Abstract
The rice SLR1 gene is an ortholog of Arabidopsis GA1 and RGA, which function as negative regulators of gibberellin (GA) signal transduction. Genetic, physiological and biochemical analyses have revealed that the SLR1 protein, which is localized in the nucleus, is degraded by an upstream GA signal to induce the downstream GA actions. In other words, SLR1 suppresses GA activity and the GA-dependent degradation of the SLR1 protein releases SLR1-suppressed GA action. We identified the link between SLR1 degradation and GA signaling when we were analyzing the rice GA-insensitive dwarf (GID2) mutant. The GID2 gene encodes a putative F-box protein that is a component of an SCF complex associated with protein degradation via the 26S proteasome. Biochemical analyses of SLR1 and GID2 suggest that the proteasome-dependent degradation of SLR1 is initiated by phosphorylatian of SLR1 and mediated by an SCF complex involving GID2. In this review, we propose a model for GA signal transduction in rice.
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References
M Akemine (1925) ArticleTitleOn the inheritance of dwarfism in rice. Nippon Gakujyutsukaihou 1 308–314
M Ashikari J Wu M Yano T Sasaki A Yoshimura (1999) ArticleTitleRice gibberellin-insensitive dwarf mutant gene Dwarf 1 encodes the alpha-subunit of GTP-binding protein. PNAS 96 10284–10289 Occurrence Handle10.1073/pnas.96.18.10284 Occurrence Handle1:CAS:528:DyaK1MXlvFens7s%3D Occurrence Handle10468600
M Ashikari A Sasaki M Ueguchi-Tanaka H Itoh A Nishimura SK Datta K Ishiyama T Saito T Kobayashi GS Khush H Kitano M Matsuoka (2002) ArticleTitleLoss-of-function of a rice gibberellin biosynthetic gene, GA20 oxidase (GA20ox-2), led to the rice ‘green revolution’. Breeding Science 52 143–150 Occurrence Handle10.1270/jsbbs.52.143 Occurrence Handle1:CAS:528:DC%2BD38XlvFOgurk%3D
PM Chandler (1998) ArticleTitleHormonal regulation of gene expression in the “slender” mutant of barley (Hordeum vulgare L. Planta 175 115–120
PM Chandler A Marion-Poll M Ellis F Gubler (2002) ArticleTitleMutants at the Slender1 locus of barley cv Himalaya. Molecular and physiological characterization. Plant Physiol 129 181–190 Occurrence Handle10.1104/pp.010917 Occurrence Handle1:CAS:528:DC%2BD38XjvFSnu7Y%3D
SJ Croker P Hedden JR Lenton J Stoddart (1990) ArticleTitleComparison of gibberellin in normal and slender barley seedlings. Plant Physiol 94 194–200 Occurrence Handle1:CAS:528:DyaK3MXjvFejtQ%3D%3D
RJ Dashaies (1999) ArticleTitleSCF and Cullin/Ring H2-based ubiquitin ligases. Annu Rev Cell 15 435–467 Occurrence Handle10611969
PJ Davies (1995) Plant hormones: physiology, biochemistry and molecular biology. Kluwer Academic Publishers. Doedrecht, the Netherlands.
