest Genetics and Plant Physiology Umeå Plant Science Centre Swedish University of Agricultural Sciences Umeå Sweden

Department of Plant Systems Biology VIB and Department of Plant Biotechnology and Bioinformatics Ghent University Ghent Belgium

IST Austria Klosterneuburg Austria

School of Life Sciences Weihenstephan Technical University of Munich Freising Germany

The Czech Academy of Sciences Institute of Experimental Botany Prague Czech Republic

See more in PubMed

Adamowski, M. & Friml, J. PIN-dependent auxin transport: action, regulation, and evolution. Plant Cell 27, 20–32 (2015).

Bennett, T. PIN proteins and the evolution of plant development. Trends Plant Sci. 20, 498–507 (2015).

Viaene, T. et al. Directional auxin transport mechanisms in early diverging land plants. Curr. Biol. 24, 2786–2791 (2014).

Leliaert, F. et al. Phylogeny and molecular evolution of the green algae. Crit. Rev. Plant Sci. 31, 1–46 (2012).

Hori, K. et al. Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat. Commun. 5, 9 (2014).

Ju, C. et al. Conservation of ethylene as a plant hormone over 450 million years of evolution. Nat. Plants 1, 14004 (2015).

Nishiyama, T. et al. The Chara genome: secondary complexity and implications for plant terrestrialization. Cell 174, 448–464 (2018).

Zizkova, E. et al. Control of cytokinin and auxin homeostasis in cyanobacteria and algae. Ann. Bot. 119, 151–166 (2017).

Boot, K. J. M., Libbenga, K. R., Hille, S. C., Offringa, R. & van Duijn, B. Polar auxin transport: an early invention. J. Exp. Bot. 63, 4213–4218 (2012).

Ohtaka, K., Hori, K., Kanno, Y., Seo, M. & Ohta, H. Primitive auxin response without TIR1 and Aux/IAA in the charophyte alga Klebsormidium nitens. Plant Physiol. 174, 1621–1632 (2017).

Luschnig, C., Gaxiola, R. A., Grisafi, P. & Fink, G. R. EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 12, 2175–2187 (1998).

Zhang, J. et al. Inositol trisphosphate-induced Ca

Xi, W. Y., Gong, X. M., Yang, Q. Y., Yu, H. & Liou, Y. C. Pin1At regulates PIN1 polar localization and root gravitropism. Nat. Commun. 7, 10 (2016).

Petrasek, J. & Zazimalova, E. Tobacco BY-2 cells: from cellular dynamics to omics. In Biotechnology in Agriculture and Forestry Vol. 58 (eds Nagata, T. et al.) 107–115 https://doi.org/10.1007/3-540-32674-X (Springer, 2006).

Ganguly, A. et al. Differential auxin-transporting activities of PIN-FORMED proteins in Arabidopsis root hair cells. Plant Physiol. 153, 1046–1061 (2010).

Fastner, A., Absmanner, B. & Hammes, U. Z. Use of Xenopus laevis oocytes to study auxin transport. In Plant Hormones: Methods and Protocols 3rd edn, Vol. 1497 (eds Kleine-Vehn, J. & Sauer, M.) 259–270 (Humana, 2017).

Zourelidou, M. et al. Auxin efflux by PIN-FORMED proteins is activated by two different protein kinases, D6 PROTEIN KINASE and PINOID. eLife 3, 68 (2014).

Muller, A. et al. AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J. 17, 6903–6911 (1998).

Paciorek, T., Sauer, M., Balla, J., Wisniewska, J. & Friml, J. Immunocytochemical technique for protein localization in sections of plant tissues. Nat. Protoc. 1, 104–107 (2006).

Petrasek, J. et al. PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312, 914–918 (2006).

Zabka, A. et al. PIN2-like proteins may contribute to the regulation of morphogenetic processes during spermatogenesis in Chara vulgaris. Plant Cell Rep. 35, 1655–1669 (2016).

Phytohormone profiling in an evolutionary framework

WAVY GROWTH Arabidopsis E3 ubiquitin ligases affect apical PIN sorting decisions

The Hydrophilic Loop of Arabidopsis PIN1 Auxin Efflux Carrier Harbors Hallmarks of an Intrinsically Disordered Protein

ER-Localized PIN Carriers: Regulators of Intracellular Auxin Homeostasis