Abstract
Key message
SCL3 inhibits transcriptional activity of IDD-DELLA complex by acting as a co-repressor and repression activity is enhanced in the presence of GAF1 in a TOPLESS-independent manner.
Abstract
GRAS [GIBBERELLIN-INSENSITIVE (GAI), REPRESSOR OF ga1-3 (RGA) and SCARECROW (SCR)] proteins are a family of plant-specific transcriptional regulators that play diverse roles in development and signaling. GRAS family DELLA proteins act as growth repressors by inhibiting gibberellin (GA) signaling in response to developmental and environmental cues. DELLAs also act as co-activators of transcription factor GAI-ASSOCIATED FACTOR1 (GAF1)/INDETERMINATE DOMAIN2 (IDD2), the GAF1-DELLA complex activating transcription of GAF1 target genes. GAF1 also interacts with TOPLESS (TPL), a transcriptional co-repressor, in the absence of DELLA, the GAF1-TPL complex repressing transcription of the target genes. SCARECROW-LIKE3 (SCL3), another member of the GRAS family, is thought to inhibit transcriptional activity of the IDD-DELLA complex through competitive interaction with IDD. Here, we also revealed that SCL3 inhibits transcriptional activation by the GAF1-DELLA complex via repression activity rather than via competitive inhibition of the GAF1-DELLA interaction. Moreover, the repression activity of SCL3 was enhanced by GAF1 in a TPL-independent manner. While the GRAS domain of DELLA has transcriptional activation activity, that of SCL3 has repression activity. SCL3 also inhibited transcriptional activity of GAF1-RGA fusion proteins. Results from the co-immunoprecipitation assays and the yeast three-hybrid assay suggested the possibility that SCL3 forms a ternary complex with GAF1 and DELLA. These findings provide important information on DELLA-regulated GA signaling and new insight into the transcriptional repression mechanism.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in this published article and its supplementary information files.
References
Aoyanagi T, Ikeya S, Kobayashi A, Kozaki A (2020) Gene regulation via the combination of transcription factors in the INDETERMINATE DOMAIN and GRAS families. Genes 11:1–18. https://doi.org/10.3390/genes11060613
Bai MY, Shang JX, Oh E, Fan M, Bai Y, Zentella R, Sun T, Wang ZY (2012) Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat Cell Biol 14:810–817. https://doi.org/10.1038/ncb2546
Bolle C (2004) The role of GRAS proteins in plant signal transduction and development. Planta 218:683–692. https://doi.org/10.1007/s00425-004-1203-z
Causier B, Ashworth M, Guo W, Davies B (2012) The TOPLESS interactome: a framework for gene repression in Arabidopsis. Plant Physiol 158:423–438. https://doi.org/10.1104/pp.111.186999
Cheng H, Qin L, Lee S, Fu X, Richards DE, Cao D, Luo D, Harberd NP, Peng J (2004) Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function. Development 131:1055–1064. https://doi.org/10.1242/dev.00992
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. https://doi.org/10.1046/j.1365-313X.1998.00343.x
Coelho CP, Huang P, Lee DY, Brutnell TP (2018) Making roots, shoots, and seeds: IDD gene family diversification in plants. Trends Plant Sci 23:66–78. https://doi.org/10.1016/j.tplants.2017.09.008
Colasanti J, Tremblay R, Wong AYM, Coneva V, Kozaki A, Mable BK (2006) The maize INDETERMINATE1 flowering time regulator defines a highly conserved zinc finger protein family in higher plants. BMC Genomics 7:158. https://doi.org/10.1186/1471-2164-7-158
Colasanti J, Yuan Z, Sundaresan V (1998) The indeterminate gene encodes a zinc finger protein and regulates a leaf-generated signal required for the transition to flowering in maize. Cell 93:593–603. https://doi.org/10.1016/S0092-8674(00)81188-5
