---
_id: '11723'
abstract:
- lang: eng
text: Plant cell growth responds rapidly to various stimuli, adapting architecture
to environmental changes. Two major endogenous signals regulating growth are the
phytohormone auxin and the secreted peptides rapid alkalinization factors (RALFs).
Both trigger very rapid cellular responses and also exert long-term effects [Du
et al., Annu. Rev. Plant Biol. 71, 379–402 (2020); Blackburn et al., Plant Physiol.
182, 1657–1666 (2020)]. However, the way, in which these distinct signaling pathways
converge to regulate growth, remains unknown. Here, using vertical confocal microscopy
combined with a microfluidic chip, we addressed the mechanism of RALF action on
growth. We observed correlation between RALF1-induced rapid Arabidopsis thaliana
root growth inhibition and apoplast alkalinization during the initial phase of
the response, and revealed that RALF1 reversibly inhibits primary root growth
through apoplast alkalinization faster than within 1 min. This rapid apoplast
alkalinization was the result of RALF1-induced net H+ influx and was mediated
by the receptor FERONIA (FER). Furthermore, we investigated the cross-talk between
RALF1 and the auxin signaling pathways during root growth regulation. The results
showed that RALF-FER signaling triggered auxin signaling with a delay of approximately
1 h by up-regulating auxin biosynthesis, thus contributing to sustained RALF1-induced
growth inhibition. This biphasic RALF1 action on growth allows plants to respond
rapidly to environmental stimuli and also reprogram growth and development in
the long term.
acknowledgement: We thank Sarah M. Assmann, Kris Vissenberg, and Nadine Paris for
kindly sharing seeds; Matyáš Fendrych for initiating this project and providing
constant support; Lukas Fiedler for revising the manuscript; and Huibin Han and
Arseny Savin for contributing to genotyping. This work was supported by the Austrian
Science Fund (FWF) I 3630-B25 (to J.F.) and the Doctoral Fellowship Progrmme of
the Austrian Academy of Sciences (to L.L.) We also acknowledge Taif University Researchers
Supporting Project TURSP-HC2021/02 and funding “Plants as a tool for sustainable
global development (no. CZ.02.1.01/0.0/0.0/16_019/0000827).”
article_number: e2121058119
article_processing_charge: No
article_type: original
author:
- first_name: Lanxin
full_name: Li, Lanxin
id: 367EF8FA-F248-11E8-B48F-1D18A9856A87
last_name: Li
orcid: 0000-0002-5607-272X
- first_name: Huihuang
full_name: Chen, Huihuang
id: 83c96512-15b2-11ec-abd3-b7eede36184f
last_name: Chen
- first_name: Saqer S.
full_name: Alotaibi, Saqer S.
last_name: Alotaibi
- first_name: Aleš
full_name: Pěnčík, Aleš
last_name: Pěnčík
- first_name: Maciek
full_name: Adamowski, Maciek
id: 45F536D2-F248-11E8-B48F-1D18A9856A87
last_name: Adamowski
orcid: 0000-0001-6463-5257
- first_name: Ondřej
full_name: Novák, Ondřej
last_name: Novák
- first_name: Jiří
full_name: Friml, Jiří
id: 4159519E-F248-11E8-B48F-1D18A9856A87
last_name: Friml
orcid: 0000-0002-8302-7596
citation:
ama: Li L, Chen H, Alotaibi SS, et al. RALF1 peptide triggers biphasic root growth
inhibition upstream of auxin biosynthesis. Proceedings of the National Academy
of Sciences. 2022;119(31). doi:10.1073/pnas.2121058119
apa: Li, L., Chen, H., Alotaibi, S. S., Pěnčík, A., Adamowski, M., Novák, O., &
Friml, J. (2022). RALF1 peptide triggers biphasic root growth inhibition upstream
of auxin biosynthesis. Proceedings of the National Academy of Sciences.
Proceedings of the National Academy of Sciences. https://doi.org/10.1073/pnas.2121058119
chicago: Li, Lanxin, Huihuang Chen, Saqer S. Alotaibi, Aleš Pěnčík, Maciek Adamowski,
Ondřej Novák, and Jiří Friml. “RALF1 Peptide Triggers Biphasic Root Growth Inhibition
Upstream of Auxin Biosynthesis.” Proceedings of the National Academy of Sciences.
Proceedings of the National Academy of Sciences, 2022. https://doi.org/10.1073/pnas.2121058119.
ieee: L. Li et al., “RALF1 peptide triggers biphasic root growth inhibition
upstream of auxin biosynthesis,” Proceedings of the National Academy of Sciences,
vol. 119, no. 31. Proceedings of the National Academy of Sciences, 2022.
ista: Li L, Chen H, Alotaibi SS, Pěnčík A, Adamowski M, Novák O, Friml J. 2022.
RALF1 peptide triggers biphasic root growth inhibition upstream of auxin biosynthesis.
