[{"file_date_updated":"2023-11-02T17:12:37Z","publication_status":"published","publication_identifier":{"issn":["0028-0836"],"eissn":["1476-4687"]},"acknowledged_ssus":[{"_id":"Bio"},{"_id":"EM-Fac"},{"_id":"LifeSc"}],"intvolume":"       609","abstract":[{"lang":"eng","text":"The phytohormone auxin triggers transcriptional reprogramming through a well-characterized perception machinery in the nucleus. By contrast, mechanisms that underlie fast effects of auxin, such as the regulation of ion fluxes, rapid phosphorylation of proteins or auxin feedback on its transport, remain unclear1,2,3. Whether auxin-binding protein 1 (ABP1) is an auxin receptor has been a source of debate for decades1,4. Here we show that a fraction of Arabidopsis thaliana ABP1 is secreted and binds auxin specifically at an acidic pH that is typical of the apoplast. ABP1 and its plasma-membrane-localized partner, transmembrane kinase 1 (TMK1), are required for the auxin-induced ultrafast global phospho-response and for downstream processes that include the activation of H+-ATPase and accelerated cytoplasmic streaming. abp1 and tmk mutants cannot establish auxin-transporting channels and show defective auxin-induced vasculature formation and regeneration. An ABP1(M2X) variant that lacks the capacity to bind auxin is unable to complement these defects in abp1 mutants. These data indicate that ABP1 is the auxin receptor for TMK1-based cell-surface signalling, which mediates the global phospho-response and auxin canalization."}],"has_accepted_license":"1","date_created":"2023-01-16T10:04:48Z","article_type":"original","volume":609,"oa_version":"Submitted Version","title":"ABP1–TMK auxin perception for global phosphorylation and auxin canalization","scopus_import":"1","day":"15","author":[{"orcid":"0000-0002-8302-7596","first_name":"Jiří","id":"4159519E-F248-11E8-B48F-1D18A9856A87","full_name":"Friml, Jiří","last_name":"Friml"},{"full_name":"Gallei, Michelle C","id":"35A03822-F248-11E8-B48F-1D18A9856A87","last_name":"Gallei","first_name":"Michelle C","orcid":"0000-0003-1286-7368"},{"first_name":"Zuzana","orcid":"0000-0003-4783-1752","last_name":"Gelová","id":"0AE74790-0E0B-11E9-ABC7-1ACFE5697425","full_name":"Gelová, Zuzana"},{"full_name":"Johnson, Alexander J","id":"46A62C3A-F248-11E8-B48F-1D18A9856A87","last_name":"Johnson","first_name":"Alexander J","orcid":"0000-0002-2739-8843"},{"first_name":"Ewa","full_name":"Mazur, Ewa","last_name":"Mazur"},{"first_name":"Aline","last_name":"Monzer","id":"2DB5D88C-D7B3-11E9-B8FD-7907E6697425","full_name":"Monzer, Aline"},{"full_name":"Rodriguez Solovey, Lesia","id":"3922B506-F248-11E8-B48F-1D18A9856A87","last_name":"Rodriguez Solovey","orcid":"0000-0002-7244-7237","first_name":"Lesia"},{"first_name":"Mark","full_name":"Roosjen, Mark","last_name":"Roosjen"},{"id":"362BF7FE-F248-11E8-B48F-1D18A9856A87","full_name":"Verstraeten, Inge","last_name":"Verstraeten","first_name":"Inge","orcid":"0000-0001-7241-2328"},{"last_name":"Živanović","full_name":"Živanović, Branka D.","first_name":"Branka D."},{"first_name":"Minxia","last_name":"Zou","full_name":"Zou, Minxia","id":"5c243f41-03f3-11ec-841c-96faf48a7ef9"},{"first_name":"Lukas","id":"7c417475-8972-11ed-ae7b-8b674ca26986","full_name":"Fiedler, Lukas","last_name":"Fiedler"},{"first_name":"Caterina","last_name":"Giannini","full_name":"Giannini, Caterina","id":"e3fdddd5-f6e0-11ea-865d-ca99ee6367f4"},{"full_name":"Grones, Peter","last_name":"Grones","first_name":"Peter"},{"id":"45A71A74-F248-11E8-B48F-1D18A9856A87","full_name":"Hrtyan, Mónika","last_name":"Hrtyan","first_name":"Mónika"},{"last_name":"Kaufmann","full_name":"Kaufmann, Walter","id":"3F99E422-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0001-9735-5315","first_name":"Walter"},{"first_name":"Andre","full_name":"Kuhn, Andre","last_name":"Kuhn"},{"orcid":"0000-0002-8600-0671","first_name":"Madhumitha","last_name":"Narasimhan","full_name":"Narasimhan, Madhumitha","id":"44BF24D0-F248-11E8-B48F-1D18A9856A87"},{"last_name":"Randuch","full_name":"Randuch, Marek","id":"6ac4636d-15b2-11ec-abd3-fb8df79972ae","first_name":"Marek"},{"first_name":"Nikola","last_name":"Rýdza","full_name":"Rýdza, Nikola"},{"full_name":"Takahashi, Koji","last_name":"Takahashi","first_name":"Koji"},{"full_name":"Tan, Shutang","id":"2DE75584-F248-11E8-B48F-1D18A9856A87","last_name":"Tan","first_name":"Shutang","orcid":"0000-0002-0471-8285"},{"last_name":"Teplova","full_name":"Teplova, Anastasiia","id":"e3736151-106c-11ec-b916-c2558e2762c6","first_name":"Anastasiia"},{"last_name":"Kinoshita","full_name":"Kinoshita, Toshinori","first_name":"Toshinori"},{"last_name":"Weijers","full_name":"Weijers, Dolf","first_name":"Dolf"},{"last_name":"Rakusová","full_name":"Rakusová, Hana","first_name":"Hana"}],"user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","citation":{"ista":"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.","chicago":"Friml, Jiří, Michelle C Gallei, Zuzana Gelová, Alexander J Johnson, Ewa Mazur, Aline Monzer, Lesia Rodriguez Solovey, et al. “ABP1–TMK Auxin Perception for Global Phosphorylation and Auxin Canalization.” <i>Nature</i>. Springer Nature, 2022. <a href=\"https://doi.org/10.1038/s41586-022-05187-x\">https://doi.org/10.1038/s41586-022-05187-x</a>.","apa":"Friml, J., Gallei, M. C., Gelová, Z., Johnson, A. J., Mazur, E., Monzer, A., … Rakusová, H. (2022). ABP1–TMK auxin perception for global phosphorylation and auxin canalization. <i>Nature</i>. Springer Nature. <a href=\"https://doi.org/10.1038/s41586-022-05187-x\">https://doi.org/10.1038/s41586-022-05187-x</a>","mla":"Friml, Jiří, et al. “ABP1–TMK Auxin Perception for Global Phosphorylation and Auxin Canalization.” <i>Nature</i>, vol. 609, no. 7927, Springer Nature, 2022, pp. 575–81, doi:<a href=\"https://doi.org/10.1038/s41586-022-05187-x\">10.1038/s41586-022-05187-x</a>.","ama":"Friml J, Gallei MC, Gelová Z, et al. ABP1–TMK auxin perception for global phosphorylation and auxin canalization. <i>Nature</i>. 2022;609(7927):575-581. doi:<a href=\"https://doi.org/10.1038/s41586-022-05187-x\">10.1038/s41586-022-05187-x</a>","ieee":"J. Friml <i>et al.</i>, “ABP1–TMK auxin perception for global phosphorylation and auxin canalization,” <i>Nature</i>, vol. 609, no. 7927. Springer Nature, pp. 575–581, 2022.","short":"J. Friml, M.C. Gallei, Z. Gelová, A.J. Johnson, E. Mazur, A. Monzer, L. Rodriguez Solovey, M. Roosjen, I. Verstraeten, B.D. Živanović, M. Zou, L. Fiedler, C. Giannini, P. Grones, M. Hrtyan, W. Kaufmann, A. Kuhn, M. Narasimhan, M. Randuch, N. Rýdza, K. Takahashi, S. Tan, A. Teplova, T. Kinoshita, D. Weijers, H. Rakusová, Nature 609 (2022) 575–581."},"issue":"7927","language":[{"iso":"eng"}],"oa":1,"file":[{"file_id":"14483","date_updated":"2023-11-02T17:12:37Z","creator":"amally","file_size":79774945,"date_created":"2023-11-02T17:12:37Z","checksum":"a6055c606aefb900bf62ae3e7d15f921","relation":"main_file","content_type":"application/pdf","access_level":"open_access","file_name":"Friml Nature 2022_merged.pdf","success":1}],"department":[{"_id":"JiFr"},{"_id":"GradSch"},{"_id":"EvBe"},{"_id":"EM-Fac"}],"month":"09","quality_controlled":"1","ddc":["580"],"page":"575-581","type":"journal_article","_id":"12291","date_updated":"2023-11-07T08:16:09Z","publisher":"Springer Nature","article_processing_charge":"No","doi":"10.1038/s41586-022-05187-x","acknowledgement":"We acknowledge K. Kubiasová for excellent technical assistance, J. Neuhold, A. Lehner and A. Sedivy for technical assistance with protein production and purification at Vienna Biocenter Core Facilities; Creoptix for performing GCI; and the Bioimaging, Electron Microscopy and Life Science Facilities at ISTA, the Plant Sciences Core Facility of CEITEC Masaryk University, the Core Facility CELLIM (MEYS CR, LM2018129 Czech-BioImaging) and J. Sprakel for their assistance. J.F. is grateful to R. Napier for many insightful suggestions and support. We thank all past and present members of the Friml group for their support and for other contributions to this effort to clarify the controversial role of ABP1 over the past seven years. The project received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement no. 742985 to J.F. and 833867 to D.W.); the Austrian Science Fund (FWF; P29988 to J.F.); the Netherlands Organization for Scientific Research (NWO; VICI grant 865.14.001 to D.W. and VENI grant VI.Veni.212.003 to A.K.); the Ministry of Education, Science and Technological Development of the Republic of Serbia (contract no. 451-03-68/2022-14/200053 to B.D.