Tracing Evolution of Auxin Transport and Polarity in Plants

Evaluation of gravitropism in non-seed plants
Y. Zhang, L. Li, J. Friml, in:, E.B. Blancaflor (Ed.), Plant Gravitropism, Springer Nature, 2021, pp. 43–51.

Auxin analog-induced Ca2+ signaling is independent of inhibition of endosomal aggregation in Arabidopsis roots
R. Wang, E. Himschoot, M. Grenzi, J. Chen, A. Safi, M. Krebs, K. Schumacher, M. Nowack, W. Moeder, K. Yoshioka, D. Van Damme, I. De Smet, D. Geelen, T. Beeckman, J. Friml, A. Costa, S. Vanneste, Journal of Experimental Botany 73 (2022).

Cellular requirements for PIN polar cargo clustering in Arabidopsis thaliana
H. Li, D. von Wangenheim, X. Zhang, S. Tan, N. Darwish-Miranda, S. Naramoto, K.T. Wabnik, R. de Rycke, W. Kaufmann, D.J. Gütl, R. Tejos, P. Grones, M. Ke, X. Chen, J. Dettmer, J. Friml, New Phytologist 229 (2021) 351–369.

Pho-view of auxin: Reversible protein phosphorylation in auxin biosynthesis, transport and signaling
S. Tan, C. Luschnig, J. Friml, Molecular Plant 14 (2021) 151–165.

Naphthylphthalamic acid associates with and inhibits PIN auxin transporters
L. Abas, M. Kolb, J. Stadlmann, D.P. Janacek, K. Lukic, C. Schwechheimer, L.A. Sazanov, L. Mach, J. Friml, U.Z. Hammes, PNAS 118 (2021).

Synaptotagmins at the endoplasmic reticulum-plasma membrane contact sites maintain diacylglycerol homeostasis during abiotic stress
N. Ruiz-Lopez, J. Pérez-Sancho, A. Esteban Del Valle, R. Haslam, S. Vanneste, R. Catalá, C. Perea-Resa, D. Van Damme, S. García-Hernández, A. Albert, J. Vallarino, J. Lin, J. Friml, A. Macho, J. Salinas, A. Rosado, J. Napier, V. Amorim-Silva, M. Botella, Plant Cell 33 (2021) 2431–2453.

PIN-mediated polar auxin transport regulations in plant tropic responses
H. Han, M. Adamowski, L. Qi, S. Alotaibi, J. Friml, New Phytologist 232 (2021) 510–522.

Auxin guides roots to avoid obstacles during gravitropic growth
Y. Zhang, J. Friml, New Phytologist 225 (2020) 1049–1052.

Auxin signalling in growth: Schrödinger's cat out of the bag
M.C. Gallei, C. Luschnig, J. Friml, Current Opinion in Plant Biology 53 (2020) 43–49.

Clathrin-mediated trafficking and PIN trafficking are required for auxin canalization and vascular tissue formation in Arabidopsis
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Evolutionarily unique mechanistic framework of clathrin-mediated endocytosis in plants
M. Narasimhan, A.J. Johnson, R. Prizak, W. Kaufmann, S. Tan, B.E. Casillas Perez, J. Friml, ELife 9 (2020).

The lipid code-dependent phosphoswitch PDK1–D6PK activates PIN-mediated auxin efflux in Arabidopsis
S. Tan, X. Zhang, W. Kong, X.-L. Yang, G. Molnar, Z. Vondráková, R. Filepová, J. Petrášek, J. Friml, H.-W. Xue, Nature Plants 6 (2020) 556–569.

Strigolactones inhibit auxin feedback on PIN-dependent auxin transport canalization
J. Zhang, E. Mazur, J. Balla, M.C. Gallei, P. Kalousek, Z. Medveďová, Y. Li, Y. Wang, T. Prat, M.K. Vasileva, V. Reinöhl, S. Procházka, R. Halouzka, P. Tarkowski, C. Luschnig, P. Brewer, J. Friml, Nature Communications 11 (2020) 3508.

