After discovering photoperiodic floral induction [1], many physiological studies have been carried on with the flowering transition. The physiological analysis and dissection of floral induction were made by introducing an experimental system based on the understanding that an external controllable stimulus can cause flowering when applied to a specific plant. The subsequent studies considered that higher plants share two essential features of floral transition: Generation of floral stimulus in leaves and its transport to the target, shoot apical meristem (SAM), which must be competent to receive it [2]. SAM’s phase conversion to the reproductive stage is demonstrated by morphological changes accompanied by an alteration in gene expression [3]. The SAM occurs in two states, the incompetent state, unable to perceive signals of floral induction, and the competent state, capable of interpreting signals and leading to flowering transition. Thus, the SAM needs to pass the developmental checkpoint between incompetent and competent states. This transition leads to alteration in gene expression and organ production. Overcoming such checkpoints enables SAM to transform into floral meristem to produce flowers, and this transformation is induced by intrinsic and extrinsic stimuli that generate floral signals. Upon elimination of PNY (PENNYWISE) and PNF (POUNDFOOLISH) function in Arabidopsis, SAM remained in a vegetative state as it could not perceive the inductive signals, which suggested the connection between meristem architecture and their response potential to floral stimuli [3]. microRNAs such as miR156 and miR172 and their corresponding targets are the key regulators of the phase changes in the floral transition [4].

2. FLORAL INDUCTION THROUGH SEVERAL PATHWAYS

Floral inductive signals induce the transformation of SAM into a floral meristem, and plants’ flowering time could be affected by growing them in varying day lengths such as shortening day length by shading or increasing the day length by incandescent light bulbs [5]. Garner and Allard [1] put forward the concept of photoperiodism after examining a short day (SD) period requiring tobacco mutant. Other SD variety Maryland Mammoth was obtained from generally day-neutral (DN) tobacco (plants flowering at their own particular time irrespective of day length). In their night break studies (utilizing brief light exposure for interruption of extended night period), they established that duration of night controls SD plant’s floral induction and not the day’s length. Knott [6] demonstrated by restricting spinach leaves and SAM to lighting and shading that leaves are the organs where inductive signals originate. Chailakhyan [7] revealed that in Perilla frutescens and Chrysanthemum, grafting of induced leaves (donor) on recipient non-induced plants results in the recipient’s early flowering. Hence, florigen theory was given by Chailakhyan, in which it was supposed that florigen formed in leaves represents a floral signal that when sent to SAM induces flowering. Both the quantity (length of light exposure) and the quality of light are essential signals for flowering, and plants possess specific receptors that perceive light exposure duration and differentiate between different wavelengths of light. Flowering is also affected by temperature, and certain wheat and rye varieties need to overwinter for flower induction. Gassner [8] showed that in winter variety flowering is accelerated if, during germination in pots, it is exposed to cold temperatures and subsequently transferred to the soil under normal temperatures. Lysenko [9] coined the vernalization term and found that increases in day length must follow cold temperature exposure. There are different developmental checkpoints that a plant must pass to flower. The intrinsic signals communicating growth status such as nutrient flow, hormones, and plant size, influence the floral induction. The studies evidence an endogenous floral inductive pathway’s existence wherein a plant variety flowers only after producing leaves of a predictable number [10].

2.1. Photoperiodic Control of Floral Induction

The plants co-ordinate their flowering by utilizing a reliable indicator of environmental changes, “changes in day length,” that can foretell the environmental changes like the cold period’s arrival, allowing plants to adjust for flowering time. Flowering in SD plants occurs upon day length shortening, whereas, in long-day plants (LD), flowering occurs with the increase in day length, and in DN (day-neutral) plants flowering occurs irrespective of day length variations [2]. The plants are categorized further as obligate and facultative within the day length responses. Absolute inductive photoperiods are mandatory for obligate plants and such plants remain in a vegetative state without such requirement. In contrast, facultative plants show accelerated flowering under inductive conditions and undergo normal flowering even in noninductive photoperiod. It is now achievable to identify the loci and genes functioning in inductive day length determination by comparing the plant species and different varieties with dissimilar day length requirements for floral induction. Genomic loci functioning in flowering, or QTL (quantitative trait loci) in species such as rice and maize, are known and through dissection and QTL, rice flowering time genes have been identified and isolated [11]. OsCOL10, a CONSTANS-like gene, has been found to repress flowering by decreasing RFT1 and Hd3a (FT-like genes) expression through Ehd1. OsCOL10 works downstream of vital LD specific repressor, Ghd7, through the decrease of Ehd1 expression [12].

