@article{21136, abstract = {The plant hormone auxin regulates growth and development through at least two distinct signaling pathways. The nuclear pathway, involving TIR1/AFB receptors, mediates transcription; whereas the cell surface ABP1-TMK1 auxin perception triggers global ultrafast phosphorylation response. Here, we revisit the rich history of the disputed ABP1 auxin receptor, highlighting recent findings of the involvement of TMKs and other molecular components and focusing on their role in auxin canalization-mediated development.}, author = {Monzer, Aline and Friml, Jiří}, issn = {3005-1401}, journal = {npj Science of Plants}, number = {1}, pages = {2}, publisher = {Springer Nature}, title = {{Historical and mechanistic perspective on ABP1-TMK1-mediated cell surface auxin signaling.}}, doi = {10.1038/s44383-025-00002-8}, volume = {1}, year = {2025}, } @article{20656, abstract = {Phytohormone auxin and its directional transport mediate much of the remarkably plastic development of higher plants. Positive feedback between auxin signaling and transport is a prerequisite for (1) self-organizing processes, including vascular tissue formation, and (2) directional growth responses such as gravitropism. Here, we identify a mechanism by which auxin signaling directly targets PIN auxin transporters. Via the cell-surface AUXIN-BINDING PROTEIN1 (ABP1)-TRANSMEMBRANE KINASE 1 (TMK1) receptor module, auxin rapidly induces phosphorylation and thus stabilization of PIN2. Following gravistimulation, initial auxin asymmetry activates autophosphorylation of the TMK1 kinase. This induces TMK1 interaction with and phosphorylation of PIN2, stabilizing PIN2 at the lower root side, thus reinforcing asymmetric auxin flow for root bending. Upstream of TMK1 in this regulation, ABP1 acts redundantly with the root-expressed ABP1-LIKE 3 (ABL3) auxin receptor. Such positive feedback between cell-surface auxin signaling and PIN-mediated polar auxin transport is fundamental for robust root gravitropism and presumably for other self-organizing developmental phenomena.}, author = {Rodriguez Solovey, Lesia and Fiedler, Lukas and Zou, Minxia and Giannini, Caterina and Monzer, Aline and Vladimirtsev, Dmitrii and Randuch, Marek and Yu, Yongfan and Gelová, Zuzana and Verstraeten, Inge and Hajny, Jakub and Chen, Meng and Tan, Shutang and Hörmayer, Lukas and Li, Lanxin and Marques-Bueno, Maria Mar and Quddoos, Zainab and Molnar, Gergely and Kulich, Ivan and Jaillais, Yvon and Friml, Jiří}, issn = {0092-8674}, journal = {Cell}, number = {22}, pages = {6138--6150.e17}, publisher = {Elsevier}, title = {{ABP1/ABL3-TMK1 cell-surface auxin signaling targets PIN2-mediated auxin fluxes for root gravitropism}}, doi = {10.1016/j.cell.2025.08.026}, volume = {188}, year = {2025}, } @phdthesis{19395, abstract = {Plant growth and development rely significantly on phytohormones, with auxin serving as a master regulator, orchestrating processes from embryogenesis to organogenesis, vascular patterning, and environmental adaptation. Since its conceptual proposition by Charles Darwin in 1880 as an endogenous chemical signal influencing phototropism in grass, auxin has captivated scientists seeking to understand how such a small molecule exerts a profound influence on plant development. One particularly fascinating aspect of auxin function is its ability to self-organize its transport. Through a feedback mechanism between auxin perception and directional transport—primarily mediated by PIN auxin transporters—auxin establishes narrow transport channels. This phenomenon, known as auxin canalization, is fundamental to vascular formation, regeneration, and other key developmental processes. Despite advances in our understanding, driven by experimental studies and computational models, auxin canalization remains an enigma, with many unanswered questions. Like other hormones, auxin functions through intricate signaling pathways. It operates through at least two distinct signaling mechanisms: the well-characterized canonical pathway and the less understood non-canonical pathway. While significant progress has been made in elucidating the canonical pathway, the non-canonical mechanisms remain less defined and require further investigation. In this study, we revisit