1 Arabidopsis Root Development
Annual Plant Reviews book series, Volume 37: Root Development
Marijn Luijten,
Renze Heidstra,
Marijn Luijten
Department of Biology, Section Molecular Genetics, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands
Search for more papers by this authorRenze Heidstra
Department of Biology, Section Molecular Genetics, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands
Search for more papers by this authorMarijn Luijten,
Renze Heidstra,
Marijn Luijten
Department of Biology, Section Molecular Genetics, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands
Search for more papers by this authorRenze Heidstra
Department of Biology, Section Molecular Genetics, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands
Search for more papers by this authorThis article was originally published in 2010 in Root Development, Volume 37 (ISBN 9781405161503) of the Annual Plant Reviews book series, this volume edited by Tom Beeckman. The article was republished in Annual Plant Reviews online in April 2018.
Abstract
In plant development, the basic body plan is laid down during embryogenesis. Development carries on postembryogenically above and below ground with the continuous formation and outgrowth of lateral organs shaping the adult plant. In the past two decades, molecular genetics has been the preferred approach to study Arabidopsis thaliana root development. These efforts have resulted in the identification of numerous genes, involved in as many regulatory processes of root growth and development. Incidentally, conserved mechanisms and genetic factors that act in root and shoot growth have been uncovered, revealing general principles of plant development. Transport-mediated graded distribution of the phytohormone auxin, for example, acts as a global organizer that is locally translated into distinct cellular responses by specific auxin/indole-3-acetic acid–AUXIN RESPONSE FACTOR pairs. In the root, these responses promote expression of the PLETHORA regulators that act dose-dependently in controlling root morphology. The stem cell niche is uniquely defined by the combinatorial activity of the PLETHORA and SHORT-ROOT/SCARECROW transcription factors yet deploy signaling mechanisms that are conserved in root and shoot stem cell maintenance. Perpetual divisions of the stem cells are tightly regulated, interconnecting epigenetic factors, hormonal control and core cell cycle components. In this chapter, we will focus on recent advances in our understanding of Arabidopsis root development. Taking embryogenesis as a starting point, we will describe the genes and mechanisms involved in root meristem and stem cell patterning and maintenance.
References
- Abe, M., Katsumata, H., Komeda, Y. and Takahashi, T. (2003). Regulation of shoot epidermal cell differentiation by a pair of homeodomain proteins in Arabidopsis . Development 130, 635–643.
- Ach, R.A., Taranto, P. and Gruissem, W. (1997). A conserved family of WD-40 proteins binds to the retinoblastoma protein in both plants and animals. Plant Cell 9, 1595–1606.
- Achard, P., Vriezen, W.H., Van Der Straeten, D. and Harberd, N.P. (2003). Ethylene regulates Arabidopsis development via the modulation of DELLA protein growth repressor function. Plant Cell 15, 2816–2825.
- Aida, M., Beis, D., Heidstra, R., Willemsen, V., Blilou, I., Galinha, C. et al. (2004). The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119, 109–120.
- Barrôco, R.M., Van Poucke, K., Bergervoet, J.H.W., De Veylder, L., Groot, S.P.C., Inzé, D. et al. (2005). The role of the cell cycle machinery in resumption of postembryonic development. Plant Physiol. 137, 127–140.
- Baum, S.F., Dubrovsky, J.G. and Rost, T.L. (2002). Apical organization and maturation of the cortex and vascular cylinder in Arabidopsis thaliana (Brassicaceae) roots. Am. J. Bot. 89, 908–920.
- Beemster, G.T.S. and Baskin, T.I. (2000). STUNTED PLANT 1 mediates effects of cytokinin, but not of auxin, on cell division and expansion in the root of Arabidopsis. Plant Physiol. 124, 1718–1727.
- Benfey, P.N., Linstead, P.J., Roberts, K., Schiefelbein, J.W., Hauser, M.-T. and Aeschbacher, R.A. (1993). Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. Development 119, 57–70.