Proceedings of the National Academy of Sciences. 119(31), e2121058119.
mla: Li, Lanxin, et al. “RALF1 Peptide Triggers Biphasic Root Growth Inhibition
Upstream of Auxin Biosynthesis.” Proceedings of the National Academy of Sciences,
vol. 119, no. 31, e2121058119, Proceedings of the National Academy of Sciences,
2022, doi:10.1073/pnas.2121058119.
short: L. Li, H. Chen, S.S. Alotaibi, A. Pěnčík, M. Adamowski, O. Novák, J. Friml,
Proceedings of the National Academy of Sciences 119 (2022).
date_created: 2022-08-04T20:06:49Z
date_published: 2022-07-25T00:00:00Z
date_updated: 2024-10-29T10:12:30Z
day: '25'
ddc:
- '580'
department:
- _id: GradSch
- _id: JiFr
doi: 10.1073/pnas.2121058119
external_id:
isi:
- '000881496900002'
pmid:
- '35878023'
file:
- access_level: open_access
checksum: ae6f19b0d9efba6687f9e4dc1bab1d6e
content_type: application/pdf
creator: dernst
date_created: 2022-08-08T07:42:09Z
date_updated: 2022-08-08T07:42:09Z
file_id: '11747'
file_name: 2022_PNAS_Li.pdf
file_size: 2506262
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success: 1
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intvolume: ' 119'
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issue: '31'
keyword:
- Multidisciplinary
language:
- iso: eng
license: https://creativecommons.org/licenses/by-nc-nd/4.0/
month: '07'
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
- _id: 26B4D67E-B435-11E9-9278-68D0E5697425
grant_number: '25351'
name: 'A Case Study of Plant Growth Regulation: Molecular Mechanism of Auxin-mediated
Rapid Growth Inhibition in Arabidopsis Root'
publication: Proceedings of the National Academy of Sciences
publication_identifier:
eissn:
- 1091-6490
issn:
- 0027-8424
publication_status: published
publisher: Proceedings of the National Academy of Sciences
quality_controlled: '1'
scopus_import: '1'
status: public
title: RALF1 peptide triggers biphasic root growth inhibition upstream of auxin biosynthesis
tmp:
image: /images/cc_by_nc_nd.png
legal_code_url: https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode
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: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 119
year: '2022'
...
---
_id: '10411'
abstract:
- lang: eng
text: The phytohormone auxin is the major growth regulator governing tropic responses
including gravitropism. Auxin build-up at the lower side of stimulated shoots
promotes cell expansion, whereas in roots it inhibits growth, leading to upward
shoot bending and downward root bending, respectively. Yet it remains an enigma
how the same signal can trigger such opposite cellular responses. In this review,
we discuss several recent unexpected insights into the mechanisms underlying auxin
regulation of growth, challenging several existing models. We focus on the divergent
mechanisms of apoplastic pH regulation in shoots and roots revisiting the classical
Acid Growth Theory and discuss coordinated involvement of multiple auxin signaling
pathways. From this emerges a more comprehensive, updated picture how auxin regulates
growth.
acknowledgement: The authors thank Alexandra Mally for editing the text. This work
was supported by the Austrian Science Fund (FWF) I 3630-B25 to Jiří Friml and the
DOC Fellowship of the Austrian Academy of Sciences to Lanxin Li. All figures were
created with BioRender.com.
article_processing_charge: No
article_type: original
author:
- first_name: Lanxin
full_name: Li, Lanxin
id: 367EF8FA-F248-11E8-B48F-1D18A9856A87
last_name: Li
orcid: 0000-0002-5607-272X
- first_name: Michelle C
full_name: Gallei, Michelle C
id: 35A03822-F248-11E8-B48F-1D18A9856A87
last_name: Gallei
orcid: 0000-0003-1286-7368
- first_name: Jiří
full_name: Friml, Jiří
id: 4159519E-F248-11E8-B48F-1D18A9856A87
last_name: Friml
orcid: 0000-0002-8302-7596
citation:
ama: 'Li L, Gallei MC, Friml J. Bending to auxin: Fast acid growth for tropisms.
Trends in Plant Science. 2022;27(5):440-449. doi:10.1016/j.tplants.2021.11.006'
apa: 'Li, L., Gallei, M. C., & Friml, J. (2022). Bending to auxin: Fast acid
growth for tropisms. Trends in Plant Science. Cell Press. https://doi.org/10.1016/j.tplants.2021.11.006'
chicago: 'Li, Lanxin, Michelle C Gallei, and Jiří Friml. “Bending to Auxin: Fast
Acid Growth for Tropisms.” Trends in Plant Science. Cell Press, 2022. https://doi.org/10.1016/j.tplants.2021.11.006.'
ieee: 'L. Li, M. C. Gallei, and J. Friml, “Bending to auxin: Fast acid growth for
tropisms,” Trends in Plant Science, vol. 27, no. 5. Cell Press, pp. 440–449,
2022.'
ista: 'Li L, Gallei MC, Friml J. 2022. Bending to auxin: Fast acid growth for tropisms.
Trends in Plant Science. 27(5), 440–449.'
mla: 'Li, Lanxin, et al. “Bending to Auxin: Fast Acid Growth for Tropisms.” Trends
in Plant Science, vol. 27, no. 5, Cell Press, 2022, pp. 440–49, doi:10.1016/j.tplants.2021.11.006.'
short: L. Li, M.C. Gallei, J. Friml, Trends in Plant Science 27 (2022) 440–449.
