Response of the Circadian Clock and Diel Starch Turnover to One Day of Low Light or Low CO₂

Abstract

Diel starch turnover responds rapidly to changes in the light regime. We investigated if these responses require changes in the temporal dynamics of the circadian clock. Arabidopsis (Arabidopsis thaliana) was grown in a 12-h photoperiod for 19 d, shifted to three different reduced light levels or to low CO 2 for one light period, and returned to growth conditions. The treatments produced widespread changes in clock transcript abundance. However, almost all of the changes were restricted to extreme treatments that led to carbon starvation and were small compared to the magnitude of the circadian oscillation. Changes included repression of EARLY FLOWERNG 4, slower decay of dusk components, and a slight phase delay at the next dawn, possibly due to abrogated Evening Complex function and sustained expression of PHYTOCHROME INTERACTING FACTORs and REVEILLEs during the night. Mobilization of starch in the night occurred in a linear manner and was paced to dawn, both in moderate treatments that did not alter clock transcripts and in extreme treatments that led to severe carbon starvation. We conclude that pacing of starch mobilization to dawn does not require retrograde carbon signaling to the transcriptional clock. On the following day, growth decreased, sugars rose, and starch accumulation was stimulated in low-light-treated plants compared to controls. This adaptive response was marked after moderate treatments and occurred independently of changes in the transcriptional clock. It is probably a time-delayed response to low-C signaling in the preceding 24-h cycle, possibly including changes in PHYTOCHROME INTERACTING FACTOR and REVEILLE expression.

All roads lead to growth: imaging-based and biochemical methods to measure plant growth

“…Nevertheless, labelling for a few hours, in either the light or the dark, is sufficient and allows growth to be measured at different times in the diel cycle. There is a good quantitative agreement between estimated RGRs based on the C balance model and the RGRs estimated by protein synthesis measurements (Sulpice et al , 2014; Ishihara et al , 2015, 2017; Moraes et al , 2019). However, it should be noted that the rate of protein synthesis is not necessarily equivalent to the net rate of growth, because of the protein degradation that happens at the same time (Ishihara et al , 2017).…”

“…Plants cannot expand in the long term without an increase in structural biomass and proteins. Sulpice et al (2014) therefore used combined measurements of photosynthesis, respiration, starch, and other metabolite levels at dawn and dusk to estimate RGR by calculating the rate of C deposition into structural biomass, and numerous studies have also used this technique (Mengin et al , 2017; Flis et al , 2019; Moraes et al , 2019). Such studies, using this so-called whole-plant C balance model, have shown that growth is slower at night than in the daytime, especially in short photoperiods (Stitt and Zeeman, 2012).…”

“…In this approach, first used by Sulpice et al , (2014), measurements of photosynthesis, respiration, and changes in starch and metabolite levels between two time-points (e.g. dawn and dusk, or vice versa) are used to estimate the rate of C deposition into biomass (Mengin et al , 2017; Flis et al , 2019; Moraes et al , 2019). In the model, the amount of C in each major metabolite (starch, malate, fumarate, sucrose, glucose, fructose, amino acids) is obtained by multiplying the amount of a given metabolite by the number of C atoms in the molecule.…”

“…C allocation to growth is estimated in the light as the net rate of C assimilation minus the rate of C deposition. C allocation at night is estimated as the rate of C deposition minus the net rate of respiratory C loss (Sulpice et al , 2014; Mengin et al , 2017; Moraes et al , 2019). This approach can be extended to investigate plant strategies to optimise growth, and to identify metabolites that correlate with biomass gain, for example the sugar-signal trehalose 6-phosphate (Tre6P) (Sulpice et al , 2014; Czedik-Eysenberg et al , 2016).…”

Nighttime gibberellin biosynthesis is influenced by fluctuating environmental conditions and contributes to growth adjustments of Arabidopsis leaves

“…Low light levels also lead to altered carbon dynamics in the subsequent day. The following day less carbon is allocated to structural biomass and subsequently soluble carbohydrates (including starch) accumulate to higher levels (32), and this accumulation the subsequent day was independent of gibberellins (Supplemental Figure 10A-B). The higher carbon availability coincided with enhanced growth during the second night after the low light treatment, especially in Col-0 where the low-light-induced expansion was of a similar magnitude as the expansion induced solely by exogenous gibberellins.…”