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First published online July 29, 2005; 10.1104/pp.105.061903 Plant Physiology 138:2280-2291 (2005) © 2005 American Society of Plant Biologists Daylength and Circadian Effects on Starch Degradation and Maltose Metabolism1Department of Botany (Y.L., T.D.S.) and Department of Biochemistry (J.P.G.), University of Wisconsin, Madison, Wisconsin 53706
Transitory starch is stored during the day inside chloroplasts and broken down at night for export. Maltose is the primary form of carbon export from chloroplasts at night. We investigated the influence of daylength and circadian rhythms on starch degradation and maltose metabolism. Starch breakdown was faster in plants of Arabidopsis (Arabidopsis thaliana) ecotype Wassilewskija growing in long days. Transcript levels of genes encoding enzymes involved in starch degradation and maltose metabolism showed a strong diurnal rhythm. Under altered photoperiods, the transcript levels and the rate of starch degradation changed within one day/night cycle. However, the amount of proteins involved in starch degradation was maintained relatively constant throughout the day/night cycle. To investigate whether the diurnal cycling of the transcript levels is only a response to light or is also regulated by a circadian clock, we measured the amount of messenger RNAs in Arabidopsis leaves under continuous light and continuous darkness. The expression of genes encoding starch degradation-related enzymes was under very strong circadian control in continuous light. Under continuous light, the amount of maltose also showed a strong endogenous rhythm close to 24 h, indicating that maltose metabolism is under circadian control. Light is necessary for the cycling of transcript levels and maltose levels. Under continuous darkness, these genes were barely expressed, and no cycling of maltose levels was observed.
Starch is the most abundant carbohydrate reserve in plants. There are two types of starch: storage starch and transitory starch. Transitory starch is stored during the day inside chloroplasts and broken down at night for export. At night, starch is converted to maltodextrin by several enzymes, such as debranching enzyme, and appears to be influenced by a glucan, water dikinase (GWD) and phosphoglucan, water dikinase (PWD) (Ritte et al., 2000  , 2002; Trethewey and Smith, 2000; Yu et al., 2001; Smith et al., 2003; Zeeman et al., 2004; Kotting et al., 2005).  -Amylase (AtAMY3) was thought to be involved in the conversion of starch to maltodextrin (Trethewey and Smith, 2000), but recent data indicate that AtAMY is not required for transitory starch breakdown in Arabidopsis (Arabidopsis thaliana) leaves (Yu et al., 2005). Maltodextrin is then converted to maltose and Glc by  -amylase (CT-BMY) and disproportionating enzyme (DPE1) in the chloroplast (Lao et al., 1999; Critchley et al., 2001; Scheidig et al., 2002; Schneider et al., 2002). Recent evidence indicates that maltose and Glc are the two major forms of carbon exported from chloroplasts at night (Weber et al., 2000; Servaites and Geiger, 2002; Weise et al., 2004). Maltose is exported by the maltose transporter MEX1 (Niittylä et al., 2004) and is metabolized in the cytosol by several enzymes, including disproportionating enzyme (DPE2) and possibly glucan phosphorylase (AtPHS2) (Chia et al., 2004; Lu and Sharkey, 2004; Schupp and Ziegler, 2004). Localization of DPE2 in the literature is conflicting. DPE2 protein from Arabidopsis was demonstrated to be present in the cytosol (Chia et al., 2004). The potato (Solanum tuberosum) isoform of DPE2 protein (stDPE2) was demonstrated to be present in chloroplasts (Lloyd et al., 2004). Inhibition of maltose export or maltose metabolism results in a 20- to 90-fold increase in leaf maltose content and a dwarf phenotype, showing that Glc cannot compensate for a loss of capacity for maltose metabolism (Lu and Sharkey, 2004; Niittylä et al., 2004). Antisense inhibition of cytosolic phosphorylase in potato plants has only little impact on carbohydrate metabolism (Duwenig et al., 1997). However, preliminary data from our lab using heterozygous AtPHS2 knockout plants of Arabidopsis indicate that lack of this enzyme also results in 164% increase in maltose level and 23% decrease in Suc level at night.