Cell-surface receptors enable perception of extracellular cytokinins
I. Antoniadi, O. Novák, Z. Gelová, A.J. Johnson, O. Plíhal, R. Simerský, V. Mik, T. Vain, E. Mateo-Bonmatí, M. Karady, M. Pernisová, L. Plačková, K. Opassathian, J. Hejátko, S. Robert, J. Friml, K. Doležal, K. Ljung, C. Turnbull, Nature Communications 11 (2020).

PIN2 polarity establishment in arabidopsis in the absence of an intact cytoskeleton
M. Glanc, M. Fendrych, J. Friml, Biomolecules 9 (2019).

Evolution of fast root gravitropism in seed plants
Y. Zhang, G. Xiao, X. Wang, X. Zhang, J. Friml, Nature Communications 10 (2019).

Receptor kinase module targets PIN-dependent auxin transport during canalization
J. Hajny, T. Prat, N. Rydza, L. Rodriguez Solovey, S. Tan, I. Verstraeten, D. Domjan, E. Mazur, E. Smakowska-Luzan, W. Smet, E. Mor, J. Nolf, B. Yang, W. Grunewald, G. Molnar, Y. Belkhadir, B. De Rybel, J. Friml, Science 370 (2020) 550–557.

Arabidopsis flippases cooperate with ARF GTPase exchange factors to regulate the trafficking and polarity of PIN auxin transporters
X. Zhang, M. Adamowski, P. Marhavá, S. Tan, Y. Zhang, L. Rodriguez Solovey, M. Zwiewka, V. Pukyšová, A.S. Sánchez, V.K. Raxwal, C.S. Hardtke, T. Nodzynski, J. Friml, The Plant Cell 32 (2020) 1644–1664.

Endocytosis of BRASSINOSTEROID INSENSITIVE1 is partly driven by a canonical tyrosine-based Motif
D. Liu, R. Kumar, C. LAN, A.J. Johnson, W. Siao, I. Vanhoutte, P. Wang, K. Bender, K. Yperman, S. Martins, X. Zhao, G. Vert, D. Van Damme, J. Friml, E. Russinova, Plant Cell 32 (2020) 3598–3612.

AGC kinases and MAB4/MEL proteins maintain PIN polarity by limiting lateral diffusion in plant cells
M. Glanc, K. Van Gelderen, L. Hörmayer, S. Tan, S. Naramoto, X. Zhang, D. Domjan, L. Vcelarova, R. Hauschild, A.J. Johnson, E. de Koning, M. van Dop, E. Rademacher, S. Janson, X. Wei, G. Molnar, M. Fendrych, B. De Rybel, R. Offringa, J. Friml, Current Biology 31 (2021) 1918–1930.

TMK1-mediated auxin signalling regulates differential growth of the apical hook
M. Cao, R. Chen, P. Li, Y. Yu, R. Zheng, D. Ge, W. Zheng, X. Wang, Y. Gu, Z. Gelová, J. Friml, H. Zhang, R. Liu, J. He, T. Xu, Nature 568 (2019) 240–243.

Directional auxin fluxes in plants by intramolecular domain‐domain co‐evolution of PIN auxin transporters
Y. Zhang, C. Hartinger, X. Wang, J. Friml, New Phytologist 227 (2020) 1406–1416.

PIN-driven auxin transport emerged early in streptophyte evolution
R. Skokan, E. Medvecká, T. Viaene, S. Vosolsobě, M. Zwiewka, K. Müller, P. Skůpa, M. Karady, Y. Zhang, D.P. Janacek, U.Z. Hammes, K. Ljung, T. Nodzyński, J. Petrášek, J. Friml, Nature Plants 5 (2019) 1114–1119.

SCF TIR1/AFB auxin signaling for bending termination during shoot gravitropism
H. Han, H. Rakusova, I. Verstraeten, Y. Zhang, J. Friml, Plant Physiology 183 (2020) 37–40.

Relative contribution of PIN-containing secretory vesicles and plasma membrane PINs to the directed auxin transport: Theoretical estimation
S. Hille, M. Akhmanova, M. Glanc, A.J. Johnson, J. Friml, International Journal of Molecular Sciences 19 (2018).

The Chara genome: Secondary complexity and implications for plant terrestrialization
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The inhibitor Endosidin 4 targets SEC7 domain-type ARF GTPase exchange factors and interferes with sub cellular trafficking in eukaryotes
U. Kania, T. Nodzyński, Q. Lu, G.R. Hicks, W. Nerinckx, K. Mishev, F. Peurois, J. Cherfils, R.R.M. De, P. Grones, S. Robert, E. Russinova, J. Friml, The Plant Cell 30 (2018) 2553–2572.

Adenylate cyclase activity of TIR1/AFB auxin receptors in plants
L. Qi, M. Kwiatkowski, H. Chen, L. Hörmayer, S.A. Sinclair, M. Zou, C.I. del Genio, M.F. Kubeš, R. Napier, K. Jaworski, J. Friml, Nature 611 (2022) 133–138.

Mechanistic framework for cell-intrinsic re-establishment of PIN2 polarity after cell division
M. Glanc, M. Fendrych, J. Friml, Nature Plants 4 (2018) 1082–1088.

Cell surface and intracellular auxin signalling for H⁺ fluxes in root growth
L. Li, I. Verstraeten, M. Roosjen, K. Takahashi, L. Rodriguez Solovey, J. Merrin, J. Chen, L. Shabala, W. Smet, H. Ren, S. Vanneste, S. Shabala, B. De Rybel, D. Weijers, T. Kinoshita, W.M. Gray, J. Friml, Nature 599 (2021) 273–277.

ABP1–TMK auxin perception for global phosphorylation and auxin canalization
Friml J, Gallei MC, Gelová Z, Johnson AJ, Mazur E, Monzer A, Rodriguez Solovey L, Roosjen M, Verstraeten I, Živanović BD, Zou M, Fiedler L, Giannini C, Grones P, Hrtyan M, Kaufmann W, Kuhn A, Narasimhan M, Randuch M, Rýdza N, Takahashi K, Tan S, Teplova A, Kinoshita T, Weijers D, Rakusová H. 2022. ABP1–TMK auxin perception for global phosphorylation and auxin canalization. Nature. 609(7927), 575–581.

Auxin and strigolactone non-canonical signaling regulating development in Arabidopsis thaliana
M.C. Gallei, Auxin and Strigolactone Non-Canonical Signaling Regulating Development in Arabidopsis Thaliana, Institute of Science and Technology Austria, 2022.

Non-steroidal anti-inflammatory drugs target TWISTED DWARF1-regulated actin dynamics and auxin transport-mediated plant development
S. Tan, M. Di Donato, M. Glanc, X. Zhang, P. Klíma, J. Liu, A. Bailly, N. Ferro, J. Petrášek, M. Geisler, J. Friml, Cell Reports 33 (2020).

RAF-like protein kinases mediate a deeply conserved, rapid auxin response
A. Kuhn, M. Roosjen, S. Mutte, S.M. Dubey, V.P. Carrillo Carrasco, S. Boeren, A. Monzer, J. Koehorst, T. Kohchi, R. Nishihama, M. Fendrych, J. Sprakel, J. Friml, D. Weijers, Cell 187 (2024) 130–148.e17.

Distinct functions of TIR1 and AFB1 receptors in auxin signalling.
H. Chen, L. Li, M. Zou, L. Qi, J. Friml, Molecular Plant 16 (2023) 1117–1119.

Divergence of trafficking and polarization mechanisms for PIN auxin transporters during land plant evolution
H. Tang, K. Lu, Y. Zhang, Y. Cheng, S. Tu, J. Friml, Plant Communications 5 (2024).

Developmental patterning function of GNOM ARF-GEF mediated from the cell periphery
M. Adamowski, I. Matijevic, J. Friml, ELife 13 (2024).

Rapid translocation of NGR proteins driving polarization of PIN-activating D6 protein kinase during root gravitropism
I. Kulich, J. Schmid, A. Teplova, L. Qi, J. Friml, ELife 12 (2024).

