Floral Regulation: The Significant Virtue of Horticultural Flowering Plants

Abstract

Flowering is a complex developmental mechanism and is essential for successful reproduction in plants. Complex regulatory networks transform vegetative shoot apical meristems into inflorescence meristems. Further, floral meristems transition to floral bud outgrowth and flowering. Floral regulatory pathways are independently involved in flowering, and most of what we know about genetic regulation comes from model plants. Despite the advancements in plant development biology, the understanding of molecular mechanisms and floral signals in horticultural plants is complex. Studies on gene regulatory mechanisms provide a global view of flowering in horticultural plants. In this paper, we discuss the flowering pathways converging on complex gene regulatory mechanisms and summarize the recent findings in horticultural plants in order to help us understand how they regulate flowering and provide an update for future research.

1. Introduction

Floral induction is a crucial switch in the plant life cycle that results in the production of seeds for successive generations. Floral induction involves the transcriptional regulation of several genes and their regulatory pathways, including numerous environmental cues that transform vegetative meristems into inflorescence meristems, which leads to floral meristem identity, floral bud outgrowth, and flowering [1,2,3]. In model plants such as Arabidopsis thaliana, flowering is triggered by molecular regulatory pathways, including vernalization, age-dependent, autonomous, and photoperiod pathways (Figure 1) [4]. Morphological flowering signs are qualitative and visible only after the complex signals have already induced flowering. This is also because direct measurements of the internal developmental state of plants during floral induction are lacking [5]. Considerable advances have been made in understanding the molecular genetic mechanisms that result in reproductive phase transition [6].

This progress in flowering-related genes has been precisely studied in model plants such as Arabidopsis and rice (Oryza sativa). One of the prime reasons for this is that large amounts of genetic and genomic resources are required to identify the regulatory mechanisms. As the number of identified genes in model plants has increased, molecular biology techniques, including genetic transformation, in vitro regeneration, and gene expression patterns, have enabled the knowledge of these genes to be applied to other plants, especially perennial plants growing in the natural environment; these genes are linked to flowering regulatory pathways [7,8]. These regulatory pathways consist of FLOWERING LOCUS T (FT), FLOWERING LOCUS C (FLC), SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1), CONSTANS (CO), LEAFY (LFY), AGAMOUS-LIKE20 (AGL20), APETALA1 (AP1), and WUSCHEL-related homeobox (WUS) genes [7,9,10,11,12]. Other floral regulators, such as SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1-like, FLOWERING LOCUS T (FT)-like, and FRIGIDA (FD)-like genes, as well as upregulation, also trigger flowering [13,14,15]. The orthologs of Arabidopsis, such as FT, SOCI, LFY, TERMINAL FLOWER1 (TFL1), and MADS-box, have been identified in Citrus (Citrus sinensis, Poncirus trifoliata, and Fortunella hindsii) [16,17,18], apple (Malus domestica Borkh.) [19], longan (Dimocarpus longan Lour.) [20], avocado (Persea americana Mill.) [21], kiwifruit vine (Actinidia deliciosa) [22], pomegranate (Punica granatum L.) [23], loquat (Eriobotrya japonica) [24], and tomato (Solanum lycopersicum L.) [25].

The FT protein is the most famous florigen (a systemic signal that promotes flowering); it is synthesized in the leaf vasculature and moves through the phloem to the shoot apical meristem [26,27]. In Citrus species, FT (CiFT, CsFT, PtFT, ToFT, CiFT, CiFT2, and CiFT3) has been found to functionally characterize and promote early flowering [28,29,30,31,32,33]. Carrizo citrange (Citrus triptera x Citrus sinensis) CcFT1, CcFT2, and CcFT3 genes overexpression induced non-inductive flowering in transgenic Carrizo rootstocks and grafted juvenile scions [32]. Grapevine (Vitis vinifera L.) VvFT overexpression in Arabidopsis promotes early flowering [34]. Apple MdFT1 overexpression induced early flowering in annual and perennial plants [19]. The transcript abundance of FT is increased by the transcriptional activator, the CO protein, which strongly influences floral regulation [35]. In tomatoes, six FT-like genes, namely, SlSP3D, SlSP6A, SlSP5G, SlSP5G1, SlSP5G2, and SlSP5G3, have been identified [25]. Mango (Mangifera indica) MiTFL1-1, MiTFL1-2, MiTFL1-3, and MiTFL1-4 overexpression in Arabidopsis repressed flowering [36]. MdTFL1-1 gene virus-induced gene silencing promotes early flowering in apple [37]. Overexpression and CRISPR/Cas9 base editing of CiMADS43 induce leaf curling and early flowering in lemon (Citrus limon) [38]. In sweet cherry (Prunus avium), PavMADS1, and PavMADS2, RNAi-based silencing enhances FT expression during dormancy [39]. Overexpression of the silver birch (Betula pendula) BpMADS4 gene in apple induced early flowering [40]. SOCI-like genes, AcSOC1e, AcSOC1f, and AcSOC1i overexpression promote flowering in kiwifruit vines [41]. Arabidopsis LFY (AtLFY), a floral meristem identity gene, has been reported to be the first transgene to accelerate flowering in perennial plants [42]. The AtLFY ortholog has also been reported in grapevine VFL [43]. VFL is highly expressed in the floral meristem that develops the following spring. This expression pattern indicates the significance of VFL in floral meristem initiation and organization, similar to other LFY-like genes in different species [44]. MdLFY overexpression in apple increases shoot diameter [45].

Other floral meristem identity genes, such as API and FRUITFUL [23], have also been characterized and named in grapevine VAP1 and VFUL-L. VFUL-L and VAPI are expressed in the very early stages of uncommitted lateral meristems, and their expression is sustained in other initiative organs, such as inflorescences or tendrils [46,47]. In tomatoes, FALSIFLORA (FA) encodes a similar protein to AtLFY. A mutation in FA causes a delay in flowering. Further, fa mutants replace flowering with leaves and inflorescence with a similar phenotype to lfy Arabidopsis [48]. FUL-like genes regulate inflorescence development and flowering in tomatoes [49]. Figure 1

Schematic representation of Arabidopsis flowering regulatory pathways [26,50,51,52,53,54,55,56,57], including floral regulators and suppressors. The black solid arrows indicate gene regulation, and the black straight lines indicate gene suppression.

[Figure omitted. See PDF]

The mechanism by which the meristem terminates involves the interaction between the meristem identity gene and the machinery that maintains the undifferentiation of the meristem, represented by the CLAVATA (CLV) and WUS pathway [58]. C. sinensis CsWUS overexpression in tobacco plays a role in floral organ development [12]. In contrast, virus-induced gene silencing causes thorn development in lemon [12]. A mutation in COMPOUND INFLORESCENCE, a homolog of WOX9 (S); the F-box gene, a homolog of UNUSUAL FLORAL ORGAN, UFO (AN); and its partner FALSIFLORA, a homolog of LFY (FA), play an essential role in inflorescence determination in tomato [59]. The tomato MADS-box gene JOINTLESS (J) is involved in flower development and pedicel differentiation, whereas jointless mutants affect the inflorescence meristem [60]. Additionally, the TOMATO MADS-box 8 gene (TM8) is highly expressed in tomato reproductive organs and plays an essential role in flower development [61]. The TOMATO MADS-Box 6 (TM6) gene acts as a transcriptional regulator during floral development [62]. A loss of function of the TOMATO AP3 (TAP3) gene results in the homeotic development of stamens and petals. TM6 and AP3 play significant roles in flower development in tomato (Figure 2) [63]. Grapevine VvMADS9 (VvPI), VvAP3, and VvTM6 have been identified. VvMADS9 shows a low-expression pattern in the latent bud, and VvTM6 is vastly expressed in reproductive organs [34].

Over the past three decades, molecular and genetic analyses have led to the identification of various genes and transcription factors (TFs) and provided insights into how they control floral development and floral meristem identity in plants. In this review, we highlight the current knowledge of floral regulation and the mechanisms of floral regulatory pathways. Figure 2

Overview of floral regulation and development in tomato plant (Solanum lycopersicum) [25,48,59,60,61,62,63,64,65,66] and chili plant (Capsicum annuum) [67,68,69]. The black solid arrows indicate gene regulation, and the black straight lines indicate gene suppression.

[Figure omitted. See PDF]

2. The Vernalization Pathway: Low-Temperature-Induced Flowering

Plants tend to flower when exposed to changing climatic conditions [70]. A period of chilling or cold exposure from −1 °C to 10 °C activates the vernalization pathway. Chilling acts as an external factor for shoot apical meristem dormancy release and promotes floral transition in plants [71,72]. FT movement via the phloem to the shoot apex is affected at low temperatures, and plants exhibit late flowering [73]. However, in many horticultural plants, such as orange (C. sinensis), olive (Olea europaea L.), litchi (Litchi chinensis Sonn.), mango, and apple, flowering can be induced by exposure to cold or chilling [74,75,76]. Low temperatures also influence the timing of bud bursts and flowering in grapevines [77].

The flowering response to low temperatures has also been reported in Satsuma mandarin (Citrus unshiu Mar.) [78]. The overexpression of Citrus CiFT induces early flowering in pear (Pyrus communis) [79]. Vernalization works by inhibiting the expression of FLC, a robust floral repressor of flowering encoded by the MADS-box protein in the shoot apical meristem [80]. The SEPALLATA-like MADS-Box gene (CaSEP5) is highly expressed in flower organs in peppers (C. annuum). CaSEP5 silencing results in leaf-like sepals and rigid, straight pedicels (Figure 2) [67]. FD acts as a floral repressor by stimulating the expression of FLC. However, it acts as an inhibitor in the independent pathway [80]. Cold exposure degrades the FRI protein and downregulates FLC [81]. Furthermore, FLC suppresses the expression of SOC1 and inhibits the upregulation of FD in the shoot apical meristem [57]. FLC binds to the promoter of SOC1 and SQUAMOSA PROMOTER BINDING-LIKE 15 (SPL15) and suppresses their expression. Floral transition in mango occurs during late autumn and early winter. Mango floral induction requires a higher temperature (10 °C to 15 °C) than vernalization [82,83]. However, M. indica cv. Dashehari promotes flowering under leaf-bearing conditions during vernalization. The expression patterns of the FRI, SUPPRESSOR OF FRIGIDA 4 (SUF4), and FLC EXPRESSOR (FLX) genes are upregulated in bearing mango leaves.

