8 Auxin Fuels the Cell Cycle Engine during Lateral Root Initiation
Steffen Vanneste
Department of Plant Systems Biology, Flanders Institute for Biotechnology, and Department of Molecular Genetics, Ghent University, Technologiepark 927, Gent, B-9052 Belgium
Search for more papers by this authorDirk Inzé
Department of Plant Systems Biology, Flanders Institute for Biotechnology, and Department of Molecular Genetics, Ghent University, Technologiepark 927, Gent, B-9052 Belgium
Search for more papers by this authorTom Beeckman
Department of Plant Systems Biology, Flanders Institute for Biotechnology, and Department of Molecular Genetics, Ghent University, Technologiepark 927, Gent, B-9052 Belgium
Search for more papers by this authorSteffen Vanneste
Department of Plant Systems Biology, Flanders Institute for Biotechnology, and Department of Molecular Genetics, Ghent University, Technologiepark 927, Gent, B-9052 Belgium
Search for more papers by this authorDirk Inzé
Department of Plant Systems Biology, Flanders Institute for Biotechnology, and Department of Molecular Genetics, Ghent University, Technologiepark 927, Gent, B-9052 Belgium
Search for more papers by this authorTom Beeckman
Department of Plant Systems Biology, Flanders Institute for Biotechnology, and Department of Molecular Genetics, Ghent University, Technologiepark 927, Gent, B-9052 Belgium
Search for more papers by this authorAbstract
The sections in this article are
- Introduction
- Cell Cycle Regulation during Lateral Root Development
- Stemness of the Xylem-Pole-Associated Pericycle
- Auxin Signalling during Lateral Root Initiation
- Post-Transcriptional Feedback Mechanisms on Auxin Signalling
- Polar Auxin Transport Defines Lateral Root Boundaries
- Cytokinins Inhibit Lateral Root Development
- Brassinosteroids Regulate Auxin Transport
- Light Alters Auxin Sensitivity
- Conclusions and Perspectives
References
- Abas, L., Benjamins, R., Malenica, N., et al. (2006) Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat Cell Biol 8, 249–256.
- Aida, M., Beis, D., Heidstra, R., et al. (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119, 109–120.
- Ang, L.-H., Chattopadhyay, S., Wei, N., et al. (1998) Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol Cell 1, 213–222.
- Bao, F., Shen, J., Brady, S.R., Muday, G.K., Asami, T. and Yang, Z. (2004) Brassinosteroids interact with auxin to promote lateral root development in Arabidopsis. Plant Physiol 134, 1624–1631.
- Beeckman, T., Burssens, S. and Inzé, D. (2001) The peri-cell-cycle in Arabidopsis . J Exp Bot 52, 403–411.
- Benfey, P.N. and Scheres, B. (2000) Root development. Curr Biol 10, R813–R815.
- Benková, E., Michniewicz, M., Sauer, M., et al. (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591–602.
- Blilou, I., Frugier, F., Folmer, S., et al. (2002) The Arabidopsis HOBBIT gene encodes a CDC27 homolog that links the plant cell cycle to progression of cell differentiation. Genes Dev 16, 2566–2575.
- Blilou, I., Xu, J., Wildwater, M., et al. (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433, 39–44.
- Boudolf, V., Barrôco, R., de Almeida Engler, J., et al. (2004a) B1-type cyclin-dependent kinases are essential for the formation of stomatal complexes in Arabidopsis thaliana . Plant Cell 16, 945–955.
- Boudolf, V., Vlieghe, K., Beemster, G.T.S., et al. (2004b) The plant-specific cyclin-dependent kinase CDKB1;1 and transcription factor E2Fa–DPa control the balance of mitotically dividing and endoreduplicating cells in Arabidopsis. Plant Cell 16, 2683–2692.
- Cluis, C.P., Mouchel, C.F. and Hardtke, C.S. (2004) The Arabidopsis transcription factor HY5 integrates light and hormone signaling pathways. Plant J 38, 332–347.
- D'Agostino, I.B., Deruère, J. and Kieber, J.J. (2000) Characterization of the response of the Arabidopsis response regulator gene family to cytokinin. Plant Physiol 124, 1706–1717.