- Benjamins, R., Quint, A., Weijers, D., Hooykaas, P. and Offringa, R. (2001). The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. Development 128, 4057–4067.
- Bennett, M.J., Marchant, A., Green, H.G., May, S.T., Ward, S.P., Millner, P.A. et al. (1996). Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273, 948–950.
- Berleth, T. and Jürgens, G. (1993). The role of the monopteros gene in organising the basal body region of the Arabidopsis embryo. Development 118, 575–587.
- Blilou, I., Frugier, F., Folmer, S., Serralbo, O., Willemsen, V., Wolkenfelt, H. 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., Willemsen, V., Paponov, I., Friml, J. et al. (2005). The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433, 39–44.
- Brand, U., Fletcher, J.C., Hobe, M., Meyerowitz, E.M. and Simon, R. (2000). Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289, 617–619.
- Capron, A., Serralbo, O., Fülöp, K., Frugier, F., Parmentier, Y., Dong, A. et al. (2003). The Arabidopsis anaphase-promoting complex or cyclosome: molecular and genetic characterization of the APC2 subunit. Plant Cell 15, 2370–2382.
- Casamitjana-Martínez, E., Hofhuis, H.F., Xu, J., Liu, C.-M., Heidstra, R. and Scheres, B. (2003). Root-specific CLE19 overexpression and the sol1/2 suppressors implicate a CLV-like pathway in the control of Arabidopsis root meristem maintenance. Curr. Biol. 13, 1435–1441.
- Casson, S.A., Chilley, P.M., Topping, J.F., Evans, I.M., Souter, M.A. and Lindsey, K. (2002). The POLARIS gene of Arabidopsis encodes a predicted peptide required for correct root growth and leaf vascular patterning. Plant Cell 14, 1705–1721.
- Cheng, J.-C., Seeley, K.A. and Sung, Z.R. (1995). RML1 and RML2, Arabidopsis genes required for cell proliferation at the root tip. Plant Physiol. 107, 365–376.
- Chilley, P.M., Casson, S.A., Tarkowski, P., Hawkins, N., Wang, K.L.-C., Hussey, P.J. etal. (2006). The POLARIS peptide of Arabidopsis regulates auxin transport and root growth via effects on ethylene signaling. Plant Cell 18, 3058–3072.
- Christensen, S.K., Dagenais, N., Chory, J. and Weigel, D. (2000). Regulation of auxin response by the protein kinase PINOID. Cell 100, 469–478.
- Cobbett, C.S., May, M.J., Howden, R. and Rolls, B. (1998). The glutathione-deficient, cadmium-sensitive mutant, cad2-1, of Arabidopsis thaliana is deficient in γ-glutamylcysteine synthetase. Plant J. 16, 73–78.
- Cui, H., Levesque, M.P., Vernoux, T., Jung, J.W., Paquette, A.J., Gallagher, K.L. et al. (2007). An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316, 421–425 [Err. Science 318, 1866].
- De Veylder, L., Beeckman, T., Beemster, G.T.S., Krols, L., Terras, F., Landrieu, I. et al. (2001). Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 13, 1653–1667.
- Dello Ioio, R., Scaglia Linhares, F., Scacchi, E., Casamitjana-Martinez, E., Heidstra, R., Costantino, P. et al. (2007). Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Curr. Biol. 17, 678–682.
- den Boer, B.G.W. and Murray, J.A.H. (2000). Triggering the cell cycle in plants. Trends Cell Biol. 10, 245–250.
- Dharmasiri, N., Dharmasiri, S. and Estelle, M. (2005). The F-box protein TIR1 is an auxin receptor. Nature 435, 441–445.
- Di Laurenzio, L., Wysocka-DIller, J., Malamy, J.E., Pysh, L., Helariutta, Y., Freshour, G. et al. (1996). The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86, 423–433.