the non-canonical auxin signaling pathway mediated by the cell-surface complex Auxin Binding Protein 1-Transmembrane Kinase 1 (ABP1-TMK1), with a particular focus on its downstream phosphorylation events. We reveal that this auxin-mediated phosphorylation is conserved across the green lineage, underscoring its fundamental role in plant development. We explore key phosphorylation targets, particularly PIN2, which is essential for root gravitropism. To further understand TMK1’s role in diverse developmental processes, we identified and investigated its interactors as potential co-receptors or regulatory components within its signaling network. Given the previously established role of ABP1-TMK1 in auxin canalization, we sought to further investigate this process and identified several TMK1 interactors also involved in this intricate mechanism. These findings provide new insights into the complex regulation of auxin canalization, highlighting a broader and more interconnected signaling framework than previously understood.}, author = {Monzer, Aline}, issn = {2663-337X}, pages = {160}, publisher = {Institute of Science and Technology Austria}, title = {{Cell-surface auxin signaling: Linking molecular pathways to plant development}}, doi = {10.15479/AT-ISTA-19395}, year = {2025}, } @unpublished{19399, abstract = {Phytohormone auxin and its directional transport mediate much of the remarkably plastic development of higher plants. Positive feedback between auxin signaling and transport is a key prerequisite for (i) self-organizing processes including vascular tissue formation and (ii) directional growth responses such as gravitropism. Here we identify a mechanism, by which auxin signaling directly targets PIN auxin transporters. Via the cell-surface ABP1-TMK1 receptor module, auxin rapidly induces phosphorylation and thus stabilization of PIN2. Following gravistimulation, initial auxin asymmetry activates autophosphorylation of the TMK1 kinase. This induces TMK1 interaction with and phosphorylation of PIN2, stabilizing PIN2 at the lower root side, thus reinforcing asymmetric auxin flow for root bending. Upstream of TMK1 in this regulation, ABP1 acts redundantly with the root-expressed ABP1-LIKE auxin receptor ABL3. Such positive feedback between cell-surface auxin signaling and PIN-mediated polar auxin transport is fundamental for robust root gravitropism and presumably also for other self-organizing developmental phenomena.}, author = {Rodriguez Solovey, Lesia and Fiedler, Lukas and Zou, Minxia and Giannini, Caterina and Monzer, Aline and Vladimirtsev, Dmitrii and Randuch, Marek and Yu, Yongfan and Gelová, Zuzana and Verstraeten, Inge and Hajny, Jakub and Chen, Meng and Tan, Shutang and Hörmayer, Lukas and Li, Lanxin and Marques-Bueno, Maria Mar and Quddoos, Zainab and Molnar, Gergely and Xu, Tongda and Kulich, Ivan and Jaillais, Yvon and Friml, Jiří}, booktitle = {bioRxiv}, title = {{ABP1/ABL3-TMK1 cell-surface auxin signaling directly targets PIN2-mediated auxin fluxes for root gravitropism}}, doi = {10.1101/2022.11.30.518503}, year = {2025}, } @unpublished{19398, abstract = {Receptor-like kinases (RLKs), particularly the Transmembrane Kinase (TMK) family, play essential roles in signaling and development, with TMKs being key components of auxin perception and downstream phosphorylation events. While TMKs’ involvement in auxin canalization, a process essential for vasculature formation and regeneration, has been established, nonetheless, the additional signaling and regulatory partners remain poorly understood. In this study, we identify and characterize seven leucine-rich repeat RLKs (TINT1–TINT7) as novel interactors of TMK1, revealing their diverse evolutionary, structural, and functional characteristics. Our results show that TINTs interact with TMK1 and highlight their roles in regulating various developmental processes. Majority of TINTs contributes, together with TMK1, to auxin canalization, with TINT5 linking TMK1 to other canalization component CAMEL. Beyond canalization, we also establish the role of TINT-TMK1 interactions in processes such as stomatal movement and the hypocotyl’s gravitropic response. These findings suggest that TINTs, through their interaction with TMK1, are integral components of various signaling networks, contributing to both auxin canalization and broader plant development.