- del Pozo, J.C., Boniotti, M.B. and Gutierrez, C. (2002a) Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin-SCFAtSKP2 pathway in response to light. Plant Cell 14, 3057–3071.
- del Pozo, J.C., Dharmasiri, S., Hellmann, H., Walker, L., Gray, W.M. and Estelle, M. (2002b) AXR1-ECR1-dependent conjugation of RUB1 to the Arabidopsis cullin AtCUL1 is required for auxin response. Plant Cell 14, 421–433.
- De Smet, I., Tetsumura, T., De Rybel, B., et al. (2007) Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis . Development 134, 681–690.
- De Veylder, L., Beeckman, T., Beemster, G.T.S., et al. (2001) Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 13, 1653–1668.
- De Veylder, L., Beeckman, T., Beemster, G.T.S., et al. (2002) Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa/DPa transcription factor. EMBO J 21, 1360–1368.
- Dewitte, W., Riou-Khamlichi, C., Scofield, S., et al. (2003) Altered cell cycle distribution, hyperplasia, and inhibited differentiation in Arabidopsis caused by the D-type cyclin CYCD3. Plant Cell 15, 79–92.
- Dharmasiri, N., Dharmasiri, S. and Estelle, M. (2005a) The F-box protein TIR1 is an auxin receptor. Nature 435, 441–445.
- Dharmasiri, N., Dharmasiri, S., Weijers, D., et al. (2005b) Plant development is regulated by a family of auxin receptor F box proteins. Dev Cell 9, 109–119.
- Dharmasiri, S., Dharmasiri, N., Hellmann, H. and Estelle, M. (2003) The RUB/Nedd8 conjugation pathway is required for early development in Arabidopsis . EMBO J 22, 1762–1770.
- Dittmer, H.J. (1937) A quanitative study of the roots and root root hairs of a winter rye plant (Secale cereale). Am J Bot 24, 417–420.
- Fukaki, H., Nakao, Y., Okushima, Y., Theologis, A. and Tasaka, M. (2005) Tissue-specific expression of stabilized SOLITARY-ROOT/IAA14 alters lateral root development in Arabidopsis. Plant J 44, 382–395.
- Fukaki, H., Tameda, S., Masuda, H. and 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.
- Geldner, N., Richter, S., Vieten, A., et al. (2004) Partial loss-of-function alleles reveal a role for GNOM in auxin transport-related, post-embryonic development of Arabidopsis . Development 131, 389–400.
- Goda, H., Sawa, S., Asami, T., Fujioka, S., Shimada, Y. and Yoshida, S. (2004) Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 134, 1555–1573.
- Gray, W.M., del Pozo, J.C., Walker, L., et al. (1999) Identification of an SCF ubiquitin-ligase complex required for auxin response in Arabidopsis thaliana . Genes Dev 13, 1678–1691.
- Gray, W.M., Kepinski, S., Rouse, D., Leyser, O. and Estelle, M. (2001) Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414, 271–276.
- Gray, W.M., Muskett, P.R., Chuang, H.W. and Parker, J.E. (2003) Arabidopsis SGT1b is required for SCFTIR1-mediated auxin response. Plant Cell 15, 1310–1319.
- Guo, H.S., Xie, Q., Fei, J.F. and Chua, N.-H. (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell 17, 1376–1386.
- Hamann, T., Mayer, U. and Jürgens, G. (1999) The auxin-insensitive bodenlos mutation affects primary root formation and apical-basal patterning in the Arabidopsis embryo. Development 126, 1387–1395.
- Hardtke, C.S., Ckurshumova, W., Vidaurre, D.P., et al. (2004) Overlapping and non-redundant functions of the Arabidopsis auxin response factors MONOPTEROS and NONPHOTOTROPIC HYPOCOTYL 4 . Development 131, 1089–1100.
- Higuchi, M., Pischke, M.S., Mähönen, A.P., et al. (2004) In planta functions of the Arabidopsis cytokinin receptor family. Proc Natl Acad Sci USA 101, 8821–8826.
- Himanen, K., Boucheron, E., Vanneste, S., de Almeida Engler, J., Inzé, D. and Beeckman, T. (2002) Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14, 2339–2351.