2.1.1. Photoreceptors: The light signal transducers

Phytochromes and cryptochromes, two essential types of photoreceptors in higher plants, play important role in flower induction. Phytochromes perceive far-red and red light, whereas cryptochromes perceive UVA and blue light. The day length response in Arabidopsis involves phytochrome A (PHYA) and B (PHYB) and cryptochrome 1(CRY1) and 2 (CRY2) [13]. In Arabidopsis, blue light and far-red promote flowering, whereas red light confers inhibition. The photo-receptors interact with their corresponding interacting proteins within a complex network to transduce the light signals. Phytochromes and cryptochromes employ a mechanism that encompasses entrainment of the circadian rhythm to communicate the photoperiodic activity. The flowering time is also affected by additional inputs from temperature changes, light quality, and quantity through the endogenous clock [14]. An additional role is supposed for light in terms of its quality perceived by plants [15]. A critical component of a possible “light quality pathway” PFT1 (PHYTOCHROME AND FLOWERING TIME 1) gene in Arabidopsis [16], acts in disease resistance, suggesting of crosstalk between various environmental factors that affect plant development [17].

2.1.2. Self-reinforcing endogenous clock/the circadian clock

Plants use a predictable mechanism that utilizes day length variation for detecting seasonal changes. The endogenous clock compares light cycle and detects day length variations through its entrainment leading to periodicity setting. An endogenous mechanism called “circadian rhythm” can sense the light-dark cycle and result in self-reinforced gene expression in rhythmic patterns [18]. Arabidopsis clock design acts as a reference clock for other plants [19]. In plants responding to day length, the endogenous rhythm changes through the periodicity changes of the light/dark cycles lead to the flowering induction through the photoperiodic pathway. In a simple negative auto-regulatory feedback loop, translation of the clock gene and subsequent accumulation of protein in the nucleus inhibits its further transcription, and inhibition is relieved when both mRNA and proteins degrade, resulting in the renewal of the cycle. Three transcription factors (TFs) that interact to form such negative autoregulatory feedback loop in Arabidopsis are CCA1 (CIRCADIAN CLOCK ASSOCIATED1), TOC1 (TIMING OF CAB EXPRESSION1), and LHY (LATE ELONGATED HYPOCOTYL) [20,21]. CCA1 upregulates FEROINA (FER), a receptor kinase, which leads to alternative splicing and accumulation of some necessary flowering transition genes transcripts [22]. TOC1 inhibition by CCA1 and LHY, moreover, encompasses a co-repressor complex including, CONSTITUTIVE PHOTOMORPHOGENIC-10 (COP10), DEETIOLATED1, and DDB1 [23]. TOC1 is from a 5-member family of ARABIDOPSIS PSEUDO-RESPONSE REGULATORS (APRR) regulated through circadian rhythms. The circadian clock (CC) working alters downstream gene expression that coincides with favorable photoperiodic conditions for flowering. FAR-RED IMPAIRED RESPONSE1 (FAR1), FAR-RED ELONGATED HYPOCOTYL3 (FHY3), and HY5 activate ELF4 during the day, while ELF4 is repressed at dawn by CCA1 and LHY through direct interaction with these activators [24]. An increasing number of reciprocal interactions suggest an intricate web of connections operate the clock [25].

2.1.3. Photoperiodic induction integration through vital genes

In Arabidopsis, CONSTANS (CO) [Table 1], a critical gene encoding a zinc finger protein functioning as TF and controlling floral inductive pathway, is regulated through circadian rhythm [26]. CO regulates flowering positively in LDs and negatively in SDs [27]. Cloning of CO was done through a map-based approach [26]. The co-mutant flowers at a normal time in short days but late during long days, whereas overexpressing of CO imparts the plant’s insensitivity to day length variation and results in early flowering [28]. The CC regulates CO expression on a 24-h cycle with its maximum at night. Hence, during short days, there is no overlapping of CO expression with the period of daylight, but in longer days, overlapping of CO expression and daylight in the evening occurs.

Table 1: Candidate genes play their roles in different pathways of floral induction.

