Plants use the circadian clock to sense photoperiod length. Seasonal responses like flowering are triggered at a critical photoperiod when a light-sensitive clock output coincides with light or darkness. However, many metabolic processes, like starch turnover, and growth respond progressively to photoperiod duration. We first tested the photoperiod response of 10 core clock genes and two output genes. qRT-PCR analyses of transcript abundance under 6, 8, 12 and 18 h photoperiods revealed 1-4 h earlier peak times under short photoperiods and detailed changes like rising PRR7 expression before dawn. Clock models recapitulated most of these changes. We explored the consequences for global gene expression by performing transcript profiling in 4, 6, 8, 12 and 18 h photoperiods. There were major changes in transcript abundance at dawn, which were as large as those between dawn and dusk in a given photoperiod. Contributing factors included altered timing of the clock relative to dawn, light signalling and changes in carbon availability at night as a result of clock-dependent regulation of starch degradation. Their interaction facilitates coordinated transcriptional regulation of key processes like starch turnover, anthocyanin, flavonoid and glucosinolate biosynthesis and protein synthesis and underpins the response of metabolism and growth to photoperiod.

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.

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Plants assimilate carbon in their photosynthetic tissues in the light. However, carbon is required during the night and in nonphotosynthetic organs. It is therefore essential that plants manage their carbon resources spatially and temporally and coordinate growth with carbon availability. In growing maize (Zea mays) leaf blades, a defined developmental gradient facilitates analyses in the cell division, elongation, and mature zones. We investigated the responses of the metabolome and transcriptome and polysome loading, as a qualitative proxy for protein synthesis, at dusk, dawn, and 6, 14, and 24 h into an extended night, and tracked whole-leaf elongation over this time course. Starch and sugars are depleted by dawn in the mature zone, but only after an extension of the night in the elongation and division zones. Sucrose (Suc) recovers partially between 14 and 24 h into the extended night in the growth zones, but not the mature zone. The global metabolome and transcriptome track these zone-specific changes in Suc. Leaf elongation and polysome loading in the growth zones also remain high at dawn, decrease between 6 and 14 h into the extended night, and then partially recover, indicating that growth processes are determined by local carbon status. The level of Suc-signaling metabolite trehalose-6-phosphate, and the trehalose-6-phosphate:Suc ratio are much higher in growth than mature zones at dusk and dawn but fall in the extended night. Candidate genes were identified by searching for transcripts that show characteristic temporal response patterns or contrasting responses to carbon starvation in growth and mature zones.