There are two possible roles for transitory starch. First, transitory starch may act as an overflow for newly assimilated carbon when assimilation exceeds the demand for Suc (Stitt and Quick, 1989
Accumulation and degradation of starch could be controlled by light, metabolites, daylength, or circadian rhythms. Light regulates transcript abundance of >100 genes, such as the RbcS (Rubisco small subunit) gene family and the CAB (chlorophyll a/b binding protein) gene family (Terzaghi and Cashmore, 1995 In this study, we investigated the influence of daylength and circadian clock on starch degradation and maltose metabolism in Arabidopsis ecotype Wassilewskija. We compared the rates of starch mobilization and carbohydrate levels in long days with those in short days. We studied how rapidly Arabidopsis can adjust the rate of starch degradation after we changed daylength. To study whether changes in carbohydrate levels and starch degradation rates are reflected in the transcript and protein levels of key enzymes, we determined the relative amount of transcripts and proteins under various conditions using real-time RT-PCR and western blots. We also analyzed whether the cycling of transcript levels, starch levels, and metabolite levels is exclusively a response to light or whether it is also regulated by a circadian clock. We determined the amount of the same transcripts, proteins, and carbohydrates under continuous light or darkness after entraining plants in a long-day regime.
Starch Breakdown Was Faster in Plants Growing in Long Days We first investigated the impact of different daylengths on the rate of starch degradation. We measured leaf starch levels of Arabidopsis plants in a 16-h-light/8-h-night regime (long days [LD]) and an 8-h-light/16-h-night regime (short days [SD]). In Arabidopsis, transitory starch was accumulated and broken down almost linearly (Fig. 1). Starch accumulation was faster in plants growing in SD than those growing in LD, but not sufficiently faster to compensate for the short photoperiod (Fig. 1; Table I). Thus, by the end of the day, plants growing in LD accumulated more starch than plants growing in SD (Fig. 1). At night, plants growing in LD/short nights had a much faster rate of starch degradation than plants growing in SD/long nights (Table I). More starch was left in the leaves at the end of night in LD (Fig. 1A) than in SD (Fig. 1B).
We next investigated whether the rate of starch degradation decreased after a transition from a LD to a SD regime. Arabidopsis plants were transferred from a 16-h-light/8-h-dark regime to an 8-h-light/16-h-dark regime. The amount of starch was measured before, during, and after this shift. The rate of starch degradation during the first elongated night (long day to short day [LS]), 4.14 ± 0.19 µmol Glc g–1 fresh weight (FW) h–1 (P < 0.0001), was much lower than that during a regular short night (LD), 13.19 ± 1.61 µmol glc g–1 FW h–1 (P < 0.05; Table I). Less starch was left in the leaves at the end of the first extended night than at the end of a regular short night (Fig. 1A). We also investigated whether the rate of starch degradation increased after a transition from a SD to a LD regime. Arabidopsis plants were transferred from an 8-h-light/16-h-dark regime to a 16-h-light/8-h-dark regime. The rate of starch degradation during the first shortened night (short day to long day [SL]), 8.22 ± 2.69 µmol glc g–1 FW h–1 (P = 0.09), was much higher than that during a regular long night (SD), 4.39 ± 0.40 µmol glc g–1 FW h–1 (P < 0.0001). More starch was left in the leaves at the end of the first shortened night than at the end of a regular long night (Fig. 1B).
To study the expression of starch degradation-related enzymes in different daylengths, we measured relative transcript abundance of starch degradation-related enzymes, including R1 protein (SEX1), chloroplastic
We next investigated whether the transcript levels of starch-related enzymes in plants are decreased during the first long night after a transition from a LD to a SD regime. We found that this is the case in Arabidopsis. There was a significant decrease in relative transcript abundance of DPE2, AtPHS2, and CT-BMY at 7 h of the first extended night and the rest of the first extended night (Fig. 2, C, E, and I). The effect of changes in daylength on the expression pattern of CT-BMY was dramatic. The dusk peak of CT-BMY transcript levels changed from local time 3 PM (1 h before the end of day) to local time 9 AM (1 h in the night) because the day was shortened from 16 to 8 h (Fig. 2I). The effect of changes in daylength on the expression pattern of RbcS1A was not as dramatic. The only significant change was the decrease of RbcS1A transcript levels at 1 h before the end of the first extended night (Fig. 2A). We also found that the transcript levels of starch-related enzymes in Arabidopsis plants are increased during the first short night after a transition from a SD to a LD regime. There was a significant increase in relative transcript abundance of DPE2, AtPHS2, SEX1, and CT-BMY at the end of the first extended day and at the first short night (Fig. 2, D, F, H, and J). The effect of changes in daylength on the expression pattern of CT-BMY was substantial. The second peak of CT-BMY transcript levels in LD, which disappeared in SD, showed up in the first extended day (Fig. 2J). There was only one RbcS1A mRNA peak at 7 h of the day in a regular SD regime (Fig. 2B). But there were two RbcS1A mRNA peaks in the first altered day/night cycle: one at 7 h of the day and the other at 15 h of the first extended day (Fig. 2B).
