Involvement of brassinosteroid signals in the floral-induction network of Arabidopsis

Journal of Experimental Botany, Oct 2010

The transition to flowering is known to be regulated by numerous interacting endogenous and environmental cues, of which brassinosteroids (BRs), a group of polyhydroxylated steroid phytohormones, appear to be linked to the regulation of flowering time. In Arabidopsis, BR biosynthetic det2 mutants exhibited delayed flowering time by at least 10 d compared with the wild type. The levels of endogenous BRs in det2 were below 10% of the wild type. The timing of flowering was also delayed in the BR biosynthetic dwf4 and cpd mutants and in the BR-insensitive bri1 mutants. Because brassinolide (BL) and different BL precursors were over-accumulated in BR biosynthetic mutants and BR-insensitive bri1 mutants, this showed that alterations in the endogenous BL content and the level of different BL precursors affect flowering time in Arabidopsis. The late-flowering phenotypes of bri1 also showed that components of the BR signal transduction pathway affect flowering time. So far, reports on a connection between BRs and flowering time are limited. This review summarizes recent advances regarding the action of BRs in the transition to flowering.

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Involvement of brassinosteroid signals in the floral-induction network of Arabidopsis

Jihong Li 0 Yuhua Li 0 Shuyan Chen 0 Lizhe An 0 0 Key Laboratory of Arid and Pasture Agroecology of Ministry of Education, School of Life Sciences, Lanzhou University , Lanzhou, Gansu, 730000 , PR China The transition to flowering is known to be regulated by numerous interacting endogenous and environmental cues, of which brassinosteroids (BRs), a group of polyhydroxylated steroid phytohormones, appear to be linked to the regulation of flowering time. In Arabidopsis, BR biosynthetic det2 mutants exhibited delayed flowering time by at least 10 d compared with the wild type. The levels of endogenous BRs in det2 were below 10% of the wild type. The timing of flowering was also delayed in the BR biosynthetic dwf4 and cpd mutants and in the BR-insensitive bri1 mutants. Because brassinolide (BL) and different BL precursors were over-accumulated in BR biosynthetic mutants and BR-insensitive bri1 mutants, this showed that alterations in the endogenous BL content and the level of different BL precursors affect flowering time in Arabidopsis. The late-flowering phenotypes of bri1 also showed that components of the BR signal transduction pathway affect flowering time. So far, reports on a connection between BRs and flowering time are limited. This review summarizes recent advances regarding the action of BRs in the transition to flowering. - One of the most important events in the life cycle of flowering plants is the transition from vegetative to reproductive growth. This process is caused by floral induction which is dependent on numerous interacting endogenous and environmental cues (Boss et al., 2004). In Arabidopsis, the results of extensive genetic studies of lateflowering mutants revealed the existence of at least four signalling pathways that co-ordinately promote flowering, including environmental induction through photoperiod, temperature, autonomous floral initiation, and regulation by gibberellins (GAs) (Michaels, 2009). In addition, endogenous ascorbic acid, ethylene, and some environmental factors, such as ambient temperature and light quality, have also been found to be critical in mediating flowering (Achard et al., 2007; Lee et al., 2007; Wollenberg et al., 2008; Kotchoni et al., 2009). Although major components regulating flowering time have been identified in Arabidopsis, other factors still await discovery. Brassinosteroids (BRs) are a class of steroidal hormones essential for plant growth and development, including skotomorphogenesis, photomorphogenesis, xylem formation, cell division, and cell elongation (Clouse, 1997; Clouse and Sasse, 1998; Yang et al., 2005). Brassinolide (BL), the most biologically active BR, was initially isolated from rape pollen of (Brassica napus) and its