A physiological overview of the genetics of flowering time control

Physiological studies on flowering time control have shown that plants integrate several environmental signals. Predictable factors, such as day length and vernalization, are regarded as 'primary', but clearly interfere with, or can even be substituted by, less predictable factors. All plant parts participate in the sensing of these interacting factors. In the case of floral induction by photoperiod, long-distance signalling is known to occur between the leaves and the shoot apical meristem (SAM) via the phloem. In the long-day plant, Sinapis alba, this long-distance signalling has also been shown to involve the root system and to include sucrose, nitrate, glutamine and cytokinins, but not gibberellins. In Arabidopsis thaliana, a number of genetic pathways controlling flowering time have been identified. Models now extend beyond 'primary' controlling factors and show an ever-increasing number of cross-talks between pathways triggered or influenced by various environmental factors and hormones (mainly gibberellins). Most of the genes involved are preferentially expressed in meristems (the SAM and the root tip), but, surprisingly, only a few are expressed preferentially or exclusively in leaves. However, long-distance signalling from leaves to SAM has been shown to occur in Arabidopsis during the induction of flowering by long days. In this review, we propose a model integrating physiological data and genes activated by the photoperiodic pathway controlling flowering time in early-flowering accessions of Arabidopsis. This model involves metabolites, hormones and gene products interacting as long- or short-distance signalling molecules.     

Photoperiodic flowering of Arabidopsis: integrating genetic and physiological approaches to characterization of the floral stimulus

In many plants the transition from vegetative growth to flowering is controlled by environmental cues. One of these cues is day length or photoperiod, which synchronizes flowering of many species with the changing seasons. Recently, advances have been made in understanding the molecular mechanisms that confer photoperiodic control of flowering and, in particular, how inductive events occurring in the leaf, where photoperiod is perceived, are linked to floral evocation that takes place at the shoot apical meristem. We discuss recent data obtained using molecular genetic approaches on the function of regulatory proteins that control flowering time in Arabidopsis thaliana. These data are compared with the results of physiological analyses of the floral transition, which were performed in a range of species and directed towards identification of the transmitted floral singals.     

Cytokinin promotes flowering of Arabidopsis via transcriptional activation of the FT paralogue TSF

Cytokinins are involved in many aspects of plant growth and development, and physiological evidence also indicates that they have a role in floral transition. In order to integrate these phytohormones into the current knowledge of genetically defined molecular pathways to flowering, we performed exogenous treatments of adult wild type and mutant Arabidopsis plants, and analysed the expression of candidate genes. We used a hydroponic system that enables synchronous growth and flowering of Arabidopsis, and allows the precise application of chemicals to the roots for defined periods of time. We show that the application of N⁶‐benzylaminopurine (BAP) promotes flowering of plants grown in non‐inductive short days. The response to cytokinin treatment does not require FLOWERING LOCUS T (FT), but activates its paralogue TWIN SISTER OF FT (TSF), as well as FD, which encodes a partner protein of TSF, and the downstream gene SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1). Treatment of selected mutants confirmed that TSF and SOC1 are necessary for the flowering response to BAP, whereas the activation cascade might partially act independently of FD. These experiments provide a mechanistic basis for the role of cytokinins in flowering, and demonstrate that the redundant genes FT and TSF are differently regulated by distinct floral‐inducing signals.     

SQUAMOSA‐PROMOTER BINDING PROTEIN 1 initiates flowering in Antirrhinum majus through the activation of meristem identity genes

The degree to which developmental genetic pathways are conserved across distantly related organisms is a major question in biology. In Arabidopsis thaliana (L.) Heynh., inflorescence development is initiated in response to a combination of external and internal floral inductive signals that are perceived across the whole plant, but are integrated within the shoot apical meristem. Recently, it was demonstrated that SQUAMOSA‐PROMOTER BINDING PROTEIN (SBP)‐box proteins regulate A. thaliana flowering time by mediating signals from the autonomous and photoperiod pathways, and by directly activating key genes involved in inflorescence and floral meristem identity, including FRUITFULL (FUL), APETALA1 (AP1) and LEAFY (LFY). In the distantly related core eudicot species Antirrhinum majus L., paralogous SBP‐box proteins SBP1 and SBP2 have likewise been implicated in regulating the AP1 ortholog SQUAMOSA (SQUA). To test the hypothesis that SBP‐box genes are also involved in the floral induction of A. majus, we used a reverse genetic approach to silence SBP1. SBP1‐silenced lines are late to nonflowering, and show reduced apical dominance. Furthermore, expression and sequence analyses suggest that the SBP1‐mediated transition to flowering occurs through the positive regulation of FUL/LFY homologs. Together, these data outline the utility of virus‐induced gene silencing in A. majus, and provide new insight into the conservation of flowering time genetic pathways across core eudicots.     

