Closely related FKBP orthologs, FKBP42/TWISTED DWARF1 (TWD1) and FKBP38, have been shown to control the biogenesis of plant and mammalian ATP-binding cassette (ABC) transporters, respectively. However, the mechanistic role of the described FKBP-ABCB interaction is widely unknown. Here, we verify cytosolic HEAT-SHOCK PROTEIN90 (HSP90) isoforms as valid interactors of TWD1 and map HSP90 binding to an amphiphilic alpha-helix preceding its TPR domain. We provide pharmacological and genetic evidence that a subset of TWD1-interacting ABCBs, in contrast to mammalian ABCBs, are constitutive HSP90 clients in plants. This effect and its specificity are presumably provided by TWD1. Our data strongly correlate the impact of HSP90 inhibition on ABCB-mediated development and ABCB plasma membrane stability on the one hand and ABCB cycling rate on the other. In summary, we uncover a dynamic mechanism of HSP90 for differential stabilization of the plasma membrane ABCB isoforms to regulate polar auxin transport and to confer developmental plasticity.

Agricultural University of Athens School of Applied Biology and Biotechnology Department of Biotechnology Athens Greece

Department of Plant and Microbial Biology University of Zürich Zürich Switzerland

LINV DIPSAA Università di Firenze Florence Italy

Mendel Centre for Plant Genomics and Proteomics Masaryk University CEITEC MU Brno Czech Republic

Technische Universität Dresden Faculty of Biology Dresden Germany

University of Fribourg Department of Biology Fribourg Switzerland

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Wang, B. et al. Arabidopsis TWISTED DWARF1 functionally interacts with auxin exporter ABCB1 on the root plasma membrane. PubMed PMC

Wu, G., Otegui, M. S. & Spalding, E. P. The ER-localized TWD1 immunophilin is necessary for localization of multidrug resistance-like proteins required for polar auxin transport in Arabidopsis roots. PubMed PMC

Geisler, M., Bailly, A. & Ivanchenko, M. Master and servant: regulation of auxin transporters by FKBPs and cyclophilins. PubMed

Geisler, M. & Murphy, A. S. The ABC of auxin transport: the role of p-glycoproteins in plant development. PubMed

Geisler, M. et al. Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. PubMed

Geisler, M. M. A retro-perspective on auxin transport. PubMed PMC

Geisler, M. & Hegedus, T. A twist in the ABC: regulation of ABC transporter trafficking and transport by FK506-binding proteins. PubMed

Vanneste, S. & Friml, J. Auxin: a trigger for change in plant development. PubMed

Hammes, U. Z., Murphy, A. S. & Schwechheimer, C. Auxin transporters—a biochemical view. PubMed PMC

Grones, P. & Friml, J. Auxin transporters and binding proteins at a glance. PubMed

Mellor, N. L. et al. Systems approaches reveal that ABCB and PIN proteins mediate co-dependent auxin efflux. PubMed PMC

Ying, W. et al. Structure and function of the Arabidopsis ABC transporter ABCB19 in brassinosteroid export. PubMed

Wei, H. et al. Structural insights into brassinosteroid export mediated by the Arabidopsis ABC transporter ABCB1. PubMed PMC

Chen, Q. et al. Structures and mechanisms of the ABC transporter ABCB1 from Arabidopsis thaliana. PubMed

Geisler, M. M. Embracing substrate multispecificity in plant ABC transporters. PubMed

Geisler, M. & Bailly, A. Tete-a-tete: the function of FKBPs in plant development. PubMed

Geisler, M. et al. TWISTED DWARF1, a unique plasma membrane-anchored immunophilin-like protein, interacts with Arabidopsis multidrug resistance-like transporters AtPGP1 and AtPGP19. PubMed PMC

Walker, V. E., Atanasiu, R., Lam, H. & Shrier, A. Co-chaperone FKBP38 promotes HERG trafficking. PubMed

Aryal, B., Laurent, C. & Geisler, M. Learning from each other: ABC transporter regulation by protein phosphorylation in plant and mammalian systems. PubMed

Banasavadi-Siddegowda, Y. K. et al. FKBP38 peptidylprolyl isomerase promotes the folding of cystic fibrosis transmembrane conductance regulator in the endoplasmic reticulum. PubMed PMC

Cant, N., Pollock, N. & Ford, R. C. CFTR structure and cystic fibrosis. PubMed

Edlich, F. et al. The Bcl-2 regulator FKBP38-calmodulin-Ca2+ is inhibited by Hsp90. PubMed