structure was determined in 1979 (Grove et al., 1979) and a variety of BRs have since been identified from a broad range of plant species. These molecules have been widely recognized as a major group of plant growth regulators (Bajguz and Tretyn, 2003; Zullo and Kohout, 2004). The typical phenotypes of BR-defective or signalling mutants include dwarfism, small dark green leaves, a compact rosette structure, delayed flowering and senescence, and reduced male fertility (Clouse, 1997). In addition, agricultural applications of BRs have been used as BR treatments can increase yield and improve stress resistance in several major crop plants (Symons et al., 2006; The Author [2010]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved. For Permissions, please e-mail: Wu et al., 2008). Although rapid advances in BR biosynthesis and signal transduction, as well as their interaction with other plant hormones have been reported (Arteca and Arteca, 2008; Kim et al., 2008), there is limited information about the functions of BRs in the flowering transition. The involvement of BRs in regulating the floral induction networks of Arabidopsis through the regulation of critical flowering-time genes is described here. Molecular pathways regulating flowering induction in Arabidopsis Photoperiod (day-length) signals were first described in plants in the early 20th century and identified as one of the most important environmental factors that affect the transition to flowering (Hayama and Coupland, 2003) (Fig. 1). Physiological and molecular genetic analyses have shown that day-length signals are perceived by phytochromes, cryptochromes, and ZEITLUPE (ZTL), which mediate the light input to the downstream components including the circadian clock (Somers et al., 1998; Martinez-Garcia et al., 2000; Devlin et al., 2007). The circadian clock generates a series of rhythmic output signals to regulate photoperiodic flowering. This process is mainly mediated by GIGANTEA (GI) (Rubio and Deng, 2007). GI-mediated photoperiodic flowering is governed by the co-ordinated interaction of two distinct genetic pathways. One is mediated via CONSTANS (CO), which encodes a positive regulator for flowering and the other is mediated via miR172 and its targets (Jung et al., 2007). The CO-dependent pathway is mediated by the blue light receptors FLAVIN BINDING, KELCH REPEAT, and F-BOX 1 (FKF1) that interact with GI to cause CYCLING OF DOF FACTOR 1 (CDF1) to release its repression of CO, thus promoting the expression of FLOWERING LOCUS T (FT) (Sawa et al., 2007). The CO-independent miR172 pathway mediates light signals from GI through miR172 to repress the expression of a set of APETALA2 (AP2)-like genes including TARGET OF EAT1 (TOE1), TOE2, and TOE3 and to promote the expression of FT (Aukerman and Sakai, 2003; Jung et al., 2007). FT and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) act as floral integrators that are repressed by FLOWERING LOCUS C (FLC) and SHORT VEGETATIVE PHASE (SVP) (Searle et al., 2006). Finally, FT is transported through the phloem to the shoot apex where it interacts with the FD, a bZIP transcription factor to activate the expression of APETALA1 (AP1), FRUITFULL (FUL), and SEPALLATA3 (SEP3) (TeperBamnolker and Samach, 2005; Wigge et al., 2005). FT and FD also promote SOC1 expression at the shoot apical meristem and then activate the expression of LEAFY (LFY) to initiate flowering (Searle et al., 2006). The vernalization pathway of Arabidopsis promotes flowering in response to extended exposure to low temperature (Fig. 1). Currently, two vernalization-related pathways have been identified. One is FLC-dependent and the other is FLC-independent (Alexandre and Hennig, 2008). Fig. 1. Model of the floral-induction networks in Arabidopsis. Arrows and perpendicular lines represent actions of promotion and inhibition, respectively. Four molecular responses pathway regulating floral induction have been identified in Arabidopsis: photoperiod pathway, vernalization pathway, autonomous pathway, and gibberellins pathway. Details and definitions are provided in the text. The FLC-dependent pathway is thought