Regulatory frameworks involved in the floral induction, formation and developmental programming of woody horticultural plants: a case study on blueberries

Abstract

Flowering represents a crucial stage in the life cycles of plants. Ensuring strong and consistent flowering is vital for maintaining crop production amidst the challenges presented by climate change. In this review, we summarized key recent efforts aimed at unraveling the complexities of plant flowering through genetic, genomic, physiological, and biochemical studies in woody species, with a special focus on the genetic control of floral initiation and activation in woody horticultural species. Key topics covered in the review include major flowering pathway genes in deciduous woody plants, regulation of the phase transition from juvenile to adult stage, the roles of CONSTANS (CO) and CO-like gene and FLOWERING LOCUS T genes in flower induction, the floral regulatory role of GA-DELLA pathway, and the multifunctional roles of MADS-box genes in flowering and dormancy release triggered by chilling. Based on our own research work in blueberries, we highlighted the central roles played by two key flowering pathway genes, FLOWERING LOCUS T and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1, which regulate floral initiation and activation (dormancy release), respectively. Collectively, our survey shows both the conserved and diverse aspects of the flowering pathway in annual and woody plants, providing insights into the potential molecular mechanisms governing woody plants. This paves the way for enhancing the resilience and productivity of fruit-bearing crops in the face of changing climatic conditions, all through the perspective of genetic interventions.

1 Introduction

Flowering represents a vital phase in the reproductive developmental of plants, ultimately resulting in the generation of seeds for subsequent generations. In agriculture, a robust flowering process, encompassing floral induction, formation, and developmental programming, stands as a fundamental prerequisite for achieving productive crop cultivation. The persistent trend of global warming, coupled with burgeoning populations and the depletion of natural resources, has presented significant challenges to agricultural production. For staple crops, warming can curtail agricultural output by shifting optimal growth zones and/or diminishing both cropping frequency and yields (Zhu et al., 2022). In the case of woody fruit crops, particularly temperate fruit trees, the impacts of global warming are profound, exerting adverse effects on floral development, dormancy release, and fruit growth (Luedeling et al., 2011). A pertinent instance is the scenario wherein insufficient chilling, triggered by climatic shifts, precipitates decreased bud break and reduced flower quality, leading to a reduction in fruit production (Atkinson et al., 2013).

Annual plants have evolved to respond to seasonal variations, facilitating a seamless transition from vegetative to reproductive phases. Extensive investigations using the model plant Arabidopsis (Arabidopsis thaliana) and cereal crops have yielded a wealth of valuable insights. These studies have unveiled pivotal regulatory nodes governing floral initiation and flowering time, encompassing pathways tied to aging, photoperiod, autonomous/vernalization, and gibberellin stimuli (see reviews by Greenup et al., 2009; Fornara et al., 2010; Andres and Coupland, 2012; Conti, 2017; Kinoshita and Richter, 2020; Izawa, 2021; Liu et al., 2021). At the center of this regulatory matrix stand two major integrators: FLOWERING LOCUS T (FT) and SUPPRESSOR OF OVEREXPRESSION OF CONSTAN 1 (SOC1). FT exerts a positive influence on SOC1, with this FT-to-SOC1 module occupying a central role in plant flowering, exhibiting evolutionary conservation across diverse plant species (Fornara et al., 2010; Lee and Lee, 2010). In Arabidopsis, FT emerges as a direct downstream target of both CONSTANS (CO) within the photoperiod pathway and FLOWERING LOCUS C (FLC) in the vernalization/autonomous pathway. SOC1, on the other hand, is under the direct sway of SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) in the aging pathway, alongside FLC and DELLA proteins within the gibberellin pathway (Wang et al., 2009; Preston and Hileman, 2013; Bao et al., 2020).

The elucidation of the intricate gene networks underpinning each flowering pathway in Arabidopsis has laid a foundational framework, setting the stage for analogous insights into the flowering mechanisms of other plants. In this review, our attention is directed towards the intricacies of flowering mechanisms in woody plants, with a particular focus on fruit-bearing crops. We provide a concise summary of recent advancements and present a gene network that explains possible flowering mechanism in woody plants, specifically focusing on deciduous temperate fruit crops. Within this framework, we underscore the role of FT in floral induction and SOC1’s involvement in floral programming. This gene-centric network not only deepens our understanding of flowering mechanisms in woody plants but also serves as a valuable knowledge resource for orchard management for fruit growers.

2 Major flowering pathway genes in deciduous woody plants

The process of flowering in deciduous woody plants is a product of intricate genetic and environmental influences and their interactions in responding to the seasonal changes (Figure 1). The phases of flowering, fruiting, and vegetative growth predominantly unfold mainly during spring and summer, coinciding with the prevalence of elevated average temperatures. Meanwhile new floral buds for many deciduous woody plants are initiated in the summer period and continuously undergo development through fall. In contrast, winter mark the completion of reproductive growth, onset of growth cessation, and the establishment of dormancy in general. During this period, declining temperatures and shortening day period act as key environmental signals to trigger and drive these biological events. It is generally within these colder months that the development of flower buds occurs and the initiation of endodormancy is likely signaled.

Figure 1

A pivotal facet that distinguishes deciduous woody plants from the vernalization/autonomous pathway observed in Arabidopsis lies in the flowering mechanism driven by chilling accumulation, termed chilling requirement (CR). This accumulation of chilling hours occurs before the eventual release of endodormancy, as temperatures start to rise in spring. This CR-mediated process imparts a unique rhythm to the flowering behavior of deciduous woody plants, in contrast to the continuous floral initiation and flowering progression exhibited by vernalized Arabidopsis plants. Deciduous woody plants often have two distinct phases emerge: the initiation of floral buds mostly during the autumn and early winter, followed by the actual blossoming of these buds in spring subsequent to CR fulfillment (Figure 1).

Flower regulation in deciduous fruit trees is distinct from annuals. In annuals, flower initiation begins with the transition from vegetative to inflorescence stage and flower formation and development are typically completed within a single season (see reviews by Baurle and Dean, 2006; Irish, 2010). On the other hand, flowers from seedling-derived fruit trees can only be initiated and developed after the tree reaches adulthood, which can take several years. Even in adult trees, flower initiation and development occur over two growing seasons, not one (Wilkie et al., 2008; Sun et al., 2022). For example, floral bud initiation in apple and peach trees occurs in summer and basic morphological structures such as sepal, petal, stamen, and carpel are developed during the fall before entering a fully dormant state, remaining in a “resting” state during winter and then resumed developmental pace before flowering next spring. Winter chilling is indispensable for driving dormancy out (Arora et al., 2003). It was also found that chilling is essential for driving morphological differentiation within buds during winter (Luna et al., 1990; Luna et al., 1991; Luna et al., 1993; Reinoso et al., 2002a; Reinoso et al., 2002b; Julian et al., 2011). In fact, the formation of specific floral tissue in response to chilling is a morphological indicator that the floral buds are out of dormant state and have entered an ecodormant state capable of responding to warm stimuli, resuming developmental pace and achieving reproduction success (Wang et al., 2004; Wang et al., 2016). Notably, floral initiation, formation and development are regulated by endogenous physiological states and seasonal thermal regimes.

2.1 Regulation of the phase transition from juvenile to adult stage

In the genetic realm, the majority of woody fruit crops exhibit a juvenile phase spanning from days to years, during which seedlings remain incapable of flowering even when subjected to suitable environmental triggers (Samach, 2012). In Arabidopsis, the transition from vegetative to inflorescence meristem appears to be regulated by the aging pathway requiring a miR156 (microRNA156) that controls PROMOTER BINDING PROTEIN-LIKE genes (SPLs) (Wang et al., 2009; Wu et al., 2009; Teotia and Tang, 2015; Xu et al., 2016b; Hyun et al., 2017). In this pathway, miR156 negatively regulates the activity of flowering activator SPLs. This family of SPLs, known for their multifunctionality, catalyzes floral transition by augmenting the expression of key genes such as LEAFY (LFY) and MADS box genes SOC1 and AP1 (Albani and Coupland, 2010; Lee and Lee, 2010; Ma et al., 2021). The engagement of the miR156-SPL module in the transition from juvenile to adult phases has been validated in various plants, including apple (Zhang et al., 2015a; Jia et al., 2017; Zheng et al., 2019), the conserved nature of this miR156-SPL module within the aging pathway is acknowledged across annual and perennial plant species. Yet, substantiating this module’s presence in other woody plants other than apple remains a necessity, along with addressing the intriguing query surrounding the divergent durations of juvenile phases observed among different woody plant species (Huijser and Schmid, 2011; Morea et al., 2016) (Figure 2).

Figure 2

Of notable significance is the involvement of the DELLA proteins that act as master regulators that rewire a multitude of transcriptional networks to control diverse biological responses (Briones-Moreno et al., 2023). One of the Arabidopsis DELLA factors exhibits a propensity to interact with distinct SPLs, yielding disparate outcomes. These interactions can either spark the initiation of floral primordia, such as through the activation of AP1 transcription via binding with SPL9, or act to inhibit SPL function, thus serving as a brake on the flowering process. This dual nature confers upon interactions of gibberellin (GA) and DELLA proteins to produce varying effects on the reproductive journey, depending on the developmental stage, all orchestrated by the intricate behavior of DELLA proteins (Yu et al., 2012; Yamaguchi et al., 2014; Bao et al., 2020).

The phase transition in fruit trees is also regulated by TFL1 and its related genes. For example, when the TFL1 gene is knocked out or down in apple plantlets, the flower inhibition imposed by juvenility is erased, allowing for flowering in re-juvenilized shoots as quickly as a few months, instead of the usual 3-6 years (Kotoda et al., 2006; Charrier et al., 2019). However, it is not yet clear how the miR156-SPL pathway interacts with TFL1.

2.2 The roles of CONSTANS- and CONSTANS-LIKE genes-FT regulatory framework in flower induction in fruit trees

Photoperiod, notably the duration of daylight, constitutes a pivotal environmental cue orchestrating plant flowering. This process elucidates the photoperiod pathway, wherein the CO gene plays a crucial role in transducing light signals to regulate FT expression (Samach et al., 2000; Kinoshita and Richter, 2020). While the CO-FT module has been unequivocally demonstrated in numerous annual plants, suggesting its theoretical conservation across all species (Putterill et al., 1995; Yano et al., 2000; Griffiths et al., 2003; Kim et al., 2008; Samach, 2012; Song et al., 2012; Lymperopoulos et al., 2018; Bao et al., 2020), the centrality of COLs (CO-LIKE genes) in the orchestration of flowering time remains a subject of contention. This is attributed in part to the intricate diversity in characterizing the COL gene family (Wong et al., 2014). Ectopic expression analyses of peach CO in Arabidopsis have indirectly supported the conservation of the CO-FT module in trees, hinting at a broader applicability (Böhlenius et al., 2006; Zhang et al., 2015b). In the case of apple, distinctive expression patterns of apple COLs in comparison to Arabidopsis genes suggest a divergent CO-FT module (Jeong et al., 1999). Expression studies have brought to light varying facets: grape CO linked to flowering initiation and COL1 associated with dormancy (Almada et al., 2009); six pear (Pyrus bretschneideri) COLs, out of a total of 15, showed circadian clock and photoperiod-regulated expression (Wang et al., 2017); and Mango (Mangifera indica L.) CO and COLs implicated in photoperiod-mediated flowering, with CO-FT conservativity warranting further clarification (Liu et al., 2020a; Liu et al., 2022). Similar investigations have extended to bamboo (Phyllostachys violascens), poplar (Populus trichocarpa), and Rabbiteye blueberries (Vaccinium virgatum Aiton), demonstrating their roles in photoperiod-controlled flowering through expression patterns or Arabidopsis ectopic expression (Xiao et al., 2018; Li et al., 2020; Omori et al., 2022).

However, the conclusive validation of the central role of the CO-FT module in woody plants awaits direct evidence from gain-of-function (e.g., overexpression) or loss-of-function (e.g., gene silencing/knockout) studies. The intricate multifunctional roles of the COLs family have added layers of complexity to their functional scrutiny. While the comprehensive understanding remains elusive, the CO-FT involvement in flowering function has yet to be ruled out. Concurrently, the interplay between CO expression and light in Arabidopsis reveals the intricate dance of phytochrome-phytohormone interactions in regulating flowering time and broader aspects of plant growth and development (Fornara et al., 2010; Lymperopoulos et al., 2018). The regulatory role of DELLAs in the GA pathway as a negative regulator of CO expression, along with the indirect influences of abscisic acid (ABA) and Jasmonate, further accentuates the intricate tapestry of these regulatory networks (Davis, 2009; Tiwari et al., 2010; Xu et al., 2016a; Bao et al., 2020; Izawa, 2021; Serrano-Bueno et al., 2021). Flower initiation in apple, peach, and other trees occurs in summer or late summer, suggesting that unlike in Arabidopsis, photoperiod signals may not play a role in flower induction. Instead, other endogenous signals such as physiological state, hormone homeostasis, or nutrient balance (e.g., photosynthetic output) might be influencing flower formation. As a result, the CO-FT module could gain new functions and interact with these endogenous signals in fruit trees to control floral initiation.

2.3 The opposite floral regulatory roles of GA-DELLA pathway in annuals and woody fruit trees

In Arabidopsis, phytohormones known as GAs play substantial roles in various aspects of plant growth and development, spanning processes such as seed germination, elongation growth, and the regulation of flowering time (Michniewicz and Lang, 1962; Yamauchi et al., 2004; Willige et al., 2007; Yamaguchi et al., 2014; Ni et al., 2015). This influence is often mediated through intricate interactions with multiple developmental pathways, facilitated by the DELLA domain which functions as a receiver domain for activated GA receptors (Yamauchi et al., 2004; Willige et al., 2007; Yamaguchi et al., 2014; Ni et al., 2015). The impact of GA on flowering time, whether promoting or inhibiting, hinges on the specific plant species and developmental stages at play (Koshita et al., 1999; Goldberg-Moeller et al., 2013; Pearce et al., 2013; Izawa, 2021). Broadly speaking, GAs tend to exert flowering promotion in long-day and biennial plants, while adopting an inhibitory role in other plant categories, encompassing fruit trees such as citrus (Citrus reticulata Blanco × Citrus temple Hort. ex Y. Tanaka) and grape (Boss and Thomas, 2002; Goldberg-Moeller et al., 2013; Li-Mallet et al., 2016; Zhang et al., 2019). Nonetheless, this species- and genotype-dependent function of GA in the intricate relationship of flowering introduces a level of uncertainty and complexity, thereby casting a degree of doubt upon GAs as strong candidates for the role of florigen. This sentiment persists despite findings in the grass species Lolium temulentum, where specific GAs (GA5 and GA6) emerge as an alternative source of florigenic signal distinct from FT, another floral signal originating from leaves (King and Evans, 2003; King et al., 2006).

However, the roles of GAs in regulation of floral formation in perennial flowering species appears to be quite different from that in annual species such as Arabidopsis. GA is thought to be inhibitory to flowering in perennials (Khan et al., 2014), as exemplified by the fact that exogenous applications of GA in citrus, apple and grapevine have been shown to inhibit flower production (Mullins, 1968; Srinivasan and Mullins, 1978; Zhu et al., 2008; Guo et al., 2018). This suggests that GA-generated/stimulated signals are rewired to distinct transcriptional pathways in perennials and annuals, resulting in opposite regulatory outputs. This finding is supported by the gain-of-function mutation of DELLAs, a main target of GA, in annual Arabidopsis and perennial grape, which led to repression and promotion of flowering, respectively (Peng and Harberd, 1997; Dill and Sun, 2001; Silverstone et al., 2001; Fleck and Harberd, 2002; Boss et al., 2006). Thus, DELLAs may be rewiring the same GA signals to transcriptional circuits or modules that have opposing functions, or targeting different factors that regulate flowering, resulting in contrasting flowering phenotypes.