Tsering, T. et al. HSP90 provides plasticity to plant development by gradually stabilizing plasma membrane presence of ABCB-type auxin transporters.

di Donato, M. & Geisler, M. HSP90 and co-chaperones: a multitaskers’ view on plant hormone biology. PubMed

Samakovli, D. et al. BRI1 and BAK1 canonical distribution in plasma membrane is HSP90 dependent. PubMed PMC

Samakovli, D., Margaritopoulou, T., Prassinos, C., Milioni, D. & Hatzopoulos, P. Brassinosteroid nuclear signaling recruits HSP90 activity. PubMed

Wang, R. et al. HSP90 regulates temperature-dependent seedling growth in Arabidopsis by stabilizing the auxin co-receptor F-box protein TIR1. PubMed PMC

Samakovli, D. et al. HSP90 affects root growth in Arabidopsis by regulating the polar distribution of PIN1. PubMed

Zhu, J. et al. TWISTED DWARF1 mediates the action of auxin transport inhibitors on actin cytoskeleton dynamics. PubMed PMC

Kamphausen, T., Fanghanel, J., Neumann, D., Schulz, B. & Rahfeld, J. U. Characterization of Arabidopsis thaliana AtFKBP42 that is membrane-bound and interacts with Hsp90. PubMed

Edlich, F. & Lucke, C. From cell death to viral replication: the diverse functions of the membrane-associated FKBP38. PubMed

Loo, M. A. et al. Perturbation of Hsp90 interaction with nascent CFTR prevents its maturation and accelerates its degradation by the proteasome. PubMed PMC

Winter, D. et al. An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PubMed PMC

Lee, K. et al. The structure of an Hsp90-immunophilin complex reveals cochaperone recognition of the client maturation state. PubMed PMC

Henrichs, S. et al. Regulation of ABCB1/PGP1-catalysed auxin transport by linker phosphorylation. PubMed PMC

Hubert, D. A., He, Y., McNulty, B. C., Tornero, P. & Dangl, J. L. Specific Arabidopsis HSP90.2 alleles recapitulate RAR1 cochaperone function in plant NB-LRR disease resistance protein regulation. PubMed PMC

Pearl, L. H. & Prodromou, C. Structure and mechanism of the Hsp90 molecular chaperone machinery. PubMed

Hutt, D. M. et al. FK506 binding protein 8 peptidylprolyl isomerase activity manages a late stage of cystic fibrosis transmembrane conductance regulator (CFTR) folding and stability. PubMed PMC

Kerr, I. D. & Bennett, M. J. New insight into the biochemical mechanisms regulating auxin transport in plants. PubMed PMC

Dettmer, J., Hong-Hermesdorf, A., Stierhof, Y. D. & Schumacher, K. Vacuolar H + -ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. PubMed PMC

Matsuoka, K., Bassham, D. C., Raikhel, N. V. & Nakamura, K. Different sensitivity to wortmannin of two vacuolar sorting signals indicates the presence of distinct sorting machineries in tobacco cells. PubMed PMC

Aryal, B. et al. An LRR receptor kinase controls ABC transporter substrate preferences during plant growth-defense decisions. PubMed

Hao, P. et al. Auxin-transporting ABC transporters are defined by a conserved D/E-P motif regulated by a prolylisomerase. PubMed PMC

Chen, J. et al. ABCB-mediated shootward auxin transport feeds into the root clock. PubMed PMC

Zhang, Y. et al. A transportome-scale amiRNA-based screen identifies redundant roles of Arabidopsis ABCB6 and ABCB20 in auxin transport. PubMed PMC

Madern, M. et al. A causal model of ion interference enables assessment and correction of ratio compression in multiplex proteomics. PubMed PMC

Wurnig, S. et al. Development of the first geldanamycin-based HSP90 degraders. PubMed PMC

Sangster, T. A. & Queitsch, C. The HSP90 chaperone complex, an emerging force in plant development and phenotypic plasticity. PubMed

Mancuso, S., Marras, A. M., Magnus, V. & Baluska, F. Noninvasive and continuous recordings of auxin fluxes in intact root apex with a carbon nanotube-modified and self-referencing microelectrode. PubMed

Bailly, A. et al. Modulation of P-glycoproteins by auxin transport inhibitors is mediated by interaction with immunophilins. PubMed

Kim, J. Y. et al. Identification of an ABCB/P-glycoprotein-specific inhibitor of auxin transport by chemical genomics. PubMed PMC

Yang, Z. et al. Structural insights into auxin recognition and efflux by Arabidopsis PIN1. PubMed PMC

Vanneste, S., Pei, Y. & Friml, J. Mechanisms of auxin action in plant growth and development. PubMed

