FKF1 F-box protein promotes flowering in part by negatively regulating DELLA protein stability under long-day photoperiod in Arabidopsis.
Arabidopsis thaliana
DELLA
FKF1
flowering
gibberellic acid
long-day photoperiod
Journal
Journal of integrative plant biology
ISSN: 1744-7909
Titre abrégé: J Integr Plant Biol
Pays: China (Republic : 1949- )
ID NLM: 101250502
Informations de publication
Date de publication:
Nov 2020
Nov 2020
Historique:
received:
08
03
2020
accepted:
18
05
2020
pubmed:
20
5
2020
medline:
22
6
2021
entrez:
20
5
2020
Statut:
ppublish
Résumé
FLAVIN-BINDING KELCH REPEAT F-BOX 1 (FKF1) encodes an F-box protein that regulates photoperiod flowering in Arabidopsis under long-day conditions (LDs). Gibberellin (GA) is also important for regulating flowering under LDs. However, how FKF1 and the GA pathway work in concert in regulating flowering is not fully understood. Here, we showed that the mutation of FKF1 could cause accumulation of DELLA proteins, which are crucial repressors in GA signaling pathway, thereby reducing plant sensitivity to GA in flowering. Both in vitro and in vivo biochemical analyses demonstrated that FKF1 directly interacted with DELLA proteins. Furthermore, we showed that FKF1 promoted ubiquitination and degradation of DELLA proteins. Analysis of genetic data revealed that FKF1 acted partially through DELLAs to regulate flowering under LDs. In addition, DELLAs exerted a negative feedback on FKF1 expression. Collectively, these findings demonstrate that FKF1 promotes flowering partially by negatively regulating DELLA protein stability under LDs, and suggesting a potential mechanism linking the FKF1 to the GA signaling DELLA proteins.
Substances chimiques
Arabidopsis Proteins
0
F-Box Proteins
0
Gibberellins
0
Transcription Factors
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1717-1740Subventions
Organisme : National Natural Science Foundation of China
Organisme : Natural Science Foundation of Hunan Province
Organisme : Basic Research Program of Shenzhen Municipal Science and Technology Innovation Committee
Organisme : Basic Research Program of Changsha Municipal Science and Technology
Informations de copyright
© 2020 Institute of Botany, Chinese Academy of Sciences.
Références
Amasino R (2010) Seasonal and developmental timing of flowering. Plant J 61: 1001-1013
Andrés F, Porri A, Torti S, Mateos J, Romera-Branchat M, García-Martínez JL, Fornara F, Gregis V, Kater MM, Coupland G (2014) SHORT VEGETATIVE PHASE reduces gibberellin biosynthesis at the Arabidopsis shoot apex to regulate the floral transition. Proc Natl Acad Sci USA 111: E2760-E2769
Bai M, Shang J, Oh E, Fan M, Bai Y, Zentella R, Sun T, Wang Z (2012) Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat Cell Biol 14: 810-817
Bao S, Hua C, Shen L, Yu H (2020) New insights into gibberellin signaling in regulating flowering in Arabidopsis. J Integr Plant Biol 62: 118-131
Blázquez MA, Green R, Nilsson O, Sussman MR, Weigel D (1998) Gibberellins promote flowering of Arabidopsis by activating the LEAFY promoter. Plant Cell 10: 791-800
Blázquez MA, Weigel D (2000) Integration of floral inductive signals in Arabidopsis. Nature 404: 889-892
Boss PK, Bastow RM, Mylne JS, Dean C (2004) Multiple pathways in the decision to flower: Enabling, promoting, and resetting. Plant Cell 16(Suppl): S18-S31