Ž.); and the MEXT/JSPS KAKENHI to K.T. (20K06685) and T.K. (20H05687 and 20H05910).","date_published":"2022-09-15T00:00:00Z","ec_funded":1,"pmid":1,"status":"public","publication":"Nature","project":[{"name":"Tracing Evolution of Auxin Transport and Polarity in Plants","grant_number":"742985","call_identifier":"H2020","_id":"261099A6-B435-11E9-9278-68D0E5697425"},{"_id":"262EF96E-B435-11E9-9278-68D0E5697425","grant_number":"P29988","name":"RNA-directed DNA methylation in plant development","call_identifier":"FWF"}],"external_id":{"pmid":["36071161"],"isi":["000851357500002"]},"year":"2022","isi":1},{"type":"journal_article","_id":"8824","date_updated":"2023-09-05T13:03:15Z","publisher":"Elsevier","article_processing_charge":"Yes (via OA deal)","doi":"10.1016/j.cub.2020.10.011","quality_controlled":"1","ddc":["570"],"external_id":{"isi":["000614361000039"],"pmid":["33157019"]},"isi":1,"year":"2021","date_published":"2021-01-11T00:00:00Z","acknowledgement":"We thank the SiCE group for discussions and comments; S. Yalovsky, B. Scheres, and the NASC/ABRC collection for providing transgenic Arabidopsis lines and plasmids; L. Kalmbach and M. Barberon for the gift of pLOK180_pFR7m34GW; A. Lacroix, J. Berger, and P. Bolland for plant care; and M. Fendrych for help with microfluidics in the J.F. lab. We acknowledge\r\nthe contribution of the SFR Biosciences (UMS3444/CNRS, US8/Inser m, ENS de Lyon, UCBL) facilities: C. Lionet, E. Chatre, and J. Brocard at LBIPLATIM-MICROSCOPY for assistance with imaging, and V. GuegenChaignon and A. Page at the Protein Science Facility (PSF) for assistance with protein purification and mass spectrometry. Y.J. was funded by ERC\r\ngrant 3363360-APPL under FP/2007–2013. Y.J. and Z.L.N. were funded by an ANR- and NSF-supported ERA-CAPS project (SICOPID: ANR-17-CAPS0003-01/NSF PGRP IOS-1841917). A.I.C.-D. is funded by an ERC consolidator grant (ERC-2015-CoG–683163) and BIO2016-78955 grant from the Spanish Ministry of Economy and Competitiveness. Exchanges between the Y.J. and T.B. laboratories were funded by Tournesol grant 35656NB. B.K.M. was\r\nfunded by the Omics@vib Marie Curie COFUND and Research Foundation Flanders for a postdoctoral fellowship.","pmid":1,"status":"public","publication":"Current Biology","date_created":"2020-12-01T13:39:46Z","article_type":"original","volume":31,"title":"Auxin-regulated reversible inhibition of TMK1 signaling by MAKR2 modulates the dynamics of root gravitropism","oa_version":"Published Version","day":"11","author":[{"full_name":"Marquès-Bueno, MM","last_name":"Marquès-Bueno","first_name":"MM"},{"full_name":"Armengot, L","last_name":"Armengot","first_name":"L"},{"last_name":"Noack","full_name":"Noack, LC","first_name":"LC"},{"full_name":"Bareille, J","last_name":"Bareille","first_name":"J"},{"last_name":"Rodriguez Solovey","full_name":"Rodriguez Solovey, Lesia","id":"3922B506-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0002-7244-7237","first_name":"Lesia"},{"first_name":"MP","full_name":"Platre, MP","last_name":"Platre"},{"full_name":"Bayle, V","last_name":"Bayle","first_name":"V"},{"full_name":"Liu, M","last_name":"Liu","first_name":"M"},{"full_name":"Opdenacker, D","last_name":"Opdenacker","first_name":"D"},{"first_name":"S","full_name":"Vanneste, S","last_name":"Vanneste"},{"last_name":"Möller","full_name":"Möller, BK","first_name":"BK"},{"full_name":"Nimchuk, ZL","last_name":"Nimchuk","first_name":"ZL"},{"first_name":"T","full_name":"Beeckman, T","last_name":"Beeckman"},{"first_name":"AI","full_name":"Caño-Delgado, AI","last_name":"Caño-Delgado"},{"last_name":"Friml","full_name":"Friml, Jiří","id":"4159519E-F248-11E8-B48F-1D18A9856A87","first_name":"Jiří","orcid":"0000-0002-8302-7596"},{"last_name":"Jaillais","full_name":"Jaillais, Y","first_name":"Y"}],"file_date_updated":"2021-02-04T11:37:50Z","publication_status":"published","publication_identifier":{"issn":["0960-9822"],"eissn":["1879-0445"]},"tmp":{"name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","short":"CC BY (4.0)"},"intvolume":"        31","abstract":[{"lang":"eng","text":"Plants are able to orient their growth according to gravity, which ultimately controls both shoot and root architecture.1 Gravitropism is a dynamic process whereby gravistimulation induces the asymmetric distribution of the plant hormone auxin, leading to asymmetric growth, organ bending, and subsequent reset of auxin distribution back to the original pre-gravistimulation situation.1,  2,  3 Differential auxin accumulation during the gravitropic response depends on the activity of polarly localized PIN-FORMED (PIN) auxin-efflux carriers.1,  2,  3,  4 In particular, the timing of this dynamic response is regulated by PIN2,5,6 but the underlying molecular mechanisms are poorly understood. Here, we show that MEMBRANE ASSOCIATED KINASE REGULATOR2 (MAKR2) controls the pace of the root gravitropic response. We found that MAKR2 is required for the PIN2 asymmetry during gravitropism by acting as a negative regulator of the cell-surface signaling mediated by the receptor-like kinase TRANSMEMBRANE KINASE1 (TMK1).2,7,  8,  9,  10 Furthermore, we show that the MAKR2 inhibitory effect on TMK1 signaling is antagonized by auxin itself, which triggers rapid MAKR2 membrane dissociation in a TMK1-dependent manner. Our findings suggest that the timing of the root gravitropic response is orchestrated by the reversible inhibition of the TMK1 signaling pathway at the cell surface."}],"has_accepted_license":"1","file":[{"date_updated":"2021-02-04T11:37:50Z","creator":"dernst","date_created":"2021-02-04T11:37:50Z","file_size":3458646,"file_id":"9090","content_type":"application/pdf","access_level":"open_access","file_name":"2021_CurrentBiology_MarquesBueno.pdf","success":1,"checksum":"30b3393d841fb2b1e2b22fb42b5c8fff","relation":"main_file"}],"department":[{"_id":"JiFr"}],"month":"01","user_id":"c635000d-4b10-11ee-a964-aac5a93f6ac1","citation":{"ama":"Marquès-Bueno M, Armengot L, Noack L, et al. Auxin-regulated reversible inhibition of TMK1 signaling by MAKR2 modulates the dynamics of root gravitropism. <i>Current Biology</i>. 2021;31(1). doi:<a href=\"https://doi.org/10.1016/j.cub.2020.10.011\">10.1016/j.cub.2020.10.011</a>","ieee":"M. Marquès-Bueno <i>et al.