Unravelling proximate cues of mass flowering in the tropical forests of South‐East Asia from gene expression analyses

Elucidating the physiological mechanisms of the irregular yet concerted flowering rhythm of mass flowering tree species in the tropics requires long‐term monitoring of flowering phenology, exogenous and endogenous environmental factors, as well as identifying interactions and dependencies among these factors. To investigate the proximate factors for floral initiation of mast seeding trees in the tropics, we monitored the expression dynamics of two key flowering genes, meteorological conditions and endogenous resources over two flowering events of Shorea curtisii and Shorea leprosula in the Malay Peninsula. Comparisons of expression dynamics of genes studied indicated functional conservation of FLOWERING LOCUS T (FT) and LEAFY (LFY) in Shorea. The genes were highly expressed at least 1 month before anthesis for both species. A mathematical model considering the synergistic effect of cool temperature and drought on activation of the flowering gene was successful in predicting the observed gene expression patterns. Requirement of both cool temperature and drought for floral transition suggested by the model implies that flowering phenologies of these species are sensitive to climate change. Our molecular phenology approach in the tropics sheds light on the conserved role of flowering genes in plants inhabiting different climate zones and can be widely applied to dissect the flowering processes in other plant species.     

FLC调控植物成花的分子机制研究新进展

FLC是植物成花关键抑制因子, 主要通过结合到其下游2个关键的成花促进基因(FT和SOC1)启动子上而抑制二者的表达。此外, 还可以与其它调控因子结合调控开花。然而, 关于FLC在成花调控中的具体分子机制仍需深入研究。该文主要结合8条成花调控遗传途径, 梳理近年来与FLC相关的新进展, 并展望了未来的研究方向。     

蝴蝶兰花发育的分子生物学研究进展

蝴蝶兰花非常独特且高度进化,如萼片瓣化、瓣片特化为唇瓣、雌雄蕊合生成合蕊柱及子房发育须由授粉启动等,是单子叶植物花发育研究的理想材料。近年来蝴蝶兰花发育分子生物学取得了重要进展。该文就近年来国内外有关蝴蝶兰开花转换及花器官发育相关基因研究以及B类基因与兰花花被的进化发育关系方面的研究进展进行综述。研究表明:MADS基因在蝴蝶兰开花转换及花器官发育过程中起重要作用,推测其中的DEF(DE-FICIENS)-like基因早期经过2轮复制,形成了4类不同的DEF-like基因,进而决定兰花花被属性。蝴蝶兰花发育分子生物学的深入研究,将极大地利于通过基因工程手段提高蝴蝶兰花品质如花色改良及花期调控等,推动分子育种进程。     

New insights into gibberellin signaling in regulating flowering in Arabidopsis

In angiosperms,floral transition is a key developmental transition from the vegetative to reproductive growth,and requires precise regulation to maximize the reproductive success.A complex regulatory network governs this transition through integrating flowering pathways in response to multiple exogenous and endogenous cues.Phytohormones are essential for proper plant developmental regulation and have been extensively studied for their involvement in the floral transition.Among various phytohormones,gibberellin(GA)plays a major role in affecting flowering in the model plant Arabidopsis thaliana.The GA pathway interact with other flowering genetic pathways and phytohormone signaling pathways through either DELLA proteins or mediating GA homeostasis.In this review,we summarize the recent advances in understanding the mechanisms of DELLA-mediated GA pathway in flowering time control in Arabidopsis,and discuss its possible link with other phytohormone pathways during the floral transition.     

What is going on with the hormonal control of flowering in plants?

