---
_id: '14339'
abstract:
- lang: eng
text: Lateral roots are typically maintained at non-vertical angles with respect
to gravity. These gravitropic setpoint angles are intriguing because their maintenance
requires that roots are able to effect growth response both with and against the
gravity vector, a phenomenon previously attributed to gravitropism acting against
an antigravitropic offset mechanism. Here we show how the components mediating
gravitropism in the vertical primary root—PINs and phosphatases acting upon them—are
reconfigured in their regulation such that lateral root growth at a range of angles
can be maintained. We show that the ability of Arabidopsis lateral roots to bend
both downward and upward requires the generation of auxin asymmetries and is driven
by angle-dependent variation in downward gravitropic auxin flux acting against
angle-independent upward, antigravitropic flux. Further, we demonstrate a symmetry
in auxin distribution in lateral roots at gravitropic setpoint angle that can
be traced back to a net, balanced polarization of PIN3 and PIN7 auxin transporters
in the columella. These auxin fluxes are shifted by altering PIN protein phosphoregulation
in the columella, either by introducing PIN3 phosphovariant versions or via manipulation
of levels of the phosphatase subunit PP2A/RCN1. Finally, we show that auxin, in
addition to driving lateral root directional growth, acts within the lateral root
columella to induce more vertical growth by increasing RCN1 levels, causing a
downward shift in PIN3 localization, thereby diminishing the magnitude of the
upward, antigravitropic auxin flux.
acknowledgement: We thank D. Weijers, C. Schwechheimer and R. Offringa for generous
sharing of published and unpublished materials and P. Masson for advice on the use
of the ARL2 promoter. We are grateful to M. Del Bianco and O. Leyser for critical
reading of the manuscript. This work was supported by the BBSRC (grants BB/N010124/1
and BB/R000859/1 to S.K.), the Gatsby Charitable Foundation and the Leverhulme Trust
(RPG-2018-137 to S.K.).
article_processing_charge: Yes (in subscription journal)
article_type: original
author:
- first_name: S
full_name: Roychoudhry, S
last_name: Roychoudhry
- first_name: K
full_name: Sageman-Furnas, K
last_name: Sageman-Furnas
- first_name: C
full_name: Wolverton, C
last_name: Wolverton
- first_name: Peter
full_name: Grones, Peter
id: 399876EC-F248-11E8-B48F-1D18A9856A87
last_name: Grones
- first_name: Shutang
full_name: Tan, Shutang
id: 2DE75584-F248-11E8-B48F-1D18A9856A87
last_name: Tan
orcid: 0000-0002-0471-8285
- first_name: Gergely
full_name: Molnar, Gergely
id: 34F1AF46-F248-11E8-B48F-1D18A9856A87
last_name: Molnar
- first_name: M
full_name: De Angelis, M
last_name: De Angelis
- first_name: HL
full_name: Goodman, HL
last_name: Goodman
- first_name: N
full_name: Capstaff, N
last_name: Capstaff
- first_name: Lloyd
full_name: JPB, Lloyd
last_name: JPB
- first_name: J
full_name: Mullen, J
last_name: Mullen
- first_name: R
full_name: Hangarter, R
last_name: Hangarter
- first_name: Jiří
full_name: Friml, Jiří
id: 4159519E-F248-11E8-B48F-1D18A9856A87
last_name: Friml
orcid: 0000-0002-8302-7596
- first_name: S
full_name: Kepinski, S
last_name: Kepinski
citation:
ama: Roychoudhry S, Sageman-Furnas K, Wolverton C, et al. Antigravitropic PIN polarization
maintains non-vertical growth in lateral roots. Nature Plants. 2023;9:1500-1513.
doi:10.1038/s41477-023-01478-x
apa: Roychoudhry, S., Sageman-Furnas, K., Wolverton, C., Grones, P., Tan, S., Molnar,
G., … Kepinski, S. (2023). Antigravitropic PIN polarization maintains non-vertical
growth in lateral roots. Nature Plants. Springer Nature. https://doi.org/10.1038/s41477-023-01478-x
chicago: Roychoudhry, S, K Sageman-Furnas, C Wolverton, Peter Grones, Shutang Tan,
Gergely Molnar, M De Angelis, et al. “Antigravitropic PIN Polarization Maintains
Non-Vertical Growth in Lateral Roots.” Nature Plants. Springer Nature,
2023. https://doi.org/10.1038/s41477-023-01478-x.
ieee: S. Roychoudhry et al., “Antigravitropic PIN polarization maintains
non-vertical growth in lateral roots,” Nature Plants, vol. 9. Springer
Nature, pp. 1500–1513, 2023.
ista: Roychoudhry S, Sageman-Furnas K, Wolverton C, Grones P, Tan S, Molnar G, De
Angelis M, Goodman H, Capstaff N, JPB L, Mullen J, Hangarter R, Friml J, Kepinski
S. 2023. Antigravitropic PIN polarization maintains non-vertical growth in lateral
roots. Nature Plants. 9, 1500–1513.