date_created: 2021-12-05T23:01:43Z
date_published: 2022-05-01T00:00:00Z
date_updated: 2024-10-29T10:12:33Z
day: '01'
ddc:
- '580'
department:
- _id: JiFr
doi: 10.1016/j.tplants.2021.11.006
external_id:
isi:
- '000793707900005'
pmid:
- '34848141'
file:
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checksum: 3d94980ee1ff6bec100dd813f6a921a6
content_type: application/pdf
creator: amally
date_created: 2023-11-02T17:00:03Z
date_updated: 2023-11-02T17:00:03Z
file_id: '14480'
file_name: Li Plants 2021_accepted.pdf
file_size: 805779
relation: main_file
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file_date_updated: 2023-11-02T17:00:03Z
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intvolume: ' 27'
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month: '05'
oa: 1
oa_version: Submitted Version
page: 440-449
pmid: 1
project:
- _id: 26538374-B435-11E9-9278-68D0E5697425
call_identifier: FWF
grant_number: I03630
name: Molecular mechanisms of endocytic cargo recognition in plants
- _id: 26B4D67E-B435-11E9-9278-68D0E5697425
grant_number: '25351'
name: 'A Case Study of Plant Growth Regulation: Molecular Mechanism of Auxin-mediated
Rapid Growth Inhibition in Arabidopsis Root'
publication: Trends in Plant Science
publication_identifier:
issn:
- 1360-1385
publication_status: published
publisher: Cell Press
quality_controlled: '1'
related_material:
record:
- id: '11626'
relation: dissertation_contains
status: public
scopus_import: '1'
status: public
title: 'Bending to auxin: Fast acid growth for tropisms'
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 27
year: '2022'
...
---
_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:
- first_name: Zuzana
full_name: Gelová, Zuzana
id: 0AE74790-0E0B-11E9-ABC7-1ACFE5697425
last_name: Gelová
orcid: 0000-0003-4783-1752
- first_name: Michelle C
full_name: Gallei, Michelle C
id: 35A03822-F248-11E8-B48F-1D18A9856A87
last_name: Gallei
orcid: 0000-0003-1286-7368
- first_name: Markéta
full_name: Pernisová, Markéta
last_name: Pernisová
- first_name: Géraldine
full_name: Brunoud, Géraldine
last_name: Brunoud
- first_name: Xixi
full_name: Zhang, Xixi
id: 61A66458-47E9-11EA-85BA-8AEAAF14E49A
last_name: Zhang
orcid: 0000-0001-7048-4627
- first_name: Matous
full_name: Glanc, Matous
id: 1AE1EA24-02D0-11E9-9BAA-DAF4881429F2
last_name: Glanc
orcid: 0000-0003-0619-7783
- first_name: Lanxin
full_name: Li, Lanxin
id: 367EF8FA-F248-11E8-B48F-1D18A9856A87
last_name: Li
orcid: 0000-0002-5607-272X
- first_name: Jaroslav
full_name: Michalko, Jaroslav
id: 483727CA-F248-11E8-B48F-1D18A9856A87
last_name: Michalko
- first_name: Zlata
full_name: Pavlovicova, Zlata
last_name: Pavlovicova
- first_name: Inge
full_name: Verstraeten, Inge
id: 362BF7FE-F248-11E8-B48F-1D18A9856A87
last_name: Verstraeten
orcid: 0000-0001-7241-2328
- first_name: Huibin
full_name: Han, Huibin
id: 31435098-F248-11E8-B48F-1D18A9856A87
last_name: Han
- first_name: Jakub
full_name: Hajny, Jakub
id: 4800CC20-F248-11E8-B48F-1D18A9856A87
last_name: Hajny
orcid: 0000-0003-2140-7195
- first_name: Robert
full_name: Hauschild, Robert
id: 4E01D6B4-F248-11E8-B48F-1D18A9856A87
last_name: Hauschild
orcid: 0000-0001-9843-3522
- first_name: Milada
full_name: Čovanová, Milada
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
last_name: Hörmayer
orcid: 0000-0001-8295-2926
- first_name: Matyas
full_name: Fendrych, Matyas
id: 43905548-F248-11E8-B48F-1D18A9856A87
last_name: Fendrych
orcid: 0000-0002-9767-8699
- first_name: Tongda
full_name: Xu, Tongda
last_name: Xu
- first_name: Teva
full_name: Vernoux, Teva
last_name: Vernoux
- first_name: Jiří
full_name: Friml, Jiří
id: 4159519E-F248-11E8-B48F-1D18A9856A87
last_name: Friml
orcid: 0000-0002-8302-7596
citation:
ama: Gelová Z, Gallei MC, Pernisová M, et al. Developmental roles of auxin binding
protein 1 in Arabidopsis thaliana. Plant Science. 2021;303. doi:10.1016/j.plantsci.2020.110750
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. Plant Science. Elsevier. https://doi.org/10.1016/j.plantsci.2020.110750
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.” Plant Science. Elsevier, 2021. https://doi.org/10.1016/j.plantsci.2020.110750.
ieee: Z. Gelová et al., “Developmental roles of auxin binding protein 1 in
Arabidopsis thaliana,” Plant Science, 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.” Plant Science, vol. 303, 110750, Elsevier, 2021, doi:10.1016/j.plantsci.2020.110750.