to be the major determinant of vernalization in Arabidopsis (Scho nrock et al., 2006). FLC is a MADS-box transcription factor that is expressed in both the vasculature of leaves and the shoot apical meristem (SAM). FLC can interact with SVP to inhibit flowering mainly through directly binding to specific regulatory elements in the FT and SOC1 loci in Arabidopsis (Searle et al., 2006; Li et al., 2008). The FLC-dependent pathway promotes flowering in winter-annual accessions of Arabidopsis through epigenetic silencing of FLC that is mediated by histone modifications at the FLC locus (Bastow et al., 2004). De Lucia et al. (2008) reported that vernalization-induced epigenetic silencing of FLC involves changed composition and dynamic redistribution of Polycomb complexes at different stages of the vernalization process. Vernalization-induced FLC repression is triggered by association of the plant homeodomain (PHD) finger protein VERNALIZATION 5 (VRN5) to a specific domain in FLC intron 1, in a process that depends on the coldinduced PHD protein VERNALIZATION INSENSITIVE 3 (VIN3). Subsequently, the VRN5 distribution changes, which is accompanied by increased trimethylation of lysine 27 of histone 3 (H3K27me3) (De Lucia et al., 2008). Maintenance of FLC repression requires H3K27me3; the Polycomb Repressive Complex 2 (PRC2) component VERNALIZATON 2 (VRN2) and the LIKE HETERCHROMATIN PROTEIN 1 (LHP1)/TERMINAL FLOWER 2 (TFL2) are also important candidates (Mylne et al., 2006; Sung et al., 2006; De Lucia et al., 2008). More recently, an FLC-independent vernalization pathway has been proposed. In this pathway, vernalization can directly promote flowering through AGAMOUSLIKE19 (AGL19) and AGAMOUS-LIKE 24 (AGL24) in Arabidopsis (Michaels et al., 2003; Alexandre and Hennig, 2008). AGL24 and AGL19 both act as activators of flowering in Arabidopsis. AGL24 and SOC1 activate each others expression to pomote flowering but AGL19 acts independently of SOC1 (Scho nrock et al., 2006; Liu et al., 2008). In the response to vernalization, AGL24 and AGL19 expression is also accompanied by chromatin modifications such as H3K27me3, and they mostly act in the late stages of vernalization (Alexandre and Hennig, 2008). The autonomous pathway constitutes a heterogeneous group of genes that includes FVE, FLOWERING LOCUS D (FLD), LUMINIDEPENDENS (LD), FLOWERING LOCUS K (FLK), FY, FCA, and FPA (Michaels and Amasino, 2001). These genes regulate flowering independently of environmental cues mainly by stably suppressing FLC expression (Michaels and Amasino, 1999, 2001). Mutations in any one of these genes result in elevated FLC expression which can be epigenetically silenced by vernalization (Michaels and Amasino, 1999; Sheldon et al., 1999, 2000). In addition, Veley and Michaels (2008) found that fpa fve double mutants are late flowering in an flc-null background, which showed that the autonomous pathway also acts through FLC-independent responses (Fig. 1). The acceleration of GAs in Arabidopsis flowering has been confirmed (Blazquez et al., 1998). The GA pathway has less influence on flowering time in long days than in short days in Arabidopsis (Wilson et al., 1992; Chandler et al., 2000). Gibberellins promote flowering in Arabidopsis through the activation of SOC1, LFY, and FT in inflorescence, floral meristems, and leaves, respectively (Lee et al., 2000; Yu et al., 2004; Eriksson et al, 2006; Hisamatsu and King, 2008) (Fig. 1). Brassinosteroid biosynthetic pathway In Arabidopsis, the main BR biosynthetic pathway has been established via extensive stepwise metabolic studies (Divi and Krishna, 2009). These studies showed that BL (C28 brassinosteroid) is synthesized from campesterol (CR), CR is first converted to campestanol (CN), which is then converted to castasterone (CS) through two parallel branched biosynthetic pathways, the early and late C-6 oxidation pathways, and CS is finally converted to BL (Noguchi et al., 2000). In the early stages of BL, the early C-22 oxidation pathway is also the main BR synthesis route. In this process, CR is initially converted to 22-OHCR, then gradually converted to 22-OH-4-en-3-one, 