Clough SJ, Bent AF (1998) Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, Coupland G (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316: 1030-1033
De Grauwe L, Vriezen WH, Bertrand S, Phillips A, Vidal AM, Hedden P, Van Der Straeten D (2007) Reciprocal influence of ethylene and gibberellins on response-gene expression in Arabidopsis thaliana. Planta 226: 485-498
De Lucas M, Davière J, 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
Dill A, Jung HS, Sun TP (2001) The DELLA motif is essential for gibberellin-induced degradation of RGA. Proc Natl Acad Sci USA 98: 14162-14167
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 TP (2004) The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degradation. Plant Cell 16: 1392-1405
Du C, Li X, Chen J, Chen W, Li B, Li C, Wang L, Li J, Zhao X, Lin J, Liu X, Luan S, Yu F (2016) Receptor kinase complex transmits RALF peptide signal to inhibit root growth in Arabidopsis. Proc Natl Acad Sci USA 113: E8326-E8334
Feng S, Martinez C, Gusmaroli G, Wang Y, Zhou J, Wang F, Chen L, Yu L, Iglesias-Pedraz JM, Kircher S, Schaefer E, Fu X, Fan L, Deng XW (2008) Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451: 475-479
Fleck B, Harberd NP (2002) Evidence that the Arabidopsis nuclear gibberellin signalling protein GAI is not destabilised by gibberellin. Plant J 32: 935-947
Fornara F, Panigrahi KC, Gissot L, Sauerbrunn N, Rühl M, Jarillo JA, Coupland G (2009) Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. Dev Cell 17: 75-86
Fu XD, Richards DE, Fleck B, Xie DX, Burton N, Harberd NP (2004) The Arabidopsis mutant sleepy1(gar2-1) protein promotes plant growth by increasing the affinity of the SCFSLY1 E3 ubiquitin ligase for DELLA protein substrates. Plant Cell 16: 1406-1418
Gallego-Bartolome J, Minguet EG, Grau-Enguix F, Abbas M, Locascio A, Thomas SG, Alabadi D, Blázquez MA (2012) Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in Arabidopsis. Proc Natl Acad Sci USA 109: 13446-13451
Gallego-Bartolome J, Minguet EG, Marin JA, Prat S, Blázquez MA, Alabadi D (2010) Transcriptional diversification and functional conservation between DELLA proteins in Arabidopsis. Mol Biol Evol 27: 1247-1256
Galvão VC, Horrer D, Kuttner F, Schmid M (2012) Spatial control of flowering by DELLA proteins in Arabidopsis thaliana. Development 139: 4072-4082
Gao XH, Huang XZ, Xiao SL, Fu XD (2008) Evolutionarily conserved DELLA-mediated gibberellin signaling in plants. J Integr Plant Biol 50: 825-834
Griffiths J, Murase K, Rieu I, Zentella R, Zhang ZL, Powers SJ, Gong F, Phillips AL, Hedden P, Sun TP, Thomas SG (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18: 3399-3414
He R, Li X, Zhong M, Yan J, Ji R, Li X, Wang Q, Wu D, Sun M, Tang D, Lin J, Li H, Liu B, Liu H, Liu X, Zhao X, Lin C (2017) A photo-responsive F-box protein FOF2 regulates floral initiation by promoting FLC expression in Arabidopsis. Plant J 91: 788-801
Hisamatsu T, King RW (2008) The nature of floral signals in Arabidopsis. II. Roles for FLOWERING LOCUS T (FT) and gibberellin. J Exp Bot 59: 3821-3829
Hou X, Zhou J, Liu C, Liu L, Shen L, Yu H (2014) Nuclear factor Y-mediated H3K27me3 demethylation of the SOC1 locus orchestrates flowering responses of Arabidopsis. Nat Commun 5: 4601
Hwang DY, Park S, Lee S, Lee SS, Imaizumi T, Song YH (2019) GIGANTEA regulates the timing stabilization of CONSTANS by altering the interaction between FKF1 and ZEITLUPE. Mol Cells 42: 693-701
