Sequential induction of auxin efflux and influx carriers regulates lateral root emergence
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 separ...
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| Format: | Article |
| Language: | English |
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Springer Nature
2013-10-01
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| Series: | Molecular Systems Biology |
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| Online Access: | https://doi.org/10.1038/msb.2013.43 |
| _version_ | 1826990447458779136 |
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| author | Benjamin Péret Alistair M Middleton Andrew P French Antoine Larrieu Anthony Bishopp Maria Njo Darren M Wells Silvana Porco Nathan Mellor Leah R Band Ilda Casimiro Jürgen Kleine‐Vehn Steffen Vanneste Ilkka Sairanen Romain Mallet Göran Sandberg Karin Ljung Tom Beeckman Eva Benkova Jiří Friml Eric Kramer John R King Ive De Smet Tony Pridmore Markus Owen Malcolm J Bennett |
| author_facet | Benjamin Péret Alistair M Middleton Andrew P French Antoine Larrieu Anthony Bishopp Maria Njo Darren M Wells Silvana Porco Nathan Mellor Leah R Band Ilda Casimiro Jürgen Kleine‐Vehn Steffen Vanneste Ilkka Sairanen Romain Mallet Göran Sandberg Karin Ljung Tom Beeckman Eva Benkova Jiří Friml Eric Kramer John R King Ive De Smet Tony Pridmore Markus Owen Malcolm J Bennett |
| author_sort | Benjamin Péret |
| collection | DOAJ |
| description | 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. |
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| format | Article |
| id | doaj.art-77b50fa5cb9845698b84b27f3678feda |
| institution | Directory Open Access Journal |
| issn | 1744-4292 |
| language | English |
| last_indexed | 2025-02-18T08:20:41Z |
| publishDate | 2013-10-01 |
| publisher | Springer Nature |
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| series | Molecular Systems Biology |
| spelling | doaj.art-77b50fa5cb9845698b84b27f3678feda2024-11-03T12:55:50ZengSpringer NatureMolecular Systems Biology1744-42922013-10-019111510.1038/msb.2013.43Sequential induction of auxin efflux and influx carriers regulates lateral root emergenceBenjamin Péret0Alistair M Middleton1Andrew P French2Antoine Larrieu3Anthony Bishopp4Maria Njo5Darren M Wells6Silvana Porco7Nathan Mellor8Leah R Band9Ilda Casimiro10Jürgen Kleine‐Vehn11Steffen Vanneste12Ilkka Sairanen13Romain Mallet14Göran Sandberg15Karin Ljung16Tom Beeckman17Eva Benkova18Jiří Friml19Eric Kramer20John R King21Ive De Smet22Tony Pridmore23Markus Owen24Malcolm J Bennett25Centre for Plant Integrative Biology, University of NottinghamCentre for Plant Integrative Biology, University of NottinghamCentre for Plant Integrative Biology, University of NottinghamCentre for Plant Integrative Biology, University of NottinghamCentre for Plant Integrative Biology, University of NottinghamDepartment of Plant Systems Biology, Flanders Institute for BiotechnologyCentre for Plant Integrative Biology, University of NottinghamCentre for Plant Integrative Biology, University of NottinghamCentre for Plant Integrative Biology, University of NottinghamCentre for Plant Integrative Biology, University of NottinghamUniversidad de Extremadura, Facultad de CienciasDepartment of Plant Systems Biology, Flanders Institute for BiotechnologyDepartment of Plant Systems Biology, Flanders Institute for BiotechnologyDepartment of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural SciencesCentre for Plant Integrative Biology, University of NottinghamDepartment of Plant Physiology, Umeå Plant Science Centre, Umeå UniversityDepartment of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural SciencesDepartment of Plant Systems Biology, Flanders Institute for BiotechnologyDepartment of Plant Systems Biology, Flanders Institute for BiotechnologyDepartment of Plant Systems Biology, Flanders Institute for BiotechnologyPhysics Department, Simon's Rock CollegeCentre for Plant Integrative Biology, University of NottinghamDivision of Plant and Crop Sciences, School of Biosciences, University of NottinghamCentre for Plant Integrative Biology, University of NottinghamCentre for Plant Integrative Biology, University of NottinghamCentre for Plant Integrative Biology, University of NottinghamAbstract 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.https://doi.org/10.1038/msb.2013.433D modellingauxin transportlateral root emergenceODE |
| spellingShingle | Benjamin Péret Alistair M Middleton Andrew P French Antoine Larrieu Anthony Bishopp Maria Njo Darren M Wells Silvana Porco Nathan Mellor Leah R Band Ilda Casimiro Jürgen Kleine‐Vehn Steffen Vanneste Ilkka Sairanen Romain Mallet Göran Sandberg Karin Ljung Tom Beeckman Eva Benkova Jiří Friml Eric Kramer John R King Ive De Smet Tony Pridmore Markus Owen Malcolm J Bennett Sequential induction of auxin efflux and influx carriers regulates lateral root emergence Molecular Systems Biology 3D modelling auxin transport lateral root emergence ODE |
| 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 |
| topic | 3D modelling auxin transport lateral root emergence ODE |
| url | https://doi.org/10.1038/msb.2013.43 |
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