}, author = {Monzer, Aline and Mazur, Ewa and Rodriguez Solovey, Lesia and Gallei, Michelle C and Zou, Minxia and Smejkal, Michael and Cervenova, Ema and Friml, Jiří}, booktitle = {bioRxiv}, title = {{TMK interacting network of receptor like kinases for auxin canalization and beyond}}, doi = {10.1101/2025.02.28.640727}, year = {2025}, } @article{15330, abstract = {Clathrin-mediated endocytosis (CME) is vital for the regulation of plant growth and development by controlling plasma membrane protein composition and cargo uptake. CME relies on the precise recruitment of regulators for vesicle maturation and release. Homologues of components of mammalian vesicle scission are strong candidates to be part of the scission machinery in plants, but the precise roles of these proteins in this process are not fully understood. Here, we characterised the roles of Plant Dynamin-Related Proteins 2 (DRP2s) and SH3-domain containing protein 2 (SH3P2), the plant homologue to Dynamins’ recruiters, like Endophilin and Amphiphysin, in the CME by combining high-resolution imaging of endocytic events in vivo and characterisation of the purified proteins in vitro. Although DRP2s and SH3P2 arrive similarly late during CME and physically interact, genetic analysis of the sh3p123 triple-mutant and complementation assays with non-SH3P2-interacting DRP2 variants suggests that SH3P2 does not directly recruit DRP2s to the site of endocytosis. These observations imply that despite the presence of many well-conserved endocytic components, plants have acquired a distinct mechanism for CME.}, author = {Gnyliukh, Nataliia and Johnson, Alexander J and Nagel, MK and Monzer, Aline and Babic, David and Hlavata, Annamaria and Alotaibi, SS and Isono, E and Loose, Martin and Friml, Jiří}, issn = {1477-9137}, journal = {Journal of Cell Science}, number = {8}, publisher = {The Company of Biologists}, title = {{Role of dynamin-related proteins 2 and SH3P2 in clathrin-mediated endocytosis in Arabidopsis thaliana}}, doi = {10.1242/jcs.261720}, volume = {137}, year = {2024}, } @article{18596, abstract = {Hormone perception and signaling pathways have a fundamental regulatory function in the physiological processes of plants. Cytokinins, a class of plant hormones, regulate cell division and meristem maintenance. The cytokinin signaling pathway is well established in the model plant Arabidopsis thaliana. Several negative feedback mechanisms, tightly controlling cytokinin signaling output, have been described previously. In this study, we identified a new feedback mechanism executed through alternative splicing of the cytokinin receptor AHK4/CRE1. A novel splicing variant named CRE1int7 results from seventh intron retention, introducing a premature termination codon in the transcript. We showed that CRE1int7 is translated in planta into a truncated receptor lacking the C-terminal receiver domain essential for signal transduction. CRE1int7 can bind cytokinin but cannot activate the downstream cascade. We present a novel negative feedback mechanism of the cytokinin signaling pathway, facilitated by a decoy receptor that can inactivate canonical cytokinin receptors via dimerization and compete with them for ligand binding. Ensuring proper plant growth and development requires precise control of the cytokinin signaling pathway at several levels. CRE1int7 represents a so-far unknown mechanism for fine-tuning the cytokinin signaling pathway in Arabidopsis.}, author = {Králová, Michaela and Kubalová, Ivona and Hajný, Jakub and Kubiasova, Karolina and Vagaská, Karolína and Ge, Zengxiang and Gallei, Michelle C and Semerádová, Hana and Kuchařová, Anna and Hönig, Martin and Monzer, Aline and Kovačik, Martin and Friml, Jiří and Novák, Ondřej and Benková, Eva and Ikeda, Yoshihisa and Zalabák, David}, issn = {1674-2052}, journal = {Molecular Plant}, number = {12}, pages = {1850--1865}, publisher = {Elsevier}, title = {{A decoy receptor derived from alternative splicing fine-tunes cytokinin signaling in Arabidopsis}}, doi = {10.1016/j.molp.2024.11.001}, volume = {17}, year = {2024}, } @article{14826, abstract = {The plant-signaling molecule auxin triggers fast and slow