Cui H, Levesque MP, Vernoux T, Jung JW, Paquette AJ, Gallagher KL, Wang JY, Blilou I, Scheres B, Benfey PN (2007) An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316:421–425. https://doi.org/10.1126/science.1139531
Davière JM, Achard P (2016) A pivotal role of DELLAs in regulating multiple hormone signals. Mol Plant 9:10–20. https://doi.org/10.1016/j.molp.2015.09.011
de Lucas M, Davière JM, Rodríguez-Falcón M, Pontin M, Iglesias-Pedraz JM, Lorrain S, Fankhauser C, Blázquez MA, Titarenko E, Prat S (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451:480–484. https://doi.org/10.1038/nature06520
Dill A, Sun T (2001) Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. Genetics 159:777–785
Dill A, Thomas SG, Hu J, Steber CM, Sun T (2004) The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degradation. Plant Cell 16:1392–1405. https://doi.org/10.1105/tpc.020958
Fang RX, Nagy F, Sivasubramaniam S, Chua NH (1989) Multiple cis regulatory elements for maximal expression of the cauliflower mosaic virus 35S promoter in transgenic plants. Plant Cell 1:141–150. https://doi.org/10.1105/tpc.1.1.141
Feng S, Martinez C, Gusmaroli G, Wang Y, Zhou J, Wang F, Chen L, Yu L, Iglesias-Pedraz JM, Kircher S et al (2008) Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451:475–479. https://doi.org/10.1038/nature06448
Fukazawa J, Ito T, Kamiya Y, Yamaguchi S, Takahashi Y (2015) Binding of GID1 to DELLAs promotes dissociation of GAF1 from DELLA in GA dependent manner. Plant Signal Behav 10:e1052923. https://doi.org/10.1080/15592324.2015.1052923
Fukazawa J, Mori M, Watanabe S, Miyamoto C, Ito T, Takahashi Y (2017) DELLA-GAF1 complex is a main component in gibberellin feedback regulation of GA20 oxidase 2. Plant Physiol 175:1395–1406. https://doi.org/10.1104/pp.17.00282
Fukazawa J, Teramura H, Murakoshi S, Nasuno K, Nishida N, Ito T, Yoshida M, Kamiya Y, Yamaguchi S, Takahashi Y (2014) DELLAs function as coactivators of GAI-ASSOCIATED FACTOR1 in regulation of gibberellin homeostasis and signaling in Arabidopsis. Plant Cell 26:2920–2938. https://doi.org/10.1105/tpc.114.125690
Gallavotti A, Long JA, Stanfield S, Yang X, Jackson D, Vollbrecht E, Schmidt RJ (2010) The control of axillary meristem fate in the maize ramosa pathway. Development 137:2849–2856. https://doi.org/10.1242/dev.051748
Gao M-J, Li X, Huang J, Gropp GM, Gjetvaj B, Lindsay DL, Wei S, Coutu C, Chen Z, Wan X-C et al (2015) SCARECROW-LIKE15 interacts with HISTONE DEACETYLASE19 and is essential for repressing the seed maturation programme. Nat Commun 6:7243. https://doi.org/10.1038/ncomms8243
Gong X, Flores-Vergara MA, Hong JH, Chu H, Lim J, Franks RG, Liu Z, Xu J (2016) SEUSS integrates gibberellin signaling with transcriptional inputs from the SHR-SCR-SCL3 module to regulate middle cortex formation in the Arabidopsis root. Plant Physiol 170:1675–1683. https://doi.org/10.1104/pp.15.01501
Goodrich JA, Hoey T, Thut CJ, Admon A, Tjian R (1993) Drosophila TAFII40 interacts with both a VP16 activation domain and the basal transcription factor TFIIB. Cell 75:519–530. https://doi.org/10.1016/0092-8674(93)90386-5
Griffiths J, Murase K, Rieu I, Zentella R, Zhang ZL, Powers SJ, Gong F, Phillips AL, Hedden P, Sun T, Thomas SG (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18:3399–3414. https://doi.org/10.1105/tpc.106.047415
Gupta R, Emili A, Pan G, Xiao H, Shales M, Greenblatt J, Ingles CJ (1996) Characterization of the interaction between the acidic activation domain of VP16 and the RNA polymerase II initiation factor TFIIB. Nucleic Acids Res 24:2324–2330. https://doi.org/10.1093/nar/24.12.2324
Hakoshima T (2018) Structural basis of the specific interactions of GRAS family proteins. FEBS Lett 592:489–501. https://doi.org/10.1002/1873-3468.12987
Hedden P, Thomas SG (2012) Gibberellin biosynthesis and its regulation. Biochem J 444:11–25. https://doi.org/10.1042/BJ20120245
Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser MT, Benfey PN (2000) The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101:555–567. https://doi.org/10.1016/S0092-8674(00)80865-X
Heo J, Chang KS, Kim IA, Lee M, Lee SA, Song S, Lee MM, Lim J (2011) Funneling of gibberellin signaling by the GRAS transcription regulator SCARECROW-LIKE 3 in the Arabidopsis root. Proc Natl Acad Sci USA 108:2166–2171. https://doi.org/10.1073/pnas.1012215108
Hirano K, Kouketu E, Katoh H, Aya K, Ueguchi-Tanaka M, Matsuoka M (2012) The suppressive function of the rice DELLA protein SLR1 is dependent on its transcriptional activation activity. Plant J 71:443–453. https://doi.org/10.1111/j.1365-313X.2012.05000.x
Hirano Y, Nakagawa M, Suyama T, Murase K, Shirakawa M, Takayama S, Sun T-P, Hakoshima T (2017) Structure of the SHR-SCR heterodimer bound to the BIRD/IDD transcriptional factor JKD. Nat plants 3:17010. https://doi.org/10.1038/nplants.2017.10
Hiratsu K, Matsui K, Koyama T, Ohme-Takagi M (2003) Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J 34:733–739. https://doi.org/10.1046/j.1365-313X.2003.01759.x
Hiratsu K, Mitsuda N, Matsui K, Ohme-Takagi M (2004) Identification of the minimal repression domain of SUPERMAN shows that the DLELRL hexapeptide is both necessary and sufficient for repression of transcription in Arabidopsis. Biochem Biophys Res Commun 321:172–178. https://doi.org/10.1016/j.bbrc.2004.06.115
Hou X, Lee LYC, Xia K, Yan Y, Yu H (2010) DELLAs modulate jasmonate signaling via competitive binding to JAZs. Dev Cell 19:884–894. https://doi.org/10.1016/j.devcel.2010.10.024
Ikeda A, Ueguchi-Tanaka M, Sonoda Y, Kitano H, Koshioka M, Futsuhara Y, Matsuoka M, Yamaguchi J (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. Plant Cell 13:999–1010. https://doi.org/10.1105/tpc.13.5.999
Ikeda M, Ohme-Takagi M (2009) A novel group of transcriptional repressors in Arabidopsis. Plant Cell Physiol 50:970–975. https://doi.org/10.1093/pcp/pcp048
Ito T, Nakata M, Fukazawa J, Ishida S, Takahashi Y (2010) Alteration of substrate specificity: the variable N-terminal domain of tobacco Ca2+-dependent protein kinase is important for substrate recognition. Plant Cell 22:1592–1604. https://doi.org/10.1105/tpc.109.073577
Itoh H, Ueguchi-Tanaka M, Sato Y, Ashikari M, Matsuoka M (2002) The gibberellin signaling pathway is regulated by the appearance and disappearance of SLENDER RICE1 in nuclei. Plant Cell 14:57–70. https://doi.org/10.1105/tpc.010319
James P, Halladay J, Craig EA (1996) Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144:1425–1436
Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907. https://doi.org/10.1002/j.1460-2075.1987.tb02730.x
Kagale S, Links MG, Rozwadowski K (2010) Genome-wide analysis of ethylene-responsive element binding factor-associated amphiphilic repression motif-containing transcriptional regulators in Arabidopsis. Plant Physiol 152:1109–1134. https://doi.org/10.1104/pp.109.151704
Ke J, Ma H, Gu X, Thelen A, Brunzelle JS, Li J, Xu HE, Melcher K (2015) Structural basis for recognition of diverse transcriptional repressors by the TOPLESS family of corepressors. Sci Adv 1:e1500107. https://doi.org/10.1126/sciadv.1500107
Keleher CA, Redd MJ, Schultz J, Carlson M, Johnson AD (1992) Ssn6-Tup1 is a general repressor of transcription in yeast. Cell 68:709–719. https://doi.org/10.1016/0092-8674(92)90146-4
King KE, Moritz T, Harberd NP (2001) Gibberellins are not required for normal stem growth in Arabidopsis thaliana in the absence of GAI and RGA. Genetics 159:767–776
Kumar M, Le DT, Hwang S, Seo PJ, Kim HU (2019) Role of the INDETERMINATE DOMAIN genes in plants. Int J Mol Sci 20:2286. https://doi.org/10.3390/ijms20092286