To study whether the diurnal cycling of transcript levels of starch degradation-related enzymes is reflected in the diurnal protein levels, we assayed the protein abundance of RbcS, SEX1, and DPE2 with western blots. The protein levels of RbcS (Fig. 3A), SEX1 (Fig. 3B), and DPE2 (Fig. 3C) were relatively constant throughout the day/night cycle in both LD and SD. The protein levels of these enzymes were constant during the first altered day/night cycle after a transition from a long- to a short-day regime (Fig. 3). They also were constant during the first altered day/night cycle after a transition from a short- to a long-day regime (SL) (Fig. 3).
Metabolite Contents Had Different Profiles at Different Day/Night Regimes
Plants growing in LD accumulated more starch and had a faster rate of starch degradation than plants growing in SD. To investigate the impact of different daylengths on the rate of starch degradation, we measured diurnal contents of G6P, Glc,
To study whether the metabolite levels in Arabidopsis leaves could change during the first altered day/night cycle after the instant changes in daylength, we measured the diurnal metabolite levels in Arabidopsis leaves after a transition from a LD to a SD regime. The amount of -maltose did not increase during the first 8 h of extended night but increased a little more during the rest of the extended night (Fig. 4A). However, the amount of Glc dropped during the first hour of the extended night and declined slowly throughout the rest of the extended night (Fig. 4C). The amount of Suc dropped substantially during the first hour of the extended night and recovered during the next 3 h of the extended night, remained constant for another 6 h, and declined again during the rest of the night (Fig. 4E). As a response to the absence of light, the transition point between daytime and nighttime Glc and Suc levels shifted from local time 4 PM to local time 8 AM (Fig. 4, C and E).
We next measured the diurnal metabolite levels in Arabidopsis leaves after a transition from a SD to a LD regime. The amount of
We estimated average rates of starch degradation by a linear regression of all the values of starch over the duration of the night at different day/night regimes (LD, LS, SD, and SL; Table I). Then we plotted the average nighttime carbohydrate levels, maximum nighttime
Transcript Levels of Starch Degradation-Related Genes Showed Strong Endogenous Rhythms under Continuous Light The transcript levels of starch degradation-related enzymes oscillated during the day/night cycle (Fig. 2). To study whether the diurnal cycling of the transcript levels is a response to the presence and absence of light or is controlled by a circadian clock, we measured the relative transcript abundance of the same genes under continuous light. Under continuous light, the transcript levels of DPE2, AtPHS2, SEX1, and CT-BMY had coherent endogenous rhythms close to 24 h (Fig. 6, C, E, G, and I). They showed little or no evidence of damping throughout four cycles. DPE2, AtPHS2, and SEX1 transcript abundance cycled with a midday-specific phase (Fig. 6, C, E, and G), while CT-BMY transcript abundance cycled with a dusk-specific phase (Fig. 6I). The oscillation of RbcS1A transcript abundance damped gradually after one cycle under continuous light (Fig. 6A).
Transcript Levels of Starch Degradation-Related Genes Damped Rapidly under Continuous Darkness To study if light is necessary in keeping the cycling of transcript levels of starch degradation-related enzymes, we measured the relative transcript abundance of the same genes under continuous darkness. We found that the transcript levels of all the genes we quantified declined rapidly during the first 15 h under continuous darkness (Fig. 6, B, D, F, H, and J). The transcript levels of SEX1 and CT-BMY showed some cycling but it damped out within the first 48 h of continuous darkness (Fig. 6, H and J).
To study if the protein levels of starch degradation-related enzymes remain constant under continuous light and damp under continuous darkness, we determined the protein abundance of RbcS, SEX1, and DPE2 under continuous light or darkness. The protein levels of RbcS remained relatively constant under continuous light or continuous darkness (Fig. 7A). The protein levels of SEX1 and DPE2 remained constantly high during the first 49 h of continuous light and declined to a lower level after 49 h of continuous light and remained low during the rest of continuous light (Fig. 7, B and C). The protein levels of SEX1 and DPE2 remained high during the first 9 h of continuous darkness and declined to a lower level after 15 h in continuous darkness (Fig. 7, B and C).
