6 Gibberellin Hormone Signal Perception: Down-Regulating DELLA Repressors of Plant Growth and Development
Annual Plant Reviews book series, Volume 49: The Gibberellins
Sven K. Nelson,
Camille M. Steber,
Sven K. Nelson
Molecular Plant Sciences Program, Washington State University, USA
Current address: USDA-ARS, Plant Genetic Research Unit, University of Missouri, USA
Search for more papers by this authorCamille M. Steber
Molecular Plant Sciences Program, Washington State University, USA
USDA-ARS, Wheat Health, Genetics, and Quality Unit, Pullman, WA, USA
Department of Crop and Soil Science, Washington State University, USA
Search for more papers by this authorSven K. Nelson,
Camille M. Steber,
Sven K. Nelson
Molecular Plant Sciences Program, Washington State University, USA
Current address: USDA-ARS, Plant Genetic Research Unit, University of Missouri, USA
Search for more papers by this authorCamille M. Steber
Molecular Plant Sciences Program, Washington State University, USA
USDA-ARS, Wheat Health, Genetics, and Quality Unit, Pullman, WA, USA
Department of Crop and Soil Science, Washington State University, USA
Search for more papers by this authorThis article was originally published in 2016 in The Gibberellins, Volume 49 (ISBN 9781119210429) of the Annual Plant Reviews book series, this volume edited by Peter Hedden and Stephen G. Thomas. The article was republished in Annual Plant Reviews online in April 2018.
Abstract
The gibberellin (GA) hormone signal is perceived by a receptor with homology to hormone-sensitive lipases, GID1 (GA-INSENSITIVE DWARF1). This leads to GA-stimulated responses, including stem elongation, seed germination and the transition to flowering. GA-binding enables GID1 to interact with and block the function of the DELLA repressors of GA responses. DELLA repression can be blocked both by proteolytic and non-proteolytic mechanisms triggered by the formation of a GID1-GA-DELLA complex. DELLA is down-regulated by the SLEEPY1/GID2 F-box proteins via the ubiquitin-proteasome pathway, and can be regulated by other post-translational modifications. This chapter reviews the structural requirements for GA-binding by GID1 and for GID1-GA-DELLA protein complex formation, and reviews the current understanding of the mechanisms regulating DELLA repressors.
References
- 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. The Plant Cell 15, 2816–2825.
- Achard, P., Cheng, H., De Grauwe, L., et al. (2006). Integration of plant responses to environmentally activated phytohormonal signals. Science 311, 91–94.
- Achard, P., Gong, F., Cheminant, S., et al. (2008). The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. The Plant Cell 20, 2117–2129.
- Allan, R.E. (1986). Agronomic comparisons among wheat lines nearly isogenic for three reduced-height genes. Crop Science 26, 707–710.
- Ariizumi, T. and Steber, C.M. (2007). Seed germination of GA-insensitive sleepy1 mutants does not require RGL2 protein disappearance in Arabidopsis . The Plant Cell 19, 791–804.
- Ariizumi, T. and Steber, C.M. (2011). Mutations in the F-box gene SNEEZY result in decreased Arabidopsis GA signaling. Plant Signaling and Behavior 6, 831–833.
- Ariizumi, T., Murase, K., Sun, T.-P. and Steber, C.M. (2008). Proteolysis-independent downregulation of DELLA repression in Arabidopsis by the gibberellin receptor GIBBERELLIN INSENSITIVE DWARF1. The Plant Cell 20, 2447–2459.
- Ariizumi, T., Lawrence, P.K. and Steber, C.M. (2011). The role of two F-box proteins, SLEEPY1 and SNEEZY, in Arabidopsis gibberellin signaling. Plant Physiology 155, 765–775.
- Ariizumi, T., Hauvermale, A.L., Nelson, S.K., et al. (2013). Lifting DELLA repression of Arabidopsis seed germination by nonproteolytic gibberellin signaling. Plant Physiology 162, 2125–2139.
- Arnaud, N., Girin, T., Sorefan, K., et al. (2010). Gibberellins control fruit patterning in Arabidopsis thaliana. Genes and Development 24, 2127–2132.
- Bai, M.-Y., Shang, J.-X., Oh, E., et al. (2012). Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis . Nature Cell Biology 14, 810–817.