2.4 Chilling-driven floral development in deciduous fruit trees

Within Arabidopsis, a collection of seven flowering-promoting genes situated within the autonomous pathway assumes a counteractive role against the MADS box gene FLC, which stands as a pivotal arbiter of flowering time within the vernalization pathway (Michaels and Amasino, 1999; Simpson, 2004; Michaels, 2009). Functioning as a negative regulator, FLC exerts control over flowering by suppressing the expression of FT and SOC1. The phenomenon of vernalization, characterized by prolonged cold exposure, effectively suppresses FLC expression, thus paving the way for the initiation of flowering. The involvement of SHORT VEGETATIVE PHASE (SVP) in this process emerges through its interaction with FLC, mirroring the function of FLC in response to vernalization by curbing GA biosynthesis (Gregis et al., 2006; Andres et al., 2014). Similarly, the vernalization pathway of wheat contains VERNALIZATION 2 (VRN2), a zinc finger protein that parallels FLC in its role within the wheat vernalization pathway. In this context, VRN1 and VRN3 function as counterparts to FT and the MADS box gene AP1, respectively (Gendall et al., 2001; Yan et al., 2003; Yan et al., 2004; Yan et al., 2006; Woods et al., 2016). It is of note that cereals harbor genes akin to FLC, although their functionalities largely remain enigmatic (Kennedy and Geuten, 2020). Collectively, this FLC-regulated vernalization pathway is generally presumed to be conserved in certain plant species, exemplified by Arabidopsis, while displaying evolutionary divergence in others, as seen in the case of cereals (Sheldon et al., 2000; Tadege et al., 2001; Alexandre and Hennig, 2008; Kennedy and Geuten, 2020).

The concept of “Chilling Requirement” (CR), in contrast to vernalization for transition of vegetative to inflorescence meristem in annual plants, elucidates the necessity for an adequate accumulation of chilling hours, pivotal for breaking dormancy and fostering the flowering process within specific woody plant species (Chouard, 1960; Jewaria et al., 2021). In terms of functionality, the CR-mediated flowering pathway in woody plants mirrors the vernalization pathway observed in annual plants (Brunner et al., 2014). The CR in fruit trees and vernalization in annuals and bi-annuals have different impact on flower regulation. Vernalization is required for transition of vegetative to inflorescence meristem while the CR is mostly for regulation of floral bud development rather initiation or formation. Only grape is exception in which conversion of vegetative anagens to inflorescences requires chilling or chilling promotes this conversion. In this sense. chilling acts as a bioregulator and is obligatory for floral development as exemplified by that warm temperature represses the floral development in dormant floral buds but chilling promotes it. As of present, the CR pathways involving FLC or VRN2 have not been definitively substantiated through both forward and reverse genetics methodologies (Table 1). However, insights from transcriptome analyses have unveiled the existence of FLC-like or VRN-like genes across numerous woody plants, including apple, grape, blueberry (Vaccinium corymbosum L.), and kiwifruit (Actinidia chinensis) (Diaz-Riquelme et al., 2009; Diaz-Riquelme et al., 2014; Varkonyi-Gasic et al., 2014; Porto et al., 2015; Kumar et al., 2016; Song and Chen, 2018b). Employing a forward genetics approach, the discovery of six interconnected Dormancy-Associated MADS-Box genes (DAMs) emerged as a hallmark of the CR pathway in the evergrowing mutant of peach. Among these, DAM5 and DAM6 were found to act as repressors of bud break, while DAM4 demonstrated pronounced chilling-induced repressor activity, particularly evident at the level of epigenetic regulation (Bielenberg et al., 2008; Jimenez et al., 2009; Li et al., 2009; Jimenez et al., 2010; Wells et al., 2015; Zhu et al., 2020a; Voogd et al., 2022). These DAMs stand as potential analogs to FLC or VRN2, possibly occupying central roles within the CR pathway (Falavigna et al., 2014; Falavigna et al., 2018; Falavigna et al., 2022). Nonetheless, the deficiency of reverse genetics evidence to confirm the functional role of DAMs in peaches stems from technical challenges arising from the absence of an efficient peach transformation system for conducting functional gene analysis. Moreover, the striking sequence similarities between DAMs, SVPs, and AGAMOUS-LIKE 24 (AGL24) of Arabidopsis, as well as their widespread presence in various woody plants (Table 1), adds to the intrigue and complexity of their roles.

Emerging as pivotal contenders within the CR pathway, both DAMs and FLC-like genes have extensively been studied across various significant woody fruit crops through techniques such as expression analysis, ectopic expression, overexpression, gene silencing, and gene knockout (Table 1). These comprehensive investigations have revealed several key insights:

• 1) The diversity and prevalence of DAMs and FLC-like genes present in woody plants.

• 2) Their integral involvement in flowering orchestrated by chilling exposure, while also revealing the nuanced role these genes play, often dependent on the specific species and genotype.

• 3) Contrary to the well-defined centrality of FLC in Arabidopsis or VRN2 in cereals within their respective vernalization pathways, no singular DAM or FLC-like gene in woody fruit crops appears to assume a universally conserved and central role in the CR pathway.

In fact, for all plant species requiring either vernalization or chilling, the pivotal factor in regulating flowering time is not individual genes like FLC in Arabidopsis, VRN1 in cereals, or DAMs (SVPs or AGL24), but rather the entire MADS-box gene family.

3 FT-dominated floral induction and SOC1-centered floral activation in deciduous woody plants

As elucidated earlier, the five well-established pathways in Arabidopsis—namely age, photoperiod, GA, autonomous, and vernalization—stand as the benchmark for unraveling flowering mechanisms in diverse plant species. The wealth of insights garnered through analyses of flowering pathways in myriad other plants has yielded a plethora of evidence. This evidence aids in discerning both conserved and nonconserved genes and intricate networks governing plant flowering. This accumulation of knowledge paves the way for endeavors aimed at manipulating individual gene(s) to regulate flowering time and enhance yields. Notably, it stands to reason that plants, including woody varieties, have, to varying degrees, evolved distinct flowering pathways. Drawing from the available literature, it becomes evident that at the core of floral induction resides FT-centered processes, while SOC1-centered mechanisms prevail in orchestrating floral activation across a wide spectrum of plants, if not universally so (Figure 2).

3.1 FT-dominated floral induction

FT acts as a critical integrator, assimilating signals for floral transition from approximately 10 activators and 30 repressors largely stemming from photoperiod and vernalization pathways, thus instigating flowering in Arabidopsis (Kobayashi et al., 1999; Wigge et al., 2005; Pin and Nilsson, 2012; Kinoshita and Richter, 2020; Liu et al., 2021). It stands prominently poised as a top contender for the florigen role (Turck et al., 2008; Turnbull, 2011; Pin and Nilsson, 2012). On the converse, TERMINAL FLOWER 1 (TFL1), a homolog of FT, exerts an opposing effect within Arabidopsis (Bradley et al., 1997; Kobayashi et al., 1999). Within the FT/TFL1 gene family, an assemblage of six members comes into view, encompassing FT, TWIN SISTER OF FT, TFL1, BROTHER OF FT AND TFL1 (BFT), MOTHER OF FT AND TFL1 (MFT), and ARABIDOPSIS THALIANA CENTROADIALIS HOMOLOGUE (ATC) (Yoo et al., 2010; Ryu et al., 2011; Liu et al., 2016). FT and TFL1 function through direct interactions with the bZIP transcription factor FD. The constitutive upregulation of FT or its orthologs (hereafter FT-CX) expression aligns with a proclivity for flowering promotion. Conversely, the persistent elevation of TFL1 or its orthologs (hereafter TFL1-CX) tends to elongate the flowering process. This dualistic phenomenon has been empirically validated across a range of plant species, including select woody plants (Table 1). Collectively, mounting evidence gleaned from ectopic expression and overexpression studies substantiates the conservation of FT and its orthologs across diverse plants, underscoring their ubiquitous roles as primary inducers within the flowering transition (Pin and Nilsson, 2012; Kinoshita and Richter, 2020; Liu et al., 2021).

The advancement of flowering in woody plants has been effectively catalyzed through the upregulation of FT-CX, as illustrated in Table 1. Noteworthy examples in deciduous fruit crops include investigations related to a blueberry FT gene, denoted as VcFT (Vc: Vaccinium corymbosum), and a poplar (Populus trichocarpa) FT1 gene (PtFT1) in European plum (Prunus domestica). PtFT1-CX induced continuous flowering as demonstrated by Srinivasan et al. (2012). Rigorous exploration has led to findings wherein the constitutive expression of VcFT (VcFT-CX) leads to a noteworthy shift in the flowering paradigm. Specifically, this alteration is characterized by the partial reversal of chilling requirements and the induction of early flowering within apical shoot meristems. In transgenic blueberry, this phenomenon resulted in the formation of multiple flower buds at each node, diverging from the single bud occurrence observed in their nontransgenic counterparts (Song et al., 2013b; Walworth et al., 2016). It is noteworthy, tough, that while VcFT-CX exerted significant influence, its effects were not fully comprehensive in substituting the requirement for chilling. Under conditions devoid of sufficient chilling hours, nearly 50% of flower buds failed to attain the requisite potential for blooming (Walworth et al., 2016). Therefore, while VcFT-CX did show phenotypic outcomes including expedited flowering and heightened floral bud formation, it remained inadequate in replicating the roles of chilling requirements intrinsic to blueberry flowering. Notably, the trend of expedited flowering attributed to the constitutive expression of FT orthologs and the contrasting delay occasioned by TFL1-CX has been extensively documented across an expanding array of woody plants. Despite this, further investigation is necessary to reveal the intricate involvement of FT in the context of CR-mediated flowering, a domain ripe for exploration (Table 1).

FT exhibits versatile functionality. Evident from previous research, the overexpression of FT orthologs in woody plants such as kiwifruit FT (AcFT) and VcFT-CX resulted in premature flowering within in vitro transformed shoots. However, this effect proved to be potentially overwhelming, hampering the shoots from evolving into viable plants (Moss et al., 2018; Song et al., 2019). The impact of FT-CX at transcript levels becomes readily apparent through comprehensive RNA sequencing analysis. Notably, instances like VcFT-CX provide insight into its extensive impact, significantly elevating VcFT expression in both leaves and flower buds; intriguingly, this upregulation was notably absent in roots. Simultaneously, thousands of differentially expressed genes (DEGs) attributed to VcFT expression varied across different tissues and developmental stages, even within the same tissue (Walworth et al., 2016; Song et al., 2019; Song et al., 2023).

When scrutinizing major blueberry flowering pathway genes including VcSOC1, VcAP1, VcFUL, VcLFY, VcSPLs, and VcSVP across three distinct tissues, intriguing patterns emerge:

• 1) In the apical shoot meristems where VcFT-CX induces early flowering, its influence extends to the upregulation of VcSOC1, VcAP1, VcFUL, VcLFY, and VcSPLs (Walworth et al., 2016).

• 2) In the mature leaves along the one-year-old shoot, where VcFT-CX results in the emergence of non-blooming floral buds, VcAP1 and VcFUL experience upregulation, while VcSOC1 and VcSVP are repressed (Walworth et al., 2016).

• 3) Within nonchilled VcFT-CX buds, VcLFY expression is elevated, whereas VcFUL, VcSOC1, and VcSVP experience repression (Walworth et al., 2016).

• 4) When considering VcFT-CX influence in roots, VcFUL and VcSPLs encounter increased expression, while VcSOC1 and VcSVP are repressed (Song et al., 2019).

These intricate observations collectively suggest that VcFT-CX induces signals for floral bud formation, at least partly through the upregulation of VcAP1 and VcFUL in leaves. Additionally, the expressions of VcSOC1 and VcSVP appear pivotal in determining the timing of both developing and mature floral bud break. The promotion of flowering by AP1 in various woody plants supports these findings (see Table 1). Counter to the flowering promotion led by VcFT-CX, the functional opposite, VcTFL1, triggers flowering delay (Omori et al., 2020; Omori et al., 2021; Omori et al., 2022). Intriguingly, VcFT-CX resulted in a reduction in VcTFL1 expression within young leaves (Walworth et al., 2016). Drawing parallels from Arabidopsis, where FT competes with TFLs for FD binding (Hanano and Goto, 2011; Zhu et al., 2020b). VcFT-CX led to a surprising decrease in VcFD expression within nonchilled flower buds. This observation underscores the likelihood of an interaction between VcFT and VcFD within floral buds, indicating their interplay.

The hereditary promotion of flowering through FT-CX has been substantiated within both self- and cross-pollinated Eucalyptus seedlings (Klocko et al., 2016). Conversely, in poplar, the constitutive expression of LFY, AP1, and CO resulted in marginal to negligible advancements in early flowering, a contrast to the robust effect observed with FT-CX (Rottmann et al., 2000; Zhang et al., 2010; Klocko et al., 2016). Similarly, the hereditary transmission of VcFT-CX translated to a remarkable reduction in flowering time for cross-pollinated, transgenic blueberry seedlings, swiftly transitioning them to bloom within a few months, in comparison to the 2-3 years characteristic of their nontransgenic counterparts (Our unpublished data). Clearly, FT-CX emerges as a potent factor in accelerating the transition from the juvenile phase.

FT has consistently remained a prominent candidate in the pursuit of identifying the elusive florigen. FT originates within leaves and subsequently moves to the meristems (Turck et al., 2008; Fornara et al., 2010; Krzymuski et al., 2015). Intriguing insights have indicated from transgrafting experiments involving FT-CX materials, underscoring the role of FT-CX in signaling the onset of flowering. In several instances, the FT-CX generated within transgenic leaves, functioning as either a direct or an indirect florigenic signal, exhibited the remarkable capacity to promote flowering in nontransgenic scions through long-distance transportation (Ye et al., 2014; Song et al., 2019; Wu et al., 2022). This phenomenon diverges distinctly from parallel transgrafting studies where FT-CX produced in transgenic roots and stems (in the absence of transgenic leaves) failed to incite flowering in nontransgenic scions (Zhang et al., 2010; Srinivasan et al., 2012; Wenzel et al., 2013; Bull et al., 2017).

In transgrafted blueberry where the transgenic leaves were retained, the influence of VcFT-CX within the transgenic rootstock precipitated floral bud formation within the shoot tips of nontransgenic scions. However, VcFT exhibited negligible alterations, while a cluster of phytohormone genes in nontransgenic scions showed varying expressions (Song et al., 2019). Collectively, the evidence demonstrates the status of FT as a universal catalyst for the initiation of floral bud formation and the hastening flowering process. To gain a more comprehensive understanding of the long-range florigenic signals originating from FT or FT-CX, whether in the form of FT protein, FT mRNA, or other derivatives such as phytohormones, further investigations are needed to unravel this intriguing aspect (Wilkie et al., 2008; Izawa, 2021).