- Hosoda, K., Imamura, A., Katoh, E., et al. (2002) Molecular structure of the GARP family of plant Myb-related DNA binding motifs of the Arabidopsis response regulators. Plant Cell 14, 2015–2029.
- Hutchison, C.E., Li, J., Argueso, C., et al. (2006) The Arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. Plant Cell 18, 3073–3087.
- Hwang, I. and Sheen, J. (2001) Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413, 383–389.
- Jönsson, H., Heisler, M.G., Shapiro, B.E., Meyerowitz, E.M. and Mjolsness, E. (2006) An auxin-driven polarized transport model for phyllotaxis. Proc Natl Acad Sci USA 103, 1633–1638.
- Kepinski, S. and Leyser, O. (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435, 446–451.
- Knox, K., Grierson, C.S. and Leyser, O. (2003) AXR3 and SHY2 interact to regulate root hair development. Development 130, 5769–5777.
- Kurihara, Y. and Watanabe, Y. (2004) Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc Natl Acad Sci USA 101, 12753–12758.
- Kurup, S., Runions, J., Köhler, U., Laplaze, L., Hodge, S. and Haseloff, J. (2005) Marking cell lineages in living tissues. Plant J 42, 444–453.
- Laskowski, M.J., Williams, M.E., Nusbaum, H.C. and Sussex, I.M. (1995) Formation of lateral root meristems is a two-stage process. Development 121, 3303–3310.
- Li, L., Xu, J., Xu, Z.-H. and Xue, H.-W. (2005). Brassinosteroids stimulate plant tropisms through modulation of polar auxin transport in Brassica and Arabidopsis . Plant Cell 17, 2738–2753.
- Li, X., Mo, X., Shou, H. and Wu, P. (2006) Cytokinin-mediated cell cycling arrest of pericycle founder cells in lateral root initiation of Arabidopsis . Plant Cell Physiol 47, 1112–1123.
- Li, Y., Hagen, G. and Guilfoyle, T.J. (1992) Altered morphology in transgenic tobacco plants that overproduce cytokinins in specific tissues and organs. Dev Biol 153, 386–395.
- Liscum, E. and Reed, J.W. (2002) Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol Biol 49, 387–400.
- Lohar, D.P., Schaff, J.E., Laskey, J.G., Kieber, J.J., Bilyeu, K.D. and Bird, D.M. (2004) Cytokinins play opposite roles in lateral root formation, and nematode and Rhizobial symbioses. Plant J 38, 203–214.
- Lohrmann, J., Sweere, U., Zabaleta, E., et al. (2001) The response regulator ARR2, a pollen-specific transcription factor involved in the expression of nuclear genes for components of mitochondrial complex I in Arabidopsis . Mol Genet Genomics 265, 2–13.
- Lui, H., Wang, H., DeLong, C., Fowke, L.C., Crosby, W.L. and Fobert, P.R. (2000) The Arabidopsis Cdc2a-interacting protein ICK2 is structurally related to ICK1 and is a potent inhibitor of cyclin-dependent kinase activity in vitro . Plant J 21, 379–385.
- Magyar, Z., De Veylder, L., Atanassova, A., Bako, L., Inzé, D. and Bögre, L. (2005) The role of the Arabidopsis E2FB transcription factor in regulating auxin-dependent cell division. Plant Cell 17, 2527–2541.
- Malamy, J.E. and Benfey, P.N. (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana . Development 124, 33–44.
- Mallory, A.C., Bartel, D.P. and Bartel, B. (2005) MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 17, 1360–1375.
- Mason, M.G., Mathews, D.E., Argyros, D.A., et al. (2005) Multiple type-B response regulators mediate cytokinin signal transduction in Arabidopsis . Plant Cell 17, 3007–3018.
- Mockaitis, K. and Estelle, M. (2004) Integrating transcriptional controls for plant cell expansion. Genome Biol 5, 245.1–245.4.
- Navarro, L., Dunoyer, P., Jay, F., et al. (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312, 436–439.
- Nemhauser, J.L., Mockler, T.C. and Chory, J. (2004) Interdependency of brassinosteroid and auxin signaling in Arabidopsis . PLoS Biol 2, e258.
- Nordström, A., Tarkowski, P., Tarkowska, D., et al. (2004) Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana, a factor of potential importance for auxin – cytokinin-regulated development. Proc Natl Acad Sci USA 101, 8039–8044.