</i>, “Auxin-regulated reversible inhibition of TMK1 signaling by MAKR2 modulates the dynamics of root gravitropism,” <i>Current Biology</i>, vol. 31, no. 1. Elsevier, 2021.","short":"M. Marquès-Bueno, L. Armengot, L. Noack, J. Bareille, L. Rodriguez Solovey, M. Platre, V. Bayle, M. Liu, D. Opdenacker, S. Vanneste, B. Möller, Z. Nimchuk, T. Beeckman, A. Caño-Delgado, J. Friml, Y. Jaillais, Current Biology 31 (2021).","chicago":"Marquès-Bueno, MM, L Armengot, LC Noack, J Bareille, Lesia Rodriguez Solovey, MP Platre, V Bayle, et al. “Auxin-Regulated Reversible Inhibition of TMK1 Signaling by MAKR2 Modulates the Dynamics of Root Gravitropism.” <i>Current Biology</i>. Elsevier, 2021. <a href=\"https://doi.org/10.1016/j.cub.2020.10.011\">https://doi.org/10.1016/j.cub.2020.10.011</a>.","ista":"Marquès-Bueno M, Armengot L, Noack L, Bareille J, Rodriguez Solovey L, Platre M, Bayle V, Liu M, Opdenacker D, Vanneste S, Möller B, Nimchuk Z, Beeckman T, Caño-Delgado A, Friml J, Jaillais Y. 2021. Auxin-regulated reversible inhibition of TMK1 signaling by MAKR2 modulates the dynamics of root gravitropism. Current Biology. 31(1).","apa":"Marquès-Bueno, M., Armengot, L., Noack, L., Bareille, J., Rodriguez Solovey, L., Platre, M., … Jaillais, Y. (2021). Auxin-regulated reversible inhibition of TMK1 signaling by MAKR2 modulates the dynamics of root gravitropism. <i>Current Biology</i>. Elsevier. <a href=\"https://doi.org/10.1016/j.cub.2020.10.011\">https://doi.org/10.1016/j.cub.2020.10.011</a>","mla":"Marquès-Bueno, MM, et al. “Auxin-Regulated Reversible Inhibition of TMK1 Signaling by MAKR2 Modulates the Dynamics of Root Gravitropism.” <i>Current Biology</i>, vol. 31, no. 1, Elsevier, 2021, doi:<a href=\"https://doi.org/10.1016/j.cub.2020.10.011\">10.1016/j.cub.2020.10.011</a>."},"issue":"1","language":[{"iso":"eng"}],"oa":1},{"related_material":{"link":[{"relation":"erratum","url":"10.1093/plphys/kiab380"}],"record":[{"id":"11626","status":"public","relation":"dissertation_contains"},{"id":"10083","relation":"dissertation_contains","status":"public"}]},"external_id":{"pmid":["33734402"],"isi":["000671555900031"]},"isi":1,"year":"2021","status":"public","publication":"Plant Physiology","project":[{"_id":"261099A6-B435-11E9-9278-68D0E5697425","call_identifier":"H2020","grant_number":"742985","name":"Tracing Evolution of Auxin Transport and Polarity in Plants"},{"_id":"26538374-B435-11E9-9278-68D0E5697425","name":"Molecular mechanisms of endocytic cargo recognition in plants","grant_number":"I03630","call_identifier":"FWF"}],"acknowledgement":"We thank Ivan Kulik for developing the Chip’n’Dale apparatus with Lanxin Li; the IST machine shop and the Bioimaging facility for their excellent support; Matouš Glanc and Matyáš Fendrych for their valuable discussions and help; Barbara Casillas-Perez for her help with statistics. This project has received funding from the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation program (grant agreement No 742985). A.J. is supported by funding from the Austrian Science Fund (FWF): I3630B25 to J.F. ","date_published":"2021-06-01T00:00:00Z","ec_funded":1,"pmid":1,"publisher":"Oxford University Press","article_processing_charge":"Yes (in subscription journal)","doi":"10.1093/plphys/kiab134","type":"journal_article","_id":"9287","date_updated":"2024-10-29T10:22:43Z","ddc":["580"],"page":"1122–1142","quality_controlled":"1","month":"06","file":[{"content_type":"application/pdf","access_level":"open_access","file_name":"2021_PlantPhysio_Narasimhan.pdf","success":1,"checksum":"532bb9469d3b665907f06df8c383eade","relation":"main_file","creator":"cziletti","date_updated":"2021-11-11T15:07:51Z","date_created":"2021-11-11T15:07:51Z","file_size":2289127,"file_id":"10273"}],"department":[{"_id":"JiFr"}],"language":[{"iso":"eng"}],"oa":1,"user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","citation":{"chicago":"Narasimhan, Madhumitha, Michelle C Gallei, Shutang Tan, Alexander J Johnson, Inge Verstraeten, Lanxin Li, Lesia Rodriguez Solovey, et al. “Systematic Analysis of Specific and Nonspecific Auxin Effects on Endocytosis and Trafficking.” <i>Plant Physiology</i>. Oxford University Press, 2021. <a href=\"https://doi.org/10.1093/plphys/kiab134\">https://doi.org/10.1093/plphys/kiab134</a>.","ista":"Narasimhan M, Gallei MC, Tan S, Johnson AJ, Verstraeten I, Li L, Rodriguez Solovey L, Han H, Himschoot E, Wang R, Vanneste S, Sánchez-Simarro J, Aniento F, Adamowski M, Friml J. 2021. Systematic analysis of specific and nonspecific auxin effects on endocytosis and trafficking. Plant Physiology. 186(2), 1122–1142.","apa":"Narasimhan, M., Gallei, M. C., Tan, S., Johnson, A. J., Verstraeten, I., Li, L., … Friml, J. (2021). Systematic analysis of specific and nonspecific auxin effects on endocytosis and trafficking. <i>Plant Physiology</i>. Oxford University Press. <a href=\"https://doi.org/10.1093/plphys/kiab134\">https://doi.org/10.1093/plphys/kiab134</a>","mla":"Narasimhan, Madhumitha, et al. “Systematic Analysis of Specific and Nonspecific Auxin Effects on Endocytosis and Trafficking.” <i>Plant Physiology</i>, vol. 186, no. 2, Oxford University Press, 2021, pp. 1122–1142, doi:<a href=\"https://doi.org/10.1093/plphys/kiab134\">10.1093/plphys/kiab134</a>.","ama":"Narasimhan M, Gallei MC, Tan S, et al. Systematic analysis of specific and nonspecific auxin effects on endocytosis and trafficking. <i>Plant Physiology</i>. 2021;186(2):1122–1142. doi:<a href=\"https://doi.org/10.1093/plphys/kiab134\">10.1093/plphys/kiab134</a>","ieee":"M. Narasimhan <i>et al.</i>, “Systematic analysis of specific and nonspecific auxin effects on endocytosis and trafficking,” <i>Plant Physiology</i>, vol. 186, no. 2. Oxford University Press, pp. 1122–1142, 2021.","short":"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."},"issue":"2","oa_version":"Published Version","title":"Systematic analysis of specific and nonspecific auxin effects on endocytosis and trafficking","day":"01","author":[{"orcid":"0000-0002-8600-0671","first_name":"Madhumitha","id":"44BF24D0-F248-11E8-B48F-1D18A9856A87","full_name":"Narasimhan, Madhumitha","last_name":"Narasimhan"},{"first_name":"Michelle C","orcid":"0000-0003-1286-7368","id":"35A03822-F248-11E8-B48F-1D18A9856A87","full_name":"Gallei, Michelle C","last_name":"Gallei"},{"first_name":"Shutang","orcid":"0000-0002-0471-8285","full_name":"Tan, Shutang","id":"2DE75584-F248-11E8-B48F-1D18A9856A87","last_name":"Tan"},{"id":"46A62C3A-F248-11E8-B48F-1D18A9856A87","full_name":"Johnson, Alexander J","last_name":"Johnson","orcid":"0000-0002-2739-8843","first_name":"Alexander J"},{"id":"362BF7FE-F248-11E8-B48F-1D18A9856A87","full_name":"Verstraeten, Inge","last_name":"Verstraeten","first_name":"Inge","orcid":"0000-0001-7241-2328"},{"orcid":"0000-0002-5607-272X","first_name":"Lanxin","last_name":"Li","full_name":"Li, Lanxin","id":"367EF8FA-F248-11E8-B48F-1D18A9856A87"},{"first_name":"Lesia","orcid":"0000-0002-7244-7237","last_name":"Rodriguez Solovey","id":"3922B506-F248-11E8-B48F-1D18A9856A87","full_name":"Rodriguez Solovey, Lesia"},{"full_name":"Han, Huibin","id":"31435098-F248-11E8-B48F-1D18A9856A87","last_name":"Han","first_name":"Huibin"},{"first_name":"E","last_name":"Himschoot","full_name":"Himschoot, E"},{"first_name":"R","full_name":"Wang, R","last_name":"Wang"},{"last_name":"Vanneste","full_name":"Vanneste, S","first_name":"S"},{"last_name":"Sánchez-Simarro","full_name":"Sánchez-Simarro, J","first_name":"J"},{"full_name":"Aniento, F","last_name":"Aniento","first_name":"F"},{"full_name":"Adamowski, Maciek","id":"45F536D2-F248-11E8-B48F-1D18A9856A87","last_name":"Adamowski","first_name":"Maciek","orcid":"0000-0001-6463-5257"},{"orcid":"0000-0002-8302-7596","first_name":"Jiří","id":"4159519E-F248-11E8-B48F-1D18A9856A87","full_name":"Friml, Jiří","last_name":"Friml"}],"date_created":"2021-03-26T12:08:38Z","article_type":"original","volume":186,"acknowledged_ssus":[{"_id":"M-Shop"},{"_id":"Bio"}],"abstract":[{"lang":"eng","text":"The phytohormone auxin and its directional transport through tissues are