3.2 SOC1-centered floral activation

SOC1 stands as a central integrator within the flowering pathway (see review by Lee and Lee, 2010). Evidence across various plant species highlights SOC1’s role as a ubiquitous accelerator of flowering, underscoring its significance (Table 1) (Lee et al., 2004; Lee et al., 2008; Seo et al., 2009; Alter et al., 2016; Han et al., 2021; Song et al., 2021). In Arabidopsis, SOC1 takes on the role of a coordinator, integrating signals from diverse pathways. These connections include the aging pathway, mediated by SPLs, the vernalization/autonomous pathway through FLC, the photoperiod pathway involving FT, and the GA pathway, facilitated by GA (Figure 2). Notably, SOC1’s influence extends to the activation of the LFY gene, a key step in establishing the identity of floral meristems or organs (Lee and Lee, 2010).

SOC1, alongside FLC, AP1, AGL24, SVP, FUL, and CAL, represents a cohort of MADS box genes encoding MIKCc type proteins characterized by four conserved domains: MADS (M-), intervening (I-), Keratin-like (K-), and C-terminal (C-) (Gramzow and Theissen, 2010; Gramzow and Theissen, 2015). This array of MADS box genes assumes dual roles, vital both in the context of the ABC model of floral development and in governing the temporal aspects of flowering (Amasino, 2010; Heijmans et al., 2012; Smaczniak et al., 2012; Su et al., 2018). Conventionally, AP1 and SOC1 have emerged as accelerators of flowering across diverse plant species. Conversely, FLC serves as a repressor, exerting repression on the expression of both FT and SOC1 in Arabidopsis. Within Arabidopsis’ vernalization pathway, the antagonistic action of negative regulators, FLC and SVP, counters the positive regulators SOC1 and AGL24 (Fornara et al., 2010; Lee and Lee, 2010). The investigations on CR-mediated flowering woody plant flowering have identified five groups of MADS box genes, specifically the orthologs of FLC, SOC1, SVP, AGL24, and DAMs (Table 1). Amidst these gene clusters, one consensus emerges: the SOC1 group, a positive regulator, can steer the course of floral initiation and hasten flowering. Yet, the roles of the remaining four gene groups exhibit divergence across diverse plant species. For instance, while FLC-like genes have been identified, the extent of their conserved functions in woody plants remains largely unknown (Table 1). Notably, apple’s FLC-like genes do not mirror FLC’s functions precisely (Porto et al., 2015; Nishiyama et al., 2021). Divergent from expectations, a kiwifruit FLC-like variant expedites flowering, in contrast to FLC’s recognized role in delaying it (Voogd et al., 2022). Similarly, the constitutive expression of an apple FLC3 variant accelerates flowering in blueberry (Zong et al., 2019; Kagaya et al., 2020).

In woody plants, the CR is orchestrated by MADS box genes DAMs, AGL24-like genes, and SVP-like genes (SVLs), which are prominent genes akin to FLC functions albeit the scarcity of reverse genetic substantiation (Zhu et al., 2020a; da Silveira Falavigna et al., 2021; Jewaria et al., 2021). These CR-associated MADS box genes act upstream of SOC1 orthologs and can steer the course of floral development. With chilling accumulation, SOC1 orthologs are activated. For instance, the grape, blueberry, and apple exhibit an increase in expression of SOC1 orthologs in response to the accrual of chilling hours (Hattasch et al., 2008; Song and Chen, 2018b; Kamal et al., 2019). In poplar (Populus tremula × alba), overexpression of a SOC1-like variant leads to bud break (Gómez-Soto et al., 2021; Goralogia et al., 2021). In kiwifruit (Actinidia delicious), SOC1-like genes potentially influence the duration of dormancy, although their role in the transition to flowering remains inconclusive (Voogd et al., 2015). Genetic investigations have shown a linkage between alleles of SOC1 orthologs and the chilling requisites in apricot (Prunus armeniaca L.) and peach genotypes, underlining a pronounced correlation (Trainin et al., 2013; Halasz et al., 2021). Collectively, it is the expression of SOC1 orthologs that governs the poised readiness for floral bud break and activation subsequent to fulfilling the chilling requirement in woody plants.

In Arabidopsis, the decreased expression of SVP during vernalization sets in motion the activation of SOC1 (or SOC1-like gene), thereby initiating the onset of flowering. However, in woody plants, the involvement of SVP homologs and SVLs in the flowering process exhibits a spectrum of variance contingent upon the particular SVP homologs in play. To illustrate, the SVP homologs and SVLs in kiwifruit, trifoliate orange (Poncirus trifoliata L. Raf.), apple, and sweet cherry (Prunus avium L.) play the role of suppressors, effectively suppressing budbreak and the flowering cycle (Gregis et al., 2006; Li et al., 2010; Wu et al., 2017a; Wu et al., 2017b; Wang et al., 2021). Meanwhile, in grapevines, the SVP homologs unveil a degree of inconsistency, alternating between acting as promoters or inhibitors of flowering (Diaz-Riquelme et al., 2012; Li-Mallet et al., 2016; Arro et al., 2019; Kamal et al., 2019; Dong et al., 2022).

4 Flowering mechanism: a case study in blueberry

The highbush blueberry (2n = 4x = 48), a prominent cultivated member of the Vaccinium fruit crop family, has a rather substantial chilling requirement, typically surpassing 800 chilling units, that must be met to initiate dormancy release during spring (Song et al., 2011; Edger et al., 2022). Over the course of past decades, extensive investigations have been carried out to reveal the flowering mechanism (Song et al., 2023). A summary of these blueberry studies can serve as an illustrative example, providing insights into the network of factors that underlie flowering mechanisms in woody plants.

4.1 VcFT is a major floral initiator

The impact of VcFT-CX is evident across different plant species. In tobacco (Nicotiana tabacum) and petunia (Petunia x hybrid), VcFT-CX not only induced early flowering but also led to plant dwarfing (Song et al., 2013b). Similarly, under nonchilling conditions, the northern highbush blueberry cultivar Aurora exhibited precocious flowering as a result of VcFT-CX (Song et al., 2013b). At the transcript level, VcFT-CX triggered a substantial increase in VcFT expression in leaves and nonchilled floral buds, while its effect on young roots was not significant (Walworth et al., 2016; Song et al., 2019; Song et al., 2023). Notably, VcFT-CX displayed distinct effects on various tissues and developmental stages (Walworth et al., 2016; Song et al., 2019; Song et al., 2023). In young leaves, it upregulated the expressions of VcAP1/VcFUL, blueberry SEPALLATA (VcSEP), VcLFY, VcSOC1, and VcTFL1, with no significant changes in VcSVP and VcFD (Figure 3A) (Walworth et al., 2016). In mature leaves, VcFT-CX enhanced VcAP1/VcFUL and VcSEP expressions, while repressing VcSOC1 and VcSVP, and it had minimal impact on VcLFY, VcFD, and VcTFL1 (Figure 3B) (Song et al., 2023). In nonchilled flower buds, VcFT-CX upregulated VcLFY expression, downregulated VcSEP, VcSOC1, VcSVP, VcFD, and VcTFL1, while VcAP1/VcFUL expression remained relatively unaffected (Figure 3C) (Song et al., 2023). In young roots, VcAP1/VcFUL expression increased, while VcSOC1 and VcSVP decreased; VcSEP, VcLFY, VcFD, and VcTFL1 showed no significant changes (Figure 3D) (Song et al., 2019). Key takeaways from the analysis of VcFT-CX tissues include: 1) Varied responses of major flowering pathway genes (e.g., VcSEP3, VcSOC1, and VcSVP) to VcFT-CX across tissues and developmental stages, with a consistent promotion of VcLFY and VcAP1/VcFUL expression; 2) Enhanced expressions of VcAP1/VcFUL and VcSEP in leaf tissues due to VcFT-CX, indicating the potential role of these genes in floral initiation, while VcFD and VcTFL1 seem less involved in promoting floral initiation; 3) Repression of VcFD and VcTFL1 expressions in nonchilled floral buds by VcFT-CX; and 4) Likely pivotal roles of VcSOC1 and VcSVP in the activation of floral buds under chilling conditions.

Figure 3

Moreover, as rootstocks, VcFT-CX produced signals in leaves that were effectively conveyed through transgrafting to nontransgenic scions (cv. Legacy), yielding a distinctive enhancement in floral bud formation (Song et al., 2019). Intriguingly, at the transcript level, VcFT-CX in rootstocks did not trigger differential expression of VcFT, VcFD, VcTFL1, VcAP1/VcFUL, VcLFY, VcSVP, and VcSEP3 in the grafted nontransgenic scions. Interestingly, expression of VcSOC1 was significantly downregulated (Figure 3E). Notably, there is an instance where none of the identified major flowering pathway genes (e.g., VcFT, VcAP1/VcFUL, VcSOC1, and VcLFY) appear to solely account for the promoted floral bud formation, indicating that an escalated VcFT expression is not always the sole requirement for initiating flowering (Song et al., 2019). As for the potential long-distance florigenic signals inducing from VcFT-CX, their precise nature remains to be discerned from candidates like VcFT protein/mRNA, cytokinin, or other hormonal factors (Gao et al., 2016; Walworth et al., 2016; Song et al., 2019).

4.2 VcSOC1 is a major floral activator

Comparative analyses of floral buds have been conducted for four genotypes, including a nontransgenic northern highbush variety Aurora, a VcFT-CX transgenic ‘Aurora’, a nontransgenic southern highbush variety Legacy, and a transgenic Legacy mutant (Mu1-Legacy) (Figure 4) (Song and Chen, 2018b; Song and Walworth, 2018; Song et al., 2023). Among these four comparisons: 1) VcFT expression demonstrated either negligible differential expression in nontransgenic cultivars or downregulation in the two transgenic genotypes, suggesting that VcFT may not a primary target of chilling accumulation for bud break; 2) Expression of VcLFY, VcTFL1, and VcFD remained either suppressed or constant post full chilling; 3) VcAP1/VcFUL expression increased in three genotypes and decreased in VcFT-CX ‘Aurora’; and 4) VcSOC1 expression was upregulated in three genotypes and exhibited no significant differential expression in VcFT-CX ‘Aurora’, while VcSVP expression was elevated in all four genotypes (Figure 4). Collectively, VcSOC1 and VcSVP played key roles in chilling requirement-mediated floral activation. Interestingly, in transcriptomic comparisons between late pink buds and fully chilled stages for two genotypes, expressions of VcFT, VcFD, VcTFL1, VcAP1/VcFUL, VcLFY, and VcSOC1 were uniformly repressed in late pink buds (Figure 4) (Song and Chen, 2018b).

Figure 4

Further evidence supporting VcSOC1 as a significant floral activator is the fact that the constitutive expression of the K domain of VcSOC1 (VcSOC1K-CX) led to the flowering of transgenic ‘Aurora’ plants under nonchilling conditions, a condition where nontransgenic ‘Aurora’ plants remained unable to flower (Song and Chen, 2018a). SOC1 is classified as a type-II plant-specific MIKC protein, characterized by its conserved MADS (M-), intervening (I), keratin-like (K-), and C-terminal (C-) domains (Theissen et al., 1996). The K domain is instrumental in facilitating interactions among various MADS box genes. Remarkably, VcSOC1K-CX has also demonstrated the ability to accelerate flowering in tobacco and maize (Song et al., 2013a; Song and Han, 2021). In blueberry, the promotion of flowering through VcSOC1K-CX was associated by the increased expression of VcSOC1, which in turn led to the repression of VcFT, VcFD, VcTFL1, VcAP1/VcFUL, VcLFY, and VcSVP, offering another piece of evidence that the elevation of VcFT expression is not always a prerequisite for flowering promotion in ‘Aurora’ (Figure 3F) (Song and Chen, 2018a).

While the expression of VcSOC1 is indeed crucial for CR-mediated floral activation in blueberry, it is important to note that VcSOC1 does not always play an obligatory role in floral bud activation. An intriguing instance is presented by the Mu1-Legacy genotype, which carries an overexpressed blueberry DWARF AND DELAYING FLOWERING 1 gene (VcDDF1), allowing it to flower under nonchilling conditions, a feat nontransgenic ‘Legacy’ plants could not achieve (Song and Walworth, 2018). Remarkably, in this scenario, none of the major genes—VcSOC1, VcFT, VcAP1/VcFUL, VcLFY, VcSVP, and VcSEP3—displayed discernible differential expression in both young leaves and floral buds (Figure 5) (Song and Walworth, 2018; Lin et al., 2019).

Figure 5

As of now, functional FLC-like candidates have not been definitively identified, despite the presence of orthologues of many other vernalization pathway genes from Arabidopsis in blueberry (Walworth et al., 2016). Notably, the intriguing case of an apple FLC3-like gene stands out, as its constitutive expression surprisingly promotes flowering instead of causing the expected delay (Zong et al., 2019). Although there have been studies examining the effects of chilling accumulation on the expression of flowering pathway genes, the impact of warm accumulation on the activation of fully chilled floral buds remains an area yet to be thoroughly explored. In light of the available literature, it is apparent that among the genes within the flowering pathway, VcSOC1 plays a pivotal role as a major floral activator.

4.3 A VcFT/VcSOC1 regulatory module in blueberry flowering

In general, the expression of FT within leaves is significantly influenced by light conditions, whereas SOC1 expression is modulated in response to temperature changes. Notably, VcFT attains its peak expression in floral buds, while VcSOC1 reaches its highest expression level in leaves (Walworth et al., 2016). Recently, a regulatory framework centered on the ratio of FT-to-SOC1 expression (VcFT/VcSOC1) has been proposed, providing a valuable lens through which to comprehend the processes of floral initiation and activation. According to this model, an elevated VcFT/VcSOC1 ratio in leaves serves to stimulate floral initiation, while heightened VcSOC1 expression can lead to early flowering. Within flower buds, the VcFT/VcSOC1 ratios often decline in chilled buds due to the increasing VcSOC1 expression during chilling accumulation, whereas emerging flower buds exhibit rising VcFT/VcSOC1 ratios due to the more rapid decline of VcSOC1 expression relative to VcFT (Song et al., 2023). This principle is further bolstered by observations of reduced FT/SOC1 ratios in polar buds during chilling accumulation, marked by an upsurge in SOC1 expression alongside neutral FT levels (Gómez-Soto et al., 2021). Nonetheless, it’s important to acknowledge that this VcFT/VcSOC1 ratio might not be universally applicable to all tested blueberry genotypes; for instance, the altered flowering pattern in the Legacy-mutant1 was not attributable to major flowering pathway genes (Song and Walworth, 2018). Collectively, this FT/SOC1 ratio emerges as a potential determinant of both leaf-based floral initiation and bud-based floral activation, given that these genes hold pivotal roles as integrators within the flowering pathway.

4.4 Other regulatory genes for floral initiation or activation beyond flowering pathway genes

In addition to the well-defined flowering pathway genes, there exists a range of genes from other pathways that exert influence over floral initiation and activation. A notable instance, as discussed earlier, is the altered floral initiation and activation process observed in Mu1-Legacy, wherein neither VcFT nor VcSOC1 played a role (Figure 5). Upon scrutinizing the transcriptomic analysis of blueberry flowering pathway genes, it becomes evident that numerous genes from hormone and sugar pathways are intricately linked to floral bud initiation or activation, whether through direct or indirect means (Gao et al., 2016; Lin et al., 2019; Song et al., 2019). This underlies the fact that hormones and sugar pathway genes, in conjunction with the flowering pathway genes, likely participate in a coordinated manner to regulate the process of flowering (Izawa, 2021).