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).
date_created: 2020-12-09T14:48:28Z
date_published: 2021-02-01T00:00:00Z
date_updated: 2024-10-29T10:22:43Z
day: '01'
ddc:
- '580'
department:
- _id: JiFr
- _id: Bio
doi: 10.1016/j.plantsci.2020.110750
ec_funded: 1
external_id:
isi:
- '000614154500001'
pmid:
- '33487339'
file:
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checksum: a7f2562bdca62d67dfa88e271b62a629
content_type: application/pdf
creator: dernst
date_created: 2021-02-04T07:49:25Z
date_updated: 2021-02-04T07:49:25Z
file_id: '9083'
file_name: 2021_PlantScience_Gelova.pdf
file_size: 12563728
relation: main_file
success: 1
file_date_updated: 2021-02-04T07:49:25Z
has_accepted_license: '1'
intvolume: ' 303'
isi: 1
keyword:
- Agronomy and Crop Science
- Plant Science
- Genetics
- General Medicine
language:
- iso: eng
license: https://creativecommons.org/licenses/by/4.0/
month: '02'
oa: 1
oa_version: Published Version
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: 26B4D67E-B435-11E9-9278-68D0E5697425
grant_number: '25351'
name: 'A Case Study of Plant Growth Regulation: Molecular Mechanism of Auxin-mediated
Rapid Growth Inhibition in Arabidopsis Root'
publication: Plant Science
publication_identifier:
issn:
- 0168-9452
publication_status: published
publisher: Elsevier
quality_controlled: '1'
related_material:
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- id: '11626'
relation: dissertation_contains
status: public
- id: '10083'
relation: dissertation_contains
status: public
scopus_import: '1'
status: public
title: Developmental roles of auxin binding protein 1 in Arabidopsis thaliana
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: 303
year: '2021'
...
---
_id: '10083'
abstract:
- lang: eng
text: "Plant motions occur across a wide spectrum of timescales, ranging from seed
dispersal through bursting (milliseconds) and stomatal opening (minutes) to long-term
adaptation of gross architecture. Relatively fast motions include water-driven
growth as exemplified by root cell expansion under abiotic/biotic stresses or
during gravitropism. A showcase is a root growth inhibition in 30 seconds triggered
by the phytohormone auxin. However, the cellular and molecular mechanisms are
still largely unknown. This thesis covers the studies about this topic as follows.
By taking advantage of microfluidics combined with live imaging, pharmaceutical
tools, and transgenic lines, we examined the kinetics of and causal relationship
among various auxininduced rapid cellular changes in root growth, apoplastic pH,
cytosolic Ca2+, cortical microtubule (CMT) orientation, and vacuolar morphology.
We revealed that CMT reorientation and vacuolar constriction are the consequence
of growth itself instead of responding directly to auxin. In contrast, auxin induces
apoplast alkalinization to rapidly inhibit root growth in 30 seconds. This auxin-triggered
apoplast alkalinization results from rapid H+- influx that is contributed by Ca2+
inward channel CYCLIC NUCLEOTIDE-GATED CHANNEL 14 (CNGC14)-dependent Ca2+ signaling.
To dissect which auxin signaling mediates the rapid apoplast alkalinization, we\r\ncombined
microfluidics and genetic engineering to verify that TIR1/AFB receptors conduct
a non-transcriptional regulation on Ca2+ and H+ -influx. This non-canonical pathway
is mostly mediated by the cytosolic portion of TIR1/AFB. On the other hand, we
uncovered, using biochemical and phospho-proteomic analysis, that auxin cell surface
signaling component TRANSMEMBRANE KINASE 1 (TMK1) plays a negative role during
auxin-trigger apoplast\r\nalkalinization and root growth inhibition through directly
activating PM H+ -ATPases. Therefore, we discovered that PM H+ -ATPases counteract
instead of mediate the auxintriggered rapid H+ -influx, and that TIR1/AFB and
TMK1 regulate root growth antagonistically. This opposite effect of TIR1/AFB and
TMK1 is consistent during auxin-induced hypocotyl elongation, leading us to explore
the relation of two signaling pathways. Assisted with biochemistry and fluorescent
imaging, we verified for the first time that TIR1/AFB and TMK1 can interact with
each other. The ability of TIR1/AFB binding to membrane lipid provides a basis
for the interaction of plasma membrane- and cytosol-localized proteins.\r\nBesides,
transgenic analysis combined with genetic engineering and biochemistry showed
that vi\r\nthey do function in the same pathway. Particularly, auxin-induced
TMK1 increase is TIR1/AFB dependent, suggesting TIR1/AFB regulation on TMK1. Conversely,
TMK1 also regulates TIR1/AFB protein levels and thus auxin canonical signaling.
To follow the study of rapid growth regulation, we analyzed another rapid growth
regulator, signaling peptide RALF1. We showed that RALF1 also triggers a rapid
and reversible growth inhibition caused by H + influx, highly resembling but not
dependent on auxin. Besides, RALF1 promotes auxin biosynthesis by increasing expression
of auxin biosynthesis enzyme YUCCAs and thus induces auxin signaling in ca. 1
hour, contributing to the sustained RALF1-triggered growth inhibition. These studies
collectively contribute to understanding rapid regulation on plant cell\r\ngrowth,
novel auxin signaling pathway as well as auxin-peptide crosstalk. "
alternative_title:
- ISTA Thesis
article_processing_charge: No
author:
- first_name: Lanxin
full_name: Li, Lanxin
last_name: Li
citation:
ama: Li L. Rapid cell growth regulation in Arabidopsis. 2021. doi:10.15479/at:ista:10083
apa: Li, L. (2021). Rapid cell growth regulation in Arabidopsis. Institute
of Science and Technology Austria. https://doi.org/10.15479/at:ista:10083
chicago: Li, Lanxin. “Rapid Cell Growth Regulation in Arabidopsis.” Institute of
Science and Technology Austria, 2021. https://doi.org/10.15479/at:ista:10083.
ieee: L. Li, “Rapid cell growth regulation in Arabidopsis,” Institute of Science
and Technology Austria, 2021.
ista: Li L. 2021. Rapid cell growth regulation in Arabidopsis. Institute of Science
and Technology Austria.
mla: Li, Lanxin. Rapid Cell Growth Regulation in Arabidopsis. Institute of
Science and Technology Austria, 2021, doi:10.15479/at:ista:10083.
