A high-throughput delayed fluorescence method reveals underlying differences in the control of circadian rhythms in Triticum aestivum and Brassica napus

Rees, Hannah; Duncan, Susan; Gould, Peter; Wells, Rachel; Greenwood, Mark; Brabbs, Thomas; Hall, Anthony

doi:10.1186/s13007-019-0436-6

Cited by 21 publications

(34 citation statements)

References 56 publications

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“…Interestingly, rhythms appeared to be most robust at 22°C, which might not be expected given that the warmest months in Sweden average around 15-17°C. A similar loss of rhythm robustness at lower temperatures has been observed in wheat(23).…”

Section: Discussionsupporting

confidence: 79%

“…Six 96-well plates can be imaged simultaneously in each cabinet. Imaging conditions were exactly those described for constant light (L:L) imaging of Brassica leaves in Rees et al 2019(23). Images were captured every hour with a 1-minute exposure time.…”

Section: Methodsmentioning

confidence: 99%

“…The extent of temperature compensation has been shown to vary between accessions(20,22). Rhythm robustness is also strongly affected by temperature, although the temperature which produces the most rhythmic oscillations appears to be dependent on the species and circadian assay used (22,23). Plants with clocks which resonate with environmental conditions are typically fittest, however it has been suggested that in climates with large seasonality there may be a compromise for clocks which are adaptable to rapidly changing day-lengths(6).…”

Section: Introductionmentioning

confidence: 99%

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Circadian diversity in SwedishArabidopsisaccessions is associated with naturally occurring genetic variation inCOR28

Rees

Joynson

Brown

et al. 2019

Preprint

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Circadian clocks have evolved to resonate with external day and night cycles. However, these entrainment signals are not consistent everywhere and vary with latitude, climate and seasonality. This leads to divergent selection for clocks which are locally adapted. To investigate the genetic basis for this, we used a Delayed Fluorescence (DF) imaging assay to screen 191 naturally occurring Swedish Arabidopsis accessions for their circadian phenotypes. We demonstrate period variation with both latitude and sub-population. Several candidate loci linked to period, phase and Relative Amplitude Error (RAE) were revealed by genome-wide association mapping and candidate genes were investigated using TDNA mutants. We show that natural variation in a single non-synonymous substitution within COR28 is associated with a long-period and late-flowering phenotype similar to that seen in TDNA knock-out mutants. COR28 is a known coordinator of flowering time, freezing tolerance and the circadian clock; all of which may form selective pressure gradients across Sweden. Finally, we tested circadian variation under reduced temperatures and show that fast and slow period phenotypic tails remain diverged and follow a distinctive ‘arrow-shaped’ trend indicative of selection for a cold-biased temperature compensation response.

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Section: Discussionsupporting

confidence: 79%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Circadian diversity in SwedishArabidopsisaccessions is associated with naturally occurring genetic variation inCOR28

Rees

Joynson

Brown

et al. 2019

Preprint

Self Cite

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“…Images were taken every 90 min for 6 d, with an exposure time of 20 min. Images were taken using a LUMO charge-coupled device camera (QImaging, Canada) controlled using Micro-Manager (V2.0; Open Imaging) as previously described [89,90]. The camera lens (Xenon 25 mm f/0.95; Schneider, Germany) was modified with a 5-mm optical spacer (Cosmicar, Japan) to increase the focal length and decrease the working distance.…”

Section: Luciferase Imagingmentioning

confidence: 99%

Coordinated circadian timing through the integration of local inputs in Arabidopsis thaliana