Other floral regulators such as AG, FUL, FPA, FCA, and FLD are also upregulated in bearing mango leaves [84]. The MdFLC3-like gene was functionally characterized to understand how chilling mediates flowering in apples. MdTFL1 overexpression delays flowering in Arabidopsis and maintains the juvenile phase in apple [85]. PcTFL1 RNAi-based silencing induces early flowering in transgenic pears [86]. In Citrus, FLC homolog (PtFLC) overexpression delays flowering in Arabidopsis [87]. Cold treatment upregulates CiFT and CiLFY expression before flower development in Satsuma mandarin buds and leaves [16,88]. Similarly, CsFT, CsLFY, and CsAP1 are upregulated in the leaves, floral meristem, and buds of sweet orange under cold treatment (Figure 3) [88,89]. In Citrus, Nuclear Factor YA (CiNF-YA) activates CiFT expression under low temperatures and drought conditions by binding to the CiFT promoter. Further, CiFT forms a complex with GOLDEN2−LIKE protein (CiFE) and stimulates CiLFY to promote flowering [90]. The Arabidopsis HD-ZIP (AtHB13) homolog PtHB13 binds to the PtFLC promoter and regulates its expression during citrus floral induction. Low temperatures affect the ectopic expression patterns of PtFLC and PtHB13 and regulate floral induction (Figure 3). In contrast, the overexpression of PtFLC and PtHB13 inhibits flowering in Arabidopsis [87]. VIN3 expression positively increases in bearing mango leaves and flowers [82].

The FT ortholog in tomato SFT plays a vital role in the primary shoot flowering time and flower morphology [65]. In tomatoes, Nuclear Factor YA3b (SlNF-YA3b) plays an essential role in floral regulation. The knockout of SlNF-YA3b results in an early flowering phenotype, whereas the overexpression of SlNF-YA3b delays flowering in tomato plants. Further study indicates that NF-YA3b binds to the CCAAT motif of the SFT promoter and represses its expression [91]. In tomatoes, the SlVIN3 gene protein is closely related to the VvVIN3 gene. The SlVIN3 gene shows high expression during floral organ differentiation and low expression during fruit development [66]. The Capsicum annuum FT/TFL orthologs CaFT and CaTFL1 show conserved functioning in floral regulation and plant development (Figure 2) [68].

The genes involved in the vernalization pathway also act on the florigen marker FT, inducing downregulation via FLC but upregulation via VRN1. TFL1 represses FT activity, which maintains an indeterminate meristem [92]. TFL1 represses the floral meristem identity genes (LFY and AP1) and is expressed only on the edges of meristem-developing primordia [93]. During the early stages of inflorescence development, latent buds exhibit a high expression of VvFT/TFL1. Still, this expression pattern is not displayed during flower development in the following season in grapevines [94]. The overexpression of VvTFL1, named VvTFL1A in Arabidopsis, causes delays in flowering time and the initiation of the floral meristem, and it yields a phenotype of complex inflorescence with multiple co-inflorescences [55,94]. In tomatoes, TERMINATING FLOWER (TMF) mutants cause early flowering and replace multi-flower inflorescence with a single flower. ANANTHA (AN) and FALSIFLORA (FA) encode the flowering specification complex and promote early flowering [64]. Tomato TMF synchronizes flower development with a slow reproductive phase transition [64]. However, SINGLE FLOWER TRUSS (SFT) regulates floral meristem identity during floral development [95]. In peppers, the fa mutant causes a reduction in flowering time, whereas CaAN is essential for floral meristem differentiation, and CaS is involved in an earlier stage of the transition to floral meristem differentiation [69]. Figure 3

The flowering regulatory pathways in horticultural perennials (Citrus, grapevine). In Citrus, PtHB13 binds to the PtFLC promoter and induces early flowering [87]. A low temperature or cold enhances the expression of CiLFY and CiFT in leaves/buds and promotes early flowering [16,88]. In contrast, PtFLC represses the expression of CsLFY, CsFT, and CsAP1 [88,89]. The citrus CsWUS gene is involved in meristem maintenance [11]. TFL1 represses FT activity, which maintains an indeterminate meristem [92]. TFL1 represses the floral meristem identity (LFY and AP1) genes [93]. The black solid arrows indicate gene regulation, and the black straight lines indicate gene suppression. The induction of CcMADS19 (FLC ortholog) represses the Citrus FT ortholog [96]. In grapevine, VFL is highly expressed in the floral meristem and involved in floral meristem initiation [44]. VAP1 and VFUL-L are expressed in the uncommitted lateral meristem [46,47]. Short-day (SD) conditions negatively regulate VvFT and PHYTOCHROME A (VvPHY A) and positively control VvPHY B in buds [97]. VvFT regulates floral induction in latent buds with the development of inflorescence, flowers, and fruits [94]. SD conditions negatively control VvFT and VvPHY A and positively control VvPHY B in grapevine buds [98]. PIF4, PIF5, and PIF7 stimulate shade (low R–FR ratio)-induced flowering through FT [99,100]. The PHY B gene negatively regulates the SAS through PIF genes; PIF4 and PIF8 act downstream of PHY B. Under SD conditions, the PHY B-PIF8 module inhibits growth by repressing the expression of the FT2 gene [97]. The PHY B/PIF8 module mediates SD-induced growth cessation [97]. VvMADS8 shows a high-expression pattern during the early stage of inflorescence development [101]. VvMADS3 is involved in vegetative organs and flower development [102,103]. The black solid arrows indicate gene regulation, and the black straight lines indicate gene suppression.

[Figure omitted. See PDF]

3. Autonomous Pathway of Flower Induction

Vernalization and autonomous pathways act opposite to each other (Figure 3). The autonomous pathway induces flowering independently under day-length conditions by repressing the central floral repressor and vernalization regulatory gene FLC [104,105,106]. FLC inhibits the expression of flowering-related genes, such as FT, SOC1, AGL20, LFY, AG, and APL3, and it delays floral transition [9,107,108]. FLOWERING LOCUS K (FLK), FY, FLOWERING LOCUS VE (FVE), LUMINIDEPENDENS (LD), FCA, and FLOWERING LOCUS D (FLD) are redundant genes that ensure the developmental turning of flowering by inhibiting FLC [55,109]. Mutations inserted in FLC did not promote plant flowering [110]. Meanwhile, mutations in autonomous pathways related to FCA, LD, FVE, FLD, FLK, and FY prolonged floral induction under LD and SD conditions. In contrast, vernalization treatment recovered the phenotype [105].

In star fruit (Averrhoa carambola L.), FCA and FVE suppress SVP. However, they promote FT and FD expression under low temperatures and regulate flowering [111]. Several previous studies have demonstrated that the EARLY IN SHORT DAYS 4 (ESD4), Developmentally Retarded Mutant1 (DRM1), Casein kinase II (CK2), RELATIVE OF EARLY FLOWERING 6 (REF6), ARABIDOPSIS THALIANA SYNTAXIN OF PLANTS 22 (SYP22), PCF11P-SIMILAR PROTEIN 4 (PCFS4), AGL28, DNA-binding protein phosphatase gene 1 (DBP1), HISTONE DEACETYLASE 5 (HDA5), and HISTONE DEACETYLASE 6 (HDA6) genes are also involved in autonomous flowering regulatory pathways [50]. In tomatoes, autonomous pathway-related genes, such as FRI-like protein 3, show a high-expression pattern at the initial stage of flower bud differentiation and then during flower development. Thus, FRI may be involved in meristem development at the initial stage of flowering and may act downstream of the gene to inhibit early flowering [112].

4. Light-Dependent Pathway/Photoperiod Pathway of Flower Induction

Photoperiod is a crucial external factor in the vegetative-to-reproductive phase transition. Photoperiod is sensed through the leaves in long-day (LD) and short-day (SD) plants. The role of light intensity in inflorescence formation has been studied in vineyards regarding the hours of sunshine [113] or shading treatment [114]. Applying high light intensities under controlled environmental conditions affects the development of inflorescence primordia depending on the conditions that depend on the photoperiod [115]. In grapevines, floral initiation and floral development are delayed by SD conditions. Previous studies have reported that growth cessation may be SD obligate and SD facultative depending on the genotype in the grapevine [116]. Flowering-related genes such as FT, G1, FD, AP1, CRY2 (CRYPTOCHROME2/FHA), ELF3 (EARLYFLOWERING3), and CO play a central role in the photoperiod pathway [117,118,119]. The flowering time regulators FD and FT control photoperiodic seasonal growth. For example, the FD-like 1 (FDL1)/FT2 complex controls the downstream target LAP1 and regulates photoperiodic growth. FLD1 triggers SD-induced transcriptional regulations in these two pathways’ adaptive responses and bud maturation [120]. ELONGATED HYPOCOTYL 5 (HY5), ATHB7, and PRR7 are expressed in grapevine buds under different photoperiod treatments and in floral meristem development, suggesting a vital role in floral and dormancy induction [121]. Grapevine VvFT is involved in floral induction in latent buds with the development of inflorescence, flowers, and fruits [34,94]. SD conditions negatively control VvFT and PHYTOCHROME A (VvPHY A) and positively control VvPHY B in grapevine buds [98]. PHYTOCHROME B (PHY B) acts as a thermal and light sensor. PHY B (PHY B1, PHY B2, and PHY B3) genes act as suppressors of shoot elongation, and their downstream targets, PHYTOCHROME INTERACTING FACTOR (PIF) genes (PIF4 and PIF8), are involved in shade avoidance syndrome, and PIF8 plays a central role in the inhibition of seasonal growth in plants [97]. In V. vinifera. cv. Thompson seedless, photoperiod drives the transition of buds into endodormancy. It modifies the expression of the VvPHY A and VvPHY B transcripts in grapevine leaves [122]. PIF4, PIF5, and PIF7 stimulate shade (low R–FR ratio)-induced flowering through a positive expression of FT and TWIN SISTER OF FT (TSF) [99,100]. The PHY B gene negatively regulates the SAS through PIF genes; PIF4 and PIF8 act downstream of PHY B. Under SD conditions, PHY B acts as a negative regulator of growth cessation, and the PHY B-PIF8 module inhibits growth by repressing the expression of the FT2 gene [97]. The PHY B/PIF8 module mediates SD-induced growth cessation in autumn and temperature-regulated bud break in spring [97].

Photoreceptors (CRY1 and CRY2) and PHY A act antagonistically to PHY B in order to stabilize the CO protein and trigger it to upregulate FT [123]. FT and FWA act downstream of CO and other pathways, whereas GI and CRY2 act upstream [124]. CRY2 interacts with the CIB1 TF in response to blue light in order to stimulate the transcription of FT, whereas CIB3 interacts with CIB1, acts synergistically with CIB1, and promotes GI transcription [125]. In tomatoes, CRY2 is significantly involved in flowering time. The PHYB gene regulates the expression patterns of the FT-like genes SlSP5G2, SlSP5G3, and SlSP5G5 and regulates flowering [126]. Further, the FT-like gene SlSPD3 encodes mobile florigen signals and promotes flowering [95].

