Sequential induction of auxin efflux and influx carriers regulates lateral root emergence. Issue 1 (22nd October 2013)

• Record Type: Journal Article
• Authors: Péret, Benjamin; Middleton, Alistair M; French, Andrew P; Larrieu, Antoine; Bishopp, Anthony; Njo, Maria; Wells, Darren M; Porco, Silvana; Mellor, Nathan; Band, Leah R; Casimiro, Ilda; Kleine‐Vehn, Jürgen; Vanneste, Steffen; Sairanen, Ilkka; Mallet, Romain; Sandberg, Göran; Ljung, Karin; Beeckman, Tom; Benkova, Eva; Friml, Jiří; Kramer, Eric; King, John R; De Smet, Ive; Pridmore, Tony; Owen, Markus; Bennett, Malcolm J
• Is Part Of: Molecular systems biology. Volume 9:Issue 1(2013)
• Page Start: n/a
• Page End: n/a
• Publication Date: 2013-10-22
• Subjects: 3D modelling -- auxin transport -- lateral root emergence -- ODE; Molecular biology -- Periodicals; Systems biology -- Periodicals; 572.8
• DOI: 10.1038/msb.2013.43
• Languages: English
• ISSNs: 1744-4292

Abstract

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. Abstract : Emergence of a new lateral root primordium through the outer layers of the parental root requires the sequential auxin‐mediated induction of two auxin transporters. This positive feedback regulatory loop coordinates patterned gene expression in outer tissues. Synopsis: Emergence of a new lateral root primordium through the outer layers of the parental root requires the sequential auxin‐mediated induction of two auxin transporters. This positive feedback regulatory loop coordinates patterned gene expression in outer tissues. The emergence of lateral roots through several tissues requires the precise regulation of gene expression in overlaying cells to trigger cell separation. Auxin derived from new lateral root primordia induces a positive feedback loop in the outer tissues by promoting the expression of the auxin influx transporter LAX3. A mathematical model based on realistic 3D geometries predicted the involvement of an auxin efflux carrier that was later identified to be PIN3. The model also revealed that PIN3 must be expressed before LAX3 to ensure a 'robust' pattern of LAX3 induction in just two overlaying cortical cell files, thereby delimiting cell separation.