short: L. Li, Rapid Cell Growth Regulation in Arabidopsis, Institute of Science
and Technology Austria, 2021.
date_created: 2021-10-04T13:33:10Z
date_published: 2021-10-06T00:00:00Z
date_updated: 2025-05-07T11:12:33Z
day: '06'
ddc:
- '575'
degree_awarded: PhD
department:
- _id: GradSch
- _id: JiFr
doi: 10.15479/at:ista:10083
ec_funded: 1
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file_id: '10139'
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file_date_updated: 2022-12-20T23:30:03Z
has_accepted_license: '1'
language:
- iso: eng
month: '10'
oa: 1
oa_version: Published Version
project:
- _id: 2564DBCA-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '665385'
name: International IST Doctoral Program
- _id: 26B4D67E-B435-11E9-9278-68D0E5697425
grant_number: '25351'
name: 'A Case Study of Plant Growth Regulation: Molecular Mechanism of Auxin-mediated
Rapid Growth Inhibition in Arabidopsis Root'
publication_identifier:
issn:
- 2663-337X
publication_status: published
publisher: Institute of Science and Technology Austria
related_material:
record:
- id: '442'
relation: part_of_dissertation
status: public
- id: '8931'
relation: part_of_dissertation
status: public
- id: '9287'
relation: part_of_dissertation
status: public
- id: '8283'
relation: part_of_dissertation
status: public
- id: '8986'
relation: part_of_dissertation
status: public
- id: '10015'
relation: part_of_dissertation
status: public
- id: '10095'
relation: part_of_dissertation
status: public
- id: '6627'
relation: part_of_dissertation
status: public
status: public
supervisor:
- first_name: Jiří
full_name: Friml, Jiří
id: 4159519E-F248-11E8-B48F-1D18A9856A87
last_name: Friml
orcid: 0000-0002-8302-7596
title: Rapid cell growth regulation in Arabidopsis
tmp:
image: /images/cc_by_nc_nd.png
legal_code_url: https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode
name: Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International
(CC BY-NC-ND 4.0)
short: CC BY-NC-ND (4.0)
type: dissertation
user_id: c635000d-4b10-11ee-a964-aac5a93f6ac1
year: '2021'
...
---
_id: '10095'
abstract:
- lang: eng
text: Growth regulation tailors plant development to its environment. A showcase
is response to gravity, where shoots bend up and roots down1. This paradox is
based on opposite effects of the phytohormone auxin, which promotes cell expansion
in shoots, while inhibiting it in roots via a yet unknown cellular mechanism2.
Here, by combining microfluidics, live imaging, genetic engineering and phospho-proteomics
in Arabidopsis thaliana, we advance our understanding how auxin inhibits root
growth. We show that auxin activates two distinct, antagonistically acting signalling
pathways that converge on the rapid regulation of the apoplastic pH, a causative
growth determinant. Cell surface-based TRANSMEMBRANE KINASE1 (TMK1) interacts
with and mediates phosphorylation and activation of plasma membrane H+-ATPases
for apoplast acidification, while intracellular canonical auxin signalling promotes
net cellular H+-influx, causing apoplast alkalinisation. The simultaneous activation
of these two counteracting mechanisms poises the root for a rapid, fine-tuned
growth modulation while navigating complex soil environment.
acknowledged_ssus:
- _id: LifeSc
- _id: M-Shop
- _id: Bio
acknowledgement: We thank Nataliia Gnyliukh and Lukas Hörmayer for technical assistance
and Nadine Paris for sharing PM-Cyto seeds. We gratefully acknowledge Life Science,
Machine Shop and Bioimaging Facilities of IST Austria. This project has received
funding from the European Research Council Advanced Grant (ETAP-742985) and the
Austrian Science Fund (FWF) I 3630-B25 to J.F., the National Institutes of Health
(GM067203) to W.M.G., the Netherlands Organization for Scientific Research (NWO;
VIDI-864.13.001.), the Research Foundation-Flanders (FWO; Odysseus II G0D0515N)
and a European Research Council Starting Grant (TORPEDO-714055) to W.S. and B.D.R.,
the VICI grant (865.14.001) from the Netherlands Organization for Scientific Research
to M.R and D.W., the Australian Research Council and China National Distinguished
Expert Project (WQ20174400441) to S.S., the MEXT/JSPS KAKENHI to K.T. (20K06685)
and T.K. (20H05687 and 20H05910), the European Union’s Horizon 2020 research and
innovation programme under the Marie Skłodowska-Curie Grant Agreement No. 665385
and the DOC Fellowship of the Austrian Academy of Sciences to L.L., the China Scholarship
Council to J.C.
article_number: '266395'
article_processing_charge: No
author:
- first_name: Lanxin
full_name: Li, Lanxin
id: 367EF8FA-F248-11E8-B48F-1D18A9856A87
last_name: Li
orcid: 0000-0002-5607-272X
- first_name: Inge
full_name: Verstraeten, Inge
id: 362BF7FE-F248-11E8-B48F-1D18A9856A87
last_name: Verstraeten
orcid: 0000-0001-7241-2328
- first_name: Mark
full_name: Roosjen, Mark
last_name: Roosjen
- first_name: Koji
full_name: Takahashi, Koji
last_name: Takahashi
- 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: Jack
full_name: Merrin, Jack
id: 4515C308-F248-11E8-B48F-1D18A9856A87
last_name: Merrin
orcid: 0000-0001-5145-4609
- first_name: Jian
full_name: Chen, Jian
last_name: Chen
- first_name: Lana
full_name: Shabala, Lana
last_name: Shabala
- first_name: Wouter
full_name: Smet, Wouter
last_name: Smet
- first_name: Hong
full_name: Ren, Hong
last_name: Ren
- first_name: Steffen
full_name: Vanneste, Steffen
last_name: Vanneste
- first_name: Sergey
full_name: Shabala, Sergey
last_name: Shabala
- first_name: Bert
full_name: De Rybel, Bert
last_name: De Rybel
- first_name: Dolf
full_name: Weijers, Dolf
last_name: Weijers
- first_name: Toshinori
full_name: Kinoshita, Toshinori
last_name: Kinoshita
- first_name: William M.