Clock resetting genes such as FLAVIN-BINDING, KELCH REPEAT, F-BOX1 (FKF1), CONSTITUTIVEPHOTOMORPHOGENIC1 (COP1), KELCHPROTEIN2 (LKP2), and ZEITLUPE (ZTL) play essential roles in the photoperiod pathway. FKF1 is involved in CO protein stabilization and directly binds to CO via the LOV domain, which triggers CO accumulation [127]. Recent studies have revealed that CRY1 stabilizes the DELLA protein through direct interactions, whereas FKF1 degrades the DELLA protein to control diurnal changes in DELLA protein stability through ubiquitination [128]. DELLA also participates in several repressor actions. For example, MYC3 not only binds to the FT promoter but also inhibits the DNA-binding activity of CO through interactions with DELLA proteins [129]. Moreover, DELLA protein expression levels become low during the night because of GA-dependent degradation [130]. ZTL and genes also act as blue light receptors that interact with G1 and regulate flowering [56,131,132]. These results indicate the crucial role of photoperiod and light in floral regulation. In tomatoes, EF (EARLY FLOWERING) is involved in early floral induction, and ef mutants cause early flowering. The EF-dominant gain-of-function allele elevates the SlFAF1/2c transcript. The overexpression of SlFAF1/2c also shows a similar phenotype of early flowering to ef mutants. Moreover, FAF1/2c interacts with CONSTITUTIVEPHOTOMORPHOGENIC9 (COP9) and reduces its protein stability and accumulation [133].

5. Gibberellic Acid Pathway: Hormonal Control of Flowering

The gibberellin (GA) pathway is actively involved in floral transition in plants because the endogenous GA level acts as an inhibitor in floral meristem development under SD conditions [134]. The GA pathway also participates in floral transition under LD conditions [135]. However, GA-deficient ga1-3 mutants promote timely flowering under LD and cause delayed flowering in SD [136]. FT and GA express seasonal cues to the shoot apical meristem. GA acts downstream of FT in seasonal growth regulation and control [137]. The antagonistic factors TFL1 and LAP1 of FT act as promoters or repressors of seasonal growth [137]. GA₃ and 1-amino cyclopropane carboxylic acid [138] treatment delays flowering in Citrus [139]. Before floral induction, the level of bioactive GAs increases in the shoot apex via the activation of GA2oox1, encoding the GA biosynthetic enzyme GA20 oxidase, which promotes the expression of the floral integrators LFY and SOC1. Under SD conditions, GA₄ is produced in leaves, transported to the meristem, upregulates LFY and SOC1, and induces flowering [140]. GA acts as a floral repressor in apples without disturbing shoot elongation—the exogenous treatment of GA results in the downregulation of GA biosynthesis. The GA transporter, GA receptor, and GA catabolic GA oxidase-related genes depend on GA feedback and feedforward regulation. Moreover, TFL1-like genes induce a swift response to GA, while the upregulation of MdTFL1 inhibits flowering in apples [141]. GA 20 oxidase genes also play a significant role in flower development in tomatoes [142].

In Arabidopsis GA receptors, GIBBERELLIN INSENSITIVE DWARF1 (GID1) plays a positive role in GA signaling [143]. GID (Cs3g13110, Cs8g05670, and Cs5g32180) and DELLA proteins (Cs6g09040 and Cs6g17530) show differential expression patterns during citrus-induced floral induction in sweet orange [1]. GA binds to GID1, which then binds to DELLA in order to form a unique GA-GID1-DELLA complex. DELLA is then recruited to the SCF^SLY1/GID2 E3 ubiquitin ligase for polyubiquitination and subsequent degradation by 26 proteosomes. This results in the plant exhibiting a GA response [144]. DELLA proteins are negative regulators in the GA signaling pathway [145,146]. DELLAs are abruptly degraded in the presence of GA [147]. DELLA mutants in Arabidopsis flower early under SD conditions. To date, five DELLA proteins have been identified in Arabidopsis, including GIBBERELLIN INSENSITIVE (GAI), REPRESSOR OF GA1-3, and RGA-LIKE 1 (RGL1) [148,149].

A previous study demonstrated that the DELLA-interacting factor GAI-ASSOCIATED FACTOR1 (GAF1) explained the role of DELLA as a transcriptional co-activator [150]. GAF1 also interacts with the co-repressor TOPLESS-RELATED (TPR), whereas DELLA and TPR are co-repressors and co-activators of GAF1. GAs alter the GAF1 complex from a transcriptional activator to a repressor and promote the expression of FT and SOC1 [145]. The GAFI TF contains a zinc finger motif and belongs to INDETERMINATE1 (ID1). In Arabidopsis, IDD members are closely related to DELLA. Arabidopsis gaf1 and idd1 mutants show a late-flowering phenotype compared to the wild type under SD conditions [150]. The PpIDD family has been identified in peach. The PpIDD family members PpIDD4, PpIDD12, and PpDD13 interact with PpDELLA1 proteins. This interaction activates PpGA20ox1 promoter transcription. This transcriptional regulation indicates that PpIDD-PpDELLA1 is involved in GA-mediated feedback regulation in peaches [151].

6. Conclusions and Perspectives

Reproductive phase transition is a critical adaptive developmental switch in plants. In-depth studies of the floral regulators or repressors will help to understand the conditions of horticultural plants’ adaptability in the near future. Various studies suggest that a plant’s genetic mechanism for flowering is highly conserved. Floral promoters or repressors, for example, the FT/TFL family and encoding proteins such as the phosphatidyl ethanolamine binding protein (PEBP), are the most promising factors for providing deep insights into floral regulation. Floral regulators and repressors are intensely studied in many horticultural plants. Biotechnology provides a significant approach to genetic improvement and speeds up efficient breeding in plants. The advancement in genetic transformation and gene editing in kumquat (Fortunella hindsii) resulted in short juvenility, with the process from explant to T₁ mutant taking 15 months [18]. The PDS gene was recently successfully edited in F. hindsii, with five months needed for regeneration from seed to T₀ plantlets and then ten months needed to obtain the T1 generation [18]. F. hindsii could be used as a model plant to understand the vegetative-to-reproductive phase transition in other citrus species.

In plants, virus-induced gene silencing is widely used to suppress the expression of endogenous genes [152]. For example, a virus-induced gene silencing vector based on TRV (tobacco rattle virus) was successfully used to silence the CsWUS gene in lemon [12]. This vector carries the CsWUS gene from C. sinensis, and it causes thorn development in gene-silenced plants [12]. A viral vector based on citrus leaf blotch virus (CLBV) carrying the FT gene predicted flowering in young citrus plants at four months post-infection, depending on the season and genotype [153,154]. Many researchers have also used the apple latent spherical virus vector ALSV for gene silencing. The inoculation of ALSV shortened the juvenile phase and induced early flowering in pears, apples, and grapevines [155,156]. RNA inference (RNAi) technology is extensively used to knock out gene function in order to promote early flowering in horticultural plants.

The RNAi-based knockdown of TFL1 reduced the juvenile phase and induced early flowering in apple and pear trees [86,157]. However, expansion in floral development in transgenic perennial plants led to reduced vegetative growth, which reduced fruit and seed production in plants. Early-induced flowers require pollination via native pollinators (honey bees). In Longan, the early induction of flowering decreased fruit yield due to the absence of native pollinators [158]. Transgenic plants are often malformed, and fruit settings are shallow [40]. However, CRISPR/Cas9 has become a prominent and efficient biotechnology for genome editing in many plant species, and it has had various success stories in the past few years [159]. CRISPR/Cas system-based genome editing can also address the early floral induction of male sterility in vines such as the kiwi vine [160]. A CRISPR/Cas9-based mutant construction of faf1/2b, faf3/4a, and trfaf3/4b induced early flowering in tomato [161]. To sum up, determining the network regulation of flowering will help us understand how horticultural plants perceive developmental signals, regulate molecular mechanisms, and then accelerate flowering, ultimately boosting commercial production.

Author Contributions

Writing—original draft preparation: F.S.K.; writing—review and editing: F.S.K. and J.-Z.Z.; Data curation: C.-Y.N. and Z.-Z.L.; supervision and conceptualization: J.-Z.Z.; resources and investigation: J.-Z.Z. and C.-G.H.; funding acquisition: J.-Z.Z. All authors have read and agreed to the published version of the manuscript.

Data Availability Statement

No new data were created or analyzed in this study.

Conflicts of Interest

The authors declare no conflicts of interest.

Footnotes

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References

1. Khan, F.S.; Gan, Z.-M.; Li, E.-Q.; Ren, M.-K.; Hu, C.-G.; Zhang, J.-Z. Transcriptomic and physiological analysis reveals interplay between salicylic acid and drought stress in citrus tree floral initiation. Planta; 2022; 255, pp. 1-22. [DOI: https://dx.doi.org/10.1007/s00425-021-03801-2] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/34928452]

2. Khan, M.R.G.; Ai, X.Y.; Zhang, J.Z. Genetic regulation of flowering time in annual and perennial plants. Wiley Interdiscip. Rev. RNA; 2014; 5, pp. 347-359. [DOI: https://dx.doi.org/10.1002/wrna.1215] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/24357620]

3. Wang, J.; Ding, J. Molecular mechanisms of flowering phenology in trees. For. Res.; 2023; 3, 2. [DOI: https://dx.doi.org/10.48130/FR-2023-0002] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/39526261]

4. Turnbull, C. Long-distance regulation of flowering time. J. Exp. Bot.; 2011; 62, pp. 4399-4413. [DOI: https://dx.doi.org/10.1093/jxb/err191] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/21778182]

5. Aikawa, S.; Kobayashi, M.J.; Satake, A.; Shimizu, K.K.; Kudoh, H. Robust control of the seasonal expression of the Arabidopsis FLC gene in a fluctuating environment. Proc. Natl. Acad. Sci. USA; 2010; 107, pp. 11632-11637. [DOI: https://dx.doi.org/10.1073/pnas.0914293107] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/20534541]

6. Auge, G.A.; Penfield, S.; Donohue, K. Pleiotropy in developmental regulation by flowering-pathway genes: Is it an evolutionary constraint?. New Phytol.; 2019; 224, pp. 55-70. [DOI: https://dx.doi.org/10.1111/nph.15901]

7. Wilkie, J.D.; Sedgley, M.; Olesen, T. Regulation of floral initiation in horticultural trees. J. Exp. Bot.; 2008; 59, pp. 3215-3228. [DOI: https://dx.doi.org/10.1093/jxb/ern188]

8. Wils, C.R.; Kaufmann, K. Gene-regulatory networks controlling inflorescence and flower development in Arabidopsis thaliana. Biochim. Biophys. Acta -Gene Regul. Mech.; 2017; 1860, pp. 95-105. [DOI: https://dx.doi.org/10.1016/j.bbagrm.2016.07.014] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/27487457]

