Genetic Linkages of the Circadian Clock-Associated Genes, TOC1, CCA1 and LHY, in the Photoperiodic Control of Flowering Time in Arabidopsis thaliana

Niwa, Yusuke; Ito, Shogo; Nakamichi, Norihito; Mizoguchi, Tsuyoshi; Niinuma, Kanae; Yamashino, Takafumi; Mizuno, Takeshi

doi:10.1093/pcp/pcm067

Cited by 123 publications

(107 citation statements)

References 52 publications

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“…We checked the timing of expression of genes under circadian clock control by analyzing GBS1 transcript levels. As expected from previous reports (19,20), peak levels occurred 3 to 4 h earlier in the mutant than in WT (Fig. 4A).…”

Section: Resultssupporting

confidence: 92%

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Circadian control of carbohydrate availability for growth inArabidopsisplants at night

Graf

Schlereth

Stitt

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

573

738

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Plant growth is driven by photosynthetic carbon fixation during the day. Some photosynthate is accumulated, often as starch, to support nocturnal metabolism and growth at night. The rate of starch degradation in Arabidopsis leaves at night is essentially linear, and is such that almost all of the starch is used by dawn. We have investigated the timer that matches starch utilization to the duration of the night. The rate of degradation adjusted immediately and appropriately to an unexpected early onset of night. Starch was still degraded in an appropriate manner when the preceding light period was interrupted by a period of darkness. However, when Arabidopsis was grown in abnormal day lengths (28 h or 17 h) starch was exhausted ∼24 h after the last dawn, irrespective of the actual dawn. A mutant lacking the LHY and CCA1 clock components exhausted its starch at the dawn anticipated by its fast-running circadian clock, rather than the actual dawn. Reduced growth of wild-type plants in 28-h days and lhy/cca1 mutants in 24-h days was attributable to the inappropriate rate of starch degradation and the consequent carbon starvation at the end of night. Thus, starch degradation is under circadian control to ensure that carbohydrate availability is maintained until the next anticipated dawn, and this control is necessary for maintaining plant productivity.circadian clock | starch degradation | carbohydrate metabolism P lants are exposed to a daily alternation between light and dark. Although growth in the light can be directly fueled by photosynthesis, in the dark it depends on stored carbohydrate. In many species, starch accumulates in the light and is broken down to provide sugars for metabolism and growth at night. The rate of starch degradation in Arabidopsis leaves at night is essentially linear under a wide range of day/night lengths, and is such that about 95% of the starch is used by dawn (1, 2). This match between the length of time taken to degrade the starch reserves and the length of the night is vitally important for the normal growth of the plant. If the night is artificially extended beyond the normal dawn, the growth rate of the plant drops abruptly (3). Mutant plants that cannot accumulate starch, or degrade it only very slowly, have much lower growth rates than wild-type plants during normal nights and a reduced overall growth rate, except in continuous light or very long days (2-4). These reductions in growth rate are accompanied by large transcriptional changes indicative of carbon starvation.Remarkably, the rate of starch degradation in Arabidopsis plants adjusts immediately to an unexpected early or late onset of night. When plants grown in 16-h light/8-h dark were subjected to darkness after only 8 h of light, the rate of starch degradation was much slower than on previous nights. Conversely, when plants grown in 8-h light/16-h dark were given a 16-h light period, the subsequent rate of starch degradation was much faster than on previous nights (5). These observations imply that a timing mechanism ...

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Section: Resultssupporting

confidence: 92%

“…The clock in cca1/lhy seedlings has a short free-running period of about 17 h under continuous light (14,17,18). Importantly for our purpose, there is also a strong phase advance (about 4 h) in the expression of clock and clockregulated genes when this mutant is grown on soil without exogenous carbohydrate in 24-h T-cycles (19,20).…”

Section: Resultsmentioning

confidence: 95%

Circadian control of carbohydrate availability for growth inArabidopsisplants at night

Graf

Schlereth

Stitt

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

573

738

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“…Interestingly, some of the phenotypes displayed by the C1 OE and C3 OE plants, including the number of rosette leaves at the reproductive transition and hypocotyl length (Table I), are reminiscent of those obtained for the loss-of-function double mutant lhy cca1, which are nuclear components of the Arabidopsis circadian clock (Mizoguchi et al, 2002(Mizoguchi et al, , 2005Ito et al, 2007;Niwa et al, 2007). Accordingly, the C1 OE and C3 OE plants show decreased expression levels of the LHY and CCA1 genes and of the circadian clock output genes LHCB1.1 and COL1 when compared with the Figure 10.…”