Imaizumi T, Schultz TF, Harmon FG, Ho LA, Kay SA (2005) FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 309: 293-297
Imaizumi T, Tran HG, Swartz TE, Briggs WR, Kay SA (2003) FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature 426: 302-306
Ito S, Song YH, Imaizumi T (2012) LOV domain-containing F-box proteins: Light-dependent protein degradation modules in Arabidopsis. Mol Plant 5: 573-582
Jaeger KE, Wigge PA (2007) FT protein acts as a long-range signal in Arabidopsis. Curr Biol 17: 1050-1054
Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D (1999) Activation tagging of the floral inducer FT. Science 286: 1962-1965
Kim WY, Fujiwara S, Suh SS, Kim J, Kim Y, Han L, David K, Putterill J, Nam HG, Somers DE (2007) ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature 449: 356-360
Lee BD, Kim MR, Kang MY, Cha JY, Han SH, Nawkar GM, Sakuraba Y, Lee SY, Imaizumi T, McClung CR, Kim WY, Paek NC (2017) The F-box protein FKF1 inhibits dimerization of COP1 in the control of photoperiodic flowering. Nat Commun 8: 1-10
Lee H, Suh SS, Park E, Cho E, Ahn JH, Kim SG, Lee JS, Kwon YM, Lee I (2000) The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev 14: 2366-2376
Lee J, Lee I (2010) Regulation and function of SOC1, a flowering pathway integrator. J Exp Bot 61: 2247-2254
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
Li K, Gao Z, He H, Terzaghi W, Fan L, Deng XW, Chen H (2015) Arabidopsis DET1 represses photomorphogenesis in part by negatively regulating DELLA protein abundance in darkness. Mol Plant 8: 622-630
Li K, Yu R, Fan LM, Wei N, Chen H, Deng XW (2016a) DELLA-mediated PIF degradation contributes to coordination of light and gibberellin signalling in Arabidopsis. Nat Commun 7: 11868
Li L, Li X, Liu Y, Liu H (2016b) Flowering responses to light and temperature. Sci China Life Sci 59: 403-408
Li M, An F, Li W, Ma M, Feng Y, Zhang X, Guo H (2016c) DELLA proteins interact with FLC to repress flowering transition. J Integr Plant Biol 58: 642-655
Li Y, Wang H, Li X, Liang G, Yu D (2017) Two DELLA-interacting proteins bHLH48 and bHLH60 regulate flowering under long-day conditions in Arabidopsis thaliana. J Exp Bot 68: 2757-2767
Liu H, Wang Q, Liu Y, Zhao X, Imaizumi T, Somers DE, Tobin EM, Lin C (2013) Arabidopsis CRY2 and ZTL mediate blue-light regulation of the transcription factor CIB1 by distinct mechanisms. Proc Natl Acad Sci USA 110: 17582-17587
Liu L, Zhang Y, Tang S, Zhao Q, Zhang Z, Zhang H, Dong L, Guo H, Xie Q (2010) An efficient system to detect protein ubiquitination by agroinfiltration in Nicotiana benthamiana. Plant J 61: 893-903
Mathieu J, Warthmann N, Kuttner F, Schmid M (2007) Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis. Curr Biol 17: 1055-1060
McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM, Sun TP, Steber CM (2003) The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15: 1120-1130
Meng Y, Li H, Wang Q, Liu B, Lin C (2013) Blue light-dependent interaction between Cryptochrome2 and CIB1 regulates transcription and leaf senescence in soybean. Plant Cell 25: 4405-4420
Moon J, Lee H, Kim M, Lee I (2005) Analysis of flowering pathway integrators in Arabidopsis. Plant Cell Physiol 46: 292-299
Moon J, Suh S, Lee H, Choi K, Hong CB, Paek N, Kim S, Lee I (2003) The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. Plant J 35: 613-623