- Diener, A.C., Li, H., Zhou, W.-X., Whoriskey, W.J., Nes, W.D. and Fink, G.R. (2000). STEROL METHYLTRANSFERASE 1 controls the level of cholesterol in plants. Plant Cell 12, 853–870.
- Dolan, L., Janmaat, K., Willemsen, V., Linstead, P., Poethig, S., Roberts, K. et al. (1993). Cellular organisation of the Arabidopsis thaliana root. Development 119, 71–84.
- Fiers, M., Golemiec, E., Xu, J., Van Der Geest, L., Heidstra, R., Stiekema, W. et al. (2005). The 14-amino acid CLV3, CLE19, and CLE40 peptides trigger consumption of the root meristem in Arabidopsis through a CLAVATA2-dependent pathway. Plant Cell 17, 2542–2553.
- Fiers, M., Hause, G., Boutilier, K., Casamitjana-Martinez, E., Weijers, D., Offringa, R. et al. (2004). Mis-expression of the CLV3/ESR-like gene CLE19 in Arabidopsis leads to a consumption of root meristem. Gene 327, 37–49.
- Fletcher, J.C., Brand, U., Running, M.P., Simon, R. and Meyerowitz, E.M. (1999). Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot systems. Science 283, 1911–1914.
- Frigerio, M., Alabadí, D., Pérez-Gómez, J., García-Cárcel, L., Phillips, A.L., Hedden, P. et al. (2006). Transcriptional regulation of gibberellin metabolism genes by auxin signaling in Arabidopsis. Plant Physiol. 142, 553–563.
- Friml, J., Benková, E., Blilou, I., Wisniewska, J., Hamann, T., Ljung, K. et al. (2002a). AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis . Cell 108, 661–673.
- Friml, J., Vieten, A., Sauer, M., Weijers, D., Schwarz, H., Hamann, T. et al. (2003). Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis . Nature 426, 147–153.
- Friml, J., Wiśniewska, J., Benková, E., Mendgen, K. and Palme, K. (2002b). Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis . Nature 415, 806–809.
- Friml, J., Yang, X., Michniewicz, M., Weijers, D., Quint, A., Tietz, O. et al. (2004). A PINOID-dependent binary switch in apical–basal PIN polar targeting directs auxin efflux. Science 306, 862–865.
- Fu, X. and Harberd, N.P. (2003). Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421, 740–743.
- Galinha, C., Hofhuis, H., Luijten, M., Willemsen, V., Blilou, I., Heidstra, R. et al. (2007). PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449, 1053–1057.
- Gallagher, K.L., Paquette, A.J., Nakajima, K. and Benfey, P.N. (2004). Mechanisms regulating SHORT-ROOT intercellular movement. Curr. Biol. 14, 1847–1851.
- Gälweiler, L., Guan, C., Müller, A., Wisman, E., Mendgen, K., Yephremov, A. et al. (1998). Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282, 2226–2230.
- Geisler, M. and Murphy, A.S. (2006). The ABC of auxin transport: the role of p-glycoproteins in plant development. FEBS Lett. 580, 1094–1102.
- Geldner, N., Anders, N., Wolters, H., Keicher, J., Kornberger, W., Muller, P. et al. (2003). The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112, 219–230.
- Grebe, M., Xu, J., Möbius, W., Ueda, T., Nakano, A., Geuze, H.J. et al. (2003). Arabidopsis sterol endocytosis involves actin-mediated trafficking via ARA6-positive early endosomes. Curr Biol. 13, 1378–1387.
- Grieneisen, V.A., Xu, J., Marée, A.F.M., Hogeweg, P. and Scheres, B. (2007). Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 449, 1008–1013.
- Guyomarc'h, S., Vernoux, T., Traas, J., Zhou, D.-X. and Delarue, M. (2004). MGOUN3, an Arabidopsis gene with TetratricoPeptide-Repeat-related motifs, regulates meristem cellular organization. J. Exp. Bot. 55, 673–684.
