Máthé, Csaba

Nick, Peter

Pasternak, Taras P.

Frontiers in Plant Science

English

PubMed

Csaba Máthé

Peter Nick

Taras P. Pasternak

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EDITORIAL
published: 06 July 2021
doi: 10.3389/fpls.2021.706892
Frontiers in Plant Science | www.frontiersin.org 1 July 2021 | Volume 12 | Article 706892
Edited by:
Zhaojun Ding,
Shandong University, China
Reviewed by:
Rucha Karnik,
University of Glasgow,
United Kingdom
Shutang Tan,
University of Science and Technology
of China, China
Jiaqi Sun,
McGill University, Canada
*Correspondence:
Csaba Máthé
mathe.csaba@science.unideb.hu
Peter Nick
peter.nick@kit.edu
Taras P. Pasternak
taras.p.pasternak@gmail.com
Specialty section:
This article was submitted to
Plant Cell Biology,
a section of the journal
Frontiers in Plant Science
Received: 08 May 2021
Accepted: 11 June 2021
Published: 06 July 2021
Citation:
Máthé C, Nick P and Pasternak TP
(2021) Editorial: How Cells Build
Plants: Regulatory Mechanisms for
Integrated Functioning of Plant Cells
and the Whole Plant Body.
Front. Plant Sci. 12:706892.
doi: 10.3389/fpls.2021.706892
Editorial: How Cells Build Plants:
Regulatory Mechanisms for
Integrated Functioning of Plant Cells
and the Whole Plant Body
Csaba Máthé 1*, Peter Nick 2* and Taras P. Pasternak 3*
1 Laboratory of Plant Cell and Developmental Biology, Department of Botany, Faculty of Science and Technology, Institute of
Biology and Ecology, University of Debrecen, Debrecen, Hungary, 2Department of Molecular Cell Biology, Botanical Institute,
Karlsruhe Institute of Technology, Karlsruhe, Germany, 3Centre for BioSystems Analysis, BIOSS Centre for Biological
Signalling Studies, Institute of Biology II/Molecular Plant Physiology, University of Freiburg, Freiburg, Germany
Keywords: cytoskeleton, vesicle traffic, SNARE, aquaporin, auxin, root development, pollen tube, allelopathy
Editorial on the Research Topic
How Cells Build Plants: Regulatory Mechanisms for Integrated Functioning of Plant Cells and
the Whole Plant Body
Plants are multicellular organisms with different cell types, developed in close connections to each
other. How cells in plants interact and how changes in each cell affect entire plants are critical
questions in plant biology. Among processes essential for coordination between different cell types,
cytoskeleton and vesicle traffic are the central hub. The main task of this Research Topic is to show
how changes in specific cells affected entire plant development, that is, how cells build the plants in
a coordinative manner.
As in all eukaryotes, the cytoskeleton, and the endomembrane system—with the primary role of
the ER-Golgi continuum as governors of vesicle traffic –play important roles in the function of the
entire plant cell. This Research Topic addresses particular aspects of this central function focusing
on the following aspects of cellular integration: (i) cytoskeletal organization and function including
pollen tube elongation as an example for directional cell growth, (ii) the role of SNARE (soluble
N-ethyl maleimide sensitive factor attachment protein receptor) proteins in vesicle traffic, and
(iii) auxin transport/signaling. As we will see, these topics are in close relationship and ultimately
contribute essentially to the understanding of the regulation of whole plant development. For
example, coordinated membrane flow is important for polar auxin transport—a central regulator
of plant ontogenesis and one of the important drivers of membrane traffic is the cytoskeleton, via
specific motor proteins (Nick, 2010; Yao and Xue, 2011). The functioning of SNAREs is closely
linked to the cytoskeleton (Steiner et al., 2016). The cytoskeleton is also integrated to the perception
and transduction of stress signals (Nick, 2013).
A nice example showing how disturbances in microtubule organization/stability will ultimately
affect root development is provided by Ovečka et al. Katanin1 is a microtubule (MT) severing
protein and loss-of-function mutations of its gene induce re-arrangement of the stem cell niche in
the apex of primary and lateral roots. Since the quiescent center (QC) has a pivotal role in building
up the root apical meristem, there are significant consequences for cellular patterning. Moreover,
the mutants showed aberrant preprophase bands (PPBs) that contributed to misorientation of
mitotic divisions. Alterations in the morphology of lateral root primordia, their cell numbers and
patterning were also observed.
Máthé et al. Editorial: How Cells Build Plants
MT organization is crucial for all stages of plant development
from its “very beginnings.” Schattner et al. show that a subfamily
of the MT binding kinesin-14 motor proteins in Arabidopsis
is involved in the saltatory movement of sperm cells inside
the pollen tube, this movement being independent from the
vegetative cell. This mechanism is contributing to the movement
of sperm cells toward the tip of pollen tube to allow subsequent
fertilization. According to the “tug-of-war” model presented,
sperm cells encaged by MTs are connected to microfilaments
(MFs) by these kinesins that direct bidirectional movement of
MTs on MFs to allow a tipward “step-by-step” mobility of sperm
cells. The article is showing the collaboration between different
cytoskeletal structures for the proper localization of a special cell
type in plants. Kollárová et al. show how the class II formin FH3,
an actin nucleating protein acts as a “moderator” of pollen tube
growth and point out the presence of braking forces to ensure the
proper velocity of this growth. They raise the possibility that this
type of actin-binding proteins (class II formins) is involved in the
regulation of vesicle traffic in plants.
The next paper links cytoskeleton associated proteins to
membrane traffic and auxin distribution and signaling in
planta. García-González et al. show how auxin regulates cell-
specific expression of ARP2/3 (Actin Related Protein 2/3), a
protein complex that promotes G-actin nucleation and the
formation of MF networks in eukaryotic cells. Moreover, in
the absence of a functional ARP2/3 complex the auxin efflux
carrier PIN3 (PIN-formed 3) will be retained in endomembranes
and PIN1 will be mislocalised in plasma membranes of
Arabidopsis epidermal pavement cells. Consequently, pavement
cell shape will be altered in arp mutants. Auxin distribution
in plant axial organs depends on a complex gene regulatory
network (Omelyanchuk et al., 2016). For example, WOX5
(Wuschel-related Homeobox 5), a member of a gene family that
regulates plant development from embryogenesis to whole-plant
cellular patterning, triggers expression of TAA1 (Tryptophan
aminotransferase of Arabidopsis 1), a protein crucial for auxin
biosynthesis as well as proper distribution of PIN efflux carriers.
Induction of ectopic WOX5 expression led to extension of the
columella stem cell niche and active cell divisions in the distal
meristem, to regulate proper identity of root apical meristems
(Savina et al.).
The cytoskeleton is also crucial for vesicle traffic [see Baskin
(2015), Máthé et al. (2021) for examples]. SNARE proteins are
important for the formation of membrane contacts and vesicle
fusion during vesicle traffic e.g., exocytosis (Yao and Xue, 2011).
Laloux et al. show the structural motifs of SYP121 (Syntaxin of
Plant 121), a Qa-SNARE involved in the interaction with the
aquaporin PIP2;7. This interaction is important for the vesicular
fusion that locates the aquaporin to the plasma membrane in
epidermal pavement cells of Arabidopsis. They demonstrate
that multiple functional regions including the transmembrane
domain of SYP121 are required for the interaction. The authors
suggest that SYP121-PIP interactions may be involved in
responses to pathogens as well by regulating H2O2 uptake of
cells during infection.What are the interactions between SNAREs
and the cytoskeleton? The interactions can be multiple. Guan
et al. show how the Arabidopsis v-SNARE AtSEC22 (Arabidopsis
thaliana secretory protein) regulates the proper development of
axial organs. Mutated protein impairs development partially by
disturbing cytoskeletal organization, of both, cortical MTs and
MFs. This will block vesicle traffic and cause trapping of several
proteins in the ER. What is the underlying mechanism? The
authors propose that traffic of cytoskeleton-associated proteins
involved in the regulation of MT and MF stability, dynamics
and bundling is blocked in mutants: dysfunctional SNARE would
block the delivery of cytoskeleton associated proteins to their
proper destination.
All these articles show how intracellular activities such
as vesicle flow or cytoskeletal dynamics contribute to the
regulation of tissue- and whole-plant development. Insight
into this integration can also lead to practical application:
Using activity-guided fractionation for germination inhibiting
compounds fromMints that suppress competitors by allelopathy,
led to the monoterpene menthone/isomenthone (Sarheed et al.).
Using tobacco BY-2 cells as a model, the activity can be linked to a
rapid and specific elimination of cortical microtubules, followed
by programmed cell death. The effect can be recapitulated in
Arabidopsis seedlings, demonstrating the use of thesemetabolites
as eco-friendly herbicides in agriculture.
AUTHOR CONTRIBUTIONS
All authors had essential contributions to this Editorial
regarding writing and corrections and all of them agreed to its
final version.
ACKNOWLEDGMENTS
The authors would like to thank all researchers who contributed
to this Research Topic of Frontiers in Plant Science.
REFERENCES
Baskin, T. (2015). “The cytoskeleton”, in Biochemistry and Molecular Biology
of Plants, editors B. B. Buchanan, W. Gruissem, R. L. Jones (Chichester:
Wiley-ASPB), 191–238.
Máthé, C. M., Hamvas, M., Freytag, C., and Garda, T. (2021). The protein
phosphatases PP2A plays multiple roles in plant development by
regulation of vesicle traffic- facts and questions. Int. J. Mol. Sci. 22:975.
doi: 10.3390/ijms22020975
Nick, P. (2010). Probing the actin-auxin oscillator. Plant Signal. Behav. 5, 4–9.
doi: 10.4161/psb.5.2.10337
Nick, P. (2013). Microtubules, signaling and abiotic stress. Plant J. 75, 309–323.
doi: 10.1111/tpj.12102
Omelyanchuk, N., Kovrizhnykh, W., Oschcepkova, E. A., Pasternak,
T. P., Palme, K., and Mironova, W. (2016). A detailed
expression map of the PIN1 auxin transporter in Arabidopsis
thaliana root. BMC Plant Biol. 16:5. doi: 10.1186/s12870-015-0
685-0
Steiner, A., Müller, L., Rybak, K., Vodermaier, V., Facher, E., Thellmann, M.,
et al. (2016). The membrane-associated Sec1/Munc18 KEULE is required for
phragmoplast, microtubule reorganization during cytokinesis in Arabidopsis.
Mol. Plant 9, 528–540. doi: 10.1016/j.molp.2015.12.005
Frontiers in Plant Science | www.frontiersin.org 2 July 2021 | Volume 12 | Article 706892
Máthé et al. Editorial: How Cells Build Plants
Yao, H. Y., and Xue, H. W. (2011). Signals and mechanisms affecting
vesicular trafficking during root growth. Curr. Opin. Plant Biol. 14, 571–579.
doi: 10.1016/j.pbi.2011.06.009
Conflict of Interest: The authors declare that the research was conducted in the
absence of any commercial or financial relationships that could be construed as a
potential conflict of interest.
Copyright © 2021 Máthé, Nick and Pasternak. This is an open-access article
distributed under the terms of the Creative Commons Attribution License (CC BY).
The use, distribution or reproduction in other forums is permitted, provided the
original author(s) and the copyright owner(s) are credited and that the original
publication in this journal is cited, in accordance with accepted academic practice.
No use, distribution or reproduction is permitted which does not comply with these
terms.
Frontiers in Plant Science | www.frontiersin.org 3 July 2021 | Volume 12 | Article 706892


Editorial: How Cells Build Plants: Regulatory Mechanisms for Integrated Functioning of Plant Cells and the Whole Plant Body

KITopen

EDITORIALpublished: 06 July 2021doi: 10.3389/fpls.2021.706892Frontiers in Plant Science | www.frontiersin.org 1 July 2021 | Volume 12 | Article 706892Edited by:Zhaojun Ding,Shandong University, ChinaReviewed by:Rucha Karnik,University of Glasgow,United KingdomShutang Tan,University of Science and Technologyof China, ChinaJiaqi Sun,McGill University, Canada*Correspondence:Csaba Máthémathe.csaba@science.unideb.huPeter Nickpeter.nick@kit.eduTaras P. Pasternaktaras.p.pasternak@gmail.comSpecialty section:This article was submitted toPlant Cell Biology,a section of the journalFrontiers in Plant ScienceReceived: 08 May 2021Accepted: 11 June 2021Published: 06 July 2021Citation:Máthé C, Nick P and Pasternak TP(2021) Editorial: How Cells BuildPlants: Regulatory Mechanisms forIntegrated Functioning of Plant Cellsand the Whole Plant Body.Front. Plant Sci. 12:706892.doi: 10.3389/fpls.2021.706892Editorial: How Cells Build Plants:Regulatory Mechanisms forIntegrated Functioning of Plant Cellsand the Whole Plant BodyCsaba Máthé 1*, Peter Nick 2* and Taras P. Pasternak 3*1 Laboratory of Plant Cell and Developmental Biology, Department of Botany, Faculty of Science and Technology, Institute ofBiology and Ecology, University of Debrecen, Debrecen, Hungary, 2Department of Molecular Cell Biology, Botanical Institute,Karlsruhe Institute of Technology, Karlsruhe, Germany, 3Centre for BioSystems Analysis, BIOSS Centre for BiologicalSignalling Studies, Institute of Biology II/Molecular Plant Physiology, University of Freiburg, Freiburg, GermanyKeywords: cytoskeleton, vesicle traffic, SNARE, aquaporin, auxin, root development, pollen tube, allelopathyEditorial on the Research TopicHow Cells Build Plants: Regulatory Mechanisms for Integrated Functioning of Plant Cells andthe Whole Plant BodyPlants are multicellular organisms with different cell types, developed in close connections to eachother. How cells in plants interact and how changes in each cell affect entire plants are criticalquestions in plant biology. Among processes essential for coordination between different cell types,cytoskeleton and vesicle traffic are the central hub. The main task of this Research Topic is to showhow changes in specific cells affected entire plant development, that is, how cells build the plants ina coordinative manner.As in all eukaryotes, the cytoskeleton, and the endomembrane system—with the primary role ofthe ER-Golgi continuum as governors of vesicle traffic –play important roles in the function of theentire plant cell. This Research Topic addresses particular aspects of this central function focusingon the following aspects of cellular integration: (i) cytoskeletal organization and function includingpollen tube elongation as an example for directional cell growth, (ii) the role of SNARE (solubleN-ethyl maleimide sensitive factor attachment protein receptor) proteins in vesicle traffic, and(iii) auxin transport/signaling. As we will see, these topics are in close relationship and ultimatelycontribute essentially to the understanding of the regulation of whole plant development. Forexample, coordinated membrane flow is important for polar auxin transport—a central regulatorof plant ontogenesis and one of the important drivers of membrane traffic is the cytoskeleton, viaspecific motor proteins (Nick, 2010; Yao and Xue, 2011). The functioning of SNAREs is closelylinked to the cytoskeleton (Steiner et al., 2016). The cytoskeleton is also integrated to the perceptionand transduction of stress signals (Nick, 2013).A nice example showing how disturbances in microtubule organization/stability will ultimatelyaffect root development is provided by Ovečka et al. Katanin1 is a microtubule (MT) severingprotein and loss-of-function mutations of its gene induce re-arrangement of the stem cell niche inthe apex of primary and lateral roots. Since the quiescent center (QC) has a pivotal role in buildingup the root apical meristem, there are significant consequences for cellular patterning. Moreover,the mutants showed aberrant preprophase bands (PPBs) that contributed to misorientation ofmitotic divisions. Alterations in the morphology of lateral root primordia, their cell numbers andpatterning were also observed.Máthé et al. Editorial: How Cells Build PlantsMT organization is crucial for all stages of plant developmentfrom its “very beginnings.” Schattner et al. show that a subfamilyof the MT binding kinesin-14 motor proteins in Arabidopsisis involved in the saltatory movement of sperm cells insidethe pollen tube, this movement being independent from thevegetative cell. This mechanism is contributing to the movementof sperm cells toward the tip of pollen tube to allow subsequentfertilization. According to the “tug-of-war” model presented,sperm cells encaged by MTs are connected to microfilaments(MFs) by these kinesins that direct bidirectional movement ofMTs on MFs to allow a tipward “step-by-step” mobility of spermcells. The article is showing the collaboration between differentcytoskeletal structures for the proper localization of a special celltype in plants. Kollárová et al. show how the class II formin FH3,an actin nucleating protein acts as a “moderator” of pollen tubegrowth and point out the presence of braking forces to ensure theproper velocity of this growth. They raise the possibility that thistype of actin-binding proteins (class II formins) is involved in theregulation of vesicle traffic in plants.The next paper links cytoskeleton associated proteins tomembrane traffic and auxin distribution and signaling inplanta. García-González et al. show how auxin regulates cell-specific expression of ARP2/3 (Actin Related Protein 2/3), aprotein complex that promotes G-actin nucleation and theformation of MF networks in eukaryotic cells. Moreover, inthe absence of a functional ARP2/3 complex the auxin effluxcarrier PIN3 (PIN-formed 3) will be retained in endomembranesand PIN1 will be mislocalised in plasma membranes ofArabidopsis epidermal pavement cells. Consequently, pavementcell shape will be altered in arp mutants. Auxin distributionin plant axial organs depends on a complex gene regulatorynetwork (Omelyanchuk et al., 2016). For example, WOX5(Wuschel-related Homeobox 5), a member of a gene family thatregulates plant development from embryogenesis to whole-plantcellular patterning, triggers expression of TAA1 (Tryptophanaminotransferase of Arabidopsis 1), a protein crucial for auxinbiosynthesis as well as proper distribution of PIN efflux carriers.Induction of ectopic WOX5 expression led to extension of thecolumella stem cell niche and active cell divisions in the distalmeristem, to regulate proper identity of root apical meristems(Savina et al.).The cytoskeleton is also crucial for vesicle traffic [see Baskin(2015), Máthé et al. (2021) for examples]. SNARE proteins areimportant for the formation of membrane contacts and vesiclefusion during vesicle traffic e.g., exocytosis (Yao and Xue, 2011).Laloux et al. show the structural motifs of SYP121 (Syntaxin ofPlant 121), a Qa-SNARE involved in the interaction with theaquaporin PIP2;7. This interaction is important for the vesicularfusion that locates the aquaporin to the plasma membrane inepidermal pavement cells of Arabidopsis. They demonstratethat multiple functional regions including the transmembranedomain of SYP121 are required for the interaction. The authorssuggest that SYP121-PIP interactions may be involved inresponses to pathogens as well by regulating H2O2 uptake ofcells during infection.What are the interactions between SNAREsand the cytoskeleton? The interactions can be multiple. Guanet al. show how the Arabidopsis v-SNARE AtSEC22 (Arabidopsisthaliana secretory protein) regulates the proper development ofaxial