A Dill HS Jung TP Sun (2001) ArticleTitleThe DELLA motif is essential for gibberellin-induced degradation of RGA. PNAS 98 14162–14167 Occurrence Handle10.1073/pnas.251534098 Occurrence Handle1:CAS:528:DC%2BD3MXovVyms7c%3D Occurrence Handle11717468
A Dill T Sun (2001) ArticleTitleSynergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. Genetics 159 777–785 Occurrence Handle1:CAS:528:DC%2BD3MXot1SrsLk%3D Occurrence Handle11606552
Q Feng Y Zhang P Hao et al. (2002) ArticleTitleSequence and analysis of rice chromosome 4. Nature 420 316–320 Occurrence Handle10.1038/nature01183 Occurrence Handle1:CAS:528:DC%2BD38XovVektL8%3D Occurrence Handle12447439
B Fleck NP Harberd (2002) ArticleTitleEvidence that the Arabidopsis nuclear gibberellin signaling protein GAI is not destabilized by gibberellin. Plant J 32 935–947 Occurrence Handle10.1046/j.1365-313X.2002.01478.x Occurrence Handle1:CAS:528:DC%2BD3sXotFerug%3D%3D Occurrence Handle12492836
CA Foster (1977) ArticleTitleSlender: an accelerated extension growth mutant of barley. Barley Genetics Newsletter 7 24–27
X Fu DE Richards T Ait-Ali LW Hynes H Ougham J Peng NP Harberd (2002) ArticleTitleGibberellin-mediated proteasome-dependent degradation of the barley DELLA protein SLN1 repressor. Plant Cell 14 3191–3200
Y Fujisawa T Kato S Ohki A Ishikawa H Kitano T Sasaki T Asahi Y Iwasaki (1999) ArticleTitleSuppression of the heterotrimeric G protein causes abnormal morphology, including dwarfism, in rice. PNAS 96 7575–7580 Occurrence Handle10.1073/pnas.96.13.7575 Occurrence Handle10377457
MD Gale KM Devos (1998) ArticleTitleComparative genetics in the grasses. PNAS 96 10284–10289
SA Goff D Ricke TH Lan et al. (2002) ArticleTitleA draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296 92–100 Occurrence Handle1:CAS:528:DC%2BD38XivVSqtrw%3D Occurrence Handle11935018
F Gubler PM Chandler RG White DJ Llewellyn JV Jacobsen (2002) ArticleTitleGibberellin signaling in barley aleurone cells. Control of SLN1 and GAMYB expression. Plant Physiol 129 191–200 Occurrence Handle10.1104/pp.010918 Occurrence Handle1:CAS:528:DC%2BD38XjvFSnu7c%3D Occurrence Handle12011350
NP Harberd M Freeling (1989) ArticleTitleGenetics of dominant gibberellin-insensitive dwarfism in maize. Genetics 121 827–838
P Hedden AL Phillips (2000) ArticleTitleGibberellin metabolism: new insights revealed by the genes. Trend Plant Sci 5 523–530 Occurrence Handle10.1016/S1360-1385(00)01790-8
R Hooley (1994) ArticleTitleGibberellin: perception, transduction and responses. Plant Mol Bio 26 1529–1555 Occurrence Handle1:CAS:528:DyaK2MXjvFeksrk%3D Occurrence Handle7858203
S Hori (1898) ArticleTitleSome observation on “Bakanae” disease of the rice plant. Mem Agric Res Sta (Tokyo) 12 110–119
A Ikeda M Ueguchi-Tanaka Y Sonoda H Kitano M Koshioka Y Futsuhara M Matsuoka J Yamaguchi (2001) ArticleTitle 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. Plant Cell 13 999–1010 Occurrence Handle1:CAS:528:DC%2BD3MXktVSlurk%3D Occurrence Handle11340177