intensively studied. However, a mechanistic understanding of auxin-mediated feedback on endocytosis and polar distribution of PIN auxin transporters remains limited due to contradictory observations and interpretations. Here, we used state-of-the-art methods to reexamine the\r\nauxin effects on PIN endocytic trafficking. We used high auxin concentrations or longer treatments versus lower concentrations and shorter treatments of natural (IAA) and synthetic (NAA) auxins to distinguish between specific and nonspecific effects. Longer treatments of both auxins interfere with Brefeldin A-mediated intracellular PIN2 accumulation and also with general aggregation of endomembrane compartments. NAA treatment decreased the internalization of the endocytic tracer dye, FM4-64; however, NAA treatment also affected the number, distribution, and compartment identity of the early endosome/trans-Golgi network (EE/TGN), rendering the FM4-64 endocytic assays at high NAA concentrations unreliable. To circumvent these nonspecific effects of NAA and IAA affecting the endomembrane system, we opted for alternative approaches visualizing the endocytic events directly at the plasma membrane (PM). Using Total Internal Reflection Fluorescence (TIRF) microscopy, we saw no significant effects of IAA or NAA treatments on the incidence and dynamics of clathrin foci, implying that these treatments do not affect the overall endocytosis rate. However, both NAA and IAA at low concentrations rapidly and specifically promoted endocytosis of photo-converted PIN2 from the PM. These analyses identify a specific effect of NAA and IAA on PIN2 endocytosis, thus contributing to its\r\npolarity maintenance and furthermore illustrate that high auxin levels have nonspecific effects on trafficking and endomembrane compartments. "}],"tmp":{"name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","short":"CC BY (4.0)"},"intvolume":"       186","has_accepted_license":"1","file_date_updated":"2021-11-11T15:07:51Z","publication_identifier":{"eissn":["1532-2548"],"issn":["0032-0889"]},"publication_status":"published"},{"month":"09","department":[{"_id":"JiFr"},{"_id":"NanoFab"}],"article_number":"266395","oa":1,"language":[{"iso":"eng"}],"citation":{"mla":"Li, Lanxin, et al. “Cell Surface and Intracellular Auxin Signalling for H+-Fluxes in Root Growth.” <i>Research Square</i>, 266395, doi:<a href=\"https://doi.org/10.21203/rs.3.rs-266395/v3\">10.21203/rs.3.rs-266395/v3</a>.","apa":"Li, L., Verstraeten, I., Roosjen, M., Takahashi, K., Rodriguez Solovey, L., Merrin, J., … Friml, J. (n.d.). Cell surface and intracellular auxin signalling for H+-fluxes in root growth. <i>Research Square</i>. <a href=\"https://doi.org/10.21203/rs.3.rs-266395/v3\">https://doi.org/10.21203/rs.3.rs-266395/v3</a>","chicago":"Li, Lanxin, Inge Verstraeten, Mark Roosjen, Koji Takahashi, Lesia Rodriguez Solovey, Jack Merrin, Jian Chen, et al. “Cell Surface and Intracellular Auxin Signalling for H+-Fluxes in Root Growth.” <i>Research Square</i>, n.d. <a href=\"https://doi.org/10.21203/rs.3.rs-266395/v3\">https://doi.org/10.21203/rs.3.rs-266395/v3</a>.","ista":"Li L, Verstraeten I, Roosjen M, Takahashi K, Rodriguez Solovey L, Merrin J, Chen J, Shabala L, Smet W, Ren H, Vanneste S, Shabala S, De Rybel B, Weijers D, Kinoshita T, Gray WM, Friml J. Cell surface and intracellular auxin signalling for H+-fluxes in root growth. Research Square, 266395.","short":"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.).","ieee":"L. Li <i>et al.</i>, “Cell surface and intracellular auxin signalling for H+-fluxes in root growth,” <i>Research Square</i>. .","ama":"Li L, Verstraeten I, Roosjen M, et al. Cell surface and intracellular auxin signalling for H+-fluxes in root growth. <i>Research Square</i>. doi:<a href=\"https://doi.org/10.21203/rs.3.rs-266395/v3\">10.21203/rs.3.rs-266395/v3</a>"},"user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","author":[{"orcid":"0000-0002-5607-272X","first_name":"Lanxin","full_name":"Li, Lanxin","id":"367EF8FA-F248-11E8-B48F-1D18A9856A87","last_name":"Li"},{"first_name":"Inge","orcid":"0000-0001-7241-2328","last_name":"Verstraeten","id":"362BF7FE-F248-11E8-B48F-1D18A9856A87","full_name":"Verstraeten, Inge"},{"full_name":"Roosjen, Mark","last_name":"Roosjen","first_name":"Mark"},{"first_name":"Koji","last_name":"Takahashi","full_name":"Takahashi, Koji"},{"last_name":"Rodriguez Solovey","id":"3922B506-F248-11E8-B48F-1D18A9856A87","full_name":"Rodriguez Solovey, Lesia","first_name":"Lesia","orcid":"0000-0002-7244-7237"},{"id":"4515C308-F248-11E8-B48F-1D18A9856A87","full_name":"Merrin, Jack","last_name":"Merrin","orcid":"0000-0001-5145-4609","first_name":"Jack"},{"first_name":"Jian","full_name":"Chen, Jian","last_name":"Chen"},{"first_name":"Lana","full_name":"Shabala, Lana","last_name":"Shabala"},{"full_name":"Smet, Wouter","last_name":"Smet","first_name":"Wouter"},{"first_name":"Hong","last_name":"Ren","full_name":"Ren, Hong"},{"last_name":"Vanneste","full_name":"Vanneste, Steffen","first_name":"Steffen"},{"full_name":"Shabala, Sergey","last_name":"Shabala","first_name":"Sergey"},{"last_name":"De Rybel","full_name":"De Rybel, Bert","first_name":"Bert"},{"first_name":"Dolf","last_name":"Weijers","full_name":"Weijers, Dolf"},{"first_name":"Toshinori","last_name":"Kinoshita","full_name":"Kinoshita, Toshinori"},{"first_name":"William M.","full_name":"Gray, William M.","last_name":"Gray"},{"last_name":"Friml","full_name":"Friml, Jiří","id":"4159519E-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0002-8302-7596","first_name":"Jiří"}],"day":"09","oa_version":"Preprint","title":"Cell surface and intracellular auxin signalling for H+-fluxes in root growth","date_created":"2021-10-06T08:56:22Z","tmp":{"name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","short":"CC BY (4.0)"},"abstract":[{"text":"Growth regulation tailors plant development to its environment. A showcase is response to gravity, where shoots bend up and roots down1. This paradox is based on opposite effects of the phytohormone auxin, which promotes cell expansion in shoots, while inhibiting it in roots via a yet unknown cellular mechanism2. Here, by combining microfluidics, live imaging, genetic engineering and phospho-proteomics in Arabidopsis thaliana, we advance our understanding how auxin inhibits root growth. We show that auxin activates two distinct, antagonistically acting signalling pathways that converge on the rapid regulation of the apoplastic pH, a causative growth determinant. Cell surface-based TRANSMEMBRANE KINASE1 (TMK1) interacts with and mediates phosphorylation and activation of plasma membrane H+-ATPases for apoplast acidification, while intracellular canonical auxin signalling promotes net cellular H+-influx, causing apoplast alkalinisation. The simultaneous activation of these two counteracting mechanisms poises the root for a rapid, fine-tuned growth modulation while navigating complex soil environment.","lang":"eng"}],"acknowledged_ssus":[{"_id":"LifeSc"},{"_id":"M-Shop"},{"_id":"Bio"}],"publication_identifier":{"issn":["2693-5015"]},"publication_status":"accepted","year":"2021","related_material":{"record":[{"relation":"dissertation_contains","status":"public","id":"10083"},{"relation":"later_version","status":"public","id":"10223"}]},"project":[{"name":"International IST Doctoral Program","grant_number":"665385","call_identifier":"H2020","_id":"2564DBCA-B435-11E9-9278-68D0E5697425"},{"call_identifier":"H2020","name":"Tracing Evolution of Auxin Transport and Polarity in Plants","grant_number":"742985","_id":"261099A6-B435-11E9-9278-68D0E5697425"},{"_id":"26538374-B435-11E9-9278-68D0E5697425","name":"Molecular