The Molecular Basis of Diversity in the Photoperiodic Flowering Responses of Arabidopsis and Rice

Abstract

Fluctuations in the length of the day affect developmental processes and behaviors of many organisms. Mammals and birds reproduce in spring in response to lengthening days and insects pupate in autumn when daylength shortens. These phenomena, called photoperiodism, allow detection of seasonal changes and anticipation of environmental conditions such as low temperatures and desiccation. Photoperiodism was first described in detail by Garner and Allard in 1920 through the demonstration that many plants flower in response to changes in daylength (Garner and Allard, 1920). Subsequently, they showed that some plant species promote flowering when daylength falls below a critical daylength, whereas other plants accelerate flowering in response to daylengths longer than a critical daylength. These plants are called short-day (SD) and long-day (LD) plants, respectively. During the last decade, molecular-genetic approaches were applied to understanding the control of flowering time, mainly in the LD plant Arabidopsis, and notable progress has been made in identifying the molecular mechanisms by which Arabidopsis recognizes daylength and promotes flowering specifically under LDs. Also, recent genetic studies in rice enabled the mechanisms of the daylength response in this SD plant to be compared with those of Arabidopsis. Here we review the recent advances in understanding the regulatory mechanisms for daylength response of flowering in Arabidopsis and compare them with those of rice. Erwin Bünning first proposed that the photoperiodic time-keeping mechanism is associated with the circadian clock (Bünning, 1936), an autonomous mechanism that generates biological rhythms with a period of approximately 24 h. This model proposes that the circadian clock generates a rhythm with an approximate 24-h period that controls flowering and is sensitive to light at a particular phase of the rhythm. Consequently, if a plant is grown under a specific daylength that causes it to be exposed to light at this particular phase, then flowering is induced if the plant shows a LD response, or repressed if the plant shows a SD response. This model, called the external coincidence model (Pittendrigh and Minis, 1964), has been supported by a number of physiological studies for the control of flowering time, indicating that the basis of daylength measurement is the interaction of an external light signal with a circadian rhythm (Thomas and Vince-Prue, 1997). In contrast, another model, called the internal coincidence model, proposes that the floral response occurs under conditions in which two differentially entrained rhythms are brought into the same phase under daylengths that promote flowering, but that under other daylengths these two rhythms are out of phase. Studies of photoperiodism in insects supported this model (Vaz Nunes and Saunders, 1999), but detailed analyses have not yet been carried out to test it in plants. Genetic studies in Arabidopsis support the involvement of the circadian clock in the control of flowering by daylength. Most mutants that were initially isolated based on an altered circadian rhythm phenotype, such as alterations in period length and/or amplitude of clock-controlled gene expression, also exhibit changes in flowering time. In addition, some mutants originally isolated based on a defect in the control of flowering by daylength also exhibit changes in circadian rhythms. The circadian clock system is often divided into three general parts (Dunlap, 1999). The central oscillator is the core of the system, responsible for driving 24-h rhythms. The oscillator is entrained to day-night or temperature cycles through a mechanism involving input pathways that transmit light or temperature signals to the core oscillator. Output pathways are controlled by the core oscillator and represent a wide range of biochemical and developmental pathways. The control of flowering by daylength is assumed to be regulated by one or more of these output branches. In this way, the core oscillator can determine the activity of diurnal rhythms in output genes, and these genes can set the light sensitive phase for triggering the floral transition. Model of the circadian system of Arabidopsis and its relationship to the flowering-time gene CO. Phytochromes and cryptochromes perceive light and are involved in resetting of the circadian clock. ELF3 and ZTL mediate between photoreceptors and the circadian clock. LHY/CCA1 and TOC1/ELF4 form a negative feedback loop within the circadian oscillator. LHY/CCA1 act as negative regulators of TOC1 and ELF4, which positively regulate the transcription of LHY/CCA1. The oscillator functions to determine the phase of CO transcription, a key gene that mediates between the circadian clock and flowering. The transcription of CO is regulated by FKF1 and GI, whose transcription is under the control of the circadian clock. FKF1 protein is directly regulated by light, and this allows FKF1 to increase CO transcr