- Hadfi, K., Speth, V. and Neuhaus, G. (1998). Auxin-induced developmental patterns in Brassica juncea embryos. Development 125, 879–887.
- Haecker, A., Groß-Hardt, R., Geiges, B., Sarkar, A., Breuninger, H., Herrmann, M. et al. (2004). Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana . Development 131, 657–668.
- Hamann, T., Benkova, E., Bäurle, I., Kientz, M. and Jürgens, G. (2002). The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev. 16, 1610–1615.
- 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. and Berleth, T. (1998). The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J. 17, 1405–1411.
- Harper, R.M., Stowe-Evans, E.L., Luesse, D.R., Muto, H., Tatematsu, K., Watahiki, M.K. et al. (2000). The NPH4 locus encodes the auxin response factor ARF7, a conditional regulator of differential growth in aerial Arabidopsis tissue. Plant Cell 12, 757–770.
- Heidstra, R., Welch, D. and Scheres, B. (2004). Mosaic analyses using marked activation and deletion clones dissect Arabidopsis SCARECROW action in asymmetric cell division. Genes Dev. 18, 1964–1969.
- Helariutta, Y., Fukaki, H., Wysocka-Diller, J., Nakajima, K., Jung, J., Sena, G. et al. (2000). The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101, 555–567.
- Hellmann, H., Hobbie, L., Chapman, A., Dharmasiri, S., Dharmasiri, N., del Pozo, C. et al. (2003). Arabidopsis AXR6 encodes CUL1 implicating SCF E3 ligases in auxin regulation of embryogenesis. EMBO J. 22, 3314–3325.
- Hobbie, L., McGovern, M., Hurwitz, L.R., Pierro, A., Liu, N.Y., Bandyopadhyay, A. et al. (2000). The axr6 mutants of Arabidopsis thaliana define a gene involved in auxin response and early development. Development 127, 23–32.
- Hobe, M., Müller, R., Grünewald, M., Brand, U. and Simon, R. (2003). Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis . Dev. Genes Evol. 213, 371–381.
- Inagaki, S., Suzuki, T., Ohto, M.-A., Urawa, H., Horiuchi, T., Nakamura, K. et al. (2006). Arabidopsis TEBICHI, with helicase and DNA polymerase domains, is required for regulated cell division and differentiation in meristems. Plant Cell 18, 879–892.
- Ito, Y., Nakanomyo, I., Motose, H., Iwamoto, K., Sawa, S., Dohmae, N. et al. (2006). Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 313, 842–845.
- Jaillais, Y., Fobis-Loisy, I., Miège, C., Rollin, C. and Gaude, T. (2006). AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis . Nature 443, 106–109.
- Jaillais, Y., Santambrogio, M., Rozier, F., Fobis-Loisy, I., Miège, C. and Gaude, T. (2007). The retromer protein VPS29 links cell polarity and organ initiation in plants. Cell 130, 1057–1070.
- Jenik, P.D., Jurkuta, R.E. and Barton, M.K. (2005). Interactions between the cell cycle and embryonic patterning in Arabidopsis uncovered by a mutation in DNA polymerase ɛ. Plant Cell 17, 3362–3377.
- Jiang, K. and Feldman, L.J. (2005). Regulation of root apical meristem development. Annu. Rev. Cell. Dev. Biol. 21, 485–509.
- Jiang, K., Meng, Y.L. and Feldman, L.J. (2003). Quiescent center formation in maize roots is associated with an auxin-regulated oxidizing environment. Development 130, 1429–1438.
- Jürgens, G. (2001). Apical–basal pattern formation in Arabidopsis embryogenesis. EMBO J. 20, 3609–3616.
- Jürgens, G. and Mayer, U. (1994). Arabidopsis. In Embryos: Colour Atlas of Development, J.B.L. Bard (ed.). London, Wolfe Publishing, pp. 7–21.
