ReviewCommon mechanisms regulate flowering and dormancy
Introduction
In most temperate perennial plants, light and temperature regulate flowering and dormancy. Based on this simple observation, several groups have hypothesized that similar mechanisms regulate both processes [1], [2], [3]. Likewise, several excellent reviews have directly or indirectly discussed possible mechanisms that relate to this hypothesis [4], [5], [6]. This review will discuss recent findings on the regulation of bud dormancy and flowering that are beginning to provide mechanistic support of this hypothesis.
Due to its importance in plant reproduction, extensive research has been conducted which has identified many of the environmental controls and genes involved in regulating flowering. Indeed there are numerous in-depth reviews on this process in both annual dicot and monocot plants [7], [8], [9], [10], [11], as well as in perennial trees [12], [13]. Flowering occurs when meristems receive developmental and or environmental signals that cause the meristem to develop into flowers. These meristems may originally be predestined to flower upon growth, or they may initially be actively growing vegetative meristems that transition to floral meristems. In either case, induction of two key genes appear to initiate a cascade of events that alters the development of organ primordia within the meristem so that sepals, petals, pistils, and stamen are produced rather than leaves and maintenance of an undifferentiated core of cells at the center of the meristem. In the well-studied systems of rice (Oryza sativa), poplar (Populus ssp.), Citrus ssp., and arabidopsis (Arabidopsis thaliana), very similar genes and signaling networks appear to regulate flowering although arguably most of the research has been done on the winter annual arabidopsis, and thus unless noted otherwise, generalizations will refer to floral regulation in this plant.
There are many genes and signals that regulate flowering, most of which converge on FLOWERING LOCUS T (FT) (Fig. 1). FT has been touted as an essential component of the graft transmissible florigen whose existence was long hypothesized [8]. FT is mostly expressed in mature leaf tissue in response to floral promoting environmental conditions; however there is evidence for its expression in young leaves in the shoot apices, and in dormant bud tissue [14], [15]. Leaf expressed FT is known to be phloem-transmissible and is transported to the meristem where it initiates floral morphogenesis.
The genes that initiate the developmental cascade towards flowering are APETELA1 (AP1) and LEAFY (LFY) [16], [17]. AP1 is directly induced by FT [18], and LFY is directly induced by SUPPRESOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) [19]. In turn, both FT and SOC1 are positively regulated by CONSTANS (CO) [20], and both are negatively regulated by the MADS-box transcription factor FLOWERING LOCUS C (FLC) [21], [22], [23]. CO is in turn regulated by light through the various genes encoding components that make up the circadian clock and by PHYTOCHROME A (PHYA) [24].
Environmental and developmental signals that include aspects of chromatin remodeling and response to extended cold temperatures needed for vernalization (the process through which seeds and sometimes buds “remember” winter conditions and become competent to flower in the following spring) also regulate FT [25], [26]. FT expression is also suppressed by another MADs-box transcription factor called SHORT VEGETATIVE PHASE (SVP) [27]. Like FLC, SVP binds to various regulatory sequences within the FT gene and inhibits its expression. However, SVP is primarily involved in ambient temperature regulation of FT [27] whereas FLC plays a more prominent role in the vernalization response.
With the exception of FLC, all plants appear to have functional homologues to these floral regulatory genes. In the two best characterized perennial model species, poplar and leafy spurge, there are homologues to genes related to FLC, specifically, MADS AFFECTING FLOWERING 2 (MAF2). It is also noteworthy that the FT gene family is expanded in perennials such as poplar [28]. However, there are differences such as altered responses of FT to CO in short day flowering rice relative to long day flowering arabidopsis [29]. This suggests that although similar genes may be involved in flowering in long day and short day plants, the precise environmental regulation and timing of the interaction among these regulatory components may be different between species.