22-OH-3-one, and 6-deoxoCT, which is finally converted to BL through the late C-6 oxidation pathways (Fujioka et al., 2002). In addition, a shortcut in BR biosynthesis has been proposed, which allows direct conversion of early 22-hydroxylated intermediates to 6-deoxo3DT and 6-deoxoTY via C-23 hydroxylation (Ohnishi et al., 2006). These cross-linked pathways together ensure the synthesis of BL (Fig. 2). In Arabidopsis, an analysis of BR-deficient mutants revealed the existence of many enzymes that catalyse BL biosynthesis. DEETIOLATED2 (DET2), a 5a-reductase, catalyses the conversion of 4-en-3-one to 3-one and 22-OH4-en-3-one to 22-OH-3-one (Fujioka et al., 1997, 2002). Some cytochrome P450 mono-oxygenases were found to catalyse multiple oxidative conversions in BL biosynthesis. The C-22 and C-23 hydroxylation reactions are mediated by the P450s DWARF4 (DWF4) and CONSTITUTIVE PHOTOMORPHOGENESIS AND DWARFISM (CPD), respectively (Szekeres et al., 1996; Choe et al., 1998), and the C-6 oxidation is catalysed by BR6ox (Shimada et al., 2001). Two BR-biosynthetic P450s CYP90C1 and CYP90D1 preferentially convert 22-OH-4-en-3-one, 22-OH-3-one, and 3-epi-6-deoxoCT to 23-hydroxylated products (Ohnishi et al., 2006). The typical phenotypes of mutants impaired in BR biosynthesis include dwarfism, small dark green leaves, a compact rosette structure, delayed flowering and senescence, and reduced male fertility which can be rescued in the wild-type when BRs are applied exogenously (Clouse, 1997). Brassinosteroid signalling pathway BRs are perceived by the cell surface receptor kinase complex including BRASSINOSTEROID INSENSITIVE 1 (BRI1), and BRI1 ASSOCIATED PROTEIN KINASE 1 (BAK1) (Li et al., 2002; Nam and Li, 2002; Tang et al., 2010). BRI1 contains an extracellular domain, a single transmembrane domain, and a cytoplasmic kinase domain that initiates intracellular signal transduction. The extracellular domain of BRI1 contains 24 leucine-rich repeats (LRRs) and an island domain (ID) between LRR20 and LRR21, and its cytoplasmic region can be subdivided into a juxtamembrane (JM) domain, a Ser/Thr kinase domain and a C-terminal (CT) domain (Vert et al., 2005). BRs bind directly to the ID LRR21 domain to activate the BRI1 kinase. Activation of BRI1 leads to disassociation with BRI1 KINASE INHIBITOR 1 (BKI1) and its association with BAK1. The activated BAK1 further transphosphorylates JM and CT domains in BRI1, thereby increasing BRI1 kinase activity (Wang et al., 2005, 2008). Activation of BRI1 leads to the phosphorylation of Ser230 of BR-SIGNALLING KINASE 1 (BSKs), which then interacts with and presumably activates BRI1 SUPPRESSOR 1 (BSU1) phosphatase (Tang et al., 2008; Kim et al., 2009). BSU1 inactivates the GSK3-like kinase BRINSENSITIVE 2 (BIN2) by dephosphorylating a conserved phospho-tyrosine residue and inhibits phosphorylation of BRASSINAZOLE RESISTANT 1 (BZR1) and BRI1-EMSSUPRESSOR 1 (BES1)/BRASSINAZOLE RESISTANT 1 (BZR2) (Kim et al., 2009). BIN2 phosphorylates BZR1 and BZR2/BES1 to inhibit their DNA binding activity and to promote their cytoplasmic retention by the 14-3-3 proteins (He et al., 2002; Bai et al., 2007). Inactivation of BIN2 allows the accumulation of unphosphorylated BZR1 and BZR2/ BES1 in the nucleus, which, in turn, will regulate BR target genes (Yin et al., 2002; He et al., 2005). BZR1 and BES1 can bind directly to the promoter regions of the BR biosynthetic genes, CPD and DWF4, and inhibit their expression, forming a negative feedback loop (Tanaka et al., 2005) (Fig. 3) Relationship between brassinosteroids and flowering time Physiological events In Arabidopsis, most BR-biosynthetic mutants and BRinsensitive mutants exhibit a prolonged vegetative phase and delayed flowering time. Under the same growth conditions, det2 mutants produced a rosette of 1963 leaves compared with 962 leaves in the wild type before flowering. det2 mutants did not flower until 33 d post-germination (delayed by at least 10 d compared with the wild type) (Chory et al., 1991). The levels of endogenous BRs in det2 are below 10% of those of the wild type (Fujioka et al., 1997), indicating that