The Transition to Flowering

Abstract

The general body plan of plants is established during embryogenesis, when the undifferentiated meristematic regions of root and shoot are set aside. However, much of plant development occurs postembryonically, through the reiterative production of organ primordia at the shoot apical meristem (SAM). In most species, the SAM initially gives rise to vegetative organs such as leaves, but at some point the SAM makes the transition to reproductive development and the production of flowers. This change in the developmental fate of primordia initiated at the SAM is controlled by environmental and endogenous signals (Bernier, 1988; McDaniel et al., 1992). However, unlike many developmental transitions in animals, the SAM of plants is not irreversibly “committed” to reproductive development once flowering commences. In some species and genotypes under certain environmental conditions, leafy shoots are formed after flowers in a phenomenon known as inflorescence reversion (see, e.g., Battey and Lyndon, 1990; Pouteau et al., 1997). This observation implies that the genes and processes involved in the transition to flowering are required to both initiate and maintain reproductive development. Because many species must reach a certain age or size before they can flower, the vegetative meristem is thought to first pass through a “juvenile” phase in which it is incompetent to respond to internal or external signals that would trigger flowering in an “adult” meristem. The acquisition of reproductive competence is often marked by changes in the morphology or physiology of vegetative structures—leaf shape offers one example—in a process known as vegetative phase change (Poethig, 1990; Lawson and Poethig, 1995). It is likely that some of the genes identified as important in controlling the transition from vegetative to reproductive development are also involved in vegetative phase change. In some species, the timing of flowering is primarily influenced by environmental factors, which serve to communicate the time of year and/or growth conditions favorable for sexual reproduction and seed maturation. These factors include photoperiod (i.e., day length), light quality (spectral composition), light quantity (photon flux density), vernalization (exposure to a long period of cold), and nutrient and water availability. Other species are less sensitive to environmental variables and appear to flower in response to internal cues such as plant size or number of vegetative nodes. Flowering can also be induced by stresses such as nutrient deficiency, drought, and overcrowding. This response enables the plant to produce seeds, which are much more likely to survive the stress than is the plant itself. Over the years, physiological studies have led to three models for the control of flowering time (reviewed in Bernier, 1988; Thomas and Vince-Prue, 1997). The florigen concept (reviewed in Lang, 1952; Evans, 1971) was based on the transmissibility of substances or signals across grafts between reproductive “donor” shoots and vegetative “recipients.” It was proposed that florigen, a flower-promoting hormone, was produced in leaves under favorable photoperiods and transported to the shoot apex in the phloem. The identification of a graft-transmissible floral inhibitor also led to the concept of a competing “antiflorigen.” Many research years were consumed hunting for florigen in the phloem sap, but its chemical nature has remained elusive. The inability to separate the hypothetical flowering hormones from assimilates led to a second model, the nutrient diversion hypothesis. This model proposed that inductive treatments result in an increase in the amount of assimilates moving to the apical meristem, which in turn induces flowering (reviewed in Sachs and Hackett, 1983; Bernier, 1988). The view that assimilates are the only important component in directing the transition to flowering was superseded by the multifactorial control model, which proposed that a number of promoters and inhibitors, including phytohormones and assimilates, are involved in controlling the developmental transition (Bernier, 1988). According to this model, flowering can only occur when the limiting factors are present at the apex in the appropriate concentrations and at the right times. This model attempted to account for the diversity of flowering responses by proposing that different factors could be limiting for flowering in different genetic backgrounds and/or under particular environmental conditions. Genetic analysis of flowering time in pea, cereals, and Arabidopsis supports the hypothesis that the transition to flowering is under multifactorial control (reviewed in Snape et al., 1996; Weller et al., 1997; Koornneef et al., 1998b). Indeed, multiple genes that control flowering time have been identified in all three of these species. Moreover, some of these genes act to promote flowering and others to repress it; some interact with environmental variables and others ap