H Itoh M Ueguchi-Tanaka N Sentoku H Kitano M Matsuoka M Kobayashi (2001) ArticleTitleCloning and functional analysis of two gibberellin 3 beta-hydroxylase genes that are differently expressed during the growth of rice. PNAS 98 8909–8914 Occurrence Handle10.1073/pnas.141239398 Occurrence Handle1:CAS:528:DC%2BD3MXls1Wiu7k%3D Occurrence Handle11438692
H Itoh M Ueguchi-Tanaka Y Sato M Ashikari M Matsuoka (2002) ArticleTitleThe gibberellin signaling pathway is regulated by the appearance and disappearance of SLENDER RICE1 in nuclei. Plant Cell 14 57–70
N Iwata T Omura (1975) ArticleTitleStudies on the trisomics in rice plants. (Oryza sativa L.), III. Relation between trisomics and genetic linkage groups. Japan J Breed 25 363–368
AM Jones (2002) ArticleTitleG-protein-coupled signaling in Arabidopsis. Curr Opin Plant Biol 5 402–407 Occurrence Handle10.1016/S1369-5266(02)00288-1 Occurrence Handle1:CAS:528:DC%2BD38XmtlGjtLo%3D Occurrence Handle12183178
GS Khush (1999) ArticleTitleGreen revolution: preparing for the 21st century. Genome 42 646–655 Occurrence Handle1:STN:280:DyaK1MzpsVSmtw%3D%3D Occurrence Handle10464789
T Kinoshita (1995) ArticleTitleReport of committee on gene symbolization, nomenclature and linkage groups. Rice Genetics Newsletter 12 9–153
M Koornneef A Elgersma CJ Hanhart EP von Loenen-Martinet L van Rign JAD Zeevaart (1985) ArticleTitleA gibberellin insensitive mutant of Arabidopsis thaliana. Physiol Plant 65 33–39 Occurrence Handle1:CAS:528:DyaL2MXlslGmtLk%3D
E Kurosawa (1926) ArticleTitleExperimental studies on the nature of the substance secreted by the “bakanae” fungus. Nat Hist Soc Formosa 16 213–227
MB Lanahan THD Ho (1988) ArticleTitleSlender barley: a constitutive gibberellin-response mutant. Planta 175 107–114 Occurrence Handle1:CAS:528:DyaL1cXlsVKnsrk%3D
DL Laurenzio J Wysocka-Diller JE Malamy L Pysh Y Helariutta G Freshour MG Hahn KA Feldmann PN Benfey (1996) ArticleTitleThe SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86 423–433 Occurrence Handle8756724
S Lee H Cheng KE King W Wang Y He A Hussain J Lo NP Harverd J Peng (2002) ArticleTitleGibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following inhibition. Gene Develop 16 646–658 Occurrence Handle10.1101/gad.969002 Occurrence Handle1:CAS:528:DC%2BD38XitVWltbY%3D
FN Li M Johnston (1997) ArticleTitleGrr1 of Saccharomyces cerevisiae is connected to the ubiquitin proteolysis machinery through Skp1: coupling glucose sensing to gene expression and the cell cycle. EMBO J 16 5629–5638 Occurrence Handle9312022
S Mitsunaga T Tashiro J Yamaguchi (1994) ArticleTitleIdentification and characterization of gibberellin-insensitive mutants selected from among dwarf mutants of rice. Theor Appl Genet 87 705–712
S Nagao M Takahashi (1963) ArticleTitleTrial construction of twelve linkage groups in Japanese rice. (Genetical studies on rice plant, XXVII). J Facul Agr Hokkaido Univ 53 72–130
