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

Molecular Systems Biology

Volumn 9, Issue , 2013, Pages

  Péret, Benjamin ^a,b   Middleton, Alistair M ^a,j   French, Andrew P ^a   Larrieu, Antoine ^a   Bishopp, Anthony ^a,c   Njo, Maria ^d,e   Wells, Darren M ^a   Porco, Silvana ^a   Mellor, Nathan ^a   Band, Leah R ^a   Casimiro, Ilda ^f   Kleine Vehn, Jürgen ^d,e   Vanneste, Steffen ^a   Sairanen, Ilkka ^g   Mallet, Romain ^a   Sandberg, Göran ^h   Ljung, Karin ^g   Beeckman, Tom ^d,e   Benkova, Eva ^d,e   Friml, Jiří ^d,e   Kramer, Eric ⁱ   King, John R ^a   De Smet, Ive ^a,d,e   Pridmore, Tony ^a   Owen, Markus ^a   Bennett, Malcolm J ^a   more..

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b University of Aix Marseille   (France)

^c UNIVERSITY OF HELSINKI   (Finland)

^d DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^e GHENT UNIVERSITY   (Belgium)

^f UNIVERSITY OF EXTREMADURA   (Spain)

^g SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^h UMEÅ UNIVERSITY   (Sweden)

ⁱ Simon's Rock College   (United States)

^j UNIVERSITY OF HEIDELBERG   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

AUXIN; CARRIER PROTEIN; LAX3 PROTEIN; PIN3 PROTEIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; ARABIDOPSIS PROTEIN; INDOLEACETIC ACID DERIVATIVE; LAX3 PROTEIN, ARABIDOPSIS; PIN3 PROTEIN, ARABIDOPSIS;

ARTICLE; AUXIN TRANSPORT; CELL SEPARATION; CONTROLLED STUDY; LATERAL ROOT PRIMORDIA; MATHEMATICAL MODEL; NONHUMAN; PLANT ROOT; PRIORITY JOURNAL; PROTEIN EXPRESSION; CELL WALL; GEOMETRY; PLANT TISSUE; PRIMORDIUM; ANTIBODY SPECIFICITY; ARABIDOPSIS; BIOLOGICAL MODEL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; SIGNAL TRANSDUCTION; TRANSPORT AT THE CELLULAR LEVEL;

ARABIDOPSIS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL TRANSPORT; CELL WALL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; INDOLEACETIC ACIDS; MEMBRANE TRANSPORT PROTEINS; MODELS, GENETIC; ORGAN SPECIFICITY; PLANT ROOTS; SIGNAL TRANSDUCTION;

EID: 84886701027     PISSN: None     EISSN: 17444292     Source Type: Journal    
DOI: 10.1038/msb.2013.43     Document Type: Article

References (33)

1. Andersen SU, Buechel S, Zhao Z, Ljung K, Novák O, Busch W, Schuster C, Lohmann JU (2008) Requirement of B2-type cyclindependent kinases for meristem integrity in Arabidopsis thaliana. Plant Cell 20: 88-100 (Pubitemid 352844036)
2. Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Ju?rgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115: 591-602 (Pubitemid 37506047)
3. Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433: 39-44 (Pubitemid 40101136)
4. Ditengou FA, Teale WD, Kochersperger P, Flittner KA, Kneuper I, van der Graaff E, Nziengui H, Pinosa F, Li X, Nitschke R, Laux T, Palme K (2008) Mechanical induction of lateral root initiation in Arabidopsis thaliana. Proc Natl Acad Sci USA 105: 18818-18823
5. Frey PJF (2001) Medit 3.0 interactive mesh visualization software http://www.ann.jussieu.fr/Bfrey/software.html
6. Friml J, Wiśniewska J, Benková E, Mendgen K, Palme K (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415: 806-809 (Pubitemid 34150504)
7. Fukaki H, Tameda S, Masuda H, Tasaka M (2002) Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J 29: 153-168 (Pubitemid 34134693)
8. Grieneisen VA, Xu J, Marée AF, Hogeweg P, Scheres B (2007) Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 449: 1008-1013 (Pubitemid 350014596)
9. Hamant O, Heisler MG, Jo?nsson H, Krupinski P, Uyttewaal M, Bokov P, Corson F, Sahlin P, Boudaoud A, Meyerowitz EM, Couder Y, Traas J (2008) Developmental patterning by mechanical signals in Arabidopsis. Science 322: 1650-1655
10. Karimi M, Bleys A, Vanderhaeghen R, Hilson P (2007) Building blocks for plant gene assembly. Plant Physiol 145: 1183-1191 (Pubitemid 350276737)
11. Karlin-Neumann GA, Brusslan JA, Tobin EM (1991) Phytochrome control of the tms2 gene in transgenic Arabidopsis: A strategy for selecting mutants in the signal transduction pathway. Plant Cell 3: 573-582 (Pubitemid 21913722)
12. Kramer EM (2006) How far can a molecule of weak acid travel in the apoplast or xylem? Plant Physiol 141: 1233-1236 (Pubitemid 44223275)
13. Kramer EM, Frazer NL, Baskin TI (2007) Measurement of diffusion within the cell wall in living roots of Arabidopsis thaliana. J Exp Bot 58: 3005-3015 (Pubitemid 47511756)
14. Kramer EM (2008) Computer models of auxin transport: A review and commentary. J Exp Bot 59: 45-53 (Pubitemid 351598959)
15. Kuppusamy KT, Walcher CL, Nemhauser JL (2009) Cross-regulatory mechanisms in hormone signaling. Plant Mol Biol 69: 375-381
16. Laplaze L, Parizot B, Baker A, Ricaud L, Martinière A, Auguy F, Franche C, Nussaume L, Bogusz D, Haseloff J (2005) GAL4-GFP enhancer trap lines for genetic manipulation of lateral root development in Arabidopsis thaliana. J Exp Bot 56: 2433-2442 (Pubitemid 41191461)
17. Laskowski M, Grieneisen VA, Hofhuis H, Hove CA, Hogeweg P, Marée AF, Scheres B (2008) Root system architecture from coupling cell shape to auxin transport. PLoS Biol 6: e307
18. Ljung K, Bhalerao RP, Sandberg G (2001) Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth. Plant J 28: 465-474 (Pubitemid 34045593)
19. Ljung K, Hull AK, Celenza J, Yamada M, Estelle M, Normanly J, Sandberg G (2005) Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell 17: 1090-1104 (Pubitemid 43142128)
20. Lucas M, Kenobi K, von Wangenheim D, Vo- U, Swarup K, De Smet I, Van Damme D, Lawrence T, Péret B, Moscardi E, Barbeau D, Godin C, Salt D, Guyomarc?h S, Stelzer EHK, Maizel A, Laplaze L, Bennett MJ (2013) Lateral root morphogenesis is dependent on the mechanical properties of the overlaying tissues. Proc Natl Acad Sci USA 110: 5229-5234
21. Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124: 33-44 (Pubitemid 27053004)
22. Marhavý P, Vanstraelen M, De Rybel B, Zhaojun D, Bennett MJ, Beeckman T, Benková E (2013) Auxin reflux between the endodermis and pericycle promotes lateral root initiation. EMBO J 32: 149-158
23. Middleton AM, King JR, Bennett MJ, Owen MR (2010) Mathematical Modelling of the Aux/IAA Negative Feedback Loop. Bull Math Biol 72: 1383-1407
24. Middleton AM, Ú beda-Tomás S, Griffiths J, Holman T, Hedden P, Thomas SG, Phillips AL, Holdsworth MJ, Bennett MJ, King JR, Owen MR (2012) Mathematical modeling elucidates the role of transcriptional feedback in gibberellin signaling. Proc Natl Acad Sci USA 109: 7571-7576
25. Mu? ller A, Guan C, Ga?lweiler L, Ta?nzler P, Huijser P, Marchant A, Parry G, Bennett M, Wisman E, Palme K (1998) AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J 17: 6903-6911 (Pubitemid 28550284)
26. Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19: 118-130 (Pubitemid 46852706)
27. Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Lui A, Nguyen D, Onodera C, Quach H, Smith A, Yu G, Theologis A (2005) Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell 17: 444-463 (Pubitemid 41672967)
28. Péret B, Larrieu A, Bennett MJ (2009) Lateral root emergence: A difficult birth. J Exp Bot 60: 3637-3643
29. Péret B, Swarup R, Jansen L, Devos G, Auguy F, Collin M, Santi C, Hocher V, Franche C, Bogusz D, Bennett M, Laplaze L (2007) Auxin influx activity is associated with Frankia infection during actinorhizal nodule formation in Casuarina glauca. Plant Physiol 144: 1852-1862 (Pubitemid 47260536)
30. Smith S, De Smet I (2012) Root system architecture: Insights from Arabidopsis and cereal crops. Philos Trans R Soc Lond B Biol Sci 367: 1441-1452
31. Swarup K, Benková E, Swarup R, Casimiro I, Péret B, Yang Y, Parry G, Nielsen E, De Smet I, Vanneste S, Levesque MP, Carrier D, James N, Calvo V, Ljung K, Kramer E, Roberts R, Graham N, Marillonnet S, Patel K et al (2008) The auxin influx carrier LAX3 promotes lateral root emergence. Nat Cell Biol 10: 946-954
32. Swarup R, Kramer EM, Perry P, Knox K, Leyser HM, Haseloff J, Beemster GT, Bhalerao R, Bennett MJ (2005) Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nat Cell Biol 7: 1057-1065
33. Udvardi MK, Czechowski T, ScheibleWR(2008) Eleven golden rules of quantitative RT-PCR. Plant Cell 20: 1736