Journal: McGraw-Hill Yearbook of Science & Technology
Manuscript ID: YB13-0050
Manuscript Type: Yearbook Article
Date Submitted by the Author: 07-May-2012
Complete List of Authors: Graf, Alexander; ETH Zürich, Department of Plant Biotechnology
Keywords: starch, carbon availability, growth, circadian clock, starvation
Topic one: Plant physiology (571110)
Topic two: Biochemistry and molecular biology (570100)
Nighttime starch degradation, the circadian clock, and plant growth
The steadily rising demand for food and renewable resources has challenged plant breeders and biotechnologists to rapidly increase crop productivity. To realize this goal, a holistic knowledge is required of how plant metabolic pathways are controlled to allow optimal growth. Today, very little is known about the partitioning of photosynthetically assimilated carbon among growth, storage, and respiration. This article describes recent progress in understanding how the model plant Arabidopsis thaliana uses its carbon resources to ensure a continuous energy supply for growth during the night.
Diurnal starch turnover in Arabidopsis plants.
During the day, plants assimilate CO2 to produce sugars (photosynthates) in the process of photosynthesis. Plants use these sugars to fuel their metabolism and growth, producing the primary carbon source for almost all nonphotosynthetic organisms. However, not all photosynthates acquired during the day are used for immediate growth. Plants partition a fraction of the assimilated carbon into storage compounds in leaves to support respiration and continued growth during the night when photosynthesis is not possible.
In many plant species, the main carbon storage compound is starch. The synthesis of starch in leaves during the day and its degradation during the night have been studied intensively in the model plant A. thaliana. During a normal day, Arabidopsis plants store approximately 50% of the carbon assimilated by photosynthesis as starch granules in the cell plastids (chloroplasts) of leaves. During the night, starch is degraded with a near-linear rate such that the starch reserves are almost completely utilized by dawn (Fig. 1a).
This match between the length of time taken to degrade the starch reserves and the length of the night is vitally important for normal plant growth. If the night is artificially extended beyond the normal dawn, the growth rate of the plant drops abruptly. Mutant plants that cannot accumulate starch or that degrade it only very slowly have much lower growth rates than wild- type plants and show a severely reduced overall rate of growth. These reductions in growth rate are accompanied by large changes in gene expression indicating carbon starvation.
Considering the importance of a continuous carbon supply during the night for plant growth, it is not surprising that starch turnover is tightly controlled. Arabidopsis plants adjust the rates of starch synthesis and degradation to different environmental conditions (for example, temperature, light levels, and day length). The rate of starch synthesis is inversely related to day length: the shorter the day, the greater the proportion of assimilated carbon that is partitioned into starch. The rate of starch degradation is also adjusted such that a linear and almost complete degradation during the night is achieved for day lengths ranging from 18 h to as short as 4 h.
Remarkably, the rate of starch degradation in Arabidopsis plants can adjust immediately in response to an unexpected early or late onset of night. If plants grown in 12 h of light/12 h of darkness are subjected to darkness after only 8 h of light, the rate of starch degradation is much slower than on previous nights, but remains constant throughout the 16-h night. These observations imply that plants at dusk integrate information about the amount of starch present in leaves and the anticipated length of the night to set the rate of starch degradation. Recent investigations have revealed that the timing of starch degradation in Arabidopsis plants is linked to the circadian clock.
The circadian clock and starch degradation.
Almost all organisms possess an endogenous oscillating timer called the circadian clock. This timer keeps track of the estimated position of an organism in the 24-h light–dark cycle. The clock controls physiological processes that function at specific, appropriate times of day and supports the anticipation of dusk and dawn. In plants, the circadian clock affects a wide range of physiological and biochemical processes, including expansion growth, flowering time, stomatal aperture, leaf movement, and responses to drought stress and pathogen attack.
An important hallmark of the circadian clock is its free-running 24-h rhythm. Free running refers to the fact that, once entrained by light signals, the circadian clock maintains a 24- h rhythm in continuous light or continuous darkness, anticipating dusk and dawn according to previously encountered conditions. In fact, the property of being a 24-h timer has revealed the involvement of the circadian clock in the control of starch degradation. When plants are grown in light–dark cycles shorter or longer than 24 h, abnormal starch degradation patterns are observed during the night. In 28-h light–dark cycles (14 h of light, 14 h of darkness), starch is degraded extremely fast, so reserves are exhausted before dawn—specifically, at 10 h into the night rather than at the actual dawn after 14 h of night (Fig. 1b). Conversely, in 20-h light–dark cycles (10 h of light, 10 h of darkness), starch is degraded too slowly, resulting in the presence of substantial reserves at dawn. If the night is extended beyond dawn, starch is eventually depleted after approximately 14 h of darkness (Fig. 1c).
Measurements of clock-related gene transcription can be used to analyze the timing of the Arabidopsis clock. So-called morning-phased clock genes show a sharp expression peak at the anticipated dawn. Quantification of transcription level and starch content during the night has revealed that the anticipation of dawn by the circadian clock coincides with the exhaustion of starch reserves in all light–dark cycles (Fig. 1). These results indicate a link between starch degradation and the timing of the circadian clock in Arabidopsis, and they offer an explanation
for the abnormal starch degradation pattern in light–dark cycles that are longer or shorter than 24 h. Thus, starch degradation is programmed so that reserves would be exhausted 24 h after the previous dawn, regardless of the timing of the actual dawn experienced by the plant throughout its development.
Work on Arabidopsis mutant plants, in which the period of the clock is altered, confirmed these findings. The Arabidopsis cca1/lhy mutant lacks two transcription factors that control functioning of the clock. This loss does not eliminate clock function, but causes the clock to run fast. Analogous to wild-type plants in light–dark cycles longer than 24 h, cca1/lhy mutants fail to correctly anticipate dawn in a 24-h light–dark cycle (Fig. 1c). The expression peak of morning- regulated clock genes, indicating the anticipation of dawn, happens 4 h before the actual dawn.
At exactly this time point, cca1/lhy mutant plants exhaust their starch reserves. Hence, despite the abnormal behavior of the circadian clock in these mutants, the link between the clock and starch degradation remains intact.
