---
OA_place: publisher
OA_type: hybrid
PlanS_conform: '1'
_id: '20656'
abstract:
- lang: eng
  text: 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.
acknowledged_ssus:
- _id: Bio
- _id: LifeSc
acknowledgement: We gratefully acknowledge Tongda Xu for experimental, material, and
  conceptual support. We thank William Gray for providing material, Nataliia Gnyliukh
  and Ema Cervenova for help with manuscript preparation, and Julia Schmid for help
  with cloning. We thank Dolf Weijers, Mark Roosjen, and Andre Kuhn for discussions
  and support with phospho-proteomic analyses. We thank the Bioimaging and Life Science
  facilities at the Institute of Science and Technology Austria (ISTA) for their excellent
  service and assistance. The research leading to these results has received funding
  from the European Union (ERC, CYNIPS, 101142681) and Austrian Science Fund (FWF;
  I 6123-B) to J.F., and Y.J. was funded by ERC no. 3363360-APPL under FP/2007-2013.
  L.R. was supported by the FP7-PEOPLE-2011-COFUND ISTFELLOW program (IC1023FELL01)
  and the European Molecular Biology Organization (EMBO) long-term postdoctoral fellowship
  (ALTF 985-2016). S.T. was supported by the National Natural Science Foundation of
  China (32321001, 32570366). The work of J.H. was supported by the project JG_2024_003
  implemented within the Palacký University Young Researcher Grant.
article_processing_charge: Yes (via OA deal)
article_type: original
author:
- first_name: Lesia
  full_name: Rodriguez Solovey, Lesia
  id: 3922B506-F248-11E8-B48F-1D18A9856A87
  last_name: Rodriguez Solovey
  orcid: 0000-0002-7244-7237
- first_name: Lukas
  full_name: Fiedler, Lukas
  id: 7c417475-8972-11ed-ae7b-8b674ca26986
  last_name: Fiedler
- first_name: Minxia
  full_name: Zou, Minxia
  id: 5c243f41-03f3-11ec-841c-96faf48a7ef9
  last_name: Zou
- first_name: Caterina
  full_name: Giannini, Caterina
  id: e3fdddd5-f6e0-11ea-865d-ca99ee6367f4
  last_name: Giannini
- first_name: Aline
  full_name: Monzer, Aline
  id: 2DB5D88C-D7B3-11E9-B8FD-7907E6697425
  last_name: Monzer
- first_name: Dmitrii
  full_name: Vladimirtsev, Dmitrii
  id: 60466724-5355-11ee-ae5a-fa55e8f99c3d
  last_name: Vladimirtsev
- first_name: Marek
  full_name: Randuch, Marek
  id: 6ac4636d-15b2-11ec-abd3-fb8df79972ae
  last_name: Randuch
- first_name: Yongfan
  full_name: Yu, Yongfan
  last_name: Yu
- first_name: Zuzana
  full_name: Gelová, Zuzana
  id: 0AE74790-0E0B-11E9-ABC7-1ACFE5697425
  last_name: Gelová
  orcid: 0000-0003-4783-1752
- first_name: Inge
  full_name: Verstraeten, Inge
  id: 362BF7FE-F248-11E8-B48F-1D18A9856A87
  last_name: Verstraeten
  orcid: 0000-0001-7241-2328
- first_name: Jakub
  full_name: Hajny, Jakub
  id: 4800CC20-F248-11E8-B48F-1D18A9856A87
  last_name: Hajny
  orcid: 0000-0003-2140-7195
- first_name: Meng
  full_name: Chen, Meng
  last_name: Chen
- first_name: Shutang
  full_name: Tan, Shutang
  id: 2DE75584-F248-11E8-B48F-1D18A9856A87
  last_name: Tan
  orcid: 0000-0002-0471-8285
- first_name: Lukas
  full_name: Hörmayer, Lukas
  id: 2EEE7A2A-F248-11E8-B48F-1D18A9856A87
  last_name: Hörmayer
  orcid: 0000-0001-8295-2926
- first_name: Lanxin
  full_name: Li, Lanxin
  id: 367EF8FA-F248-11E8-B48F-1D18A9856A87
  last_name: Li
  orcid: 0000-0002-5607-272X
- first_name: Maria Mar
  full_name: Marques-Bueno, Maria Mar
  last_name: Marques-Bueno
- first_name: Zainab
  full_name: Quddoos, Zainab
  id: 32ff3c64-04a0-11f0-a50f-d0c45bfac466
  last_name: Quddoos
- first_name: Gergely
  full_name: Molnar, Gergely
  id: 34F1AF46-F248-11E8-B48F-1D18A9856A87
  last_name: Molnar
- first_name: Ivan
  full_name: Kulich, Ivan
  id: 57a1567c-8314-11eb-9063-c9ddc3451a54
  last_name: Kulich
- first_name: Yvon
  full_name: Jaillais, Yvon
  last_name: Jaillais
- first_name: Jiří
  full_name: Friml, Jiří
  id: 4159519E-F248-11E8-B48F-1D18A9856A87
  last_name: Friml
  orcid: 0000-0002-8302-7596
citation:
  ama: Rodriguez Solovey L, Fiedler L, Zou M, et al. ABP1/ABL3-TMK1 cell-surface auxin
    signaling targets PIN2-mediated auxin fluxes for root gravitropism. <i>Cell</i>.
    2025;188(22):6138-6150.e17. doi:<a href="https://doi.org/10.1016/j.cell.2025.08.026">10.1016/j.cell.2025.08.026</a>
  apa: Rodriguez Solovey, L., Fiedler, L., Zou, M., Giannini, C., Monzer, A., Vladimirtsev,
    D., … Friml, J. (2025). ABP1/ABL3-TMK1 cell-surface auxin signaling targets PIN2-mediated
    auxin fluxes for root gravitropism. <i>Cell</i>. Elsevier. <a href="https://doi.org/10.1016/j.cell.2025.08.026">https://doi.org/10.1016/j.cell.2025.08.026</a>
  chicago: Rodriguez Solovey, Lesia, Lukas Fiedler, Minxia Zou, Caterina Giannini,
    Aline Monzer, Dmitrii Vladimirtsev, Marek Randuch, et al. “ABP1/ABL3-TMK1 Cell-Surface
    Auxin Signaling Targets PIN2-Mediated Auxin Fluxes for Root Gravitropism.” <i>Cell</i>.
    Elsevier, 2025. <a href="https://doi.org/10.1016/j.cell.2025.08.026">https://doi.org/10.1016/j.cell.2025.08.026</a>.
  ieee: L. Rodriguez Solovey <i>et al.</i>, “ABP1/ABL3-TMK1 cell-surface auxin signaling
    targets PIN2-mediated auxin fluxes for root gravitropism,” <i>Cell</i>, vol. 188,
    no. 22. Elsevier, p. 6138–6150.e17, 2025.
  ista: Rodriguez Solovey L, Fiedler L, Zou M, Giannini C, Monzer A, Vladimirtsev
    D, Randuch M, Yu Y, Gelová Z, Verstraeten I, Hajny J, Chen M, Tan S, Hörmayer
    L, Li L, Marques-Bueno MM, Quddoos Z, Molnar G, Kulich I, Jaillais Y, Friml J.
    2025. ABP1/ABL3-TMK1 cell-surface auxin signaling targets PIN2-mediated auxin
    fluxes for root gravitropism. Cell. 188(22), 6138–6150.e17.
  mla: Rodriguez Solovey, Lesia, et al. “ABP1/ABL3-TMK1 Cell-Surface Auxin Signaling
    Targets PIN2-Mediated Auxin Fluxes for Root Gravitropism.” <i>Cell</i>, vol. 188,
    no. 22, Elsevier, 2025, p. 6138–6150.e17, doi:<a href="https://doi.org/10.1016/j.cell.2025.08.026">10.1016/j.cell.2025.08.026</a>.
  short: L. Rodriguez Solovey, L. Fiedler, M. Zou, C. Giannini, A. Monzer, D. Vladimirtsev,
    M. Randuch, Y. Yu, Z. Gelová, I. Verstraeten, J. Hajny, M. Chen, S. Tan, L. Hörmayer,
    L. Li, M.M. Marques-Bueno, Z. Quddoos, G. Molnar, I. Kulich, Y. Jaillais, J. Friml,
    Cell 188 (2025) 6138–6150.e17.
corr_author: '1'
date_created: 2025-11-19T09:44:31Z
date_published: 2025-10-30T00:00:00Z
date_updated: 2026-07-06T12:51:13Z
day: '30'
ddc:
- '580'
department:
- _id: JiFr
- _id: XiFe
doi: 10.1016/j.cell.2025.08.026
ec_funded: 1
external_id:
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  - '001616077900005'
  pmid:
  - '41043433'
file:
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issue: '22'
language:
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license: https://creativecommons.org/licenses/by/4.0/
month: '10'
oa: 1
oa_version: Published Version
page: 6138-6150.e17
pmid: 1
project:
- _id: 8f347782-16d5-11f0-9cad-8c19706ee739
  grant_number: '101142681'
  name: Cyclic nucleotides as second messengers in plants
- _id: bd76d395-d553-11ed-ba76-f678c14f9033
  grant_number: I06123
  name: Peptide receptors for auxin canalization in Arabidopsis
- _id: 26060676-B435-11E9-9278-68D0E5697425
  grant_number: ALTF 985-2016
  name: Cell surface receptor complexes for auxin signaling in plants
- _id: 25681D80-B435-11E9-9278-68D0E5697425
  call_identifier: FP7
  grant_number: '291734'
  name: International IST Postdoc Fellowship Programme
publication: Cell
publication_identifier:
  issn:
  - 0092-8674
publication_status: published
publisher: Elsevier
quality_controlled: '1'
related_material:
  record:
  - id: '19399'
    relation: earlier_version
    status: public
status: public
title: ABP1/ABL3-TMK1 cell-surface auxin signaling targets PIN2-mediated auxin fluxes
  for root gravitropism
tmp:
  image: /images/cc_by.png
  legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
  name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
  short: CC BY (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 188
year: '2025'
...
---
OA_place: repository
OA_type: green
_id: '19399'
abstract:
- lang: eng
  text: 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.
acknowledged_ssus:
- _id: Bio
- _id: LifeSc
acknowledgement: 'We thank W. Gray for providing material; N. Gnyliukh and E. Cervenova
  for help with manuscript preparation; J. Schmid for help with cloning. We thank
  Dolf Weijers, Mark Roosjen, and Andre Kuhn for discussions and support with phospho-proteomic
  analyses. We thank the Bioimaging and Life Science facilities at ISTA for their
  excellent service and assistance. The research leading to these results has received
  funding from the European Research Council (ERC) under the European Union’s Horizon
  2020 research and innovation program grant agreement No 742985 and Austrian Science
  Fund (FWF): I3630-775 B25 to J.F; National Natural Science Foundation of China (Grant
  32130010, 31422008), start-up funds from FAFU to T.X., Y.J. was funded by ERC no.
