Multiple Pathways in the Decision to Flower: Enabling, Promoting, and Resetting

Abstract

At a certain point in their life cycle, annual plants undergo a major developmental transition and switch from vegetative to reproductive development. This process is rarely reversible, and ensuring that the timing of this transition is optimal for pollination and seed development is a major factor in reproductive success. Physiological and genetic analysis of flowering has shown that multiple environmental and endogenous inputs influence the timing of the switch. The molecular identity of these different inputs is being dissected using molecular genetic approaches in Arabidopsis. The multiple pathways quantitatively regulate an overlapping set of common targets, the floral pathway integrators, whose activities convert the shoot apical meristem to a reproductive fate. An emerging idea is that changing the predominance of these input pathways could account for much of the plasticity and diversity of flowering time control within and between plant species (Simpson and Dean, 2002). During the last few years, the data relevant to a molecular understanding of flowering time control have increased rapidly, making it unwieldy to comprehensively review the field. In addition, there have been numerous and excellent recent reviews on various aspects of flowering time control (Mouradov et al., 2002; Ratcliffe and Riechmann, 2002; Simpson and Dean, 2002; Henderson et al., 2003; Yanovsky and Kay, 2003). To complement these, we have chosen, in this review, to group genes involved in flowering time into pathways that enable the floral transition and those that promote it. We also discuss the role of genes defined through early-flowering mutants. Are they specific floral repressors or more global regulators needed to reset patterns of gene expression? Pathways That Enable or Promote the Floral Transition Determine Flowering Time. The different pathways are grouped into those that promote and those that enable the floral transition. The enabling pathways regulate the ability of the meristem to respond to floral promotive signals from different environmental and endogenous cues. Pathways That Enable the Floral Transition. A central regulator of the enabling pathways is the floral repressor FLC. High levels of FLC repress the activity of the floral pathway integrators, and this antagonizes their activation by floral promotion pathways. Many genes are involved in regulating FLC expression. FCA, FY, FVE, FPA, and vernalization repress FLC (FLD and LD are not included here because they are not required in all genotypes). FRI, VIP3/4, ESD4, and EFS upregulate FLC. TFL1 and SVP also may antagonize the activation of the floral pathway integrators but are not included here because their regulation and interaction with FLC are unclear. This concept of pathways that enable the floral transition emerged from the analysis of double and triple combinations of mutants from the classically defined photoperiod, gibberellin (GA), and autonomous pathways (Reeves and Coupland, 2001). Single autonomous pathway mutants (fca-1), which had high levels of FLC, flowered much later than single photoperiod pathway (constans-2 [co-2]) or GA pathway (ga1-3) mutants under long-day conditions. Under the same conditions, co-2 ga1-3 double mutants (in which FCA is active) flowered extremely late, if they flowered at all, and were later flowering than co-2 fca-1 and ga1-3 fca-1. Therefore, FCA activity by itself has little promotive effect on flowering time. However, if FCA activity is absent and FLC levels are high, the plant does not respond as well to promotive flowering signals. The pathways that enable the floral transition could be likened to the control of a sluice gate in a lock on a canal. The plant is like a boat waiting to move from one lock to the next (vegetative to reproductive development). The floral repressors act as the gate itself, inhibiting the passage of water (floral promotion) into the lock. However, there are multiple controls that can open or close the sluice gate, and their combined action determines how high the gate rises and thus how much water is permitted to flow through. It is the water itself that allows the boat to move on to the next lock, but how long the water takes reach the right level is determined by the control of the sluice gate. FLC is a MADS box transcriptional regulator, expressed predominantly in shoot and root apices (Michaels and Amasino, 2000), that acts to quantitatively repress flowering (Michaels and Amasino, 1999a; Sheldon et al., 1999) through repression of the floral pathway integrators FT, SOC1, and LFY (Nilsson et al., 1998; Kardailsky et al., 1999; Kobayashi et al., 1999; Blaézquez and Weigel, 2000; Lee et al., 2000; Samach et al., 2000). FLC plays a central role in vernalization requirement and response. Arabidopsis mutants and that a vernalization requirement have increased FLC and plants have FLC levels et al., and Amasino, et al., 2002). of FLC in flowering in which is vernalization but in plant