Maltose Contents Oscillated with a Strong Endogenous Rhythm under Continuous Light
To study if the metabolism of starch, maltose, and other carbohydrates is under circadian control, we measured the amount of starch, G6P, Glc,
In continuous darkness, the amount of starch, maltose, Glc, and Suc declined quickly during the first 15 h (Fig. 8, B, D, F, and H). There was a small amount of starch that was never broken down, and Glc, G6P, and Suc were never depleted throughout the 85 h in the dark. Unlike starch, Glc, G6P, or Suc, there was little maltose after the first 15 h in continuous darkness.
Plants May Adjust Their Rate of Starch Degradation According to the Changes in Daylength
We focused on how the rate of starch degradation is regulated to match the amount of starch in the leaf. Assuming starch is inert, it is hard to imagine that the level of starch could regulate the rate of degradation. One possible explanation is that a lower amount of Glc and/or higher amount of Suc at the end of the day in LD triggers the faster rate of starch degradation. Sugars can regulate carbon metabolism, gene expression, and posttranslational modification of some enzymes in starch metabolism (Koch, 1996
Among the four genes, DPE2, AtPHS2, and SEX1 share the same expression pattern, suggesting coordinate regulation (Smith et al., 2004
Protein levels of two of the corresponding enzymes, SEX1 and DPE2, do not change as daylength changes. Under a 12-h-light/12-h-dark photoperiod, transcript levels of SEX1 and DPE2 peak at the end of the light period and 8 h of the light period, respectively, but the protein levels are relatively constant throughout the day/night cycle (Yu et al., 2001
The lack of correspondence between transcript levels and protein levels suggests that posttranscriptional and posttranslational regulation might be important in controlling the amount of enzymes and their activities in vivo (Smith et al., 2004
Transcript levels of starch degradation-related enzymes show robust endogenous rhythms under continuous light. This indicates that the variation of transcript levels under a regular day/night regime is not just a response to light. Circadian control plays a very important role in the oscillation of transcript levels of starch degradation-related enzymes. In Arabidopsis, novel putative
The current model for the central oscillator in Arabidopsis is a negative feedback loop between three proteins: two myb-like DNA binding proteins, CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATION HYPOCOTYL (LHY), and the TIMING OF CAB EXPRESSION 1 (TOC1) protein (Alabadi et al., 2001
Arabidopsis plants used in this report are exposed to another time cue, temperature cycles (22°C during the day and 20°C during the night), besides light cycles. Both cues serve to synchronize the endogenous clock with local time or growth chamber time (Michael et al., 2003
Glc and Suc levels drop quickly during the first hour of the night in both LD and SD as a response to the absence of light. The drop of Glc and Suc levels happens earlier if daylength is shortened and happens later if daylength is extended. We hypothesize that the profile of Glc and Suc contents is primarily light dependent and that the endogenous rhythm does not play a primary role in the changes seen through the day and night. Glc and Suc levels oscillate without a clear pattern in continuous light and damp out in continuous darkness. This further proves that Glc and Suc levels are primarily light regulated, and circadian clock doesn't play a major role in regulating the amount of Glc and Suc in Arabidopsis leaves. The amounts of maltose increase quickly during the first hour of the night in LD. This massive production of maltose is not shifted earlier when darkness is imposed earlier. We hypothesize that both light and the endogenous rhythm play important roles in the cycling of maltose. Maltose levels under continuous light have a robust endogenous rhythm and damp out in continuous darkness. This further proves that maltose metabolism is under strong circadian control.
Starch increases almost linearly during the first 48 h of continuous light with a decrease during the first subjective night. A similar pattern of starch accumulation under 48 h of continuous light was found in C3 M. crystallinum (Dodd et al., 2003
Under continuous darkness, carbohydrate levels drop quickly during the first 15 h. Previously expressed starch-degrading enzymes may result in this rapid decrease. Interestingly, the protein abundance of SEX1 and DPE2 also drops after 15 h under continuous darkness. Because the transcript abundance declines quickly during the first 15 h, de novo translation of SEX1 and DPE2 is impossible. This also suggests that protein degradation happens under continuous darkness. Thimm et al. (2004) To sum up, plants may sense changes in daylength and adjust their rate of starch degradation the following night. The expression of genes encoding starch degradation-related enzymes is regulated by daylength and a circadian clock. The protein levels of these enzymes are constant throughout the day/night cycle, indicating that posttranscriptional regulation might be important in controlling the amount of enzymes and their activities in vivo. The amount of Glc and Suc is primarily light dependent, while the amount of maltose is regulated both by light and by the circadian clock.