mechanisms of endocytic cargo recognition in plants","grant_number":"I03630","call_identifier":"FWF"},{"grant_number":"25351","name":"A Case Study of Plant Growth Regulation: Molecular Mechanism of Auxin-mediated Rapid Growth Inhibition in Arabidopsis Root","_id":"26B4D67E-B435-11E9-9278-68D0E5697425"}],"status":"public","publication":"Research Square","ec_funded":1,"acknowledgement":"We thank Nataliia Gnyliukh and Lukas Hörmayer for technical assistance and Nadine Paris for sharing PM-Cyto seeds. We gratefully acknowledge Life Science, Machine Shop and Bioimaging Facilities of IST Austria. This project has received funding from the European Research Council Advanced Grant (ETAP-742985) and the Austrian Science Fund (FWF) I 3630-B25 to J.F., the National Institutes of Health (GM067203) to W.M.G., the Netherlands Organization for Scientific Research (NWO; VIDI-864.13.001.), the Research Foundation-Flanders (FWO; Odysseus II G0D0515N) and a European Research Council Starting Grant (TORPEDO-714055) to W.S. and B.D.R., the VICI grant (865.14.001) from the Netherlands Organization for Scientific Research to M.R and D.W., the Australian Research Council and China National Distinguished Expert Project (WQ20174400441) to S.S., the MEXT/JSPS KAKENHI to K.T. (20K06685) and T.K. (20H05687 and 20H05910),  the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie Grant Agreement No. 665385 and the DOC Fellowship of the Austrian Academy of Sciences to L.L., the China Scholarship Council to J.C.","date_published":"2021-09-09T00:00:00Z","doi":"10.21203/rs.3.rs-266395/v3","article_processing_charge":"No","date_updated":"2024-10-29T10:22:44Z","_id":"10095","type":"preprint","main_file_link":[{"open_access":"1","url":"https://www.doi.org/10.21203/rs.3.rs-266395/v3"}]},{"intvolume":"       599","abstract":[{"lang":"eng","text":"Growth regulation tailors development in plants to their environment. A prominent example of this is the response to gravity, in which shoots bend up and roots bend down1. This paradox is based on opposite effects of the phytohormone auxin, which promotes cell expansion in shoots while inhibiting it in roots via a yet unknown cellular mechanism2. Here, by combining microfluidics, live imaging, genetic engineering and phosphoproteomics in Arabidopsis thaliana, we advance understanding of how auxin inhibits root growth. We show that auxin activates two distinct, antagonistically acting signalling pathways that converge on rapid regulation of apoplastic pH, a causative determinant of growth. Cell surface-based TRANSMEMBRANE KINASE1 (TMK1) interacts with and mediates phosphorylation and activation of plasma membrane H+-ATPases for apoplast acidification, while intracellular canonical auxin signalling promotes net cellular H+ influx, causing apoplast alkalinization. Simultaneous activation of these two counteracting mechanisms poises roots for rapid, fine-tuned growth modulation in navigating complex soil environments."}],"acknowledged_ssus":[{"_id":"LifeSc"},{"_id":"M-Shop"},{"_id":"Bio"}],"publication_status":"published","publication_identifier":{"issn":["00280836"],"eissn":["14764687"]},"author":[{"full_name":"Li, Lanxin","id":"367EF8FA-F248-11E8-B48F-1D18A9856A87","last_name":"Li","first_name":"Lanxin","orcid":"0000-0002-5607-272X"},{"full_name":"Verstraeten, Inge","id":"362BF7FE-F248-11E8-B48F-1D18A9856A87","last_name":"Verstraeten","orcid":"0000-0001-7241-2328","first_name":"Inge"},{"full_name":"Roosjen, Mark","last_name":"Roosjen","first_name":"Mark"},{"last_name":"Takahashi","full_name":"Takahashi, Koji","first_name":"Koji"},{"full_name":"Rodriguez Solovey, Lesia","id":"3922B506-F248-11E8-B48F-1D18A9856A87","last_name":"Rodriguez Solovey","orcid":"0000-0002-7244-7237","first_name":"Lesia"},{"last_name":"Merrin","full_name":"Merrin, Jack","id":"4515C308-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0001-5145-4609","first_name":"Jack"},{"first_name":"Jian","full_name":"Chen, Jian","last_name":"Chen"},{"full_name":"Shabala, Lana","last_name":"Shabala","first_name":"Lana"},{"first_name":"Wouter","full_name":"Smet, Wouter","last_name":"Smet"},{"last_name":"Ren","full_name":"Ren, Hong","first_name":"Hong"},{"first_name":"Steffen","last_name":"Vanneste","full_name":"Vanneste, Steffen"},{"first_name":"Sergey","last_name":"Shabala","full_name":"Shabala, Sergey"},{"last_name":"De Rybel","full_name":"De Rybel, Bert","first_name":"Bert"},{"first_name":"Dolf","full_name":"Weijers, Dolf","last_name":"Weijers"},{"first_name":"Toshinori","full_name":"Kinoshita, Toshinori","last_name":"Kinoshita"},{"first_name":"William M.","last_name":"Gray","full_name":"Gray, William M."},{"last_name":"Friml","full_name":"Friml, Jiří","id":"4159519E-F248-11E8-B48F-1D18A9856A87","first_name":"Jiří","orcid":"0000-0002-8302-7596"}],"scopus_import":"1","day":"11","oa_version":"Preprint","title":"Cell surface and intracellular auxin signalling for H<sup>+</sup> fluxes in root growth","volume":599,"article_type":"original","date_created":"2021-11-07T23:01:25Z","oa":1,"language":[{"iso":"eng"}],"issue":"7884","citation":{"ieee":"L. Li <i>et al.</i>, “Cell surface and intracellular auxin signalling for H<sup>+</sup> fluxes in root growth,” <i>Nature</i>, vol. 599, no. 7884. Springer Nature, pp. 273–277, 2021.","short":"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.","ama":"Li L, Verstraeten I, Roosjen M, et al. Cell surface and intracellular auxin signalling for H<sup>+</sup> fluxes in root growth. <i>Nature</i>. 2021;599(7884):273-277. doi:<a href=\"https://doi.org/10.1038/s41586-021-04037-6\">10.1038/s41586-021-04037-6</a>","apa":"Li, L., Verstraeten, I., Roosjen, M., Takahashi, K., Rodriguez Solovey, L., Merrin, J., … Friml, J. (2021). Cell surface and intracellular auxin signalling for H<sup>+</sup> fluxes in root growth. <i>Nature</i>. Springer Nature. <a href=\"https://doi.org/10.1038/s41586-021-04037-6\">https://doi.org/10.1038/s41586-021-04037-6</a>","mla":"Li, Lanxin, et al. “Cell Surface and Intracellular Auxin Signalling for H<sup>+</sup> Fluxes in Root Growth.” <i>Nature</i>, vol. 599, no. 7884, Springer Nature, 2021, pp. 273–77, doi:<a href=\"https://doi.org/10.1038/s41586-021-04037-6\">10.1038/s41586-021-04037-6</a>.","ista":"Li L, Verstraeten I, Roosjen M, Takahashi K, Rodriguez Solovey L, Merrin J, Chen J, Shabala L, Smet W, Ren H, Vanneste S, Shabala S, De Rybel B, Weijers D, Kinoshita T, Gray WM, Friml J. 2021. Cell surface and intracellular auxin signalling for H<sup>+</sup> fluxes in root growth. Nature. 599(7884), 273–277.","chicago":"Li, Lanxin, Inge Verstraeten, Mark Roosjen, Koji Takahashi, Lesia Rodriguez Solovey, Jack Merrin, Jian Chen, et al. “Cell Surface and Intracellular Auxin Signalling for H<sup>+</sup> Fluxes in Root Growth.” <i>Nature</i>. Springer Nature, 2021. <a href=\"https://doi.org/10.1038/s41586-021-04037-6\">https://doi.org/10.1038/s41586-021-04037-6</a>."