Hammes, U. Z. & Pedersen, B. P. Structure and function of auxin transporters. PubMed

Brunoud, G. et al. A novel sensor to map auxin response and distribution at high spatio-temporal resolution. PubMed

Bouchard, R. et al. Immunophilin-like TWISTED DWARF1 modulates auxin efflux activities of Arabidopsis P-glycoproteins. PubMed

Prigge, M. J. et al. Genetic analysis of the Arabidopsis TIR1/AFB auxin receptors reveals both overlapping and specialized functions. PubMed PMC

Dharmasiri, N. et al. Plant development is regulated by a family of auxin receptor F box proteins. PubMed

Kim, T. W. et al. Elongation and gravitropic responses of Arabidopsis roots are regulated by brassinolide and IAA. PubMed

Bailly, A. et al. Expression of TWISTED DWARF1 lacking its in-plane membrane anchor leads to increased cell elongation and hypermorphic growth. PubMed

Cho, M. & Cho, H. T. The function of ABCB transporters in auxin transport. PubMed PMC

Geldner, N., Friml, J., Stierhof, Y. D., Jurgens, G. & Palme, K. Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. PubMed

Cho, M., Lee, Z. W. & Cho, H. T. ATP-binding cassette B4, an auxin-efflux transporter, stably associates with the plasma membrane and shows distinctive intracellular trafficking from that of PIN-FORMED proteins. PubMed PMC

Adamowski, M. & Friml, J. PIN-dependent auxin transport: action, regulation, and evolution. PubMed PMC

Zhao, B. et al. TWISTED DWARF 1 associates with BRASSINOSTEROID-INSENSITIVE 1 to regulate early events of the brassinosteroid signaling pathway. PubMed

Chaiwanon, J., Garcia, V. J., Cartwright, H., Sun, Y. & Wang, Z. Y. Immunophilin-like FKBP42/TWISTED DWARF1 interacts with the receptor kinase BRI1 to regulate brassinosteroid signaling in Arabidopsis. PubMed PMC

Geisler, M., Wang, B. & Zhu, J. Auxin transport during root gravitropism: transporters and techniques. PubMed

Noureddine, J. et al. Knockout of endoplasmic reticulum-localized molecular chaperone HSP90.7 impairs seedling development and cellular auxin homeostasis in Arabidopsis. PubMed

Paciorek, T. et al. Auxin inhibits endocytosis and promotes its own efflux from cells. PubMed

Titapiwatanakun, B. et al. ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis. PubMed

Blakeslee, J. J. et al. Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis. PubMed PMC

Peterson, L. B., Eskew, J. D., Vielhauer, G. A. & Blagg, B. S. The hERG channel is dependent upon the Hsp90alpha isoform for maturation and trafficking. PubMed PMC

Farinha, C. M. & Canato, S. From the endoplasmic reticulum to the plasma membrane: mechanisms of CFTR folding and trafficking. PubMed PMC

Deslauriers, S. D. & Spalding, E. P. Electrophysiological study of Arabidopsis ABCB4 and PIN2 auxin transporters: Evidence of auxin activation and interaction enhancing auxin selectivity. PubMed PMC

Spalding, E. P. Diverting the downhill flow of auxin to steer growth during tropisms. PubMed

Wu, G., Lewis, D. R. & Spalding, E. P. Mutations in Arabidopsis multidrug resistance-like ABC transporters separate the roles of acropetal and basipetal auxin transport in lateral root development. PubMed PMC

Mravec, J. et al. Interaction of PIN and PGP transport mechanisms in auxin distribution-dependent development. PubMed

Lewis, D. R., Miller, N. D., Splitt, B. L., Wu, G. & Spalding, E. P. Separating the roles of acropetal and basipetal auxin transport on gravitropism with mutations in two Arabidopsis multidrug resistance-like ABC transporter genes. PubMed PMC

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. PubMed PMC

Cho, M., Lee, S. H. & Cho, H. T. P-glycoprotein4 displays auxin efflux transporter-like action in Arabidopsis root hair cells and tobacco cells. PubMed PMC

Abas, L. et al. Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. PubMed

Matern, A. et al. A substrate of the ABC transporter PEN3 stimulates bacterial flagellin (flg22)-induced callose deposition in Arabidopsis thaliana. PubMed PMC

Lewis, D. R. & Muday, G. K. Measurement of auxin transport in Arabidopsis thaliana. PubMed

Ludwig-Muller, J. et al. Two auxinic herbicides affect Brassica napus plant hormone levels and induce molecular changes in transcription. PubMed PMC