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

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...

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Main Authors: 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.
Format: Article
Published: Nature Publishing Group 2013
Online Access:https://eprints.nottingham.ac.uk/2941/
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author 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.
author_facet 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.
author_sort Peret, Benjamin
building Nottingham Research Data Repository
collection Online Access
description 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.
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spelling nottingham-29412020-05-04T16:39:16Z https://eprints.nottingham.ac.uk/2941/ 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. 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. Nature Publishing Group 2013-10-22 Article PeerReviewed 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. and Bennett, Malcolm J. (2013) Sequential induction of auxin efflux and influx carriers regulates lateral root emergence. Molecular Systems Biology, 9 (1). 699/1-699/15. ISSN 1744-4292 http://msb.embopress.org/content/9/1/699 doi:10.1038/msb.2013.43 doi:10.1038/msb.2013.43
spellingShingle 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.
Sequential induction of auxin efflux and influx carriers regulates lateral root emergence
title Sequential induction of auxin efflux and influx carriers regulates lateral root emergence
title_full Sequential induction of auxin efflux and influx carriers regulates lateral root emergence
title_fullStr Sequential induction of auxin efflux and influx carriers regulates lateral root emergence
title_full_unstemmed Sequential induction of auxin efflux and influx carriers regulates lateral root emergence
title_short Sequential induction of auxin efflux and influx carriers regulates lateral root emergence
title_sort sequential induction of auxin efflux and influx carriers regulates lateral root emergence
url https://eprints.nottingham.ac.uk/2941/
https://eprints.nottingham.ac.uk/2941/
https://eprints.nottingham.ac.uk/2941/