},"user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","month":"11","department":[{"_id":"JiFr"},{"_id":"NanoFab"}],"page":"273-277","main_file_link":[{"url":"https://www.doi.org/10.21203/rs.3.rs-266395/v3","open_access":"1"}],"quality_controlled":"1","doi":"10.1038/s41586-021-04037-6","article_processing_charge":"No","publisher":"Springer Nature","date_updated":"2024-10-29T10:22:45Z","_id":"10223","type":"journal_article","project":[{"_id":"261099A6-B435-11E9-9278-68D0E5697425","grant_number":"742985","name":"Tracing Evolution of Auxin Transport and Polarity in Plants","call_identifier":"H2020"},{"_id":"26538374-B435-11E9-9278-68D0E5697425","grant_number":"I03630","name":"Molecular mechanisms of endocytic cargo recognition in plants","call_identifier":"FWF"},{"_id":"2564DBCA-B435-11E9-9278-68D0E5697425","grant_number":"665385","name":"International IST Doctoral Program","call_identifier":"H2020"},{"grant_number":"25351","name":"A Case Study of Plant Growth Regulation: Molecular Mechanism of Auxin-mediated Rapid Growth Inhibition in Arabidopsis Root","_id":"26B4D67E-B435-11E9-9278-68D0E5697425"}],"publication":"Nature","status":"public","pmid":1,"ec_funded":1,"acknowledgement":"We thank N. Gnyliukh and L. Hörmayer for technical assistance and N. Paris for sharing PM-Cyto seeds. We gratefully acknowledge the Life Science, Machine Shop and Bioimaging Facilities of IST Austria. This project has received funding from the European Research Council Advanced Grant (ETAP-742985) and the Austrian Science Fund (FWF) under I 3630-B25 to J.F., the National Institutes of Health (GM067203) to W.M.G., the Netherlands Organization for Scientific Research (NWO; VIDI-864.13.001), Research Foundation-Flanders (FWO; Odysseus II G0D0515N) and a European Research Council Starting Grant (TORPEDO-714055) to W.S. and B.D.R., the VICI grant (865.14.001) from the Netherlands Organization for Scientific Research to M.R. and D.W., the Australian Research Council and China National Distinguished Expert Project (WQ20174400441) to S.S., the MEXT/JSPS KAKENHI to K.T. (20K06685) and T.K. (20H05687 and 20H05910), the European Union’s Horizon 2020 research and innovation programme under Marie Skłodowska-Curie grant agreement no. 665385 and the DOC Fellowship of the Austrian Academy of Sciences to L.L., and the China Scholarship Council to J.C.","date_published":"2021-11-11T00:00:00Z","year":"2021","isi":1,"external_id":{"pmid":["34707283"],"isi":["000713338100006"]},"related_material":{"record":[{"relation":"earlier_version","status":"public","id":"10095"}],"link":[{"relation":"press_release","url":"https://ist.ac.at/en/news/stop-and-grow/","description":"News on IST Webpage"}]},"keyword":["Multidisciplinary"]},{"isi":1,"year":"2020","external_id":{"isi":["000583031800041"],"pmid":["33122378"]},"related_material":{"link":[{"relation":"press_release","description":"News on IST Homepage","url":"https://ist.ac.at/en/news/molecular-compass-for-cell-orientation/"}]},"pmid":1,"ec_funded":1,"date_published":"2020-10-30T00:00:00Z","acknowledgement":"We acknowledge M. Glanc and Y. Zhang for providing entryclones; Vienna Biocenter Core Facilities (VBCF) for recombinantprotein production and purification; Vienna Biocenter Massspectrometry Facility, Bioimaging, and Life Science Facilities at IST Austria and Proteomics Core Facility CEITEC for a great assistance.Funding:This project received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement 742985) and Austrian Science Fund (FWF): I 3630-B25 to J.F.and by grants from the Austrian Academy of Science through the Gregor Mendel Institute (Y.B.) and the Austrian Agency for International Cooperation in Education and Research (D.D.); the Netherlands Organization for Scientific Research (NWO; VIDI-864.13.001) (W.S.); the Research Foundation–Flanders (FWO;Odysseus II G0D0515N) and a European Research Council grant (ERC; StG TORPEDO; 714055) to B.D.R., B.Y., and E.M.; and the Hertha Firnberg Programme postdoctoral fellowship (T-947) from the FWF Austrian Science Fund to E.S.-L.; J.H. is the recipient of a DOC Fellowship of the Austrian Academy of Sciences at IST Austria.","project":[{"_id":"261099A6-B435-11E9-9278-68D0E5697425","name":"Tracing Evolution of Auxin Transport and Polarity in Plants","grant_number":"742985","call_identifier":"H2020"},{"_id":"26538374-B435-11E9-9278-68D0E5697425","name":"Molecular mechanisms of endocytic cargo recognition in plants","grant_number":"I03630","call_identifier":"FWF"},{"grant_number":"25239","name":"Cell surface receptor complexes for PIN polarity and auxin-mediated development","_id":"2699E3D2-B435-11E9-9278-68D0E5697425"}],"status":"public","publication":"Science","date_updated":"2023-09-05T12:02:35Z","_id":"8721","type":"journal_article","doi":"10.1126/science.aba3178","article_processing_charge":"No","publisher":"American Association for the Advancement of Science","main_file_link":[{"url":"https://europepmc.org/article/MED/33122378#free-full-text","open_access":"1"}],"quality_controlled":"1","page":"550-557","department":[{"_id":"JiFr"}],"month":"10","issue":"6516","citation":{"ama":"Hajny J, Prat T, Rydza N, et al. Receptor kinase module targets PIN-dependent auxin transport during canalization. <i>Science</i>. 2020;370(6516):550-557. doi:<a href=\"https://doi.org/10.1126/science.aba3178\">10.1126/science.aba3178</a>","ieee":"J. Hajny <i>et al.</i>, “Receptor kinase module targets PIN-dependent auxin transport during canalization,” <i>Science</i>, vol. 370, no. 6516. American Association for the Advancement of Science, pp. 550–557, 2020.","short":"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.","chicago":"Hajny, Jakub, Tomas Prat, N Rydza, Lesia Rodriguez Solovey, Shutang Tan, Inge Verstraeten, David Domjan, et al. “Receptor Kinase Module Targets PIN-Dependent Auxin Transport during Canalization.” <i>Science</i>. American Association for the Advancement of Science, 2020. <a href=\"https://doi.org/10.1126/science.aba3178\">https://doi.org/10.1126/science.aba3178</a>.","ista":"Hajny J, Prat T, Rydza N, Rodriguez Solovey L, Tan S, Verstraeten I, Domjan D, Mazur E, Smakowska-Luzan E, Smet W, Mor E, Nolf J, Yang B, Grunewald W, Molnar G, Belkhadir Y, De Rybel B, Friml J. 2020. Receptor kinase module targets PIN-dependent auxin transport during canalization. Science. 370(6516), 550–557.","apa":"Hajny, J., Prat, T., Rydza, N., Rodriguez Solovey, L., Tan, S., Verstraeten, I., … Friml, J. (2020). Receptor kinase module targets PIN-dependent auxin transport during canalization. <i>Science</i>. American Association for the Advancement of Science. <a href=\"https://doi.org/10.1126/science.aba3178\">https://doi.org/10.1126/science.aba3178</a>","mla":"Hajny, Jakub, et al. “Receptor Kinase Module Targets PIN-Dependent Auxin Transport during Canalization.” <i>Science</i>, vol. 370, no. 6516, American Association for the Advancement of Science, 2020, pp. 550–57, doi:<a href=\"https://doi.org/10.1126/science.aba3178\">10.1126/science.aba3178</a>."},"user_id":"c635000d-4b10-11ee-a964-aac5a93f6ac1","oa":1,"language":[{"iso":"eng"}],"volume":370,"article_type":"original","date_created":"2020-11-02T10:04:46Z","author":[{"orcid":"0000-0003-2140-7195","first_name":"Jakub","last_name":"Hajny","full_name":"Hajny, Jakub","id":"4800CC20-F248-11E8-B48F-1D18A9856A87"},{"first_name":"Tomas","last_name":"Prat","full_name":"Prat, Tomas","id":"3DA3BFEE-F248-11E8-B48F-1D18A9856A87"},{"first_name":"N","last_name":"Rydza","full_name":"Rydza, N"},{"id":"3922B506-F248-11E8-B48F-1D18A9856A87","full_name":"Rodriguez Solovey, Lesia","last_name":"Rodriguez Solovey","first_name":"Lesia","orcid":"0000-0002-7244-7237"},{"full_name":"Tan, Shutang","id":"2DE75584-F248-11E8-B48F-1D18A9856A87","last_name":"Tan","first_name":"Shutang","orcid":"0000-0002-0471-8285"},{"orcid":"0000-0001-7241-2328","first_name":"Inge","last_name":"Verstraeten","id":"362BF7FE-F248-11E8-B48F-1D18A9856A87","full_name":"Verstraeten, Inge"},{"last_name":"Domjan","full_name":"Domjan, David","id":"C684CD7A-257E-11EA-9B6F-D8588B4F947F","orcid":"0000-0003-2267-106X","first_name":"David"},{"first_name":"E","full_name":"Mazur, E","last_name":"Mazur"},{"full_name":"Smakowska-Luzan, E","last_name":"Smakowska-Luzan","first_name":"E"},{"last_name":"Smet","full_name":"Smet, W","first_name":"W"},{"last_name":"Mor","full_name":"Mor, E","first_name":"E"},{"last_name":"Nolf","full_name":"Nolf, J","first_name":"J"},{"full_name":"Yang, B","last_name":"Yang","first_name":"B"},{"last_name":"Grunewald","full_name":"Grunewald, W","first_name":"W"},{"last_name":"Molnar","id":"34F1AF46-F248-11E8-B48F-1D18A9856A87","full_name":"Molnar, Gergely","first_name":"Gergely"},{"first_name":"Y","last_name":"Belkhadir","full_name":"Belkhadir, Y"},{"first_name":"B","full_name":"De