Murase K, Hirano Y, Sun TP, Hakoshima T (2008) Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456: 459-463
Mutasa-Gottgens E, Hedden P (2009) Gibberellin as a factor in floral regulatory networks. J Exp Bot 60: 1979-1989
Nelson DC, Lasswell J, Rogg LE, Cohen MA, Bartel B (2000) FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis. Cell 101: 331-340
Nohales MA, Kay SA (2019) GIGANTEA gates gibberellin signaling through stabilization of the DELLA proteins in Arabidopsis. Proc Natl Acad Sci USA 116: 21893-21899
Osnato M, Castillejo C, Matias-Hernandez L, Pelaz S (2012) TEMPRANILLO genes link photoperiod and gibberellin pathways to control flowering in Arabidopsis. Nat Commun 3: 808
Peng J, Carol P, Richards DE, King KE, Cowling RJ, Murphy GP, Harberd NP (1997) The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev 11: 3194-3205
Peng J, Yu D, Wang L, Xie M, Yuan C, Wang Y, Tang D, Zhao X, Liu X (2012) Arabidopsis F-box gene FOA1 involved in ABA signaling. Sci China Life Sci 55: 497-506
Porri A, Torti S, Romera-Branchat M, Coupland G (2012) Spatially distinct regulatory roles for gibberellins in the promotion of flowering of Arabidopsis under long photoperiods. Development 139: 2198-2209
Qi T, Huang H, Wu D, Yan J, Qi Y, Song S, Xie D (2014) Arabidopsis DELLA and JAZ proteins bind the WD-repeat/bHLH/MYB complex to modulate gibberellin and jasmonate signaling synergy. Plant Cell 26: 1118-1133
Qin Q, Wang W, Guo X, Yue J, Huang Y, Xu X, Li J, Hou S (2014) Arabidopsis DELLA protein degradation is controlled by a type-one protein phosphatase, TOPP4. PLoS Genet 10: e1004464
Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288: 1613-1616
Sawa M, Nusinow DA, Kay SA, Imaizumi T (2007) FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318: 261-265
Silverstone AL, Jung HS, Dill A, Kawaide H, Kamiya Y, Sun TP (2001) Repressing a repressor: Gibberellin-induced rapid reduction of the RGA protein in Arabidopsis. Plant Cell 13: 1555-1566
Song YH, Estrada DA, Johnson RS, Kim SK, Lee SY, MacCoss MJ, Imaizumi T (2014) Distinct roles of FKF1, GIGANTEA, and ZEITLUPE proteins in the regulation of CONSTANS stability in Arabidopsis photoperiodic flowering. Proc Natl. Acad Sci USA 111: 17672-17677
Song YH, Ito S, Imaizumi T (2013) Flowering time regulation: Photoperiod- and temperature-sensing in leaves. Trends Plant Sci 18: 575-583
Song YH, Smith RW, To BJ, Millar AJ, Imaizumi T (2012) FKF1 conveys timing information for CONSTANS stabilization in photoperiodic flowering. Science 336: 1045-1049
Sparkes IA, Runions J, Kearns A, Hawes C (2006) Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protoc 1: 2019-2025
Srikanth A, Schmid M (2011) Regulation of flowering time: All roads lead to Rome. Cell Mol Life Sci 68: 2013-2037
Sun T, Goodman HM, Ausubel FM (1992) Cloning the Arabidopsis GA1 locus by genomic subtraction. Plant Cell 4: 119-128
Takase T, Nishiyama Y, Tanihigashi H, Ogura Y, Miyazaki Y, Yamada Y, Kiyosue T (2011) LOV KELCH PROTEIN2 and ZEITLUPE repress Arabidopsis photoperiodic flowering under non-inductive conditions, dependent on FLAVIN-BINDING KELCH REPEAT F-BOX1. Plant J 67: 608-621
Teotia S, Tang G (2015) To bloom or not to bloom: Role of microRNAs in plant flowering. Mol Plant 8: 359-377