- Okushima, Y., Overvoorde, P.J., Arima, K., et al. (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.
- Osterlund, M.T., Hardtke, C.S., Wei, N. and Deng, X.W. (2000) Targeted destabilization of HY5 during light-regulated development of Arabidopsis . Nature 405, 462–466.
- Overvoorde, P.J., Okushima, Y., Alonso, J.M., et al. (2005) Functional genomic analysis of the AUXIN/INDOLE-3-ACETIC ACID gene family members in Arabidopsis thaliana . Plant Cell 17, 3282–3300.
- Oyama, T., Shimura, Y. and Okada, K. (1997) The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. Genes Dev 11, 2983–2995.
- Parker, G.C., Anastassova-Kristeva, M., Eisenberg, L.M., et al. (2005) Stem cells: shibboleths of development, part II: toward a functional definition. Stem Cells Dev 14, 463–469.
- Petrášek, J., Mravec, J., Bouchard, R., et al. (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312, 914–918.
- Ramos, J.A., Zenser, N., Leyser, O. and Callis, J. (2001) Rapid degradation of auxin/indoleacetic acid proteins requires conserved amino acids of domain II and is proteasome dependent. Plant Cell 13, 2349–2360.
- Rashotte, A.M., Carson, S.D.B., To, J.P.C. and Kieber, J.J. (2003) Expression profiling of cytokinin action in Arabidopsis. Plant Physiol 132, 1998–2011.
- Reinhardt, D. (2005) Phyllotaxis – a new chapter in an old tale about beauty and magic numbers. Curr Opin Plant Biol 8, 487–493.
- Reinhardt, D., Pesce, E.-R., Stieger, P., et al. (2003) Regulation of phyllotaxis by polar auxin transport. Nature 426, 255–260.
- Riefler, M., Novak, O., Strnad, M. and Schmülling, T. (2006) Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18, 40–54.
- Rogg, L.E., Lasswell, J. and Bartel, B. (2001) A gain-of-function mutation in IAA28 suppresses lateral root development. Plant Cell 13, 465–480.
- Rouse, D., Mackay, P., Stirnberg, P., Estelle, M. and Leyser, O. (1998) Changes in auxin response from mutation in an AUX/IAA gene. Science 279, 1371–1373.
- Sabatini, S., Beis, D., Wolkenfelt, H., et al. (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99, 463–472.
- Sakai, H., Honma, T., Aoyama, T., et al. (2001) ARR1, a transcription factor for genes immediately responsive to cytokinins. Science 294, 1519–1521.
- Segers, G., Gadisseur, I., Bergounioux, C., et al. (1996) The Arabidopsis cyclin-dependent kinase gene cdc2bAt is preferentially expressed during S and G2 phases of the cell cycle. Plant J 10, 601–612.
- Shen, W.-H. (2002) The plant E2F–Rb pathway and epigenetic control. Trends Plant Sci 7, 505–511.
- Shostak, S. (2006) (Re)defining stem cells. BioEssays 28, 301–308.
- Sieberer, T., Seifert, G.J., Hauser, M.-T., Grisafi, P., Fink, G.R. and Luschnig, C. (2000) Post-transcriptional control of the Arabidopsis auxin efflux carrier EIR1 requires AXR1. Curr Biol 10, 1595–1598.
- Smith, R.S., Guyomarc'h, S., Mandel, T., Reinhardt, D., Kuhlemeier, C. and Prusinkiewicz, P. (2006) A plausible model of phyllotaxis. Proc Natl Acad Sci USA 103, 1301–1306.
- Sorin, C., Bussell, J.D., Camus, I., et al. (2005) Auxin and light control of adventitious rooting in Arabidopsis require ARGONAUTE1. Plant Cell 17, 1343–1359.
- Sun, Q., Yoda, K. and Suzuki, H. (2005) Internal axial light conduction in the stems and roots of herbaceous plants. J Exp Bot 56, 191–203.
- Sun, Q., Yoda, K., Suzuki, M. and Suzuki, H. (2003) Vascular tissue in the stem and roots of woody plants can conduct light. J Exp Bot 54, 1627–1635.
