Physiological Signals That induce Flowering
Georges Bernier, Andr6e Havelange, Claude Houssa, Anne Petitjean, and Pierre Lejeune
Laboratoire de Physiologie Végétale, Département de Botanique, Universite de Liège, Sart Tilman, 84000 Liège, Belgium
The Plant Cell, Vol. 5, 1147-1 155, October 1993.
The timing of the transition from vegetative growth to flowering is of paramount importance in agriculture, horticulture, and plant breeding because flowering is the first step of sexual reproduction. Studies to understand how this transition is controlled have occupied countless physiologists during the past half century and have produced an almost unmanageably large amount of information (Bernier et al., 1981a; Halevy, 1985-1989; Bernier, 1988; Kinet, 1993).
A majority of plants use environmental cues to regulate the transition to flowering because all individuals of a species must flower synchronously for successful outcrossing and because all species must complete their sexual reproduction under favorable externa1 conditions. Any environmental variables exhibiting regular seasonal changes are potential factors that control the transition to flowering. The major factors are photoperiod, temperature, and water availability. Plants that do not require a particular photoperiod or temperature to flower, i.e., the so-called “autonomous-flowering” plants, are usually sensitive to irradiance. The environmental factors are perceived by different parts of the plant. Photoperiod and irradiance are perceived mainly by mature leaves in intact plants. Temperature is perceived by all plant parts, although low temperature (vernalization) is often perceived mainly by the shoot apex. Water availability is perceived by the root system.
There are strong interactions between these different factors, so that each factor can change the threshold value for the effectiveness of the others. Plants, as opportunists, will thus make use of a different critical factor in different environments. Melilotus officinalis, for example, is a biennial with a vernalization requirement in temperate zones and an annual long-day (LD) plant with no cold requirement in arctic regions. In photoperiodic species, such as the short-day (SD) plant Pharbitis nil and the LD plant Silene armeria, flowering in unfavorable photoperiods can be caused by changing temperature, irradiance, or nutrition or by removing the roots. Similarly, in some late-flowering mutants of Arabidopsis, vernalization and an increase in the proportion of far-red light in the light source can substitute for one another in promoting the transition to flowering (Martínez-Zapater and Somerville, 1990; Bagnall, 1992). Clearly, there are alternate pathways to flowering in most, if not all, plants. Because the different flowering-promoting factors are perceived by different parts of the plant, this implies that these parts interact and that the fate of the apical meristem- remaining vegetative or becoming reproductive-is controlled by an array of long-distance signals from the entire plant.
The ability of subsets of plant parts to control flowering is also underscored by the fact that some plants may flower almost normally after complete defoliation (Hyoscyamus niger, red Perilla, Chenopodium amaranticolor) or derooting (Perilla, Lolium temulentum, Sinapis alba). This does not mean that these plant parts, when present, do not participate in the control of flowering. Plants are well adapted to partia1 destruction, for example by herbivorous animals, and it is known that the remaining parts can often substitute for the transiently missing part in providing the appropriate nutrients and signals.
Evidence that photoperiod leads to the production of transmissible flowering signals has come from grafting experiments. Such experiments have shown that leaves of photoperiodic plants produce promoters and inhibitors of flowering when exposed to favorable and unfavorable daylength regimes, respectively. These signals are generally transported from leaves to the apical meristem in the phloem with the assimilates. On the other hand, signals originating in roots are presumably transmitted in the xylem with the transpiration stream.
The nature of these transmissible signals is still a controversial issue (ONeill, 1992). Three major theories attempt to explain the chemical control of the transition to flowering. The “florigen/antiflorigen” concept (Lang, 1984) proposes that the floral promoter and inhibitor are each a simple, specific, and universal hormone that remain to be isolated and identified. The “nutrient diversion” hypothesis (Sachs and Hackett, 1983) postulates that floral induction, whatever the nature of the involved environmental factors, is a means of modifying the source/sink relationships within the plant in such a way that the shoot apex receives a better supply of assimilates than under noninductive conditions. Finally, the theory of “multifactorial control” (Bernier et al., 1981b; Bernier, 1988) postulates that severa1 chemicals-assimilates and known phytohormones-participate in floral induction. Genetic variation, as well as past and present growing conditions, result in different factor(s) of the complex becoming the limiting factor(s) in different species or genotypes or in a given genotype grown in different environments.
Identification of these signals is of the utmost fundamental and practical importance. Our aim here is to explore recent physiological and genetic approaches to this problem, focusing on some model experimental plants. We shall discuss the results obtained with S. alba and Arabidopsis, two mustard species between which we believe knowledge is easily transferable. Our analysis shows that both physiological and genetic results support the theory of a multifactorial control of flowering.