Time Lag Between Light and Heat Diurnal Cycles Modulates CIRCADIAN CLOCK ASSOCIATION 1 Rhythm and Growth in Arabidopsis thaliana

Abstract

Plant growth responses to cues such as light, temperature, and humidity enable the entrainment of the circadian rhythms with diurnal cycles. For example, the temperature variations between day and night affect plant growth and accompany the time lag to light cycle. Despite its importance, there has been no systematic investigation into time lags, and the mechanisms behind the entrainment of the circadian rhythms with multiple cycles remain unknown. Here, we investigated systemically the effects of the time lag on the circadian rhythm and growth in Arabidopsis thaliana. To investigate the entrainment status of the circadian clock, the rhythm of the clock gene CIRCADIAN CLOCK ASSOCIATION 1 (CCA1) was measured with a luciferase reporter assay. As a result, the rhythm was significantly modulated by the time lag with +10°C heating for 4 h every day but not −10°C cooling. A model based on coupled cellular oscillators successfully described these rhythm modulations. In addition, seedling growth depended on the time lag of the heating cycle but not that of the cooling cycle. Based on the relationship between the CCA1 rhythms and growth, we established an estimation method for the effects of the time lag. Our results found that plant growth relates to the CCA1 rhythm and provides a method by which to estimate the appropriate combination of light–dark and temperature cycles.

The adaptive nature of the plant circadian clock in natural environments

“…The interaction between time of day and temperature signaling can also influence clock function. In Arabidopsis grown under LD conditions, a 4-h temperature cycle of ±10°C given at different times of day causes unique effects on the oscillator ( Masuda et al, 2020 ). A 10°C increase had a more dramatic effect on CCA1 promoter expression that was time of day dependent compared to a 10°C drop, which had minimal effects overall.…”

“…A 10°C increase had a more dramatic effect on CCA1 promoter expression that was time of day dependent compared to a 10°C drop, which had minimal effects overall. The 10°C increase was associated with greater fresh weight when given at 8 h compared to 14 h after dawn, with a linear relationship between CCA1 amplitude and growth ( Masuda et al, 2020 ). This response may be tuned to the expectation that the warmest part of the day usually occurs in the mid-afternoon rather than near dusk ( Figure 1 ).…”

Transcriptional Regulation of Metabolic and Cellular Processes in Durum Wheat (Triticum turgidum subsp. durum) in the Face of Temperature Increasing

“…This acceleration of plant development has been proposed as an effect of the modification of the circadian clock [24]; some of the signals regulating this mechanism include light and temperature and are associated with the compensation of plant growth in seasonal changes [25]. A study in A. thaliana reported that circadian modifications and their physiological effects, such as an accelerated change to the reproductive stage, are more significant in the increase in temperature than in the decrease [26].…”

CG and CHG Methylation Contribute to the Transcriptional Control of OsPRR37-Output Genes in Rice

“…Circadian clock comprises multiple transcription-translation feedback loops, which function to improve plant environmental adaptation. Altered expression of circadian clock genes, such as CIRCADIAN CLOCK ASSOCIATED1 ( CCA1 ), can increase levels of plant growth and fitness ( Dodd et al, 2005 ; Masuda et al, 2020 ). Meanwhile, expression amplitude of CCA1 is associated with the CHH methylation level in the promoter region, which determines plant growth vigor ( Ng et al, 2014 ).…”