full_name: Gray, William M.
last_name: Gray
- first_name: Jiří
full_name: Friml, Jiří
id: 4159519E-F248-11E8-B48F-1D18A9856A87
last_name: Friml
orcid: 0000-0002-8302-7596
citation:
ama: Li L, Verstraeten I, Roosjen M, et al. Cell surface and intracellular auxin
signalling for H+-fluxes in root growth. Research Square. doi:10.21203/rs.3.rs-266395/v3
apa: Li, L., Verstraeten, I., Roosjen, M., Takahashi, K., Rodriguez Solovey, L.,
Merrin, J., … Friml, J. (n.d.). Cell surface and intracellular auxin signalling
for H+-fluxes in root growth. Research Square. https://doi.org/10.21203/rs.3.rs-266395/v3
chicago: Li, Lanxin, Inge Verstraeten, Mark Roosjen, Koji Takahashi, Lesia Rodriguez
Solovey, Jack Merrin, Jian Chen, et al. “Cell Surface and Intracellular Auxin
Signalling for H+-Fluxes in Root Growth.” Research Square, n.d. https://doi.org/10.21203/rs.3.rs-266395/v3.
ieee: L. Li et al., “Cell surface and intracellular auxin signalling for
H+-fluxes in root growth,” Research Square. .
ista: Li L, Verstraeten I, Roosjen M, Takahashi K, Rodriguez Solovey L, Merrin J,
Chen J, Shabala L, Smet W, Ren H, Vanneste S, Shabala S, De Rybel B, Weijers D,
Kinoshita T, Gray WM, Friml J. Cell surface and intracellular auxin signalling
for H+-fluxes in root growth. Research Square, 266395.
mla: Li, Lanxin, et al. “Cell Surface and Intracellular Auxin Signalling for H+-Fluxes
in Root Growth.” Research Square, 266395, doi:10.21203/rs.3.rs-266395/v3.
short: L. Li, I. Verstraeten, M. Roosjen, K. Takahashi, L. Rodriguez Solovey, J.
Merrin, J. Chen, L. Shabala, W. Smet, H. Ren, S. Vanneste, S. Shabala, B. De Rybel,
D. Weijers, T. Kinoshita, W.M. Gray, J. Friml, Research Square (n.d.).
date_created: 2021-10-06T08:56:22Z
date_published: 2021-09-09T00:00:00Z
date_updated: 2024-10-29T10:22:44Z
day: '09'
department:
- _id: JiFr
- _id: NanoFab
doi: 10.21203/rs.3.rs-266395/v3
ec_funded: 1
language:
- iso: eng
main_file_link:
- open_access: '1'
url: https://www.doi.org/10.21203/rs.3.rs-266395/v3
month: '09'
oa: 1
oa_version: Preprint
project:
- _id: 2564DBCA-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '665385'
name: International IST Doctoral Program
- _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: 26B4D67E-B435-11E9-9278-68D0E5697425
grant_number: '25351'
name: 'A Case Study of Plant Growth Regulation: Molecular Mechanism of Auxin-mediated
Rapid Growth Inhibition in Arabidopsis Root'
publication: Research Square
publication_identifier:
issn:
- 2693-5015
publication_status: accepted
related_material:
record:
- id: '10083'
relation: dissertation_contains
status: public
- id: '10223'
relation: later_version
status: public
status: public
title: Cell surface and intracellular auxin signalling for H+-fluxes in root growth
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: preprint
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
year: '2021'
...
---
_id: '10223'
abstract:
- lang: eng
text: Growth regulation tailors development in plants to their environment. A prominent
example of this is the response to gravity, in which shoots bend up and roots
bend down1. This paradox is based on opposite effects of the phytohormone auxin,
which promotes cell expansion in shoots while inhibiting it in roots via a yet
unknown cellular mechanism2. Here, by combining microfluidics, live imaging, genetic
engineering and phosphoproteomics in Arabidopsis thaliana, we advance understanding
of how auxin inhibits root growth. We show that auxin activates two distinct,
antagonistically acting signalling pathways that converge on rapid regulation
of apoplastic pH, a causative determinant of growth. Cell surface-based TRANSMEMBRANE
KINASE1 (TMK1) interacts with and mediates phosphorylation and activation of plasma
membrane H+-ATPases for apoplast acidification, while intracellular canonical
auxin signalling promotes net cellular H+ influx, causing apoplast alkalinization.