Lee S, Cheng H, King KE, Wang W, He Y, Hussain A, Lo J, Harberd NP, Peng J (2002) Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes Dev 16:646–658. https://doi.org/10.1101/gad.969002
Li E, Wang S, Liu Y, Chen JG, Douglas CJ (2011) OVATE FAMILY PROTEIN4 (OFP4) interaction with KNAT7 regulates secondary cell wall formation in Arabidopsis thaliana. Plant J 67:328–341. https://doi.org/10.1111/j.1365-313X.2011.04595.x
Li S, Zhao Y, Zhao Z, Wu X, Sun L, Liu Q, Wu Y (2016) Crystal structure of the GRAS domain of SCARECROW-LIKE7 in Oryza sativa. Plant Cell 28:1025–1034. https://doi.org/10.1105/tpc.16.00018
Liu Y, Douglas CJ (2015) A role for OVATE FAMILY PROTEIN1 (OFP1) and OFP4 in a BLH6-KNAT7 multi-protein complex regulating secondary cell wall formation in Arabidopsis thaliana. Plant Signal Behav 10:e1033126. https://doi.org/10.1080/15592324.2015.1033126
Liu Y, You S, Taylor-Teeples M, Li WL, Schuetz M, Brady SM, Douglasa CJ (2014) BEL1-LIKE HOMEODOMAIN6 and KNOTTED ARABIDOPSIS THALIANA7 interact and regulate secondary cell wall formation via repression of REVOLUTA. Plant Cell 26:4843–4861. https://doi.org/10.1105/tpc.114.128322
Liu Z, Karmarkar V (2008) Groucho/Tup1 family co-repressors in plant development. Trends Plant Sci 13:137–144. https://doi.org/10.1016/j.tplants.2007.12.005
Long JA, Ohno C, Smith ZR, Meyerowitz EM (2006) TOPLESS regulates apical embryonic fate in Arabidopsis. Science 312:1520–1523. https://doi.org/10.1126/science.1123841
Long Y, Smet W, Cruz-Ramírez A, Castelijns B, de Jonge W, Mähönen AP, Bouchet BP, Perez GS, Akhmanova A, Scheres B et al (2015) Arabidopsis BIRD zinc finger proteins jointly stabilize tissue boundaries by confining the cell fate regulator SHORT-ROOT and contributing to fate specification. Plant Cell 27:1185–1199. https://doi.org/10.1105/tpc.114.132407
Marín-de la Rosa N, Pfeiffer A, Hill K, Locascio A, Bhalerao RP, Miskolczi P, Gronlund AL, Wanchoo-Kohli A, Thomas SG, Bennett MJ et al (2015) Genome wide binding site analysis reveals transcriptional coactivation of cytokinin-responsive genes by DELLA proteins. PLoS Genet 11:e1005337. https://doi.org/10.1371/journal.pgen.1005337
Matsui K, Umemura Y, Ohme-Takagi M (2008) AtMYBL2, a protein with a single MYB domain, acts as a negative regulator of anthocyanin biosynthesis in Arabidopsis. Plant J 55:954–967. https://doi.org/10.1111/j.1365-313X.2008.03565.x
Matsushita A, Furumoto T, Ishida S, Takahashi Y (2007) AGF1, an AT-hook protein, is necessary for the negative feedback of AtGA3ox1 encoding GA 3-oxidase. Plant Physiol 143:1152–1162. https://doi.org/10.1104/pp.106.093542
McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM, Sun T, Steber CM (2003) The ArabidopsisSLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15:1120–1130. https://doi.org/10.1105/tpc.010827
Meier C, Bouquin T, Nielsen ME, Raventos D, Mattsson O, Rocher A, Schomburg F, Amasino RM, Mundy J (2001) Gibberellin response mutants identified by luciferase imaging. Plant J 25:509–519. https://doi.org/10.1046/j.1365-313x.2001.00980.x
Nakajima K, Sena G, Nawy T, Benfey PN (2001) Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413:307–311. https://doi.org/10.1038/35095061
Odell JT, Nagy F, Chua N-H (1985) Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter. Nature 313:810–812. https://doi.org/10.1038/313810a0
Ogasawara H, Kaimi R, Colasanti J, Kozaki A (2011) Activity of transcription factor JACKDAW is essential for SHR/SCR-dependent activation of SCARECROW and MAGPIE and is modulated by reciprocal interactions with MAGPIE, SCARECROW and SHORT ROOT. Plant Mol Biol 77:489–499. https://doi.org/10.1007/s11103-011-9826-5
Ohta M, Matsui K, Hiratsu K, Shinshi H, Ohme-Takagi M (2001) Repression domains of class II ERF transcriptional repressors share an essential motif for active repression. Plant Cell 13:1959–1968. https://doi.org/10.1105/tpc.010127