- Kaya, H., Shibahara, K.-I., Taoka, K.-I., Iwabuchi, M., Stillman, B. and Araki, T. (2001). FASCIATA genes for chromatin assembly factor-1 in Arabidopsis maintain the cellular organization of apical meristems. Cell 104, 131–142.
- Kepinski, S. and Leyser, O. (2005). The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435, 446–451.
- Kondo, T., Sawa, S., Kinoshita, A., Mizuno, S., Kakimoto, T., Fukuda, H. et al. (2006). A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science 313, 845–848.
- Koornneef, M., Bentsink, L. and Hilhorst, H. (2002). Seed dormancy and germination. Curr. Opin. Plant Biol. 5, 33–36.
- Kornet, N. and Scheres, B. (2009). Members of the GCN5 histone acetyltransferase complex regulate PLETHORA-mediated stem cell niche maintenance and transit amplifying cell proliferation in Arabidopsis. Plant Cell 21, 1070–1079.
- Kwee, H.-S. and Sundaresan, V. (2003). The NOMEGA gene required for female gametophyte development encodes the putative APC6/CDC16 component of the Anaphase Promoting Complex in Arabidopsis . Plant J. 36, 853–866.
- Laux, T., Mayer, K.F.X., Berger, J. and Jürgens, G. (1996). The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis . Development 122, 87–96.
- Levesque, M.P., Vernoux, T., Busch, W., Cui, H., Wang, J.Y., Blilou, I. et al. (2006). Whole-genome analysis of the SHORT-ROOT developmental pathway in Arabidopsis . PLoS Biol. 4 (e143), 0739–0752.
- Leyser, H.M.O. and Furner, I.J. (1992). Characterisation of three shoot apical meristem mutants of Arabidopsis thaliana . Development 116, 397–403.
- 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.
- Liu, C.-M., Xu, Z.-H. and Chua, N.-H. (1993). Auxin polar transport is essential for the establishment of bilateral symmetry during early plant embryogenesis. Plant Cell 5, 621–630.
- Lu, P., Porat, R., Nadeau, J.A. and O'Neill, S.D. (1996). Identification of a meristem L1 layer-specific gene in Arabidopsis that is expressed during embryonic pattern formation and defines a new class of homeobox genes. Plant Cell 8, 2155–2168.
- Lukowitz, W., Roeder, A., Parmenter, D. and Somerville, C. (2004). A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis . Cell 116, 109–119.
- Mansfield, S.G. and Briarty, L.G. (1991). Early embryogenesis in Arabidopsis thaliana. II. The developing embryo. Can. J. Bot. 69, 461–476.
- Masubelele, N.H., Dewitte, W., Menges, M., Maughan, S., Collins, C., Huntley, R. et al. (2005). D-type cyclins activate division in the root apex to promote seed germination in Arabidopsis . Proc. Natl. Acad. Sci. U. S. A. 102, 15694–15699.
- Mayer, K.F.X., Schoof, H., Haecker, A., Lenhard, M., Jürgens, G. and Laux, T. (1998). Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95, 805–815.
- Mayer, U., Büttner, G. and Jürgens, G. (1993). Apical–basal pattern formation in the Arabidopsis embryo: studies on the role of the gnom gene. Development 117, 149–162.
- Meshorer, E. and Misteli, T. (2006). Chromatin in pluripotent embryonic stem cells and differentiation. Nat. Rev. Mol. Cell. Biol. 7, 540–546.
- Meyer, A.J. and Hell, R. (2005). Glutathione homeostasis and redox-regulation by sulfhydryl groups. Photosynth. Res. 86, 435–457.
- Michniewicz, M., Zago, M.K., Abas, L., Weijers, D., Schweighofer, A., Meskiene, I. et al. (2007). Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130, 1044–1056.