Pathway of floral induction	Candidate genes
Photoperiodic pathway	CONSTANS (CO) [26], GIGANTEA (GI), FLAVIN-BINDING, KELCH REPEAT (FKF1) [29], CONSTANS LIKE 4 (COL4) [36], PSEUDO RESPONSE REGULATORS (PRR1, 5, 7, and 9) [35], CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1) [32], CRYPTOCHROME CIRCADIAN REGULATOR 1& 2 (CRY1 & CRY2) [33], PHYTOCHROME A (PHYA) [34], FLOWERING LOCUS T (FT) [32], PICKLE (PKL) [45], HOMOLOG OF TRITHORAX1 (ATX1) [45], FT-INTERACTIVE PROTEIN 1 (FTIP1) [47], SYNTAXIN OF PLANTS 121 (SYP121) [47], QUIRKY (QKY) [47], SODIUM POTASSIUM ROOT DEFECTIVE 1 (NaKR1) [43], FLOWERING LOCUS D (FLD) [59], TERMINAL FLOWER 1 (TFL1) [49], Transcriptional factors TCP17, TCP13, TCP5, SQUAMOSA PROMOTER-BINDING-LIKE PROTEIN 3 (SPL3), SPL4, and SPL5 [50], APETALA 1 (AP1) [129].
Autonomous pathway	FLOWER ING LOCUS C (FLC) [60], LUMINIDEPENDENS (LD), SUF4 (SUPPRESSOR OF FRIGIDA) [61], FLOWERING LOCUS CA (FCA) [55], FLOWERING LOCUS Y (FY) [55], FLOWERING LOCUS D (FLD) [59], PCF11P-SIMILAR PROTEIN 4 (PCSS4) [60], FLOWERING LOCUS VE (FVE), HISTONE DEACETYLASE 5 (HDA5), HISTONE DEACETYLASE 6 (HDA6), RELATIVE OF EARLY FLOWERING 6 (REF6), EARLY IN SHORT DAYS 4 (ESD4), and DBP1 (DNA-BINDING PROTEIN PHOSPHATASE 1) [61, 62].
Vernalization pathway	FLOWER ING LOCUS C (FLC) [60], VERNALIZATION 1 and 2 (VRN1 and 2) [77], VERNALIZATION INSENSITIVE 3 (VIN3) [69], VERNALIZATION 5 (VRN5) [79], LIKE HETERO-CHROMATIN PROTEIN 1 (LHP1), VP1/ABI3-LIKE 1 (VAL1) and VAL2 [79,80].
Gibberellin promotion pathway	AtMYB33 [88], Repressor of ga1-3 (RGA), GIBBERELLIC ACID INSENSITIVE (GAI) [90], JASMONATE-ZIM (JAZ1) [96], GA3-oxidase2 (GA3ox2), GA30x1 [102], TEM1 (TEMPRANILLO 1) and TEM2, SHORT VEGETATIVE PHASE (SVP) [103].

Light stabilizes CO expression, whereas during night CO protein is degraded through the proteasome, suggesting that the CC controls temporal CO expression. CDF (CYCLING DOF FACTOR) represses CO in the morning, whereas CDF2 and CDF1 are regulated through proteolytic degradation by a light-requiring complex of the clock proteins, GI (GIGANTEA), and FKF1 (FLAVIN-BINDING, KELCH REPEAT) [Table 1] [29]. FKF1 binds GI and targets CO’s suppressors, resulting in CO expression [30]. GI’s ability to bind CO promoter is restricted during the night as ELF4 regulates its entry to chromatin by sequestration into subnuclear bodies [31]. FKF1 activates CO and FT (FLOWERING LOCUS T) expression upon light activation and through COP1 homodimerization inhibition [Table 1] [32]. CRY2 and CRY1 inhibit COP1-SPA1 (COP1-SUPPRESSOR OF PHYTOCHROME A-105) complex by sequestering SPA1 and result in CO protein stabilization [Table 1] [33]. Phytochrome A (phyA) disrupts COP1-SPA1complex upon far-red activation in the afternoon, while in the morning, phytochrome B (phyB) mediates the CO protein degradation [34]. PSEUDO-RESPONSE REGULATORS (PRR 1, 5, 7, and 9) stabilize the CO product in the late afternoon through repression of CDF1 [35]. Another floral repressor, COL4 (CONSTANS LIKE 4), co-localizing with CO in the nucleus, acts antagonistically to CO and provides another floral regulation level [36] [Figure 1].