Plant Growth Conditions Plants of Arabidopsis (Arabidopsis thaliana) ecotype Wassilewskija were grown under a 16-h-light/8-h-dark (LD) or an 8-h-light/16-h-dark photoperiod (SD), 150 µmol photon m–2 s–1. The temperature was 22°C during the day and 20°C during the night. Humidity was maintained at 60%. Plants used in the experiments were between 3 and 5 weeks old. Plants under different photoperiods were analyzed at the same leaf size. To investigate whether plants can adjust their rate of starch degradation in the first altered photoperiod, we transferred plants in LS after 8 h in the light, which shortened daylength by half. We also transferred plants in SL after 8 h in the light, which doubled daylength. To investigate whether the expression of genes encoding starch degradation-related enzymes is controlled by a circadian clock, we transferred plants entrained in 16-h-lignt/8-h-dark cycles to continuous light at the end of their regular dark period, and we transferred entrained plants to continuous darkness at the end of their regular light period. The temperature was 22°C during subjective days and 20°C during subjective nights.
Five rosette leaves per time point were taken and added to microfuge tubes containing 750 µL 80% (v/v) ethanol and 5% (v/v) formic acid and were frozen in liquid N2. Starch and other carbohydrates were extracted according to Lu and Sharkey (2004)
Total RNA was extracted from Arabidopsis rosette leaves as described (Takaha et al., 1993 Gene-specific primers were designed to span two exons and were synthesized at Integrated DNA Technologies (Coralville, IA): 5'-TTC CTG ACC TTA CCG ATT CC-3' and 5'-GCA TTG GGG TAC TCC TTC TT-3' for RbcS1A; 5'-TAC GTC AAC TGG AGC ACC TC-3' and 5'-TCA TAG CAT GAG CTG GAA GC-3' for DPE2; 5'-CGC CAA GTA CAG TCC ACA TT-3' and 5'-CAA GCT CAT AAC CCA GCG TA-3' for AtPHS2; 5'-TGG GAA CGT AAG GGT AAA CA-3' and 5'-GCT CTG GTT GCT TGG AAA CT-3' for SEX1; 5'-AAA GCA CGG TCT CAA ACT CC-3' and 5'-CAC AGA ATC ACA TCC CAA GG-3' for CT-BMY; 5'-CAT CCA AGC TGT TCT CTC CT-3' and 5'-CTT ACA ATT TCC CGC TCT GC-3' for Actin 2 (ACT2). Quantitative PCR was performed on a Stratagene Mx3000P QPCR system with Brilliant SYBR Green master mix according to the manufacturer's instructions (Stratagene, La Jolla, CA). All samples were assayed in triplicate. The following standard thermal profile was used for all PCR reactions: 95°C for 10 min; 40 cycles of 95°C for 30 s, 55°C for 1 min, and 72°C for 1 min. Absence of genomic DNA contamination was confirmed by the dissociation curve following 40 PCR cycles according to the manufacturer's instructions. Ct values for all analyzed genes were normalized to the threshold cycle (Ct) values of ACT2. PCR efficiency was estimated from the standard curve for each gene with purified PCR products as the template. Validation of the RT-PCR data was confirmed by standard curves of individual RT-PCR products.
Total soluble protein was extracted from Arabidopsis rosette leaves as described by Heck et al. (1995)
Sequence data from this article have been deposited with the EMBL/GenBank data libraries under the following accession numbers: At1g10760 (GWD1, SEX1), At1g67090 (RbcS1A), At2g40840 (DPE2), At3g18780 (ACT2), At3g46970 (AtPHS2), At4g15210 (At
We thank Gerhard Ritte for providing antiserum to potato SEX1 protein and Alison M. Smith for providing peptide-specific antiserum to DPE2. We also thank Anne M. Borland, C. Robertson McClung, Gerhard Ritte, and Andreas P.M. Weber for critical reading of the manuscript. Received February 24, 2005; returned for revision April 13, 2005; accepted April 20, 2005.
1 This work was supported by the Chemical Sciences, Geosciences, and Biosciences Division, U.S. Department of Energy.  Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.061903. * Corresponding author; e-mail tsharkey{at}wisc.edu; fax 608–262–7509.
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