- Mouchel, C.F., Briggs, G.C. and Hardtke, C.S. (2004). Natural genetic variation in Arabidopsis identifies BREVIS RADIX, a novel regulator of cell proliferation and elongation in the root. Genes Dev. 18, 700–714.
- Mouchel, C.F., Osmont, K.S. and Hardtke, C.S. (2006). BRX mediates feedback between brassinosteroid levels and auxin signalling in root growth. Nature 443, 458–461.
- Müller, A., Guan, C., Gälweiler, L., Tänzler, P., Huijser, P., Marchant, A. et al. (1998). AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J. 17, 6903–6911.
- Müssig, C., Shin, G.-H. and Altmann, T. (2003). Brassinosteroids promote root growth in Arabidopsis. Plant Physiol. 133, 1261–1271.
- Nakajima, K., Sena, G., Nawy, T. and Benfey, P.N. (2001). Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413, 307–311.
- Nawy, T., Lee, J.-Y., Colinas, J., Wang, J.Y., Thongrod, S.C., Malamy, J.E. et al. (2005). Transcriptional profile of the Arabidopsis root quiescent center. Plant Cell 17, 1908–1925.
- Nodine, M.D., Yadegari, R. and Tax, F.E. (2007). RPK1 and TOAD2 are two receptor-like kinases redundantly required for Arabidopsis embryonic pattern formation. Dev. Cell 12, 943–956.
- Ogawa, M., Shinohara, H., Sakagami, Y. and Matsubayashi, Y. (2008). Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319, 294–294 [Err. Science 319, 901].
- Okushima, Y., Overvoorde, P.J., Arima, K., Alonso, J.M., Chan, A., Chang, C. 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.
- Ortega-Martínez, O., Pernas, M., Carol, R.J. and Dolan, L. (2007). Ethylene modulates stem cell division in the Arabidopsis thaliana root. Science 317, 507–510.
- Ottenschläger, I., Wolff, P., Wolverton, C., Bhalerao, R.P., Sandberg, G., Ishikawa, H. et al. (2003). Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc. Natl. Acad. Sci. U. S. A. 100, 2987–2991.
- Paponov, I.A., Teale, W.D., Trebar, M., Blilou, I. and Palme, K. (2005). The PIN auxin efflux facilitators: evolutionary and functional perspectives. Trends Plant Sci. 10, 170–177.
- Paquette, A.J. and Benfey, P.N. (2005). Maturation of the ground tissue of the root is regulated by gibberellin and SCARECROW and requires SHORT-ROOT . Plant Physiol. 138, 636–640.
- Pérez-Pérez, J.M., Serralbo, O., Vanstraelen, M., González, C., Criqui, M.-C., Genschik, P. et al. (2008). Specialization of CDC27 function in the Arabidopsis thaliana anaphase-promoting complex (APC/C). Plant J. 53, 78–89.
- Quint, M. and Gray, W.M. (2006). Auxin signaling. Curr. Opin. Plant Biol. 9, 448–453.
- Růžička, K., Ljung, K., Vanneste, S., Podhorská, R., Beeckman, T., Friml, J. et al. (2007). Ethylene regulates root growth through effect on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 19, 2197–2212.
- Sabatini, S., Beis, D., Wolkenfelt, H., Murfett, J., Guilfoyle, T., Malamy, J. et al. (1999). An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99, 463–472.
- Sabatini, S., Heidstra, R., Wildwater, M. and Scheres, B. (2003). SCARECROW is involved in positioning the stem cell niche in the Arabidopsis meristem. Genes Dev. 17, 354–358.
- Sánchez-Fernández, R., Fricker, M., Corben, L.B., White, N.S., Sheard, N., Leaver, C.J. et al. (1997). Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control. Proc. Natl. Acad. Sci. U. S. A. 94, 2745–2750.
- Sarkar, A.K., Luijten, M., Miyashima, S., Lenhard, M., Hashimoto, T., Nakajima, K. et al. (2007). Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446, 811–814.