5 Conclusion

The well-established genetic framework governing flowering pathways in Arabidopsis has served as a cornerstone for unraveling the intricate mechanisms operating in other plants. Woody plants, however, have developed notably complex flowering pathways compared to Arabidopsis, although some key flowering pathway genes maintain largely conserved roles (Table 1, Figure 2). The CO-FT module within the photoperiod pathway, which is crucial in Arabidopsis, appears to be considerably conserved in woody plants, although the functions of CO or COL orthologues in this context warrant further investigation. The miR156-SPL module of the age pathway exhibits conservation across all plant species, notwithstanding the varied roles of SPLs in woody plants. In the GA pathway, the interactions involving GA and DELLA factors demand deeper exploration in both Arabidopsis and woody plants due to their extensive influence on both floral initiation and activation. The FLC-mediated vernalization pathway, a central mechanism in Arabidopsis, exhibits the least conservation in woody plants, where effective chilling is requisite to initiate flowering. Nonetheless, it’s noteworthy that MADS-box genes play significant roles in floral activation. In essence, among the individual flowering pathway genes, FT and its orthologues serve as pivotal floral initiators, while SOC1 and its orthologs stand as the principal floral activators. Remarkably, this pattern remains highly conserved across plant species.

References

• 1

  AlbaniM. C.CouplandG. (2010). Comparative analysis of flowering in annual and perennial plants. Curr. Top. Dev. Biol.91, 323–348. doi: 10.1016/s0070-2153(10)91011-9

  • CrossRef
  • Google Scholar

• 2

  AlexandreC. M.HennigL. (2008). FLC or not FLC: the other side of vernalization. J. Exp. Bot.59 (6), 1127–1135. doi: 10.1093/jxb/ern070

  • CrossRef
  • Google Scholar

• 3

  AlmadaR.CabreraN.CasarettoJ. A.Ruiz-LaraS.Gonzalez VillanuevaE. (2009). VvCO and VvCOL1, two CONSTANS homologous genes, are regulated during flower induction and dormancy in grapevine buds. Plant Cell Rep.28 (8), 1193–1203. doi: 10.1007/s00299-009-0720-4

  • CrossRef
  • Google Scholar

• 4

  AlterP.BirchenederS.ZhouL. Z.SchluterU.GahrtzM.SonnewaldU.et al. (2016). Flowering time-regulated genes in maize include the transcription factor zmMADS1. Plant Physiol.172 (1), 389–404. doi: 10.1104/pp.16.00285

  • CrossRef
  • Google Scholar

• 5

  AmasinoR. (2010). Seasonal and developmental timing of flowering. Plant J.61 (6), 1001–1013. doi: 10.1111/j.1365-313X.2010.04148.x

  • CrossRef
  • Google Scholar

• 6

  AndresF.CouplandG. (2012). The genetic basis of flowering responses to seasonal cues. Nat. Rev. Genet.13 (9), 627–639. doi: 10.1038/nrg3291

  • CrossRef
  • Google Scholar

• 7

  AndresF.PorriA.TortiS.MateosJ.Romera-BranchatM.Garcia-MartinezJ. L.et al. (2014). SHORT VEGETATIVE PHASE reduces gibberellin biosynthesis at the Arabidopsis shoot apex to regulate the floral transition. Proc. Natl. Acad. Sci. United. States America111 (26), E2760–E2769. doi: 10.1073/pnas.1409567111

  • CrossRef
  • Google Scholar

• 8

  AroraR.RowlandL. J.TaninoK. (2003). Induction and release of bud dormancy in woody perennials: a science comes of age. HortScience38, 11. doi: 10.21273/HORTSCI.38.5.911

  • CrossRef
  • Google Scholar

• 9

  ArroJ.YangY.SongG.-Q.ZhongG.-Y. (2019). RNA-Seq reveals new DELLA targets and regulation in transgenic GA-insensitive grapevines. BMC Plant Biol.19 (1), 80. doi: 10.1186/s12870-019-1675-4

  • CrossRef
  • Google Scholar

• 10

  AtkinsonC. J.BrennanR. M.JonesH. G. (2013). Declining chilling and its impact on temperate perennial crops. Environ. Exp. Bot.91, 48–62. doi: 10.1016/j.envexpbot.2013.02.004

  • CrossRef
  • Google Scholar

• 11

  BaiS.TuanP. A.SaitoT.ItoA.UbiB. E.BanY.et al. (2017). Repression of TERMINAL FLOWER1 primarily mediates floral induction in pear (Pyrus pyrifolia Nakai) concomitant with change in gene expression of plant hormone-related genes and transcription factors. J. Exp. Bot.68 (17), 4899–4914. doi: 10.1093/jxb/erx296

  • CrossRef
  • Google Scholar

• 12

  BaoS. J.HuaC. M.ShenL. S.YuH. (2020). New insights into gibberellin signaling in regulating flowering in Arabidopsis. J. Integr. Plant Biol.62 (1), 118–131. doi: 10.1111/jipb.12892

  • CrossRef
  • Google Scholar

• 13

  BaurleI.DeanC. (2006). The timing of developmental transitions in plants. Cell125 (4), 655–664. doi: 10.1016/j.cell.2006.05.005

  • CrossRef
  • Google Scholar

• 14

  BielenbergD. G.WangY.LiZ. G.ZhebentyayevaT.FanS. H.ReighardG. L.et al. (2008). Sequencing and annotation of the evergrowing locus in peach [Prunus persica (L.) Batsch] reveals a cluster of six MADS-box transcription factors as candidate genes for regulation of terminal bud formation. Tree Genet. Genomes4 (3), 495–507. doi: 10.1007/s11295-007-0126-9

  • CrossRef
  • Google Scholar

• 15

  BöhleniusH.HuangT.Charbonnel-CampaaL.BrunnerA. M.JanssonS.StraussS. H.et al. (2006). CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science312 (5776), 1040–1043. doi: 10.1126/science.1126038

  • CrossRef
  • Google Scholar

• 16

  BossP. K.SreekantanL.ThomasM. R. (2006). A grapevine TFL1 homologue can delay flowering and alter floral development when overexpressed in heterologous species. Funct. Plant Biol.33 (1), 31–41. doi: 10.1071/fp05191

  • CrossRef
  • Google Scholar

• 17

  BossP. K.ThomasM. R. (2002). Association of dwarfism and floral induction with a grape ‘green revolution’ mutation. Nature416 (6883), 847–850. doi: 10.1038/416847a

  • CrossRef
  • Google Scholar

• 18

  BradleyD.RatcliffeO.VincentC.CarpenterR.CoenE. (1997). Inflorescence commitment and architecture in Arabidopsis. Science275 (5296), 80–83. doi: 10.1126/science.275.5296.80

  • CrossRef
  • Google Scholar

• 19

  BranchereauC.Quero-GarciaJ.Zaracho-EchagueN. H.LambelinL.FoucheM.WendenB.et al. (2022). New insights into flowering date in Prunus: fine mapping of a major QTL in sweet cherry. Horticult. Res.9, uhac042. doi: 10.1093/hr/uhac042

  • CrossRef
  • Google Scholar

• 20

  Briones-MorenoA.Hernández-GarcíaJ.Vargas-ChávezC.Blanco-TouriñánN.PhokasA.ÚrbezC.et al. (2023). DELLA functions evolved by rewiring of associated transcriptional networks. Nat. Plants9 (4), 535–543. doi: 10.1038/s41477-023-01372-6

  • CrossRef
  • Google Scholar

• 21

  BrunnerA. M.EvansL. M.HsuC. Y.ShengX. (2014). Vernalization and the chilling requirement to exit bud dormancy: shared or separate regulation? Front. Plant Sci.5. doi: 10.3389/fpls.2014.00732

  • CrossRef
  • Google Scholar

• 22

  BullS. E.AlderA.BarsanC.KohlerM.HennigL.GruissemW.et al. (2017). FLOWERING LOCUS T triggers early and fertile flowering in glasshouse cassava (Manihot esculenta crantz). Plants (Basel)6 (2), 22. doi: 10.3390/plants6020022

  • CrossRef
  • Google Scholar

• 23

  CharrierA.VergneE.DoussetN.RicherA.PetiteauA.ChevreauE. (2019). Efficient targeted mutagenesis in apple and first time edition of pear using the CRISPR-cas9 system. Front. Plant Sci.10. doi: 10.3389/fpls.2019.00040

  • CrossRef
  • Google Scholar

• 24

  ChenY. H.JiangP.ThammannagowdaS.LiangH. Y.WildeH. D. (2013). Characterization of peach TFL1 and comparison with FT/TFL1 gene families of the rosaceae. J. Am. Soc. Hortic. Sci.138 (1), 12–17. doi: 10.21273/Jashs.138.1.12

  • CrossRef
  • Google Scholar

• 25

  ChouardP. (1960). Vernalization and its relations to dormancy. Annu. Rev. Plant Physiol. Plant Mol. Biol.11, 191–238. doi: 10.1146/annurev.pp.11.060160.001203

  • CrossRef
  • Google Scholar

• 26

  ContiL. (2017). Hormonal control of the floral transition: Can one catch them all? Dev. Biol.430 (2), 288–301. doi: 10.1016/j.ydbio.2017.03.024

  • CrossRef
  • Google Scholar

• 27

  da Silveira FalavignaV.SeveringE.LaiX.EstevanJ.FarreraI.HugouvieuxV.et al. (2021). Unraveling the role of MADS transcription factor complexes in apple tree dormancy. New Phytol.232 (5), 2071–2088. doi: 10.1111/nph.17710

  • CrossRef
  • Google Scholar

• 28

  DavisS. J. (2009). Integrating hormones into the floral-transition pathway of Arabidopsis thaliana. Plant Cell Environ.32 (9), 1201–1210. doi: 10.1111/j.1365-3040.2009.01968.x

  • CrossRef
  • Google Scholar

• 29

  Diaz-RiquelmeJ.GrimpletJ.Martinez-ZapaterJ. M.CarmonaM. J. (2012). Transcriptome variation along bud development in grapevine (Vitis vinifera L.). BMC Plant Biol.12, 181. doi: 10.1186/1471-2229-12-181

  • CrossRef
  • Google Scholar

• 30

  Diaz-RiquelmeJ.LijavetzkyD.Martinez-ZapaterJ. M.CarmonaM. J. (2009). Genome-wide analysis of MIKCC-type MADS box genes in grapevine. Plant Physiol.149 (1), 354–369. doi: 10.1104/pp.108.131052

  • CrossRef
  • Google Scholar

• 31

  Diaz-RiquelmeJ.Martinez-ZapaterJ. M.CarmonaM. J. (2014). Transcriptional analysis of tendril and inflorescence development in grapevine (Vitis vinifera L.). PloS One9 (3), e92339. doi: 10.1371/journal.pone.0092339

  • CrossRef
  • Google Scholar

• 32

  DillA.SunT. (2001). Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. Genetics159 (2), 777–785. doi: 10.1093/genetics/159.2.777

  • CrossRef
  • Google Scholar

• 33

  DoV. G.LeeY.KimS.KweonH.DoG. (2022). Antisense expression of apple TFL1-like gene (MdTFL1) promotes early flowering and causes phenotypic changes in tobacco. Int. J. Mol. Sci.23 (11), 6006. doi: 10.3390/ijms23116006

  • CrossRef
  • Google Scholar

• 34

  DongY.Khalil-Ur-RehmanM.LiuX.WangX.YangL.TaoJ.et al. (2022). Functional characterisation of five SVP genes in grape bud dormancy and flowering. Plant Growth Regul.97 (3), 511–522. doi: 10.1007/s10725-022-00817-w

  • CrossRef
  • Google Scholar

• 35

  EdgerP. P.IorizzoM.BassilN. V.BenevenutoJ.FerrãoL. F. V.GiongoL.et al. (2022). There and back again; historical perspective and future directions for Vaccinium breeding and research studies. Horticult. Res.9, uhac083. doi: 10.1093/hr/uhac083

  • CrossRef
  • Google Scholar

• 36

  FalavignaV. D. S.GuittonB.CostesE.AndresF. (2018). I want to (Bud) break free: the potential role of DAM and SVP-like genes in regulating dormancy cycle in temperate fruit trees. Front. Plant Sci.9. doi: 10.3389/fpls.2018.01990

  • CrossRef
  • Google Scholar

• 37

  FalavignaV. D.PortoD. D.BuffonV.Margis-PinheiroM.PasqualiG.ReversL. F. (2014). Differential transcriptional profiles of dormancy-related genes in apple buds. Plant Mol. Biol. Rep.32 (4), 796–813. doi: 10.1007/s11105-013-0690-0

  • CrossRef
  • Google Scholar

• 38

  FalavignaV. S.SeveringE.EstevanJ.FarreraI.HugouvieuxV.ReversL. F.et al. (2022). Potential role of apple SOC1-like transcription factors in gene regulatory networks involved in bud dormancy. Acta Hortic.1342), 8. doi: 10.17660/ActaHortic.2022.1342.6

  • CrossRef
  • Google Scholar

• 39

  FangZ. Z.KuiL. W.DaiH.ZhouD. R.JiangC. C.EspleyR. V.et al. (2022). The genome of low-chill Chinese plum “Sanyueli” (Prunus salicina Lindl.) provides insights into the regulation of the chilling requirement of flower buds. Mol. Ecol. Resour.22 (5), 1919–1938. doi: 10.1111/1755-0998.13585

  • CrossRef
  • Google Scholar

• 40

  FlachowskyH.HattaschC.HoferM.PeilA.HankeM. V. (2010). Overexpression of LEAFY in apple leads to a columnar phenotype with shorter internodes. Planta231 (2), 251–263. doi: 10.1007/s00425-009-1041-0

  • CrossRef
  • Google Scholar

• 41

  FlachowskyH.SzankowskiI.WaidmannS.PeilA.TranknerC.HankeM. V. (2012). The MdTFL1 gene of apple (Malus x domestica Borkh.) reduces vegetative growth and generation time. Tree Physiol.32 (10), 1288–1301. doi: 10.1093/treephys/tps080

  • CrossRef
  • Google Scholar

• 42

  FleckB.HarberdN. P. (2002). Evidence that the Arabidopsis nuclear gibberellin signalling protein GAI is not destabilised by gibberellin. Plant J.32 (6), 935–947. doi: 10.1046/j.1365-313X.2002.01478.x

  • CrossRef
  • Google Scholar

• 43

  FornaraF.de MontaiguA.CouplandG. (2010). SnapShot: control of flowering in arabidopsis. Cell141 (3), 550–550e2. doi: 10.1016/j.cell.2010.04.024

  • CrossRef
  • Google Scholar

• 44

  FreimanA.GolobovitchS.YablovitzZ.BelausovE.DahanY.PeerR.et al. (2015). Expression of flowering locus T2 transgene from Pyrus communis L. delays dormancy and leaf senescence in Malus x domestica Borkh, and causes early flowering in tobacco. Plant Sci.241, 164–176. doi: 10.1016/j.plantsci.2015.09.012

  • CrossRef
  • Google Scholar

• 45

  GaoX.WalworthA. E.MackieC.SongG. Q. (2016). Overexpression of blueberry FLOWERING LOCUS T is associated with changes in the expression of phytohormone-related genes in blueberry plants. Hortic. Res.3, 16053. doi: 10.1038/hortres.2016.53

