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

被引:101
作者
Peret, Benjamin [1 ,2 ,3 ]
Middleton, Alistair M. [1 ,2 ,4 ]
French, Andrew P. [1 ,2 ]
Larrieu, Antoine [1 ,2 ]
Bishopp, Anthony [1 ,2 ,5 ]
Njo, Maria [6 ,7 ]
Wells, Darren M. [1 ,2 ]
Porco, Silvana [1 ,2 ]
Mellor, Nathan [1 ,2 ]
Band, Leah R. [1 ,2 ,4 ]
Casimiro, Ilda [8 ]
Kleine-Vehn, Juergen [6 ,7 ]
Vanneste, Steffen [6 ,7 ]
Sairanen, Ilkka [9 ]
Mallet, Romain [1 ,2 ]
Sandberg, Goran [10 ]
Ljung, Karin [9 ]
Beeckman, Tom [6 ,7 ]
Benkova, Eva [6 ,7 ]
Friml, Jiri [6 ,7 ]
Kramer, Eric [11 ]
King, John R. [1 ,4 ]
De Smet, Ive [2 ,6 ,7 ]
Pridmore, Tony [1 ]
Owen, Markus [1 ,4 ]
Bennett, Malcolm J. [1 ,2 ]
机构
[1] Univ Nottingham, Ctr Plant Integrat Biol, Loughborough LE12 5RD, Leics, England
[2] Univ Nottingham, Sch Biosci, Div Plant & Crop Sci, Loughborough LE12 5RD, Leics, England
[3] Aix Marseille Univ, CNRS, Commissariat Energie Atom & Energies Alternat, Lab Biol Dev Plantes,UMR 7265, St Paul Les Durance, France
[4] Univ Nottingham, Ctr Math Med & Biol, Sch Math Sci, Nottingham NG7 2RD, England
[5] Univ Helsinki, Inst Biotechnol, Dept Biosci, Helsinki, Finland
[6] Flanders Inst Biotechnol, Dept Plant Syst Biol, Ghent, Belgium
[7] Univ Ghent, Dept Plant Biotechnol & Genet, B-9000 Ghent, Belgium
[8] Univ Extremadura, Fac Ciencias, Badajoz, Spain
[9] Swedish Univ Agr Sci, Umea Plant Sci Ctr, Dept Forest Genet & Plant Physiol, S-90183 Umea, Sweden
[10] Umea Univ, Dept Plant Physiol, Umea Plant Sci Ctr, S-90187 Umea, Sweden
[11] Simons Rock Coll, Dept Phys, Great Barrington, MA USA
基金
英国生物技术与生命科学研究理事会; 英国工程与自然科学研究理事会; 瑞典研究理事会;
关键词
3D modelling; auxin transport; lateral root emergence; ODE; ARABIDOPSIS-THALIANA; SYSTEM ARCHITECTURE; TRANSPORT; GENE; GROWTH; BIOSYNTHESIS; INITIATION; SIGNAL; SITES; ARF19;
D O I
10.1038/msb.2013.43
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
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.
引用
收藏
页数:15
相关论文
共 33 条
[1]   Requirement of B2-type cyclin-dependent kinases for meristem integrity in Arabidopsis thaliana [J].
Andersen, Stig Uggerhoj ;
Buechel, Sabine ;
Zhao, Zhong ;
Ljung, Karin ;
Novak, Ondrej ;
Busch, Wolfgang ;
Schuster, Christoph ;
Lohmann, Jan U. .
PLANT CELL, 2008, 20 (01) :88-100
[2]   Local, efflux-dependent auxin gradients as a common module for plant organ formation [J].
Benková, E ;
Michniewicz, M ;
Sauer, M ;
Teichmann, T ;
Seifertová, D ;
Jürgens, G ;
Friml, J .
CELL, 2003, 115 (05) :591-602
[3]   The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots [J].
Blilou, I ;
Xu, J ;
Wildwater, M ;
Willemsen, V ;
Paponov, I ;
Friml, J ;
Heidstra, R ;
Aida, M ;
Palme, K ;
Scheres, B .
NATURE, 2005, 433 (7021) :39-44
[4]   Mechanical induction of lateral root initiation in Arabidopsis thaliana [J].
Ditengou, Franck Anicet ;
Tealea, William D. ;
Kochersperger, Philip ;
Flittner, Karl Andreas ;
Kneuper, Irina ;
van der Graaff, Eric ;
Nziengui, Hugues ;
Pinosa, Francesco ;
Li, Xugang ;
Nitschke, Roland ;
Laux, Thomas ;
Palme, Klaus .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2008, 105 (48) :18818-18823
[5]  
Frey PJF, 2001, MEDIT 3 0 INTERACTIV
[6]   Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis [J].
Friml, J ;
Wisniewska, J ;
Benkova, E ;
Mendgen, K ;
Palme, K .
NATURE, 2002, 415 (6873) :806-809
[7]   Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis [J].
Fukaki, H ;
Tameda, S ;
Masuda, H ;
Tasaka, M .
PLANT JOURNAL, 2002, 29 (02) :153-168
[8]   Auxin transport is sufficient to generate a maximum and gradient guiding root growth [J].
Grieneisen, Veronica A. ;
Xu, Jian ;
Maree, Athanasius F. M. ;
Hogeweg, Paulien ;
Scheres, Ben .
NATURE, 2007, 449 (7165) :1008-1013
[9]   Developmental Patterning by Mechanical Signals in Arabidopsis [J].
Hamant, Olivier ;
Heisler, Marcus G. ;
Jonsson, Henrik ;
Krupinski, Pawel ;
Uyttewaal, Magalie ;
Bokov, Plamen ;
Corson, Francis ;
Sahlin, Patrik ;
Boudaoud, Arezki ;
Meyerowitz, Elliot M. ;
Couder, Yves ;
Traas, Jan .
SCIENCE, 2008, 322 (5908) :1650-1655
[10]   Building blocks for plant gene assembly [J].
Karimi, Mansour ;
Bleys, Annick ;
Vanderhaeghen, Rudy ;
Hilson, Pierre .
PLANT PHYSIOLOGY, 2007, 145 (04) :1183-1191