SR Neves PT Ram R Iyengar (2002) ArticleTitleG protein pathways. Science 296 1636–1639 Occurrence Handle10.1126/science.1071550 Occurrence Handle1:CAS:528:DC%2BD38XktlChtrY%3D Occurrence Handle12040175
RC Nolan THD Ho (1988) ArticleTitleHormonal regulation of gene expression in barley aleurone layers. Planta 174 551–560 Occurrence Handle1:CAS:528:DyaL1cXkslSmtLo%3D
M Ogawa T Kusano M Katsumi H Sano (2000) ArticleTitleRice giberellin-insensitive gene homolog, OsGAI, encodes a nuclear-localized protein capable of gene activation at transcriptional level. Gene 245 21–29 Occurrence Handle10.1016/S0378-1119(00)00018-4 Occurrence Handle1:CAS:528:DC%2BD3cXhsFanu78%3D Occurrence Handle10713441
N Olszewski TP Sun F Gubler (2002) ArticleTitleGibberellin signaling: biosynthesis, catabolism, and response pathway. Plant Cell 14 61–80
J Peng NP Harberd (1993) ArticleTitleDerivative alleles of the Arabidopsis gibberellin-insensitive (gai) mutation confer a wild-type phenotype. Plant Cell 5 351–360
J Peng P Carol DE Richards KE King RJ Cowling GP Murphy NP Harberd (1997) ArticleTitleThe Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Gene Develop 11 3194–3205 Occurrence Handle1:CAS:528:DyaK1cXntlKr
J Peng DE Richards NM Hartley et al. (1999) ArticleTitle‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400 256–261 Occurrence Handle1:CAS:528:DyaK1MXkvFWltbg%3D Occurrence Handle10421366
JC Pozo MB Boniotti C Gutierrez (2002) ArticleTitle Arabidopsis E2Fc function in cell division and is degraded by the ubiquitin-SCFAtSKP2 pathway in response to light. Plant Cell 14 3057–3071
LD Pysh JW Wysocka-Diller C Camilleri D Bouchez PN Benfey (1999) ArticleTitleThe GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J 18 111–119 Occurrence Handle10.1046/j.1365-313X.1999.00431.x Occurrence Handle10341448
JB Reid (1993) ArticleTitlePlant hormone mutants. J Plant Growth Regul 12 207–226 Occurrence Handle1:CAS:528:DyaK2cXisVSjtr8%3D
JJ Ross IC Murfet JB Reid (1997) ArticleTitleGibberellin mutants. Physiol Plant 100 550–560 Occurrence Handle10.1034/j.1399-3054.1997.1000317.x Occurrence Handle1:CAS:528:DyaK2sXks1yqs7o%3D
A Sasaki M Ashikari M Ueguchi-Tanaka et al. (2002) ArticleTitleGreen revolution: a mutant gibberellin-synthesis gene in rice. Nature 416 701–702 Occurrence Handle10.1038/416701a Occurrence Handle1:CAS:528:DC%2BD38XjtVKks78%3D Occurrence Handle11961544
A Sasaki H Itoh K Gomi M Ueguchi-Tanaka K Ishiyama M Kobayashi D-H Jeong G An H , Kitano M Ashikari M Matsuoka (2003) ArticleTitleA defect in an F-box gene causes accumulation of the phosphorylated repressor protein for GA signaling. . Occurrence Handle10.1103/PhysRevB.67.035303
T Sasaki T Matsumoto K Yamamoto et al. (2002) ArticleTitleThe genome sequence and structure of rice chromosome 1. Nature 420 312–316 Occurrence Handle10.1038/nature01184 Occurrence Handle1:CAS:528:DC%2BD38XovVektLw%3D Occurrence Handle12447438
K Sawada (1912) ArticleTitleThe disease of crops in Taiwan. Formosan Agricultural Review.