- Beitz, E. (2000). TEXshade: shading and labeling of multiple sequence alignments using LATEX2 epsilon. Bioinformatics 16, 135–139.
- Bolle, C. (2004). The role of GRAS proteins in plant signal transduction and development. Planta 218, 683–692.
- Cao, D., Hussain, A., Cheng, H. and Peng, J. (2005). Loss of function of four DELLA genes leads to light- and gibberellin-independent seed germination in Arabidopsis . Planta 223, 105–113.
- Chandler, P. and Robertson, M. (1999). Gibberellin dose-response curves and the characterization of dwarf mutants of barley. Plant Physiology 120, 623–632.
- Chandler, P.M., Marion-Poll, A., Ellis, M. and Gubler, F. (2002). Mutants at the Slender1 locus of barley cv Himalaya. molecular and physiological characterization. Plant Physiology 129, 181–190.
- Chandler, P.M., Harding, C.A., Ashton, A.R. et al. (2008). Characterization of gibberellin receptor mutants of barley (Hordeum vulgare L.). Molecular Plant 1, 285–294.
- Cheng, H., Qin, L., Lee, S., et al. (2004). Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function. Development 131, 1055–1064.
- Conti, L., Conti, L., Nelis, S., et al. (2014). Small Ubiquitin-like Modifier Protein SUMO enables plants to control growth independently of the phytohormone gibberellin. Developmental Cell 28, 102–110.
- Cui, H. and Benfey, P.N. (2009). Interplay between SCARECROW, GA and LIKE HETEROCHROMATIN PROTEIN 1 in ground tissue patterning in the Arabidopsis root. The Plant Journal 58, 1016–1027.
- Dai, C. and Xue, H.-W. (2010). Rice early flowering1, a CKI, phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signalling. The EMBO Journal 29, 1916–1927.
- de Lucas, M., Davière, J.-M., Rodríguez-Falcón, M., et al. (2008). A molecular framework for light and gibberellin control of cell elongation. Nature 451, 480–484.
- Dill, A. and Sun, T-p. (2001). Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana . Genetics 159, 777–785.
- Dill, A., Thomas, S.G., Hu, J., Steber, C.M. and Sun, T.-P. (2004). The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degradation. The Plant Cell 16, 1392–1405.
- Dill, K.A. (1990). The meaning of hydrophobicity. Science 250, 297–298.
- Dunker, A.K., Obradovic, Z., Romero, P., Garner, E.C. and Brown, C.J. (2000). Intrinsic protein disorder in complete genomes. Genome Informatics 11, 161–171.
- Engstrom, E.M. (2011). Phylogenetic analysis of GRAS proteins from moss, lycophyte and vascular plant lineages reveals that GRAS genes arose and underwent substantial diversification in the ancestral lineage common to bryophytes and vascular plants. Plant Signaling and Behavior 6, 850–854.
- Feng, S., Martinez, C., Gusmaroli, G., et al. (2008). Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451, 475–479.
- Filardo, F., Robertson, M., Singh, D.P., Parish, R.W. and Swain, S.M. (2009). Functional analysis of HvSPY, a negative regulator of GA response, in barley aleurone cells and Arabidopsis . Planta 229, 523–537.
- Fu, X., Richards, D.E., Ait-ali, T., et al. (2002). Gibberellin-mediated proteasome-dependent degradation of the barley DELLA protein SLN1 repressor. The Plant Cell 14, 3191–3200.
- Fu, X., Richards, D.E., Fleck, B., et al. (2004). The Arabidopsis mutant sleepy1gar2-1 protein promotes plant growth by increasing the affinity of the SCFSLY1 E3 ubiquitin ligase for DELLA protein substrates. The Plant Cell 16, 1406–1418.
- Fukao, T. and Bailey-Serres, J. (2008). Submergence tolerance conferred by Sub1A is mediated by SLR1 and SLRL1 restriction of gibberellin responses in rice. Proceedings of the National Academy of Sciences USA 105, 16814–16819.
- Fuxreiter, M., Simon, I., Friedrich, P. and Tompa, P. (2004). Preformed structural elements feature in partner recognition by intrinsically unstructured proteins. Journal of Molecular Biology 338, 1015–1026.
- Gagne, J.M., Downes, B.P., Shiu, S.H., Durski, A.M. and Vierstra, R.D. (2002). The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis . Proceedings of the National Academy of Sciences USA 99, 11519–11524.