Figure 1: Mechanisms of floral induction and integration of different pathways. [Click here to view]

Two regions, a zinc-finger motif and a CCT region of CO protein, are vital for its proper functioning. CCT region found in TOC1, CO, and CO-LIKE genes help in the nuclear localization of these proteins [37]. FKBP12 in Arabidopsis interacts with CCT domain of CO affecting its stability and hence function [38]. Although expressed in several cell types, CO expression specific to companion cells confers timely flowering, and that if expressed only in SAM, early flowering does not occur [39]. Confinement of CO expression to small veins’ companion cells using galactinol synthase promoter results in timely flowering under noninductive SDs. Flowering was also accelerated in co-mutant receptor plants when the leaves expressing minor vein CO were grafted to them [40]. Thus, CO is supposed to mediate the floral stimulus generated through photoperiod in leaves and transporting it to SAM by the phloem. CO and FT expression is promoted by PFT1/MED25 (a subunit of mediator complex, which bridges RNA polymerase II and transcriptional factors) in a CO-independent manner [41]. The function of PFT1 is governed by photoperiod and length of short tandem repeat region that encodes 90 amino acid regions rich in glutamine [42].

FT protein is a direct downstream target of CO, and genetic screen of CO overexpressing lines led to the isolation of ft mutants that flower late. As FT represses the overexpression phenotype, its position can be suggested as down-stream of CO and specifies that an alternative target gene exists, acting parallel to CO. In LDs, the CO protein peaks in the late afternoon bind to the FT promoter and interact with the NF-Y–FE complex resulting in FT transcriptional activation [43]. VAL1 (VIVIPAROUS1/ABSCISIC ACID INSENSITIVE3-LIKE1) binds to FT and arranges polycomb repressive complex 2 (PRC 2) components to silence the FT epigenetically at night and before dusk [44]. The PRC2 silencing of FT is prevented by the interaction of PICKLE (PKL) with CO and ATX1 (HOMOLOG OF TRITHORAX1) [Table 1] [45]. Multiple enhancers affecting the flowering time seem to regulate FT in inductive conditions, and one such enhancer was identified recently [46]. FT-INTERACTIVE PROTEIN 1 (FTIP1), ER membrane protein, facilitates export of FT to sieve elements and FT movement through companion cell plasmalemma is regulated by the interaction of SYP121 (SYNTAXIN OF PLANTS 121) with QKY/MCTP15 (QUIRKY) [Table 1] [47]. From leaves, FT transport to SAM is facilitated by NaKR1 (SODIUM POTASSIUM ROOT DEFECTIVE 1) after its activation through interaction with FE and CO [43]. At SAM, FT complexes with FD (B-zip TF), regulating the expression of downstream targets like AP1 (APETALA 1) [48]. TFL1 (TERMINAL FLOWER 1), a floral repressor, remains bound to FD in an elaborate (FD-TFL1 complex), maintaining the FD in an inactive state at SAM, and activation of FD into a florigen activation complex (FAC) occurs through its phosphorylation catalyzed by CDPK6 (CALCIUM DEPENDENT PROTEIN KINASE 6) and CDPK33 [49] [Figure 1]. TFs, TCP17, TCP13, TCP5, SPL3, SPL4, and SPL5 interact with FD and facilitate its DNA binding and activating AP1 expression [Table 1] [50].

The homologs for CO and FT occur in both dicot and monocot species, suggesting their role in flower transition in other plants. The CO complemented the loss of co-function in Arabidopsis mutants from Pharbitis nil and Brassica napus [51]. The QTL related to flowering time mutants in rice, called Heading date, encodes CO and FT genes. Heading Date 1 (Hd1), CO homolog, affects the early transition and inhibition of flowering in inductive SD conditions and LD conditions, respectively. Hd1 displays a diurnal expression pattern with highest levels at night and dawn under LD conditions, coinciding with the CC expression pattern [52]. The hd1 mutants, exhibiting late-flowering phenotype, show lower expression levels of an essential flower timing gene Heading date 3a (Hd3a), which share high sequence to FT gene [53], and hd3a mutants show late flowering under SD conditions than wild-type plants. Thus, in rice, the CO/FT interaction seems to be preserved, though SD, not the LD, induces flowering in rice. Hd1 inhibits Hd3a expression under LD and induces it under SD when the Hd3a expression reaches highest during the day and with no expression under LD treatments [52]. As the CC regulates the family of CO-like genes in both dicots and monocots, the photoperiodic inductive mechanism can be said to be evolutionarily conserved. Even though CO and FT are conserved in numerous species, other self-determining parallel mechanisms regulate photoperiodic floral induction.