endogenous BR levels are closely linked to the flowering time. dwf4, another BR biosynthetic mutant, also possessed a prolonged vegetative phase and produced twice the number of rosette leaves than the wild type. The flowering time was delayed by 4 d in dwf4 mutants (Azpiroz et al., 1998). Shimada et al. (2003) reported that the highest level of endogenous BRs and the highest expression of the DWF4, BR6ox1, and BR6ox2 genes in Arabidopsis were observed in apical shoots. bri1 and cpd mutants exhibited a modest late-flowering phenotype (bolting after ;13 leaves), but when flowering time was measured as days to the start of bolting, cpd flowered later than bri1 (41 d versus 33.8 d) (Li and Chory, 1997; Domagalska et al., 2007). Although there are no precise reports on the BL precursor levels in cpd and dwf4 mutants, the BR-biosynthetic pathway has been shown to be blocked in cpd and dwf4 mutants, which probably results in the over-accumulation of different BL precursors (Szekeres et al., 1996; Azpiroz et al., 1998). By contrast, it is clear that bri1 mutants accumulated very high levels of endogenous BRs, such as typhasterol (TY), CS, and BL (Noguchi et al., 1999). These results indicated that alterations in the endogenous BL content and different BL precursor levels affect flowering time in Arabidopsis. Meanwhile, the lateflowering phenotypes of bri1 also showed that components of the BR signal transduction pathway affect flowering time. Molecular events CPD: CPD encodes a C-23 steroid hydroxylase CYP90A1, which acts at one of the later steps of BR biosynthesis in Arabidopsis (Szekeres et al., 1996). Bancos et al. (2006) reported diurnal changes in CPD expression by analysis of the CPD:LUC transgenic line and these changes were clearly observed when the CPD:LUC seedlings were grown under continuous white light (LL) and continuous dark (DD), following alternation of 12 h of light and 12 h of darkness (LD) for 7 d. Circadian oscillations in CPD expression were observed in LL for at least 96 h. In DD, circadian activity of the CPD promoter was also observed for 3 d. Furthermore, the diurnal rhythmicity of CPD is not determined by feedback regulation because diurnal expression of CPD is maintained in the bri1 mutant. It was also indicated that endogenous BR content exhibits diurnal changes, leading to BL accumulation in the middle of the day. Bancos et al. (2006) speculated that the diurnal control of transcription may involve the AAAATCT motif present in both the CPD and CYP85A2 promoters because this sequence is a potential binding site of CIRCADIAN CLOCK ASSOCIATED 1 (CCA1), a core circadian clock component. Hanano et al. (2006) reported that BR (homobrasinolide) application shortened the period of the circadian rhythms of CHLOROPHYLL A/B BINDING PROTEIN (CAB2), COLD AND CIRCADIAN-REGULATED 2 (CCR2), and CCA1 under both LL and DD. Moreover, cpd mutants displayed a 3 h long-period of the CCR2 phenotype under LL, since cpd mutants have impaired BR biosynthesis, all these results indicated that BR can modulate the circadian rhythms of these genes. They also reported that BRs play an important role in promoting periodicity because periodicity of CAB2 rhythms in DD was significantly lower after BR treatment than without it. The circadian clock is an endogenous mechanism that is able to generate biological rhythms with a 24-h period to regulate metabolism and physiology in plants (Harmer, 2009). CCA1 is a morning-expressed Myb-transcription factors, and LATE ELONGATED HYPOCOTYL (LHY) and the evening-phased pseudoresponse regulator TIMING OF CAB EXPRESSION 1 (TOC1) constitute the core feedback loop of the circadian oscillator (Salome and McClung, 2004; McClung, 2006). In Arabidopsis, the circadian system has dramatic effects on flowering time, which it regulates through the CO and FT genes (SuarezLopez et al., 2001; Yanovsky and Kay, 2002). Niwa et al. (2007) suggested that CCA1/LHY act redundantly as negative regulators of the photoperiodic flowering pathway, but the TOC1 gene serves as an activator. In their model, the core CCA1LHY/TOC1 coordinately modulate the COFT photoperiodic flowerig