- Scheres, B., Di Laurenzio, L., Willemsen, V., Hauser, M.-T., Janmaat, K., Weisbeek, P. et al. (1995). Mutations affecting the radial organisation of the Arabidopsis root display specific defects throughout the embryonic axis. Development 121, 53–62.
- Scheres, B., Wolkenfelt, H., Willemsen, V., Terlouw, M., Lawson, E., Dean, C. et al. (1994). Embryonic origin of the Arabidopsis primary root and root meristem initials. Development 120, 2475–2487.
- Schoof, H., Lenhard, M., Haecker, A., Mayer, K.F.X., Jürgens, G. and Laux, T. (2000). The stem cell population of Arabidopsis shoot meristem is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100, 635–644.
- Sena, G., Jung, J.W. and Benfey, P.N. (2004). A broad competence to respond to SHORT ROOT revealed by tissue-specific ectopic expression. Development 131, 2817–2826.
- Serralbo, O., Pérez-Pérez, J.M., Heidstra, R. and Scheres, B. (2006). Non-cell-autonomous rescue of anaphase-promoting complex function revealed by mosaic analysis of HOBBIT, an Arabidopsis CDC27 homolog. Proc. Natl. Acad. Sci. U. S. A. 103, 13250–13255.
- Srivastava, L. (2002). Plant Growth and Development: Hormones and Environment. New York, Academic Press.
- Steinmann, T., Geldner, N., Grebe, M., Mangold, S., Jackson, C.L., Paris, S. et al. (1999). Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286, 316–318.
- Stepanova, A.N., Hoyt, J.M., Hamilton, A.A. and Alonso, J.M. (2005). A link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis. Plant Cell 17, 2239–2242.
- Stepanova, A.N., Yun, J., Likhacheva, A.V. and Alonso, J.M. (2007). Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell 19, 2169–2185.
- Suzuki, T., Inagaki, S., Nakajima, S., Akashi, T., Ohto, M.-A., Kobayashi, M. et al. (2004). A novel Arabidopsis gene TONSOKU is required for proper cell arrangement in root and shoot apical meristems. Plant J. 38, 673–684.
- Suzuki, T., Nakajima, S., Inagaki, S., Hirano-Nakakita, M., Matsuoka, K., Demura, T. et al. (2005). TONSOKU is expressed in S phase of the cell cycle and its defect delays cell cycle progression in Arabidopsis . Plant Cell Physiol. 46, 736–742.
- Swarup, R., Perry, P., Hagenbeek, D., Van Der Straeten, D., Beemster, G.T.S., Sandberg, G. et al. (2007). Ethylene up regulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 19, 2186–2196.
- Szemenyei, H., Hannon, M. and Long, J.A. (2008). TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319, 1384–1386.
- Takeda, S., Tadele, Z., Hofmann, I., Probst, A.V., Angelis, K.J., Kaya, H. et al. (2004). BRU1, a novel link between responses to DNA damage and epigenetic gene silencing in Arabidopsis . Genes Dev. 18, 782–793.
- Tiwari, S.B., Hagen, G. and Guilfoyle, T.J. (2004). Aux/IAA proteins contain a potent transcriptional repression domain. Plant Cell 16, 533–543.
- Ueda, M., Matsui, K., Ishiguro, S., Sano, R., Wada, T., Paponov, I. et al. (2004). The HALTED ROOT gene encoding the 26S proteasome subunit RPT2a is essential for the maintenance of Arabidopsis meristems. Development 131, 2101–2111.
- Van Den Berg, C., Willemsen, V., Hage, W., Weisbeek, P. and Scheres, B. (1995). Cell fate in the Arabidopsis root meristem determined by directional signalling. Nature 378, 62–65.
- Van Den Berg, C., Willemsen, V., Hendriks, G., Weisbeek, P. and Scheres, B. (1997). Short-range control of cell differentiation in the Arabidopsis root meristem. Nature 390, 287–289.