mla: Roychoudhry, S., et al. “Antigravitropic PIN Polarization Maintains Non-Vertical
Growth in Lateral Roots.” Nature Plants, vol. 9, Springer Nature, 2023,
pp. 1500–13, doi:10.1038/s41477-023-01478-x.
short: S. Roychoudhry, K. Sageman-Furnas, C. Wolverton, P. Grones, S. Tan, G. Molnar,
M. De Angelis, H. Goodman, N. Capstaff, L. JPB, J. Mullen, R. Hangarter, J. Friml,
S. Kepinski, Nature Plants 9 (2023) 1500–1513.
date_created: 2023-09-15T09:56:01Z
date_published: 2023-09-01T00:00:00Z
date_updated: 2023-12-13T12:23:49Z
day: '01'
ddc:
- '580'
department:
- _id: JiFr
doi: 10.1038/s41477-023-01478-x
external_id:
isi:
- '001069238800014'
pmid:
- '37666965'
file:
- access_level: open_access
checksum: 3d6d5d5abb937c14a5f6f0afba3b8624
content_type: application/pdf
creator: dernst
date_created: 2023-09-20T10:51:31Z
date_updated: 2023-09-20T10:51:31Z
file_id: '14351'
file_name: 2023_NaturePlants_Roychoudhry.pdf
file_size: 9647103
relation: main_file
success: 1
file_date_updated: 2023-09-20T10:51:31Z
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intvolume: ' 9'
isi: 1
language:
- iso: eng
month: '09'
oa: 1
oa_version: Published Version
page: 1500-1513
pmid: 1
publication: Nature Plants
publication_identifier:
issn:
- 2055-0278
publication_status: published
publisher: Springer Nature
quality_controlled: '1'
status: public
title: Antigravitropic PIN polarization maintains non-vertical growth in lateral roots
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: 9
year: '2023'
...
---
_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. Current
Biology. 2021;31(9):1918-1930. doi:10.1016/j.cub.2021.02.028
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. Current Biology. Elsevier. https://doi.org/10.1016/j.cub.2021.02.028
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.” Current Biology.
Elsevier, 2021. https://doi.org/10.1016/j.cub.2021.02.028.
ieee: M. Glanc et al., “AGC kinases and MAB4/MEL proteins maintain PIN polarity
by limiting lateral diffusion in plant cells,” Current Biology, 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.” Current Biology, vol. 31,
no. 9, Elsevier, 2021, pp. 1918–30, doi:10.1016/j.cub.2021.02.028.
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.
date_created: 2021-03-26T12:09:33Z
date_published: 2021-03-10T00:00:00Z
date_updated: 2023-09-05T13:03:34Z
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'
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: '8721'
abstract:
- lang: eng
text: Spontaneously arising channels that transport the phytohormone auxin provide
positional cues for self-organizing aspects of plant development such as flexible
vasculature regeneration or its patterning during leaf venation. The auxin canalization
hypothesis proposes a feedback between auxin signaling and transport as the underlying
mechanism, but molecular players await discovery. We identified part of the machinery
that routes auxin transport. The auxin-regulated receptor CAMEL (Canalization-related
Auxin-regulated Malectin-type RLK) together with CANAR (Canalization-related Receptor-like
kinase) interact with and phosphorylate PIN auxin transporters. camel and canar
mutants are impaired in PIN1 subcellular trafficking and auxin-mediated PIN polarization,
which macroscopically manifests as defects in leaf venation and vasculature regeneration
after wounding. The CAMEL-CANAR receptor complex is part of the auxin feedback
that coordinates polarization of individual cells during auxin canalization.
acknowledged_ssus:
- _id: Bio
- _id: LifeSc
acknowledgement: 'We acknowledge M. Glanc and Y. Zhang for providing entryclones;
Vienna Biocenter Core Facilities (VBCF) for recombinantprotein production and purification;
Vienna Biocenter Massspectrometry Facility, Bioimaging, and Life Science Facilities
at IST Austria and Proteomics Core Facility CEITEC for a great assistance.Funding:This
project received funding from the European Research Council (ERC) under the European
Union’s Horizon 2020 research and innovation program (grant agreement 742985) and
Austrian Science Fund (FWF): I 3630-B25 to J.F.and by grants from the Austrian Academy
of Science through the Gregor Mendel Institute (Y.B.) and the Austrian Agency for
International Cooperation in Education and Research (D.D.); the Netherlands Organization
for Scientific Research (NWO; VIDI-864.13.001) (W.S.); the Research Foundation–Flanders
(FWO;Odysseus II G0D0515N) and a European Research Council grant (ERC; StG TORPEDO;
714055) to B.D.R., B.Y., and E.M.; and the Hertha Firnberg Programme postdoctoral
fellowship (T-947) from the FWF Austrian Science Fund to E.S.-L.; J.H. is the recipient
of a DOC Fellowship of the Austrian Academy of Sciences at IST Austria.'