cellular responses across land plants and algae. The nuclear auxin pathway mediates gene expression and controls growth and development in land plants, but this pathway is absent from algal sister groups. Several components of rapid responses have been identified in Arabidopsis, but it is unknown if these are part of a conserved mechanism. We recently identified a fast, proteome-wide phosphorylation response to auxin. Here, we show that this response occurs across 5 land plant and algal species and converges on a core group of shared targets. We found conserved rapid physiological responses to auxin in the same species and identified rapidly accelerated fibrosarcoma (RAF)-like protein kinases as central mediators of auxin-triggered phosphorylation across species. Genetic analysis connects this kinase to both auxin-triggered protein phosphorylation and rapid cellular response, thus identifying an ancient mechanism for fast auxin responses in the green lineage.}, author = {Kuhn, Andre and Roosjen, Mark and Mutte, Sumanth and Dubey, Shiv Mani and Carrillo Carrasco, Vanessa Polet and Boeren, Sjef and Monzer, Aline and Koehorst, Jasper and Kohchi, Takayuki and Nishihama, Ryuichi and Fendrych, Matyas and Sprakel, Joris and Friml, Jiří and Weijers, Dolf}, issn = {1097-4172}, journal = {Cell}, keywords = {General Biochemistry, Genetics and Molecular Biology}, number = {1}, pages = {130--148.e17}, publisher = {Elsevier}, title = {{RAF-like protein kinases mediate a deeply conserved, rapid auxin response}}, doi = {10.1016/j.cell.2023.11.021}, volume = {187}, year = {2024}, } @unpublished{14591, abstract = {Clathrin-mediated endocytosis (CME) is vital for the regulation of plant growth and development by controlling plasma membrane protein composition and cargo uptake. CME relies on the precise recruitment of regulators for vesicle maturation and release. Homologues of components of mammalian vesicle scission are strong candidates to be part of the scissin machinery in plants, but the precise roles of these proteins in this process is not fully understood. Here, we characterised the roles of Plant Dynamin-Related Proteins 2 (DRP2s) and SH3-domain containing protein 2 (SH3P2), the plant homologue to Dynamins’ recruiters, like Endophilin and Amphiphysin, in the CME by combining high-resolution imaging of endocytic events in vivo and characterisation of the purified proteins in vitro. Although DRP2s and SH3P2 arrive similarly late during CME and physically interact, genetic analysis of the Dsh3p1,2,3 triple-mutant and complementation assays with non-SH3P2-interacting DRP2 variants suggests that SH3P2 does not directly recruit DRP2s to the site of endocytosis. These observations imply that despite the presence of many well-conserved endocytic components, plants have acquired a distinct mechanism for CME. One Sentence Summary In contrast to predictions based on mammalian systems, plant Dynamin-related proteins 2 are recruited to the site of Clathrin-mediated endocytosis independently of BAR-SH3 proteins.}, author = {Gnyliukh, Nataliia and Johnson, Alexander J and Nagel, Marie-Kristin and Monzer, Aline and Hlavata, Annamaria and Isono, Erika and Loose, Martin and Friml, Jiří}, booktitle = {bioRxiv}, title = {{Role of dynamin-related proteins 2 and SH3P2 in clathrin-mediated endocytosis in plants}}, doi = {10.1101/2023.10.09.561523}, year = {2023}, } @article{12291, abstract = {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.}, author = {Friml, Jiří and Gallei, Michelle C and Gelová, Zuzana and Johnson, Alexander J and Mazur, Ewa and Monzer, Aline and Rodriguez Solovey, Lesia and Roosjen, Mark and Verstraeten, Inge and Živanović, Branka D. and Zou, Minxia and Fiedler, Lukas and Giannini, Caterina and Grones, Peter and Hrtyan, Mónika and Kaufmann, Walter and Kuhn, Andre and Narasimhan, Madhumitha and Randuch, Marek and Rýdza, Nikola and Takahashi, Koji and Tan, Shutang and Teplova, Anastasiia and Kinoshita, Toshinori and Weijers, Dolf and Rakusová, Hana}, issn = {1476-4687}, journal = {Nature}, number = {7927}, pages = {575--581}, publisher = {Springer Nature}, title = {{ABP1–TMK auxin perception for global phosphorylation and auxin canalization}}, doi = {10.1038/s41586-022-05187-x}, volume = {609}, year = {2022}, }