9. Michaels, S.D. Flowering time regulation produces much fruit. Curr. Opin. Plant Biol.; 2009; 12, pp. 75-80. [DOI: https://dx.doi.org/10.1016/j.pbi.2008.09.005]

10. Lee, J.; Lee, I. Regulation and function of SOC1, a flowering pathway integrator. J. Exp. Bot.; 2010; 61, pp. 2247-2254. [DOI: https://dx.doi.org/10.1093/jxb/erq098] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/20413527]

11. Tan, F.C.; Swain, S.M. Functional characterization of AP3, SOC1 and WUS homologues from citrus (Citrus sinensis). Physiol. Plant.; 2007; 131, pp. 481-495. [DOI: https://dx.doi.org/10.1111/j.1399-3054.2007.00971.x]

12. Shafique Khan, F.; Zeng, R.-F.; Gan, Z.-M.; Zhang, J.-Z.; Hu, C.-G. Genome-wide identification and expression profiling of the WOX gene family in Citrus sinensis and functional analysis of a CsWUS member. Int. J. Mol. Sci.; 2021; 22, 4919. [DOI: https://dx.doi.org/10.3390/ijms22094919]

13. Samach, A.; Onouchi, H.; Gold, S.E.; Ditta, G.S.; Schwarz-Sommer, Z.; Yanofsky, M.F.; Coupland, G. Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science; 2000; 288, pp. 1613-1616. [DOI: https://dx.doi.org/10.1126/science.288.5471.1613]

14. Abe, M.; Kobayashi, Y.; Yamamoto, S.; Daimon, Y.; Yamaguchi, A.; Ikeda, Y.; Ichinoki, H.; Notaguchi, M.; Goto, K.; Araki, T. FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science; 2005; 309, pp. 1052-1056. [DOI: https://dx.doi.org/10.1126/science.1115983] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/16099979]

15. Wigge, P.A.; Kim, M.C.; Jaeger, K.E.; Busch, W.; Schmid, M.; Lohmann, J.U.; Weigel, D. Integration of spatial and temporal information during floral induction in Arabidopsis. Science; 2005; 309, pp. 1056-1059. [DOI: https://dx.doi.org/10.1126/science.1114358]

16. Endo, T.; Shimada, T.; Fujii, H.; Nishikawa, F.; Sugiyama, A.; Nakano, M.; Shimizu, T.; Kobayashi, Y.; Araki, T.; Peña, L. Development of a CiFT co-expression system for functional analysis of genes in citrus flowers and fruit. J. Jpn. Soc. Hortic. Sci.; 2009; 78, pp. 74-83. [DOI: https://dx.doi.org/10.2503/jjshs1.78.74]

17. Zhang, J.-Z.; Ai, X.-Y.; Sun, L.-M.; Zhang, D.-L.; Guo, W.-W.; Deng, X.-X.; Hu, C.-G. Molecular cloning and functional characterization of genes associated with flowering in citrus using an early-flowering trifoliate orange (Poncirus trifoliata L. Raf.) mutant. Plant Mol. Biol.; 2011; 76, pp. 187-204. [DOI: https://dx.doi.org/10.1007/s11103-011-9780-2]

18. Zhu, C.; Zheng, X.; Huang, Y.; Ye, J.; Chen, P.; Zhang, C.; Zhao, F.; Xie, Z.; Zhang, S.; Wang, N. Genome sequencing and CRISPR/Cas9 gene editing of an early flowering Mini-Citrus (Fortunella hindsii). Plant Biotechnol. J.; 2019; 17, pp. 2199-2210. [DOI: https://dx.doi.org/10.1111/pbi.13132] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/31004551]

19. Tränkner, C.; Lehmann, S.; Hoenicka, H.; Hanke, M.-V.; Fladung, M.; Lenhardt, D.; Dunemann, F.; Gau, A.; Schlangen, K.; Malnoy, M. Over-expression of an FT-homologous gene of apple induces early flowering in annual and perennial plants. Planta; 2010; 232, pp. 1309-1324. [DOI: https://dx.doi.org/10.1007/s00425-010-1254-2]

20. Winterhagen, P.; Tiyayon, P.; Samach, A.; Hegele, M.; Wünsche, J.N. Isolation and characterization of FLOWERING LOCUS T subforms and APETALA1 of the subtropical fruit tree Dimocarpus longan. Plant Physiol. Biochem.; 2013; 71, pp. 184-190. [DOI: https://dx.doi.org/10.1016/j.plaphy.2013.07.013] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/23954797]

21. Ziv, D.; Zviran, T.; Zezak, O.; Samach, A.; Irihimovitch, V. Expression profiling of FLOWERING LOCUS T-Like Gene in alternate bearing ‘Hass’ Avocado trees suggests a role for PaFT in Avocado flower induction. PLoS ONE; 2014; 9, e110613. [DOI: https://dx.doi.org/10.1371/journal.pone.0110613] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/25330324]

22. Voogd, C.; Brian, L.A.; Wang, T.; Allan, A.C.; Varkonyi-Gasic, E. Three FT and multiple CEN and BFT genes regulate maturity, flowering, and vegetative phenology in kiwifruit. J. Exp. Bot.; 2017; 68, pp. 1539-1553. [DOI: https://dx.doi.org/10.1093/jxb/erx044] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/28369532]

23. Patil, H.B.; Chaurasia, A.K.; Kumar, S.; Krishna, B.; Subramaniam, V.R.; Sane, A.P.; Sane, P.V. Synchronized flowering in pomegranate, following pruning, is associated with expression of the FLOWERING LOCUS T homolog, PgFT1. Physiol. Plant.; 2022; 174, e13620. [DOI: https://dx.doi.org/10.1111/ppl.13620]

24. Jiang, Y.; Zhu, Y.; Peng, Z.; Su, W.; Peng, J.; Yuan, Y.; Zhang, L.; Zhang, Z.; Yang, X.; Gao, Y. Two FT genes synergistically regulate the reproductive transition of loquat. Hortic. Plant J.; 2024; [DOI: https://dx.doi.org/10.1016/j.hpj.2023.08.003]

25. Cao, K.; Cui, L.; Zhou, X.; Ye, L.; Zou, Z.; Deng, S. Four tomato FLOWERING LOCUS T-like proteins act antagonistically to regulate floral initiation. Front. Plant Sci.; 2016; 6, 1213. [DOI: https://dx.doi.org/10.3389/fpls.2015.01213]

26. Corbesier, L.; Vincent, C.; Jang, S.; Fornara, F.; Fan, Q.; Searle, I.; Giakountis, A.; Farrona, S.; Gissot, L.; Turnbull, C. FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science; 2007; 316, pp. 1030-1033. [DOI: https://dx.doi.org/10.1126/science.1141752]

27. Pin, P.; Nilsson, O. The multifaceted roles of FLOWERING LOCUS T in plant development. Plant, cell environment; 2012; 35, pp. 1742-1755. [DOI: https://dx.doi.org/10.1111/j.1365-3040.2012.02558.x]

28. Endo, T.; Shimada, T.; Fujii, H.; Kobayashi, Y.; Araki, T.; Omura, M. Ectopic expression of an FT homolog from Citrus confers an early flowering phenotype on trifoliate orange (Poncirus trifoliata L. Raf.). Transgenic Res.; 2005; 14, pp. 703-712. [DOI: https://dx.doi.org/10.1007/s11248-005-6632-3]

29. Nishikawa, F.; Endo, T.; Shimada, T.; Fujii, H.; Shimizu, T.; Omura, M.; Ikoma, Y. Increased CiFT abundance in the stem correlates with floral induction by low temperature in Satsuma mandarin (Citrus unshiu Marc.). J. Exp. Bot.; 2007; 58, pp. 3915-3927. [DOI: https://dx.doi.org/10.1093/jxb/erm246]

30. Nishikawa, F.; Iwasaki, M.; Fukamachi, H.; Nonaka, K.; Imai, A.; Endo, T. Seasonal changes of citrus FLOWERING LOCUS T gene expression in kumquat. Bull. Natl. Inst. Fruit Tree Sci.; 2011; 12, pp. 27-32.

31. Wu, Y.-M.; Ma, Y.-J.; Wang, M.; Zhou, H.; Gan, Z.-M.; Zeng, R.-F.; Ye, L.-X.; Zhou, J.-J.; Zhang, J.-Z.; Hu, C.-G. Mobility of FLOWERING LOCUS T protein as a systemic signal in trifoliate orange and its low accumulation in grafted juvenile scions. Hortic. Res.; 2022; 9, uhac056. [DOI: https://dx.doi.org/10.1093/hr/uhac056]

32. Soares, J.M.; Weber, K.C.; Qiu, W.; Stanton, D.; Mahmoud, L.M.; Wu, H.; Huyck, P.; Zale, J.; Al Jasim, K.; Grosser, J.W. The vascular targeted citrus FLOWERING LOCUS T3 gene promotes non-inductive early flowering in transgenic Carrizo rootstocks and grafted juvenile scions. Sci. Rep.; 2020; 10, 21404. [DOI: https://dx.doi.org/10.1038/s41598-020-78417-9] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/33293614]

33. Pajon, M.; Febres, V.J.; Moore, G.A. Expression patterns of flowering genes in leaves of ‘Pineapple’sweet orange [Citrus sinensis (L.) Osbeck] and pummelo (Citrus grandis Osb eck). BMC Plant Biol.; 2017; 17, pp. 1-7. [DOI: https://dx.doi.org/10.1186/s12870-017-1094-3]

34. Sreekantan, L.; Thomas, M.R. VvFT and VvMADS8, the grapevine homologues of the floral integrators FT and SOC1, have unique expression patterns in grapevine and hasten flowering in Arabidopsis. Funct. Plant Biol.; 2006; 33, pp. 1129-1139. [DOI: https://dx.doi.org/10.1071/FP06144]

35. Srikanth, A.; Schmid, M. Regulation of flowering time: All roads lead to Rome. Cell. Mol. Life Sci.; 2011; 68, pp. 2013-2037. [DOI: https://dx.doi.org/10.1007/s00018-011-0673-y] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/21611891]

36. Wang, Y.-H.; He, X.-H.; Yu, H.-X.; Mo, X.; Fan, Y.; Fan, Z.-Y.; Xie, X.-J.; Liu, Y.; Luo, C. Overexpression of four MiTFL1 genes from mango delays the flowering time in transgenic Arabidopsis. BMC Plant Biol.; 2021; 21, pp. 1-16. [DOI: https://dx.doi.org/10.1186/s12870-021-03199-9] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/34493220]

37. Yamagishi, N.; Sasaki, S.; Yamagata, K.; Komori, S.; Nagase, M.; Wada, M.; Yamamoto, T.; Yoshikawa, N. Promotion of flowering and reduction of a generation time in apple seedlings by ectopical expression of the Arabidopsis thaliana FT gene using the Apple latent spherical virus vector. Plant Mol. Biol.; 2011; 75, pp. 193-204. [DOI: https://dx.doi.org/10.1007/s11103-010-9718-0]