Rybel, B","last_name":"De Rybel"},{"first_name":"Jiří","orcid":"0000-0002-8302-7596","id":"4159519E-F248-11E8-B48F-1D18A9856A87","full_name":"Friml, Jiří","last_name":"Friml"}],"scopus_import":"1","day":"30","title":"Receptor kinase module targets PIN-dependent auxin transport during canalization","oa_version":"Published Version","publication_status":"published","publication_identifier":{"eissn":["1095-9203"],"issn":["0036-8075"]},"intvolume":"       370","abstract":[{"lang":"eng","text":"Spontaneously arising channels that transport the phytohormone auxin provide positional cues for self-organizing aspects of plant development such as flexible vasculature regeneration or its patterning during leaf venation. The auxin canalization hypothesis proposes a feedback between auxin signaling and transport as the underlying mechanism, but molecular players await discovery. We identified part of the machinery that routes auxin transport. The auxin-regulated receptor CAMEL (Canalization-related Auxin-regulated Malectin-type RLK) together with CANAR (Canalization-related Receptor-like kinase) interact with and phosphorylate PIN auxin transporters. camel and canar mutants are impaired in PIN1 subcellular trafficking and auxin-mediated PIN polarization, which macroscopically manifests as defects in leaf venation and vasculature regeneration after wounding. The CAMEL-CANAR receptor complex is part of the auxin feedback that coordinates polarization of individual cells during auxin canalization."}],"acknowledged_ssus":[{"_id":"Bio"},{"_id":"LifeSc"}]},{"isi":1,"year":"2020","related_material":{"record":[{"status":"public","relation":"dissertation_contains","id":"10083"}]},"external_id":{"isi":["000599903600014"],"pmid":["33310852"]},"status":"public","publication":"Science Advances","project":[{"grant_number":"742985","name":"Tracing Evolution of Auxin Transport and Polarity in Plants","call_identifier":"H2020","_id":"261099A6-B435-11E9-9278-68D0E5697425"},{"call_identifier":"FWF","name":"Molecular mechanisms of endocytic cargo recognition in plants","grant_number":"I03630","_id":"26538374-B435-11E9-9278-68D0E5697425"},{"_id":"26B4D67E-B435-11E9-9278-68D0E5697425","name":"A Case Study of Plant Growth Regulation: Molecular Mechanism of Auxin-mediated Rapid Growth Inhibition in Arabidopsis Root","grant_number":"25351"}],"ec_funded":1,"pmid":1,"acknowledgement":"We thank C.Löhne (Botanic Gardens, University of Bonn) for providing us with A. trichopoda. We would like to thank T.Han, A.Mally (IST, Austria), and C.Hartinger (University of Oxford) for constructive comment and careful reading. Funding: The research leading to these results has received funding from the European Union’s Horizon 2020 Research and Innovation Programme (ERC grant agreement number 742985), Austrian Science Fund (FWF, grant number I 3630-B25), DOC Fellowship of the Austrian Academy of Sciences, and IST Fellow program. ","date_published":"2020-12-11T00:00:00Z","article_processing_charge":"No","doi":"10.1126/sciadv.abc8895","publisher":"AAAS","_id":"8986","date_updated":"2024-10-29T10:22:43Z","type":"journal_article","ddc":["580"],"quality_controlled":"1","month":"12","department":[{"_id":"JiFr"}],"file":[{"file_size":10578145,"date_created":"2021-01-07T12:44:33Z","creator":"dernst","date_updated":"2021-01-07T12:44:33Z","file_id":"8994","success":1,"file_name":"2020_ScienceAdvances_Zhang.pdf","access_level":"open_access","content_type":"application/pdf","relation":"main_file","checksum":"5ac2500b191c08ef6dab5327f40ff663"}],"article_number":"eabc8895","oa":1,"language":[{"iso":"eng"}],"citation":{"short":"Y. Zhang, L. Rodriguez Solovey, L. Li, X. Zhang, J. Friml, Science Advances 6 (2020).","ieee":"Y. Zhang, L. Rodriguez Solovey, L. Li, X. Zhang, and J. Friml, “Functional innovations of PIN auxin transporters mark crucial evolutionary transitions during rise of flowering plants,” <i>Science Advances</i>, vol. 6, no. 50. AAAS, 2020.","ama":"Zhang Y, Rodriguez Solovey L, Li L, Zhang X, Friml J. Functional innovations of PIN auxin transporters mark crucial evolutionary transitions during rise of flowering plants. <i>Science Advances</i>. 2020;6(50). doi:<a href=\"https://doi.org/10.1126/sciadv.abc8895\">10.1126/sciadv.abc8895</a>","mla":"Zhang, Yuzhou, et al. “Functional Innovations of PIN Auxin Transporters Mark Crucial Evolutionary Transitions during Rise of Flowering Plants.” <i>Science Advances</i>, vol. 6, no. 50, eabc8895, AAAS, 2020, doi:<a href=\"https://doi.org/10.1126/sciadv.abc8895\">10.1126/sciadv.abc8895</a>.","apa":"Zhang, Y., Rodriguez Solovey, L., Li, L., Zhang, X., &#38; Friml, J. (2020). Functional innovations of PIN auxin transporters mark crucial evolutionary transitions during rise of flowering plants. <i>Science Advances</i>. AAAS. <a href=\"https://doi.org/10.1126/sciadv.abc8895\">https://doi.org/10.1126/sciadv.abc8895</a>","chicago":"Zhang, Yuzhou, Lesia Rodriguez Solovey, Lanxin Li, Xixi Zhang, and Jiří Friml. “Functional Innovations of PIN Auxin Transporters Mark Crucial Evolutionary Transitions during Rise of Flowering Plants.” <i>Science Advances</i>. AAAS, 2020. <a href=\"https://doi.org/10.1126/sciadv.abc8895\">https://doi.org/10.1126/sciadv.abc8895</a>.","ista":"Zhang Y, Rodriguez Solovey L, Li L, Zhang X, Friml J. 2020. Functional innovations of PIN auxin transporters mark crucial evolutionary transitions during rise of flowering plants. Science Advances. 6(50), eabc8895."},"issue":"50","user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","day":"11","scopus_import":"1","author":[{"first_name":"Yuzhou","orcid":"0000-0003-2627-6956","last_name":"Zhang","full_name":"Zhang, Yuzhou","id":"3B6137F2-F248-11E8-B48F-1D18A9856A87"},{"id":"3922B506-F248-11E8-B48F-1D18A9856A87","full_name":"Rodriguez Solovey, Lesia","last_name":"Rodriguez Solovey","orcid":"0000-0002-7244-7237","first_name":"Lesia"},{"orcid":"0000-0002-5607-272X","first_name":"Lanxin","id":"367EF8FA-F248-11E8-B48F-1D18A9856A87","full_name":"Li, Lanxin","last_name":"Li"},{"id":"61A66458-47E9-11EA-85BA-8AEAAF14E49A","full_name":"Zhang, Xixi","last_name":"Zhang","orcid":"0000-0001-7048-4627","first_name":"Xixi"},{"last_name":"Friml","full_name":"Friml, Jiří","id":"4159519E-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0002-8302-7596","first_name":"Jiří"}],"title":"Functional innovations of PIN auxin transporters mark crucial evolutionary transitions during rise of flowering plants","oa_version":"Published Version","volume":6,"date_created":"2021-01-03T23:01:23Z","article_type":"original","has_accepted_license":"1","tmp":{"name":"Creative Commons Attribution-NonCommercial 4.0 International (CC BY-NC 4.0)","legal_code_url":"https://creativecommons.org/licenses/by-nc/4.0/legalcode","image":"/images/cc_by_nc.png","short":"CC BY-NC (4.0)"},"abstract":[{"text":"Flowering plants display the highest diversity among plant species and have notably shaped terrestrial landscapes. Nonetheless, the evolutionary origin of their unprecedented morphological complexity remains largely an enigma. Here, we show that the