et al. 2019

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Individual plant cells have a genetic circuit, the circadian clock, that times key processes to the day-night cycle. These clocks are aligned to the day-night cycle by multiple environmental signals that vary across the plant. How does the plant integrate clock rhythms, both within and between organs, to ensure coordinated timing? To address this question, we examined the clock at the sub-tissue level across Arabidopsis thaliana seedlings under multiple environmental conditions and genetic backgrounds. Our results show that the clock runs at different speeds (periods) in each organ, which causes the clock to peak at different times across the plant in both constant environmental conditions and light-dark (LD) cycles. Closer examination reveals that spatial waves of clock gene expression propagate both within and between organs. Using a combination of modeling and experiment, we reveal that these spatial waves are the result of the period differences between organs and local coupling, rather than long-distance signaling. With further experiments we show that the endogenous period differences, and thus the spatial waves, can be generated by the organ specificity of inputs into the clock. We demonstrate this by modulating periods using light and metabolic signals, as well as with genetic perturbations. Our results reveal that plant clocks can be set locally by organ-specific inputs but coordinated globally via spatial waves of clock gene expression.PLOS Biology | https://doi.org/10.days at near-cellular resolution (Materials and methods). This reporter line was chosen because of its strong expression level and its similar spatial expression to other clock components [5].In order to observe the endogenous component of the rhythms, we first imaged seedlings under LL, having previously grown them under LD cycles (LD-to-LL; Fig 2A and Materials and methods). Under the LD-to-LL condition we observed phase differences of GI::LUC expression between organs ( Fig 2B and 2C). The cotyledon and hypocotyl peaked before the root, but the tip of the root peaked before the middle region of the root (Fig 2C, S1 Fig, and S1 Video). Furthermore, we observed a decrease in coherence between regions over time, with a range between the earliest and latest peaking region of 4.92 ± 3.79 h (mean ± standard deviation) in the first and 18.36 ± 5.67 h in the final oscillation. This is due to the emergence of period differences between all regions ( Fig 2D). The cotyledon maintained a mean period of 23.82 ± 0.60 h, whereas the hypocotyl and root ran at 25.41 ± 0.91 h and 28.04 ± 0.86 h, respectively. However, the root tip ran slightly faster than the middle of the root, with a mean period of 26.90 ± 0.45 h, demonstrating the presence of endogenous period differences across all regions. We verified that our results were not specific to the GI::LUC reporter, as we observed similar differences in periods and phases across the plant using luciferase reporters for promoter activity of the core clock genes PSEUDO-RESPONSE REGULATOR 9 (PRR9) [31], TI...

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“…The extent of temperature compensation has been shown to vary between Arabidopsis accessions (Gould et al, 2006; Kusakina, Gould, & Hall, 2014). Rhythm robustness is also strongly affected by temperature, although the temperature which produces the most rhythmic oscillations appears to be dependent on the species and circadian assay used (Kusakina et al, 2014; Rees et al, 2019). Plants with clocks which resonate with environmental conditions are typically fittest, however it has been suggested that in climates with large seasonality there may be a compromise for clocks which are adaptable to rapidly changing day‐lengths (Michael et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

Naturally occurring circadian rhythm variation associated with clock gene loci in Swedish Arabidopsis accessions

Rees

Joynson

Brown

et al. 2021

Plant Cell & Environment

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Circadian clocks have evolved to resonate with external day and night cycles. However, these entrainment signals are not consistent everywhere and vary with latitude, climate and seasonality. This leads to divergent selection for clocks which are locally adapted. To investigate the genetic basis for this circadian variation, we used a delayed fluorescence imaging assay to screen 191 naturally occurring Swedish Arabidopsis accessions for their circadian phenotypes. We demonstrate that the period length co‐varies with both geography and population sub‐structure. Several candidate loci linked to period, phase and relative amplitude error (RAE) were revealed by genome‐wide association mapping and candidate genes were investigated using TDNA mutants. We show that natural variation in a single non‐synonymous substitution within COR28 is associated with a long‐period and late‐flowering phenotype similar to that seen in TDNA knock‐out mutants. COR28 is a known coordinator of flowering time, freezing tolerance and the circadian clock; all of which may form selective pressure gradients across Sweden. We demonstrate the effect of the COR28‐58S SNP in increasing period length through a co‐segregation analysis. Finally, we show that period phenotypic tails remain diverged under lower temperatures and follow a distinctive “arrow‐shaped” trend indicative of selection for a cold‐biased temperature compensation response.

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A high-throughput delayed fluorescence method reveals underlying differences in the control of circadian rhythms in Triticum aestivum and Brassica napus

Cited by 21 publications

References 56 publications

Circadian diversity in SwedishArabidopsisaccessions is associated with naturally occurring genetic variation inCOR28

Circadian diversity in SwedishArabidopsisaccessions is associated with naturally occurring genetic variation inCOR28

Coordinated circadian timing through the integration of local inputs in Arabidopsis thaliana

Naturally occurring circadian rhythm variation associated with clock gene loci in Swedish Arabidopsis accessions

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