- Taniguchi, M., Kiba, T., Sakakibara, H., Ueguchi, C., Mizuno, T. and Sugiyama, T. (1998) Expression of Arabidopsis response regulator homologs is induced by cytokinins and nitrate. FEBS Lett 429, 259–262.
- Tatematsu, K., Kumagai, S., Muto, H., et al. (2004) MASSUGU2 encodes Aux/IAA19, an auxin-regulated protein that functions together with the transcriptional activator NPH4/ARF7 to regulate differential growth responses of hypocotyl and formation of lateral roots in Arabidopsis thaliana . Plant Cell 16, 379–393.
- Thrower, J.S., Hoffman, L., Rechsteiner, M. and Pickart, C.M. (2000) Recognition of the polyubiquitin proteolytic signal. EMBO J 19, 94–102.
- Tian, Q. and Reed, J.W. (1999) Control of auxin-regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene. Development 126, 711–721.
- Timpte, C., Wilson, A.K. and Estelle, M. (1994) The axr2–1 mutation of Arabidopsis thaliana is a gain-of-function mutation that disrupts an early step in auxin response. Genetics 138, 1239–1249.
- To, J.P.C., Haberer, G., Ferreira, F.J., et al. (2004) Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling. Plant Cell 16, 658–671.
- Vanneste, S., De Rybel, B., Beemster, G.T.S., et al. (2005) Cell cycle progression in the pericycle is not sufficient for SOLITARY ROOT/IAA14-mediated lateral root initiation in Arabidopsis thaliana . Plant Cell 17, 3035–3050.
- Vaucheret, H., Vazquez, F., Crete, P. and Bartel, D.P. (2004) The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev 18, 1187–1197.
- Verkest, A., de O. Manes, C.-L., Vercruysse, S., et al. (2005) The cyclin-dependent kinase inhibitor KRP2 controls the onset of the endoreduplication cycle during Arabidopsis leaf development through inhibition of mitotic CDKA;1 kinase complexes. Plant Cell 17, 1723–1736.
- Vieten, A., Vanneste, S., Wisniewska, J., et al. (2005) Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression. Development 132, 4521–4531.
- Wang, J.-W., Wang, L.-J., Mao, Y.-B., Cai, W.-J., Xue, H.-W. and Chen, X.-Y. (2005) Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis. Plant Cell 17, 2204–2216.
- Weijers, D., Benkova, E., Jäger, K.E., et al. (2005) Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators. EMBO J 24, 1874–1885.
- Werner, T., Motyka, V., Laucou, V., Smets, R., Van Onckelen, H. and Schmülling, T. (2003) Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15, 2532–2550.
- Werner, T., Motyka, V., Strnad, M. and Schmülling, T. (2001) Regulation of plant growth by cytokinin. Proc Natl Acad Sci USA 98, 10487–10492.
- Wildwater, M., Campilho, A., Perez-Perez, J.M., et al. (2005) The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots. Cell 123, 1337–1349.
- Wilmoth, J.C., Wang, S., Tiwari, S.B., et al. (2005) NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. Plant J 43, 118–130.
- Xie, Q., Frugis, G., Colgan, D. and Chua, N.-H. (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev 14, 3024–3036.
- Xie, Q., Guo, H.S., Dallman, G., Fang, S., Weissman, A.M. and Chua, N.-H. (2002) SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals. Nature 419, 167–170.
- Xu, J., Hofhuis, H., Heidstra, R., Sauer, M., Friml, J. and Scheres, B. (2006) A molecular framework for plant regeneration. Science 311, 385–388.
- Yang, X., Lee, S., So, J.-H., et al. (2004) The IAA1 protein is encoded by AXR5 and is a substrate of SCFTIR1 . Plant J 40, 772–782.
- Yi, C. and Deng, X.W. (2005) COP1 – from plant photomorphogenesis to mammalian tumorigenesis. Trends Cell Biol 15, 618–625.
- Zhang, R., Zhang, X., Wang, J., Letham, D.S., McKinney, S.A. and Higgins, T.J.V. (1995) The effect of auxin on cytokinin levels and metabolism in transgenic tobacco tissue expressing an ipt gene. Planta 196, 84–94.
Citing Literature
Browse other articles of this reference work: