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Sequential induction of auxin efflux and influx carriers regulates lateral root emergence

Peret, Benjamin; Middleton, Alistair M.; French, Andrew P.; Larrieu, Antoine; Bishopp, Antony; Njo, Maria; Wells, Darren M.; Porco, Silvana; Mellor, Nathan.; Band, Leah R.; Casimiro, Ilda; Kleine-Vehn, Jurgen; Vanneste, Steffen; Sairanen, Ilkka; Mallet, Romain; Sandberg, Goran; Ljung, Karin; Beeckman, Tom; Benkova, Eva; Friml, Jiri; Kramer, Eric; King, John R.; De Smet, Ive; Pridmore, Tony; Owen, Markus R.; Bennett, Malcolm J.

Authors

Benjamin Peret

Alistair M. Middleton

Andrew P. French andrew.p.french@nottingham.ac.uk

Antoine Larrieu

Antony Bishopp

Maria Njo

Darren M. Wells

Silvana Porco

Nathan. Mellor

Leah R. Band

Ilda Casimiro

Jurgen Kleine-Vehn

Steffen Vanneste

Ilkka Sairanen

Romain Mallet

Goran Sandberg

Karin Ljung

Tom Beeckman

Eva Benkova

Jiri Friml

Eric Kramer

John R. King

Ive De Smet

Tony Pridmore

Markus R. Owen Markus.Owen@nottingham.ac.uk

Malcolm J. Bennett

Abstract

In Arabidopsis, lateral roots originate from pericycle cells deep within the primary root. New lateral root primordia (LRP) have to emerge through several overlaying tissues. Here, we report that auxin produced in new LRP is transported towards the outer tissues where it triggers cell separation by inducing both the auxin influx carrier LAX3 and cell‐wall enzymes. LAX3 is expressed in just two cell files overlaying new LRP. To understand how this striking pattern of LAX3 expression is regulated, we developed a mathematical model that captures the network regulating its expression and auxin transport within realistic three‐dimensional cell and tissue geometries. Our model revealed that, for the LAX3 spatial expression to be robust to natural variations in root tissue geometry, an efflux carrier is required—later identified to be PIN3. To prevent LAX3 from being transiently expressed in multiple cell files, PIN3 and LAX3 must be induced consecutively, which we later demonstrated to be the case. Our study exemplifies how mathematical models can be used to direct experiments to elucidate complex developmental processes.

Journal Article Type Article
Publication Date Oct 22, 2013
Journal Molecular Systems Biology
Electronic ISSN 1744-4292
Publisher Wiley
Peer Reviewed Peer Reviewed
Volume 9
Issue 1
Article Number 699
DOI https://doi.org/10.1038/msb.2013.43
Publisher URL http://msb.embopress.org/content/9/1/699
Copyright Statement Copyright information regarding this work can be found at the following address: http://creativecommons.org/licenses/by/4.0

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