- Gallego-Bartolomé, J., Minguet, E.G., Marín, J.A., et al. (2010). Transcriptional diversification and functional conservation between DELLA proteins in Arabidopsis . Molecular Biology and Evolution 27, 1247–1256.
- Gallego-Bartolomé, J., Minguet, E.G., Grau-Enguix, F., et al. (2012). Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in Arabidopsis . Proceedings of the National Academy of Sciences USA 109, 13446–13451.
- Gilroy, S. and Jones, R.L. (1994). Perception of gibberellin and abscisic acid at the external face of the plasma membrane of barley (Hordeum vulgare L.) aleurone protoplasts. Plant Physiology 104, 1185–1192.
- Gomi, K., Sasaki, A., Itoh, H., et al. (2004). GID2, an F-box subunit of the SCF E3 complex, specifically interacts with phosphorylated SLR1 protein and regulates the gibberellin-dependent degradation of SLR1 in rice. The Plant Journal 37, 626–634.
- Gray, W.M., Hellmann, H., Dharmasiri, S. and Estelle, M. (2002). Role of the Arabidopsis RING-H2 protein RBX1 in RUB modification and SCF function. The Plant Cell 14, 2137–2144.
- Griffiths, J., Murase, K., Rieu, I., et al. (2006). Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis . The Plant Cell 18, 3399–3414.
- Hao, G.-F., Yang, S.-G., Yang, G.-F. and Zhan, C.-G. (2013). Computational gibberellin-binding channel discovery unraveling the unexpected perception mechanism of hormone signal by gibberellin receptor. Journal of Computational Chemistry 34, 2055–2064.
- Hauvermale, A.L., Ariizumi, T. and Steber, C.M. (2012). Gibberellin signaling: a theme and variations on DELLA repression. Plant Physiology 160, 83–92.
- Hauvermale, A.L., Ariizumi, T. and Steber, C.M. (2014). The roles of the GA receptors GID1a, GID1b, and GID1c in sly1-independent GA signaling. Plant Signaling and Behavior 9, e28030.
- Heo, J.-O., Chang, K.S., Kim, I.A., et al. (2011). Funneling of gibberellin signaling by the GRAS transcription regulator SCARECROW-LIKE 3 in the Arabidopsis root. Proceedings of the National Academy of Sciences USA 108, 2166–2171.
- Hirano, K., Nakajima, M., Asano, K., et al. (2007). The GID1-mediated gibberellin perception mechanism is conserved in the Lycophyte Selaginella moellendorffii but not in the Bryophyte Physcomitrella patens . The Plant Cell 19, 3058–3079.
- Hirano, K., Ueguchi-Tanaka, M. and Matsuoka, M. (2008). GID1-mediated gibberellin signaling in plants. Trends in Plant Science 13, 192–199.
- Hirano, K., Asano, K., Tsuji, H., et al. (2010). Characterization of the molecular mechanism underlying gibberellin perception complex formation in rice. The Plant Cell 22, 2680–2696.
- Hirano, K., Kouketu, E., Katoh, H., et al. (2012). The suppressive function of the rice DELLA protein SLR1 is dependent on its transcriptional activation activity. The Plant Journal 71, 443–453.
- Hirsch, S., Hirsch, S., Kim, J., et al. (2009). GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula . The Plant Cell 21, 545–557.
- Hooley, R., Beale, M.H. and Smith, S.J. (1991). Gibberellin perception at the plasma membrane of Avena fatua aleurone protoplasts. Planta 183, 274–280.
- Hou, X., Lee, L.Y.C., Xia, K., Yan, Y. and Yu, H. (2010). DELLAs modulate jasmonate signaling via competitive binding to JAZs. Developmental Cell 19, 884–894.
- Huang, E.S., Subbiah, S. and Levitt, M. (1995). Recognizing native folds by the arrangement of hydrophobic and polar residues. Journal of Molecular Biology 252, 709–720.
- Hussain, A., Cao, D., Cheng, H., Wen, Z. and Peng, J. (2005). Identification of the conserved serine/threonine residues important for gibberellin-sensitivity of Arabidopsis RGL2 protein. The Plant Journal 44, 88–99.