  3363360-APPL under FP/2007-2013. L.R. was supported by FP7-PEOPLE-2011-COFUND ISTFELLOW
  program (IC1023FELL01) and the European Molecular Biology Organization (EMBO) long-term
  postdoctoral fellowship (ALTF 985- 2016). S.T. was supported by the National Natural
  Science Foundation of China (32321001).'
article_processing_charge: No
author:
- first_name: Lesia
  full_name: Rodriguez Solovey, Lesia
  id: 3922B506-F248-11E8-B48F-1D18A9856A87
  last_name: Rodriguez Solovey
  orcid: 0000-0002-7244-7237
- first_name: Lukas
  full_name: Fiedler, Lukas
  id: 7c417475-8972-11ed-ae7b-8b674ca26986
  last_name: Fiedler
- first_name: Minxia
  full_name: Zou, Minxia
  id: 5c243f41-03f3-11ec-841c-96faf48a7ef9
  last_name: Zou
- first_name: Caterina
  full_name: Giannini, Caterina
  id: e3fdddd5-f6e0-11ea-865d-ca99ee6367f4
  last_name: Giannini
- first_name: Aline
  full_name: Monzer, Aline
  id: 2DB5D88C-D7B3-11E9-B8FD-7907E6697425
  last_name: Monzer
- first_name: Dmitrii
  full_name: Vladimirtsev, Dmitrii
  id: 60466724-5355-11ee-ae5a-fa55e8f99c3d
  last_name: Vladimirtsev
- first_name: Marek
  full_name: Randuch, Marek
  id: 6ac4636d-15b2-11ec-abd3-fb8df79972ae
  last_name: Randuch
- first_name: Yongfan
  full_name: Yu, Yongfan
  last_name: Yu
- first_name: Zuzana
  full_name: Gelová, Zuzana
  id: 0AE74790-0E0B-11E9-ABC7-1ACFE5697425
  last_name: Gelová
  orcid: 0000-0003-4783-1752
- first_name: Inge
  full_name: Verstraeten, Inge
  id: 362BF7FE-F248-11E8-B48F-1D18A9856A87
  last_name: Verstraeten
  orcid: 0000-0001-7241-2328
- first_name: Jakub
  full_name: Hajny, Jakub
  id: 4800CC20-F248-11E8-B48F-1D18A9856A87
  last_name: Hajny
  orcid: 0000-0003-2140-7195
- first_name: Meng
  full_name: Chen, Meng
  last_name: Chen
- first_name: Shutang
  full_name: Tan, Shutang
  id: 2DE75584-F248-11E8-B48F-1D18A9856A87
  last_name: Tan
  orcid: 0000-0002-0471-8285
- first_name: Lukas
  full_name: Hörmayer, Lukas
  id: 2EEE7A2A-F248-11E8-B48F-1D18A9856A87
  last_name: Hörmayer
  orcid: 0000-0001-8295-2926
- first_name: Lanxin
  full_name: Li, Lanxin
  id: 367EF8FA-F248-11E8-B48F-1D18A9856A87
  last_name: Li
  orcid: 0000-0002-5607-272X
- first_name: Maria Mar
  full_name: Marques-Bueno, Maria Mar
  last_name: Marques-Bueno
- first_name: Zainab
  full_name: Quddoos, Zainab
  id: 32ff3c64-04a0-11f0-a50f-d0c45bfac466
  last_name: Quddoos
- first_name: Gergely
  full_name: Molnar, Gergely
  id: 34F1AF46-F248-11E8-B48F-1D18A9856A87
  last_name: Molnar
- first_name: Tongda
  full_name: Xu, Tongda
  last_name: Xu
- first_name: Ivan
  full_name: Kulich, Ivan
  id: 57a1567c-8314-11eb-9063-c9ddc3451a54
  last_name: Kulich
- first_name: Yvon
  full_name: Jaillais, Yvon
  last_name: Jaillais
- first_name: Jiří
  full_name: Friml, Jiří
  id: 4159519E-F248-11E8-B48F-1D18A9856A87
  last_name: Friml
  orcid: 0000-0002-8302-7596
citation:
  ama: Rodriguez Solovey L, Fiedler L, Zou M, et al. ABP1/ABL3-TMK1 cell-surface auxin
    signaling directly targets PIN2-mediated auxin fluxes for root gravitropism. <i>bioRxiv</i>.
    doi:<a href="https://doi.org/10.1101/2022.11.30.518503">10.1101/2022.11.30.518503</a>
  apa: Rodriguez Solovey, L., Fiedler, L., Zou, M., Giannini, C., Monzer, A., Vladimirtsev,
    D., … Friml, J. (n.d.). ABP1/ABL3-TMK1 cell-surface auxin signaling directly targets
    PIN2-mediated auxin fluxes for root gravitropism. <i>bioRxiv</i>. <a href="https://doi.org/10.1101/2022.11.30.518503">https://doi.org/10.1101/2022.11.30.518503</a>
  chicago: Rodriguez Solovey, Lesia, Lukas Fiedler, Minxia Zou, Caterina Giannini,
    Aline Monzer, Dmitrii Vladimirtsev, Marek Randuch, et al. “ABP1/ABL3-TMK1 Cell-Surface
    Auxin Signaling Directly Targets PIN2-Mediated Auxin Fluxes for Root Gravitropism.”
    <i>BioRxiv</i>, n.d. <a href="https://doi.org/10.1101/2022.11.30.518503">https://doi.org/10.1101/2022.11.30.518503</a>.
  ieee: L. Rodriguez Solovey <i>et al.</i>, “ABP1/ABL3-TMK1 cell-surface auxin signaling
    directly targets PIN2-mediated auxin fluxes for root gravitropism,” <i>bioRxiv</i>.
    .
  ista: Rodriguez Solovey L, Fiedler L, Zou M, Giannini C, Monzer A, Vladimirtsev
    D, Randuch M, Yu Y, Gelová Z, Verstraeten I, Hajny J, Chen M, Tan S, Hörmayer
    L, Li L, Marques-Bueno MM, Quddoos Z, Molnar G, Xu T, Kulich I, Jaillais Y, Friml
    J. ABP1/ABL3-TMK1 cell-surface auxin signaling directly targets PIN2-mediated
    auxin fluxes for root gravitropism. bioRxiv, <a href="https://doi.org/10.1101/2022.11.30.518503">10.1101/2022.11.30.518503</a>.
  mla: Rodriguez Solovey, Lesia, et al. “ABP1/ABL3-TMK1 Cell-Surface Auxin Signaling
    Directly Targets PIN2-Mediated Auxin Fluxes for Root Gravitropism.” <i>BioRxiv</i>,
    doi:<a href="https://doi.org/10.1101/2022.11.30.518503">10.1101/2022.11.30.518503</a>.
  short: L. Rodriguez Solovey, L. Fiedler, M. Zou, C. Giannini, A. Monzer, D. Vladimirtsev,
    M. Randuch, Y. Yu, Z. Gelová, I. Verstraeten, J. Hajny, M. Chen, S. Tan, L. Hörmayer,
    L. Li, M.M. Marques-Bueno, Z. Quddoos, G. Molnar, T. Xu, I. Kulich, Y. Jaillais,
    J. Friml, BioRxiv (n.d.).
corr_author: '1'
das_tickbox: '1'
date_created: 2025-03-13T08:36:48Z
date_published: 2025-02-20T00:00:00Z
date_updated: 2026-07-06T12:51:14Z
day: '20'
ddc:
- '580'
department:
- _id: JiFr
- _id: XiFe
doi: 10.1101/2022.11.30.518503
ec_funded: 1
language:
- iso: eng
main_file_link:
- open_access: '1'
  url: https://doi.org/10.1101/2022.11.30.518503
month: '02'
oa: 1
oa_version: Published Version
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
  call_identifier: FWF
  grant_number: I03630
  name: Molecular mechanisms of endocytic cargo recognition in plants
- _id: 25681D80-B435-11E9-9278-68D0E5697425
  call_identifier: FP7
  grant_number: '291734'
  name: International IST Postdoc Fellowship Programme
- _id: 26060676-B435-11E9-9278-68D0E5697425
  grant_number: ALTF 985-2016
  name: Cell surface receptor complexes for auxin signaling in plants
publication: bioRxiv
publication_status: draft
related_material:
  record:
  - id: '20656'
    relation: later_version
    status: public
  - id: '19395'
    relation: dissertation_contains
    status: public
  - id: '20364'
    relation: dissertation_contains
    status: public
status: public
title: ABP1/ABL3-TMK1 cell-surface auxin signaling directly targets PIN2-mediated
  auxin fluxes for root gravitropism
type: preprint
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
year: '2025'
...
---
_id: '15301'
abstract:
- lang: eng
  text: Plant morphogenesis relies exclusively on oriented cell expansion and division.
    Nonetheless, the mechanism(s) determining division plane orientation remain elusive.
    Here, we studied tissue healing after laser-assisted wounding in roots of Arabidopsis
    thaliana and uncovered how mechanical forces stabilize and reorient the microtubule
    cytoskeleton for the orientation of cell division. We identified that root tissue
    functions as an interconnected cell matrix, with a radial gradient of tissue extendibility
    causing predictable tissue deformation after wounding. This deformation causes
    instant redirection of expansion in the surrounding cells and reorientation of
    microtubule arrays, ultimately predicting cell division orientation. Microtubules
    are destabilized under low tension, whereas stretching of cells, either through
    wounding or external aspiration, immediately induces their polymerization. The
    higher microtubule abundance in the stretched cell parts leads to the reorientation
    of microtubule arrays and, ultimately, informs cell division planes. This provides
    a long-sought mechanism for flexible re-arrangement of cell divisions by mechanical
    forces for tissue reconstruction and plant architecture.
acknowledged_ssus:
- _id: Bio
- _id: LifeSc
acknowledgement: We are thankful to Simon Gilroy, Alexander Jones, and Lieven De Veylder
  for sharing published material. We thank the Imaging & Optics and Life Science Facilities
  at IST Austria, the Biooptics facility at GMI, and the Cellular Imaging Facility
  at DBMV UNIL for providing invaluable assistance. The research leading to these
  results has received funding from the European Research Council under the European
  Union's Seventh Framework Programme (FP7/2007-2013)/ERC grant agreement no. 742985,
  from the FWF under the stand-alone grant P29988, and from EMBO (ALTF 253-2023).
article_processing_charge: Yes (via OA deal)
article_type: original
author:
- first_name: Lukas
  full_name: Hörmayer, Lukas
  id: 2EEE7A2A-F248-11E8-B48F-1D18A9856A87
  last_name: Hörmayer
  orcid: 0000-0001-8295-2926
- first_name: Juan C
  full_name: Montesinos López, Juan C
  id: 310A8E3E-F248-11E8-B48F-1D18A9856A87
  last_name: Montesinos López
  orcid: 0000-0001-9179-6099
- first_name: N
  full_name: Trozzi, N
  last_name: Trozzi
- first_name: Leonhard
  full_name: Spona, Leonhard
  id: b52391fb-f636-11ee-939c-8a8c47552e8a
  last_name: Spona
- first_name: Saiko
  full_name: Yoshida, Saiko
  id: 2E46069C-F248-11E8-B48F-1D18A9856A87
  last_name: Yoshida
- first_name: Petra
  full_name: Marhavá, Petra
  id: 44E59624-F248-11E8-B48F-1D18A9856A87
  last_name: Marhavá
- first_name: Silvia
  full_name: Caballero Mancebo, Silvia
  id: 2F1E1758-F248-11E8-B48F-1D18A9856A87
  last_name: Caballero Mancebo
  orcid: 0000-0002-5223-3346
- first_name: Eva
  full_name: Benková, Eva
  id: 38F4F166-F248-11E8-B48F-1D18A9856A87
  last_name: Benková
  orcid: 0000-0002-8510-9739
- first_name: Carl-Philipp J
  full_name: Heisenberg, Carl-Philipp J
  id: 39427864-F248-11E8-B48F-1D18A9856A87
  last_name: Heisenberg
  orcid: 0000-0002-0912-4566
- first_name: Y
  full_name: Dagdas, Y
  last_name: Dagdas
- first_name: M
  full_name: Majda, M
  last_name: Majda
- first_name: Jiří
  full_name: Friml, Jiří
  id: 4159519E-F248-11E8-B48F-1D18A9856A87
  last_name: Friml
  orcid: 0000-0002-8302-7596
citation:
  ama: Hörmayer L, Montesinos López JC, Trozzi N, et al. Mechanical forces in plant
    tissue matrix orient cell divisions via microtubule stabilization. <i>Developmental
    Cell</i>. 2024;59(10):1333-1344.e4. doi:<a href="https://doi.org/10.1016/j.devcel.2024.03.009">10.1016/j.devcel.2024.03.009</a>
  apa: Hörmayer, L., Montesinos López, J. C., Trozzi, N., Spona, L., Yoshida, S.,
    Marhavá, P., … Friml, J. (2024). Mechanical forces in plant tissue matrix orient
    cell divisions via microtubule stabilization. <i>Developmental Cell</i>. Elsevier.
    <a href="https://doi.org/10.1016/j.devcel.2024.03.009">https://doi.org/10.1016/j.devcel.2024.03.009</a>
  chicago: Hörmayer, Lukas, Juan C Montesinos López, N Trozzi, Leonhard Spona, Saiko
    Yoshida, Petra Marhavá, Silvia Caballero Mancebo, et al. “Mechanical Forces in
    Plant Tissue Matrix Orient Cell Divisions via Microtubule Stabilization.” <i>Developmental
    Cell</i>. Elsevier, 2024. <a href="https://doi.org/10.1016/j.devcel.2024.03.009">https://doi.org/10.1016/j.devcel.2024.03.009</a>.
  ieee: L. Hörmayer <i>et al.</i>, “Mechanical forces in plant tissue matrix orient
    cell divisions via microtubule stabilization,” <i>Developmental Cell</i>, vol.
    59, no. 10. Elsevier, p. 1333–1344.e4, 2024.
  ista: Hörmayer L, Montesinos López JC, Trozzi N, Spona L, Yoshida S, Marhavá P,
    Caballero Mancebo S, Benková E, Heisenberg C-PJ, Dagdas Y, Majda M, Friml J. 2024.
    Mechanical forces in plant tissue matrix orient cell divisions via microtubule
    stabilization. Developmental Cell. 59(10), 1333–1344.e4.
  mla: Hörmayer, Lukas, et al. “Mechanical Forces in Plant Tissue Matrix Orient Cell
    Divisions via Microtubule Stabilization.” <i>Developmental Cell</i>, vol. 59,
    no. 10, Elsevier, 2024, p. 1333–1344.e4, doi:<a href="https://doi.org/10.1016/j.devcel.2024.03.009">10.1016/j.devcel.2024.03.009</a>.
  short: L. Hörmayer, J.C. Montesinos López, N. Trozzi, L. Spona, S. Yoshida, P. Marhavá,
    S. Caballero Mancebo, E. Benková, C.-P.J. Heisenberg, Y. Dagdas, M. Majda, J.
    Friml, Developmental Cell 59 (2024) 1333–1344.e4.
corr_author: '1'
date_created: 2024-04-08T12:07:57Z
date_published: 2024-05-20T00:00:00Z
date_updated: 2025-09-04T13:32:08Z
day: '20'
ddc:
- '570'
department:
- _id: JiFr
- _id: EvBe
- _id: CaHe
doi: 10.1016/j.devcel.2024.03.009
ec_funded: 1
external_id:
  isi:
  - '001301584600001'
  pmid:
  - '38579717'
file:
- access_level: open_access
  checksum: 22b374fb50a40d380b7686c84258d271
  content_type: application/pdf
  creator: dernst
  date_created: 2024-08-20T11:22:16Z
  date_updated: 2024-08-20T11:22:16Z
  file_id: '17452'
  file_name: 2024_DevelopmentalCell_Hoermayer.pdf
  file_size: 5195262
  relation: main_file
  success: 1
file_date_updated: 2024-08-20T11:22:16Z
has_accepted_license: '1'
intvolume: '        59'
isi: 1
issue: '10'
language:
- iso: eng
month: '05'
oa: 1
oa_version: Published Version
page: 1333-1344.e4
pmid: 1
project:
- _id: 261099A6-B435-11E9-9278-68D0E5697425
  call_identifier: H2020
  grant_number: '742985'
  name: Tracing Evolution of Auxin Transport and Polarity in Plants
- _id: 262EF96E-B435-11E9-9278-68D0E5697425
  call_identifier: FWF
  grant_number: P29988
  name: RNA-directed DNA methylation in plant development
publication: Developmental Cell
publication_identifier:
  eissn:
  - 1878-1551
  issn:
  - 1534-5807
publication_status: published
publisher: Elsevier
quality_controlled: '1'
related_material:
  link:
  - description: News on ISTA website
    relation: press_release
    url: https://ista.ac.at/en/news/how-plants-heal-wounds/
scopus_import: '1'
status: public
title: Mechanical forces in plant tissue matrix orient cell divisions via microtubule
  stabilization
tmp:
  image: /images/cc_by.png
  legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
  name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
  short: CC BY (4.0)
type: journal_article
user_id: 317138e5-6ab7-11ef-aa6d-ffef3953e345
volume: 59
year: '2024'
...
---
OA_type: closed access
_id: '18311'
abstract:
- lang: eng
  text: Local wound signaling in plants informs the surrounding tissues about an injury
    and initiates the regeneration process. In a recent paper published in Cell, Yang
    and colleagues show the involvement of a single Pep family member from tomato
    in wound signaling and how exogenous application of this regeneration factor enhances
    transformation efficiency in crops.
article_processing_charge: No
article_type: original
author:
- first_name: Lukas
  full_name: Hörmayer, Lukas
  id: 2EEE7A2A-F248-11E8-B48F-1D18A9856A87
  last_name: Hörmayer
  orcid: 0000-0001-8295-2926
- first_name: Jiří
  full_name: Friml, Jiří
  id: 4159519E-F248-11E8-B48F-1D18A9856A87
  last_name: Friml
  orcid: 0000-0002-8302-7596
citation:
  ama: 'Hörmayer L, Friml J. Feeling the danger: Local wound signaling in plants.
    <i>Cell Research</i>. 2024;34:761-762. doi:<a href="https://doi.org/10.1038/s41422-024-01035-x">10.1038/s41422-024-01035-x</a>'
  apa: 'Hörmayer, L., &#38; Friml, J. (2024). Feeling the danger: Local wound signaling
    in plants. <i>Cell Research</i>. Springer Nature. <a href="https://doi.org/10.1038/s41422-024-01035-x">https://doi.org/10.1038/s41422-024-01035-x</a>'
  chicago: 'Hörmayer, Lukas, and Jiří Friml. “Feeling the Danger: Local Wound Signaling
    in Plants.” <i>Cell Research</i>. Springer Nature, 2024. <a href="https://doi.org/10.1038/s41422-024-01035-x">https://doi.org/10.1038/s41422-024-01035-x</a>.'
  ieee: 'L. Hörmayer and J. Friml, “Feeling the danger: Local wound signaling in plants,”
    <i>Cell Research</i>, vol. 34. Springer Nature, pp. 761–762, 2024.'
  ista: 'Hörmayer L, Friml J. 2024. Feeling the danger: Local wound signaling in plants.
    Cell Research. 34, 761–762.'
  mla: 'Hörmayer, Lukas, and Jiří Friml. “Feeling the Danger: Local Wound Signaling
    in Plants.” <i>Cell Research</i>, vol. 34, Springer Nature, 2024, pp. 761–62,
    doi:<a href="https://doi.org/10.1038/s41422-024-01035-x">10.1038/s41422-024-01035-x</a>.'
  short: L. Hörmayer, J. Friml, Cell Research 34 (2024) 761–762.
corr_author: '1'
date_created: 2024-10-13T22:01:51Z
date_published: 2024-11-01T00:00:00Z
date_updated: 2025-09-08T09:57:18Z
day: '01'
department:
- _id: JiFr
doi: 10.1038/s41422-024-01035-x
external_id:
  isi:
  - '001326684200001'
  pmid:
  - '39354142'
intvolume: '        34'
isi: 1
language:
- iso: eng
month: '11'
oa_version: None
page: 761-762
pmid: 1
publication: Cell Research
publication_identifier:
  eissn:
  - 1748-7838
  issn:
  - 1001-0602
publication_status: published
publisher: Springer Nature
quality_controlled: '1'
scopus_import: '1'
status: public
title: 'Feeling the danger: Local wound signaling in plants'
type: journal_article
user_id: 317138e5-6ab7-11ef-aa6d-ffef3953e345
volume: 34
year: '2024'
...
---
_id: '12052'
abstract:
- lang: eng
  text: Directionality in the intercellular transport of the plant hormone auxin is
    determined by polar plasma membrane localization of PIN-FORMED (PIN) auxin transport
    proteins. However, apart from PIN phosphorylation at conserved motifs, no further
    determinants explicitly controlling polar PIN sorting decisions have been identified.
    Here we present Arabidopsis WAVY GROWTH 3 (WAV3) and closely related RING-finger
    E3 ubiquitin ligases, whose loss-of-function mutants show a striking apical-to-basal
    polarity switch in PIN2 localization in root meristem cells. WAV3 E3 ligases function
    as essential determinants for PIN polarity, acting independently from PINOID/WAG-dependent
    PIN phosphorylation. They antagonize ectopic deposition of de novo synthesized
    PIN proteins already immediately following completion of cell division, presumably
    via preventing PIN sorting into basal, ARF GEF-mediated trafficking. Our findings
    reveal an involvement of E3 ligases in the selective targeting of apically localized
    PINs in higher plants.
acknowledgement: We would like to thank Tatsuo Sakai, Marcus Heisler, Toru Fujiwara,
  Lucia Strader, Christian Hardtke, Malcolm Bennett, Claus Schwechheimer, Gerd Jürgens
  and Remko Offringa for sharing published materials and Alba Grau Gimeno for support.
  We are greatly indebted to Bert de Rybel for supporting N.K. and M.G. to work on
  the final stages of manuscript preparation as postdocs in his laboratory. A full-length
  SOR1 cDNA clone (J090099M14) was obtained from the National Agriculture and Food
  Research Organization (NARO, Japan). Support by the Multiscale Imaging Core Facility
  at the BOKU is greatly acknowledged. This work has been supported by grants from
  the Austrian Science Fund (FWF P25931-B16; P31493-B25 to Christian Luschnig; I3630-B25
  to Jiří Friml; P30850-B32 to Barbara Korbei) and from the Swiss National Funds (31003A-165877/1
  to Markus Geisler) and the European Union’s Horizon 2020 research and innovation
  program (Marie Skłodowska-Curie grant agreement No 885979 to Matouš Glanc).
article_number: '5147'
article_processing_charge: No
article_type: original
author:
- first_name: N
  full_name: Konstantinova, N
  last_name: Konstantinova
- first_name: Lukas
  full_name: Hörmayer, Lukas
  id: 2EEE7A2A-F248-11E8-B48F-1D18A9856A87
  last_name: Hörmayer
  orcid: 0000-0001-8295-2926
- first_name: Matous
  full_name: Glanc, Matous
  id: 1AE1EA24-02D0-11E9-9BAA-DAF4881429F2
  last_name: Glanc
  orcid: 0000-0003-0619-7783
- first_name: R
  full_name: Keshkeih, R
  last_name: Keshkeih
- first_name: Shutang
  full_name: Tan, Shutang
  id: 2DE75584-F248-11E8-B48F-1D18A9856A87
  last_name: Tan
  orcid: 0000-0002-0471-8285
- first_name: M
  full_name: Di Donato, M
  last_name: Di Donato
- first_name: K
  full_name: Retzer, K
  last_name: Retzer
- first_name: J
  full_name: Moulinier-Anzola, J
  last_name: Moulinier-Anzola
- first_name: M
  full_name: Schwihla, M
  last_name: Schwihla
- first_name: B
  full_name: Korbei, B
  last_name: Korbei
- first_name: M
  full_name: Geisler, M
  last_name: Geisler
- first_name: Jiří
  full_name: Friml, Jiří
  id: 4159519E-F248-11E8-B48F-1D18A9856A87
  last_name: Friml
  orcid: 0000-0002-8302-7596
- first_name: C
  full_name: Luschnig, C
  last_name: Luschnig
citation:
  ama: Konstantinova N, Hörmayer L, Glanc M, et al. WAVY GROWTH Arabidopsis E3 ubiquitin
    ligases affect apical PIN sorting decisions. <i>Nature Communications</i>. 2022;13.
    doi:<a href="https://doi.org/10.1038/s41467-022-32888-8">10.1038/s41467-022-32888-8</a>
  apa: Konstantinova, N., Hörmayer, L., Glanc, M., Keshkeih, R., Tan, S., Di Donato,
    M., … Luschnig, C. (2022). WAVY GROWTH Arabidopsis E3 ubiquitin ligases affect
    apical PIN sorting decisions. <i>Nature Communications</i>. Springer Nature. <a
    href="https://doi.org/10.1038/s41467-022-32888-8">https://doi.org/10.1038/s41467-022-32888-8</a>
  chicago: Konstantinova, N, Lukas Hörmayer, Matous Glanc, R Keshkeih, Shutang Tan,
    M Di Donato, K Retzer, et al. “WAVY GROWTH Arabidopsis E3 Ubiquitin Ligases Affect
    Apical PIN Sorting Decisions.” <i>Nature Communications</i>. Springer Nature,
    2022. <a href="https://doi.org/10.1038/s41467-022-32888-8">https://doi.org/10.1038/s41467-022-32888-8</a>.
  ieee: N. Konstantinova <i>et al.</i>, “WAVY GROWTH Arabidopsis E3 ubiquitin ligases
    affect apical PIN sorting decisions,” <i>Nature Communications</i>, vol. 13. Springer
    Nature, 2022.
  ista: Konstantinova N, Hörmayer L, Glanc M, Keshkeih R, Tan S, Di Donato M, Retzer
    K, Moulinier-Anzola J, Schwihla M, Korbei B, Geisler M, Friml J, Luschnig C. 2022.
    WAVY GROWTH Arabidopsis E3 ubiquitin ligases affect apical PIN sorting decisions.
    Nature Communications. 13, 5147.
  mla: Konstantinova, N., et al. “WAVY GROWTH Arabidopsis E3 Ubiquitin Ligases Affect
    Apical PIN Sorting Decisions.” <i>Nature Communications</i>, vol. 13, 5147, Springer
    Nature, 2022, doi:<a href="https://doi.org/10.1038/s41467-022-32888-8">10.1038/s41467-022-32888-8</a>.
  short: N. Konstantinova, L. Hörmayer, M. Glanc, R. Keshkeih, S. Tan, M. Di Donato,
    K. Retzer, J. Moulinier-Anzola, M. Schwihla, B. Korbei, M. Geisler, J. Friml,
    C. Luschnig, Nature Communications 13 (2022).
date_created: 2022-09-07T14:19:26Z
date_published: 2022-09-01T00:00:00Z
date_updated: 2025-04-15T07:32:09Z
day: '01'
ddc:
- '580'
department:
- _id: JiFr
doi: 10.1038/s41467-022-32888-8
external_id:
  isi:
  - '000848744900004'
  pmid:
  - '36050482'
file:
- access_level: open_access
  checksum: 43336758c89cd6c045839089af070afe
  content_type: application/pdf
  creator: dernst
  date_created: 2022-09-08T07:46:16Z
  date_updated: 2022-09-08T07:46:16Z
  file_id: '12063'
  file_name: 2022_NatureCommunications_Konstantinova.pdf
  file_size: 6678579
  relation: main_file
  success: 1
file_date_updated: 2022-09-08T07:46:16Z
has_accepted_license: '1'
intvolume: '        13'
isi: 1
language:
- iso: eng
month: '09'
oa: 1
oa_version: Published Version
pmid: 1
project:
- _id: 26538374-B435-11E9-9278-68D0E5697425
  call_identifier: FWF
  grant_number: I03630
  name: Molecular mechanisms of endocytic cargo recognition in plants
publication: Nature Communications
publication_identifier:
  issn:
  - 2041-1723
publication_status: published
publisher: Springer Nature
quality_controlled: '1'
related_material:
  link:
  - relation: erratum
    url: https://doi.org/10.1038/s41467-022-33198-9
scopus_import: '1'
status: public
title: WAVY GROWTH Arabidopsis E3 ubiquitin ligases affect apical PIN sorting decisions
tmp:
  image: /images/cc_by.png
  legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
  name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
  short: CC BY (4.0)
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 13
year: '2022'
...
---
_id: '12144'
abstract:
- lang: eng
  text: The phytohormone auxin is the major coordinative signal in plant development1,
    mediating transcriptional reprogramming by a well-established canonical signalling
    pathway. TRANSPORT INHIBITOR RESPONSE 1 (TIR1)/AUXIN-SIGNALING F-BOX (AFB) auxin
    receptors are F-box subunits of ubiquitin ligase complexes. In response to auxin,
    they associate with Aux/IAA transcriptional repressors and target them for degradation
    via ubiquitination2,3. Here we identify adenylate cyclase (AC) activity as an
    additional function of TIR1/AFB receptors across land plants. Auxin, together
    with Aux/IAAs, stimulates cAMP production. Three separate mutations in the AC
    motif of the TIR1 C-terminal region, all of which abolish the AC activity, each
    render TIR1 ineffective in mediating gravitropism and sustained auxin-induced
    root growth inhibition, and also affect auxin-induced transcriptional regulation.
    These results highlight the importance of TIR1/AFB AC activity in canonical auxin
    signalling. They also identify a unique phytohormone receptor cassette combining
    F-box and AC motifs, and the role of cAMP as a second messenger in plants.
acknowledged_ssus:
- _id: LifeSc
- _id: Bio
acknowledgement: This research was supported by the Lab Support Facility (LSF) and
  the Imaging and Optics Facility (IOF) of IST Austria. We thank C. Gehring for suggestions
  and advice; and K. U. Torii and G. Stacey for seeds and plasmids. This project was
  funded by a European Research Council Advanced Grant (ETAP-742985). M.F.K. and R.N.
  acknowledge the support of the EU MSCA-IF project CrysPINs (792329). M.K. was supported
  by the project POWR.03.05.00-00-Z302/17 Universitas Copernicana Thoruniensis in
  Futuro–IDS “Academia Copernicana”. CIDG acknowledges support from UKRI under Future
  Leaders Fellowship grant number MR/T020652/1.
article_processing_charge: No
article_type: original
author:
- first_name: Linlin
  full_name: Qi, Linlin
  id: 44B04502-A9ED-11E9-B6FC-583AE6697425
  last_name: Qi
  orcid: 0000-0001-5187-8401
- first_name: Mateusz
  full_name: Kwiatkowski, Mateusz
  last_name: Kwiatkowski
- first_name: Huihuang
  full_name: Chen, Huihuang
  id: 83c96512-15b2-11ec-abd3-b7eede36184f
  last_name: Chen
- first_name: Lukas
  full_name: Hörmayer, Lukas
  id: 2EEE7A2A-F248-11E8-B48F-1D18A9856A87
  last_name: Hörmayer
  orcid: 0000-0001-8295-2926
- first_name: Scott A
  full_name: Sinclair, Scott A
  id: 2D99FE6A-F248-11E8-B48F-1D18A9856A87
  last_name: Sinclair
  orcid: 0000-0002-4566-0593
- first_name: Minxia
  full_name: Zou, Minxia
  id: 5c243f41-03f3-11ec-841c-96faf48a7ef9
  last_name: Zou
- first_name: Charo I.
  full_name: del Genio, Charo I.
  last_name: del Genio
- first_name: Martin F.
  full_name: Kubeš, Martin F.
  last_name: Kubeš
- first_name: Richard
  full_name: Napier, Richard
  last_name: Napier
- first_name: Krzysztof
  full_name: Jaworski, Krzysztof
  last_name: Jaworski
- first_name: Jiří
  full_name: Friml, Jiří
  id: 4159519E-F248-11E8-B48F-1D18A9856A87
  last_name: Friml
  orcid: 0000-0002-8302-7596
citation:
  ama: Qi L, Kwiatkowski M, Chen H, et al. Adenylate cyclase activity of TIR1/AFB
    auxin receptors in plants. <i>Nature</i>. 2022;611(7934):133-138. doi:<a href="https://doi.org/10.1038/s41586-022-05369-7">10.1038/s41586-022-05369-7</a>
  apa: Qi, L., Kwiatkowski, M., Chen, H., Hörmayer, L., Sinclair, S. A., Zou, M.,
    … Friml, J. (2022). Adenylate cyclase activity of TIR1/AFB auxin receptors in
    plants. <i>Nature</i>. Springer Nature. <a href="https://doi.org/10.1038/s41586-022-05369-7">https://doi.org/10.1038/s41586-022-05369-7</a>
  chicago: Qi, Linlin, Mateusz Kwiatkowski, Huihuang Chen, Lukas Hörmayer, Scott A
    Sinclair, Minxia Zou, Charo I. del Genio, et al. “Adenylate Cyclase Activity of
    TIR1/AFB Auxin Receptors in Plants.” <i>Nature</i>. Springer Nature, 2022. <a
    href="https://doi.org/10.1038/s41586-022-05369-7">https://doi.org/10.1038/s41586-022-05369-7</a>.
  ieee: L. Qi <i>et al.</i>, “Adenylate cyclase activity of TIR1/AFB auxin receptors
    in plants,” <i>Nature</i>, vol. 611, no. 7934. Springer Nature, pp. 133–138, 2022.
  ista: Qi L, Kwiatkowski M, Chen H, Hörmayer L, Sinclair SA, Zou M, del Genio CI,
    Kubeš MF, Napier R, Jaworski K, Friml J. 2022. Adenylate cyclase activity of TIR1/AFB
    auxin receptors in plants. Nature. 611(7934), 133–138.
  mla: Qi, Linlin, et al. “Adenylate Cyclase Activity of TIR1/AFB Auxin Receptors
    in Plants.” <i>Nature</i>, vol. 611, no. 7934, Springer Nature, 2022, pp. 133–38,
    doi:<a href="https://doi.org/10.1038/s41586-022-05369-7">10.1038/s41586-022-05369-7</a>.
  short: L. Qi, M. Kwiatkowski, H. Chen, L. Hörmayer, S.A. Sinclair, M. Zou, C.I.
    del Genio, M.F. Kubeš, R. Napier, K. Jaworski, J. Friml, Nature 611 (2022) 133–138.
corr_author: '1'
date_created: 2023-01-12T12:06:05Z
date_published: 2022-11-03T00:00:00Z
date_updated: 2025-04-14T07:45:02Z
day: '03'
department:
- _id: JiFr
doi: 10.1038/s41586-022-05369-7
ec_funded: 1
external_id:
  isi:
  - '000875061600013'
  pmid:
  - '36289340'
intvolume: '       611'
isi: 1
issue: '7934'
language:
- iso: eng
main_file_link:
- open_access: '1'
  url: http://wrap.warwick.ac.uk/168325/1/WRAP-denylate-cyclase-activity-TIR1-AFB-auxin-receptors-root-growth-22.pdf
month: '11'
oa: 1
oa_version: Submitted Version
page: 133-138
pmid: 1
project:
- _id: 261099A6-B435-11E9-9278-68D0E5697425
  call_identifier: H2020
  grant_number: '742985'
  name: Tracing Evolution of Auxin Transport and Polarity in Plants
publication: Nature
publication_identifier:
  eissn:
  - 1476-4687
  issn:
  - 0028-0836
publication_status: published
publisher: Springer Nature
quality_controlled: '1'
scopus_import: '1'
status: public
title: Adenylate cyclase activity of TIR1/AFB auxin receptors in plants
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 611
year: '2022'
...
---
_id: '10268'
abstract:
- lang: eng
  text: The analysis of dynamic cellular processes such as plant cytokinesis stands
    and falls with live-cell time-lapse confocal imaging. Conventional approaches
    to time-lapse imaging of cell division in Arabidopsis root tips are tedious and
    have low throughput. Here, we describe a protocol for long-term time-lapse simultaneous
    imaging of multiple root tips on a vertical-stage confocal microscope with automated
    root tracking. We also provide modifications of the basic protocol to implement
    this imaging method in the analysis of genetic, pharmacological or laser ablation
    wounding-mediated experimental manipulations. Our method dramatically improves
    the efficiency of cell division time-lapse imaging by increasing the throughput,
    while reducing the person-hour requirements of such experiments.
acknowledged_ssus:
- _id: Bio
acknowledgement: We thank B. De Rybel for allowing M.G. to work on this manuscript
  during a postdoc in his laboratory, and EMBO for supporting M.G. with a Long-Term
  fellowship (ALTF 1005-2019) during this time. We acknowledge the service and support
  by the Bioimaging Facility at IST Austria, and finally, we thank A. Mally for proofreading
  and correcting the manuscript.
alternative_title:
- Methods in Molecular Biology
article_processing_charge: No
author:
- first_name: Lukas
  full_name: Hörmayer, Lukas
  id: 2EEE7A2A-F248-11E8-B48F-1D18A9856A87
  last_name: Hörmayer
- first_name: Jiří
  full_name: Friml, Jiří
  id: 4159519E-F248-11E8-B48F-1D18A9856A87
  last_name: Friml
  orcid: 0000-0002-8302-7596
- first_name: Matous
  full_name: Glanc, Matous
  id: 1AE1EA24-02D0-11E9-9BAA-DAF4881429F2
  last_name: Glanc
  orcid: 0000-0003-0619-7783
citation:
  ama: 'Hörmayer L, Friml J, Glanc M. Automated time-lapse imaging and manipulation
    of cell divisions in Arabidopsis roots by vertical-stage confocal microscopy.
    In: <i>Plant Cell Division</i>. Vol 2382. MIMB. Humana Press; 2021:105-114. doi:<a
    href="https://doi.org/10.1007/978-1-0716-1744-1_6">10.1007/978-1-0716-1744-1_6</a>'
  apa: Hörmayer, L., Friml, J., &#38; Glanc, M. (2021). Automated time-lapse imaging
    and manipulation of cell divisions in Arabidopsis roots by vertical-stage confocal
    microscopy. In <i>Plant Cell Division</i> (Vol. 2382, pp. 105–114). Humana Press.
    <a href="https://doi.org/10.1007/978-1-0716-1744-1_6">https://doi.org/10.1007/978-1-0716-1744-1_6</a>
  chicago: Hörmayer, Lukas, Jiří Friml, and Matous Glanc. “Automated Time-Lapse Imaging
    and Manipulation of Cell Divisions in Arabidopsis Roots by Vertical-Stage Confocal
    Microscopy.” In <i>Plant Cell Division</i>, 2382:105–14. MIMB. Humana Press, 2021.
    <a href="https://doi.org/10.1007/978-1-0716-1744-1_6">https://doi.org/10.1007/978-1-0716-1744-1_6</a>.
  ieee: L. Hörmayer, J. Friml, and M. Glanc, “Automated time-lapse imaging and manipulation
    of cell divisions in Arabidopsis roots by vertical-stage confocal microscopy,”
    in <i>Plant Cell Division</i>, vol. 2382, Humana Press, 2021, pp. 105–114.
  ista: 'Hörmayer L, Friml J, Glanc M. 2021.Automated time-lapse imaging and manipulation
    of cell divisions in Arabidopsis roots by vertical-stage confocal microscopy.
    In: Plant Cell Division. Methods in Molecular Biology, vol. 2382, 105–114.'
  mla: Hörmayer, Lukas, et al. “Automated Time-Lapse Imaging and Manipulation of Cell
    Divisions in Arabidopsis Roots by Vertical-Stage Confocal Microscopy.” <i>Plant
    Cell Division</i>, vol. 2382, Humana Press, 2021, pp. 105–14, doi:<a href="https://doi.org/10.1007/978-1-0716-1744-1_6">10.1007/978-1-0716-1744-1_6</a>.
  short: L. Hörmayer, J. Friml, M. Glanc, in:, Plant Cell Division, Humana Press,
    2021, pp. 105–114.
date_created: 2021-11-11T10:03:30Z
date_published: 2021-10-28T00:00:00Z
date_updated: 2022-06-03T06:47:06Z
day: '28'
department:
- _id: JiFr
doi: 10.1007/978-1-0716-1744-1_6
external_id:
  pmid:
  - '34705235'
intvolume: '      2382'
language:
- iso: eng
month: '10'
oa_version: None
page: 105-114
pmid: 1
publication: Plant Cell Division
publication_identifier:
  eisbn:
  - 978-1-0716-1744-1
  eissn:
  - 1940-6029
  isbn:
  - 978-1-0716-1743-4
  issn:
  - 1064-3745
publication_status: published
publisher: Humana Press
quality_controlled: '1'
scopus_import: '1'
series_title: MIMB
status: public
title: Automated time-lapse imaging and manipulation of cell divisions in Arabidopsis
  roots by vertical-stage confocal microscopy
type: book_chapter
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 2382
year: '2021'
...
---
_id: '9254'
abstract:
- lang: eng
  text: 'Auxin is a key regulator of plant growth and development. Local auxin biosynthesis
    and intercellular transport generates regional gradients in the root that are
    instructive for processes such as specification of developmental zones that maintain
    root growth and tropic responses. Here we present a toolbox to study auxin-mediated
    root development that features: (i) the ability to control auxin synthesis with
    high spatio-temporal resolution and (ii) single-cell nucleus tracking and morphokinetic
    analysis infrastructure. Integration of these two features enables cutting-edge
    analysis of root development at single-cell resolution based on morphokinetic
    parameters under normal growth conditions and during cell-type-specific induction
    of auxin biosynthesis. We show directional auxin flow in the root and refine the
    contributions of key players in this process. In addition, we determine the quantitative
    kinetics of Arabidopsis root meristem skewing, which depends on local auxin gradients
    but does not require PIN2 and AUX1 auxin transporter activities. Beyond the mechanistic
    insights into root development, the tools developed here will enable biologists
    to study kinetics and morphology of various critical processes at the single cell-level
    in whole organisms.'
acknowledgement: This work was supported by grants from the Israel Science Foundation
  (2378/19 to E.S.), the Joint NSFC-ISF Research Grant (3419/20 to E.S. and Z.D.),
  the Human Frontier Science Program (HFSP—LIY000540/2020 to E.S.), the European Research
  Council Starting Grant (757683- RobustHormoneTrans to E.S.), PBC postdoctoral fellowships
  (to Y.H. and M.O.), NIH (GM114660 to Y.Z.), Breast Cancer Research Foundation (BCRF
  to I.T.).
article_number: '1657'
article_processing_charge: No
article_type: original
author:
- first_name: Yangjie
  full_name: Hu, Yangjie
  last_name: Hu
- first_name: Moutasem
  full_name: Omary, Moutasem
  last_name: Omary
- first_name: Yun
  full_name: Hu, Yun
  last_name: Hu
- first_name: Ohad
  full_name: Doron, Ohad
  last_name: Doron
- first_name: Lukas
  full_name: Hörmayer, Lukas
  id: 2EEE7A2A-F248-11E8-B48F-1D18A9856A87
  last_name: Hörmayer
  orcid: 0000-0001-8295-2926
- first_name: Qingguo
  full_name: Chen, Qingguo
  last_name: Chen
- first_name: Or
  full_name: Megides, Or
  last_name: Megides
- first_name: Ori
  full_name: Chekli, Ori
  last_name: Chekli
- first_name: Zhaojun
  full_name: Ding, Zhaojun
  last_name: Ding
- first_name: Jiří
  full_name: Friml, Jiří
  id: 4159519E-F248-11E8-B48F-1D18A9856A87
  last_name: Friml
  orcid: 0000-0002-8302-7596
- first_name: Yunde
  full_name: Zhao, Yunde
  last_name: Zhao
- first_name: Ilan
  full_name: Tsarfaty, Ilan
  last_name: Tsarfaty
- first_name: Eilon
  full_name: Shani, Eilon
  last_name: Shani
citation:
  ama: Hu Y, Omary M, Hu Y, et al. Cell kinetics of auxin transport and activity in
    Arabidopsis root growth and skewing. <i>Nature Communications</i>. 2021;12. doi:<a
    href="https://doi.org/10.1038/s41467-021-21802-3">10.1038/s41467-021-21802-3</a>
  apa: Hu, Y., Omary, M., Hu, Y., Doron, O., Hörmayer, L., Chen, Q., … Shani, E. (2021).
    Cell kinetics of auxin transport and activity in Arabidopsis root growth and skewing.
    <i>Nature Communications</i>. Springer Nature. <a href="https://doi.org/10.1038/s41467-021-21802-3">https://doi.org/10.1038/s41467-021-21802-3</a>
  chicago: Hu, Yangjie, Moutasem Omary, Yun Hu, Ohad Doron, Lukas Hörmayer, Qingguo
    Chen, Or Megides, et al. “Cell Kinetics of Auxin Transport and Activity in Arabidopsis
    Root Growth and Skewing.” <i>Nature Communications</i>. Springer Nature, 2021.
    <a href="https://doi.org/10.1038/s41467-021-21802-3">https://doi.org/10.1038/s41467-021-21802-3</a>.
  ieee: Y. Hu <i>et al.</i>, “Cell kinetics of auxin transport and activity in Arabidopsis
    root growth and skewing,” <i>Nature Communications</i>, vol. 12. Springer Nature,
    2021.
  ista: Hu Y, Omary M, Hu Y, Doron O, Hörmayer L, Chen Q, Megides O, Chekli O, Ding
    Z, Friml J, Zhao Y, Tsarfaty I, Shani E. 2021. Cell kinetics of auxin transport
    and activity in Arabidopsis root growth and skewing. Nature Communications. 12,
    1657.
  mla: Hu, Yangjie, et al. “Cell Kinetics of Auxin Transport and Activity in Arabidopsis
    Root Growth and Skewing.” <i>Nature Communications</i>, vol. 12, 1657, Springer
    Nature, 2021, doi:<a href="https://doi.org/10.1038/s41467-021-21802-3">10.1038/s41467-021-21802-3</a>.
  short: Y. Hu, M. Omary, Y. Hu, O. Doron, L. Hörmayer, Q. Chen, O. Megides, O. Chekli,
    Z. Ding, J. Friml, Y. Zhao, I. Tsarfaty, E. Shani, Nature Communications 12 (2021).
date_created: 2021-03-21T23:01:19Z
date_published: 2021-03-12T00:00:00Z
date_updated: 2026-04-02T13:57:40Z
day: '12'
ddc:
- '580'
department:
- _id: JiFr
doi: 10.1038/s41467-021-21802-3
external_id:
  isi:
  - '000630419400048'
  pmid:
  - '33712581'
file:
- access_level: open_access
  checksum: e1022f3aee349853ded2b2b3e092362d
  content_type: application/pdf
  creator: dernst
  date_created: 2021-03-22T11:18:58Z
  date_updated: 2021-03-22T11:18:58Z
  file_id: '9275'
  file_name: 2021_NatureComm_Hu.pdf
  file_size: 8602096
  relation: main_file
  success: 1
file_date_updated: 2021-03-22T11:18:58Z
has_accepted_license: '1'
intvolume: '        12'
isi: 1
language:
- iso: eng
month: '03'
oa: 1
oa_version: Published Version
pmid: 1
publication: Nature Communications
publication_identifier:
  eissn:
  - 2041-1723
publication_status: published
publisher: Springer Nature
quality_controlled: '1'
scopus_import: '1'
status: public
title: Cell kinetics of auxin transport and activity in Arabidopsis root growth and
  skewing
tmp:
  image: /images/cc_by.png
  legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
  name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
  short: CC BY (4.0)
type: journal_article
user_id: ba8df636-2132-11f1-aed0-ed93e2281fdd
volume: 12
year: '2021'
...
---
_id: '9290'
abstract:
- lang: eng
  text: Polar subcellular localization of the PIN exporters of the phytohormone auxin
    is a key determinant of directional, intercellular auxin transport and thus a
    central topic of both plant cell and developmental biology. Arabidopsis mutants
    lacking PID, a kinase that phosphorylates PINs, or the MAB4/MEL proteins of unknown
    molecular function display PIN polarity defects and phenocopy pin mutants, but
    mechanistic insights into how these factors convey PIN polarity are missing. Here,
    by combining protein biochemistry with quantitative live-cell imaging, we demonstrate
    that PINs, MAB4/MELs, and AGC kinases interact in the same complex at the plasma
    membrane. MAB4/MELs are recruited to the plasma membrane by the PINs and in concert
    with the AGC kinases maintain PIN polarity through limiting lateral diffusion-based
    escape of PINs from the polar domain. The PIN-MAB4/MEL-PID protein complex has
    self-reinforcing properties thanks to positive feedback between AGC kinase-mediated
    PIN phosphorylation and MAB4/MEL recruitment. We thus uncover the molecular mechanism
    by which AGC kinases and MAB4/MEL proteins regulate PIN localization and plant
    development.
acknowledged_ssus:
- _id: Bio
acknowledgement: We acknowledge Ben Scheres, Christian Luschnig, and Claus Schwechheimer
  for sharing published material. We thank Monika Hrtyan and Dorota Jaworska at IST
  Austria and Gerda Lamers and Ward de Winter at IBL Netherlands for technical assistance;
  Corinna Hartinger, Jakub Hajný, Lesia Rodriguez, Mingyue Li, and Lindy Abas for
  experimental support; and the Bioimaging Facility at IST Austria and the Bioimaging
  Core at VIB for imaging support. We are grateful to Christian Luschnig, Lindy Abas,
  and Roman Pleskot for valuable discussions. We also acknowledge the EMBO for supporting
  M.G. with a long-term fellowship ( ALTF 1005-2019 ) during the finalization and
  revision of this manuscript in the laboratory of B.D.R., and we thank R. Pierik
  for allowing K.V.G. to work on this manuscript during a postdoc in his laboratory
  at Utrecht University. This work was supported by grants from the European Research
  Council under the European Union’s Seventh Framework Programme (ERC grant agreements
  742985 to J.F., 714055 to B.D.R., and 803048 to M.F.), the Austrian Science Fund
  (FWF; I 3630-B25 to J.F.), Chemical Sciences (partly) financed by the Dutch Research
  Council (NWO-CW TOP 700.58.301 to R.O.), the Dutch Research Council (NWO-VICI 865.17.002
  to R. Pierik), Grants-in-Aid from the Ministry of Education, Culture, Sports, Science
  and Technology, Japan (KAKENHI grant 17K17595 to S.N.), the Ministry of Education,
  Youth and Sports of the Czech Republic (MŠMT project NPUI-LO1417 ), and a China
  Scholarship Council (to X.W.).
article_processing_charge: No
article_type: original
author:
- first_name: Matous
  full_name: Glanc, Matous
  id: 1AE1EA24-02D0-11E9-9BAA-DAF4881429F2
  last_name: Glanc
  orcid: 0000-0003-0619-7783
- first_name: K
  full_name: Van Gelderen, K
  last_name: Van Gelderen
- first_name: Lukas
  full_name: Hörmayer, Lukas
  id: 2EEE7A2A-F248-11E8-B48F-1D18A9856A87
  last_name: Hörmayer
  orcid: 0000-0001-8295-2926
- first_name: Shutang
  full_name: Tan, Shutang
  id: 2DE75584-F248-11E8-B48F-1D18A9856A87
  last_name: Tan
  orcid: 0000-0002-0471-8285
- first_name: S
  full_name: Naramoto, S
  last_name: Naramoto
- first_name: Xixi
  full_name: Zhang, Xixi
  id: 61A66458-47E9-11EA-85BA-8AEAAF14E49A
  last_name: Zhang
  orcid: 0000-0001-7048-4627
- first_name: David
  full_name: Domjan, David
  id: C684CD7A-257E-11EA-9B6F-D8588B4F947F
  last_name: Domjan
  orcid: 0000-0003-2267-106X
- first_name: L
  full_name: Vcelarova, L
  last_name: Vcelarova
- first_name: Robert
  full_name: Hauschild, Robert
  id: 4E01D6B4-F248-11E8-B48F-1D18A9856A87
  last_name: Hauschild
  orcid: 0000-0001-9843-3522
- first_name: Alexander J
  full_name: Johnson, Alexander J
  id: 46A62C3A-F248-11E8-B48F-1D18A9856A87
  last_name: Johnson
  orcid: 0000-0002-2739-8843
- first_name: E
  full_name: de Koning, E
  last_name: de Koning
- first_name: M
  full_name: van Dop, M
  last_name: van Dop
- first_name: E
  full_name: Rademacher, E
  last_name: Rademacher
- first_name: S
  full_name: Janson, S
  last_name: Janson
- first_name: X
  full_name: Wei, X
  last_name: Wei
- first_name: Gergely
  full_name: Molnar, Gergely
  id: 34F1AF46-F248-11E8-B48F-1D18A9856A87
  last_name: Molnar
- first_name: Matyas
  full_name: Fendrych, Matyas
  id: 43905548-F248-11E8-B48F-1D18A9856A87
  last_name: Fendrych
  orcid: 0000-0002-9767-8699
- first_name: B
  full_name: De Rybel, B
  last_name: De Rybel
- first_name: R
  full_name: Offringa, R
  last_name: Offringa
- first_name: Jiří
  full_name: Friml, Jiří
  id: 4159519E-F248-11E8-B48F-1D18A9856A87
  last_name: Friml
  orcid: 0000-0002-8302-7596
citation:
  ama: Glanc M, Van Gelderen K, Hörmayer L, et al. AGC kinases and MAB4/MEL proteins
    maintain PIN polarity by limiting lateral diffusion in plant cells. <i>Current
    Biology</i>. 2021;31(9):1918-1930. doi:<a href="https://doi.org/10.1016/j.cub.2021.02.028">10.1016/j.cub.2021.02.028</a>
  apa: Glanc, M., Van Gelderen, K., Hörmayer, L., Tan, S., Naramoto, S., Zhang, X.,
    … Friml, J. (2021). AGC kinases and MAB4/MEL proteins maintain PIN polarity by
    limiting lateral diffusion in plant cells. <i>Current Biology</i>. Elsevier. <a
    href="https://doi.org/10.1016/j.cub.2021.02.028">https://doi.org/10.1016/j.cub.2021.02.028</a>
  chicago: Glanc, Matous, K Van Gelderen, Lukas Hörmayer, Shutang Tan, S Naramoto,
    Xixi Zhang, David Domjan, et al. “AGC Kinases and MAB4/MEL Proteins Maintain PIN
    Polarity by Limiting Lateral Diffusion in Plant Cells.” <i>Current Biology</i>.
    Elsevier, 2021. <a href="https://doi.org/10.1016/j.cub.2021.02.028">https://doi.org/10.1016/j.cub.2021.02.028</a>.
  ieee: M. Glanc <i>et al.</i>, “AGC kinases and MAB4/MEL proteins maintain PIN polarity
    by limiting lateral diffusion in plant cells,” <i>Current Biology</i>, vol. 31,
    no. 9. Elsevier, pp. 1918–1930, 2021.
  ista: Glanc M, Van Gelderen K, Hörmayer L, Tan S, Naramoto S, Zhang X, Domjan D,
    Vcelarova L, Hauschild R, Johnson AJ, de Koning E, van Dop M, Rademacher E, Janson
    S, Wei X, Molnar G, Fendrych M, De Rybel B, Offringa R, Friml J. 2021. AGC kinases
    and MAB4/MEL proteins maintain PIN polarity by limiting lateral diffusion in plant
    cells. Current Biology. 31(9), 1918–1930.
  mla: Glanc, Matous, et al. “AGC Kinases and MAB4/MEL Proteins Maintain PIN Polarity
    by Limiting Lateral Diffusion in Plant Cells.” <i>Current Biology</i>, vol. 31,
    no. 9, Elsevier, 2021, pp. 1918–30, doi:<a href="https://doi.org/10.1016/j.cub.2021.02.028">10.1016/j.cub.2021.02.028</a>.
  short: M. Glanc, K. Van Gelderen, L. Hörmayer, S. Tan, S. Naramoto, X. Zhang, D.
    Domjan, L. Vcelarova, R. Hauschild, A.J. Johnson, E. de Koning, M. van Dop, E.
    Rademacher, S. Janson, X. Wei, G. Molnar, M. Fendrych, B. De Rybel, R. Offringa,
    J. Friml, Current Biology 31 (2021) 1918–1930.
corr_author: '1'
date_created: 2021-03-26T12:09:33Z
date_published: 2021-03-10T00:00:00Z
date_updated: 2025-04-14T07:45:00Z
day: '10'
ddc:
- '580'
department:
- _id: JiFr
doi: 10.1016/j.cub.2021.02.028
ec_funded: 1
external_id:
  isi:
  - '000653077800004'
  pmid:
  - '33705718'
file:
- access_level: open_access
  checksum: b1723040ecfd8c81194185472eb62546
  content_type: application/pdf
  creator: dernst
  date_created: 2021-04-01T10:53:42Z
  date_updated: 2021-04-01T10:53:42Z
  file_id: '9303'
  file_name: 2021_CurrentBiology_Glanc.pdf
  file_size: 4324371
  relation: main_file
  success: 1
file_date_updated: 2021-04-01T10:53:42Z
has_accepted_license: '1'
intvolume: '        31'
isi: 1
issue: '9'
language:
- iso: eng
month: '03'
oa: 1
oa_version: Published Version
page: 1918-1930
pmid: 1
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
  call_identifier: FWF
  grant_number: I03630
  name: Molecular mechanisms of endocytic cargo recognition in plants
publication: Current Biology
publication_identifier:
  eissn:
  - 1879-0445
  issn:
  - 0960-9822
publication_status: published
publisher: Elsevier
quality_controlled: '1'
scopus_import: '1'
status: public
title: AGC kinases and MAB4/MEL proteins maintain PIN polarity by limiting lateral
  diffusion in plant cells
tmp:
  image: /images/cc_by.png
  legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
  name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
  short: CC BY (4.0)
type: journal_article
user_id: c635000d-4b10-11ee-a964-aac5a93f6ac1
volume: 31
year: '2021'
...
---
_id: '8931'
abstract:
- lang: eng
  text: "Auxin is a major plant growth regulator, but current models on auxin perception
    and signaling cannot explain the whole plethora of auxin effects, in particular
    those associated with rapid responses. A possible candidate for a component of
    additional auxin perception mechanisms is the AUXIN BINDING PROTEIN 1 (ABP1),
    whose function in planta remains unclear.\r\nHere we combined expression analysis
    with gain- and loss-of-function approaches to analyze the role of ABP1 in plant
    development. ABP1 shows a broad expression largely overlapping with, but not regulated
    by, transcriptional auxin response activity. Furthermore, ABP1 activity is not
    essential for the transcriptional auxin signaling. Genetic in planta analysis
    revealed that abp1 loss-of-function mutants show largely normal development with
    minor defects in bolting. On the other hand, ABP1 gain-of-function alleles show
    a broad range of growth and developmental defects, including root and hypocotyl
    growth and bending, lateral root and leaf development, bolting, as well as response
    to heat stress. At the cellular level, ABP1 gain-of-function leads to impaired
    auxin effect on PIN polar distribution and affects BFA-sensitive PIN intracellular
    aggregation.\r\nThe gain-of-function analysis suggests a broad, but still mechanistically
    unclear involvement of ABP1 in plant development, possibly masked in abp1 loss-of-function
    mutants by a functional redundancy."
acknowledged_ssus:
- _id: Bio
- _id: LifeSc
acknowledgement: We would like to acknowledge Bioimaging and Life Science Facilities
  at IST Austria for continuous support and also the Plant Sciences Core Facility
  of CEITEC Masaryk University for their support with obtaining a part of the scientific
  data. We gratefully acknowledge Lindy Abas for help with ABP1::GFP-ABP1 construct
  design. 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] and Austrian Science Fund (FWF) [I 3630-B25] to J.F.; DOC Fellowship
  of the Austrian Academy of Sciences to L.L.; the European Structural and Investment
  Funds, Operational Programme Research, Development and Education - Project „MSCAfellow@MUNI“
  [CZ.02.2.69/0.0/0.0/17_050/0008496] to M.P.. This project was also supported by
  the Czech Science Foundation [GA 20-20860Y] to M.Z and MEYS CR [project no.CZ.02.1.01/0.0/0.0/16_019/0000738]
  to M. Č.
article_number: '110750'
article_processing_charge: Yes (via OA deal)
article_type: original
author:
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  last_name: Čovanová
- first_name: Marta
  full_name: Zwiewka, Marta
  last_name: Zwiewka
- first_name: Lukas
  full_name: Hörmayer, Lukas
  id: 2EEE7A2A-F248-11E8-B48F-1D18A9856A87
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- first_name: Matyas
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  last_name: Fendrych
  orcid: 0000-0002-9767-8699
- first_name: Tongda
  full_name: Xu, Tongda
  last_name: Xu
- first_name: Teva
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citation:
  ama: Gelová Z, Gallei MC, Pernisová M, et al. Developmental roles of auxin binding
    protein 1 in Arabidopsis thaliana. <i>Plant Science</i>. 2021;303. doi:<a href="https://doi.org/10.1016/j.plantsci.2020.110750">10.1016/j.plantsci.2020.110750</a>
  apa: Gelová, Z., Gallei, M. C., Pernisová, M., Brunoud, G., Zhang, X., Glanc, M.,
    … Friml, J. (2021). Developmental roles of auxin binding protein 1 in Arabidopsis
    thaliana. <i>Plant Science</i>. Elsevier. <a href="https://doi.org/10.1016/j.plantsci.2020.110750">https://doi.org/10.1016/j.plantsci.2020.110750</a>
  chicago: Gelová, Zuzana, Michelle C Gallei, Markéta Pernisová, Géraldine Brunoud,
    Xixi Zhang, Matous Glanc, Lanxin Li, et al. “Developmental Roles of Auxin Binding
    Protein 1 in Arabidopsis Thaliana.” <i>Plant Science</i>. Elsevier, 2021. <a href="https://doi.org/10.1016/j.plantsci.2020.110750">https://doi.org/10.1016/j.plantsci.2020.110750</a>.
  ieee: Z. Gelová <i>et al.</i>, “Developmental roles of auxin binding protein 1 in
    Arabidopsis thaliana,” <i>Plant Science</i>, vol. 303. Elsevier, 2021.
  ista: Gelová Z, Gallei MC, Pernisová M, Brunoud G, Zhang X, Glanc M, Li L, Michalko
    J, Pavlovicova Z, Verstraeten I, Han H, Hajny J, Hauschild R, Čovanová M, Zwiewka
    M, Hörmayer L, Fendrych M, Xu T, Vernoux T, Friml J. 2021. Developmental roles
    of auxin binding protein 1 in Arabidopsis thaliana. Plant Science. 303, 110750.
  mla: Gelová, Zuzana, et al. “Developmental Roles of Auxin Binding Protein 1 in Arabidopsis
    Thaliana.” <i>Plant Science</i>, vol. 303, 110750, Elsevier, 2021, doi:<a href="https://doi.org/10.1016/j.plantsci.2020.110750">10.1016/j.plantsci.2020.110750</a>.
  short: Z. Gelová, M.C. Gallei, M. Pernisová, G. Brunoud, X. Zhang, M. Glanc, L.
    Li, J. Michalko, Z. Pavlovicova, I. Verstraeten, H. Han, J. Hajny, R. Hauschild,
    M. Čovanová, M. Zwiewka, L. Hörmayer, M. Fendrych, T. Xu, T. Vernoux, J. Friml,
    Plant Science 303 (2021).
corr_author: '1'
date_created: 2020-12-09T14:48:28Z
date_published: 2021-02-01T00:00:00Z
date_updated: 2026-07-08T22:30:51Z
day: '01'
ddc:
- '580'
department:
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title: Developmental roles of auxin binding protein 1 in Arabidopsis thaliana
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  text: "Blood – this is what animals use to heal wounds fast and efficient. Plants
    do not have blood circulation and their cells cannot move. However, plants have
    evolved remarkable capacities to regenerate tissues and organs preventing further
    damage. In my PhD research, I studied the wound healing in the Arabidopsis root.
    I used a UV laser to ablate single cells in the root tip and observed the consequent
    wound healing. Interestingly, the inner adjacent cells induced a\r\ndivision plane
    switch and subsequently adopted the cell type of the killed cell to replace it.
    We termed this form of wound healing “restorative divisions”. This initial observation
    triggered the questions of my PhD studies: How and why do cells orient their division
    planes, how do they feel the wound and why does this happen only in inner adjacent
    cells.\r\nFor answering these questions, I used a quite simple experimental setup:
    5 day - old seedlings were stained with propidium iodide to visualize cell walls
    and dead cells; ablation was carried out using a special laser cutter and a confocal
    microscope. Adaptation of the novel vertical microscope system made it possible
    to observe wounds in real time. This revealed that restorative divisions occur
    at increased frequency compared to normal divisions. Additionally,\r\nthe major
    plant hormone auxin accumulates in wound adjacent cells and drives the expression
    of the wound-stress responsive transcription factor ERF115. Using this as a marker
    gene for wound responses, we found that an important part of wound signalling
    is the sensing of the collapse of the ablated cell. The collapse causes a radical
    pressure drop, which results in strong tissue deformations. These deformations
    manifest in an invasion of the now free spot specifically by the inner adjacent
    cells within seconds, probably because of higher pressure of the inner tissues.
    Long-term imaging revealed that those deformed cells continuously expand towards
    the wound hole and that this is crucial for the restorative division. These wound-expanding
    cells exhibit an abnormal, biphasic polarity of microtubule arrays\r\nbefore the
    division. Experiments inhibiting cell expansion suggest that it is the biphasic
    stretching that induces those MT arrays. Adapting the micromanipulator aspiration
    system from animal scientists at our institute confirmed the hypothesis that stretching
    influences microtubule stability. In conclusion, this shows that microtubules
    react to tissue deformation\r\nand this facilitates the observed division plane
    switch. This puts mechanical cues and tensions at the most prominent position
    for explaining the growth and wound healing properties of plants. Hence, it shines
    light onto the importance of understanding mechanical signal transduction. "
acknowledged_ssus:
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author:
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citation:
  ama: Hörmayer L. Wound healing in the Arabidopsis root meristem. 2021. doi:<a href="https://doi.org/10.15479/at:ista:9992">10.15479/at:ista:9992</a>
  apa: Hörmayer, L. (2021). <i>Wound healing in the Arabidopsis root meristem</i>.
    Institute of Science and Technology Austria. <a href="https://doi.org/10.15479/at:ista:9992">https://doi.org/10.15479/at:ista:9992</a>
  chicago: Hörmayer, Lukas. “Wound Healing in the Arabidopsis Root Meristem.” Institute
    of Science and Technology Austria, 2021. <a href="https://doi.org/10.15479/at:ista:9992">https://doi.org/10.15479/at:ista:9992</a>.
  ieee: L. Hörmayer, “Wound healing in the Arabidopsis root meristem,” Institute of
    Science and Technology Austria, 2021.
  ista: Hörmayer L. 2021. Wound healing in the Arabidopsis root meristem. Institute
    of Science and Technology Austria.
  mla: Hörmayer, Lukas. <i>Wound Healing in the Arabidopsis Root Meristem</i>. Institute
    of Science and Technology Austria, 2021, doi:<a href="https://doi.org/10.15479/at:ista:9992">10.15479/at:ista:9992</a>.
  short: L. Hörmayer, Wound Healing in the Arabidopsis Root Meristem, Institute of
    Science and Technology Austria, 2021.
corr_author: '1'
date_created: 2021-09-09T07:37:20Z
date_published: 2021-09-13T00:00:00Z
date_updated: 2026-04-08T07:11:47Z
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oa_version: Published Version
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  grant_number: P29988
  name: RNA-directed DNA methylation in plant development
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  call_identifier: H2020
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  name: Tracing Evolution of Auxin Transport and Polarity in Plants
publication_identifier:
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publisher: Institute of Science and Technology Austria
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supervisor:
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title: Wound healing in the Arabidopsis root meristem
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abstract:
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  text: Wound healing in plant tissues, consisting of rigid cell wall-encapsulated
    cells, represents a considerable challenge and occurs through largely unknown
    mechanisms distinct from those in animals. Owing to their inability to migrate,
    plant cells rely on targeted cell division and expansion to regenerate wounds.
    Strict coordination of these wound-induced responses is essential to ensure efficient,
    spatially restricted wound healing. Single-cell tracking by live imaging allowed
    us to gain mechanistic insight into the wound perception and coordination of wound
    responses after laser-based wounding in Arabidopsis root. We revealed a crucial
    contribution of the collapse of damaged cells in wound perception and detected
    an auxin increase specific to cells immediately adjacent to the wound. This localized
    auxin increase balances wound-induced cell expansion and restorative division
    rates in a dose-dependent manner, leading to tumorous overproliferation when the
    canonical TIR1 auxin signaling is disrupted. Auxin and wound-induced turgor pressure
    changes together also spatially define the activation of key components of regeneration,
    such as the transcription regulator ERF115. Our observations suggest that the
    wound signaling involves the sensing of collapse of damaged cells and a local
    auxin signaling activation to coordinate the downstream transcriptional responses
    in the immediate wound vicinity.
acknowledged_ssus:
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- _id: LifeSc
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author:
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  id: 2EEE7A2A-F248-11E8-B48F-1D18A9856A87
  last_name: Hörmayer
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- first_name: Juan C
  full_name: Montesinos López, Juan C
  id: 310A8E3E-F248-11E8-B48F-1D18A9856A87
  last_name: Montesinos López
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  last_name: Benková
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- first_name: Saiko
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  last_name: Yoshida
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- first_name: Jiří
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  id: 4159519E-F248-11E8-B48F-1D18A9856A87
  last_name: Friml
  orcid: 0000-0002-8302-7596
citation:
  ama: Hörmayer L, Montesinos López JC, Marhavá P, Benková E, Yoshida S, Friml J.
    Wounding-induced changes in cellular pressure and localized auxin signalling spatially
    coordinate restorative divisions in roots. <i>Proceedings of the National Academy
    of Sciences of the United States of America</i>. 2020;117(26). doi:<a href="https://doi.org/10.1073/pnas.2003346117">10.1073/pnas.2003346117</a>
  apa: Hörmayer, L., Montesinos López, J. C., Marhavá, P., Benková, E., Yoshida, S.,
    &#38; Friml, J. (2020). Wounding-induced changes in cellular pressure and localized
    auxin signalling spatially coordinate restorative divisions in roots. <i>Proceedings
    of the National Academy of Sciences of the United States of America</i>. National
    Academy of Sciences. <a href="https://doi.org/10.1073/pnas.2003346117">https://doi.org/10.1073/pnas.2003346117</a>
  chicago: Hörmayer, Lukas, Juan C Montesinos López, Petra Marhavá, Eva Benková, Saiko
    Yoshida, and Jiří Friml. “Wounding-Induced Changes in Cellular Pressure and Localized
    Auxin Signalling Spatially Coordinate Restorative Divisions in Roots.” <i>Proceedings
    of the National Academy of Sciences of the United States of America</i>. National
    Academy of Sciences, 2020. <a href="https://doi.org/10.1073/pnas.2003346117">https://doi.org/10.1073/pnas.2003346117</a>.
  ieee: L. Hörmayer, J. C. Montesinos López, P. Marhavá, E. Benková, S. Yoshida, and
    J. Friml, “Wounding-induced changes in cellular pressure and localized auxin signalling
    spatially coordinate restorative divisions in roots,” <i>Proceedings of the National
    Academy of Sciences of the United States of America</i>, vol. 117, no. 26. National
    Academy of Sciences, 2020.
  ista: Hörmayer L, Montesinos López JC, Marhavá P, Benková E, Yoshida S, Friml J.
    2020. Wounding-induced changes in cellular pressure and localized auxin signalling
    spatially coordinate restorative divisions in roots. Proceedings of the National
    Academy of Sciences of the United States of America. 117(26), 202003346.
  mla: Hörmayer, Lukas, et al. “Wounding-Induced Changes in Cellular Pressure and
    Localized Auxin Signalling Spatially Coordinate Restorative Divisions in Roots.”
