Photoreceptors and Regulation of Flowering Time

Abstract

One of the most important environmental factors affecting flowering time is the daily duration of light, the photoperiod, which was first discovered by Garner and Allard in the 1920s (Thomas and Vince-Prue, 1997, and refs. therein). Plants in which flowering occurs or is accelerated in short days (SD) or long days (LD) are known as SD plants or LD plants, respectively. LD plants often flower in later spring or early summer (when the daylength becomes longer) to set seeds in a favorable season. SD plants generally flower in fall (when photoperiods are getting shorter) to finish reproduction before the cold winter arrives. Synchronization of flowering time with a reliable environmental cue such as the photoperiod also increases the chance of out-breeding and genetic recombination. The photoperiodic control of flowering is brought about by the interactions of genes involved in the developmental control of floral initiation, the regulation of the circadian clock, and the signal transduction of photoreceptors (Thomas and Vince-Prue, 1997). Recent molecular genetic studies in a facultative LD plant, Arabidopsis, have made notable progress in identifying genetic pathways and molecular components associated with the control of flowering time and the function of the circadian clock, which have been discussed in two recent Updates (Pineiro and Coupland, 1998; Somers, 1999). This Update focuses on the recent advances in our understanding of plant photoreceptors phytochromes and cryptochromes, and their roles in the regulation of flowering time. Flower formation is initiated by the transition of the apical meristem from a vegetative fate to a floral fate. Mechanisms that control the timing of floral initiation have been extensively studied in Arabidopsis by the identification of mutations that flower earlier or later than the wild type but otherwise remain healthy (Koornneef et al., 1998). These mutations are known as flowering-time mutations and the corresponding genes are known as flowering-time genes. In addition, many genes that were initially studied for their roles in other aspects of plant development, such as light perception, hormone metabolism, signal transduction, and floral meristem specification, also play roles in the regulation of flowering time and are sometimes also referred to as flowering-time genes. Based on phenotypic and genetic epistasis analysis of these mutations, flowering-time genes have been grouped into several signal transduction pathways that either suppress or promote floral initiation. These signaling pathways transmit either the developmental or environmental signals to regulate the expression of the floral-meristem-identity genes that control the formation of the floral meristem. Readers are referred to two recent reviews for detailed discussions of genes associated with these pathways in Arabidopsis (Koornneef et al., 1998;Levy and Dean, 1998). One of the major signal transduction pathways regulating flowering time is known as either the LD promotion pathway (Koornneef et al., 1998) or the photoperiodic pathway (Levy and Dean, 1998), which relays light and photoperiodic timing signals to the floral initiation process. Mutations of genes in this pathway reduce a plant's responsiveness to photoperiods. As a facultative LD plant, Arabidopsis grown in LD conditions flowers earlier than when grown withinSD. Misexpression of genes associated with the LD pathway may also delay the flowering of Arabidopsis plants grown in LD, but does not alter the flowering time of plants grown inSD, resulting in reduced sensitivity (hyposensitive) to photoperiod. Mutations in genes such as CO(CONSTANS; Putterill et al., 1995),PHYA (phytochrome A; Johnson et al., 1994; Reed et al., 1994), CRY2 (cryptochrome 2; Guo et al., 1998), andGI (GIGANTEA; Fowler et al., 1999; Park et al., 1999), are of this type. The elevated expression of the CCA1(circadian clock associated; Wang and Tobin, 1998) and LHY(late elongated hypocotyl; Schaffer et al., 1998) genes also results in photoperiod-hyposensitive late-flowering. On the other hand, a mutant that flowers earlier than the wild type in both LD and SD may also have reduced sensitivity to photoperiod. Early-flowering mutations in genes such as PHYB(phytochrome B; Goto et al., 1991), PHYD (phytochrome D;Aukerman et al., 1997; Devlin et al., 1999b), PHYE(phytochrome E; Devlin et al., 1999a), ELF3 (early flowering; Hicks et al., 1996; Zagotta et al., 1996), andPEF (phytochrome early flowering; Ahmad and Cashmore, 1996) belong to this group. We often assume that a late-flowering mutation corresponds to a gene product that normally promotes floral initiation, whereas an early-flowering mutant implies that the corresponding gene product is a suppressor of floral initiation. Not surprisingly, many genes isolated to date that are associated with the photoperiodic pathway encode either photoreceptors or proteins associated with the circadian clock. The primary photosensory rece