A Self-Organized PLT/Auxin/ARR-B Network Controls the Dynamics of Root Zonation Development in Arabidopsis thaliana

Elena Salvi; Jacob Pieter Rutten; Riccardo Di Mambro; Laura Polverari; Valerio Licursi; Rodolfo Negri; Raffaele Dello Ioio; Sabrina Sabatini; Kirsten Ten Tusscher

doi:10.1016/j.devcel.2020.04.004

A Self-Organized PLT/Auxin/ARR-B Network Controls the Dynamics of Root Zonation Development in Arabidopsis thaliana

Elena Salvi, Jacob Pieter Rutten, Riccardo Di Mambro, Laura Polverari, Valerio Licursi, Rodolfo Negri, Raffaele Dello Ioio, Sabrina Sabatini^*, Kirsten Ten Tusscher

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

During organogenesis, coherent organ growth arises from spatiotemporally coordinated decisions of individual cells. In the root of Arabidopsis thaliana, this coordination results in the establishment of a division and a differentiation zone. Cells continuously move through these zones; thus, a major question is how the boundary between these domains, the transition zone, is formed and maintained. By combining molecular genetics with computational modeling, we reveal how an auxin/PLETHORA/ARR-B network controls these dynamic patterning processes. We show that after germination, cell division causes a drop in distal PLT2 levels that enables transition zone formation and ARR12 activation. The resulting PLT2-ARR12 antagonism controls expansion of the division zone (the meristem). The successive ARR1 activation antagonizes PLT2 through inducing the cell-cycle repressor KRP2, thus setting final meristem size. Our work indicates a key role for the interplay between cell division dynamics and regulatory networks in root zonation and transition zone patterning.

Original language	English
Pages (from-to)	431-443.e23
Number of pages	37
Journal	Developmental Cell
Volume	53
Issue number	4
DOIs	https://doi.org/10.1016/j.devcel.2020.04.004
Publication status	Published - 18 May 2020

Funding

We thank Noemi Svolacchia, Gaia Bertolotti, Emanuela Pierdonati, and Elena Pacifici for technical support and Thea van den Berg for reading the manuscript and helpful discussions. We also thank Renze Heidstra, Ari Pekka Mähönen, Lieven De Veylder, and Walter Dewitte for providing material. The ChIP-seq data have been deposited in the NCBI Gene Expression Omnibus under GEO: GSE134695 . This work was supported by the European Research Council grant number 260368 (to S.S. and E.S.), the Company of Biologists Limited grant number DEVTF-170510 (to E.S.), and the NWO (Dutch Organization for Scientific Research) grant number 864.14.009 (to J.R. and K.T.T.).

Keywords

cell differentiation
cell division
computational modeling
cytokinin
organ growth
PLETHORAs
root development

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10.1016/j.devcel.2020.04.004

1-s2.0-S1534580720302719-mainFinal published version, 5.92 MBLicence: Taverne

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title = "A Self-Organized PLT/Auxin/ARR-B Network Controls the Dynamics of Root Zonation Development in Arabidopsis thaliana",

abstract = "During organogenesis, coherent organ growth arises from spatiotemporally coordinated decisions of individual cells. In the root of Arabidopsis thaliana, this coordination results in the establishment of a division and a differentiation zone. Cells continuously move through these zones; thus, a major question is how the boundary between these domains, the transition zone, is formed and maintained. By combining molecular genetics with computational modeling, we reveal how an auxin/PLETHORA/ARR-B network controls these dynamic patterning processes. We show that after germination, cell division causes a drop in distal PLT2 levels that enables transition zone formation and ARR12 activation. The resulting PLT2-ARR12 antagonism controls expansion of the division zone (the meristem). The successive ARR1 activation antagonizes PLT2 through inducing the cell-cycle repressor KRP2, thus setting final meristem size. Our work indicates a key role for the interplay between cell division dynamics and regulatory networks in root zonation and transition zone patterning.",

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author = "Elena Salvi and Rutten, {Jacob Pieter} and {Di Mambro}, Riccardo and Laura Polverari and Valerio Licursi and Rodolfo Negri and {Dello Ioio}, Raffaele and Sabrina Sabatini and {Ten Tusscher}, Kirsten",

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AU - Salvi, Elena

AU - Rutten, Jacob Pieter

AU - Di Mambro, Riccardo

AU - Polverari, Laura

AU - Licursi, Valerio

AU - Negri, Rodolfo

AU - Dello Ioio, Raffaele

AU - Sabatini, Sabrina

AU - Ten Tusscher, Kirsten

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N2 - During organogenesis, coherent organ growth arises from spatiotemporally coordinated decisions of individual cells. In the root of Arabidopsis thaliana, this coordination results in the establishment of a division and a differentiation zone. Cells continuously move through these zones; thus, a major question is how the boundary between these domains, the transition zone, is formed and maintained. By combining molecular genetics with computational modeling, we reveal how an auxin/PLETHORA/ARR-B network controls these dynamic patterning processes. We show that after germination, cell division causes a drop in distal PLT2 levels that enables transition zone formation and ARR12 activation. The resulting PLT2-ARR12 antagonism controls expansion of the division zone (the meristem). The successive ARR1 activation antagonizes PLT2 through inducing the cell-cycle repressor KRP2, thus setting final meristem size. Our work indicates a key role for the interplay between cell division dynamics and regulatory networks in root zonation and transition zone patterning.

AB - During organogenesis, coherent organ growth arises from spatiotemporally coordinated decisions of individual cells. In the root of Arabidopsis thaliana, this coordination results in the establishment of a division and a differentiation zone. Cells continuously move through these zones; thus, a major question is how the boundary between these domains, the transition zone, is formed and maintained. By combining molecular genetics with computational modeling, we reveal how an auxin/PLETHORA/ARR-B network controls these dynamic patterning processes. We show that after germination, cell division causes a drop in distal PLT2 levels that enables transition zone formation and ARR12 activation. The resulting PLT2-ARR12 antagonism controls expansion of the division zone (the meristem). The successive ARR1 activation antagonizes PLT2 through inducing the cell-cycle repressor KRP2, thus setting final meristem size. Our work indicates a key role for the interplay between cell division dynamics and regulatory networks in root zonation and transition zone patterning.

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KW - cell division

KW - computational modeling

KW - cytokinin

KW - organ growth

KW - PLETHORAs

KW - root development

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JF - Developmental Cell

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ER -

A Self-Organized PLT/Auxin/ARR-B Network Controls the Dynamics of Root Zonation Development in Arabidopsis thaliana

Abstract

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Keywords

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