    <i>Proceedings of the National Academy of Sciences of the United States of America</i>,
    vol. 117, no. 26, 202003346, National Academy of Sciences, 2020, doi:<a href="https://doi.org/10.1073/pnas.2003346117">10.1073/pnas.2003346117</a>.
  short: L. Hörmayer, J.C. Montesinos López, P. Marhavá, E. Benková, S. Yoshida, J.
    Friml, Proceedings of the National Academy of Sciences of the United States of
    America 117 (2020).
corr_author: '1'
date_created: 2020-06-22T13:33:52Z
date_published: 2020-06-30T00:00:00Z
date_updated: 2026-07-08T22:31:18Z
day: '30'
ddc:
- '580'
department:
- _id: JiFr
- _id: EvBe
doi: 10.1073/pnas.2003346117
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  name: Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International
    (CC BY-NC-ND 4.0)
  short: CC BY-NC-ND (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 117
year: '2020'
...
---
_id: '6351'
abstract:
- lang: eng
  text: "A process of restorative patterning in plant roots correctly replaces eliminated
    cells to heal local injuries despite the absence of cell migration, which underpins
    wound healing in animals. \r\n\r\nPatterning in plants relies on oriented cell
    divisions and acquisition of specific cell identities. Plants regularly endure
    wounds caused by abiotic or biotic environmental stimuli and have developed extraordinary
    abilities to restore their tissues after injuries. Here, we provide insight into
    a mechanism of restorative patterning that repairs tissues after wounding. Laser-assisted
    elimination of different cells in Arabidopsis root combined with live-imaging
    tracking during vertical growth allowed analysis of the regeneration processes
    in vivo. Specifically, the cells adjacent to the inner side of the injury re-activated
    their stem cell transcriptional programs. They accelerated their progression through
    cell cycle, coordinately changed the cell division orientation, and ultimately
    acquired de novo the correct cell fates to replace missing cells. These observations
    highlight existence of unknown intercellular positional signaling and demonstrate
    the capability of specified cells to re-acquire stem cell programs as a crucial
    part of the plant-specific mechanism of wound healing."
acknowledged_ssus:
- _id: Bio
article_processing_charge: No
author:
- first_name: Petra
  full_name: Marhavá, Petra
  id: 44E59624-F248-11E8-B48F-1D18A9856A87
  last_name: Marhavá
- first_name: Lukas
  full_name: Hörmayer, Lukas
  id: 2EEE7A2A-F248-11E8-B48F-1D18A9856A87
  last_name: Hörmayer
  orcid: 0000-0001-8295-2926
- first_name: Saiko
  full_name: Yoshida, Saiko
  id: 2E46069C-F248-11E8-B48F-1D18A9856A87
  last_name: Yoshida
  orcid: 0000-0001-6111-9353
- first_name: Peter
  full_name: Marhavy, Peter
  id: 3F45B078-F248-11E8-B48F-1D18A9856A87
  last_name: Marhavy
  orcid: 0000-0001-5227-5741
- first_name: Eva
  full_name: Benková, Eva
  id: 38F4F166-F248-11E8-B48F-1D18A9856A87
  last_name: Benková
  orcid: 0000-0002-8510-9739
- first_name: Jiří
  full_name: Friml, Jiří
  id: 4159519E-F248-11E8-B48F-1D18A9856A87
  last_name: Friml
  orcid: 0000-0002-8302-7596
citation:
  ama: Marhavá P, Hörmayer L, Yoshida S, Marhavý P, Benková E, Friml J. Re-activation
    of stem cell pathways for pattern restoration in plant wound healing. <i>Cell</i>.
    2019;177(4):957-969.e13. doi:<a href="https://doi.org/10.1016/j.cell.2019.04.015">10.1016/j.cell.2019.04.015</a>
  apa: Marhavá, P., Hörmayer, L., Yoshida, S., Marhavý, P., Benková, E., &#38; Friml,
    J. (2019). Re-activation of stem cell pathways for pattern restoration in plant
    wound healing. <i>Cell</i>. Elsevier. <a href="https://doi.org/10.1016/j.cell.2019.04.015">https://doi.org/10.1016/j.cell.2019.04.015</a>
  chicago: Marhavá, Petra, Lukas Hörmayer, Saiko Yoshida, Peter Marhavý, Eva Benková,
    and Jiří Friml. “Re-Activation of Stem Cell Pathways for Pattern Restoration in
    Plant Wound Healing.” <i>Cell</i>. Elsevier, 2019. <a href="https://doi.org/10.1016/j.cell.2019.04.015">https://doi.org/10.1016/j.cell.2019.04.015</a>.
  ieee: P. Marhavá, L. Hörmayer, S. Yoshida, P. Marhavý, E. Benková, and J. Friml,
    “Re-activation of stem cell pathways for pattern restoration in plant wound healing,”
    <i>Cell</i>, vol. 177, no. 4. Elsevier, p. 957–969.e13, 2019.
  ista: Marhavá P, Hörmayer L, Yoshida S, Marhavý P, Benková E, Friml J. 2019. Re-activation
    of stem cell pathways for pattern restoration in plant wound healing. Cell. 177(4),
    957–969.e13.
  mla: Marhavá, Petra, et al. “Re-Activation of Stem Cell Pathways for Pattern Restoration
    in Plant Wound Healing.” <i>Cell</i>, vol. 177, no. 4, Elsevier, 2019, p. 957–969.e13,
    doi:<a href="https://doi.org/10.1016/j.cell.2019.04.015">10.1016/j.cell.2019.04.015</a>.
  short: P. Marhavá, L. Hörmayer, S. Yoshida, P. Marhavý, E. Benková, J. Friml, Cell
    177 (2019) 957–969.e13.
corr_author: '1'
date_created: 2019-04-28T21:59:14Z
date_published: 2019-05-02T00:00:00Z
date_updated: 2026-07-08T22:31:18Z
day: '02'
ddc:
- '570'
department:
- _id: JiFr
- _id: EvBe
doi: 10.1016/j.cell.2019.04.015
ec_funded: 1
external_id:
  isi:
  - '000466843000015'
  pmid:
  - '31051107'
file:
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  date_created: 2019-05-13T06:12:45Z
  date_updated: 2020-07-14T12:47:28Z
  file_id: '6411'
  file_name: 2019_Cell_Marhava.pdf
  file_size: 10272032
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file_date_updated: 2020-07-14T12:47:28Z
has_accepted_license: '1'
intvolume: '       177'
isi: 1
issue: '4'
language:
- iso: eng
month: '05'
oa: 1
oa_version: Published Version
page: 957-969.e13
pmid: 1
project:
- _id: 261099A6-B435-11E9-9278-68D0E5697425
  call_identifier: H2020
  grant_number: '742985'
  name: Tracing Evolution of Auxin Transport and Polarity in Plants
publication: Cell
publication_identifier:
  eissn:
  - 1097-4172
  issn:
  - 0092-8674
publication_status: published
publisher: Elsevier
quality_controlled: '1'
related_material:
  link:
  - description: News on IST Homepage
    relation: press_release
    url: https://ist.ac.at/en/news/specialized-plant-cells-regain-stem-cell-features-to-heal-wounds/
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  - id: '9992'
    relation: dissertation_contains
    status: public
scopus_import: '1'
status: public
title: Re-activation of stem cell pathways for pattern restoration in plant wound
  healing
tmp:
  image: /images/cc_by.png
  legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
  name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
  short: CC BY (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 177
year: '2019'
...
---
_id: '6943'
abstract:
- lang: eng
  text: Plants as sessile organisms are constantly under attack by herbivores, rough
    environmental situations, or mechanical pressure. These challenges often lead
    to the induction of wounds or destruction of already specified and developed tissues.
    Additionally, wounding makes plants vulnerable to invasion by pathogens, which
    is why wound signalling often triggers specific defence responses. To stay competitive
    or, eventually, survive under these circumstances, plants need to regenerate efficiently,
    which in rigid, tissue migration-incompatible plant tissues requires post-embryonic
    patterning and organogenesis. Now, several studies used laser-assisted single
    cell ablation in the Arabidopsis root tip as a minimal wounding proxy. Here, we
    discuss their findings and put them into context of a broader spectrum of wound
    signalling, pathogen responses and tissue as well as organ regeneration.
article_processing_charge: No
article_type: original
author:
- first_name: Lukas
  full_name: Hörmayer, Lukas
  id: 2EEE7A2A-F248-11E8-B48F-1D18A9856A87
  last_name: Hörmayer
  orcid: 0000-0001-8295-2926
- first_name: Jiří
  full_name: Friml, Jiří
  id: 4159519E-F248-11E8-B48F-1D18A9856A87
  last_name: Friml
  orcid: 0000-0002-8302-7596
citation:
  ama: Hörmayer L, Friml J. Targeted cell ablation-based insights into wound healing
    and restorative patterning. <i>Current Opinion in Plant Biology</i>. 2019;52:124-130.
    doi:<a href="https://doi.org/10.1016/j.pbi.2019.08.006">10.1016/j.pbi.2019.08.006</a>
  apa: Hörmayer, L., &#38; Friml, J. (2019). Targeted cell ablation-based insights
    into wound healing and restorative patterning. <i>Current Opinion in Plant Biology</i>.
    Elsevier. <a href="https://doi.org/10.1016/j.pbi.2019.08.006">https://doi.org/10.1016/j.pbi.2019.08.006</a>
  chicago: Hörmayer, Lukas, and Jiří Friml. “Targeted Cell Ablation-Based Insights
    into Wound Healing and Restorative Patterning.” <i>Current Opinion in Plant Biology</i>.
    Elsevier, 2019. <a href="https://doi.org/10.1016/j.pbi.2019.08.006">https://doi.org/10.1016/j.pbi.2019.08.006</a>.
  ieee: L. Hörmayer and J. Friml, “Targeted cell ablation-based insights into wound
    healing and restorative patterning,” <i>Current Opinion in Plant Biology</i>,
    vol. 52. Elsevier, pp. 124–130, 2019.
  ista: Hörmayer L, Friml J. 2019. Targeted cell ablation-based insights into wound
    healing and restorative patterning. Current Opinion in Plant Biology. 52, 124–130.
  mla: Hörmayer, Lukas, and Jiří Friml. “Targeted Cell Ablation-Based Insights into
    Wound Healing and Restorative Patterning.” <i>Current Opinion in Plant Biology</i>,
    vol. 52, Elsevier, 2019, pp. 124–30, doi:<a href="https://doi.org/10.1016/j.pbi.2019.08.006">10.1016/j.pbi.2019.08.006</a>.
  short: L. Hörmayer, J. Friml, Current Opinion in Plant Biology 52 (2019) 124–130.
corr_author: '1'
date_created: 2019-10-14T07:00:24Z
date_published: 2019-12-01T00:00:00Z
date_updated: 2026-07-08T22:31:17Z
day: '01'
ddc:
- '580'
department:
- _id: JiFr
doi: 10.1016/j.pbi.2019.08.006
ec_funded: 1
external_id:
  isi:
  - '000502890600017'
  pmid:
  - '31585333'
file:
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  date_created: 2019-10-14T14:48:21Z
  date_updated: 2020-07-14T12:47:45Z
  file_id: '6946'
  file_name: 2019_CurrentOpinionPlant_Hoermayer.pdf
  file_size: 1659288
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file_date_updated: 2020-07-14T12:47:45Z
has_accepted_license: '1'
intvolume: '        52'
isi: 1
language:
- iso: eng
month: '12'
oa: 1
oa_version: Published Version
page: 124-130
pmid: 1
project:
- _id: 261099A6-B435-11E9-9278-68D0E5697425
  call_identifier: H2020
  grant_number: '742985'
  name: Tracing Evolution of Auxin Transport and Polarity in Plants
publication: Current Opinion in Plant Biology
publication_identifier:
  issn:
  - 1369-5266
publication_status: published
publisher: Elsevier
quality_controlled: '1'
related_material:
  record:
  - id: '9992'
    relation: dissertation_contains
    status: public
scopus_import: '1'
status: public
title: Targeted cell ablation-based insights into wound healing and restorative patterning
tmp:
  image: /images/cc_by.png
  legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
  name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
  short: CC BY (4.0)
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 52
year: '2019'
...