38. Ye, L.-X.; Zhang, J.-X.; Hou, X.-J.; Qiu, M.-Q.; Wang, W.-F.; Zhang, J.-X.; Hu, C.-G.; Zhang, J.-Z. A MADS-box gene CiMADS43 is involved in citrus flowering and leaf development through interaction with CiAGL9. Int. J. Mol. Sci.; 2021; 22, 5205. [DOI: https://dx.doi.org/10.3390/ijms22105205]

39. Rothkegel, K.; Sánchez, E.; Montes, C.; Greve, M.; Tapia, S.; Bravo, S.; Prieto, H.; Almeida, A.M. DNA methylation and small interference RNAs participate in the regulation of MADS-box genes involved in dormancy in sweet cherry (Prunus avium L.). Tree Physiol.; 2017; 37, pp. 1739-1751. [DOI: https://dx.doi.org/10.1093/treephys/tpx055]

40. Flachowsky, H.; Peil, A.; Sopanen, T.; Elo, A.; Hanke, V. Overexpression of BpMADS4 from silver birch (Betula pendula Roth.) induces early-flowering in apple (Malus× domestica Borkh.). Plant Breed.; 2007; 126, pp. 137-145. [DOI: https://dx.doi.org/10.1111/j.1439-0523.2007.01344.x]

41. Voogd, C.; Wang, T.; Varkonyi-Gasic, E. Functional and expression analyses of kiwifruit SOC1-like genes suggest that they may not have a role in the transition to flowering but may affect the duration of dormancy. J. Exp. Bot.; 2015; 66, pp. 4699-4710. [DOI: https://dx.doi.org/10.1093/jxb/erv234]

42. Weigel, D.; Nilsson, O. A developmental switch sufficient for flower initiation in diverse plants. Nature; 1995; 377, pp. 495-500. [DOI: https://dx.doi.org/10.1038/377495a0] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/7566146]

43. Carmona, M.J.; Cubas, P.; Martınez-Zapater, J.M. VFL, the grapevine FLORICAULA/LEAFY ortholog, is expressed in meristematic regions independently of their fate. Plant Physiol.; 2002; 130, pp. 68-77. [DOI: https://dx.doi.org/10.1104/pp.002428]

44. Maizel, A.; Busch, M.A.; Tanahashi, T.; Perkovic, J.; Kato, M.; Hasebe, M.; Weigel, D. The floral regulator LEAFY evolves by substitutions in the DNA binding domain. Science; 2005; 308, pp. 260-263. [DOI: https://dx.doi.org/10.1126/science.1108229] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/15821093]

45. Flachowsky, H.; Hättasch, C.; Höfer, M.; Peil, A.; Hanke, M.-V. Overexpression of LEAFY in apple leads to a columnar phenotype with shorter internodes. Planta; 2010; 231, pp. 251-263. [DOI: https://dx.doi.org/10.1007/s00425-009-1041-0]

46. Calonje, M.; Cubas, P.; Martínez-Zapater, J.M.; Carmona, M.a.J. Floral meristem identity genes are expressed during tendril development in grapevine. Plant Physiol.; 2004; 135, pp. 1491-1501. [DOI: https://dx.doi.org/10.1104/pp.104.040832] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/15247405]

47. Theißen, G. Development of floral organ identity: Stories from the MADS house. Curr. Opin. Plant Biol.; 2001; 4, pp. 75-85. [DOI: https://dx.doi.org/10.1016/S1369-5266(00)00139-4]

48. Molinero-Rosales, N.; Jamilena, M.; Zurita, S.; Gómez, P.; Capel, J.; Lozano, R. FALSIFLORA, the tomato orthologue of FLORICAULA and LEAFY, controls flowering time and floral meristem identity. Plant J.; 1999; 20, pp. 685-693. [DOI: https://dx.doi.org/10.1046/j.1365-313X.1999.00641.x]

49. Jiang, X.; Lubini, G.; Hernandes-Lopes, J.; Rijnsburger, K.; Veltkamp, V.; de Maagd, R.A.; Angenent, G.C.; Bemer, M. FRUITFULL-like genes regulate flowering time and inflorescence architecture in tomato. Plant Cell; 2022; 34, pp. 1002-1019. [DOI: https://dx.doi.org/10.1093/plcell/koab298]

50. Cheng, J.-Z.; Zhou, Y.-P.; Lv, T.-X.; Xie, C.-P.; Tian, C.-E. Research progress on the autonomous flowering time pathway in Arabidopsis. Physiol. Mol. Biol. Plants; 2017; 23, pp. 477-485. [DOI: https://dx.doi.org/10.1007/s12298-017-0458-3]

51. Cheng, H.; Qin, L.; Lee, S.; Fu, X.; Richards, D.E.; Cao, D.; Luo, D.; Harberd, N.P.; Peng, J. Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function. Development; 2004; 131, pp. 1055-1064. [DOI: https://dx.doi.org/10.1242/dev.00992] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/14973286]

52. Helliwell, C.A.; Wood, C.C.; Robertson, M.; James Peacock, W.; Dennis, E.S. The Arabidopsis FLC protein interacts directly in vivo with SOC1 and FT chromatin and is part of a high-molecular-weight protein complex. Plant J.; 2006; 46, pp. 183-192. [DOI: https://dx.doi.org/10.1111/j.1365-313X.2006.02686.x]

53. Kim, H.-J.; Hyun, Y.; Park, J.-Y.; Park, M.-J.; Park, M.-K.; Kim, M.D.; Kim, H.-J.; Lee, M.H.; Moon, J.; Lee, I. A genetic link between cold responses and flowering time through FVE in Arabidopsis thaliana. Nat. Genet.; 2004; 36, pp. 167-171. [DOI: https://dx.doi.org/10.1038/ng1298]

54. Liu, X.L.; Covington, M.F.; Fankhauser, C.; Chory, J.; Wagner, D.R. ELF3 encodes a circadian clock–regulated nuclear protein that functions in an Arabidopsis PHYB signal transduction pathway. Plant Cell; 2001; 13, pp. 1293-1304.

55. Marquardt, S.; Boss, P.; Hadfield, J.; Dean, C. Additional targets of the Arabidopsis autonomous pathway members, FCA and FY. J. Exp. Bot.; 2006; 57, pp. 3379-3386. [DOI: https://dx.doi.org/10.1093/jxb/erl073]

56. Sawa, M.; Nusinow, D.A.; Kay, S.A.; Imaizumi, T. FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science; 2007; 318, pp. 261-265. [DOI: https://dx.doi.org/10.1126/science.1146994]

57. Searle, I.; He, Y.; Turck, F.; Vincent, C.; Fornara, F.; Kröber, S.; Amasino, R.A.; Coupland, G. The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes Dev.; 2006; 20, pp. 898-912. [DOI: https://dx.doi.org/10.1101/gad.373506]

58. Xin, W.; Wang, Z.; Liang, Y.; Wang, Y.; Hu, Y. Dynamic expression reveals a two-step patterning of WUS and CLV3 during axillary shoot meristem formation in Arabidopsis. J. Plant Physiol.; 2017; 214, pp. 1-6. [DOI: https://dx.doi.org/10.1016/j.jplph.2017.03.017] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/28399422]

59. Park, S.J.; Jiang, K.; Schatz, M.C.; Lippman, Z.B. Rate of meristem maturation determines inflorescence architecture in tomato. Proc. Natl. Acad. Sci. USA; 2012; 109, pp. 639-644. [DOI: https://dx.doi.org/10.1073/pnas.1114963109]

60. Mao, L.; Begum, D.; Chuang, H.-w.; Budiman, M.A.; Szymkowiak, E.J.; Irish, E.E.; Wing, R.A. JOINTLESS is a MADS-box gene controlling tomato flower abscissionzone development. Nature; 2000; 406, pp. 910-913. [DOI: https://dx.doi.org/10.1038/35022611]

61. Daminato, M.; Masiero, S.; Resentini, F.; Lovisetto, A.; Casadoro, G. Characterization of TM8, a MADS-box gene expressed in tomato flowers. BMC Plant Biol.; 2014; 14, pp. 1-15. [DOI: https://dx.doi.org/10.1186/s12870-014-0319-y] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/25433802]

62. Fonseca, R.; Capel, C.; Lebrón, R.; Ortiz-Atienza, A.; Yuste-Lisbona, F.J.; Angosto, T.; Capel, J.; Lozano, R. Insights into the functional role of tomato TM6 as a transcriptional regulator of flower development. Hortic. Res.; 2024; 11, uhae019. [DOI: https://dx.doi.org/10.1093/hr/uhae019] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/38464473]

63. de Martino, G.; Pan, I.; Emmanuel, E.; Levy, A.; Irish, V.F. Functional analyses of two tomato APETALA3 genes demonstrate diversification in their roles in regulating floral development. Plant Cell; 2006; 18, pp. 1833-1845. [DOI: https://dx.doi.org/10.1105/tpc.106.042978] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/16844904]

64. MacAlister, C.A.; Park, S.J.; Jiang, K.; Marcel, F.; Bendahmane, A.; Izkovich, Y.; Eshed, Y.; Lippman, Z.B. Synchronization of the flowering transition by the tomato TERMINATING FLOWER gene. Nat. Genet.; 2012; 44, pp. 1393-1398. [DOI: https://dx.doi.org/10.1038/ng.2465]

65. Lifschitz, E.; Eviatar, T.; Rozman, A.; Shalit, A.; Goldshmidt, A.; Amsellem, Z.; Alvarez, J.P.; Eshed, Y. The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc. Natl. Acad. Sci. USA; 2006; 103, pp. 6398-6403. [DOI: https://dx.doi.org/10.1073/pnas.0601620103]

66. Almutairi, Z.; Sadder, M. Cloning and expression profiling polycomb gene VERNALIZATION INSENSITIVE 3 in tomato. Biol. Plant.; 2014; 58, pp. 419-426. [DOI: https://dx.doi.org/10.1007/s10535-014-0421-x]

67. Guo, J.; Cheng, Q.; Sun, L.; Zhang, C.; Shen, H. The SEPALLATA-like CaSEP5 gene regulates flower sepal, pedicel, and fruit development in pepper (Capsicum annuum L.). Sci. Hortic.; 2024; 330, 113100. [DOI: https://dx.doi.org/10.1016/j.scienta.2024.113100]

68. Wu, X.; Gan, Z.; Xu, F.; Qian, J.; Qian, M.; Ai, H.; Feng, T.; Lu, X.; Li, R.; Huang, X. Molecular characterization of pepper PEBP genes reveals the diverse functions of CaFTs in flowering and plant architecture. Sci. Hortic.; 2024; 335, 113345. [DOI: https://dx.doi.org/10.1016/j.scienta.2024.113345]