- Vernoux, T., Wilson, R.C., Seeley, K.A., Reichheld, J.-P., Muroy, S., Brown, S. et al. (2000). The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 12, 97–110.
- Vidaurre, D.P., Ploense, S., Krogan, N.T. and Berleth, T. (2007). AMP1 and MP antagonistically regulate embryo and meristem development in Arabidopsis . Development 134, 2561–2567.
- Vieten, A., Vanneste, S., Wiśniewska, J., Benková, E., Benjamins, R., Beeckman, T. 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., Schlereth, A., Hamann, T., Kientz, M. et al. (2005). Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators. EMBO J. 24, 1874–1885.
- Weijers, D. and Jürgens, G. (2005). Auxin and embryo axis formation: the ends in sight? Curr. Opin. Plant Biol. 8, 32–37.
- Weijers, D., Schlereth, A., Ehrismann, J.S., Schwank, G., Kientz, M. and Jürgens, G. (2006). Auxin triggers transient local signaling for cell specification in Arabidopsis embryogenesis. Dev. Cell 10, 265–270.
- Weinberg, R.A. (1995). The retinoblastoma protein and cell cycle control. Cell 81, 323–330.
- Welch, D., Hassan, H., Blilou, I., Immink, R., Heidstra, R. and Scheres, B. (2007). Arabidopsis JACKDAW and MAGPIE zinc finger proteins delimit asymmetric cell division and stabilize tissue boundaries by restricting SHORT-ROOT action. Genes Dev. 21, 2196–2204.
- 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.
- Wildwater, M., Campilho, A., Perez-Perez, J.M., Heidstra, R., Blilou, I., Korthout, H. et al. (2005). The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots. Cell 123, 1337–1349.
- Willemsen, V., Friml, J., Grebe, M., Van Den Toorn, A., Palme, K. and Scheres, B. (2003). Cell polarity and PIN protein positioning in Arabidopsis require STEROL METHYLTRANSFERASE1 function. Plant Cell 15, 612–625.
- Willemsen, V., Wolkenfelt, H., de Vrieze, G., Weisbeek, P. and Scheres, B. (1998). The HOBBIT gene is required for formation of the root meristem in the Arabidopsis embryo. Development 125, 521–531.
- Willemsen, V., Bauch, M., Bennett, T., Campilho, A., Wolkenfelt, H., Xu, J. et al. (2008). The NAC domain transcription factors FEZ and SOMBRERO control the orientation of cell division plane in Arabidopsis root stem cells. Dev. Cell 15, 913–922.
- Wiśniewska, J., Xu, J., Seifertová, D., Brewer, P.B., Růžička, K., Blilou, I. et al. (2006). Polar PIN localization directs auxin flow in plants. Science 312, 883–883.
- Wu, X., Chory, J. and Weigel, D. (2007). Combinations of WOX activities regulate tissue proliferation during Arabidopsis embryonic development. Dev. Biol. 309, 306–316.
- Wysocka-Diller, J.W., Helariutta, Y., Fukaki, H., Malamy, J.E. and Benfey, P.N. (2000). Molecular analysis of SCARECROW function reveals a radial patterning mechanism common to root and shoot. Development 127, 595–603.
- Xu, J., Hofhuis, H., Heidstra, R., Sauer, M., Friml, J. and Scheres, B. (2006). A molecular framework for plant regeneration. Science 311, 385–388.
- Yeung, E.C. and Meinke, D.W. (1993). Embryogenesis in angiosperms: development of the suspensor. Plant Cell 5, 1371–1381.
- Zhu, Y., Dong, A., Meyer, D., Pichon, O., Renou, J.-P., Cao, K. et al. (2006). Arabidopsis NRP1 and NRP2 encode histone chaperones and are required for maintaining postembryonic root growth. Plant Cell 18, 2879–2892.
Citing Literature
Browse other articles of this reference work:
