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

B. Péret, A. Middleton, A. French, A. Larrieu, A. Bishopp, M. Njo, D. Wells, S. Porco, N. Mellor, L. Band, I. Casimiro, J. Kleine Vehn, S. Vanneste, I. Sairanen, R. Mallet, G. Sandberg, K. Ljung, T. Beeckman, E. Benková, J. Friml, E. Kramer, J. King, I. De Smet, T. Pridmore, M. Owen, M. Bennett, Molecular Systems Biology 9 (2013).

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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.
Publishing Year
Date Published
2013-10-22
Journal Title
Molecular Systems Biology
Acknowledgement
This work was supported by an FEBS Long‐Term Fellowship (BP), an Intra‐European Fellowship for Career Development under the 7th framework of the European Commission (IEF‐2008‐220506 to BP), an EMBO Long‐Term Fellowship (BP), an European Reintegration Grant under the 7th framework of the European Commission (ERG‐2010‐276662 to BP) and the Swedish Research Council (VR 621‐2010‐5720 to IS, GS and KL). AMM, APF, AL, LRB, SP, NM, DMW, MO, JRK and MJB acknowledge the support of the Biotechnology and Biological Sciences Research Council (BBSRC) and Engineering and Physical Sciences Research Council (EPSRC) funding to the Centre for Plant Integrative Biology (CPIB); BBSRC Professorial Research Fellowship funding to DMW and MJB; Belgian Scientific policy (BELSPO contract MARS) to TB and MJB. We thank Bert de Rybel for his help in Multisite Gateway cloning.
Volume
9
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Péret B, Middleton A, French A, et al. Sequential induction of auxin efflux and influx carriers regulates lateral root emergence. Molecular Systems Biology. 2013;9. doi:10.1038/msb.2013.43
Péret, B., Middleton, A., French, A., Larrieu, A., Bishopp, A., Njo, M., … Bennett, M. (2013). Sequential induction of auxin efflux and influx carriers regulates lateral root emergence. Molecular Systems Biology, 9. https://doi.org/10.1038/msb.2013.43
Péret, Benjamin, Alistair Middleton, Andrew French, Antoine Larrieu, Anthony Bishopp, Maria Njo, Darren Wells, et al. “Sequential Induction of Auxin Efflux and Influx Carriers Regulates Lateral Root Emergence.” Molecular Systems Biology 9 (2013). https://doi.org/10.1038/msb.2013.43.
B. Péret et al., “Sequential induction of auxin efflux and influx carriers regulates lateral root emergence,” Molecular Systems Biology, vol. 9, 2013.
Péret B, Middleton A, French A, Larrieu A, Bishopp A, Njo M, Wells D, Porco S, Mellor N, Band L, Casimiro I, Kleine Vehn J, Vanneste S, Sairanen I, Mallet R, Sandberg G, Ljung K, Beeckman T, Benková E, Friml J, Kramer E, King J, De Smet I, Pridmore T, Owen M, Bennett M. 2013. Sequential induction of auxin efflux and influx carriers regulates lateral root emergence. Molecular Systems Biology. 9.
Péret, Benjamin, et al. “Sequential Induction of Auxin Efflux and Influx Carriers Regulates Lateral Root Emergence.” Molecular Systems Biology, vol. 9, Nature Publishing Group, 2013, doi:10.1038/msb.2013.43.

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