- Iakoucheva, L.M., Brown, C.J., Lawson, J.D., Obradović, Z. and Dunker, A.K. (2002). Intrinsic disorder in cell-signaling and cancer-associated proteins. Journal of Molecular Biology 323, 573–584.
- Ikeda, A., Ikeda, A., Ueguchi-Tanaka, M., et al. (2001). slender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the height-regulating gene GAI/RGA/RHT/D8 . The Plant Cell 13, 999–1010.
- Itoh, H., Ueguchi-Tanaka, M., Sato, Y., Ashikari, M. and Matsuoka, M. (2002). The gibberellin signaling pathway is regulated by the appearance and disappearance of SLENDER RICE1 in nuclei. The Plant Cell 14, 57–70.
- Itoh, H., Matsuoka, M. and Steber, C.M. (2003). A role for the ubiquitin-26S-proteasome pathway in gibberellin signaling. Trends in Plant Science 8, 492–497.
- Itoh, H., Sasaki, A., Ueguchi-Tanaka, M., et al. (2005a). Dissection of the phosphorylation of rice DELLA protein, SLENDER RICE1. Plant and Cell Physiology 46, 1392–1399.
- Itoh, H., Shimada, A., Ueguchi-Tanaka, M., et al. (2005b). Overexpression of a GRAS protein lacking the DELLA domain confers altered gibberellin responses in rice. The Plant Journal 44, 669–679.
- Iuchi, S., Suzuki, H., Kim, Y.-C., et al. (2007). Multiple loss-of-function of Arabidopsis gibberellin receptor AtGID1s completely shuts down a gibberellin signal. The Plant Journal 50, 958–966.
- Jacobsen, S.E. and Olszewski, N.E. (1993). Mutations at the SPINDLY locus of Arabidopsis alter gibberellin signal transduction. The Plant Cell 5, 887–896.
- Jones, D.T., Taylor, W.R. and Thornton, J.M. (1992). The rapid generation of mutation data matrices from protein sequences. Computer Applications in the Biosciences 8, 275–282.
- King, K.E., Moritz, T. and Harberd, N.P. (2001). Gibberellins are not required for normal stem growth in Arabidopsis thaliana in the absence of GAI and RGA. Genetics 159, 767–776.
- Koornneef, M. and van der Veen, J.H. (1980). Induction and analysis of gibberellin sensitive mutants in Arabidopsis thaliana (L.) heynh. Theoretical and Applied Genetics 58, 257–263.
- Koornneef, M., Elgersma, A., Hanhart, C.J., et al. (1985). A gibberellin insensitive mutant of Arabidopsis thaliana . Physiologia Plantarum 65, 33–39.
- Lee, S., Cheng, H., King, K.E., et al. (2002). Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes and Development 16, 646–658.
- Levy, D.E. and Darnell, J.E. (2002). Stats: transcriptional control and biological impact. Nature Reviews Molecular Cell Biology 3, 651–662.
- Lin, Q., Li, J., Smith, R.D. and Walker, J.C. (1998). Molecular cloning and chromosomal mapping of type one serine/threonine protein phosphatases in Arabidopsis thaliana . Plant Molecular Biology 37, 471–481.
- Livne, S., and Weiss, D. (2014). Cytosolic activity of the gibberellin receptor GIBBERELLIN INSENSITIVE DWARF1a. Plant and Cell Physiology 55, 1727–1733.
- McCubbin, A.G., Ritchie, S.M., Swanson, S.J. and Gilroy, S. (2004). The calcium-dependent protein kinase HvCDPK1 mediates the gibberellic acid response of the barley aleurone through regulation of vacuolar function. The Plant Journal 39, 206–218.
- McGinnis, K.M., Thomas, S.G., Soule, J.D., et al. (2003). The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. The Plant Cell 15, 1120–1130.
- Mohan, A., Oldfield, C.J., Radivojac, P., et al. (2006). Analysis of molecular recognition features (MoRFs). Journal of Molecular Biology 362, 1043–1059.
- Murase, K., Hirano, Y., Sun, T.-P. and Hakoshima, T. (2008). Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456, 459–463.
- Nakajima, M., Takita, K., Wada, H., et al. (1997). Partial purification and characterization of a gibberellin-binding protein from seedlings of Azukia angularis . Biochemical and Biophysical Research Communications 241, 782–786.
