Structures and mechanism of the plant PIN-FORMED auxin transporter

TY - JOUR

T1 - Structures and mechanism of the plant PIN-FORMED auxin transporter

AU - Ung, Kien Lam

AU - Winkler, Mikael

AU - Schulz, Lukas

AU - Kolb, Martina

AU - Janacek, Dorina P.

AU - Dedic, Emil

AU - Stokes, David L.

AU - Hammes, Ulrich Z.

AU - Pedersen, Bjørn Panyella

N1 - Funding Information: We acknowledge the EMBION Cryo-EM Facility at iNANO, Aarhus University, for time under application ID 0137, where all data was collected with the assistance of A. Bøggild, J. Lykkegaard Karlsen and T. Boesen. We also thank eBIC (proposal BI27980) for data collection on the detergent PIN8 sample. This project has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement no. 101000936) to B.P.P. U.Z.H. is funded by the Deutsche Forschungsgemeinschaft (HA3468/6-1 and HA3468/6-3) and SFB924. D.L.S. is funded by the National Institutes of Health (R35 GM144109). Funding Information: We acknowledge the EMBION Cryo-EM Facility at iNANO, Aarhus University, for time under application ID 0137, where all data was collected with the assistance of A. Bøggild, J. Lykkegaard Karlsen and T. Boesen. We also thank eBIC (proposal BI27980) for data collection on the detergent PIN8 sample. This project has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement no. 101000936) to B.P.P. U.Z.H. is funded by the Deutsche Forschungsgemeinschaft (HA3468/6-1 and HA3468/6-3) and SFB924. D.L.S. is funded by the National Institutes of Health (R35 GM144109). Publisher Copyright: © 2022, The Author(s).

PY - 2022/9/15

Y1 - 2022/9/15

N2 - Auxins are hormones that have central roles and control nearly all aspects of growth and development in plants1–3. The proteins in the PIN-FORMED (PIN) family (also known as the auxin efflux carrier family) are key participants in this process and control auxin export from the cytosol to the extracellular space4–9. Owing to a lack of structural and biochemical data, the molecular mechanism of PIN-mediated auxin transport is not understood. Here we present biophysical analysis together with three structures of Arabidopsis thaliana PIN8: two outward-facing conformations with and without auxin, and one inward-facing conformation bound to the herbicide naphthylphthalamic acid. The structure forms a homodimer, with each monomer divided into a transport and scaffold domain with a clearly defined auxin binding site. Next to the binding site, a proline–proline crossover is a pivot point for structural changes associated with transport, which we show to be independent of proton and ion gradients and probably driven by the negative charge of the auxin. The structures and biochemical data reveal an elevator-type transport mechanism reminiscent of bile acid/sodium symporters, bicarbonate/sodium symporters and sodium/proton antiporters. Our results provide a comprehensive molecular model for auxin recognition and transport by PINs, link and expand on a well-known conceptual framework for transport, and explain a central mechanism of polar auxin transport, a core feature of plant physiology, growth and development.

AB - Auxins are hormones that have central roles and control nearly all aspects of growth and development in plants1–3. The proteins in the PIN-FORMED (PIN) family (also known as the auxin efflux carrier family) are key participants in this process and control auxin export from the cytosol to the extracellular space4–9. Owing to a lack of structural and biochemical data, the molecular mechanism of PIN-mediated auxin transport is not understood. Here we present biophysical analysis together with three structures of Arabidopsis thaliana PIN8: two outward-facing conformations with and without auxin, and one inward-facing conformation bound to the herbicide naphthylphthalamic acid. The structure forms a homodimer, with each monomer divided into a transport and scaffold domain with a clearly defined auxin binding site. Next to the binding site, a proline–proline crossover is a pivot point for structural changes associated with transport, which we show to be independent of proton and ion gradients and probably driven by the negative charge of the auxin. The structures and biochemical data reveal an elevator-type transport mechanism reminiscent of bile acid/sodium symporters, bicarbonate/sodium symporters and sodium/proton antiporters. Our results provide a comprehensive molecular model for auxin recognition and transport by PINs, link and expand on a well-known conceptual framework for transport, and explain a central mechanism of polar auxin transport, a core feature of plant physiology, growth and development.

UR - http://www.scopus.com/inward/record.url?scp=85133139184&partnerID=8YFLogxK

U2 - 10.1038/s41586-022-04883-y

DO - 10.1038/s41586-022-04883-y

M3 - Journal article

C2 - 35768502

AN - SCOPUS:85133139184

SN - 0028-0836

VL - 609

SP - 605

EP - 610

JO - Nature

JF - Nature

IS - 7927

ER -