The circadian clock mutantlhy cca1 elf3paces starch mobilization to dawn despite severely disrupted circadian clock function

Abstract

Many plants, including Arabidopsis (Arabidopsis thaliana), accumulate starch in the daytime and remobilize it to support maintenance and growth at night. Starch accumulation is increased when carbon is in short supply, for example, in short photoperiods. Mobilization is paced to exhaust starch around dawn, as anticipated by the circadian clock. This diel pattern of turnover is largely robust against loss of day, dawn, dusk, or evening clock components. Here, we investigated diel starch turnover in the triple circadian clock mutant lhy cca1 elf3, which lacks the LATE ELONGATED HYPOCOTYL (LHY) and the CIRCADIAN CLOCK ASSOCIATED1 (CCA1) dawn components and the EARLY FLOWERING3 (ELF3) evening components of the circadian clock. The diel oscillations of transcripts for the remaining clock components and related genes like REVEILLE and PHYTOCHROME INTERACING FACTOR family members exhibited attenuated amplitudes and altered peak time, weakened dawn-dominance, and decreased robustness against changes in the external light-dark cycle. The triple mutant was unable to increase starch accumulation in short photoperiods. However, it was still able to pace starch mobilization to around dawn in different photoperiods and growth irradiances and to around 24 h after the previous dawn in T17 and T28 cycles. The triple mutant was able to slow down starch mobilization after a sudden low-light day or a sudden early dusk, although in the latter case it did not fully compensate for the lengthened night. Overall, there was a slight trend to less linear mobilization of starch. Thus, starch mobilization can be paced rather robustly to dawn despite a major disruption of the transcriptional clock. It is proposed that temporal information can be delivered from clock components or a semi-autonomous oscillator.

New Horizons in Plant Photoperiodism

“…Recently, a series of carefully designed experiments showed that the percentage of photoassimilates dedicated to starch is dependent on daylength but independent of light intensity and the daily light integral, a so-called truly photoperiodic process that responds to the duration of the light rather than the photon flux intensity ( 89 ). This was subsequently shown to be under the control of the circadian clock when a cca1 lhy elf3 triple mutant was unable to increase photoassimilate partitioning to starch in SDs, but maintained the ability to adjust starch degradation to accommodate the long night ( 3 ). This indicates that there are separate daylength measurement systems to alter starch synthesis and degradation rates in response to changing photoperiods.…”

Assessing the impacts of genetic defects on starch metabolism in Arabidopsis plants using the carbon homeostasis model

“…By contrast, the long period mutant pseudo-response regulator 7/9 ( prr7/9 ) (a free-running period of 29.4 h [ 10 ]) delays the onset of starch degradation, resulting in continuous starch accumulation throughout the day [ 9 ]. More recently, the use of a triple mutant with impaired clock functions, cca1/lhy/elf3 , which also lacks the EARLY FLOWERING3 ( ELF3 ), unravelled that plants with a dysfunctional clock are unable to adjust the starch accumulation rate, but they can still adjust the pace of starch degradation [ 11 ]. This means that the circadian oscillator might operate in a semi-autonomous mode to integrate temporal information in a complex network [ 11 ].…”

“…More recently, the use of a triple mutant with impaired clock functions, cca1/lhy/elf3 , which also lacks the EARLY FLOWERING3 ( ELF3 ), unravelled that plants with a dysfunctional clock are unable to adjust the starch accumulation rate, but they can still adjust the pace of starch degradation [ 11 ]. This means that the circadian oscillator might operate in a semi-autonomous mode to integrate temporal information in a complex network [ 11 ].…”