Okegawa Y, Motohashi K (2015) A simple and ultra-low cost homemade seamless ligation cloning extract (SLiCE) as an alternative to a commercially available seamless DNA cloning kit. Biochem Biophys reports 4:148–151. https://doi.org/10.1016/j.bbrep.2015.09.005
Paroush Z, Finley RL, Kidd T, Wainwright SM, Ingham PW, Brent R, Ish-Horowicz D (1994) Groucho is required for Drosophila neurogenesis, segmentation, and sex determination and interacts directly with hairy-related bHLH proteins. Cell 79:805–815. https://doi.org/10.1016/0092-8674(94)90070-1
Pauwels L, Barbero GF, Geerinck J, Tilleman S, Grunewald W, Pérez AC, Chico JM, Vanden BR, Sewell J, Gil E et al (2010) NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464:788–791. https://doi.org/10.1038/nature08854
Pennacchio LA, Bickmore W, Dean A, Nobrega MA, Bejerano G (2013) Enhancers: five essential questions. Nat Rev Genet 14:288–295. https://doi.org/10.1038/nrg3458
Pysh LD, Wysocka-Diller JW, Camilleri C, Bouchez D, Benfey PN (1999) The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J 18:111–119. https://doi.org/10.1046/j.1365-313X.1999.00431.x
Sasaki A, Itoh H, Gomi K, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M, Jeong DH, An G, Kitano H, Ashikari M, Matsuoka M (2003) Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science 299:1896–1898. https://doi.org/10.1126/science.1081077
Silverstone AL, Mak PY, Martínez EC, Sun TP (1997) The new RGA locus encodes a negative regulator of gibberellin response in Arabidopsis thaliana. Genetics 146:1087–1099
Stringer KF, Ingles CJ, Greenblatt J (1990) Direct and selective binding of an acidic transcriptional activation domain to the TATA-box factor TFIID. Nature 345:783–786. https://doi.org/10.1038/345783a0
Sun TP (2011) The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr Biol 21:R338-345. https://doi.org/10.1016/j.cub.2011.02.036
Sun TP, Kamiya Y (1994) The ArabidopsisGA1 locus encodes the cyclase ent-kaurene synthetase A of gibberellin biosynthesis. Plant Cell 6:1509–1518. https://doi.org/10.1105/tpc.6.10.1509
Sun X, Jones WT, Rikkerink EHA (2012) GRAS proteins: the versatile roles of intrinsically disordered proteins in plant signalling. Biochem J 442:1–12. https://doi.org/10.1042/BJ20111766
Szemenyei H, Hannon M, Long JA (2008) TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319:1384–1386. https://doi.org/10.1126/science.1151461
Takeo K, Ito T (2017) Subcellular localization of VIP1 is regulated by phosphorylation and 14–3-3 proteins. FEBS Lett 591:1972–1981. https://doi.org/10.1002/1873-3468.12686
Tian C, Wan P, Sun S, Li J, Chen M (2004) Genome-wide analysis of the GRAS gene family in rice and Arabidopsis. Plant Mol Biol 54:519–532. https://doi.org/10.1023/B:PLAN.0000038256.89809.57
Tiwari SB, Hagen G, Guilfoyle TJ (2004) Aux/IAA proteins contain a potent transcriptional repression domain. Plant Cell 16:533–543. https://doi.org/10.1105/tpc.017384
Trinh R, Gurbaxani B, Morrison SL, Seyfzadeh M (2004) Optimization of codon pair use within the (GGGGS)3 linker sequence results in enhanced protein expression. Mol Immunol 40:717–722. https://doi.org/10.1016/j.molimm.2003.08.006
Tyler L, Thomas SG, Hu J, Dill A, Alonso JM, Ecker JR, Sun TP (2004) DELLA proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant Physiol 135:1008–1019. https://doi.org/10.1104/pp.104.039578
Ubeda-Tomás S, Federici F, Casimiro I, Beemster GTS, Bhalerao R, Swarup R, Doerner P, Haseloff J, Bennett MJ (2009) Gibberellin signaling in the endodermis controls Arabidopsis root meristem size. Curr Biol 19:1194–1199. https://doi.org/10.1016/j.cub.2009.06.023
Ubeda-Tomás S, Swarup R, Coates J, Swarup K, Laplaze L, Beemster GTS, Hedden P, Bhalerao R, Bennett MJ (2008) Root growth in Arabidopsis requires gibberellin/DELLA signalling in the endodermis. Nat Cell Biol 10:625–628. https://doi.org/10.1038/ncb1726
Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E, Kobayashi M, Chow T, Hsing YC, Kitano H, Yamaguchi I, Matsuoka M (2005) GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437:693–698. https://doi.org/10.1038/nature04028
Ueguchi-Tanaka M, Nakajima M, Katoh E, Ohmiya H, Asano K, Saji S, Hongyu X, Ashikari M, Kitano H, Yamaguchi I, Matsuoka M (2007) Molecular interactions of a soluble gibberellin receptor, GID1, with a rice DELLA protein, SLR1, and gibberellin. Plant Cell 19:2140–2155. https://doi.org/10.1105/tpc.106.043729
Van De Velde K, Ruelens P, Geuten K, Rohde A, Van Der Straeten D (2017) Exploiting DELLA signaling in cereals. Trends Plant Sci 22:880–893. https://doi.org/10.1016/j.tplants.2017.07.010
Welch D, Hassan H, Blilou I, Immink R, Heidstra R, 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. https://doi.org/10.1101/gad.440307
Wu F-H, Shen S-C, Lee L-Y, Lee S-H, Chan M-T, Lin C-S (2009) Tape-Arabidopsis Sandwich—a simpler Arabidopsis protoplast isolation method. Plant Methods 5:16. https://doi.org/10.1186/1746-4811-5-16
Xu YL, Li L, Gage DA, Zeevaart JA (1999) Feedback regulation of GA5 expression and metabolic engineering of gibberellin levels in Arabidopsis. Plant Cell 11:927–936. https://doi.org/10.1105/tpc.11.5.927
Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251. https://doi.org/10.1146/annurev.arplant.59.032607.092804
Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572. https://doi.org/10.1038/nprot.2007.199
Yoshida H, Hirano K, Sato T, Mitsuda N, Nomoto M, Maeo K, Koketsu E, Mitani R, Kawamura M, Ishiguro S, Tada Y, Ohme-Takagi M, Matsuoka M, Ueguchi-Tanaka M (2014) DELLA protein functions as a transcriptional activator through the DNA binding of the indeterminate domain family proteins. Proc Natl Acad Sci USA 111:7861–7866. https://doi.org/10.1073/pnas.1321669111
Zentella R, Zhang ZL, Park M, Thomas SG, Endo A, Murase K, Fleet CM, Jikumaru Y, Nambara E, Kamiya Y, Sun TP (2007) Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19:3037–3057. https://doi.org/10.1105/tpc.107.054999
Zhang Z, Ogawa M, Fleet CM, Zentella R, Hu J, Heo J, Lim J, Kamiya Y, Yamaguchi S, Sun T (2011) SCARECROW-LIKE 3 promotes gibberellin signaling by antagonizing master growth repressor DELLA in Arabidopsis. Proc Natl Acad Sci USA 108:2160–2165. https://doi.org/10.1073/pnas.1012232108
Zhu Z, Xu F, Zhang Y, Cheng YT, Wiermer M, Li X, Zhang Y (2010) Arabidopsis resistance protein SNC1 activates immune responses through association with a transcriptional corepressor. Proc Natl Acad Sci U S A 107:13960–13965. https://doi.org/10.1073/pnas.1002828107
Acknowledgements
We thank Kazuya Miyahara, Takayoshi Katsube, Naoyuki Okada, Naoki Taguma, Ayaka Terawaki, Nao Takahashi and Koichi Takeo for their technical support, Dr. Masaru Ohme-Takagi for providing 35S-5×GAL4-TATA:LUC and 5×GAL4-TATA:LUC vectors, Dr. Makoto Kusaba for providing time to write this paper, and Dr. Yohsuke Takahashi for his valuable advice. This work was supported by a grant from the Japan Society for the Promotion of Science awarded to T.I. (17K15143).
Funding
This study was funded by the Japan Society for the Promotion of Science (grant no. 17K15143).
Author information
Authors and Affiliations
Contributions
T.I. conceived the research. T.I. and J.F. designed and performed the experiments. T.I. wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ito, T., Fukazawa, J. SCARECROW-LIKE3 regulates the transcription of gibberellin-related genes by acting as a transcriptional co-repressor of GAI-ASSOCIATED FACTOR1. Plant Mol Biol 105, 463–482 (2021). https://doi.org/10.1007/s11103-020-01101-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-020-01101-z