AL Silverstone PY Mak EC Martinez TP Sun (1997) ArticleTitleThe new RGA locus encodes a negative regulator of gibberellin response in Arabidopsis thaliana . Genetics 146 1087–1099 Occurrence Handle1:CAS:528:DyaK2sXmsVarur4%3D Occurrence Handle9215910
AL Silverstone CN Ciampaglio TS Sun (1998) ArticleTitleThe Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell 10 155–169 Occurrence Handle1:CAS:528:DyaK1cXhsF2mtr8%3D Occurrence Handle9490740
AL Silverstone HS Jung A Dill H Kawaide Y Kamiya TS Sun (2001) ArticleTitleRepressing a repressor: gibberellin-induced rapid reduction of the RGA protein in Arabidopsis. Plant Cell 13 1555–1566
D Skowyra KL Craig M Tyers SJ Elledge JW Harper (1997) ArticleTitleF-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 91 209–219 Occurrence Handle1:CAS:528:DyaK2sXntVyiu7s%3D Occurrence Handle9346238
W Spielmeyer MH Ellis PM Chandler (2002) ArticleTitleSemidwarf (sd-1) “green revolution” rice, contains a defective gibberellin 20-oxidase gene. PNAS 99 9043–9048 Occurrence Handle10.1073/pnas.132266399 Occurrence Handle1:CAS:528:DC%2BD38XltF2hu74%3D Occurrence Handle12077303
U Suharsono Y Fujisawa T Kawasaki Y Iwasaki H Satoh K Shimamoto (2002) ArticleTitleThe heterotrimeric G protein alpha subunit acts upstream of the small GTPase Rac in disease resistance of rice. PNAS 99 13307–13312 Occurrence Handle10.1073/pnas.192244099 Occurrence Handle1:CAS:528:DC%2BD38XnvFGgs7c%3D Occurrence Handle12237405
TM Thornton SM Swain NE Olszewski (1999) ArticleTitleGibberellin signal transduction presents ellipsisthe SPY who O-GleNAc’d me. Trends Plant Sci 4 424–428 Occurrence Handle10.1016/S1360-1385(99)01485-5 Occurrence Handle10529823
M Ueguchi-Tanaka Y Fujisawa M Kobayashi M Ashikari Y Iwasaki H Kitano M Matsuoka (2000) ArticleTitleRice dwarf mutant d1, which is defective in the subunit of the heterotrimeric G protein, affects gibberellin signal transduction. PNAS 97 11638–11643 Occurrence Handle10.1073/pnas.97.21.11638 Occurrence Handle1:CAS:528:DC%2BD3cXnsF2qtr8%3D Occurrence Handle11027362
CK Wen C Chang (2002) ArticleTitle Arabidopsis RGL1 encodes a negative regulator of gibberellin response. Plant Cell 14 87–1000
PT White (1994) ArticleTitleRice: the essential harvest. Natl Geogr 185 48–79
RG Winkler M Freeling (1994) ArticleTitlePhysiological genetics of the dominant gibberellin-nonresponsive maize dwarf, Dwarf8 and Dwarf9. Planta 193 341–348 Occurrence Handle1:CAS:528:DyaK2cXisVSgs70%3D
JT Winston P Strack P Beer-Romero CY Chu SJ Elledge JW Harper (1999) ArticleTitleThe SCF-TRCP-ubiquitin ligase complex associates specifically with phosphorylated destruction motifs in IB and -catenin and stimulates IB ubiquitination in vitro. Genes Dev 13 270–283 Occurrence Handle10.1101/gad.13.21.2751 Occurrence Handle1:CAS:528:DyaK1MXht1Kgtrs%3D Occurrence Handle9990852
YL Xu L Li DA Gage JA Zeevaart (1999) ArticleTitleFeedback regulation of GAS expression and metabolic engineering of gibberellin levels in Arabidopsis. Plant Cell 11 927–936
T Yabuta Y Sumiki (1938) ArticleTitleOn the crystal of gibberellin, a substance to promote plant growth. J Agric Chem Soc Japan 14 1526
M Yang Y Hu M Lodhi WR McCombie H Ma (1999) ArticleTitleThe Arabidapsis SKP1-LIKE1 gene is essential for male meiosis and may control homologue separation. PNAS 96 11416–11421 Occurrence Handle10.1073/pnas.96.20.11416 Occurrence Handle1:CAS:528:DyaK1MXmvVCmsbc%3D Occurrence Handle10500191
J Yu S Hu J Wang et al. (2002) ArticleTitleA draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296 79–92 Occurrence Handle1:CAS:528:DC%2BD38XivVSqtr8%3D Occurrence Handle11935017
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Ashikari, M., Hironori, I., Miyako, UT. et al. Gibberellin Signal Transduction in Rice . J Plant Growth Regul 22, 141–151 (2003). https://doi.org/10.1007/s00344-003-0033-8
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DOI: https://doi.org/10.1007/s00344-003-0033-8