pathway particularly through the flowering-associated GI, CDF1, and FKF1. Thus, based on the above findings, BR influences the circadian clock, and the circadian clock regulates flowering time, which might imply that BR regulates flowering time through the circadian clock system (Fig. 4). BRI1: In Arabidopsis, Domagalska et al. (2007) found that BRs regulate flowering time by regulating expression of FLC. FLC is a potent floral repressor, at least in part, by binding directly to CArG boxes within the first intron of FT and the promoter regions of SOC1 and FD (Searle et al., 2006). LD and FCA are included in the autonomous pathway. FLC transcript levels are higher and flowering is later in autonomous mutants such as ld mutants than in wild-type Arabidopsis grown under the same conditions (Michaels and Amasino, 1999). Domagalska et al. (2007) reported that bri1 delays flowering of the autonomouspathway mutant ld, fca, and the dominant FRI line through enhancing FLC expression. Moreover, the late-flowering phenotype of bri1 ld, bri1 fca, and bri1 FRI can be suppressed by vernalization or FLC-RNAi constructs. In addition, bri1 the increased levels of histone H3 acetylation at the FLC locus in the ld background. Histone acetylation at the FLC genomic locus was found to be correlated with actively transcribed FLC (He et al., 2003; Ausin et al., 2004). These results showed that BR signalling promotes flowering by enhancing the repression of the autonomous pathway gene LD and FCA on FLC (Fig. 4). Further, they found that the flowering time of double mutants bri1 gi and ga1 bri1 was earlier than that of bri1 ld, bri1 fca, and bri1 FRI mutants. The gi mutant, impaired in the photoperiod pathway, was the very late-flowering single mutant under LL and was slightly later flowering under DD. ga1, a gibberellin-deficient mutant, had a mild late-flowering phenotype. These results showed that the BRI1 pathway might not function via the photoperiod and the gibberellin pathways. Meantime, bri1 mutants responded only partially to vernalization and the expression of autonomous pathway genes were not changed in bri1, which indicated that BR signalling acts to repress the expression of FLC and that it does so independently of vernalization and the autonomous pathway (Domagalska et al., 2007). Thus, BR signalling probably has previously unidentified independent genetic function in the repression of FLC (Domagalska et al., 2007). However, because single bri1 mutants only displayed a weak late-flowering phenotype, BR probably has a role assisting a different floral indution pathway in the repression of FLC. BES1: Evidence for another molecular interaction between components of the BR signalling pathway and the flowering pathway came from the research of Yu et al. (2008). The study demonstrated that BES1 recruits two JmjN/C domain-containing proteins, EARLY FLOWERING 6 (ELF6) and RELATIVE OF EARLY FLOWERING 6 (REF6), to regulate the expression of target gene (Fig. 4). Previous genetic analyses showed that ELF6 and REF6 influenced flowering time (Noh et al., 2004; Clouse, 2008). ELF6 is an upstream repressor in the photoperiodic flowering pathway and elf6 causes early flowering. REF6 acts as a repressor of FLC, leading to the accumulation of FLC transcripts in ref6 mutants, which results in late flowering (Noh et al., 2004). In addition to the flowering phenotype, Yu et al. (2008) revealed that elf6 and ref6 mutants display BR-response phenotypes, such as reduced cell elongation and shorter leaf petioles compared with the wild type. The ref6 mutation can also enhance the bri1-5 phenotype, resulting in even shorter hypocotyls as well as darker green and more curled leaves. Many BR-induced genes are downregulated in ref6 and elf6 knockout mutants, which futher revealed that ELF6 and REF6 can function as activators of BR-regulated genes. In addition, ELF6 and REF6 are recruited by BES1 to modulate gene expression through histone modifications. The repression of FLC by REF6 is associated with histone modifications in FLC chromatin (Noh et al., 2004). Collectively, the interaction between BES1 and ELF6/REF6 