Simultaneous activation of these two counteracting mechanisms poises roots for
rapid, fine-tuned growth modulation in navigating complex soil environments.
acknowledged_ssus:
- _id: LifeSc
- _id: M-Shop
- _id: Bio
acknowledgement: We thank N. Gnyliukh and L. Hörmayer for technical assistance and
N. Paris for sharing PM-Cyto seeds. We gratefully acknowledge the Life Science,
Machine Shop and Bioimaging Facilities of IST Austria. This project has received
funding from the European Research Council Advanced Grant (ETAP-742985) and the
Austrian Science Fund (FWF) under I 3630-B25 to J.F., the National Institutes of
Health (GM067203) to W.M.G., the Netherlands Organization for Scientific Research
(NWO; VIDI-864.13.001), Research Foundation-Flanders (FWO; Odysseus II G0D0515N)
and a European Research Council Starting Grant (TORPEDO-714055) to W.S. and B.D.R.,
the VICI grant (865.14.001) from the Netherlands Organization for Scientific Research
to M.R. and D.W., the Australian Research Council and China National Distinguished
Expert Project (WQ20174400441) to S.S., the MEXT/JSPS KAKENHI to K.T. (20K06685)
and T.K. (20H05687 and 20H05910), the European Union’s Horizon 2020 research and
innovation programme under Marie Skłodowska-Curie grant agreement no. 665385 and
the DOC Fellowship of the Austrian Academy of Sciences to L.L., and the China Scholarship
Council to J.C.
article_processing_charge: No
article_type: original
author:
- first_name: Lanxin
full_name: Li, Lanxin
id: 367EF8FA-F248-11E8-B48F-1D18A9856A87
last_name: Li
orcid: 0000-0002-5607-272X
- first_name: Inge
full_name: Verstraeten, Inge
id: 362BF7FE-F248-11E8-B48F-1D18A9856A87
last_name: Verstraeten
orcid: 0000-0001-7241-2328
- first_name: Mark
full_name: Roosjen, Mark
last_name: Roosjen
- first_name: Koji
full_name: Takahashi, Koji
last_name: Takahashi
- 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: Jack
full_name: Merrin, Jack
id: 4515C308-F248-11E8-B48F-1D18A9856A87
last_name: Merrin
orcid: 0000-0001-5145-4609
- first_name: Jian
full_name: Chen, Jian
last_name: Chen
- first_name: Lana
full_name: Shabala, Lana
last_name: Shabala
- first_name: Wouter
full_name: Smet, Wouter
last_name: Smet
- first_name: Hong
full_name: Ren, Hong
last_name: Ren
- first_name: Steffen
full_name: Vanneste, Steffen
last_name: Vanneste
- first_name: Sergey
full_name: Shabala, Sergey
last_name: Shabala
- first_name: Bert
full_name: De Rybel, Bert
last_name: De Rybel
- first_name: Dolf
full_name: Weijers, Dolf
last_name: Weijers
- first_name: Toshinori
full_name: Kinoshita, Toshinori
last_name: Kinoshita
- first_name: William M.
full_name: Gray, William M.
last_name: Gray
- first_name: Jiří
full_name: Friml, Jiří
id: 4159519E-F248-11E8-B48F-1D18A9856A87
last_name: Friml
orcid: 0000-0002-8302-7596
citation:
ama: Li L, Verstraeten I, Roosjen M, et al. Cell surface and intracellular auxin
signalling for H+ fluxes in root growth. Nature. 2021;599(7884):273-277.
doi:10.1038/s41586-021-04037-6
apa: Li, L., Verstraeten, I., Roosjen, M., Takahashi, K., Rodriguez Solovey, L.,
Merrin, J., … Friml, J. (2021). Cell surface and intracellular auxin signalling
for H+ fluxes in root growth. Nature. Springer Nature. https://doi.org/10.1038/s41586-021-04037-6
chicago: Li, Lanxin, Inge Verstraeten, Mark Roosjen, Koji Takahashi, Lesia Rodriguez
Solovey, Jack Merrin, Jian Chen, et al. “Cell Surface and Intracellular Auxin
Signalling for H+ Fluxes in Root Growth.” Nature. Springer Nature,
2021. https://doi.org/10.1038/s41586-021-04037-6.
ieee: L. Li et al., “Cell surface and intracellular auxin signalling for
H+ fluxes in root growth,” Nature, vol. 599, no. 7884. Springer
Nature, pp. 273–277, 2021.
ista: Li L, Verstraeten I, Roosjen M, Takahashi K, Rodriguez Solovey L, Merrin J,
Chen J, Shabala L, Smet W, Ren H, Vanneste S, Shabala S, De Rybel B, Weijers D,
Kinoshita T, Gray WM, Friml J. 2021. Cell surface and intracellular auxin signalling
for H+ fluxes in root growth. Nature. 599(7884), 273–277.
mla: Li, Lanxin, et al. “Cell Surface and Intracellular Auxin Signalling for H+
Fluxes in Root Growth.” Nature, vol. 599, no. 7884, Springer Nature, 2021,
pp. 273–77, doi:10.1038/s41586-021-04037-6.
short: L. Li, I. Verstraeten, M. Roosjen, K. Takahashi, L. Rodriguez Solovey, J.
Merrin, J. Chen, L. Shabala, W. Smet, H. Ren, S. Vanneste, S. Shabala, B. De Rybel,
D. Weijers, T. Kinoshita, W.M. Gray, J. Friml, Nature 599 (2021) 273–277.
date_created: 2021-11-07T23:01:25Z
date_published: 2021-11-11T00:00:00Z
date_updated: 2024-10-29T10:22:45Z
day: '11'
department:
- _id: JiFr
- _id: NanoFab
doi: 10.1038/s41586-021-04037-6
ec_funded: 1
external_id:
isi:
- '000713338100006'
pmid:
- '34707283'
intvolume: ' 599'
isi: 1
issue: '7884'
keyword:
- Multidisciplinary
language:
- iso: eng
main_file_link:
- open_access: '1'
url: https://www.doi.org/10.21203/rs.3.rs-266395/v3
month: '11'
oa: 1
oa_version: Preprint
page: 273-277
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: 2564DBCA-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '665385'
name: International IST Doctoral Program
- _id: 26B4D67E-B435-11E9-9278-68D0E5697425
grant_number: '25351'
name: 'A Case Study of Plant Growth Regulation: Molecular Mechanism of Auxin-mediated
Rapid Growth Inhibition in Arabidopsis Root'
publication: Nature
publication_identifier:
eissn:
- '14764687'
issn:
- '00280836'
publication_status: published
publisher: Springer Nature
quality_controlled: '1'
related_material:
link:
- description: News on IST Webpage
relation: press_release
url: https://ist.ac.at/en/news/stop-and-grow/
record:
- id: '10095'
relation: earlier_version
status: public
scopus_import: '1'
status: public
title: Cell surface and intracellular auxin signalling for H+ fluxes in
root growth
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 599
year: '2021'
...
---
_id: '8986'
abstract:
- lang: eng
text: 'Flowering plants display the highest diversity among plant species and have
notably shaped terrestrial landscapes. Nonetheless, the evolutionary origin of
their unprecedented morphological complexity remains largely an enigma. Here,
we show that the coevolution of cis-regulatory and coding regions of PIN-FORMED
(PIN) auxin transporters confined their expression to certain cell types and directed
their subcellular localization to particular cell sides, which together enabled
dynamic auxin gradients across tissues critical to the complex architecture of
flowering plants. Extensive intraspecies and interspecies genetic complementation
experiments with PINs from green alga up to flowering plant lineages showed that
PIN genes underwent three subsequent, critical evolutionary innovations and thus
acquired a triple function to regulate the development of three essential components
of the flowering plant Arabidopsis: shoot/root, inflorescence, and floral organ.
Our work highlights the critical role of functional innovations within the PIN
gene family as essential prerequisites for the origin of flowering plants.'
acknowledgement: 'We thank C.Löhne (Botanic Gardens, University of Bonn) for providing
us with A. trichopoda. We would like to thank T.Han, A.Mally (IST, Austria), and
C.Hartinger (University of Oxford) for constructive comment and careful reading.
Funding: The research leading to these results has received funding from the European
Union’s Horizon 2020 Research and Innovation Programme (ERC grant agreement number
742985), Austrian Science Fund (FWF, grant number I 3630-B25), DOC Fellowship of
the Austrian Academy of Sciences, and IST Fellow program. '
article_number: eabc8895
article_processing_charge: No
article_type: original
author:
- first_name: Yuzhou
full_name: Zhang, Yuzhou
id: 3B6137F2-F248-11E8-B48F-1D18A9856A87
last_name: Zhang
orcid: 0000-0003-2627-6956
- 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: Lanxin
full_name: Li, Lanxin
id: 367EF8FA-F248-11E8-B48F-1D18A9856A87
last_name: Li
orcid: 0000-0002-5607-272X
- first_name: Xixi
full_name: Zhang, Xixi
id: 61A66458-47E9-11EA-85BA-8AEAAF14E49A
last_name: Zhang
orcid: 0000-0001-7048-4627
- first_name: Jiří
full_name: Friml, Jiří
id: 4159519E-F248-11E8-B48F-1D18A9856A87
last_name: Friml
orcid: 0000-0002-8302-7596
citation:
ama: Zhang Y, Rodriguez Solovey L, Li L, Zhang X, Friml J. Functional innovations
of PIN auxin transporters mark crucial evolutionary transitions during rise of
flowering plants. Science Advances. 2020;6(50). doi:10.1126/sciadv.abc8895
apa: Zhang, Y., Rodriguez Solovey, L., Li, L., Zhang, X., & Friml, J. (2020).
Functional innovations of PIN auxin transporters mark crucial evolutionary transitions
during rise of flowering plants. Science Advances. AAAS. https://doi.org/10.1126/sciadv.abc8895
chicago: Zhang, Yuzhou, Lesia Rodriguez Solovey, Lanxin Li, Xixi Zhang, and Jiří
Friml. “Functional Innovations of PIN Auxin Transporters Mark Crucial Evolutionary
Transitions during Rise of Flowering Plants.” Science Advances. AAAS, 2020.
https://doi.org/10.1126/sciadv.abc8895.
ieee: Y. Zhang, L. Rodriguez Solovey, L. Li, X. Zhang, and J. Friml, “Functional
innovations of PIN auxin transporters mark crucial evolutionary transitions during
rise of flowering plants,” Science Advances, vol. 6, no. 50. AAAS, 2020.
ista: Zhang Y, Rodriguez Solovey L, Li L, Zhang X, Friml J. 2020. Functional innovations
of PIN auxin transporters mark crucial evolutionary transitions during rise of
flowering plants. Science Advances. 6(50), eabc8895.
mla: Zhang, Yuzhou, et al. “Functional Innovations of PIN Auxin Transporters Mark
Crucial Evolutionary Transitions during Rise of Flowering Plants.” Science
Advances, vol. 6, no. 50, eabc8895, AAAS, 2020, doi:10.1126/sciadv.abc8895.
short: Y. Zhang, L. Rodriguez Solovey, L. Li, X. Zhang, J. Friml, Science Advances
6 (2020).
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