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Talking with the neighbours: Understanding spatial accommodation during plant development

English title Talking with the neighbours: Understanding spatial accommodation during plant development
Applicant Vermeer Joop
Number 157524
Funding scheme SNSF Professorships
Research institution Institut für Pflanzen- und Mikrobiologie Universität Zürich
Institution of higher education University of Zurich - ZH
Main discipline Embryology, Developmental Biology
Start/End 01.10.2015 - 30.09.2021
Approved amount 1'897'502.00
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All Disciplines (4)

Discipline
Embryology, Developmental Biology
Genetics
Cellular Biology, Cytology
Molecular Biology

Keywords (7)

spatial accommodation; intercellular communication; organ initiation; Arabidopsis thaliana; cell volume regulation; lateral roots; mechanical constraints

Lay Summary (Italian)

Lead
Talking with the neighbours: Understanding spatial accommodation during plant development
Lay summary

In sintesi

Le cellule vegetali sono immobili, interconnesse attraverso la parete cellulare e sottoposte ad un’ altissima pressione, che può essere maggiore di quella di un pneumatico. Pertanto, le cellule vegetali hanno sviluppato meccanismi unici per coordinare la formazione dei loro organi. Lo scopo di questo progetto è studiare questi meccanismi durante lo sviluppo delle radici laterali nel modello Arabidopisis.

Soggetto e obiettivi

La formazione delle radici laterali è essenziale per la sopravvivenza delle piante. Dà vita ad un sistema di radici ramificato che permette alle piante sia di esplorare il terreno che le circonda alla ricerca di acqua e nutrienti, che di ancorarsi al suolo.  Le radici laterali si sviluppano dallo strato cellulare più interno della radice primaria e devono attraversare tre strati cellulari sovrastanti per emergere sulla superficie della radice. In un lavoro recente, abbiamo dimostrato che lo sviluppo delle radici laterali richiede una perdita controllata del volume delle cellule attraversate e coinvolge la regolazione di forze meccaniche. Lo scopo di questo progetto è di investigare i meccanismi molecolari che regolano lo sviluppo delle radici secondarie. Questo porterà a nuove conoscenze sui processi che regolano lo sviluppo delle piante.

Contesto socio-scientifico

Questa ricerca premetterà di ottenere nuove e fondamentali informazioni sui meccanismi di sviluppo delle piante, informazioni che potranno essere applicate anche a specie d’interesse agronomico. Più nello specifico, questo aprirà alla possibilità di sviluppare colture con sistemi di radici più efficienti in condizioni estreme, riducendo così l’utilizzo di fertilizzanti.

Parole chiave

Arabidopsis, radici laterali, percezione delle forze meccaniche, controllo del volume cellulare, morfologia, sviluppo.

Direct link to Lay Summary Last update: 15.05.2015

Responsible applicant and co-applicants

Employees

Publications

Publication
Dynamic cytokinin signalling landscapes during lateral root formation in Arabidopsis
Nenadić Milica, Vermeer Joop E. M. (2021), Dynamic cytokinin signalling landscapes during lateral root formation in Arabidopsis, in Quantitative Plant Biology, 2, e13-e13.
GDSL-domain proteins have key roles in suberin polymerization and degradation
Ursache Robertas, De Jesus Vieira Teixeira Cristovāo, Dénervaud Tendon Valérie, Gully Kay, De Bellis Damien, Schmid-Siegert Emanuel, Grube Andersen Tonni, Shekhar Vinay, Calderon Sandra, Pradervand Sylvain, Nawrath Christiane, Geldner Niko, Vermeer Joop E. M. (2021), GDSL-domain proteins have key roles in suberin polymerization and degradation, in Nature Plants, 7, 353-364.
Pluripotent Pericycle Cells Trigger Different Growth Outputs by Integrating Developmental Cues into Distinct Regulatory Modules
Xiao Wei, Molina David, Wunderling Anna, Ripper Dagmar, Vermeer Joop E.M., Ragni Laura (2020), Pluripotent Pericycle Cells Trigger Different Growth Outputs by Integrating Developmental Cues into Distinct Regulatory Modules, in Current Biology, 30(22), 4384-4398.e5.
Plant Biology: Journey to the Center of the Casparian Strip
Stöckle Dorothee, Vermeer Joop EM. (2020), Plant Biology: Journey to the Center of the Casparian Strip, in Current Biology, 30(20), R1273-R1275.
Translating Ribosome Affinity Purification (TRAP) to Investigate Arabidopsis thaliana Root Development at a Cell Type-Specific Scale
Thellmann Martha, Andersen Tonni Grube, Vermeer Joop EM (2020), Translating Ribosome Affinity Purification (TRAP) to Investigate Arabidopsis thaliana Root Development at a Cell Type-Specific Scale, in Journal of Visualized Experiments, (159), 1-15.
Geometric cues forecast the switch from two‐ to three‐dimensional growth in Physcomitrella patens
Tang Han, Duijts Kilian, Bezanilla Magdalena, Scheres Ben, Vermeer Joop E. M., Willemsen Viola (2019), Geometric cues forecast the switch from two‐ to three‐dimensional growth in Physcomitrella patens, in New Phytologist, nph.16276-nph.16276.
Cytoskeleton Dynamics Are Necessary for Early Events of Lateral Root Initiation in Arabidopsis
Vilches Barro Amaya, Stöckle Dorothee, Thellmann Martha, Ruiz-Duarte Paola, Bald Lotte, Louveaux Marion, von Born Patrick, Denninger Philipp, Goh Tatsuaki, Fukaki Hidehiro, Vermeer Joop E.M., Maizel Alexis (2019), Cytoskeleton Dynamics Are Necessary for Early Events of Lateral Root Initiation in Arabidopsis, in Current Biology, 1.
Exocyst subunit Sec6 is positioned by microtubule overlaps in the moss phragmoplast prior to the arrival of cell plate membrane
Tang Han, de Keijzer Jeroen, Overdijk Elysa, Sweep Els, Steentjes Maikel, Vermeer Joop EM, Janson Marcel, Ketelaar Tijs (2019), Exocyst subunit Sec6 is positioned by microtubule overlaps in the moss phragmoplast prior to the arrival of cell plate membrane, in BioRxiv, 1.
The role of plant root systems in evolutionary adaptation
Shekhar Vinay, Stӧckle Dorothee, Thellmann Martha, Vermeer Joop E.M. (2019), The role of plant root systems in evolutionary adaptation, in Grossniklaus Ueli (ed.), Elsevier, London, 55-80.
Root branching toward water involves posttranslational modification of transcription factor ARF7
Orosa-Puente Beatriz, Leftley Nicola, von Wangenheim Daniel, Banda Jason, Srivastava Anjil K., Hill Kristine, Truskina Jekaterina, Bhosale Rahul, Morris Emily, Srivastava Moumita, Kümpers Britta, Goh Tatsuaki, Fukaki Hidehiro, Vermeer Joop E. M., Vernoux Teva, Dinneny José R., French Andrew P., Bishopp Anthony, Sadanandom Ari, Bennett Malcolm J. (2018), Root branching toward water involves posttranslational modification of transcription factor ARF7, in Science, 362(6421), 1407-1410.
Diffusible repression of cytokinin signalling produces endodermal symmetry and passage cells
Andersen Tonni Grube, Naseer Sadaf, Ursache Robertas, Wybouw Brecht, Smet Wouter, De Rybel Bert, Vermeer Joop E. M., Geldner Niko (2018), Diffusible repression of cytokinin signalling produces endodermal symmetry and passage cells, in Nature, 555(7697), 529-533.
Arabidopsis Phospholipase C3 is Involved in Lateral Root Initiation and ABA Responses in Seed Germination and Stomatal Closure
Zhang Qianqian, van Wijk Ringo, Shahbaz Muhammad, Roels Wendy, Schooten Bas van, Vermeer Joop E M, Zarza Xavier, Guardia Aisha, Scuffi Denise, Garc�a-Mata Carlos, Laha Debabrata, Williams Phoebe, Willems Leo A J, Ligterink Wilco, Hoffmann-Benning Susanne, Gillaspy Glenda, Schaaf Gabriel, Haring Michel A, Laxalt Ana M, Munnik Teun (2018), Arabidopsis Phospholipase C3 is Involved in Lateral Root Initiation and ABA Responses in Seed Germination and Stomatal Closure, in Plant and Cell Physiology, 59(3), 469-486.
Green light for quantitative live-cell imaging in plants.
Grossman G, Krebs M, Maizel A, Stahl Y, Vermeer JE, OttT (2018), Green light for quantitative live-cell imaging in plants., in Journal of Cell Science, 131(2), 1-14.
Breakout - Lateral root emergence in Arabidopsis thaliana
Stoeckle D, Thellmann M, Vermeer JEM (2017), Breakout - Lateral root emergence in Arabidopsis thaliana, in Current Opinion in Plant Biology, 41, 67-72.
Perturbing phosphoinositide homeostasis oppositely affects vascular differentiation in Arabidopsis thaliana roots.
Gujas B, Cruz TMD, Kastanaki E, Vermeer JEM, Munnik T, Rodriguez-Villalon A (2017), Perturbing phosphoinositide homeostasis oppositely affects vascular differentiation in Arabidopsis thaliana roots., in Development, 144(19), 3578-3589.
In Vivo Imaging of Diacylglycerol at the Cytoplasmic Leaflet of Plant Membranes
Vermeer Joop, van Wijk R, Goedhart J, Geldner N, Chory J, Gadella TWJ jr., Munnik T (2017), In Vivo Imaging of Diacylglycerol at the Cytoplasmic Leaflet of Plant Membranes, in Plant Cell and Physiology, 58(7), 1196-1207.

Collaboration

Group / person Country
Types of collaboration
Niko Geldner / University of Lausanne Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
Joachim Goedhart / University of Amsterdam Netherlands (Europe)
- in-depth/constructive exchanges on approaches, methods or results
Alexis Maizel / COS Heidelberg Germany (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
Tom Beeckman / VIB Belgium (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Ari Sadanandom group Great Britain and Northern Ireland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
Malcolm Bennett / CPIB Nottingham Great Britain and Northern Ireland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
Ullrich Hammes / Regensburg University Germany (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Research Infrastructure
Olivier Hamant / ENS Lyon France (Europe)
- in-depth/constructive exchanges on approaches, methods or results

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
SEB 2021-Virtual Talk given at a conference Pericycle – endodermis communication shapes lateral root formation in Arabidopsis 29.06.2021 Antwerp, Belgium Stöckle Dorothee; Vermeer Joop; Thellmann Martha;
ICAR 2021 Virtual Talk given at a conference MAPping the role of the cytoskeleton during LR formation 21.06.2021 Seatle (VIRTUAL MEETING), United States of America Stöckle Dorothee; Vermeer Joop; Thellmann Martha; Nenadic Milica;
2019 Lateral Root Workshop Talk given at a conference MAPping the role of microtubules during lateral root formation. 13.09.2019 Leuven, Belgium Stöckle Dorothee; Nenadic Milica;
Mechanisms in Plant Development Talk given at a conference Partners in crime – Microtubules & Associates during lateral root formation 28.07.2019 Olean, New York, United States of America Stöckle Dorothee;
EPSR2019 Talk given at a conference Towards understanding spatial accommodating responses during plant development 08.07.2019 Nottingham, Great Britain and Northern Ireland Vermeer Joop;
9th International plant biomechanics conference Talk given at a conference MAPpin the roles of the cytoskeleton during lateral root formation. 09.08.2018 Montreal, Canada Stöckle Dorothee;
ISSR-10: Exposing the hidden half. Poster Forward genetic screen to understand pericycle-endodermis communication 08.07.2018 Ma'ale HaHamisha, Israel Shekhar Vinay Soma;
SEB Florence 2018 Talk given at a conference Towards understanding cellular communication in lateral root formation 03.07.2018 Florence, Italy Thellmann Martha;
International Symposium on Auxins and Cytokinins in Plant Development - ACPD 2018 Poster Shaping signalling landscapes during lateral root formation 01.07.2018 Prague, Czech Republic Vermeer Joop;
International Conference on Arabidopsis Research 2018 Talk given at a conference Functional deep imaging using 2-photon microscopy 25.06.2018 Turku, Finland Vermeer Joop; Thellmann Martha;
Mechanisms in Plant Development Talk given at a conference Cell volume regulation during lateral root formation in Arabidopsis. 30.07.2017 Saxtons River, VT, United States of America Vermeer Joop;
Rooting2017 Talk given at a conference Cell volume regulation during lateral root formation in Arabidopsis 29.05.2017 Umea, Sweden Thellmann Martha; Vermeer Joop;
Auxin2016 Talk given at a conference Cell volume regulation during lateral root formation in Arabidopsis 20.10.2016 Hainan, China Vermeer Joop;
International Conference on Arabidopsis Research Poster Cell volume regulation during lateral root formation in Arabidopsis 29.06.2016 Gyeongju, Korean Republic (South Korea) Vermeer Joop;
International Workshop on Plant Membrane Biology Talk given at a conference Cell volume regulation during lateral root formation in Arabidopsis 05.06.2016 Maryland, United States of America Vermeer Joop;


Self-organised

Title Date Place
Auxentric Zurich 2019 12.09.2019 Zurich, Switzerland

Associated projects

Number Title Start Funding scheme
171682 PSC Creative Camps for Youth 01.04.2017 Agora
164086 Imaging of Deep-Lying Tissues with Enhanced Resolution and Sensitivity to Study Plant Development 01.12.2015 R'EQUIP
197568 Spatial accommodation during plant development - adding new pieces to the puzzle 01.10.2020 Project funding

Abstract

Turgor-driven pressure of plant cells can be higher than that of a car tire. It puts tremendous forces onto cell walls and drives changes in cell shape. This has driven unique mechanisms to control organ formation in comparison to metazoans. The fascinating interplay between forces and local cellular reorganization is poorly understood. Growth of lateral roots is a prominent example of a developmental process in which mechanical forces are generated. Lateral roots grow from a single cell layer that resides deep within the primary root. On its way out, lateral roots grow through endodermal, cortical and epidermal cell layers. I recently demonstrated that endodermal cells actively accommodate lateral root formation. Responses include a dramatic volume loss and a controlled degradation of their lignin-based paracellular diffusion barrier. Interfering genetically with these accommodating responses in the endodermis completely blocks cell proliferation in the pericycle. The lateral root system provides a unique opportunity to elucidate the molecular and cellular mechanisms underlying spatial accommodation in plant development. I will combine genetic screens, state-of-the-art transcript profiling and advanced microscopy to identify the molecular players and mechanisms regulating spatial accommodation. Beyond its importance for lateral root formation, this research can provide fundamental new insights into many other developmental processes that heavily depend on spatial accommodation by surrounding tissue. These include the growth of pollen tubes and infection threads, the development of sclerenchyma fibre cells or the intracellular accommodation of symbionts.
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