article_processing_charge: No
article_type: original
author:
- first_name: Jakub
full_name: Hajny, Jakub
id: 4800CC20-F248-11E8-B48F-1D18A9856A87
last_name: Hajny
orcid: 0000-0003-2140-7195
- first_name: Tomas
full_name: Prat, Tomas
id: 3DA3BFEE-F248-11E8-B48F-1D18A9856A87
last_name: Prat
- first_name: N
full_name: Rydza, N
last_name: Rydza
- 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: Shutang
full_name: Tan, Shutang
id: 2DE75584-F248-11E8-B48F-1D18A9856A87
last_name: Tan
orcid: 0000-0002-0471-8285
- first_name: Inge
full_name: Verstraeten, Inge
id: 362BF7FE-F248-11E8-B48F-1D18A9856A87
last_name: Verstraeten
orcid: 0000-0001-7241-2328
- first_name: David
full_name: Domjan, David
id: C684CD7A-257E-11EA-9B6F-D8588B4F947F
last_name: Domjan
orcid: 0000-0003-2267-106X
- first_name: E
full_name: Mazur, E
last_name: Mazur
- first_name: E
full_name: Smakowska-Luzan, E
last_name: Smakowska-Luzan
- first_name: W
full_name: Smet, W
last_name: Smet
- first_name: E
full_name: Mor, E
last_name: Mor
- first_name: J
full_name: Nolf, J
last_name: Nolf
- first_name: B
full_name: Yang, B
last_name: Yang
- first_name: W
full_name: Grunewald, W
last_name: Grunewald
- first_name: Gergely
full_name: Molnar, Gergely
id: 34F1AF46-F248-11E8-B48F-1D18A9856A87
last_name: Molnar
- first_name: Y
full_name: Belkhadir, Y
last_name: Belkhadir
- first_name: B
full_name: De Rybel, B
last_name: De Rybel
- first_name: Jiří
full_name: Friml, Jiří
id: 4159519E-F248-11E8-B48F-1D18A9856A87
last_name: Friml
orcid: 0000-0002-8302-7596
citation:
ama: Hajny J, Prat T, Rydza N, et al. Receptor kinase module targets PIN-dependent
auxin transport during canalization. Science. 2020;370(6516):550-557. doi:10.1126/science.aba3178
apa: Hajny, J., Prat, T., Rydza, N., Rodriguez Solovey, L., Tan, S., Verstraeten,
I., … Friml, J. (2020). Receptor kinase module targets PIN-dependent auxin transport
during canalization. Science. American Association for the Advancement
of Science. https://doi.org/10.1126/science.aba3178
chicago: Hajny, Jakub, Tomas Prat, N Rydza, Lesia Rodriguez Solovey, Shutang Tan,
Inge Verstraeten, David Domjan, et al. “Receptor Kinase Module Targets PIN-Dependent
Auxin Transport during Canalization.” Science. American Association for
the Advancement of Science, 2020. https://doi.org/10.1126/science.aba3178.
ieee: J. Hajny et al., “Receptor kinase module targets PIN-dependent auxin
transport during canalization,” Science, vol. 370, no. 6516. American Association
for the Advancement of Science, pp. 550–557, 2020.
ista: Hajny J, Prat T, Rydza N, Rodriguez Solovey L, Tan S, Verstraeten I, Domjan
D, Mazur E, Smakowska-Luzan E, Smet W, Mor E, Nolf J, Yang B, Grunewald W, Molnar
G, Belkhadir Y, De Rybel B, Friml J. 2020. Receptor kinase module targets PIN-dependent
auxin transport during canalization. Science. 370(6516), 550–557.
mla: Hajny, Jakub, et al. “Receptor Kinase Module Targets PIN-Dependent Auxin Transport
during Canalization.” Science, vol. 370, no. 6516, American Association
for the Advancement of Science, 2020, pp. 550–57, doi:10.1126/science.aba3178.
short: J. Hajny, T. Prat, N. Rydza, L. Rodriguez Solovey, S. Tan, I. Verstraeten,
D. Domjan, E. Mazur, E. Smakowska-Luzan, W. Smet, E. Mor, J. Nolf, B. Yang, W.
Grunewald, G. Molnar, Y. Belkhadir, B. De Rybel, J. Friml, Science 370 (2020)
550–557.
date_created: 2020-11-02T10:04:46Z
date_published: 2020-10-30T00:00:00Z
date_updated: 2023-09-05T12:02:35Z
day: '30'
department:
- _id: JiFr
doi: 10.1126/science.aba3178
ec_funded: 1
external_id:
isi:
- '000583031800041'
pmid:
- '33122378'
intvolume: ' 370'
isi: 1
issue: '6516'
language:
- iso: eng
main_file_link:
- open_access: '1'
url: https://europepmc.org/article/MED/33122378#free-full-text
month: '10'
oa: 1
oa_version: Published Version
page: 550-557
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
- _id: 2699E3D2-B435-11E9-9278-68D0E5697425
grant_number: '25239'
name: Cell surface receptor complexes for PIN polarity and auxin-mediated development
publication: Science
publication_identifier:
eissn:
- 1095-9203
issn:
- 0036-8075
publication_status: published
publisher: American Association for the Advancement of Science
quality_controlled: '1'
related_material:
link:
- description: News on IST Homepage
relation: press_release
url: https://ist.ac.at/en/news/molecular-compass-for-cell-orientation/
scopus_import: '1'
status: public
title: Receptor kinase module targets PIN-dependent auxin transport during canalization
type: journal_article
user_id: c635000d-4b10-11ee-a964-aac5a93f6ac1
volume: 370
year: '2020'
...
---
_id: '7427'
abstract:
- lang: eng
text: Plants, like other multicellular organisms, survive through a delicate balance
between growth and defense against pathogens. Salicylic acid (SA) is a major defense
signal in plants, and the perception mechanism as well as downstream signaling
activating the immune response are known. Here, we identify a parallel SA signaling
that mediates growth attenuation. SA directly binds to A subunits of protein phosphatase
2A (PP2A), inhibiting activity of this complex. Among PP2A targets, the PIN2 auxin
transporter is hyperphosphorylated in response to SA, leading to changed activity
of this important growth regulator. Accordingly, auxin transport and auxin-mediated
root development, including growth, gravitropic response, and lateral root organogenesis,
are inhibited. This study reveals how SA, besides activating immunity, concomitantly
attenuates growth through crosstalk with the auxin distribution network. Further
analysis of this dual role of SA and characterization of additional SA-regulated
PP2A targets will provide further insights into mechanisms maintaining a balance
between growth and defense.
acknowledged_ssus:
- _id: Bio
- _id: LifeSc
acknowledgement: "We thank Shigeyuki Betsuyaku (University of Tsukuba), Alison Delong
(Brown University), Xinnian Dong (Duke University), Dolf Weijers (Wageningen University),
Yuelin Zhang (UBC), and Martine Pastuglia (Institut Jean-Pierre Bourgin) for sharing
published materials; Jana Riederer for help with cantharidin physiological analysis;
David Domjan for help with cloning pET28a-PIN2HL; Qing Lu for help with DARTS; Hana
Kozubı´kova´ for technical support on SA derivative synthesis; Zuzana Vondra´ kova´
for technical support with tobacco cells; Lucia Strader (Washington University),
Bert De Rybel (Ghent University), Bartel Vanholme (Ghent University), and Lukas
Mach (BOKU) for helpful discussions; and bioimaging and life science facilities
of IST Austria for continuous support. We gratefully acknowledge the Nottingham
Arabidopsis Stock Center (NASC) for providing T-DNA insertional mutants. The DSC
and SPR instruments were provided by the EQ-BOKU VIBT GmbH and the BOKU Core Facility
for Biomolecular and Cellular Analysis, with help of Irene Schaffner. The research
leading to these results has received funding from the European Union’s Horizon
2020 program (ERC grant agreement no. 742985 to J.F.) and the People Programme (Marie
Curie Actions) of the European Union’s Seventh Framework Programme (FP7/2007-2013)
under REA grant agreement no. 291734. S.T. was supported by a European Molecular
Biology Organization (EMBO) long-term postdoctoral fellowship (ALTF 723-2015). O.N.
was supported by the Ministry of Education, Youth and Sports of the Czech Republic
(European Regional Development Fund-Project ‘‘Centre for Experimental Plant Biology’’
no. CZ.02.1.01/0.0/0.0/16_019/0000738). J. Pospısil was supported by European Regional
Development Fund Project ‘‘Centre for Experimental Plant Biology’’\r\n(no. CZ.02.1.01/0.0/0.0/16_019/0000738).
J. Petrasek was supported by EU Operational Programme Prague-Competitiveness (no.
CZ.2.16/3.1.00/21519). "
article_processing_charge: No
article_type: original
author:
- first_name: Shutang
full_name: Tan, Shutang
id: 2DE75584-F248-11E8-B48F-1D18A9856A87
last_name: Tan
orcid: 0000-0002-0471-8285
- first_name: Melinda F
full_name: Abas, Melinda F
id: 3CFB3B1C-F248-11E8-B48F-1D18A9856A87
last_name: Abas
- first_name: Inge
full_name: Verstraeten, Inge
id: 362BF7FE-F248-11E8-B48F-1D18A9856A87
last_name: Verstraeten
orcid: 0000-0001-7241-2328
- first_name: Matous
full_name: Glanc, Matous
id: 1AE1EA24-02D0-11E9-9BAA-DAF4881429F2
last_name: Glanc
orcid: 0000-0003-0619-7783
- first_name: Gergely
full_name: Molnar, Gergely
id: 34F1AF46-F248-11E8-B48F-1D18A9856A87
last_name: Molnar
- first_name: Jakub
full_name: Hajny, Jakub
id: 4800CC20-F248-11E8-B48F-1D18A9856A87
last_name: Hajny
orcid: 0000-0003-2140-7195
- first_name: Pavel
full_name: Lasák, Pavel
last_name: Lasák
- first_name: Ivan
full_name: Petřík, Ivan
last_name: Petřík
- first_name: Eugenia
full_name: Russinova, Eugenia
last_name: Russinova
- first_name: Jan
full_name: Petrášek, Jan
last_name: Petrášek
- first_name: Ondřej
full_name: Novák, Ondřej
last_name: Novák
- first_name: Jiří
full_name: Pospíšil, Jiří
last_name: Pospíšil
- first_name: Jiří
full_name: Friml, Jiří
id: 4159519E-F248-11E8-B48F-1D18A9856A87
last_name: Friml
orcid: 0000-0002-8302-7596
citation:
ama: Tan S, Abas MF, Verstraeten I, et al. Salicylic acid targets protein phosphatase
2A to attenuate growth in plants. Current Biology. 2020;30(3):381-395.e8.
doi:10.1016/j.cub.2019.11.058
apa: Tan, S., Abas, M. F., Verstraeten, I., Glanc, M., Molnar, G., Hajny, J., …
Friml, J. (2020). Salicylic acid targets protein phosphatase 2A to attenuate growth
in plants. Current Biology. Cell Press. https://doi.org/10.1016/j.cub.2019.11.058
chicago: Tan, Shutang, Melinda F Abas, Inge Verstraeten, Matous Glanc, Gergely Molnar,
Jakub Hajny, Pavel Lasák, et al. “Salicylic Acid Targets Protein Phosphatase 2A
to Attenuate Growth in Plants.” Current Biology. Cell Press, 2020. https://doi.org/10.1016/j.cub.2019.11.058.
ieee: S. Tan et al., “Salicylic acid targets protein phosphatase 2A to attenuate
growth in plants,” Current Biology, vol. 30, no. 3. Cell Press, p. 381–395.e8,
2020.
ista: Tan S, Abas MF, Verstraeten I, Glanc M, Molnar G, Hajny J, Lasák P, Petřík
I, Russinova E, Petrášek J, Novák O, Pospíšil J, Friml J. 2020. Salicylic acid
targets protein phosphatase 2A to attenuate growth in plants. Current Biology.
30(3), 381–395.e8.
mla: Tan, Shutang, et al. “Salicylic Acid Targets Protein Phosphatase 2A to Attenuate
Growth in Plants.” Current Biology, vol. 30, no. 3, Cell Press, 2020, p.
381–395.e8, doi:10.1016/j.cub.2019.11.058.
short: S. Tan, M.F. Abas, I. Verstraeten, M. Glanc, G. Molnar, J. Hajny, P. Lasák,
I. Petřík, E. Russinova, J. Petrášek, O. Novák, J. Pospíšil, J. Friml, Current
Biology 30 (2020) 381–395.e8.
date_created: 2020-02-02T23:01:00Z
date_published: 2020-02-03T00:00:00Z
date_updated: 2024-03-25T23:30:20Z
day: '03'
ddc:
- '580'
department:
- _id: JiFr
- _id: EvBe
doi: 10.1016/j.cub.2019.11.058
ec_funded: 1
external_id:
isi:
- '000511287900018'
pmid:
- '31956021'
file:
- access_level: open_access
checksum: 16f7d51fe28f91c21e4896a2028df40b
content_type: application/pdf
creator: dernst
date_created: 2020-09-22T09:51:28Z
date_updated: 2020-09-22T09:51:28Z
file_id: '8555'
file_name: 2020_CurrentBiology_Tan.pdf
file_size: 5360135
relation: main_file
success: 1
file_date_updated: 2020-09-22T09:51:28Z
has_accepted_license: '1'
intvolume: ' 30'
isi: 1
issue: '3'
language:
- iso: eng
month: '02'
oa: 1
oa_version: Published Version
page: 381-395.e8
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: 25681D80-B435-11E9-9278-68D0E5697425
call_identifier: FP7
grant_number: '291734'
name: International IST Postdoc Fellowship Programme
- _id: 256FEF10-B435-11E9-9278-68D0E5697425
grant_number: 723-2015
name: Long Term Fellowship
publication: Current Biology
publication_identifier:
issn:
- '09609822'
publication_status: published
publisher: Cell Press
quality_controlled: '1'
related_material:
record:
- id: '8822'
relation: dissertation_contains
status: public
scopus_import: '1'
status: public
title: Salicylic acid targets protein phosphatase 2A to attenuate growth in plants
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: 30
year: '2020'
...
---
_id: '7600'
abstract:
- lang: eng
text: Directional intercellular transport of the phytohormone auxin mediated by
PIN FORMED (PIN) efflux carriers plays essential roles in both coordinating patterning
processes and integrating multiple external cues by rapidly redirecting auxin
fluxes. Multilevel regulations of PIN activity under internal and external cues
are complicated; however, the underlying molecular mechanism remains elusive.
Here we demonstrate that 3’-Phosphoinositide-Dependent Protein Kinase1 (PDK1),
which is conserved in plants and mammals, functions as a molecular hub integrating
the upstream lipid signalling and the downstream substrate activity through phosphorylation.
