Plant Circadian Rhythms

Abstract

The earth rotates on its axis every 24 h, with the result that any position on the earth's surface alternately faces toward or away from the sun—day and night. That the metabolism, physiology, and behavior of most organisms changes profoundly between day and night is obvious to even the most casual observer. These biological oscillations are apparent as diurnal rhythms. It is less obvious that most organisms have the innate ability to measure time. Indeed, most organisms do not simply respond to sunrise but, rather, anticipate the dawn and adjust their biology accordingly. When deprived of exogenous time cues, many of these diurnal rhythms persist, indicating their generation by an endogenous biological circadian clock. Until recently, the molecular mechanisms by which organisms functioned in this fourth dimension, time, remained mysterious. However, over the last 30 or so years, the powerful approaches of molecular genetics have revealed the molecular underpinnings of a cellular circadian clockwork as complicated and as beautiful as the wonderful chronometers developed in the 18th century. Then, the need to accurately measure time to precisely determine longitude sparked an international competition to claim a prize, the princely sum of 20,000 pounds sterling, offered by the British Crown (Sobel, 1995). Critical Terms Used to Describe Circadian Rhythms. Period is defined as the time to complete one cycle. It is commonly measured from peak to peak but could equally be measured from trough to trough or from any specified phase marker. Phase is the time of day for any given event. For example, if the peak in a rhythm occurred at dawn, the phase of the peak would be defined as 0 h. If a rhythm peaked 6 h after dawn, its phase would be 6 h, and so on. Phase is often defined in zeitgeber time (ZT). Zeitgeber is German for time giver, and any stimulus that imparts time information to the clock is a zeitgeber. The onset of light is a powerful zeitgeber, and dawn is defined as ZT0. The amplitude of the rhythm is defined as one-half the peak-to-trough distance. Only in exceptional circumstances, such as in the laboratory, is an organism deprived of environmental time cues, such as light/dark cycles or temperature cycles, that derive from the alternation of day and night. These environmental time cues, termed zeitgebers (German for time givers), entrain the endogenous timing system to a period of 24 h, precisely corresponding to the exogenous period of the earth's rotation. The ability of a stimulus to reset the clock is a function of the time of day (phase; see Figure 1) at which the stimulus is administered. A pulse of light given before dawn will advance the phase of the clock, yet the same pulse of light given after dusk will delay the phase. If given at noon, the same pulse of light will have no effect at all. From this it is apparent that the clock regulates its own sensitivity to environmental stimuli. This varying sensitivity can be quantified and displayed as a phase response curve, in which one plots the shift in phase in response to a stimulus applied at different times across the circadian cycle (Dunlap et al., 2004). The first writings, at least in the western canon, to recognize diurnal rhythms come from the fourth century BC. Androsthenes described the observation of daily leaf movements of the tamarind tree, Tamarindus indicus, that were observed on the island of Tylos (now Bahrein) in the Persian Gulf during the marches of Alexander the Great (Bretzl, 1903). There was no suggestion that the endogenous origin of these rhythms was suspected at the time, and it took more than two millennia for this to be experimentally tested. The scientific literature on circadian rhythms began in 1729 when the French astronomer de Mairan reported that the daily leaf movements of the sensitive heliotrope plant (probably Mimosa pudica) persisted in constant darkness, demonstrating their endogenous origin (de Mairan, 1729). Presciently, de Mairan suggested that these rhythms were related to the sleep rhythms of bedridden humans. It took 30 years before de Mairan's observations were independently repeated (Hill, 1757; Duhamel duMonceau, 1759; Zinn, 1759). These studies excluded temperature variation as a possible zeitgeber driving the leaf movement rhythms. Leaf Movements of a Representative Species. (A) Sleep movements of Phaseolus coccineus. The position of the primary leaves of a seedling at night is at the left and during the day is at the right. (B) Circadian rhythm of leaf movements of P. coccineus entrained to light/dark cycles and monitored in continuous light. As can be inferred from the leaf positions in (A), the peaks of the curve represent the nighttime leaf position. The vertical lines indicate 24-h intervals. The period for this trace is ∼27 h. (A) was originally published as Figure 14 and (B) as Figure 4 in Chapter 2 in Bünning (1973). Both are reproduced with kind permission of Springer Science and Busine