  • CrossRef
  • Google Scholar

• 46

  GaoY. H.YangQ. S.YanX. H.WuX. Y.YangF.LiJ. Z.et al. (2021). High-quality genome assembly of ‘Cuiguan’ pear (Pyrus pyrifolia) as a reference genome for identifying regulatory genes and epigenetic modifications responsible for bud dormancy. Horticult. Res.8 (1), 197. doi: 10.1038/s41438-021-00632-w

  • CrossRef
  • Google Scholar

• 47

  GendallA. R.LevyY. Y.WilsonA.DeanC. (2001). The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell107 (4), 525–535. doi: 10.1016/S0092-8674(01)00573-6

  • CrossRef
  • Google Scholar

• 48

  Goldberg-MoellerR.ShalomL.ShlizermanL.SamuelsS.ZurN.OphirR.et al. (2013). Effects of gibberellin treatment during flowering induction period on global gene expression and the transcription of flowering-control genes in Citrus buds. Plant Sci.198, 46–57. doi: 10.1016/j.plantsci.2012.09.012

  • CrossRef
  • Google Scholar

• 49

  Gómez-SotoD.Ramos-SánchezJ. M.AliqueD.CondeD.TriozziP. M.PeralesM.et al. (2021). Overexpression of a SOC1-related gene promotes bud break in ecodormant poplars. Front. Plant Sci.12. doi: 10.3389/fpls.2021.670497

  • CrossRef
  • Google Scholar

• 50

  GoralogiaG. S.HoweG. T.BrunnerA. M.HelliwellE.NagleM. F.MaC.et al. (2021). Overexpression of SHORT VEGETATIVE PHASE-LIKE (SVL) in Populus delays onset and reduces abundance of flowering in field-grown trees. Hortic. Res.8 (1), 167. doi: 10.1038/s41438-021-00600-4

  • CrossRef
  • Google Scholar

• 51

  GramzowL.TheissenG. (2010). A hitchhiker’s guide to the MADS world of plants. Genome Biol.11 (6), 214. doi: 10.1186/gb-2010-11-6-214

  • CrossRef
  • Google Scholar

• 52

  GramzowL.TheissenG. (2015). Phylogenomics reveals surprising sets of essential and dispensable clades of MIKC(c)-group MADS-box genes in flowering plants. J. Exp. Zool. B. Mol. Dev. Evol.324 (4), 353–362. doi: 10.1002/jez.b.22598

  • CrossRef
  • Google Scholar

• 53

  GreenupA.PeacockW. J.DennisE. S.TrevaskisB. (2009). The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals. Ann. Bot.103 (8), 1165–1172. doi: 10.1093/aob/mcp063

  • CrossRef
  • Google Scholar

• 54

  GregisV.SessaA.ColomboL.KaterM. M. (2006). AGL24, SHORT VEGETATIVE PHASE, and APETALA1 redundantly control AGAMOUS during early stages of flower development in Arabidopsis. Plant Cell18 (6), 1373–1382. doi: 10.1105/tpc.106.041798

  • CrossRef
  • Google Scholar

• 55

  GriffithsS.DunfordR. P.CouplandG.LaurieD. A. (2003). The evolution of CONSTANS-like gene families in barley, rice, and Arabidopsis. Plant Physiol.131 (4), 1855–1867. doi: 10.1104/pp.102.016188

  • CrossRef
  • Google Scholar

• 56

  GuoR.WangB.LinL.ChengG.ZhouS.XieS.et al. (2018). Evolutionary, interaction and expression analysis of floral meristem identity genes in inflorescence induction of the second crop in two-crop-a-year grape culture system. J. Genet.97 (2), 439–451. doi: 10.1007/s12041-018-0929-5

  • CrossRef
  • Google Scholar

• 57

  HalaszJ.HegedusA.KarsaiI.TosakiA.SzalayL. (2021). Correspondence between SOC1 genotypes and time of endodormancy break in peach (Prunus persica L. Batsch) cultivars. Agronomy-Basel11 (7), 1298. doi: 10.3390/agronomy11071298

  • CrossRef
  • Google Scholar

• 58

  HanY.TangA. Y.YuJ. Y.ChengT. R.WangJ.YangW. R.et al. (2019). RcAP1, a homolog of APETALA1, is associated with flower bud differentiation and floral organ morphogenesis in rosa chinensis. Int. J. Mol. Sci.20 (14), 3557. doi: 10.3390/ijms20143557

  • CrossRef
  • Google Scholar

• 59

  HanX.WangD. C.SongG. Q. (2021). Expression of a maize SOC1 gene enhances soybean yield potential through modulating plant growth and flowering. Sci. Rep.11 (1), 12758. doi: 10.1038/s41598-021-92215-x

  • CrossRef
  • Google Scholar

• 60

  HananoS.GotoK. (2011). Arabidopsis TERMINAL FLOWER1 is involved in the regulation of flowering time and inflorescence development through transcriptional repression. Plant Cell23 (9), 3172–3184. doi: 10.1105/tpc.111.088641

  • CrossRef
  • Google Scholar

• 61

  HattaschC.FlachowskyH.KapturskaD.HankeM. V. (2008). Isolation of flowering genes and seasonal changes in their transcript levels related to flower induction and initiation in apple (Malus domestica). Tree Physiol.28 (10), 1459–1466. doi: 10.1093/treephys/28.10.1459

  • CrossRef
  • Google Scholar

• 62

  HeijmansK.MorelP.VandenbusscheM. (2012). MADS-box genes and floral development: the dark side. J. Exp. Bot.63 (15), 5397–5404. doi: 10.1093/jxb/ers233

  • CrossRef
  • Google Scholar

• 63

  HuijserP.SchmidM. (2011). The control of developmental phase transitions in plants. Development138 (19), 4117–4129. doi: 10.1242/dev.063511

  • CrossRef
  • Google Scholar

• 64

  HyunY.RichterR.CouplandG. (2017). Competence to flower: age-controlled sensitivity to environmental cues. Plant Physiol.173 (1), 36–46. doi: 10.1104/pp.16.01523

  • CrossRef
  • Google Scholar

• 65

  IrishV. F. (2010). The flowering of Arabidopsis flower development. Plant J.61 (6), 1014–1028. doi: 10.1111/j.1365-313X.2009.04065.x

  • CrossRef
  • Google Scholar

• 66

  IzawaT. (2021). What is going on with the hormonal control of flowering in plants? Plant J.105 (2), 431–445. doi: 10.1111/tpj.15036

  • CrossRef
  • Google Scholar

• 67

  JeongD.-H.SungS.-K.AnG. (1999). Molecular cloning and characterization of constans-like cDNA clones of the fuji apple. J. Plant Biol.42 (1), 23–31. doi: 10.1007/BF03031143

  • CrossRef
  • Google Scholar

• 68

  JewariaP. K.HanninenH.LiX.BhaleraoR. P.ZhangR. (2021). A hundred years after: endodormancy and the chilling requirement in subtropical trees. New Phytol.231 (2), 565–570. doi: 10.1111/nph.17382

  • CrossRef
  • Google Scholar

• 69

  JiaX. L.ChenY. K.XuX. Z.ShenF.ZhengQ. B.DuZ.et al. (2017). miR156 switches on vegetative phase change under the regulation of redox signals in apple seedlings. Sci. Rep.7 (1), 14223. doi: 10.1038/s41598-017-14671-8

  • CrossRef
  • Google Scholar

• 70

  JiangY.PengJ.WangM.SuW.GanX.JingY.et al. (2019a). The role of ejSPL3, ejSPL4, ejSPL5, and ejSPL9 in regulating flowering in loquat (Eriobotrya japonica lindl.). Int. J. Mol. Sci.21 (1), 248. doi: 10.3390/ijms21010248

  • CrossRef
  • Google Scholar

• 71

  JiangY.PengJ.ZhangZ.LinS.LinS.YangX. (2019b). The role of ejSVPs in flower initiation in eriobotrya japonica. Int. J. Mol. Sci.20 (23), 5933. doi: 10.3390/ijms20235933

  • CrossRef
  • Google Scholar

• 72

  JiangY.PengJ.ZhuY.SuW.ZhangL.JingY.et al. (2019c). The role of ejSOC1s in flower initiation in eriobotrya japonica. Front. Plant Sci.10. doi: 10.3389/fpls.2019.00253

  • CrossRef
  • Google Scholar

• 73

  JiangY.ZhuY.ZhangL.SuW.PengJ.YangX.et al. (2020). EjTFL1 genes promote growth but inhibit flower bud differentiation in loquat. Front. Plant Sci.11. doi: 10.3389/fpls.2020.00576

  • CrossRef
  • Google Scholar

• 74

  JimenezS.Lawton-RauhA. L.ReighardG. L.AbbottA. G.BielenbergD. G. (2009). Phylogenetic analysis and molecular evolution of the dormancy associated MADS-box genes from peach. BMC Plant Biol.9, 81. doi: 10.1186/1471-2229-9-81

  • CrossRef
  • Google Scholar

• 75

  JimenezS.ReighardG. L.BielenbergD. G. (2010). Gene expression of DAM5 and DAM6 is suppressed by chilling temperatures and inversely correlated with bud break rate. Plant Mol. Biol.73 (1-2), 157–167. doi: 10.1007/s11103-010-9608-5

  • CrossRef
  • Google Scholar

• 76

  JulianC.RodrigoJ.HerreroM. (2011). Stamen development and winter dormancy in apricot (Prunus Armeniaca). Ann. Bot.108 (4), 617–625. doi: 10.1093/aob/mcr056

  • CrossRef
  • Google Scholar

• 77

  KagayaH.ItoN.ShibuyaT.KomoriS.KatoK.KanayamaY. (2020). Characterization of FLOWERING LOCUS C homologs in apple as a model for fruit trees. Int. J. Mol. Sci.21 (12). doi: 10.3390/ijms21124562

  • CrossRef
  • Google Scholar

• 78

  KamalN.OchßnerI.SchwandnerA.ViehöverP.HausmannL.TöpferR.et al. (2019). Characterization of genes and alleles involved in the control of flowering time in grapevine. PloS One14 (7), e0214703. doi: 10.1371/journal.pone.0214703

  • CrossRef
  • Google Scholar

• 79

  KennedyA.GeutenK. (2020). The role of FLOWERING LOCUS C relatives in cereals. Front. Plant Sci.11. doi: 10.3389/fpls.2020.617340

  • CrossRef
  • Google Scholar

• 80

  KhanM. R.AiX. Y.ZhangJ. Z. (2014). Genetic regulation of flowering time in annual and perennial plants. Wiley. Interdiscip. Rev. RNA5 (3), 347–359. doi: 10.1002/wrna.1215

  • CrossRef
  • Google Scholar

• 81

  KimS. Y.YuX.MichaelsS. D. (2008). Regulation of CONSTANS and FLOWERING LOCUS T expression in response to changing light quality. Plant Physiol.148 (1), 269–279. doi: 10.1104/pp.108.122606

  • CrossRef
  • Google Scholar

• 82

  KingR. W.EvansL. T. (2003). Gibberellins and flowering of grasses and cereals: prizing open the lid of the “florigen” black box. Annu. Rev. Plant Biol.54, 307–328. doi: 10.1146/annurev.arplant.54.031902.135029

  • CrossRef
  • Google Scholar

• 83

  KingR. W.MoritzT.EvansL. T.MartinJ.AndersenC. H.BlundellC.et al. (2006). Regulation of flowering in the long-day grass Lolium temulentum by gibberellins and the FLOWERING LOCUS T gene. Plant Physiol.141 (2), 498–507. doi: 10.1104/pp.106.076760

  • CrossRef
  • Google Scholar

• 84

  KinoshitaA.RichterR. (2020). Genetic and molecular basis of floral induction in Arabidopsis thaliana. J. Exp. Bot.71 (9), 2490–2504. doi: 10.1093/jxb/eraa057

  • CrossRef
  • Google Scholar

• 85

  KlockoA. L.GoddardA. L.JacobsonJ. R.MagnusonA. C.StraussS. H. (2021). RNAi suppression of LEAFY gives stable floral sterility, and reduced growth rate and leaf size, in field-grown poplars. Plants (Basel)10 (8), 1594. doi: 10.3390/plants10081594

  • CrossRef
  • Google Scholar

• 86

  KlockoA. L.MaC.RobertsonS.EsfandiariE.NilssonO.StraussS. H. (2016). FT overexpression induces precocious flowering and normal reproductive development in Eucalyptus. Plant Biotechnol. J.14 (2), 808–819. doi: 10.1111/pbi.12431

  • CrossRef
  • Google Scholar

• 87

  KobayashiY.KayaH.GotoK.IwabuchiM.ArakiT. (1999). A pair of related genes with antagonistic roles in mediating flowering signals. Science286 (5446), 1960–1962. doi: 10.1126/science.286.5446.1960

  • CrossRef
  • Google Scholar

• 88

  KoshitaY.TakaharaT.OgataT.GotoA. (1999). Involvement of endogenous plant hormones (IAA, ABA, GAs) in leaves and flower bud formation of satsuma mandarin (Citrus unshiu Marc.). Sci. Hortic.79 (3-4), 185–194. doi: 10.1016/S0304-4238(98)00209-X

  • CrossRef
  • Google Scholar

• 89

  KotodaN.HayashiH.SuzukiM.IgarashiM.HatsuyamaY.KidouS.et al. (2010). Molecular characterization of FLOWERING LOCUS T-like genes of apple (Malus x domestica Borkh.). Plant Cell Physiol.51 (4), 561–575. doi: 10.1093/pcp/pcq021

  • CrossRef
  • Google Scholar

• 90

  KotodaN.IwanamiH.TakahashiS.AbeK. (2006). Antisense expression of MdTFL1, a TFL1-like gene, reduces the juvenile phase in apple. J. Am. Soc. Hortic. Sci.131 (1), 74–81. doi: 10.21273/JASHS.131.1.74

  • CrossRef
  • Google Scholar

• 91

  KotodaN.WadaM.KusabaS.Kano-MurakamiY.MasudaT.SoejimaJ. (2002). Overexpression of MdMADS5, an APETALA1-like gene of apple, causes early flowering in transgenic Arabidopsis. Plant Sci.162 (5), 679–687. doi: 10.1016/S0168-9452(02)00024-9

  • CrossRef
  • Google Scholar

• 92

  KrzymuskiM.AndresF.CagnolaJ. I.JangS.YanovskyM. J.CouplandG.et al. (2015). The dynamics of FLOWERING LOCUS T expression encodes long-day information. Plant J.83 (6), 952–961. doi: 10.1111/tpj.12938

  • CrossRef
  • Google Scholar

• 93

  KumarG.AryaP.GuptaK.RandhawaV.AcharyaV.SinghA. K. (2016). Comparative phylogenetic analysis and transcriptional profiling of MADS-box gene family identified DAM and FLC-like genes in apple (Malusx domestica). Sci. Rep.6, 20695. doi: 10.1038/srep20695

  • CrossRef
  • Google Scholar

• 94

  LeeS.KimJ.HanJ. J.HanM. J.AnG. (2004). Functional analyses of the flowering time gene OsMADS50, the putative SUPPRESSOR OF OVEREXPRESSION OF CO 1/AGAMOUS-LIKE 20 (SOC1/AGL20) ortholog in rice. Plant J.38 (5), 754–764. doi: 10.1111/j.1365-313X.2004.02082.x