Genetic analysis uncovers that loss-of-function Arabidopsis mutant pdk1.1 pdk1.2
exhibits a plethora of abnormalities in organogenesis and growth, due to the defective
PIN-dependent auxin transport. Further cellular and biochemical analyses reveal
that PDK1 phosphorylates D6 Protein Kinase to facilitate its activity towards
PIN proteins. Our studies establish a lipid-dependent phosphorylation cascade
connecting membrane composition-based cellular signalling with plant growth and
patterning by regulating morphogenetic auxin fluxes.
acknowledged_ssus:
- _id: Bio
- _id: LifeSc
article_processing_charge: No
article_type: original
author:
- first_name: Shutang
full_name: Tan, Shutang
id: 2DE75584-F248-11E8-B48F-1D18A9856A87
last_name: Tan
orcid: 0000-0002-0471-8285
- first_name: Xixi
full_name: Zhang, Xixi
id: 61A66458-47E9-11EA-85BA-8AEAAF14E49A
last_name: Zhang
orcid: 0000-0001-7048-4627
- first_name: Wei
full_name: Kong, Wei
last_name: Kong
- first_name: Xiao-Li
full_name: Yang, Xiao-Li
last_name: Yang
- first_name: Gergely
full_name: Molnar, Gergely
id: 34F1AF46-F248-11E8-B48F-1D18A9856A87
last_name: Molnar
- first_name: Zuzana
full_name: Vondráková, Zuzana
last_name: Vondráková
- first_name: Roberta
full_name: Filepová, Roberta
last_name: Filepová
- first_name: Jan
full_name: Petrášek, Jan
last_name: Petrášek
- first_name: Jiří
full_name: Friml, Jiří
id: 4159519E-F248-11E8-B48F-1D18A9856A87
last_name: Friml
orcid: 0000-0002-8302-7596
- first_name: Hong-Wei
full_name: Xue, Hong-Wei
last_name: Xue
citation:
ama: Tan S, Zhang X, Kong W, et al. The lipid code-dependent phosphoswitch PDK1–D6PK
activates PIN-mediated auxin efflux in Arabidopsis. Nature Plants. 2020;6:556-569.
doi:10.1038/s41477-020-0648-9
apa: Tan, S., Zhang, X., Kong, W., Yang, X.-L., Molnar, G., Vondráková, Z., … Xue,
H.-W. (2020). The lipid code-dependent phosphoswitch PDK1–D6PK activates PIN-mediated
auxin efflux in Arabidopsis. Nature Plants. Springer Nature. https://doi.org/10.1038/s41477-020-0648-9
chicago: Tan, Shutang, Xixi Zhang, Wei Kong, Xiao-Li Yang, Gergely Molnar, Zuzana
Vondráková, Roberta Filepová, Jan Petrášek, Jiří Friml, and Hong-Wei Xue. “The
Lipid Code-Dependent Phosphoswitch PDK1–D6PK Activates PIN-Mediated Auxin Efflux
in Arabidopsis.” Nature Plants. Springer Nature, 2020. https://doi.org/10.1038/s41477-020-0648-9.
ieee: S. Tan et al., “The lipid code-dependent phosphoswitch PDK1–D6PK activates
PIN-mediated auxin efflux in Arabidopsis,” Nature Plants, vol. 6. Springer
Nature, pp. 556–569, 2020.
ista: Tan S, Zhang X, Kong W, Yang X-L, Molnar G, Vondráková Z, Filepová R, Petrášek
J, Friml J, Xue H-W. 2020. The lipid code-dependent phosphoswitch PDK1–D6PK activates
PIN-mediated auxin efflux in Arabidopsis. Nature Plants. 6, 556–569.
mla: Tan, Shutang, et al. “The Lipid Code-Dependent Phosphoswitch PDK1–D6PK Activates
PIN-Mediated Auxin Efflux in Arabidopsis.” Nature Plants, vol. 6, Springer
Nature, 2020, pp. 556–69, doi:10.1038/s41477-020-0648-9.
short: S. Tan, X. Zhang, W. Kong, X.-L. Yang, G. Molnar, Z. Vondráková, R. Filepová,
J. Petrášek, J. Friml, H.-W. Xue, Nature Plants 6 (2020) 556–569.
date_created: 2020-03-21T16:34:16Z
date_published: 2020-05-01T00:00:00Z
date_updated: 2023-08-18T07:05:57Z
day: '01'
department:
- _id: JiFr
doi: 10.1038/s41477-020-0648-9
ec_funded: 1
external_id:
isi:
- '000531787500006'
pmid:
- '32393881'
intvolume: ' 6'
isi: 1
language:
- iso: eng
main_file_link:
- open_access: '1'
url: https://doi.org/10.1101/755504
month: '05'
oa: 1
oa_version: Preprint
page: 556-569
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: 256FEF10-B435-11E9-9278-68D0E5697425
grant_number: 723-2015
name: Long Term Fellowship
publication: Nature Plants
publication_identifier:
eissn:
- '20550278'
publication_status: published
publisher: Springer Nature
quality_controlled: '1'
related_material:
link:
- relation: erratum
url: https://doi.org/10.1038/s41477-020-0719-y
scopus_import: '1'
status: public
title: The lipid code-dependent phosphoswitch PDK1–D6PK activates PIN-mediated auxin
efflux in Arabidopsis
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 6
year: '2020'
...
---
_id: '449'
abstract:
- lang: eng
text: Auxin is unique among plant hormones due to its directional transport that
is mediated by the polarly distributed PIN auxin transporters at the plasma membrane.
The canalization hypothesis proposes that the auxin feedback on its polar flow
is a crucial, plant-specific mechanism mediating multiple self-organizing developmental
processes. Here, we used the auxin effect on the PIN polar localization in Arabidopsis
thaliana roots as a proxy for the auxin feedback on the PIN polarity during canalization.
We performed microarray experiments to find regulators of this process that act
downstream of auxin. We identified genes that were transcriptionally regulated
by auxin in an AXR3/IAA17- and ARF7/ARF19-dependent manner. Besides the known
components of the PIN polarity, such as PID and PIP5K kinases, a number of potential
new regulators were detected, among which the WRKY23 transcription factor, which
was characterized in more detail. Gain- and loss-of-function mutants confirmed
a role for WRKY23 in mediating the auxin effect on the PIN polarity. Accordingly,
processes requiring auxin-mediated PIN polarity rearrangements, such as vascular
tissue development during leaf venation, showed a higher WRKY23 expression and
required the WRKY23 activity. Our results provide initial insights into the auxin
transcriptional network acting upstream of PIN polarization and, potentially,
canalization-mediated plant development.
article_processing_charge: Yes
author:
- first_name: Tomas
full_name: Prat, Tomas
id: 3DA3BFEE-F248-11E8-B48F-1D18A9856A87
last_name: Prat
- first_name: Jakub
full_name: Hajny, Jakub
id: 4800CC20-F248-11E8-B48F-1D18A9856A87
last_name: Hajny
orcid: 0000-0003-2140-7195
- first_name: Wim
full_name: Grunewald, Wim
last_name: Grunewald
- first_name: Mina K
full_name: Vasileva, Mina K
id: 3407EB18-F248-11E8-B48F-1D18A9856A87
last_name: Vasileva
- first_name: Gergely
full_name: Molnar, Gergely
id: 34F1AF46-F248-11E8-B48F-1D18A9856A87
last_name: Molnar
- first_name: Ricardo
full_name: Tejos, Ricardo
last_name: Tejos
- first_name: Markus
full_name: Schmid, Markus
last_name: Schmid
- first_name: Michael
full_name: Sauer, Michael
last_name: Sauer
- first_name: Jirí
full_name: Friml, Jirí
id: 4159519E-F248-11E8-B48F-1D18A9856A87
last_name: Friml
orcid: 0000-0002-8302-7596
citation:
ama: Prat T, Hajny J, Grunewald W, et al. WRKY23 is a component of the transcriptional
network mediating auxin feedback on PIN polarity. PLoS Genetics. 2018;14(1).
doi:10.1371/journal.pgen.1007177
apa: Prat, T., Hajny, J., Grunewald, W., Vasileva, M. K., Molnar, G., Tejos, R.,
… Friml, J. (2018). WRKY23 is a component of the transcriptional network mediating
auxin feedback on PIN polarity. PLoS Genetics. Public Library of Science.
https://doi.org/10.1371/journal.pgen.1007177
chicago: Prat, Tomas, Jakub Hajny, Wim Grunewald, Mina K Vasileva, Gergely Molnar,
Ricardo Tejos, Markus Schmid, Michael Sauer, and Jiří Friml. “WRKY23 Is a Component
of the Transcriptional Network Mediating Auxin Feedback on PIN Polarity.” PLoS
Genetics. Public Library of Science, 2018. https://doi.org/10.1371/journal.pgen.1007177.
ieee: T. Prat et al., “WRKY23 is a component of the transcriptional network
mediating auxin feedback on PIN polarity,” PLoS Genetics, vol. 14, no.
1. Public Library of Science, 2018.
ista: Prat T, Hajny J, Grunewald W, Vasileva MK, Molnar G, Tejos R, Schmid M, Sauer
M, Friml J. 2018. WRKY23 is a component of the transcriptional network mediating
auxin feedback on PIN polarity. PLoS Genetics. 14(1).
mla: Prat, Tomas, et al. “WRKY23 Is a Component of the Transcriptional Network Mediating
Auxin Feedback on PIN Polarity.” PLoS Genetics, vol. 14, no. 1, Public
Library of Science, 2018, doi:10.1371/journal.pgen.1007177.