coevolution of cis-regulatory and coding regions of PIN-FORMED (PIN) auxin transporters confined their expression to certain cell types and directed their subcellular localization to particular cell sides, which together enabled dynamic auxin gradients across tissues critical to the complex architecture of flowering plants. Extensive intraspecies and interspecies genetic complementation experiments with PINs from green alga up to flowering plant lineages showed that PIN genes underwent three subsequent, critical evolutionary innovations and thus acquired a triple function to regulate the development of three essential components of the flowering plant Arabidopsis: shoot/root, inflorescence, and floral organ. Our work highlights the critical role of functional innovations within the PIN gene family as essential prerequisites for the origin of flowering plants.","lang":"eng"}],"intvolume":"         6","file_date_updated":"2021-01-07T12:44:33Z","publication_identifier":{"eissn":["2375-2548"]},"publication_status":"published"},{"year":"2020","isi":1,"external_id":{"isi":["000545741500030"],"pmid":["32193204"]},"pmid":1,"ec_funded":1,"date_published":"2020-05-01T00:00:00Z","project":[{"_id":"261099A6-B435-11E9-9278-68D0E5697425","name":"Tracing Evolution of Auxin Transport and Polarity in Plants","grant_number":"742985","call_identifier":"H2020"},{"_id":"26538374-B435-11E9-9278-68D0E5697425","name":"Molecular mechanisms of endocytic cargo recognition in plants","grant_number":"I03630","call_identifier":"FWF"}],"publication":"The Plant Cell","status":"public","date_updated":"2023-09-05T12:21:06Z","_id":"7619","type":"journal_article","doi":"10.1105/tpc.19.00869","article_processing_charge":"No","publisher":"American Society of Plant Biologists","main_file_link":[{"url":"https://doi.org/10.1105/tpc.19.00869","open_access":"1"}],"quality_controlled":"1","page":"1644-1664","department":[{"_id":"JiFr"}],"month":"05","issue":"5","citation":{"apa":"Zhang, X., Adamowski, M., Marhavá, P., Tan, S., Zhang, Y., Rodriguez Solovey, L., … Friml, J. (2020). Arabidopsis flippases cooperate with ARF GTPase exchange factors to regulate the trafficking and polarity of PIN auxin transporters. <i>The Plant Cell</i>. American Society of Plant Biologists. <a href=\"https://doi.org/10.1105/tpc.19.00869\">https://doi.org/10.1105/tpc.19.00869</a>","mla":"Zhang, Xixi, et al. “Arabidopsis Flippases Cooperate with ARF GTPase Exchange Factors to Regulate the Trafficking and Polarity of PIN Auxin Transporters.” <i>The Plant Cell</i>, vol. 32, no. 5, American Society of Plant Biologists, 2020, pp. 1644–64, doi:<a href=\"https://doi.org/10.1105/tpc.19.00869\">10.1105/tpc.19.00869</a>.","chicago":"Zhang, Xixi, Maciek Adamowski, Petra Marhavá, Shutang Tan, Yuzhou Zhang, Lesia Rodriguez Solovey, Marta Zwiewka, et al. “Arabidopsis Flippases Cooperate with ARF GTPase Exchange Factors to Regulate the Trafficking and Polarity of PIN Auxin Transporters.” <i>The Plant Cell</i>. American Society of Plant Biologists, 2020. <a href=\"https://doi.org/10.1105/tpc.19.00869\">https://doi.org/10.1105/tpc.19.00869</a>.","ista":"Zhang X, Adamowski M, Marhavá P, Tan S, Zhang Y, Rodriguez Solovey L, Zwiewka M, Pukyšová V, Sánchez AS, Raxwal VK, Hardtke CS, Nodzynski T, Friml J. 2020. Arabidopsis flippases cooperate with ARF GTPase exchange factors to regulate the trafficking and polarity of PIN auxin transporters. The Plant Cell. 32(5), 1644–1664.","ieee":"X. Zhang <i>et al.</i>, “Arabidopsis flippases cooperate with ARF GTPase exchange factors to regulate the trafficking and polarity of PIN auxin transporters,” <i>The Plant Cell</i>, vol. 32, no. 5. American Society of Plant Biologists, pp. 1644–1664, 2020.","short":"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.","ama":"Zhang X, Adamowski M, Marhavá P, et al. Arabidopsis flippases cooperate with ARF GTPase exchange factors to regulate the trafficking and polarity of PIN auxin transporters. <i>The Plant Cell</i>. 2020;32(5):1644-1664. doi:<a href=\"https://doi.org/10.1105/tpc.19.00869\">10.1105/tpc.19.00869</a>"},"user_id":"c635000d-4b10-11ee-a964-aac5a93f6ac1","oa":1,"language":[{"iso":"eng"}],"volume":32,"article_type":"original","date_created":"2020-03-28T07:39:22Z","author":[{"full_name":"Zhang, Xixi","id":"61A66458-47E9-11EA-85BA-8AEAAF14E49A","last_name":"Zhang","orcid":"0000-0001-7048-4627","first_name":"Xixi"},{"first_name":"Maciek","orcid":"0000-0001-6463-5257","last_name":"Adamowski","full_name":"Adamowski, Maciek","id":"45F536D2-F248-11E8-B48F-1D18A9856A87"},{"first_name":"Petra","full_name":"Marhavá, Petra","id":"44E59624-F248-11E8-B48F-1D18A9856A87","last_name":"Marhavá"},{"last_name":"Tan","id":"2DE75584-F248-11E8-B48F-1D18A9856A87","full_name":"Tan, Shutang","orcid":"0000-0002-0471-8285","first_name":"Shutang"},{"orcid":"0000-0003-2627-6956","first_name":"Yuzhou","last_name":"Zhang","full_name":"Zhang, Yuzhou","id":"3B6137F2-F248-11E8-B48F-1D18A9856A87"},{"id":"3922B506-F248-11E8-B48F-1D18A9856A87","full_name":"Rodriguez Solovey, Lesia","last_name":"Rodriguez Solovey","first_name":"Lesia","orcid":"0000-0002-7244-7237"},{"full_name":"Zwiewka, Marta","last_name":"Zwiewka","first_name":"Marta"},{"full_name":"Pukyšová, Vendula","last_name":"Pukyšová","first_name":"Vendula"},{"first_name":"Adrià Sans","full_name":"Sánchez, Adrià Sans","last_name":"Sánchez"},{"first_name":"Vivek Kumar","full_name":"Raxwal, Vivek Kumar","last_name":"Raxwal"},{"first_name":"Christian S.","full_name":"Hardtke, Christian S.","last_name":"Hardtke"},{"first_name":"Tomasz","last_name":"Nodzynski","full_name":"Nodzynski, Tomasz"},{"last_name":"Friml","id":"4159519E-F248-11E8-B48F-1D18A9856A87","full_name":"Friml, Jiří","orcid":"0000-0002-8302-7596","first_name":"Jiří"}],"day":"01","scopus_import":"1","title":"Arabidopsis flippases cooperate with ARF GTPase exchange factors to regulate the trafficking and polarity of PIN auxin transporters","oa_version":"Published Version","publication_status":"published","publication_identifier":{"issn":["1040-4651"],"eissn":["1532-298X"]},"intvolume":"        32","abstract":[{"lang":"eng","text":"Cell polarity is a fundamental feature of all multicellular organisms. In plants, prominent cell polarity markers are PIN auxin transporters crucial for plant development. To identify novel components involved in cell polarity establishment and maintenance, we carried out a forward genetic screening with PIN2:PIN1-HA;pin2 Arabidopsis plants, which ectopically express predominantly basally localized PIN1 in the root epidermal cells leading to agravitropic root growth. From the screen, we identified the regulator of PIN polarity 12 (repp12) mutation, which restored gravitropic root growth and caused PIN1-HA polarity switch from basal to apical side of root epidermal cells. Complementation experiments established the repp12 causative mutation as an amino acid substitution in Aminophospholipid ATPase3 (ALA3), a phospholipid flippase with predicted function in vesicle formation. ala3 T-DNA mutants show defects in many auxin-regulated processes, in asymmetric auxin distribution and in PIN trafficking. Analysis of quintuple and sextuple mutants confirmed a crucial role of ALA proteins in regulating plant development and in PIN trafficking and polarity. Genetic and physical interaction studies revealed that ALA3 functions together with GNOM and BIG3 ARF GEFs. Taken together, our results identified ALA3 flippase as an important interactor and regulator of ARF GEF functioning in PIN polarity, trafficking and auxin-mediated development."}],"acknowledged_ssus":[{"_id":"Bio"}]}]