  • CrossRef
  • Google Scholar

• 95

  LeeJ.LeeI. (2010). Regulation and function of SOC1, a flowering pathway integrator. J. Exp. Bot.61 (9), 2247–2254. doi: 10.1093/jxb/erq098

  • CrossRef
  • Google Scholar

• 96

  LeeJ.OhM.ParkH.LeeI. (2008). SOC1 translocated to the nucleus by interaction with AGL24 directly regulates leafy. Plant J.55 (5), 832–843. doi: 10.1111/j.1365-313X.2008.03552.x

  • CrossRef
  • Google Scholar

• 97

  LiJ.GaoK.YangX.KhanW. U.GuoB.GuoT.et al. (2020). Identification and characterization of the CONSTANS-like gene family and its expression profiling under light treatment in Populus. Int. J. Biol. Macromol.161, 999–1010. doi: 10.1016/j.ijbiomac.2020.06.056

  • CrossRef
  • Google Scholar

• 98

  LiZ.ReighardG. L.AbbottA. G.BielenbergD. G. (2009). Dormancy-associated MADS genes from the EVG locus of peach [Prunus persica (L.) Batsch] have distinct seasonal and photoperiodic expression patterns. J. Exp. Bot.60 (12), 3521–3530. doi: 10.1093/jxb/erp195

  • CrossRef
  • Google Scholar

• 99

  LiZ.-M.ZhangJ.-Z.MeiL.DengX.-X.HuC.-G.YaoJ.-L. (2010). PtSVP, an SVP homolog from trifoliate orange (Poncirus trifoliata L. Raf.), shows seasonal periodicity of meristem determination and affects flower development in transgenic Arabidopsis and tobacco plants. Plant Mol. Biol.74 (1), 129–142. doi: 10.1007/s11103-010-9660-1

  • CrossRef
  • Google Scholar

• 100

  Li-MalletA.RabotA.GenyL. (2016). Factors controlling inflorescence primordia formation of grapevine: their role in latent bud fruitfulness? A review. Botany94 (3), 247–163. doi: 10.1139/cjb-2015-0108

  • CrossRef
  • Google Scholar

• 101

  LinT. Y.WalworthA.ZongX. J.DanialG. H.TomaszewskiE. M.CallowP.et al. (2019). VcRR2 regulates chilling-mediated flowering through expression of hormone genes in a transgenic blueberry mutant. Horticult. Res.6, 96. doi: 10.1038/s41438-019-0180-0

  • CrossRef
  • Google Scholar

• 102

  LiuY. X.HuG. B.LinS. Q.HanZ. H. (2011). Ectopic expression of LFY and AP1 homologues of loquat. Iii. Int. Symposium. Loquat.887, 227–232. doi: 10.17660/ActaHortic.2011.887.37

  • CrossRef
  • Google Scholar

• 103

  LiuY. X.KongJ.LiT. Z.WangY.WangA. D.HanZ. H. (2013a). Isolation and characterization of an APETALA1-like gene from pear (Pyrus pyrifolia). Plant Mol. Biol. Rep.31 (4), 1031–1039. doi: 10.1007/s11105-012-0540-5

  • CrossRef
  • Google Scholar

• 104

  LiuY.LuoC.LiangR.LanM.YuH.GuoY.et al. (2022). Genome-wide identification of the mango CONSTANS (CO) family and functional analysis of two MiCOL9 genes in transgenic Arabidopsis. Front. Plant Sci.13. doi: 10.3389/fpls.2022.1028987

  • CrossRef
  • Google Scholar

• 105

  LiuY.LuoC.ZhangX.-J.LuX.-X.YuH.-X.XieX.-J.et al. (2020a). Overexpression of the mango MiCO gene delayed flowering time in transgenic Arabidopsis. Plant Cell Tissue Organ Culture (PCTOC)143 (1), 219–228. doi: 10.1007/s11240-020-01894-3

  • CrossRef
  • Google Scholar

• 106

  LiuY. X.SongH. W.LiuZ. L.HuG. B.LinS. Q. (2013b). Molecular characterization of loquat EjAP1 gene in relation to flowering. Plant Growth Regul.70 (3), 287–296. doi: 10.1007/s10725-013-9800-0

  • CrossRef
  • Google Scholar

• 107

  LiuZ.WuX.ChengM.XieZ.XiongC.ZhangS.et al. (2020b). Identification and functional characterization of SOC1-like genes in Pyrus bretschneideri. Genomics112 (2), 1622–1632. doi: 10.1016/j.ygeno.2019.09.011

  • CrossRef
  • Google Scholar

• 108

  LiuL.XuanL. J.JiangY. P.YuH. (2021). Regulation by FLOWERING LOCUS T and TERMINAL FLOWER 1 in flowering time and plant architecture. Small. Structures2 (4), 2000125. doi: 10.1002/sstr.202000125

  • CrossRef
  • Google Scholar

• 109

  LiuY. Y.YangK. Z.WeiX. X.WangX. Q. (2016). Revisiting the phosphatidylethanolamine-binding protein (PEBP) gene family reveals cryptic FLOWERING LOCUS T gene homologs in gymnosperms and sheds new light on functional evolution. New Phytol.212 (3), 730–744. doi: 10.1111/nph.14066

  • CrossRef
  • Google Scholar

• 110

  LuedelingE.GirvetzE. H.SemenovM. A.BrownP. H. (2011). Climate change affects winter chill for temperate fruit and nut trees. PloS One6 (5), e20155. doi: 10.1371/journal.pone.0020155

  • CrossRef
  • Google Scholar

• 111

  LunaV.LorenzoE.ReinosoH.TordableM. C.AbdalaG.PharisR. P.et al. (1990). Dormancy in Peach (Prunus persica L.) Flower Buds: I. Floral Morphogenesis and Endogenous Gibberellins at the End of the Dormancy Period. Plant Physiol.93 (1), 20–25. doi: 10.1104/pp.93.1.20

  • CrossRef
  • Google Scholar

• 112

  LunaV.ReinosoH.LorenzoE.BottiniR.AbdalaG. (1991). Dormancy in peach (Prunus persica L.) flower buds. Trees5 (4), 244–246. doi: 10.1007/BF00227532

  • CrossRef
  • Google Scholar

• 113

  LunaV.SorianoM.BottiniR.ShengC.PharisR. (1993). Dormancy in peach (Prunus persica L.) flower buds. III. Levels of endogenous gibberellins, abscisic acid, indole-3- acetic acid, and naringenin during dormancy of peach flower buds. Acta Hortic.329, 4.

  • Google Scholar

• 114

  LymperopoulosP.MsanneJ.RabaraR. (2018). Phytochrome and phytohormones: working in tandem for plant growth and development. Front. Plant Sci.9. doi: 10.3389/fpls.2018.01037

  • CrossRef
  • Google Scholar

• 115

  MaY.XueH.ZhangF.JiangQ.YangS.YueP. T.et al. (2021). The miR156/SPL module regulates apple salt stress tolerance by activating MdWRKY100 expression. Plant Biotechnol. J.19 (2), 311–323. doi: 10.1111/pbi.13464

  • CrossRef
  • Google Scholar

• 116

  MichaelsS. D. (2009). Flowering time regulation produces much fruit. Curr. Opin. Plant Biol.12 (1), 75–80. doi: 10.1016/j.pbi.2008.09.005

  • CrossRef
  • Google Scholar

• 117

  MichaelsS. D.AmasinoR. M. (1999). FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell11 (5), 949–956. doi: 10.1105/tpc.11.5.949

  • CrossRef
  • Google Scholar

• 118

  MichniewiczM.LangA. (1962). Effect of nine different gibberellins on stem elongation and flower formation in cold-requiring and photoperiodic plants grown under non-inductive conditions. Planta58 (5), 549–563. doi: 10.1007/bf01928367

  • CrossRef
  • Google Scholar

• 119

  MimidaN.KotodaN.UedaT.IgarashiM.HatsuyamaY.IwanamiH.et al. (2009). Four TFL1/CEN-like genes on distinct linkage groups show different expression patterns to regulate vegetative and reproductive development in apple (Malus x domestica Borkh.). Plant Cell Physiol.50 (2), 394–412. doi: 10.1093/pcp/pcp001

  • CrossRef
  • Google Scholar

• 120

  MimidaN.SaitoT.MoriguchiT.SuzukiA.KomoriS.WadaM. (2015). Expression of DORMANCY-ASSOCIATED MADS-BOX (DAM)-like genes in apple. Biol. Plantarum.59 (2), 237–244. doi: 10.1007/s10535-015-0503-4

  • CrossRef
  • Google Scholar

• 121

  MohamedR.WangC. T.MaC.ShevchenkoO.DyeS. J.PuzeyJ. R.et al. (2010). Populus CEN/TFL1 regulates first onset of flowering, axillary meristem identity and dormancy release in Populus. Plant J.62 (4), 674–688. doi: 10.1111/j.1365-313X.2010.04185.x

  • CrossRef
  • Google Scholar

• 122

  MoreaE. G.da SilvaE. M.e SilvaG. F.ValenteG. T.Barrera RojasC. H.VincentzM.et al. (2016). Functional and evolutionary analyses of the miR156 and miR529 families in land plants. BMC Plant Biol.16, 40. doi: 10.1186/s12870-016-0716-5

  • CrossRef
  • Google Scholar

• 123

  MossS. M. A.WangT. C.VoogdC.BrianL. A.WuR. M.HellensR. P.et al. (2018). AcFT promotes kiwifruit in vitro flowering when overexpressed and Arabidopsis flowering when expressed in the vasculature under its own promoter. Plant Direct.2 (7), 68. doi: 10.1002/pld3.68

  • CrossRef
  • Google Scholar

• 124

  MullinsM. G. (1968). Regulation of inflorescence growth in cuttings of the grape vine (Vitis vinifera L.). J. Exp. Bot.19 (3), 532–543. doi: 10.1093/jxb/19.3.532

  • CrossRef
  • Google Scholar

• 125

  NiJ.GaoC.ChenM. S.PanB. Z.YeK.XuZ. F. (2015). Gibberellin promotes shoot branching in the perennial woody plant jatropha curcas. Plant Cell Physiol.56 (8), 1655–1666. doi: 10.1093/pcp/pcv089

  • CrossRef
  • Google Scholar

• 126

  NishiyamaS.MatsushitaM. C.YamaneH.HondaC.OkadaK.TamadaY.et al. (2021). Functional and expressional analyses of apple FLC-like in relation to dormancy progress and flower bud development. Tree Physiol.41 (4), 562–570. doi: 10.1093/treephys/tpz111

  • CrossRef
  • Google Scholar

• 127

  OmoriM.ChengC.-C.HsuF.-C.ChenS.-J.YamaneH.TaoR.et al. (2022). Off-season flowering and expression of flowering-related genes during floral bud differentiation of rabbiteye blueberry in a subtropical climate. Sci. Hortic.306, 111458. doi: 10.1016/j.scienta.2022.111458

  • CrossRef
  • Google Scholar

• 128

  OmoriM.YamaneH.LiK.-T.MatsuzakiR.EbiharaS.LiT.-S.et al. (2020). Expressional analysis of FT and CEN genes in a continuously flowering highbush blueberry ‘Blue Muffin’. Acta Hortic.1280), 6. doi: 10.17660/ActaHortic.2020.1280.27

  • CrossRef
  • Google Scholar

• 129

  OmoriM.YamaneH.OsakabeK.OsakabeY.TaoR. (2021). Targeted mutagenesis of CENTRORADIALIS using CRISPR/Cas9 system through the improvement of genetic transformation efficiency of tetraploid highbush blueberry. J. Hortic. Sci. Biotechnol.96 (2), 153–161. doi: 10.1080/14620316.2020.1822760

  • CrossRef
  • Google Scholar

• 130

  PearceS.VanzettiL. S.DubcovskyJ. (2013). Exogenous gibberellins induce wheat spike development under short days only in the presence of VERNALIZATION1. Plant Physiol.163 (3), 1433–1445. doi: 10.1104/pp.113.225854

  • CrossRef
  • Google Scholar

• 131

  PenaL.Martin-TrilloM.JuarezJ.PinaJ. A.NavarroL.Martinez-ZapaterJ. M. (2001). Constitutive expression of Arabidopsis LEAFY or APETALA1 genes in citrus reduces their generation time. Nat. Biotechnol.19 (3), 263–267. doi: 10.1038/85719

  • CrossRef
  • Google Scholar

• 132

  PengJ.HarberdN. P. (1997). Gibberellin deficiency and response mutations suppress the stem elongation phenotype of phytochrome-deficient mutants of Arabidopsis. Plant Physiol.113 (4), 1051–1058. doi: 10.1104/pp.113.4.1051

  • CrossRef
  • Google Scholar

• 133

  PillitteriL. J.LovattC. J.WallingL. L. (2004). Isolation and characterization of LEAFY and APETALA1 homologues from Citrus sinensis L. Osbeck ‘Washington’. J. Am. Soc. Hortic. Sci.129 (6), 846–856. doi: 10.21273/Jashs.129.6.0846

  • CrossRef
  • Google Scholar

• 134

  PinP. A.NilssonO. (2012). The multifaceted roles of FLOWERING LOCUS T in plant development. Plant Cell Environ.35 (10), 1742–1755. doi: 10.1111/j.1365-3040.2012.02558.x

  • CrossRef
  • Google Scholar

• 135

  PortoD. D.BruneauM.PeriniP.AnzanelloR.RenouJ. P.dos SantosH. P.et al. (2015). Transcription profiling of the chilling requirement for bud break in apples: a putative role for FLC-like genes. J. Exp. Bot.66 (9), 2659–2672. doi: 10.1093/jxb/erv061

  • CrossRef
  • Google Scholar

• 136

  PrestonJ. C.HilemanL. C. (2013). Functional evolution in the plant SQUAMOSA-PROMOTER BINDING PROTEIN-LIKE (SPL) gene family. Front. Plant Sci.4. doi: 10.3389/fpls.2013.00080

  • CrossRef
  • Google Scholar

• 137

  PutterillJ.RobsonF.LeeK.SimonR.CouplandG. (1995). The CONSTANS gene of arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell80 (6), 847–857. doi: 10.1016/0092-8674(95)90288-0

  • CrossRef
  • Google Scholar

• 138

  Quesada-TraverC.GuerreroB. I.BadenesM. L.RodrigoJ.RiosG.LloretA. (2020). Structure and expression of bud dormancy-associated MADS-box genes (DAM) in european plum. Front. Plant Sci.11. doi: 10.3389/fpls.2020.01288

  • CrossRef
  • Google Scholar

• 139

  RandouxM.DaviereJ. M.JeauffreJ.ThouroudeT.PierreS.ToualbiaY.et al. (2014). RoKSN, a floral repressor, forms protein complexes with RoFD and RoFT to regulate vegetative and reproductive development in rose. New Phytol.202 (1), 161–173. doi: 10.1111/nph.12625

  • CrossRef
  • Google Scholar

• 140

  ReinosoH.LunaV.DauriíaC.PharisR.BottiniR. (2002a). Dormancy in peach (Prunus persica) flower buds. VI. Effects of gibberellins and an acylcyclohexanedione (trinexapac-ethyl) on bud morphogenesis in field experiments with orchard trees and on cuttings. Can. J. Bot.80, 11. doi: 10.1139/b02-051

  • CrossRef
  • Google Scholar

• 141

  ReinosoH.LunaV.PharisR.BottiniR. (2002b). Dormancy in peach (Prunus persica) flower buds. V. Anatomy of bud development in relation to phenological stage. Can. J. Bot.80, 8. doi: 10.1139/b02-052

  • CrossRef
  • Google Scholar

• 142

  RothkegelK.SanchezE.MontesC.GreveM.TapiaS.BravoS.et al. (2017). 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.37 (12), 1739–1751. doi: 10.1093/treephys/tpx055

  • CrossRef
  • Google Scholar

• 143

  RottmannW. H.MeilanR.SheppardL. A.BrunnerA. M.SkinnerJ. S.MaC.et al. (2000). Diverse effects of overexpression of LEAFY and PTLF, a poplar (Populus) homolog of LEAFY/FLORICAULA, in transgenic poplar and Arabidopsis. Plant J.22 (3), 235–245. doi: 10.1046/j.1365-313x.2000.00734.x

  • CrossRef
  • Google Scholar

• 144

  RyuJ. Y.ParkC. M.SeoP. J. (2011). The floral repressor BROTHER OF FT AND TFL1 (BFT) modulates flowering initiation under high salinity in Arabidopsis. Mol. Cells32 (3), 295–303. doi: 10.1007/s10059-011-0112-9

  • CrossRef
  • Google Scholar

• 145

  SamachA. (2012). “25 - control of flowering,” in Plant biotechnology and agriculture. Eds. AltmanA.HasegawaP. M. (San Diego: Academic Press), 387–404.