organs. Mutated protein impairs development partially bydisturbing cytoskeletal organization, of both, cortical MTs andMFs. This will block vesicle traffic and cause trapping of severalproteins in the ER. What is the underlying mechanism? Theauthors propose that traffic of cytoskeleton-associated proteinsinvolved in the regulation of MT and MF stability, dynamicsand bundling is blocked in mutants: dysfunctional SNARE wouldblock the delivery of cytoskeleton associated proteins to theirproper destination.All these articles show how intracellular activities suchas vesicle flow or cytoskeletal dynamics contribute to theregulation of tissue- and whole-plant development. Insightinto this integration can also lead to practical application:Using activity-guided fractionation for germination inhibitingcompounds fromMints that suppress competitors by allelopathy,led to the monoterpene menthone/isomenthone (Sarheed et al.).Using tobacco BY-2 cells as a model, the activity can be linked to arapid and specific elimination of cortical microtubules, followedby programmed cell death. The effect can be recapitulated inArabidopsis seedlings, demonstrating the use of thesemetabolitesas eco-friendly herbicides in agriculture.AUTHOR CONTRIBUTIONSAll authors had essential contributions to this Editorialregarding writing and corrections and all of them agreed to itsfinal version.ACKNOWLEDGMENTSThe authors would like to thank all researchers who contributedto this Research Topic of Frontiers in Plant Science.REFERENCESBaskin, T. (2015). “The cytoskeleton”, in Biochemistry and Molecular Biologyof Plants, editors B. B. Buchanan, W. Gruissem, R. L. Jones (Chichester:Wiley-ASPB), 191–238.Máthé, C. M., Hamvas, M., Freytag, C., and Garda, T. (2021). The proteinphosphatases PP2A plays multiple roles in plant development byregulation of vesicle traffic- facts and questions. Int. J. Mol. Sci. 22:975.doi: 10.3390/ijms22020975Nick, P. (2010). Probing the actin-auxin oscillator. Plant Signal. Behav. 5, 4–9.doi: 10.4161/psb.5.2.10337Nick, P. (2013). Microtubules, signaling and abiotic stress. Plant J. 75, 309–323.doi: 10.1111/tpj.12102Omelyanchuk, N., Kovrizhnykh, W., Oschcepkova, E. A., Pasternak,T. P., Palme, K., and Mironova, W. (2016). A detailedexpression map of the PIN1 auxin transporter in Arabidopsisthaliana root. BMC Plant Biol. 16:5. doi: 10.1186/s12870-015-0685-0Steiner, A., Müller, L., Rybak, K., Vodermaier, V., Facher, E., Thellmann, M.,et al. (2016). The membrane-associated Sec1/Munc18 KEULE is required forphragmoplast, microtubule reorganization during cytokinesis in Arabidopsis.Mol. Plant 9, 528–540. doi: 10.1016/j.molp.2015.12.005Frontiers in Plant Science | www.frontiersin.org 2 July 2021 | Volume 12 | Article 706892Máthé et al. Editorial: How Cells Build PlantsYao, H. Y., and Xue, H. W. (2011). Signals and mechanisms affectingvesicular trafficking during root growth. Curr. Opin. Plant Biol. 14, 571–579.doi: 10.1016/j.pbi.2011.06.009Conflict of Interest: The authors declare that the research was conducted in theabsence of any commercial or financial relationships that could be construed as apotential conflict of interest.Copyright © 2021 Máthé, Nick and Pasternak. This is an open-access articledistributed under the terms of the Creative Commons Attribution License (CC BY).The use, distribution or reproduction in other forums is permitted, provided theoriginal author(s) and the copyright owner(s) are credited and that the originalpublication in this journal is cited, in accordance with accepted academic practice.No use, distribution or reproduction is permitted which does not comply with theseterms.Frontiers in Plant Science | www.frontiersin.org 3 July 2021 | Volume 12 | Article 706892

http://dx.doi.org/10.3389/fpls.2021.706892

Editorial: How Cells Build Plants: Regulatory Mechanisms for Integrated Functioning of Plant Cells and the Whole Plant Body

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