Bud dormancy in temperate perennials is a well-studied phenomenon at the physiological level [1], [4], [30], but the molecular and genetic components of the signaling networks regulating dormancy are as yet poorly described (relative to flowering). Bud dormancy is complicated by the fact that buds may fail to grow due to a number of interacting developmental and physiological processes, and that buds of some perennials may be dormant at formation, while others may be actively growing and then transition to a dormant state. There also appears to be differences in dormancy status and responses depending on where the buds are located on the plant, and if the buds are floral or vegetative.
Precise definitions of dormancy processes such as those described by Lang can mitigate these complicating factors to some extent [31] (Fig. 2). In this system, dormancy states could be separated into paradormancy by which buds are prevented from growing due to signals produced in distal parts of the plant. In most cases, auxin and other signals regulate paradormancy. Paradormancy has also been described as correlative inhibition or apical dominance. There are several excellent reviews of the signals regulating this type of dormancy [32], [33]. Buds may also be characterized as ecodormant. Harsh environmental conditions prevent bud growth during ecodormancy. For example, buds may cease growth during periods of drought, low temperatures, or in some cases short day lengths. However, ecodormant buds will grow immediately upon resumption of growth-conducive conditions. In the early autumn in most temperate climates, the buds of many perennial plants will become endodormant. Endodormant buds will have greatly delayed and often reduced grow rates relative to non-dormant buds when the plant is placed in growth-conducive conditions.
Short day lengths promote endodormancy in plants such as poplar while in others such as apples and leafy spurge, short periods of cold temperature induce endodormancy, while yet others including dogwood, response to cold and light is ecotype dependent [34], [35], [36], [37]. It usually requires an extended cold or drought treatment, akin to vernalization, to break endodormancy and reinstate growth-competency to the buds. The similarities between the environmental signals regulating endodormancy induction and release and those regulating flowering and vernalization were the first clues that signaling mechanisms might be shared between these processes [2]. We are only beginning to identify genes and molecular signaling processes regulating endodormancy induction and release. So far, evidence exists for only two gene families in altering endodormancy. One set of genes include FT and a closely related gene named CENTRORADIALIS (CEN) for which direct or indirect over-expression in poplar was associated with failure of buds to enter endodormancy following dormancy-inducing short day conditions [15], [38]. The other set of genes have been collectively named DORMANCY ASSOCIATED MADS-BOX (DAM) genes. DAM genes comprise a small gene family in poplar and deletion of a locus containing six DAM genes in peach produces trees which have terminal buds that are incapable of going into endodormancy under short day conditions [39], [40]. DAM genes have also been cloned and expression analysis has linked them to endodormancy induction and release in peach, poplar, apricot, raspberry, and leafy spurge [14], [34], [41], [42], [43].
Section snippets
Circadian regulation of endodormancy and flowering, a likely connection
Because perception of day length appears to play a role in both flowering and endodormancy induction in some plants, the genes and processes responsible for perceiving and disseminating these day length signals likely control both these developmental processes. This system has been dubbed the “circadian clock,” and both light and temperature influence the timing and impact of circadian clock gene expression. Many of the circadian clock genes were discovered due to their impact on flower time
Hormonal regulation of endodormancy and flowering
GA is required for initiation of flowering under short day conditions [83], through regulation of SOC1 and LFY [84], [85]. Indeed, some GA deficient mutants cannot flower at all under short day conditions. However, over-expression of FT in these mutants allows flowering suggesting that GA acts at least partially upstream of the induction of FT [86]. Abscisic acid (ABA) is often antagonistic to GA. Thus, it is not surprising that ABA has been shown to inhibit floral formation. Interestingly,
Conclusion
It is not surprising that many circadian response genes are regulated differentially during dormancy and flowering transitions. After all, differential day lengths are a common trigger for both dormancy and flowering transitions. However, studies on PHYA over-expressing plants clearly indicate some light sensing proteins can directly impact dormancy and flowering outside the circadian regulatory pathway. More studies are needed to identify the mechanisms through which circadian regulated genes
Acknowledgments
I would like to thank all those including Dr. Antje Rhode, Dr. Maria Eriksson, Dr. Michael Campbell, and Dr. Christian van der Schoot who have read and commented on this and/or previous versions of the manuscript.
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