Tiwari SB, Shen Y, Chang HC, Hou Y, Harris A, Ma SF, McPartland M, Hymus GJ, Adam L, Marion C, Belachew A, Repetti PP, Reuber TL, Ratcliffe OJ (2010) The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element. New Phytol 187: 57-66
Turck F, Fornara F, Coupland G (2008) Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu Rev Plant Biol 59: 573-594
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
Wang F, Zhu D, Huang X, Li S, Gong Y, Yao Q, Fu X, Fan LM, Deng XW (2009) Biochemical insights on degradation of Arabidopsis DELLA proteins gained from a cell-free assay system. Plant Cell 21: 2378-2390
Wang H, Pan J, Li Y, Lou D, Hu Y, Yu D (2016) The DELLA-CONSTANS transcription factor cascade integrates gibberellic acid and photoperiod signaling to regulate flowering. Plant Physiol 172: 479-488
Wellmer F, Riechmann JL (2010) Gene networks controlling the initiation of flower development. Trends Genet 26: 519-527
Wen CK, Chang C (2002) Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. Plant Cell 14: 87-100
Willige BC, Ghosh S, Nill C, Zourelidou M, Dohmann EM, Maier A, Schwechheimer C (2007) The DELLA domain of GA-INSENSITIVE mediates the interaction with the GA-INSENSITIVE DWARF1A gibberellin receptor of Arabidopsis. Plant Cell 19: 1209-1220
Wilson RN, Heckman JW, Somerville CR (1992) Gibberellin is required for flowering in Arabidopsis thaliana under short days. Plant Physiol 100: 403-408
Xu F, Li T, Xu PB, Li L, Du SS, Lian HL, Yang HQ (2016) DELLA proteins physically interact with CONSTANS to regulate flowering under long days in Arabidopsis. FEBS Lett 590: 541-549
Yanagisawa S (2002) The Dof family of plant transcription factors. Trends Plant Sci 7: 555-560
Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: A versatile cell system for transient gene expression analysis. Nat Protoc 2: 1565-1572
Yoo SK, Chung KS, Kim J, Lee JH, Hong SM, Yoo SJ, Yoo SY, Lee JS, Ahn JH (2005) CONSTANS activates SUPPRESSOR OFOVEREXPRESSION OFCONSTANS 1 through FLOWERING LOCUS T to promote flowering in Arabidopsis. Plant Physiol 139: 770-778
Yu S, Galvão VC, Zhang YC, Horrer D, Zhang TQ, Hao YH, Feng YQ, Wang S, Schmid M, Wang JW (2012) Gibberellin regulates the Arabidopsis floral transition through miR156-targeted SQUAMOSA promoter binding-like transcription factors. Plant Cell 24: 3320-3332
Yu X, Klejnot J, Lin C (2006) Florigen: One found, more to follow? J Integr Plant Biol 48: 617-621
Zentella R, Zhang Z, Park M, Thomas SG, Endo A, Murase K, Fleet CM, Jikumaru Y, Nambara E, Kamiya Y, Sun T (2007) Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19: 3037-3057
Zhang L, Chen L, Yu D (2018) Transcription factor WRKY75 interacts with DELLA proteins to affect flowering. Plant Physiol 176: 790-803
Zhang QQ, Wang JG, Wang LY, Wang JF, Wang Q, Yu P, Bai MY, Fan M (2020) Gibberellin repression of axillary bud formation in Arabidopsis by modulation of DELLA-SPL9 complex activity. J Integr Plant Biol 62: 421-432
Zhang ZL, Ogawa M, Fleet CM, Zentella R, Hu J, Heo JO, Lim J, Kamiya Y, Yamaguchi S, Sun TP (2011) SCARECROW-LIKE 3 promotes gibberellin signaling by antagonizing master growth repressor DELLA in Arabidopsis. Proc Natl Acad Sci USA 108: 2160-2165
Zhao X, Yu X, Foo E, Symons GM, Lopez J, Bendehakkalu KT, Xiang J, Weller JL, Liu X, Reid JB, Lin C (2007) A study of gibberellin homeostasis and cryptochrome-mediated blue light inhibition of hypocotyl elongation. Plant Physiol 145: 106-118