69. Cohen, O.; Borovsky, Y.; David-Schwartz, R.; Paran, I. Capsicum annuum S (CaS) promotes reproductive transition and is required for flower formation in pepper (Capsicum annuum). New Phytol.; 2014; 202, pp. 1014-1023. [DOI: https://dx.doi.org/10.1111/nph.12711] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/24716519]

70. Kazan, K.; Lyons, R. The link between flowering time and stress tolerance. J. Exp. Bot.; 2016; 67, pp. 47-60. [DOI: https://dx.doi.org/10.1093/jxb/erv441]

71. Cooke, J.E.; Eriksson, M.E.; Junttila, O. The dynamic nature of bud dormancy in trees: Environmental control and molecular mechanisms. Plant Cell Environ.; 2012; 35, pp. 1707-1728. [DOI: https://dx.doi.org/10.1111/j.1365-3040.2012.02552.x] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/22670814]

72. Simpson, G.G.; Dean, C. Arabidopsis, the Rosetta stone of flowering time?. Science; 2002; 296, pp. 285-289. [DOI: https://dx.doi.org/10.1126/science.296.5566.285] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/11951029]

73. Liu, L.; Zhang, Y.; Yu, H. Florigen trafficking integrates photoperiod and temperature signals in Arabidopsis. J. Integr. Plant Biol.; 2020; 62, pp. 1385-1398. [DOI: https://dx.doi.org/10.1111/jipb.13000] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/32729982]

74. Menzel, C.; Simpson, D. Temperatures above 20 C reduce flowering in lychee (Litchi chinensis Sonn.). J. Hortic. Sci.; 1995; 70, pp. 981-988. [DOI: https://dx.doi.org/10.1080/14620316.1995.11515374]

75. Moss, G. Temperature effects on flower initiation in sweet orange (Citrus sinensis). Aust. J. Agric. Res.; 1976; 27, pp. 399-407. [DOI: https://dx.doi.org/10.1071/AR9760399]

76. Hackett, W.P.; Hartmann, H. Inflorescence formation in olive as influenced by low temperature, photoperiod, and leaf area. Bot. Gaz.; 1964; 125, pp. 65-72. [DOI: https://dx.doi.org/10.1086/336247]

77. Eltom, M.; Trought, M.C.; Agnew, R.; Parker, A.; Winefield, C.S. Pre-budburst temperature influences the inner and outer arm morphology, phenology, flower number, fruitset, TSS accumulation and variability of Vitis vinifera L. Sauvignon Blanc bunches. Aust. J. Grape Wine Res.; 2017; 23, pp. 280-286. [DOI: https://dx.doi.org/10.1111/ajgw.12260]

78. García-Luís, A.; Kandušer, M. Changes in dormancy and sensitivity to vernalization in axillary buds of satsuma mandarin examined in vitro during the annual cycle. Ann. Bot.; 1995; 76, pp. 451-455. [DOI: https://dx.doi.org/10.1006/anbo.1995.1119]

79. Matsuda, N.; Ikeda, K.; Kurosaka, M.; Takashina, T.; Isuzugawa, K.; Endo, T.; Omura, M. Early flowering phenotype in transgenic pears (Pyrus communis L.) expressing the CiFT gene. J. Jpn. Soc. Hortic. Sci.; 2009; 78, pp. 410-416. [DOI: https://dx.doi.org/10.2503/jjshs1.78.410]

80. Michaels, S.D.; Amasino, R.M. Flowering locus C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell; 1999; 11, pp. 949-956. [DOI: https://dx.doi.org/10.1105/tpc.11.5.949]

81. Hu, X.; Kong, X.; Wang, C.; Ma, L.; Zhao, J.; Wei, J.; Zhang, X.; Loake, G.J.; Zhang, T.; Huang, J. Proteasome-mediated degradation of FRIGIDA modulates flowering time in Arabidopsis during vernalization. Plant Cell; 2014; 26, pp. 4763-4781. [DOI: https://dx.doi.org/10.1105/tpc.114.132738]

82. Whiley, A.; Rasmussen, T.; Saranah, J.; Wolstenholme, B.J.J.o.H.S. Effect of temperature on growth, dry matter production and starch accumulation in ten mango (Mangifera indica L.) cultivars. J. Hortic. Sci.; 1989; 64, pp. 753-765. [DOI: https://dx.doi.org/10.1080/14620316.1989.11516018]

83. Chaikiattiyos, S.; Menzel, C.; Rasmussen, T. Floral induction in tropical fruit trees: Effects of temperature and water supply. J. Hortic. Sci.; 1994; 69, pp. 397-415. [DOI: https://dx.doi.org/10.1080/14620316.1994.11516469]

84. Kaur, H.; Sidhu, G.S.; Mittal, A.; Yadav, I.S.; Mittal, M.; Singla, D.; Singh, N.; Chhuneja, P. Comparative transcriptomics in alternate bearing cultivar Dashehari reveals the genetic model of flowering in mango. Front. Genet.; 2023; 13, 1061168. [DOI: https://dx.doi.org/10.3389/fgene.2022.1061168] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/36704344]

85. Kotoda, N.; Iwanami, H.; Takahashi, S.; Abe, K. Antisense expression of MdTFL1, a TFL1-like gene, reduces the juvenile phase in apple. J. Am. Soc. Hortic. Sci.; 2006; 131, pp. 74-81. [DOI: https://dx.doi.org/10.21273/JASHS.131.1.74]

86. Freiman, A.; Shlizerman, L.; Golobovitch, S.; Yablovitz, Z.; Korchinsky, R.; Cohen, Y.; Samach, A.; Chevreau, E.; Le Roux, P.-M.; Patocchi, A. Development of a transgenic early flowering pear (Pyrus communis L.) genotype by RNAi silencing of PcTFL1-1 and PcTFL1-2. Planta; 2012; 235, pp. 1239-1251. [DOI: https://dx.doi.org/10.1007/s00425-011-1571-0] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/22203321]

87. Ma, Y.-J.; Li, P.-T.; Sun, L.-M.; Zhou, H.; Zeng, R.-F.; Ai, X.-Y.; Zhang, J.-Z.; Hu, C.-G. HD-ZIP I transcription factor (pthb13) negatively regulates citrus flowering through binding to FLOWERING LOCUS C Promoter. Plants; 2020; 9, 114. [DOI: https://dx.doi.org/10.3390/plants9010114] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/31963238]

88. Nishikawa, F. Regulation of floral induction in citrus. J. Jpn. Soc. Hortic. Sci.; 2013; 82, pp. 283-292. [DOI: https://dx.doi.org/10.2503/jjshs1.82.283]

89. Chica, E.J.; Albrigo, L.G. Expression of flower promoting genes in sweet orange during floral inductive water deficits. J. Am. Soc. Hortic. Sci.; 2013; 138, pp. 88-94. [DOI: https://dx.doi.org/10.21273/JASHS.138.2.88]

90. Zhou, H.; Zeng, R.F.; Liu, T.J.; Ai, X.Y.; Ren, M.K.; Zhou, J.J.; Hu, C.G.; Zhang, J.Z. Drought and low temperature-induced NF-YA1 activates FT expression to promote citrus flowering. Plant Cell Environ.; 2022; 45, pp. 3505-3522. [DOI: https://dx.doi.org/10.1111/pce.14442]

91. Zhang, D.; Ji, K.; Wang, J.; Liu, X.; Zhou, Z.; Huang, R.; Ai, G.; Li, Y.; Wang, X.; Wang, T. Nuclear factor Y-A3b binds to the SINGLE FLOWER TRUSS promoter and regulates flowering time in tomato. Hortic. Res.; 2024; 11, uhae088. [DOI: https://dx.doi.org/10.1093/hr/uhae088] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/38799124]

92. Bradley, D.; Carpenter, R.; Copsey, L.; Vincent, C.; Rothstein, S.; Coen, E. Control of inflorescence architecture in Antirrhinum. Nature; 1996; 379, pp. 791-797. [DOI: https://dx.doi.org/10.1038/379791a0]

93. Ratcliffe, O.J.; Bradley, D.J.; Coen, E.S. Separation of shoot and floral identity in Arabidopsis. Development; 1999; 126, pp. 1109-1120. [DOI: https://dx.doi.org/10.1242/dev.126.6.1109]

94. Carmona, M.J.; Calonje, M.; Martínez-Zapater, J.M.J.P.m.b. The FT/TFL1 gene family in grapevine. Plant Mol. Biol.; 2007; 63, pp. 637-650. [DOI: https://dx.doi.org/10.1007/s11103-006-9113-z]

95. Molinero-Rosales, N.; Latorre, A.; Jamilena, M.; Lozano, R. SINGLE FLOWER TRUSS regulates the transition and maintenance of flowering in tomato. Planta; 2004; 218, pp. 427-434. [DOI: https://dx.doi.org/10.1007/s00425-003-1109-1]

96. Mesejo, C.; Marzal, A.; Martínez-Fuentes, A.; Reig, C.; de Lucas, M.; Iglesias, D.J.; Primo-Millo, E.; Blazquez, M.A.; Agustí, M. Reversion of fruit-dependent inhibition of flowering in Citrus requires sprouting of buds with epigenetically silenced CcMADS19. New Phytol.; 2022; 233, pp. 526-533. [DOI: https://dx.doi.org/10.1111/nph.17681]

97. Ding, J.; Zhang, B.; Li, Y.; André, D.; Nilsson, O. Phytochrome B and PHYTOCHROME INTERACTING FACTOR8 modulate seasonal growth in trees. New Phytol.; 2021; 232, pp. 2339-2352. [DOI: https://dx.doi.org/10.1111/nph.17350]

98. Dantas, D.; Bressan-Smith, R.; Noriega, X.; Pérez, F.J. Buds of “Italia melhorada” grapevines grown under tropical conditions develop a quiescent state. Environ. Exp. Bot.; 2020; 171, 103951. [DOI: https://dx.doi.org/10.1016/j.envexpbot.2019.103951]

99. Kumar, S.V.; Lucyshyn, D.; Jaeger, K.E.; Alós, E.; Alvey, E.; Harberd, N.P.; Wigge, P.A. Transcription factor PIF4 controls the thermosensory activation of flowering. Nature; 2012; 484, pp. 242-245. [DOI: https://dx.doi.org/10.1038/nature10928] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/22437497]

100. Zhang, R.; Yang, C.; Jiang, Y.; Li, L. A PIF7-CONSTANS-centered molecular regulatory network underlying shade-accelerated flowering. Mol. Plant; 2019; 12, pp. 1587-1597. [DOI: https://dx.doi.org/10.1016/j.molp.2019.09.007] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/31568831]

101. Carmona, M.J.; Chaïb, J.; Martínez-Zapater, J.M.; Thomas, M.R. A molecular genetic perspective of reproductive development in grapevine. J. Exp. Bot.; 2008; 59, pp. 2579-2596. [DOI: https://dx.doi.org/10.1093/jxb/ern160]

102. Boss, P.K.; Sensi, E.; Hua, C.; Davies, C.; Thomas, M.R. Cloning and characterisation of grapevine (Vitis vinifera L.) MADS-box genes expressed during inflorescence and berry development. Plant Sci.; 2002; 162, pp. 887-895. [DOI: https://dx.doi.org/10.1016/S0168-9452(02)00034-1]

103. Alvarez-Buylla, E.R.; Liljegren, S.J.; Pelaz, S.; Gold, S.E.; Burgeff, C.; Ditta, G.S.; Vergara-Silva, F.; Yanofsky, M.F. MADS-box gene evolution beyond flowers: Expression in pollen, endosperm, guard cells, roots and trichomes. Plant J.; 2000; 24, pp. 457-466.