short: T. Prat, J. Hajny, W. Grunewald, M.K. Vasileva, G. Molnar, R. Tejos, M. Schmid,
M. Sauer, J. Friml, PLoS Genetics 14 (2018).
date_created: 2018-12-11T11:46:32Z
date_published: 2018-01-29T00:00:00Z
date_updated: 2025-05-07T11:12:28Z
day: '29'
ddc:
- '581'
department:
- _id: JiFr
doi: 10.1371/journal.pgen.1007177
ec_funded: 1
external_id:
isi:
- '000423718600034'
file:
- access_level: open_access
checksum: 0276d66788ec076f4924164a39e6a712
content_type: application/pdf
creator: system
date_created: 2018-12-12T10:10:52Z
date_updated: 2020-07-14T12:46:30Z
file_id: '4843'
file_name: IST-2018-967-v1+1_journal.pgen.1007177.pdf
file_size: 24709062
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file_date_updated: 2020-07-14T12:46:30Z
has_accepted_license: '1'
intvolume: ' 14'
isi: 1
issue: '1'
language:
- iso: eng
month: '01'
oa: 1
oa_version: Published Version
project:
- _id: 25716A02-B435-11E9-9278-68D0E5697425
call_identifier: FP7
grant_number: '282300'
name: Polarity and subcellular dynamics in plants
publication: PLoS Genetics
publication_status: published
publisher: Public Library of Science
publist_id: '7373'
pubrep_id: '967'
quality_controlled: '1'
related_material:
record:
- id: '1127'
relation: dissertation_contains
status: public
- id: '7172'
relation: dissertation_contains
status: public
- id: '8822'
relation: dissertation_contains
status: public
scopus_import: '1'
status: public
title: WRKY23 is a component of the transcriptional network mediating auxin feedback
on PIN polarity
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: 14
year: '2018'
...
---
_id: '1345'
abstract:
- lang: eng
text: The electrostatic charge at the inner surface of the plasma membrane is strongly
negative in higher organisms. A new study shows that phosphatidylinositol-4-phosphate
plays a critical role in establishing plasma membrane surface charge in Arabidopsis,
which regulates the correct localization of signalling components.
article_number: '16102'
author:
- 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: Jirí
full_name: Friml, Jirí
id: 4159519E-F248-11E8-B48F-1D18A9856A87
last_name: Friml
orcid: 0000-0002-8302-7596
citation:
ama: 'Molnar G, Fendrych M, Friml J. Plasma membrane: Negative attraction. Nature
Plants. 2016;2. doi:10.1038/nplants.2016.102'
apa: 'Molnar, G., Fendrych, M., & Friml, J. (2016). Plasma membrane: Negative
attraction. Nature Plants. Nature Publishing Group. https://doi.org/10.1038/nplants.2016.102'
chicago: 'Molnar, Gergely, Matyas Fendrych, and Jiří Friml. “Plasma Membrane: Negative
Attraction.” Nature Plants. Nature Publishing Group, 2016. https://doi.org/10.1038/nplants.2016.102.'
ieee: 'G. Molnar, M. Fendrych, and J. Friml, “Plasma membrane: Negative attraction,”
Nature Plants, vol. 2. Nature Publishing Group, 2016.'
ista: 'Molnar G, Fendrych M, Friml J. 2016. Plasma membrane: Negative attraction.
Nature Plants. 2, 16102.'
mla: 'Molnar, Gergely, et al. “Plasma Membrane: Negative Attraction.” Nature
Plants, vol. 2, 16102, Nature Publishing Group, 2016, doi:10.1038/nplants.2016.102.'
short: G. Molnar, M. Fendrych, J. Friml, Nature Plants 2 (2016).
date_created: 2018-12-11T11:51:30Z
date_published: 2016-07-01T00:00:00Z
date_updated: 2021-01-12T06:50:02Z
day: '01'
ddc:
- '581'
department:
- _id: JiFr
doi: 10.1038/nplants.2016.102
file:
- access_level: open_access
checksum: 9ba65f558563b287f875f48fa9f30fb2
content_type: application/pdf
creator: system
date_created: 2018-12-12T10:12:36Z
date_updated: 2020-07-14T12:44:45Z
file_id: '4954'
file_name: IST-2018-1007-v1+1_Molnar_NatPlants_2016.pdf
file_size: 127781
relation: main_file
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checksum: 550d252be808d8ca2b43e83dddb4212f
content_type: application/pdf
creator: system
date_created: 2018-12-12T10:12:37Z
date_updated: 2020-07-14T12:44:45Z
file_id: '4955'
file_name: IST-2018-1007-v1+2_Molnar_NatPlants_2016_editor_statement.pdf
file_size: 430556
relation: main_file
file_date_updated: 2020-07-14T12:44:45Z
has_accepted_license: '1'
intvolume: ' 2'
language:
- iso: eng
month: '07'
oa: 1
oa_version: Published Version
publication: Nature Plants
publication_status: published
publisher: Nature Publishing Group
publist_id: '5907'
pubrep_id: '1007'
quality_controlled: '1'
scopus_import: 1
status: public
title: 'Plasma membrane: Negative attraction'
type: journal_article
user_id: 3E5EF7F0-F248-11E8-B48F-1D18A9856A87
volume: 2
year: '2016'
...