3. AUTONOMOUS PATHWAY

Most plants’ flowering occurs without extrinsic inductive signals and plants that exhibit obligate requirements of such extrinsic signals are infrequent. Thus, additional intrinsic factors are supposed to provide signals for floral induction. Such constitutive or autonomous signals are derivative of the plant’s physiological outputs that determine the readiness to flower such as plant age, size, or the number of leaves. These endogenous signals are possibly related directly to the number of plant accumulated resources [54]. Several mutants in Arabidopsis flower late irrespective of noninductive and inductive photoperiods and represent the autonomous pathway, different from the photoperiodic pathway. However, many such mutant genes react to the vernalization pathway elements, suggesting the intersection of these two pathways at specific points. The general assumption about the autonomous signal is that it consists of nutrient combinations and phytohormones such as cytokinins or gibberellins, which move to SAM from leaves to induce flowering [54]. Other factors that can be part of the signal might be RNA and proteins in phloem sap. However, the precise nature of these components is yet to be revealed. Nevertheless, genes involved in the autonomous pathway encode factors that maintain the epigenetic state and RNA processing of critical genes [55]. FLOWER ING LOCUS C (FLC) gene in Arabidopsis is a shared component of vernalization and autonomous pathways that act as an essential node for signal integration and offers a valuable model to understand floral inductive signals’ molecular nature [Table 1].

4. VERNALIZATION PATHWAY

Exposure to temperature, especially low temperature (vernalization), helps regulate the plants’ onset of flowering. Vernalization thus is regarded as a checkpoint mandatory to be crossed by several plants to undergo flowering [69]. The SAM perceives the signal of vernalization and floral induction in several plants depends on the subsequent photoperiodic response after their prolonged exposure to cold temperature, avoiding precocious flowering because of a short warm spell before the arrival of cold conditions. Vernalization includes two separate processes, perception of a prolonged spell of cold temperature and “remembering” that perception to induce flowering later in the spring or summer. The vernalization represents the somatically heritable condition, induced by prolonged cold exposure that the descendant cells retain from vernalization-induced SAM cells [70].

5. GIBBERELLIN PROMOTION PATHWAY

In Arabidopsis, gibberellic acid (GA) affects the flowering time is well known. The GA application results in premature flowering in LD and SD and bypasses several mutants’ late-flowering phenotype from the rest three pathways [82]. Environmental and developmental signals regulate the GA’s biosynthesis and signal transduction; besides, GA, turnover, and concentration are most important [83]. GA promotes flowering through FT activation in leaves, and ga1-3 (GA-deficient) mutant plants show reduced FT expression while exogenous GA application to such plants increases the FT expression [84,85].

The signal generation by GA1, GA pathway’s early step, produces copalyl pyrophosphate from geranylgeranyl pyrophosphate, but the signal that induces GA1 is unknown. GA’s role in floral induction is established by the GA biosynthesis deficient mutants, which cannot flower in SDs because of active GA absence [86]. Mutational scrutiny of genes involved in the GA pathway shows that it is not the GA itself but the generation of the signal that leads to floral induction. The molecular targets for GA first defined in barley defined GAMYB gene as critical for GA signal transduction. The effects of GA application get mimicked by over-expression of GAMYB [87]. GAMYB binds to GARE (GA-response element), distinct DNA sequences within promoters of genes upregulated by GA. Three genes in Arabidopsis exhibiting similarity to barley GAMYB have been found, and among these, AtMYB33 shows the highest resemblance. AtMYB33 acts in Arabidopsis flowering through binding to the GARE sequence upstream of LEAFY [Table 1]. For regulating floral induction, AtMYB33 is presumed to act along with additional LFY inducers like SOC1 [88] [Figure 1].