104. Yan, Z.; Liang, D.; Liu, H.; Zheng, G. FLC: A key regulator of flowering time in Arabidopsis. Russ. J. Plant Physiol.; 2010; 57, pp. 166-174. [DOI: https://dx.doi.org/10.1134/S1021443710020020]

105. Abou-Elwafa, S.F.; Büttner, B.; Chia, T.; Schulze-Buxloh, G.; Hohmann, U.; Mutasa-Göttgens, E.; Jung, C.; Müller, A.E. Conservation and divergence of autonomous pathway genes in the flowering regulatory network of Beta vulgaris. J. Exp. Bot.; 2011; 62, pp. 3359-3374. [DOI: https://dx.doi.org/10.1093/jxb/erq321] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/20974738]

106. Michaels, S.D.; He, Y.; Scortecci, K.C.; Amasino, R.M. Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. Proc. Natl. Acad. Sci. USA; 2003; 100, pp. 10102-10107. [DOI: https://dx.doi.org/10.1073/pnas.1531467100] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/12904584]

107. Boss, P.K.; Bastow, R.M.; Mylne, J.S.; Dean, C. Multiple pathways in the decision to flower: Enabling, promoting, and resetting. The Plant Cell; 2004; 16, pp. S18-S31. [DOI: https://dx.doi.org/10.1105/tpc.015958]

108. Kobayashi, Y.; Weigel, D. Move on up, it’s time for change—Mobile signals controlling photoperiod-dependent flowering. Genes Dev.; 2007; 21, pp. 2371-2384. [DOI: https://dx.doi.org/10.1101/gad.1589007]

109. Simpson, G.G. The autonomous pathway: Epigenetic and post-transcriptional gene regulation in the control of Arabidopsis flowering time. Curr. Opin. Plant Biol.; 2004; 7, pp. 570-574. [DOI: https://dx.doi.org/10.1016/j.pbi.2004.07.002]

110. Sheldon, C.C.; Rouse, D.T.; Finnegan, E.J.; Peacock, W.J.; Dennis, E.S. The molecular basis of vernalization: The central role of FLOWERING LOCUS C (FLC). Proc. Natl. Acad. Sci. USA; 2000; 97, pp. 3753-3758. [DOI: https://dx.doi.org/10.1073/pnas.97.7.3753]

111. Zhang, Q.; Zhong, S.; Dong, Q.; Yang, H.; Yang, H.; Tan, F.; Chen, C.; Ren, T.; Shen, J.; Cao, G. Identification of Photoperiod-and Phytohormone-Responsive DNA-Binding One Zinc Finger (Dof) Transcription Factors in Akebia trifoliata via Genome-Wide Expression Analysis. Int. J. Mol. Sci.; 2023; 24, 4973. [DOI: https://dx.doi.org/10.3390/ijms24054973]

112. Wang, H.; Yang, Y.; Zhang, Y.; Zhao, T.; Jiang, J.; Li, J.; Xu, X.; Yang, H. Transcriptome analysis of flower development and mining of genes related to flowering time in tomato (Solanum lycopersicum). Int. J. Mol. Sci.; 2021; 22, 8128. [DOI: https://dx.doi.org/10.3390/ijms22158128]

113. Baldwin, J. The relation between weather and fruitfulness of the Sultana vine. Aust. J. Agric. Res.; 1964; 15, pp. 920-928. [DOI: https://dx.doi.org/10.1071/AR9640920]

114. May, P.; Antcliff, A. The effect of shading on fruitfulness and yield in the Sultana. J. Hortic. Sci.; 1963; 38, pp. 85-94. [DOI: https://dx.doi.org/10.1080/00221589.1963.11514062]

115. Buttrose, M. Climatic factors and fruitfulness in grapevines. Hortic. Abstr.; 1974; 44, 6.

116. Fennell, A.; Hoover, E. Photoperiod influences growth, bud dormancy, and cold acclimation in Vitis labruscana and V. riparia. J. Am. Soc. Hortic. Sci.; 1991; 116, pp. 270-273. [DOI: https://dx.doi.org/10.21273/JASHS.116.2.270]

117. Brandoli, C.; Petri, C.; Egea-Cortines, M.; Weiss, J. Gigantea: Uncovering new functions in flower development. Genes; 2020; 11, 1142. [DOI: https://dx.doi.org/10.3390/genes11101142] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/32998354]

118. Andrade, L.; Lu, Y.; Cordeiro, A.; Costa, J.M.; Wigge, P.A.; Saibo, N.J.; Jaeger, K.E. The evening complex integrates photoperiod signals to control flowering in rice. Proc. Natl. Acad. Sci. USA; 2022; 119, e2122582119. [DOI: https://dx.doi.org/10.1073/pnas.2122582119]

119. Anwer, M.U.; Davis, A.; Davis, S.J.; Quint, M. Photoperiod sensing of the circadian clock is controlled by EARLY FLOWERING 3 and GIGANTEA. Plant J.; 2020; 101, pp. 1397-1410. [DOI: https://dx.doi.org/10.1111/tpj.14604]

120. Tylewicz, S.; Tsuji, H.; Miskolczi, P.; Petterle, A.; Azeez, A.; Jonsson, K.; Shimamoto, K.; Bhalerao, R.P. Dual role of tree florigen activation complex component FD in photoperiodic growth control and adaptive response pathways. Proc. Natl. Acad. Sci. USA; 2015; 112, pp. 3140-3145. [DOI: https://dx.doi.org/10.1073/pnas.1423440112]

121. Sreekantan, L.; Mathiason, K.; Grimplet, J.; Schlauch, K.; Dickerson, J.A.; Fennell, A.Y. Differential floral development and gene expression in grapevines during long and short photoperiods suggests a role for floral genes in dormancy transitioning. Plant Mol. Biol.; 2010; 73, pp. 191-205. [DOI: https://dx.doi.org/10.1007/s11103-010-9611-x]

122. Pérez, F.J.; Kühn, N.; Ormeño-Nuñez, J.; Rubio, S. The expression of VvPHYA and VvPHYB transcripts is differently regulated by photoperiod in leaves and buds of grapevines. Plant Signal. Behav.; 2009; 4, pp. 614-616. [DOI: https://dx.doi.org/10.4161/psb.4.7.8907] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/19820336]

123. Valverde, F.; Mouradov, A.; Soppe, W.; Ravenscroft, D.; Samach, A.; Coupland, G. Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science; 2004; 303, pp. 1003-1006. [DOI: https://dx.doi.org/10.1126/science.1091761]

124. Suárez-López, P.; Wheatley, K.; Robson, F.; Onouchi, H.; Valverde, F.; Coupland, G. CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature; 2001; 410, pp. 1116-1120. [DOI: https://dx.doi.org/10.1038/35074138] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/11323677]

125. Zhou, L.; Lu, Y.; Huang, J.; Sha, Z.; Mo, W.; Xue, J.; Ma, S.; Shi, W.; Yang, Z.; Gao, J. Arabidopsis CIB3 regulates photoperiodic flowering in an FKF1-dependent way. Biosci. Biotechnol. Biochem.; 2021; 85, pp. 765-774. [DOI: https://dx.doi.org/10.1093/bbb/zbaa120] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/33686404]

126. Giliberto, L.; Perrotta, G.; Pallara, P.; Weller, J.L.; Fraser, P.D.; Bramley, P.M.; Fiore, A.; Tavazza, M.; Giuliano, G. Manipulation of the blue light photoreceptor cryptochrome 2 in tomato affects vegetative development, flowering time, and fruit antioxidant content. Plant Physiol.; 2005; 137, pp. 199-208. [DOI: https://dx.doi.org/10.1104/pp.104.051987] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/15618424]

127. Song, Y.H.; Smith, R.W.; To, B.J.; Millar, A.J.; Imaizumi, T. FKF1 conveys timing information for CONSTANS stabilization in photoperiodic flowering. Science; 2012; 336, pp. 1045-1049. [DOI: https://dx.doi.org/10.1126/science.1219644] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/22628657]

128. Xu, P.; Chen, H.; Li, T.; Xu, F.; Mao, Z.; Cao, X.; Miao, L.; Du, S.; Hua, J.; Zhao, J. Blue light-dependent interactions of CRY1 with GID1 and DELLA proteins regulate gibberellin signaling and photomorphogenesis in Arabidopsis. Plant Cell; 2021; 33, pp. 2375-2394. [DOI: https://dx.doi.org/10.1093/plcell/koab124] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/34046684]

129. Bao, S.; Hua, C.; Huang, G.; Cheng, P.; Gong, X.; Shen, L.; Yu, H. Molecular basis of natural variation in photoperiodic flowering responses. Dev. Cell; 2019; 50, pp. 90-101. e103. [DOI: https://dx.doi.org/10.1016/j.devcel.2019.05.018]

130. Arana, M.V.; Marín-de la Rosa, N.; Maloof, J.N.; Blázquez, M.A.; Alabadí, D. Circadian oscillation of gibberellin signaling in Arabidopsis. Proc. Natl. Acad. Sci. USA; 2011; 108, pp. 9292-9297. [DOI: https://dx.doi.org/10.1073/pnas.1101050108]

131. Fowler, S.; Lee, K.; Onouchi, H.; Samach, A.; Richardson, K.; Morris, B.; Coupland, G.; Putterill, J. GIGANTEA: A circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J.; 1999; 18, pp. 4679-4688. [DOI: https://dx.doi.org/10.1093/emboj/18.17.4679] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/10469647]

132. Kim, W.-Y.; Fujiwara, S.; Suh, S.-S.; Kim, J.; Kim, Y.; Han, L.; David, K.; Putterill, J.; Nam, H.G.; Somers, D.E. ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature; 2007; 449, pp. 356-360. [DOI: https://dx.doi.org/10.1038/nature06132]