Molecular genetic studies using Arabidopsis thaliana as a model system have overwhelmingly revealed many important molecular mechanisms underlying the control of various biological events, including floral induction in plants. The major genetic pathways of flowering have been characterized in-depth, and include the photoperiod, vernalization, autonomous and gibberellin pathways. In recent years, novel flowering pathways are increasingly being identified. These include age, thermosensory, sugar, stress and hormonal signals to control floral transition. Among them, hormonal control of flowering except the gibberellin pathway is not formally considered a major flowering pathway per se, due to relatively weak and often pleiotropic genetic effects, complex phenotypic variations, including some controversial ones. However, a number of recent studies have suggested that various stress signals may be mediated by hormonal regulation of flowering. In view of molecular diversity in plant kingdoms, this review begins with an assessment of photoperiodic flowering, not in A. thaliana, but in rice (Oryza sativa); rice is a staple crop for human consumption worldwide, and is a model system of short-day plants, cereals and breeding crops. The rice flowering pathway is then compared with that of A. thaliana. This review then aims to update our knowledge on hormonal control of flowering, and integrate it into the entire flowering gene network.     

Floral transition mutants in Arabidopsis

An inventory of genetic differences in flowering time in Arabidopsis is presented and discussed. Many genes influence the transition to flowering in a quantitative way. Two groups of mutants and natural variants can be distinguished: those that are responsive to environmental factors and those that are less responsive or unresponsive. It is possible that all late/early-flowering mutants isolated to date carry a mutation with an effect, either promotive or repressive, on a floral repressor. The interaction between light perception and flowering has been studied by analysis of phytochrome- and cryptochrome-deficient mutants, which showed that phyA and probably also cryptochrome have a promotive role in flowering, whereas phyB and other stable phytochromes have an inhibitory role. A circadian rhythm is important in establishing daylength sensitivity, as was shown by the phenotype of the elf 3 mutants.     

Overexpression of a Kunitz-type trypsin inhibitor (AtKTI1) causes early flowering in Arabidopsis

An early flowering mutant of Arabidopsis, elf32-D was isolated from activation tagging screening. The mutant flowered earlier than wild type under both long day and short day conditions. The mutant phenotype was caused by overexpression of a Kunitz-type trypsin inhibitor gene (AtKTI1). The expression of AtKTI1 was detected in leaves, flowers, siliques and roots. In the vegetative state, no change of flowering integrator gene expression was observed for AtKTI1 overexpressing plants. In contrast, at the reproductive stage, its overexpression resulted in the down-regulation of FLC, a strong floral repressor which integrates the autonomous and vernalization pathways and also the up-regulation of FT and AP1, which are downstream floral integrator genes. It is probable that the AtKTI1 overexpression inhibits components of the flowering signaling pathway upstream of FLC, eventually regulating expression of FLC, or causing perturbations in plant metabolism and thus indirectly affecting flowering.     

Florigen goes molecular: Seventy years of the hormonal theory of flowering regulation

As early as in 1936, the comprehensive studies of flowering led M.Kh. Chailakhyan to the concept of florigen, a hormonal floral stimulus, and let him establish several characteristics of this stimulus. These studies set up for many years the main avenues for research into the processes that control plant flowering, and the notion of florigen became universally accepted by scientists worldwide. The present-day evidence of genetic control of plant flowering supports the idea that florigen participates in floral signal transduction. The recent study of arabidopsis plants led the authors to conclusion that the immediate products of the gene FLOWERING LOCUS I, its mRNA and/or protein, move from an induced leaf into the shoot apex and evoke flowering therein.     

The quest for florigen: a review of recent progress

The photoperiodic induction of flowering is a systemic process requiring translocation of a floral stimulus from the leaves to the shoot apical meristem. In response to this stimulus, the apical meristem stops producing leaves to initiate floral development; this switch in morphogenesis involves a change in the identity of the primordia initiated and in phyllotaxis. The physiological study of the floral transition has led to the identification of several putative floral signals such as sucrose, cytokinins, gibberellins, and reduced N-compounds that are translocated in the phloem sap from leaves to the shoot apical meristem. On the other hand, the genetic approach developed more recently in Arabidopsis thaliana allowed the discovery of many genes that control flowering time. These genes function in 'cascades' within four promotive pathways, the 'photoperiodic', 'autonomous', 'vernalization', and 'gibberellin' pathways, which all converge on the 'integrator' genes SUPPRESSOR OF OVEREXPRESSION OF CO 1 (SOC1) and FLOWERING LOCUS T (FT). Recently, several studies have highlighted a role for a product of FT as a component of the floral stimulus or 'florigen'. These recent advances and the proposed mode of action of FT are discussed here.     