Two floral transition repressors, RGA (Repressor of ga1-3) and GIBBERELLIC ACID INSENSITIVE (GAI), both of which are DELLA class proteins, are affected by GA [89]. DELLA proteins possess a DELLA domain at N-terminal, which is presumed to act as the target for GA-directed ubiquitination subsequently proteasome-facilitated destruction. The finding evidences the importance of RGA and GAI in inhibiting the flowering that GAI represses SOC1 expression, but no such direct effect of GAI on LFY is found [90]. GAI and RGA suppress the microRNA miR159, a 21-bp sequence with substantial identity to the AtMYB genes [91]. miR159 overexpression leads to decreased AtMYB33 levels in leaves resulting in a significant delay in flowering. The lower AtMYB33 levels are possibly due to miRNA-facilitated destruction. miR159 levels seem to vary with variations in the GA signaling pathway and in response to auxin and ethylene that affect DELLA protein levels [90]. AtMYB33, having a putative GARE motif, regulates miR159 positively, proposing overexpression prevention through a negative feedback loop resulting in early flowering. SOC1 repression in Arabidopsis is supposed to be overcome by GA-facilitated DELLA proteins ubiquitination, and proteasome-mediated protein degradation [90]. Floral repression is alleviated, and LFY expression is induced by promoting SOC1 and AtMYB33 when the GAI and RGA are degraded. DELLA proteins interact with CO, disrupting its function, and preventing it from binding FT promoter and downregulate it [92]. DELLA proteins can also suppress flowering by inhibiting CO to interact with NF-Y and interact with PIF4 preventing its binding to the FT promoter [93]. DELLA proteins show interaction with FT suppressors such as MYC3, a bHLH TF, and suppressing FT expression. Under SD conditions, lower GA levels promote a higher level of DELLAs and MYC3, showing enhanced expression, stabilized by DELLAs out-compete CO, thereby repressing FT expression and eventually prevent precocious flowering [94]. DELLAs can interact with FLC, promoting downstream genes, including FT [95]. FT expression is also mediated in both SDs and LDs through MYC function modulation by DELLAs, involving JA signaling. The competition between MYC2 and DELLAs to bind JAZ1 (JASMONATE-ZIM) protein determines the JA-mediated gene expression [Table 1] [96]. DELLAs bind to JAZ1 and free MYC at low GA levels promoting JA-mediated gene expression, whereas DELLAs get degraded at high GA levels, and the MYC2-JAZ1 complex formed represses the JA-mediated genes. As JA represses the flowering, such repression occurs through MYC2 binding directly to FT promoter in LDs and pointing toward the existence of DELLA-MYC2-JAZ1 module for floral induction [97] [Figure 1].

DELLA proteins antagonize a universal GA response promoter, PKL, and compromise the SPL gene activation at the transcriptional level, whereas post-translationally, DELLA proteins inhibit SPL transactivation activity through binding them [98,99]. Furthermore, DELLAs and SPLs function antagonistically on common gene targets such as FUL and SOC1 [99]. WRKY TFs, containing WRKY domains of 60–70 amino acids, also are involved in GA mediated floral induction such as WRKY 12 and 13 interact with RGL1 and GAI modulating the transcriptional activity of WRKYs [100]. In SDs, WRKY 12 and 13, though both are expressed in SAM, WRK12 promotes FUL expression while WRK13 represses it, thereby exhibiting the opposite role in floral regulation [Figure 1]. Likewise, WRKY75 is also inhibited by its interaction with DELLAs such as GAI, RGA, and RGL1, thereby not allowing FT expression [101].

GA biosynthesis regulated spatially and temporally also mediates the floral induction. GA biosynthesis genes show spatial regulation, as is evidenced by the leaf vasculature localized accumulation of GA3ox2 (GA3-oxidase2), which catalyzes GA precursor conversion into bioactive GAs [102]. TEM1 (TEMPRANILLO 1) and TEM2, TFs that repress FT, suppress GA3ox2 and GA30x1, contributing to the diurnal GA3ox1 expression pattern in SDs [103]. The increased level of GA20ox2 (GA20-oxidase2) in the SAM under LD conditions is partly attributed to the downregulation of SVP (SHORT VEGETATIVE PHASE), floral repressor [104]. Along with FLC, SVP also regulates other GA metabolic genes like GA2ox8, and SVP/FLC complex regulates GA3ox1 indirectly by promoting TEM2 and suppression of TEM1 [105] [Figure 1]. The conserved regulatory pathway functions for different developmental purposes as microRNA regulation, and the GA-facilitated DELLA protein destruction and pathway of DELLA protein repression have been found in other plants and other developmental pathways.