- Nakajima, M., Shimada, A., Takashi, Y., et al. (2006). Identification and characterization of Arabidopsis gibberellin receptors. The Plant Journal 46, 880–889.
- Nguyen, L.K., Kolch, W. and Kholodenko, B.N. (2013). When ubiquitination meets phosphorylation: a systems biology perspective of EGFR/MAPK signalling. Cell Communication and Signaling 11: 52.
- Oldfield, C.J., Cheng, Y., Cortese, M.S., et al. (2005). Coupled folding and binding with alpha-helix-forming molecular recognition elements. Biochemistry 44, 12454–12470.
- Østerlund, T. (2001). Structure-function relationships of hormone-sensitive lipase. European Journal of Biochemistry 268, 1899–1907.
- Park, S.-H., Nakajima, M., Hasegawa, M. and Yamaguchi, I. (2005). Similarities and differences between the characteristics of gibberellin-binding protein and gibberellin 2-oxidases in adzuki bean (Vigna angularis) seedlings. Bioscience, Biotechnology, and Biochemistry 69, 1508–1514.
- Peng, J., Carol, P., Richards, D.E., et al. (1997). The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes and Development 11, 3194–3205.
- Peng, J., Richards, D.E., Hartley, N.M., et al. (1999). ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400, 256–261.
- Piskurewicz, U. and Lopez-Molina, L. (2009). The GA-signaling repressor RGL3 represses testa rupture in response to changes in GA and ABA levels. Plant Signaling and Behavior 4, 63–65.
- Plackett, A.R.G., Ferguson, A.C., Powers, S.J., et al. (2014). DELLA activity is required for successful pollen development in the Columbia ecotype of Arabidopsis . The New Phytologist 201, 825–836.
- Qin, Q., Wang, W., Guo, X., et al. (2014). Arabidopsis DELLA protein degradation is controlled by a type-one protein phosphatase, TOPP4. PLoS Genetics 10, e1004464.
-
Richards, D.E., Peng, J. and Harberd, N.P. (2000). Plant GRAS and metazoan STATs: one family?
BioEssays
22, 573–577.
10.1002/(SICI)1521-1878(200006)22:6<573::AID-BIES10>3.0.CO;2-H CAS PubMed Web of Science® Google Scholar
- Risseeuw, E.P., Daskalchuk, T.E., Banks, T.W., et al. (2003). Protein interaction analysis of SCF ubiquitin E3 ligase subunits from Arabidopsis . The Plant Journal 34, 753–767.
- Robertson, M., Swain, S.M., Chandler, P.M. and Olszewski, N.E. (1998). Identification of a negative regulator of gibberellin action, HvSPY, in barley. The Plant Cell 10, 995–1007.
- Rose, G.D., Geselowitz, A.R., Lesser, G.J., Lee, R.H. and Zehfus, M.H. (1985). Hydrophobicity of amino acid residues in globular proteins. Science 229, 834–838.
- Sarnowska, E.A., Sarnowska, E.A., Rolicka, A.T., et al. (2013). DELLA-interacting SWI3C core subunit of switch/sucrose nonfermenting chromatin remodeling complex modulates gibberellin responses and hormonal cross talk in Arabidopsis. Plant Physiology 163, 305–317.
- Sasaki, A., Itoh, H., Gomi, K., et al. (2003). Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science 299, 1896–1898.
- Sato, T., Miyanoiri, Y., Takeda, M., et al. (2014). Expression and purification of a GRAS domain of SLR1, the rice DELLA protein. Protein Expression and Purification 95, 248–258.
- Schulman, B.A., Carrano, A.C., Jeffrey, P.D., et al. (2000). Insights into SCF ubiquitin ligases from the structure of the Skp1-Skp2 complex. Nature 408, 381–386.
- Sheerin, D.J., Buchanan, J., Kirk, C., et al. (2011). Inter- and intra-molecular interactions of Arabidopsis thaliana DELLA protein RGL1. The Biochemical Journal 435, 629–639.
- Shimada, A., Ueguchi-Tanaka, M., Sakamoto, T., et al. (2006). The rice SPINDLY gene functions as a negative regulator of gibberellin signaling by controlling the suppressive function of the DELLA protein, SLR1, and modulating brassinosteroid synthesis. The Plant Journal 48, 390–402.
- Shimada, A., Ueguchi-Tanaka, M., Nakatsu, T., et al. (2008). Structural basis for gibberellin recognition by its receptor GID1. Nature 456, 520–523.
- Sievers, F., Wilm, A., Dineen, D., et al. (2011). Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Molecular Systems Biology 7: 539.
- Silverstone, A.L., Chang, C., Krol, E. and Sun, T.-P. (1997a). Developmental regulation of the gibberellin biosynthetic gene GA1 in Arabidopsis thaliana . The Plant Journal 12, 9–19.
- Silverstone, A.L., Mak, P.Y., Martínez, E.C. and Sun, T.-P. (1997b). The new RGA locus encodes a negative regulator of gibberellin response in Arabidopsis thaliana . Genetics 146, 1087–1099.
- Silverstone, A.L., Ciampaglio, C.N. and Sun, T. (1998). The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. The Plant Cell 10, 155–169.
- Silverstone, A.L., Jung, H.S., Dill, A., et al. (2001). Repressing a repressor: gibberellin-induced rapid reduction of the RGA protein in Arabidopsis . The Plant Cell 13, 1555–1566.
- Silverstone, A.L., Tseng, T.-S., Swain, S.M., et al. (2007). Functional analysis of SPINDLY in gibberellin signaling in Arabidopsis. Plant Physiology 143, 987–1000.
- Smalle, J. and Vierstra, R.D. (2004). The ubiquitin 26S proteasome proteolytic pathway. Annual Review of Plant Biology 55, 555–590.
- Smith, R.D. and Walker, J.C. (1993). Expression of multiple type 1 phosphoprotein phosphatases in Arabidopsis thaliana . Plant Molecular Biology 21, 307–316.
- Stavang, J.A., Gallego-Bartolomé, J., Gómez, M.D., et al. (2009). Hormonal regulation of temperature-induced growth in Arabidopsis . The Plant Journal 60, 589–601.
- Steber, C.M. and McCourt, P. (2001). A role for brassinosteroids in germination in Arabidopsis. Plant Physiology 125, 763–769.
- Steber, C.M., Cooney, S.E. and McCourt, P. (1998). Isolation of the GA-response mutant sly1 as a suppressor of ABI1-1 in Arabidopsis thaliana . Genetics 149, 509–521.
- Strader, L.C., Ritchie, S., Soule, J.D., McGinnis, K.M. and Steber, C.M. (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.
- Sun, T.-P. and Gubler, F. (2004). Molecular mechanism of gibberellin signaling in plants. Annual Review of Plant Biology 55, 197–223.
- Sun, T.-P. and Kamiya, Y. (1994). The Arabidopsis GA1 locus encodes the cyclase ent-kaurene synthetase A of gibberellin biosynthesis. The Plant Cell 6, 1509–1518.
- Sun, X., Jones, W.T., Harvey, D., et al. (2010). N-terminal domains of DELLA proteins are intrinsically unstructured in the absence of interaction with GID1/gibberellic acid receptors. Journal of Biological Chemistry 285, 11557–11571.
- Suzuki, H., Park, S.-H., Okubo, K., et al. (2009). Differential expression and affinities of Arabidopsis gibberellin receptors can explain variation in phenotypes of multiple knock-out mutants. The Plant Journal 60, 48–55.
- Swain, S.M., Tseng, T.S. and Olszewski, N.E. (2001). Altered expression of SPINDLY affects gibberellin response and plant development. Plant Physiology 126, 1174–1185.
- Tyler, L., Thomas, S.G., Hu, J., et al. (2004). DELLA proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant Physiology 135, 1008–1019.
- Ueguchi-Tanaka, M. and Matsuoka, M. (2010). The perception of gibberellins: clues from receptor structure. Current Opinion in Plant Biology 13, 503–508.
- Ueguchi-Tanaka, M., Ashikari, M., Nakajima, M., et al. (2005). GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437, 693–698.
- Ueguchi-Tanaka, M., Nakajima, M., Katoh, E., et al. (2007a). Molecular interactions of a soluble gibberellin receptor, GID1, with a rice DELLA protein, SLR1, and gibberellin. The Plant Cell 19, 2140–2155.
- Ueguchi-Tanaka, M., Nakajima, M., Motoyuki, A. and Matsuoka, M. (2007b). Gibberellin receptor and its role in gibberellin signaling in plants. Annual Review of Plant Biology 58, 183–198.