Mechanical forces in plant tissue matrix orient cell divisions via microtubule stabilization
L. Hörmayer, J.C. Montesinos López, N. Trozzi, L. Spona, S. Yoshida, P. Marhavá, S. Caballero Mancebo, E. Benková, C.-P.J. Heisenberg, Y. Dagdas, M. Majda, J. Friml, Dev Cell (2024) S1534-5807(24)00177–1.

Wound healing in the Arabidopsis root meristem
L. Hörmayer, Wound Healing in the Arabidopsis Root Meristem, Institute of Science and Technology Austria, 2021.

Wounding-induced changes in cellular pressure and localized auxin signalling spatially coordinate restorative divisions in roots
L. Hörmayer, J.C. Montesinos López, P. Marhavá, E. Benková, S. Yoshida, J. Friml, Proceedings of the National Academy of Sciences 117 (2020).

Re-activation of stem cell pathways for pattern restoration in plant wound healing
P. Marhavá, L. Hörmayer, S. Yoshida, P. Marhavý, E. Benková, J. Friml, Cell 177 (2019) 957–969.e13.

Targeted cell ablation-based insights into wound healing and restorative patterning
L. Hörmayer, J. Friml, Current Opinion in Plant Biology 52 (2019) 124–130.

Salicylic acid targets protein phosphatase 2A to attenuate growth in plants
S. Tan, M.F. Abas, I. Verstraeten, M. Glanc, G. Molnar, J. Hajny, P. Lasák, I. Petřík, E. Russinova, J. Petrášek, O. Novák, J. Pospíšil, J. Friml, Current Biology 30 (2020) 381–395.e8.

Auxin canalization and vascular tissue formation by TIR1/AFB-mediated auxin signaling in arabidopsis
E. Mazur, I. Kulik, J. Hajny, J. Friml, New Phytologist 226 (2020) 1375–1383.

PID/WAG-mediated phosphorylation of the Arabidopsis PIN3 auxin transporter mediates polarity switches during gravitropism
P. Grones, M.F. Abas, J. Hajny, A. Jones, S. Waidmann, J. Kleine Vehn, J. Friml, Scientific Reports 8 (2018).

Pinstatic acid promotes auxin transport by inhibiting PIN internalization
A. Oochi, J. Hajny, K. Fukui, Y. Nakao, M.C. Gallei, M. Quareshy, K. Takahashi, T. Kinoshita, S. Harborough, S. Kepinski, H. Kasahara, R. Napier, J. Friml, K. Hayashi, Plant Physiology 180 (2019) 1152–1165.

Developmental roles of auxin binding protein 1 in Arabidopsis thaliana
Z. Gelová, M.C. Gallei, M. Pernisová, G. Brunoud, X. Zhang, M. Glanc, L. Li, J. Michalko, Z. Pavlovicova, I. Verstraeten, H. Han, J. Hajny, R. Hauschild, M. Čovanová, M. Zwiewka, L. Hörmayer, M. Fendrych, T. Xu, T. Vernoux, J. Friml, Plant Science 303 (2021).

Systematic analysis of specific and nonspecific auxin effects on endocytosis and trafficking
M. Narasimhan, M.C. Gallei, S. Tan, A.J. Johnson, I. Verstraeten, L. Li, L. Rodriguez Solovey, H. Han, E. Himschoot, R. Wang, S. Vanneste, J. Sánchez-Simarro, F. Aniento, M. Adamowski, J. Friml, Plant Physiology 186 (2021) 1122–1142.

Functional innovations of PIN auxin transporters mark crucial evolutionary transitions during rise of flowering plants
Y. Zhang, L. Rodriguez Solovey, L. Li, X. Zhang, J. Friml, Science Advances 6 (2020).

Cell surface and intracellular auxin signalling for H+-fluxes in root growth
L. Li, I. Verstraeten, M. Roosjen, K. Takahashi, L. Rodriguez Solovey, J. Merrin, J. Chen, L. Shabala, W. Smet, H. Ren, S. Vanneste, S. Shabala, B. De Rybel, D. Weijers, T. Kinoshita, W.M. Gray, J. Friml, Research Square (n.d.).