Multiple circadian clock outputs regulate diel turnover of carbon and nitrogen reserves

Abstract

Plants accumulate reserves in the daytime to support growth at night. Circadian regulation of diel reserve turnover was investigated by profiling starch, sugars, glucose 6-phosphate, organic acids and amino acids during a light-dark cycle and after transfer to continuous light in Arabidopsis wild-types and in mutants lacking dawn (lhy cca1), morning (prr7 prr9), dusk (toc1, gi) or evening (elf3) clock components. The metabolite time-series were integrated with published time-series for circadian clock transcripts to identify circadian outputs that regulate central metabolism. i) Starch accumulation was slower in elf3 and prr7 prr9. It is proposed that ELF3 positively regulates starch accumulation. ii) Reducing sugars were high early in the T-cycle in elf3, revealing that ELF3 negatively regulates sucrose recycling. iii) The pattern of starch mobilization was modified in all five mutants. A model is proposed in which dawn and dusk/evening components interact to pace degradation to anticipated dawn. iv) An endogenous oscillation of glucose 6-phosphate revealed that the clock buffers metabolism against the large influx of carbon from photosynthesis. v) Low levels of organic and amino acids in lhy cca1 and high levels in prr7 prr9 provide evidence that the dawn components positively regulate the accumulation of amino acid reserves.

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

“…Arabidopsis (Arabidopsis thaliana) allocates 30%-40% of its photosynthate to starch in long photoperiods, rising to over 60% in short photoperiods (Sulpice et al, 2013;Mengin et al, 2017). At night, starch is degraded in a near-linear manner at a rate such that starch is almost but not completely exhausted at dawn (Graf et al, 2010;Scialdone et al, 2013: Flis et al, 2019. This pattern of mobilization is robust across a wide range of photoperiods and growth irradiances (Gibon et al, 2009;Sulpice et al, 2014;Mengin et al, 2017).…”

“…The clock is involved in the regulation of starch turnover (Graf et al, 2010;Scialdone et al, 2013;Pokhilko et al, 2014;Seki et al, 2017;Flis et al, 2019). The Arabidopsis clock can be schematized as an interconnected network of "dawn," "day," "dusk," and "evening" components (Nakamichi, 2011;Pokhilko et al, 2012;Fogelmark and Troein, 2014;Millar, 2016).…”

“…T is unlikely to correspond to a classical clock output because the rate of starch degradation can be set and reset between about ZeitgeberTime (ZT) 4 and ZT18 (Graf et al, 2010;Pyl et al, 2012;Scialdone et al, 2013;Sulpice et al, 2014). It has been proposed that T is a semiautonomous variable, which is set by the clock early in the 24-h cycle and decays during the remainder of the cycle (Scialdone et al, 2013;Seaton et al, 2013;Flis et al, 2019). Alternative models have been proposed in which retrograde metabolic signaling modifies clock gene expression and clock phase, which in turn affect starch turnover (termed here RMS models; Feugier and Satake, 2013;Seki et al, 2017).…”

Two Nucleoporin 98 homologous genes jointly participate in the regulation of starch degradation to enhance growth in Arabidopsis

“…Previous studies show that the circadian clock regulate starch metabolism in plants [61,62]. EARLY FLOWERING3 (ELF3) positively regulates starch accumulation and degradation of starch was significantly slower in elf3 mutant plants than in the corresponding wild types [63]. ELF3 and other clock evening genes (ELF4 and LUX ARRHYTHMO) also affect leaf senescence [64,65].…”

Phytochrome light receptors control metabolic flux, and their action during seedling development sets the trajectory for biomass production

“…This is at least partly due to a restriction of C utilization for growth in the light in short photoperiods (Mengin et al 2017) and it has been proposed that this may be due to light signalling being more fully reversed at dawn after a long night than short night (Flis et al 2016). As high reducing sugars were also found in the elf3 mutant (Flis et al 2019) (Flis et al, 2019), it is possible that Phy signalling interacts with outputs from the EC to control leaf sugar dynamics.…”