  • Google Scholar

• 146

  SamachA.OnouchiH.GoldS. E.DittaG. S.Schwarz-SommerZ.YanofskyM. F.et al. (2000). Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science288 (5471), 1613–1616. doi: 10.1126/science.288.5471.1613

  • CrossRef
  • Google Scholar

• 147

  SasakiR.YamaneH.OokaT.JotatsuH.KitamuraY.AkagiT.et al. (2011). Functional and expressional analyses of PmDAM genes associated with endodormancy in Japanese apricot. Plant Physiol.157 (1), 485–497. doi: 10.1104/pp.111.181982

  • CrossRef
  • Google Scholar

• 148

  SeoE.LeeH.JeonJ.ParkH.KimJ.NohY. S.et al. (2009). Crosstalk between cold response and flowering in Arabidopsis is mediated through the flowering-time gene SOC1 and its upstream negative regulator FLC. Plant Cell21 (10), 3185–3197. doi: 10.1105/tpc.108.063883

  • CrossRef
  • Google Scholar

• 149

  Serrano-BuenoG.Sanchez de Medina HernandezV.ValverdeF. (2021). Photoperiodic signaling and senescence, an ancient solution to a modern problem? Front. Plant Sci.12. doi: 10.3389/fpls.2021.634393

  • CrossRef
  • Google Scholar

• 150

  SheldonC. C.RouseD. T.FinneganE. J.PeacockW. J.DennisE. S. (2000). The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). Proc. Natl. Acad. Sci. U.S.A.97 (7), 3753–3758. doi: 10.1073/pnas.060023597

  • CrossRef
  • Google Scholar

• 151

  SilverstoneA. L.JungH. S.DillA.KawaideH.KamiyaY.SunT. P. (2001). Repressing a repressor: gibberellin-induced rapid reduction of the RGA protein in Arabidopsis. Plant Cell13 (7), 1555–1566. doi: 10.1105/tpc.010047

  • CrossRef
  • Google Scholar

• 152

  SimpsonG. G. (2004). The autonomous pathway: epigenetic and post-transcriptional gene regulation in the control of Arabidopsis flowering time. Curr. Opin. Plant Biol.7 (5), 570–574. doi: 10.1016/j.pbi.2004.07.002

  • CrossRef
  • Google Scholar

• 153

  SinnJ. P.HeldJ. B.VosburgC.KleeS. M.OrbovicV.TaylorE. L.et al. (2021). Flowering Locus T chimeric protein induces floral precocity in edible citrus. Plant Biotechnol. J.19 (2), 215–217. doi: 10.1111/pbi.13463

  • CrossRef
  • Google Scholar

• 154

  SmaczniakC.ImminkR. G.AngenentG. C.KaufmannK. (2012). Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies. Development139 (17), 3081–3098. doi: 10.1242/dev.074674

  • CrossRef
  • Google Scholar

• 155

  SoaresJ. M.WeberK. C.QiuW.StantonD.MahmoudL. M.WuH.et al. (2020). The vascular targeted citrus FLOWERING LOCUS T3 gene promotes non-inductive early flowering in transgenic Carrizo rootstocks and grafted juvenile scions. Sci. Rep.10 (1), 21404. doi: 10.1038/s41598-020-78417-9

  • CrossRef
  • Google Scholar

• 156

  SongG. Q.CarterB. B.ZhongG. Y. (2023). Multiple transcriptome comparisons reveal the essential roles of FLOWERING LOCUS T in floral initiation and SOC1 and SVP in floral activation in blueberry. Front. Genet.14. doi: 10.3389/fgene.2023.1105519

  • CrossRef
  • Google Scholar

• 157

  SongG.-Q.ChenQ. (2018a). Overexpression of the MADS-box gene K-domain increases the yield potential of blueberry. Plant Sci.276, 10. doi: 10.1016/j.plantsci.2018.07.018

  • CrossRef
  • Google Scholar

• 158

  SongG. Q.ChenQ. (2018b). Comparative transcriptome analysis of nonchilled, chilled, and late-pink bud reveals flowering pathway genes involved in chilling-mediated flowering in blueberry. BMC Plant Biol.18 (1), 98. doi: 10.1186/s12870-018-1311-8

  • CrossRef
  • Google Scholar

• 159

  SongG.-q.HanX. (2021). K-domain technology: constitutive expression of a blueberry keratin-like domain mimics expression of multiple MADS-box genes in enhancing maize grain yield. Front. Plant Sci.12 (844). doi: 10.3389/fpls.2021.664983

  • CrossRef
  • Google Scholar

• 160

  SongG. Q.HanX.RynerJ. T.ThompsonA.WangK. (2021). Utilizing MIKC-type MADS-box protein SOC1 for yield potential enhancement in maize. Plant Cell Rep.40 (9), 1679–1693. doi: 10.1007/s00299-021-02722-4

  • CrossRef
  • Google Scholar

• 161

  SongG.-Q.HancockJ. F.KoleC. (2011). “Vaccinium,” in Wild Crop Relatives: Genomic and Breeding Resources: Temperate Fruits (SpringerVerlag Berlin Heidelberg: Springer), 197–221. doi: 10.1007/978-3-642-16057-8_10

  • CrossRef
  • Google Scholar

• 162

  SongY. H.SmithR. W.ToB. J.MillarA. J.ImaizumiT. (2012). FKF1 conveys timing information for CONSTANS stabilization in photoperiodic flowering. Science336 (6084), 1045–1049. doi: 10.1126/science.1219644

  • CrossRef
  • Google Scholar

• 163

  SongG. Q.WalworthA. (2018). An invaluable transgenic blueberry for studying chilling-induced flowering in woody plants. BMC Plant Biol.18 (1), 265. doi: 10.1186/s12870-018-1494-z

  • CrossRef
  • Google Scholar

• 164

  SongG. Q.WalworthA.LinT.ChenQ.HanX.Irina ZahariaL.et al. (2019). VcFT-induced mobile florigenic signals in transgenic and transgrafted blueberries. Hortic. Res.6, 105. doi: 10.1038/s41438-019-0188-5

  • CrossRef
  • Google Scholar

• 165

  SongG. Q.WalworthA.ZhaoD. Y.HildebrandtB.LeasiaM. (2013a). Constitutive expression of the K-domain of a Vaccinium corymbosum SOC1-like (VcSOC1-K) MADS-box gene is sufficient to promote flowering in tobacco. Plant Cell Rep.32 (11), 1819–1826. doi: 10.1007/S00299-013-1495-1

  • CrossRef
  • Google Scholar

• 166

  SongG. Q.WalworthA.ZhaoD. Y.JiangN.HancockJ. F. (2013b). The Vaccinium corymbosum FLOWERING LOCUS T-like gene (VcFT): a flowering activator reverses photoperiodic and chilling requirements in blueberry. Plant Cell Rep.32 (11), 1759–1769. doi: 10.1007/S00299-013-1489-Z

  • CrossRef
  • Google Scholar

• 167

  SreekantanL.ThomasM. R. (2006). 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.33 (12), 1129–1139. doi: 10.1071/Fp06144

  • CrossRef
  • Google Scholar

• 168

  SrinivasanC.DardickC.CallahanA.ScorzaR. (2012). Plum (Prunus domestica) trees transformed with poplar FT1 result in altered architecture, dormancy requirement, and continuous flowering. PloS One7 (7), e40715. doi: 10.1371/journal.pone.0040715

  • CrossRef
  • Google Scholar

• 169

  SrinivasanC.MullinsM. G. (1978). Control of flowering in the grapevine (Vitis vinifera L.): formation of inflorescences in vitro by isolated tendrils. Plant Physiol.61 (1), 127–130. doi: 10.1104/pp.61.1.127

  • CrossRef
  • Google Scholar

• 170

  SuM.WangN.JiangS.FangH.XuH.WangY.et al. (2018). Molecular characterization and expression analysis of the critical floral gene MdAGL24-like in red-fleshed apple. Plant Sci.276, 189–198. doi: 10.1016/j.plantsci.2018.08.021

  • CrossRef
  • Google Scholar

• 171

  SunL.NieT.ChenY.YinZ. (2022). From floral induction to blooming: the molecular mysteries of flowering in woody plants. Int. J. Mol. Sci.23 (18), 10959. doi: 10.3390/ijms231810959

  • CrossRef
  • Google Scholar

• 172

  TadegeM.SheldonC. C.HelliwellC. A.StoutjesdijkP.DennisE. S.PeacockW. J. (2001). Control of flowering time by FLC orthologues in Brassica napus. Plant J.28 (5), 545–553. doi: 10.1046/j.1365-313X.2001.01182.x

  • CrossRef
  • Google Scholar

• 173

  TanF. C.SwainS. M. (2007). Functional characterization of AP3, SOC1 and WUS homologues from citrus (Citrus sinensis). Physiol. Plant131 (3), 481–495. doi: 10.1111/j.1399-3054.2007.00971.x

  • CrossRef
  • Google Scholar

• 174

  TeotiaS.TangG. (2015). To bloom or not to bloom: role of microRNAs in plant flowering. Mol. Plant8 (3), 359–377. doi: 10.1016/j.molp.2014.12.018

  • CrossRef
  • Google Scholar

• 175

  TheissenG.KimJ. T.SaedlerH. (1996). Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes. J. Mol. Evol.43 (5), 484–516. doi: 10.1007/BF02337521

  • CrossRef
  • Google Scholar

• 176

  TiwariS. B.ShenY.ChangH. C.HouY. L.HarrisA.MaS. F.et al. (2010). The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element. New Phytol.187 (1), 57–66. doi: 10.1111/j.1469-8137.2010.03251.x

  • CrossRef
  • Google Scholar

• 177

  TomesS.GunaseelanK.DragulescuM.WangY.-Y.GuoL.SchafferR. J.et al. (2023). A MADS-box gene-induced early flowering pear (Pyrus communis L.) for accelerated pear breeding. Front. Plant Sci.14. doi: 10.3389/fpls.2023.1235963

  • CrossRef
  • Google Scholar

• 178

  TraininT.Bar-Ya’akovI.HollandD. (2013). ParSOC1, a MADS-box gene closely related to Arabidopsis AGL20/SOC1, is expressed in apricot leaves in a diurnal manner and is linked with chilling requirements for dormancy break. Tree Genet. Genomes9 (3), 753–766. doi: 10.1007/s11295-012-0590-8

  • CrossRef
  • Google Scholar

• 179

  TranknerC.LehmannS.HoenickaH.HankeM. V.FladungM.LenhardtD.et al. (2010). Over-expression of an FT-homologous gene of apple induces early flowering in annual and perennial plants. Planta232 (6), 1309–1324. doi: 10.1007/s00425-010-1254-2

  • CrossRef
  • Google Scholar

• 180

  TuanP. A.BaiS.SaitoT.ItoA.MoriguchiT. (2017). Dormancy-associated MADS-box (DAM) and the abscisic acid pathway regulate pear endodormancy through a feedback mechanism. Plant Cell Physiol.58 (8), 1378–1390. doi: 10.1093/pcp/pcx074

  • CrossRef
  • Google Scholar

• 181

  TurckF.FornaraF.CouplandG. (2008). Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu. Rev. Plant Biol.59 (1), 573–594. doi: 10.1146/annurev.arplant.59.032607.092755

  • CrossRef
  • Google Scholar

• 182

  TurnbullC. (2011). Long-distance regulation of flowering time. J. Exp. Bot.62 (13), 4399–4413. doi: 10.1093/jxb/err191

  • CrossRef
  • Google Scholar

• 183

  UbiB. E.SakamotoD.BanY.ShimadaT.ItoA.NakajimaI.et al. (2010). Molecular cloning of dormancy-associated MADS-box gene homologs and their characterization during seasonal endodormancy transitional phases of Japanese pear. J. Am. Soc. Hortic. Sci.135 (2), 174–182. doi: 10.21273/JASHS.135.2.174

  • CrossRef
  • Google Scholar

• 184

  Varkonyi-GasicE.WangT.KarunairetnamS.NainB.WuR.HellensR. P. (2014). Analysis of kiwifruit MADS box genes with potential roles in bud dormancy and flower development. Ii. Int. Symposium. Biotechnol. Fruit Species.1048, 107–112.