- Ueguchi-Tanaka, M., Hirano, K., Hasegawa, Y., Kitano, H. and Matsuoka, M. (2008). Release of the repressive activity of rice DELLA protein SLR1 by gibberellin does not require SLR1 degradation in the gid2 mutant. The Plant Cell 20, 2437–2446.
- Uversky, V.N. (2002). What does it mean to be natively unfolded? European Journal of Biochemistry 269, 2–12.
- Vierstra, R.D. (2012). The expanding universe of ubiquitin and ubiquitin-like modifiers. Plant Physiology 160, 2–14.
- Voegele, A., Linkies, A., Müller, K. and Leubner-Metzger, G. (2011). Members of the gibberellin receptor gene family GID1 (GIBBERELLIN INSENSITIVE DWARF1) play distinct roles during Lepidium sativum and Arabidopsis thaliana seed germination. Journal of Experimental Botany 62, 5131–5147.
- Wang, F. and Deng, X.W. (2011). Plant ubiquitin-proteasome pathway and its role in gibberellin signaling. Cell Research 21, 1286–1294.
- Wang, F., Zhu, D., Huang, X., et al. (2009). Biochemical insights on degradation of Arabidopsis DELLA proteins gained from a cell-free assay system. The Plant Cell 21, 2378–2390.
- Wells, L., Kreppel, L.K., Comer, F.I., Wadzinski, B.E. and Hart, G.W. (2004). O-GlcNAc transferase is in a functional complex with protein phosphatase 1 catalytic subunits. Journal of Biological Chemistry 279, 38466–38470.
- Wen, C.-K., Wen, C.-K., Chang, C. and Chang, C. (2002). Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. The Plant Cell 14, 87–100.
- Wild, M., Daviere, J.M., Cheminant, S. et al., (2012). The Arabidopsis DELLA RGA-LIKE3 is a direct target of MYC2 and modulates jasmonate signaling responses. The Plant Cell 24, 3307–19.
-
Willems, A.R., Goh, T., Taylor, L., et al. (1999). SCF ubiquitin protein ligases and phosphorylation-dependent proteolysis. Philosophical Transactions B
354, 1533–1550.
10.1098/rstb.1999.0497 Google Scholar
- Willige, B.C., Ghosh, S., Nill, C., et al. (2007). The DELLA domain of GA INSENSITIVE mediates the interaction with the GA INSENSITIVE DWARF1A gibberellin receptor of Arabidopsis . The Plant Cell 19, 1209–1220.
- Wilson, R.N., Heckman, J.W. and Somerville, C.R. (1992). Gibberellin is required for flowering in Arabidopsis thaliana under short days. Plant Physiology 100, 403–408.
- Yamaguchi, S. (2008). Gibberellin metabolism and its regulation. Annual Review of Plant Biology 59, 225–251.
- Yamamoto, Y., Hirai, T., Yamamoto, E., et al. (2010). A rice gid1 suppressor mutant reveals that gibberellin is not always required for interaction between its receptor, GID1, and DELLA proteins. The Plant Cell 22, 3589–3602.
- Yano, K., Aya, K., Hirano, K., et al. (2015). Comprehensive gene expression analysis of rice aleurone cells: Probing the existence of an alternative gibberellin receptor. Plant Physiology 167, 531–544.
- Yu, H., Ito, T., Zhao, Y., et al. (2004). Floral homeotic genes are targets of gibberellin signaling in flower development. Proceedings of the National Academy of Sciences USA 101, 7827–7832.
- Zentella, R., Zhang, Z.-L., Park, M., et al. (2007). Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis . The Plant Cell 19, 3037–3057.
- Zhang, Y., Liu, Z., Wang, L., et al. (2010). Sucrose-induced hypocotyl elongation of Arabidopsis seedlings in darkness depends on the presence of gibberellins. Journal of Plant Physiology 167, 1130–1136.
- Zhang, Z.-L., Ogawa, M., Fleet, C.M., et al. (2011). SCARECROW-LIKE 3 promotes gibberellin signaling by antagonizing master growth repressor DELLA in Arabidopsis . Proceedings of the National Academy of Sciences USA 108, 2160–2165.
Citing Literature
Browse other articles of this reference work:
