Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW

Hormone signalling and root development: an update on the latest Arabidopsis thaliana research

Jose Manuel Perez-Perez
+ Author Affiliations
- Author Affiliations

Division de Genetica and Instituto de Bioingenieria, Universidad Miguel Hernandez, Edificio Vinalopo, Avda. de la Universidad s/n, 03202 Elche (Alicante), Spain. Email: jmperez@umh.es

Functional Plant Biology 34(3) 163-171 https://doi.org/10.1071/FP06341
Submitted: 27 December 2006  Accepted: 23 February 2007   Published: 22 March 2007

Abstract

Plants are sessile organisms whose developmental programs depend mainly on environmental cues that are sensed and interpreted through hormonal signalling pathways. Roots are specialised plant organs that are instrumental during water and nutrient uptake, biotic interactions, stress responses and for mechanical support. Our knowledge about the basic molecular events shaping root patterning and growth has advanced significantly in the past few years thanks to the use of Arabidopsis thaliana (L.) Heynh. as a model system. In this review, I will discuss recent findings that indicate crosstalk between growth regulators and hormone signalling pathways during primary root development. Further comparative research using non-model species will shed light on the conserved developmental modules among distant lineages involved in root architecture.

Additional keywords: cell fate, hormone crosstalk, pattern formation, signal transduction, transcription factor.


Acknowledgements

I thank Ari Pekka Mahonen, Ben Scheres and two anonymous referees for their suggestions to improve the manuscript. Thanks to the Spanish Ministry of Science and Education (MEC) for funding. JMP-P. holds a ‘Juan de la Cierva’ research contract at the Universidad Miguel Hernandez (UMH).


References


Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van Der Straeten D, Peng J, Harberd NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311, 91–94.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh YS, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119, 109–120.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Altmann T (1998) Recent advances in brassinosteroid molecular genetics. Current Opinion in Plant Biology 1, 378–383.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Asami T, Nakano T, Fujioka S (2005) Plant brassinosteroid hormones. Vitamins and Hormones 72, 479–504.
PubMed |
open url image1

Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281–297.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Baskin TI (2000) On the constancy of cell division rate in the root meristem. Plant Molecular Biology 43, 545–554.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

van den Berg C, Willemsen V, Hendriks G, Weisbeek P, Scheres B (1997) Short-range control of cell differentiation in the Arabidopsis root meristem. Nature 390, 287–289.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Birnbaum K, Benfey PN (2004) Network building: transcriptional circuits in the root. Current Opinion in Plant Biology 7, 582–588.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Birnbaum K, Shasha DE, Wang JY, Jung JW, Lambert GM, Galbraith DW, Benfey PN (2003) A gene expression map of the Arabidopsis root. Science 302, 1956–1960.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Blakeslee JJ, Peer WA, Murphy AS (2005) Auxin transport. Current Opinion in Plant Biology 8, 494–500.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bonke M, Thitamadee S, Mahonen AP, Hauser MT, Helariutta Y (2003) APL regulates vascular tissue identity in Arabidopsis. Nature 426, 181–186.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Carlsbecker A, Helariutta Y (2005) Phloem and xylem specification: pieces of the puzzle emerge. Current Opinion in Plant Biology 8, 512–517.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang H, Casero P, Sandberg G, Bennett MJ (2003) Dissecting Arabidopsis lateral root development. Trends in Plant Science 8, 165–171.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chavarria-Krauser C, Jager W, Schurr U (2005) Primary root growth: a biophysical model of auxin-related control. Functional Plant Biology 32, 849–862.
Crossref | GoogleScholarGoogle Scholar | open url image1