6. MEANS OF FLORAL TRANSITION INTEGRATION AND INSTIGATION

Notwithstanding the signal’s origin, floral induction’s ultimate purpose is SAM’s transformation to the reproductive state [106]. There occurs convergence of pathways of flowering time in particular genes called flowering-time integrators. In Arabidopsis, many floral pathways that perceive different developmental and environmental stimuli converge to some integrators of flowering such as FT, AGL24 (AGAMOUS-LIKE 24), and SOC1 (SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1) [107] that are activated through downregulation of FLC as in the autonomous and vernalization pathways, through CC-regulated CONSTANS (CO) expression as in photoperiodic pathway or directly as in gibberellin promotion pathway. PhyB interacting proteins, VASCULAR ONE ZINC FINGER 1 and 2 (VOZ1 and 2), function in the photoperiodic and vernalization pathways, as double mutants voz1 voz2 flower late and show increased FLC expression without vernalization, whereas vernalization exposure reverses such phenotype [108].

ICE1 (INDUCER OF CBF EXPRESSION1) integrates the vernalization and photoperiod pathways through SOC1 and FLC regulation. Under cold temperature, ICE1 binds FLC promoter and leads to delayed flowering, whereas inductive LDs lead to SOC1 activation, which prevents FLC activation through ICE1 [109]. LFY positively regulates AP1, and flower commitment is determined through AP1-LFY positive feedback interaction [Figure 1]. Thus, all pathways intersect at the activity of a subset of flowering-time integrator genes, either directly or through FLC. At a given time, flowering-time genes face some degree of inhibition due to FLC activity and some degree of activation due to CO activity and gibberellin-induced signals. Flowering-time integrators will express, and the floral transition will occur only when activation signals are more robust than FLC-based inhibition.

7. CONCLUSION AND FUTURE PERSPECTIVES

Much research has been done to know the underlying mechanism of floral induction in different flowering plants. First, the focus was laid on the physiological experiments to understand the significant cues which lead to the floral induction, and then attention was shifted to the molecular approaches to know the key genetic players involved and their possible role in this process. External stimuli are essential for the plants to undergo flowering, but in most plants, flowering can occur in the absence of such stimuli, suggesting intrinsic factors to plant growth provide the floral induction signals. Multiple complex pathways regulate floral induction. Many key genetic players have been discovered to be either specific to a floral induction pathway or are playing their role in other floral induction pathways, suggesting the possible intersection of different floral induction pathways. The regulation of these pathways occurs at the genetic as well as the protein level. microRNAs (microRNAs) regulate the specific genes acting in floral induction both at transcriptional and post-transcriptional levels. The pathways mediating floral induction has several nodes that signify the site of signal transduction, and the pathways are integrated that result in a co-ordinated initiation of flowering. Despite much research going on, the full mechanism operative in floral induction is not yet apparent. Not much is known about how the known floral regulators integrate into the flowering gene network and their target genes and activity mechanisms. Furthermore, how the collective action of TFs, epigenetic regulators, hormones, and small RNAs controls the floral induction needs to be fully unraveled. Future research can target such aspects by employing novel molecular approaches such as proteomics, genomics, transcriptomics, and targeted genome engineering approaches like CRISPR/CAS system to establish and perfect floral induction molecular mechanisms.

8. AUTHORS’ CONTRIBUTIONS

Authors Latif Ahmad Peer, Mohd Yaqub Bhat, and Bilal Ahmad Mir contributed to the conception of the study, preparation and design of this review article. The literature survey was done by the author Latif Ahmad Peer. Latif Ahmad Peer wrote the first draft of the manuscript and all authors made their comments on it. All authors read, revised, and approved the final manuscript.

9. CONFLICTS OF INTEREST

The authors declare no conflict of interest

10. FUNDING

There is no funding to report.

11. ETHICAL APPROVALS

This study does not involve experiments on animals or human subjects.

12. PUBLISHER’S NOTE

This journal remains neutral with regard to jurisdictional claims in published institutional affiliation.

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