133. Zhang, D.; Ai, G.; Ji, K.; Huang, R.; Chen, C.; Yang, Z.; Wang, J.; Cui, L.; Li, G.; Tahira, M. EARLY FLOWERING is a dominant gain-of-function allele of FANTASTIC FOUR 1/2c that promotes early flowering in tomato. Plant Biotechnol. J.; 2024; 22, pp. 698-711. [DOI: https://dx.doi.org/10.1111/pbi.14217] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/37929693]

134. Bao, S.; Hua, C.; Shen, L.; Yu, H. New insights into gibberellin signaling in regulating flowering in Arabidopsis. J. Integr. Plant Biol.; 2020; 62, pp. 118-131. [DOI: https://dx.doi.org/10.1111/jipb.12892]

135. Porri, A.; Torti, S.; Romera-Branchat, M.; Coupland, G. Spatially distinct regulatory roles for gibberellins in the promotion of flowering of Arabidopsis under long photoperiods. Development; 2012; 139, pp. 2198-2209. [DOI: https://dx.doi.org/10.1242/dev.077164]

136. Wilson, R.N.; Heckman, J.W.; Somerville, C.R. Gibberellin is required for flowering in Arabidopsis thaliana under short days. Plant Physiol.; 1992; 100, pp. 403-408. [DOI: https://dx.doi.org/10.1104/pp.100.1.403] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/16652976]

137. Miskolczi, P.; Singh, R.K.; Tylewicz, S.; Azeez, A.; Maurya, J.P.; Tarkowská, D.; Novák, O.; Jonsson, K.; Bhalerao, R.P. Long-range mobile signals mediate seasonal control of shoot growth. Proc. Natl. Acad. Sci. USA; 2019; 116, pp. 10852-10857. [DOI: https://dx.doi.org/10.1073/pnas.1902199116] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/31085653]

138. Salonia, F.; Ciacciulli, A.; Poles, L.; Pappalardo, H.D.; La Malfa, S.; Licciardello, C. New plant breeding techniques in citrus for the improvement of important agronomic traits. A Review. Front. Plant Sci.; 2020; 11, 1234. [DOI: https://dx.doi.org/10.3389/fpls.2020.01234] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/32922420]

139. Chu, L.-L.; Zheng, W.-X.; Liu, H.-Q.; Sheng, X.-X.; Wang, Q.-Y.; Wang, Y.; Hu, C.-G.; Zhang, J.-Z. ACC SYNTHASE4 inhibits gibberellin biosynthesis and FLOWERING LOCUS T expression during citrus flowering. Plant Physiol.; 2024; 195, pp. 479-501. [DOI: https://dx.doi.org/10.1093/plphys/kiae022]

140. Eriksson, S.; Böhlenius, H.; Moritz, T.; Nilsson, O. GA4 is the active gibberellin in the regulation of LEAFY transcription and Arabidopsis floral initiation. Plant Cell; 2006; 18, pp. 2172-2181. [DOI: https://dx.doi.org/10.1105/tpc.106.042317]

141. Zhang, S.; Gottschalk, C.; van Nocker, S. Genetic mechanisms in the repression of flowering by gibberellins in apple (Malus x domestica Borkh.). BMC Genom.; 2019; 20, pp. 1-15. [DOI: https://dx.doi.org/10.1186/s12864-019-6090-6]

142. Rebers, M.; Kaneta, T.; Kawaide, H.; Yamaguchi, S.; Yang, Y.Y.; Imai, R.; Sekimoto, H.; Kamiya, Y. Regulation of gibberellin biosynthesis genes during flower and early fruit development of tomato. Plant J.; 1999; 17, pp. 241-250. [DOI: https://dx.doi.org/10.1046/j.1365-313X.1999.00366.x]

143. Ariizumi, T.; Hauvermale, A.L.; Nelson, S.K.; Hanada, A.; Yamaguchi, S.; Steber, C.M. Lifting DELLA repression of Arabidopsis seed germination by nonproteolytic gibberellin signaling. Plant Physiol.; 2013; 162, pp. 2125-2139. [DOI: https://dx.doi.org/10.1104/pp.113.219451] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/23818171]

144. Sasaki, A.; Itoh, H.; Gomi, K.; Ueguchi-Tanaka, M.; Ishiyama, K.; Kobayashi, M.; Jeong, D.-H.; An, G.; Kitano, H.; Ashikari, M. Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science; 2003; 299, pp. 1896-1898. [DOI: https://dx.doi.org/10.1126/science.1081077]

145. Fukazawa, J.; Ohashi, Y.; Takahashi, R.; Nakai, K.; Takahashi, Y. DELLA degradation by gibberellin promotes flowering via GAF1-TPR-dependent repression of floral repressors in Arabidopsis. Plant Cell; 2021; 33, pp. 2258-2272. [DOI: https://dx.doi.org/10.1093/plcell/koab102]

146. Hauvermale, A.L.; Ariizumi, T.; Steber, C.M. Gibberellin signaling: A theme and variations on DELLA repression. Plant Physiol.; 2012; 160, pp. 83-92. [DOI: https://dx.doi.org/10.1104/pp.112.200956] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/22843665]

147. Thomas, S.G.; Blázquez, M.A.; Alabadí, D. Della proteins: Master regulators of gibberellin-responsive growth and development. Annual Plant Reviews, Volume 49: Gibberellins, The; John Wiley & Sons, Ltd.: Hoboken, NJ, USA, 2016; pp. 189-228.

148. Sun, T.-p.; Gubler, F. Molecular mechanism of gibberellin signaling in plants. Annu. Rev. Plant Biol.; 2004; 55, pp. 197-223. [DOI: https://dx.doi.org/10.1146/annurev.arplant.55.031903.141753] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/15377219]

149. Mutasa-Göttgens, E.; Hedden, P. Gibberellin as a factor in floral regulatory networks. J. Exp. Bot.; 2009; 60, pp. 1979-1989. [DOI: https://dx.doi.org/10.1093/jxb/erp040] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/19264752]

150. Fukazawa, J.; Teramura, H.; Murakoshi, S.; Nasuno, K.; Nishida, N.; Ito, T.; Yoshida, M.; Kamiya, Y.; Yamaguchi, S.; Takahashi, Y. DELLAs function as coactivators of GAI-ASSOCIATED FACTOR1 in regulation of gibberellin homeostasis and signaling in Arabidopsis. Plant Cell; 2014; 26, pp. 2920-2938. [DOI: https://dx.doi.org/10.1105/tpc.114.125690] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/25035403]

151. Jiang, Y.; Chen, J.; Zheng, X.; Tan, B.; Ye, X.; Wang, W.; Zhang, L.; Li, J.; Li, Z.; Cheng, J. Multiple indeterminate domain (IDD)–DELLA1 complexes participate in gibberellin feedback regulation in peach. Plant Mol. Biol.; 2022; 109, pp. 147-157. [DOI: https://dx.doi.org/10.1007/s11103-022-01263-y]

152. Senthil-Kumar, M.; Mysore, K.S. New dimensions for VIGS in plant functional genomics. Trends Plant Sci.; 2011; 16, pp. 656-665. [DOI: https://dx.doi.org/10.1016/j.tplants.2011.08.006]

153. Galipienso, L.; Navarro, L.; Ballester-Olmos, J.F.; Pina, J.A.; Moreno, P.; Guerri, J. Host range and symptomatology of a graft-transmissible pathogen causing bud union crease of citrus on trifoliate rootstocks. Plant Pathol.; 2000; 49, pp. 308-314. [DOI: https://dx.doi.org/10.1046/j.1365-3059.2000.00449.x]

154. Velázquez, K.; Agüero, J.; Vives, M.C.; Aleza, P.; Pina, J.A.; Moreno, P.; Navarro, L.; Guerri, J. Precocious flowering of juvenile citrus induced by a viral vector based on Citrus leaf blotch virus: A new tool for genetics and breeding. Plant Biotechnol. J.; 2016; 14, pp. 1976-1985. [DOI: https://dx.doi.org/10.1111/pbi.12555] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/26920394]

155. Maeda, K.; Kikuchi, T.; Kasajima, I.; Li, C.; Yamagishi, N.; Yamashita, H.; Yoshikawa, N. Virus-induced flowering by apple latent spherical virus vector: Effective use to accelerate breeding of grapevine. Viruses; 2020; 12, 70. [DOI: https://dx.doi.org/10.3390/v12010070] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/31936111]

156. Sasaki, S.; Yamagishi, N.; Yoshikawa, N. Efficient virus-induced gene silencing in apple, pear and Japanese pear using Apple latent spherical virus vectors. Plant Methods; 2011; 7, 70. [DOI: https://dx.doi.org/10.1186/1746-4811-7-15] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/21658286]

157. Szankowski, I.; Waidmann, S.; El-Din Saad Omar, A.; Flachowsky, H.; Hättasch, C.; Hanke, M.-V. RNAi-silencing of MdTFL1 induces early flowering in apple. Proceedings of the I International Symposium on Biotechnology of Fruit Species: Biotechfruit; Dresden, Germany, 1–5 September 2008; Volume 839, pp. 633-636.

158. Sritongchuay, T.; Wayo, K.; Orr, M.C.; Hughes, A.C. Insufficient native pollinators during artificially induced early flowering decrease yield and long-term economic viability of a tropical fruit crop. J. Appl. Ecol.; 2021; 58, pp. 80-91. [DOI: https://dx.doi.org/10.1111/1365-2664.13787]

159. Khan, F.S.; Goher, F.; Zhang, D.; Shi, P.; Li, Z.; Htwe, Y.M.; Wang, Y. Is CRISPR/Cas9 a way forward to fast-track genetic improvement in commercial palms? Prospects and limits. Front. Plant Sci.; 2022; 13, 1042828. [DOI: https://dx.doi.org/10.3389/fpls.2022.1042828] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/36578341]

160. Herath, D.; Voogd, C.; Mayo-Smith, M.; Yang, B.; Allan, A.C.; Putterill, J.; Varkonyi-Gasic, E. CRISPR-Cas9-mediated mutagenesis of kiwifruit BFT genes results in an evergrowing but not early flowering phenotype. Plant Biotechnol. J.; 2022; 20, pp. 2064-2076. [DOI: https://dx.doi.org/10.1111/pbi.13888]

161. Shang, L.; Tao, J.; Song, J.; Wang, Y.; Zhang, X.; Ge, P.; Li, F.; Dong, H.; Gai, W.; Grierson, D. CRISPR/Cas9-mediated mutations of FANTASTIC FOUR gene family for creating early flowering mutants in tomato. Plant Biotechnol. J.; 2024; 22, pp. 774-784. [DOI: https://dx.doi.org/10.1111/pbi.14223] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/37942846]