De Smet I, Vanneste S, Inze D, Beeckman T (2006) Lateral root initiation or the birth of a new meristem. Plant Molecular Biology 60, 871–887.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ferreira FJ, Kieber JJ (2005) Cytokinin signaling. Current Opinion in Plant Biology 8, 518–525.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Franco-Zorrilla JM, Martin AC, Solano R, Rubio V, Leyva A, Paz-Ares J (2002) Mutations at CRE1 impair cytokinin-induced repression of phosphate starvation responses in Arabidopsis. The Plant Journal 32, 353–360.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Franco-Zorrilla JM, Gonzalez E, Bustos R, Linhares F, Leyva A, Paz-Ares J (2004) The transcriptional control of plant responses to phosphate limitation. Journal of Experimental Botany 55, 285–293.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Franco-Zorrilla JM, Martin AC, Leyva A, Paz-Ares J (2005) Interaction between phosphate-starvation, sugar, and cytokinin signaling in Arabidopsis and the roles of cytokinin receptors CRE1/AHK4 and AHK3. Plant Physiology 138, 847–857.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Frigerio M, Alabadi D, Perez-Gomez J, Garcia-Carcel L, Phillips AL, Hedden P, Blazquez MA (2006) Transcriptional regulation of gibberellin metabolism genes by auxin signaling in Arabidopsis. Plant Physiology 142, 553–563.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jurgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426, 147–153.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421, 740–743.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fukuda H (2004) Signals that control plant vascular cell differentiation. Nature Reviews. Molecular Cell Biology 5, 379–391.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Haecker A, Gross-Hardt R, Geiges B, Sarkar A, Breuninger H, Herrmann M, Laux T (2004) Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131, 657–668.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Halliday KJ (2004) Plant hormones: the interplay of brassinosteroids and auxin. Current Biology 14, R1008–R1010.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hamann T, Benkova E, Baurle I, Kientz M, Jurgens G (2002) The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes & Development 16, 1610–1615.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hardtke CS (2006) Root development–branching into novel spheres. Current Opinion in Plant Biology 9, 66–71.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hardtke CS, Ckurshumova W, Vidaurre DP, Singh SA, Stamatiou G, Tiwari SB, Hagen G, Guilfoyle TJ, Berleth T (2004) Overlapping and non-redundant functions of the Arabidopsis auxin response factors MONOPTEROS and NONPHOTOTROPIC HYPOCOTYL 4. Development 131, 1089–1100.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Higuchi M, Pischke MS, Mahonen AP, Miyawaki K, Hashimoto Y , et al. (2004) In planta functions of the Arabidopsis cytokinin receptor family. Proceedings of the National Academy of Sciences USA 101, 8821–8826.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jiang K, Feldman LJ (2005) Regulation of root apical meristem development. Annual Review of Cell and Developmental Biology 21, 485–509.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kakimoto T (2003) Perception and signal transduction of cytokinins. Annual Review of Plant Biology 54, 605–627.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Koornneef M, Alonso-Blanco C, Vreugdenhil D (2004) Naturally occurring genetic variation in Arabidopsis thaliana. Annual Review of Plant Biology 55, 141–172.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kramer EM, Bennett MJ (2006) Auxin transport: a field in flux. Trends in Plant Science 11, 382–386.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Laux T, Wurschum T, Breuninger H (2004) Genetic regulation of embryonic pattern formation. The Plant Cell 16, S190–S202.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lee JY, Colinas J, Wang JY, Mace D, Ohler U, Benfey PN (2006) Transcriptional and posttranscriptional regulation of transcription factor expression in Arabidopsis roots. Proceedings of the National Academy of Sciences USA 103, 6055–6060.
Crossref | GoogleScholarGoogle Scholar | open url image1

Leibfried A, To JP, Busch W, Stehling S, Kehle A, Demar M, Kieber JJ, Lohmann JU (2005) WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature 438, 1172–1175.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Levesque MP, Vernoux T, Busch W, Cui H, Wang JY , et al. (2006) Whole-genome analysis of the SHORT-ROOT developmental pathway in Arabidopsis. PLoS Biology 4, e143.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lopez-Bucio J, Cruz-Ramirez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Current Opinion in Plant Biology 6, 280–287.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lopez-Bucio J, Hernandez-Abreu E, Sanchez-Calderon L, Perez-Torres A, Rampey RA, Bartel B, Herrera-Estrella L (2005) An auxin transport independent pathway is involved in phosphate stress-induced root architectural alterations in Arabidopsis. Identification of BIG as a mediator of auxin in pericycle cell activation. Plant Physiology 137, 681–691.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mahonen AP, Bonke M, Kauppinen L, Riikonen M, Benfey PN, Helariutta Y (2000) A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes & Development 14, 2938–2943.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mahonen AP, Bishopp A, Higuchi M, Nieminen KM, Kinoshita K, Tormakangas K, Ikeda Y, Oka A, Kakimoto T, Helariutta Y (2006a) Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science 311, 94–98.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mahonen AP, Higuchi M, Tormakangas K, Miyawaki K, Pischke MS, Sussman MR, Helariutta Y, Kakimoto T (2006b) Cytokinins regulate a bidirectional phosphorelay network in Arabidopsis. Current Biology 16, 1116–1122.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Malamy JE (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant, Cell & Environment 28, 67–77.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mallory AC, Bartel DP, Bartel B (2005) MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. The Plant Cell 17, 1360–1375.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mok DW, Mok MC (2001) Cytokinin metabolism and action. Annual Review of Plant Physiology and Plant Molecular Biology 52, 89–118.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mouchel CF, Briggs GC, Hardtke CS (2004) Natural genetic variation in Arabidopsis identifies BREVIS RADIX, a novel regulator of cell proliferation and elongation in the root. Genes & Development 18, 700–714.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mouchel CF, Osmont KS, Hardtke CS (2006) BRX mediates feedback between brassinosteroid levels and auxin signalling in root growth. Nature 443, 458–461.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mussig C, Shin GH, Altmann T (2003) Brassinosteroids promote root growth in Arabidopsis. Plant Physiology 133, 1261–1271.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Nacry P, Canivenc G, Muller B, Azmi A, Van Onckelen H, Rossignol M, Doumas P (2005) A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in Arabidopsis. Plant Physiology 138, 2061–2074.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Nakamura A, Goda H, Shimada Y, Yoshida S (2004) Brassinosteroid selectively regulates PIN gene expression in Arabidopsis. Bioscience, Biotechnology, and Biochemistry 68, 952–954.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Nawy T, Lee JY, Colinas J, Wang JY, Thongrod SC, Malamy JE, Birnbaum K, Benfey PN (2005) Transcriptional profile of the Arabidopsis root quiescent center. The Plant Cell 17, 1908–1925.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Nemhauser JL, Mockler TC, Chory J (2004) Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biology 2, E258.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Paciorek T, Friml J (2006) Auxin signaling. Journal of Cell Science 119, 1199–1202.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Paciorek T, Zazimalova E, Ruthardt N, Petrasek J, Stierhof YD , et al. (2005) Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435, 1251–1256.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Paquette AJ, Benfey PN (2005) Maturation of the ground tissue of the root is regulated by gibberellin and SCARECROW and requires SHORT-ROOT. Plant Physiology 138, 636–640.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Parizotto EA, Dunoyer P, Rahm N, Himber C, Voinnet O (2004) In vivo investigation of the transcription, processing, endonucleolytic activity, and functional relevance of the spatial distribution of a plant miRNA. Genes & Development 18, 2237–2242.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rashotte AM, Carson SD, To JP, Kieber JJ (2003) Expression profiling of cytokinin action in Arabidopsis. Plant Physiology 132, 1998–2011.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rashotte AM, Mason MG, Hutchison CE, Ferreira FJ, Schaller GE, Kieber JJ (2006) A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a two-component pathway. Proceedings of the National Academy of Sciences USA 103, 11081–11085.
Crossref | GoogleScholarGoogle Scholar | open url image1