Reduction of the geomagnetic field delays Arabidopsis thaliana flowering time through downregulation of flowering‐related genes

Variations in magnetic field (MF) intensity are known to induce plant morphological and gene expression changes. In Arabidopsis thaliana Col‐0, near‐null magnetic field (NNMF, i.e., <100 nT MF) causes a delay in the transition to flowering, but the expression of genes involved in this response has been poorly studied. Here, we showed a time‐course quantitative analysis of the expression of both leaf (including clock genes, photoperiod pathway, GA20ox, SVP, and vernalization pathway) and floral meristem (including GA2ox, SOC1, AGL24, LFY, AP1, FD, and FLC) genes involved in the transition to flowering in A. thaliana under NNMF. NNMF induced a delayed flowering time and a significant reduction of leaf area index and flowering stem length, with respect to controls under geomagnetic field. Generation experiments (F₁‐ and F₂‐NNMF) showed retention of flowering delay. The quantitative expression (qPCR) of some A. thaliana genes expressed in leaves and floral meristem was studied during transition to flowering. In leaves and flowering meristem, NNMF caused an early downregulation of clock, photoperiod, gibberellin, and vernalization pathways and a later downregulation of TSF, AP1, and FLC. In the floral meristem, the downregulation of AP1, AGL24, FT, and FLC in early phases of floral development was accompanied by a downregulation of the gibberellin pathway. The progressive upregulation of AGL24 and AP1 was also correlated to the delayed flowering by NNMF. The flowering delay is associated with the strong downregulation of FT, FLC, and GA20ox in the floral meristem and FT, TSF, FLC, and GA20ox in leaves. Bioelectromagnetics. 39:361–374, 2018. © 2018 The Authors. Bioelectromagnetics Published by Wiley Periodicals, Inc.     

The gigas mutant in pea is deficient in the floral stimulus

Identification of a gene acting in the floral stimulus pathway should provide a basis for determining the identity of this elusive substance. Our tests indicate the Gi (gigas) gene in pea (Pisum sativum L.) acts in this manner. The gigas mutant was selected by Dl M. Vassiteva following gamma radiation of the late flowering, quantitative long day cultivar Virtus. The gigas trait showed single gene recessive inheritance and the mutant allele was symbolised gi consistent with our preliminary report. Gigas plants were later flowering than the initial line in all conditions tested and they showed an enhanced response to photoperiod and vernalisation. Unvernalised gigas plants did not flower under a 24-h photoperiod comprising 8 h of daylight and 16 h of weak (3μmol m^?2 s^?1) incandescent light and they took on a phenotype similar to the vegl (vegetative) mutant in pea. However, genetic tests showed the two mutants were not allelic. Three or four weeks vernalisation at 4^?C resulted in 100% flowering of gigas plants under the 24-h photoperiod. Applied gibberellin A₃ inhibited flowering in gigas plants given partial cold induction. Grafting studies showed the promotive effect of vernalisation occurred in the shoot. Grafting studies were also used to examine the physiological basis of delayed flowering in the gigas mutant. These studies indicated that gigas plants produced normal levels of flower inhibitor and they responded in a normal manner to the floral stimulus, Reciprocal grafts were made between the gigas mutant and the wild-type initial line. Under the 24-h photoperiod, either a wild-type root-stock with cotyledons or a wild-type shoot induced flowering in a gigas graft partner. However, under a 9-h photoperiod, flowering was only induced if the wild-type partner possessed both roots and a shoot. We conclude that gigas plants are deficient in the floral stimulus or a precursor which can be supplied across a graft union by a wild-type donor. Of the 12 major flowering genes known in pea, Gi is the first found to act on the synthesis pathway for the floral stimulus.