Section: Copt1 and Copt3 Overexpression Effects Inmentioning

confidence: 93%

“…These additional phenotypes further highlight the importance of the spatiotemporal control of Cu homeostasis to ensure appropriate growth and development in higher plants. It is noteworthy that none of these phenotypes was observed when the Arabidopsis wildtype plants were grown on soil with elevated Cu levels, although some of them were rather reminiscent of plants with altered circadian rhythms (Mizoguchi et al, 2002(Mizoguchi et al, , 2005Ito et al, 2007;Niwa et al, 2007;Lu et al, 2009), suggesting potential alterations in the perception of light or circadian rhythms in the plants where Cu homeostasis is deregulated.…”

Section: Additional Phenotypes Associated With the Copt-overexpressinmentioning

confidence: 99%

“…The LHY and CCA1 proteins bind to the same region of their target promoters, form homodimers or heterodimers, and colocalize within the nucleus, where they function synergistically (Lu et al, 2009). The loss-of-function double mutants lhy cca1 show short periods of free-running circadian rhythms, affected photoperiodic control of flowering time, modified hypocotyl length, and reduced plant height (Mizoguchi et al, 2002(Mizoguchi et al, , 2005Ito et al, 2007;Niwa et al, 2007;Lu et al, 2009). Plants whose clock period matches to the environmental cycles show photosynthetic and competitive advantages (Dodd et al, 2005).…”

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confidence: 99%

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Deregulated Copper Transport Affects Arabidopsis Development Especially in the Absence of Environmental Cycles

et al. 2010

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Copper is an essential cofactor for key processes in plants, but it exerts harmful effects when in excess. Previous work has shown that the Arabidopsis (Arabidopsis thaliana) COPT1 high-affinity copper transport protein participates in copper uptake through plant root tips. Here, we show that COPT1 protein localizes to the plasma membrane of Arabidopsis cells and the phenotypic effects of transgenic plants overexpressing either COPT1 or COPT3, the latter being another high-affinity copper transport protein family member. Both transgenic lines exhibit increased endogenous copper levels and are sensitive to the copper in the growth medium. Additional phenotypes include decreased hypocotyl growth in red light and differentially affected flowering times depending on the photoperiod. Furthermore, in the absence of environmental cycles, such as light and temperature, the survival of plants overexpressing COPT1 or COPT3 is compromised. Consistent with altered circadian rhythms, the expression of the nuclear circadian clock genes CIRCADIAN CLOCK-ASSOCIATED1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY) is substantially reduced in either COPT1-or COPT3-overexpressing plants. Copper affects the amplitude and the phase, but not the period, of the CCA1 and LHY oscillations in wild-type plants. Copper also drives a reduction in the expression of circadian clock output genes. These results reveal that the spatiotemporal control of copper transport is a key aspect of metal homeostasis that is required for Arabidopsis fitness, especially in the absence of environmental cues.

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Myb‐like transcription factors have epistatic effects on circadian clock function but additive effects on plant growth

Hughes,

Harmer

2023

Plant Direct

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The functions of closely related Myb‐like repressor and Myb‐like activator proteins within the plant circadian oscillator have been well‐studied as separate groups, but the genetic interactions between them are less clear. We hypothesized that these repressors and activators would interact additively to regulate both circadian and growth phenotypes. We used CRISPR‐Cas9 to generate new mutant alleles and performed physiological and molecular characterization of plant mutants for five of these core Myb‐like clock factors compared with a repressor mutant and an activator mutant. We first examined circadian clock function in plants likely null for both the repressor proteins, CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY), and the activator proteins, REVEILLE 4 (RVE4), REVEILLE (RVE6), and REVEILLE (RVE8). The rve468 triple mutant has a long period and flowers late, while cca1 lhy rve468 quintuple mutants, similarly to cca1 lhy mutants, have poor circadian rhythms and flower early. This suggests that CCA1 and LHY are epistatic to RVE4, RVE6, and RVE8 for circadian clock and flowering time function. We next examined hypocotyl elongation and rosette leaf size in these mutants. The cca1 lhy rve468 mutants have growth phenotypes intermediate between cca1 lhy and rve468 mutants, suggesting that CCA1, LHY, RVE4, RVE6, and RVE8 interact additively to regulate growth. Together, our data suggest that these five Myb‐like factors interact differently in regulation of the circadian clock versus growth. More generally, the near‐norm al seedling phenotypes observed in the largely arrhythmic quintuple mutant demonstrate that circadian‐regulated output processes, like control of hypocotyl elongation, do not always depend upon rhythmic oscillator function.

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Genetic Linkages of the Circadian Clock-Associated Genes, TOC1, CCA1 and LHY, in the Photoperiodic Control of Flowering Time in Arabidopsis thaliana

Cited by 123 publications

References 52 publications

Circadian control of carbohydrate availability for growth inArabidopsisplants at night

Circadian control of carbohydrate availability for growth inArabidopsisplants at night

Deregulated Copper Transport Affects Arabidopsis Development Especially in the Absence of Environmental Cycles

Myb‐like transcription factors have epistatic effects on circadian clock function but additive effects on plant growth

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