  • Google Scholar

• 185

  Varkonyi-GasicE.WangT.VoogdC.JeonS.DrummondR. S. M.GleaveA. P.et al. (2019). Mutagenesis of kiwifruit CENTRORADIALIS-like genes transforms a climbing woody perennial with long juvenility and axillary flowering into a compact plant with rapid terminal flowering. Plant Biotechnol. J.17 (5), 869–880. doi: 10.1111/pbi.13021

  • CrossRef
  • Google Scholar

• 186

  VergaraR.NoriegaX.PérezF. J. (2021). VvDAM-SVPs genes are regulated by FLOWERING LOCUS T (VvFT) and not by ABA/low temperature-induced VvCBFs transcription factors in grapevine buds. Planta253 (2), 31. doi: 10.1007/s00425-020-03561-5

  • CrossRef
  • Google Scholar

• 187

  VoogdC.BrianL. A.WuR. M.WangT. C.AllanA. C.Varkonyi-GasicE. (2022). A MADS-box gene with similarity to FLC is induced by cold and correlated with epigenetic changes to control budbreak in kiwifruit. New Phytol.233 (5), 2111–2126. doi: 10.1111/nph.17916

  • CrossRef
  • Google Scholar

• 188

  VoogdC.WangT.Varkonyi-GasicE. (2015). 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.66 (15), 4699–4710. doi: 10.1093/jxb/erv234

  • CrossRef
  • Google Scholar

• 189

  WadaM.CaoQ. F.KotodaN.SoejimaJ.MasudaT. (2002). Apple has two orthologues of FLORICAULA/LEAFY involved in flowering. Plant Mol. Biol.49 (6), 567–577. doi: 10.1023/A:1015544207121

  • CrossRef
  • Google Scholar

• 190

  WalworthA. E.ChaiB.SongG. Q. (2016). Transcript profile of flowering regulatory genes in vcFT-overexpressing blueberry plants. PloS One11 (6), e0156993. doi: 10.1371/journal.pone.0156993

  • CrossRef
  • Google Scholar

• 191

  WangJ. W.CzechB.WeigelD. (2009). miR156-regulated SPL transcription factors define an endogenous flowering pathway in arabidopsis thaliana. Cell138 (4), 738–749. doi: 10.1016/j.cell.2009.06.014

  • CrossRef
  • Google Scholar

• 192

  WangJ.GaoZ.LiH.JiuS.QuY.WangL.et al. (2020). Dormancy-associated MADS-box (DAM) genes influence chilling requirement of sweet cherries and co-regulate flower development with SOC1 gene. Int. J. Mol. Sci.21 (3), 921. doi: 10.3390/ijms21030921

  • CrossRef
  • Google Scholar

• 193

  WangJ.JiuS.XuY.SabirI. A.WangL.MaC.et al. (2021). SVP-like gene PavSVP potentially suppressing flowering with PavSEP, PavAP1, and PavJONITLESS in sweet cherries (Prunus avium L.). Plant Physiol. Biochem.159, 277–284. doi: 10.1016/j.plaphy.2020.12.013

  • CrossRef
  • Google Scholar

• 194

  WangP.LiuZ.CaoP.LiuX. Y.WuX. P.QiK. J.et al. (2017). PbCOL8 is a clock-regulated flowering time repressor in pear. Tree Genet. Genomes13 (5), 107. doi: 10.1007/s11295-017-1188-y

  • CrossRef
  • Google Scholar

• 195

  WangY.PijutP. M. (2013). Isolation and characterization of a TERMINAL FLOWER 1 homolog from Prunus serotina Ehrh. Tree Physiol.33 (8), 855–865. doi: 10.1093/treephys/tpt051

  • CrossRef
  • Google Scholar

• 196

  WangS.YuanC.DaiY.ShuH.YangT.ZhangC. (2004). Development of flower organs in sweet cherry in shanghai area. Acta Hortic. Sin.31 (3), 357–359.

  • Google Scholar

• 197

  WangL.ZhangL.MaC.XuW.-p.LiuZ.-r.ZhangC.-x.et al. (2016). Impact of chilling accumulation and hydrogen cyanamide on floral organ development of sweet cherry in a warm region. J. Integr. Agric.15 (11), 2529–2538. doi: 10.1016/S2095-3119(16)61341-2

  • CrossRef
  • Google Scholar

• 198

  WangJ.ZhangX. M.YanG. H.ZhouY.ZhangK. C. (2013). Over-expression of the PaAP1 gene from sweet cherry (Prunus avium L.) causes early flowering in Arabidopsis thaliana. J. Plant Physiol.170 (3), 315–320. doi: 10.1016/j.jplph.2012.09.015

  • CrossRef
  • Google Scholar

• 199

  WellsC. E.VendraminE.Jimenez TarodoS.VerdeI.BielenbergD. G. (2015). A genome-wide analysis of MADS-box genes in peach [Prunus persica (L.) Batsch]. BMC Plant Biol.15, 41. doi: 10.1186/s12870-015-0436-2

  • CrossRef
  • Google Scholar

• 200

  WenzelS.FlachowskyH.HankeM.-V. (2013). The Fast-track breeding approach can be improved by heat-induced expression of the FLOWERING LOCUS T genes from poplar (Populus trichocarpa) in apple (Malus × domestica Borkh.). Plant Cell. Tissue Organ Culture. (PCTOC).115 (2), 127–137. doi: 10.1007/s11240-013-0346-7

  • CrossRef
  • Google Scholar

• 201

  WiggeP. A.KimM. C.JaegerK. E.BuschW.SchmidM.LohmannJ. U.et al. (2005). Integration of spatial and temporal information during floral induction in Arabidopsis. Science309 (5737), 1056–1059. doi: 10.1126/science.1114358

  • CrossRef
  • Google Scholar

• 202

  WilkieJ. D.SedgleyM.OlesenT. (2008). Regulation of floral initiation in horticultural trees. J. Exp. Bot.59 (12), 3215–3228. doi: 10.1093/jxb/ern188

  • CrossRef
  • Google Scholar

• 203

  WilligeB. C.GhoshS.NillC.ZourelidouM.DohmannE. M.MaierA.et al. (2007). The DELLA domain of GA INSENSITIVE mediates the interaction with the GA INSENSITIVE DWARF1A gibberellin receptor of Arabidopsis. Plant Cell19 (4), 1209–1220. doi: 10.1105/tpc.107.051441

  • CrossRef
  • Google Scholar

• 204

  WongA. C.HechtV. F.PicardK.DiwadkarP.LaurieR. E.WenJ.et al. (2014). Isolation and functional analysis of CONSTANS-LIKE genes suggests that a central role for CONSTANS in flowering time control is not evolutionarily conserved in Medicago truncatula. Front. Plant Sci.5. doi: 10.3389/fpls.2014.00486

  • CrossRef
  • Google Scholar

• 205

  WoodsD. P.McKeownM. A.DongY.PrestonJ. C.AmasinoR. M. (2016). Evolution of VRN2/ghd7-like genes in vernalization-mediated repression of grass flowering. Plant Physiol.170 (4), 2124–2135. doi: 10.1104/pp.15.01279

  • CrossRef
  • Google Scholar

• 206

  WuR.CooneyJ.TomesS.RebstockR.KarunairetnamS.AllanA. C.et al. (2021). RNAi-mediated repression of dormancy-related genes results in evergrowing apple trees. Tree Physiol.41 (8), 1510–1523. doi: 10.1093/treephys/tpab007

  • CrossRef
  • Google Scholar

• 207

  WuY. M.MaY. J.WangM.ZhouH.GanZ. M.ZengR. F.et al. (2022). Mobility of FLOWERING LOCUS T protein as a systemic signal in trifoliate orange and its low accumulation in grafted juvenile scions. Horticult. Res.9, uhac056. doi: 10.1093/hr/uhac056

  • CrossRef
  • Google Scholar

• 208

  WuG.ParkM. Y.ConwayS. R.WangJ. W.WeigelD.PoethigR. S. (2009). The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell138 (4), 750–759. doi: 10.1016/j.cell.2009.06.031

  • CrossRef
  • Google Scholar

• 209

  WuR.TomesS.KarunairetnamS.TustinS. D.HellensR. P.AllanA. C.et al. (2017a). SVP-like MADS box genes control dormancy and budbreak in apple. Front. Plant Sci.8. doi: 10.3389/fpls.2017.00477

  • CrossRef
  • Google Scholar

• 210

  WuR.WangT.McGieT.VoogdC.AllanA. C.HellensR. P.et al. (2014). Overexpression of the kiwifruit SVP3 gene affects reproductive development and suppresses anthocyanin biosynthesis in petals, but has no effect on vegetative growth, dormancy, or flowering time. J. Exp. Bot.65 (17), 4985–4995. doi: 10.1093/jxb/eru264

  • CrossRef
  • Google Scholar

• 211

  WuR.WangT.WarrenB. A. W.AllanA. C.MacknightR. C.Varkonyi-GasicE. (2017b). Kiwifruit SVP2 gene prevents premature budbreak during dormancy. J. Exp. Bot.68 (5), 1071–1082. doi: 10.1093/jxb/erx014

  • CrossRef
  • Google Scholar

• 212

  XiaoG.LiB.ChenH.ChenW.WangZ.MaoB.et al. (2018). Overexpression of PvCO1, a bamboo CONSTANS-LIKE gene, delays flowering by reducing expression of the FT gene in transgenic Arabidopsis. BMC Plant Biol.18 (1), 232. doi: 10.1186/s12870-018-1469-0

  • CrossRef
  • Google Scholar

• 213

  XuM. L.HuT. Q.ZhaoJ. F.ParkM. Y.EarleyK. W.WuG.et al. (2016b). Developmental Functions of miR156-Regulated SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) Genes in Arabidopsis thaliana. PloS Genet.12 (8). doi: 10.1371/journal.pgen.1006263

  • CrossRef
  • Google Scholar

• 214

  XuF.LiT.XuP. B.LiL.DuS. S.LianH. L.et al. (2016a). DELLA protein e1006263s physically interact with CONSTANS to regulate flowering under long days in Arabidopsis. FEBS Lett.590 (4), 541–549. doi: 10.1002/1873-3468.12076

  • CrossRef
  • Google Scholar

• 215

  YamaguchiN.WinterC. M.WuM. F.KannoY.YamaguchiA.SeoM.et al. (2014). Gibberellin acts positively then negatively to control onset of flower formation in Arabidopsis. Science344 (6184), 638–641. doi: 10.1126/science.1250498

  • CrossRef
  • Google Scholar

• 216

  YamauchiY.OgawaM.KuwaharaA.HanadaA.KamiyaY.YamaguchiS. (2004). Activation of gibberellin biosynthesis and response pathways by low temperature during imbibition of Arabidopsis thaliana seeds. Plant Cell16 (2), 367–378. doi: 10.1105/tpc.018143

  • CrossRef
  • Google Scholar

• 217

  YanL.FuD.LiC.BlechlA.TranquilliG.BonafedeM.et al. (2006). The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc. Natl. Acad. Sci. U.S.A.103 (51), 19581–19586. doi: 10.1073/pnas.0607142103

  • CrossRef
  • Google Scholar

• 218

  YanL. L.LoukoianovA.BlechlA.TranquilliG.RamakrishnaW.SanMiguelP.et al. (2004). The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science303 (5664), 1640–1644. doi: 10.1126/science.1094305

  • CrossRef
  • Google Scholar

• 219

  YanL.LoukoianovA.TranquilliG.HelgueraM.FahimaT.DubcovskyJ. (2003). Positional cloning of the wheat vernalization gene VRN1. Proc. Natl. Acad. Sci. U.S.A.100 (10), 6263–6268. doi: 10.1073/pnas.0937399100

  • CrossRef
  • Google Scholar

• 220

  YanoM.KatayoseY.AshikariM.YamanouchiU.MonnaL.FuseT.et al. (2000). Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the arabidopsis flowering time gene CONSTANS. Plant Cell12 (12), 2473–2483. doi: 10.1105/tpc.12.12.2473

  • CrossRef
  • Google Scholar

• 221

  YarurA.SotoE.LenG.AlmeidaA. M. (2016). The sweet cherry (Prunus avium) FLOWERING LOCUS T gene is expressed during floral bud determination and can promote flowering in a winter-annual Arabidopsis accession. Plant Reprod.29 (4), 311–322. doi: 10.1007/s00497-016-0296-4

  • CrossRef
  • Google Scholar

• 222

  YeJ.GengY.ZhangB.MaoH.QuJ.ChuaN. H. (2014). The Jatropha FT ortholog is a systemic signal regulating growth and flowering time. Biotechnol. Biofuels71, 10. doi: 10.1186/1754-6834-7-91

  • CrossRef
  • Google Scholar

• 223

  YooS. J.ChungK. S.JungS. H.YooS. Y.LeeJ. S.AhnJ. H. (2010). BROTHER OF FT AND TFL1 (BFT) has TFL1-like activity and functions redundantly with TFL1 in inflorescence meristem development in Arabidopsis. Plant J.63 (2), 241–253. doi: 10.1111/j.1365-313X.2010.04234.x

  • CrossRef
  • Google Scholar

• 224

  YuS.GalvãoV. C.ZhangY.-C.HorrerD.ZhangT.-Q.HaoY.-H.et al. (2012). Gibberellin Regulates the Arabidopsis Floral Transition through miR156-Targeted SQUAMOSA PROMOTER BINDING–LIKE Transcription Factors. Plant Cell24 (8), 3320–3332. doi: 10.1105/tpc.112.101014

  • CrossRef
  • Google Scholar

• 225

  ZhangX.AnL.NguyenT. H.LiangH.WangR.LiuX.et al. (2015b). The cloning and functional characterization of peach CONSTANS and FLOWERING LOCUS T homologous genes ppCO and ppFT. PloS One10 (4), e0124108. doi: 10.1371/journal.pone.0124108

  • CrossRef
  • Google Scholar

• 226

  ZhangS.GottschalkC.van NockerS. (2019). Genetic mechanisms in the repression of flowering by gibberellins in apple (Malus x domestica Borkh.). BMC Genomics20 (1), 747. doi: 10.1186/s12864-019-6090-6

  • CrossRef
  • Google Scholar

• 227

  ZhangH.HarryD. E.MaC.YuceerC.HsuC. Y.VikramV.et al. (2010). Precocious flowering in trees: the FLOWERING LOCUS T gene as a research and breeding tool in Populus. J. Exp. Bot.61 (10), 2549–2560. doi: 10.1093/jxb/erq092

  • CrossRef
  • Google Scholar

• 228

  ZhangL.HuY. B.WangH. S.FengS. J.ZhangY. T. (2015a). Involvement of miR156 in the regulation of vegetative phase change in plants. J. Am. Soc. Hortic. Sci.140 (5), 387–395. doi: 10.21273/Jashs.140.5.387

  • CrossRef
  • Google Scholar

• 229

  ZhengJ.MaY.ZhangM.LyuM.YuanY.WuB. (2019). Expression Pattern of FT/TFL1 and miR156-Targeted SPL Genes Associated with Developmental Stages in Dendrobium catenatum. Int. J. Mol. Sci.20 (11), 2725. doi: 10.3390/ijms20112725

  • CrossRef
  • Google Scholar

• 230

  ZhuP.BurneyJ.ChangJ. F.JinZ. N.MuellerN. D.XinQ. C.et al. (2022). Warming reduces global agricultural production by decreasing cropping frequency and yields. Nat. Climate Change12 (11), 1016–101+. doi: 10.1038/s41558-022-01492-5

  • CrossRef
  • Google Scholar

• 231

  ZhuH.ChenP. Y.ZhongS.DardickC.CallahanA.AnY. Q.et al. (2020a). Thermal-responsive genetic and epigenetic regulation of DAM cluster controlling dormancy and chilling requirement in peach floral buds. Hortic. Res.7 (1), 114. doi: 10.1038/s41438-020-0336-y

  • CrossRef
  • Google Scholar

• 232

  ZhuY.KlasfeldS.JeongC. W.JinR.GotoK.YamaguchiN.et al. (2020b). TERMINAL FLOWER 1-FD complex target genes and competition with FLOWERING LOCUS T. Nat. Commun.11 (1), 5118. doi: 10.1038/s41467-020-18782-1

  • CrossRef
  • Google Scholar

• 233

  ZhuL. H.LiX. Y.WelanderM. (2008). Overexpression of the Arabidopsis gai gene in apple significantly reduces plant size. Plant Cell Rep.27 (2), 289–296. doi: 10.1007/s00299-007-0462-0

  • CrossRef
  • Google Scholar

• 234

  ZongX.ZhangY.WalworthA.TomaszewskiE. M.CallowP.ZhongG. Y.et al. (2019). Constitutive expression of an apple FLC3-like gene promotes flowering in transgenic blueberry under nonchilling conditions. Int. J. Mol. Sci.20 (11), 2775. doi: 10.3390/ijms20112775

  • CrossRef
  • Google Scholar

• 235

  ZuoX.XiangW.ZhangL.GaoC.AnN.XingL.et al. (2021). Identification of apple TFL1-interacting proteins uncovers an expanded flowering network. Plant Cell Rep.40 (12), 2325–2340. doi: 10.1007/s00299-021-02770-w

  • CrossRef
  • Google Scholar