Remington DL, Vision TJ, Guilfoyle TJ, Reed JW (2004) Contrasting modes of diversification in the Aux/IAA and ARF gene families. Plant Physiology 135, 1738–1752.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T , et al. (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99, 463–472.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sabatini S, Heidstra R, Wildwater M, Scheres B (2003) SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes & Development 17, 354–358.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sanchez-Calderon L, Lopez-Bucio J, Chacon-Lopez A, Cruz-Ramirez A, Nieto-Jacobo F, Dubrovsky JG, Herrera-Estrella L (2005) Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant & Cell Physiology 46, 174–184.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Scheres B, Xu J (2006) Polar auxin transport and patterning: grow with the flow. Genes & Development 20, 922–926.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Shimada Y, Goda H, Nakamura A, Takatsuto S, Fujioka S, Yoshida S (2003) Organ-specific expression of brassinosteroid-biosynthetic genes and distribution of endogenous brassinosteroids in Arabidopsis. Plant Physiology 131, 287–297.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Skoog F, Miller CO (1957) Chemical regulation of growth and organ formation in plant tissues cultured in vivo. Symposia Society for Experimental Biology 54, 118–130. open url image1

Stahl Y, Simon R (2005) Plant stem cell niches. International Journal of Developmental Biology 49, 479–489.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Strader LC, Ritchie S, Soule JD, McGinnis KM, Steber CM (2004) Recessive-interfering mutations in the gibberellin signaling gene SLEEPY1 are rescued by overexpression of its homologue, SNEEZY. Proceedings of the National Academy of Sciences USA 101, 12771–12776.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sun TP, Gubler F (2004) Molecular mechanism of gibberellin signaling in plants. Annual Review of Plant Biology 55, 197–223.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Thomas SG, Sun TP (2004) Update on gibberellin signaling. A tale of the tall and the short. Plant Physiology 135, 668–676.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ueda M, Koshino-Kimura Y, Okada K (2005) Stepwise understanding of root development. Current Opinion in Plant Biology 8, 71–76.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wang JW, Wang LJ, Mao YB, Cai WJ, Xue HW, Chen XY (2005) Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis. The Plant Cell 17, 2204–2216.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Weijers D, Jurgens G (2004) Funneling auxin action: specificity in signal transduction. Current Opinion in Plant Biology 7, 687–693.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Weijers D, Benkova E, Jager KE, Schlereth A, Hamann T, Kientz M, Wilmoth JC, Reed JW, Jurgens G (2005) Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators. EMBO Journal 24, 1874–1885.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Weijers D, Schlereth A, Ehrismann JS, Schwank G, Kientz M, Jurgens G (2006) Auxin triggers transient local signaling for cell specification in Arabidopsis embryogenesis. Developmental Cell 10, 265–270.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1