Circadian control of carbohydrate availability for growth inArabidopsisplants at night

Abstract

Plant growth is driven by photosynthetic carbon fixation during the day. Some photosynthate is accumulated, often as starch, to support nocturnal metabolism and growth at night. The rate of starch degradation in Arabidopsis leaves at night is essentially linear, and is such that almost all of the starch is used by dawn. We have investigated the timer that matches starch utilization to the duration of the night. The rate of degradation adjusted immediately and appropriately to an unexpected early onset of night. Starch was still degraded in an appropriate manner when the preceding light period was interrupted by a period of darkness. However, when Arabidopsis was grown in abnormal day lengths (28 h or 17 h) starch was exhausted ∼24 h after the last dawn, irrespective of the actual dawn. A mutant lacking the LHY and CCA1 clock components exhausted its starch at the dawn anticipated by its fast-running circadian clock, rather than the actual dawn. Reduced growth of wild-type plants in 28-h days and lhy/cca1 mutants in 24-h days was attributable to the inappropriate rate of starch degradation and the consequent carbon starvation at the end of night. Thus, starch degradation is under circadian control to ensure that carbohydrate availability is maintained until the next anticipated dawn, and this control is necessary for maintaining plant productivity.circadian clock | starch degradation | carbohydrate metabolism P lants are exposed to a daily alternation between light and dark. Although growth in the light can be directly fueled by photosynthesis, in the dark it depends on stored carbohydrate. In many species, starch accumulates in the light and is broken down to provide sugars for metabolism and growth at night. The rate of starch degradation in Arabidopsis leaves at night is essentially linear under a wide range of day/night lengths, and is such that about 95% of the starch is used by dawn (1, 2). This match between the length of time taken to degrade the starch reserves and the length of the night is vitally important for the normal growth of the plant. If the night is artificially extended beyond the normal dawn, the growth rate of the plant drops abruptly (3). Mutant plants that cannot accumulate starch, or degrade it only very slowly, have much lower growth rates than wild-type plants during normal nights and a reduced overall growth rate, except in continuous light or very long days (2-4). These reductions in growth rate are accompanied by large transcriptional changes indicative of carbon starvation.Remarkably, the rate of starch degradation in Arabidopsis plants adjusts immediately to an unexpected early or late onset of night. When plants grown in 16-h light/8-h dark were subjected to darkness after only 8 h of light, the rate of starch degradation was much slower than on previous nights. Conversely, when plants grown in 8-h light/16-h dark were given a 16-h light period, the subsequent rate of starch degradation was much faster than on previous nights (5). These observations imply that a timing mechanism ...

Gene Regulation and Survival under Hypoxia Requires Starch Availability and Metabolism

“…Given that transitory starch degradation is under circadian control (Graf et al, 2010), these results suggests that starch degradation in submerged plants is preserved both at the level of regulation and enzymatic efficiency, although we cannot exclude that differences exist in the mechanism operating under submergence. Remarkably, the energy-requiring step catalyzed by GWD was required for starch degradation under submergence (Fig.…”

Callose Synthase GSL7 Is Necessary for Normal Phloem Transport and Inflorescence Growth in Arabidopsis

“…This "starvation response" is seen, for example, when the night is extended beyond the normal dawn and in mutants defective in the storage or utilization of starch reserves during the night (Smith and Stitt, 2007). The starvation response can be monitored by measuring transcript levels of genes for which expression is known to be specifically responsive to carbohydrate levels (Gibon et al, 2004;Bläsing et al, 2005;Osuna et al, 2007;Usadel et al, 2008;Graf et al, 2010). We investigated whether the reduced carbohydrate levels in the terminal cluster of flowers and buds of gsl7 inflorescences triggered a starvation response by determining the expression of four starvation-induced genes (At1g76410, At3g59940, At1g08630, and At1g10070) and one sugar-induced gene (At3g13470; Supplemental Table S4).…”

Regulation of Leaf Starch Degradation by Abscisic Acid Is Important for Osmotic Stress Tolerance in Plants

“…Mutant Arabidopsis thaliana plants that fail to synthesize or degrade starch in the leaves have reduced growth rates under most conditions (Yazdanbakhsh and Fisahn, 2011;Usadel et al, 2008b). This nearly linear pattern of starch biosynthesis and degradation is retained under changing photoperiods or if plants are subject to a sudden early or late dusk, as long as the total circadian rhythm remains at 24 h (Sulpice et al, 2014;Graf et al, 2010). It is indeed observed that plants degrade starch faster in long days than in short days, demonstrating that plants somehow anticipate the length on the following night (Gibon et al, 2004;Lu et al, 2005).…”