established another link between floral induction and the BR pathway. Recent studies demonstrated that all three rice SHORT VEGETATIVE PHASE (SVP)-group genes OsMADS22, OsMADS47, and OsMADS55 act as negative regulators of BR responses (Duan et al., 2006; Lee et al., 2008). However, the rice SVP-group genes seem not to be involved in controlling flowering time. The heading dates were only slightly delayed in the OsMADS22-OsMADS55 double and OsMADS22-OsMADS47-OsMADS55 triple RNAi plants (Lee et al., 2008). The complementation tests also showed that the rice OsMADS22 and OsMADS47 are unable to reverse the flowering-time phenotypes of two Arabidopsis SVP-group gene mutants (Fornara et al., 2008). Phylogenetic analysis showed that OsMADS47 is grouped with Arabidopsis SHORT VEGETATIVE PHASE (SVP), whereas OsMADS22 and OsMADS55 are clustered with Arabidopsis AGAMOUS-LIKE24 (AGL24) (Lee et al., 2003). SVP and AGL24 are two closely related Arabidopsis MADS-box genes that control the floral transition. AGL24 acts as a dosage-dependent promoter of flowering (Michaels et al., 2003). AGL24 and SOC1 regulate each other to provide positive-feedback control of their expression at the shoot apex to promote the flowering transition (Liu et al., 2008). By contrast, SVP functions as a dosage-dependent repressor of flowering (Hartmann et al., 2000). SVP Plant flowering time is controlled by networks of signals. Four major pathways regulating flowering transition have been identified in Arabidopsis: photoperiod, vernalization, autonomous, and gibberellin pathways. In addition, many other factors are critical for flowering transition. BRs are important plant hormones and the BR-deficient det2, cpd, and dwf4 mutants and the BR-insensitive bri1 mutants all showed late-flowering-time phenotypes (Chory et al., 1991; Azpiroz et al., 1998; Domagalska et al., 2007). det2 was particularly late flowering and was classified as a lateflowering mutant (Chory et al., 1991). Because endogenous BR production is blocked in det2, cpd, and dwf4 mutants, alterations in the endogenous BR content affect flowering time in Arabidopsis. The late-flowering phenotypes of bri1 also showed that components of the BR signal transduction pathway affect flowering time. Recently, several lines of molecular evidence showed that BR biosynthesis genes and BR signal transduction genes interact with flowering-time genes directly or indirectly. First, CPD expression exhibited diurnal and circadian rhythmicity and endogenous BR showed diurnal changes leading to BL accumulation in the middle of the light phase (Bancos et al., 2006). BR application shortened the period of the circadian rhythms of CCR2, CAB2, and CCA1 under both LL and DD (Hanano et al., 2006). These results indicated that endogenous BR levels and the circadian clock rhythms influence each other. In Arabidopsis, the circadian system influences flowering time. Thus, endogenous BR levels might affect flowering time indirectly via their influence on the circadian system. Second, BRs regulate the timing of the floral transition by regulating FLC expression. The late-flowering phenotype of ld is enhanced in bri1 and cpd mutants of Arabidopsis through enhancing FLC expression. Moreover, bri1 increased levels of histone H3 acetylation at the FLC locus in the ld background. Interestingly, these experimental results indicate that BR signalling functions independently of the four major flowering pathways in repressing FLC expression (Domagalska et al., 2007). Thus, BR signalling might represent a new avenue in the floral-regulating network. Third, the recruitment of ELF6 and REF6 by BES1 to regulate the target gene expression established another link between floral induction and the BR pathway Acknowledgements We thank Professor Jia Li, Professor Tianshan Zha, and two anonymous reviewers for their valuable comments on the manuscript. 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Jihong Li, Yuhua Li, Shuyan Chen, Lizhe An. Involvement of brassinosteroid signals in the floral-induction network of Arabidopsis, Journal of Experimental Botany, 2010, 4221-4230, DOI: 10.1093/jxb/erq241