Early detection of daylength variations with a feedforward circuit co-regulated by circadian rhythm and diel light-dark cycle

Abstract Light-entrained circadian clocks confer rhythmic dynamics of cellular and molecular activities to animals and plants. These intrinsic clocks allow stable anticipations to light-dark (diel) cycles. Many genes in the model plant Arabidopsis thaliana are regulated by diel cycles via pathways independent of the clock, suggesting that the integration of circadian and light signals is important for the fitness of plants. Previous studies of light-clock signal integrations have focused on moderate phase adjustment of the two signals. However, dynamical features of integrations across a broad range of phases remain elusive. We recently found that phosphorylation of RIBOSOMAL PROTEIN OF THE SMALL SUBUNIT 6 (RPS6 or eS6), a ubiquitous post-translational modification across kingdoms, is influenced by the circadian clock and the light-dark (diel) cycle in an opposite manner. In order to understand this striking phenomenon and its underlying information processing capabilities, we built a mathematical model for the eS6-P control circuit. We found that the dynamics of eS6-P can be explained by a feedforward circuit with inputs from both circadian and diel cycles. Furthermore, the early-day response of this circuit with dual rhythmic inputs is sensitive to the changes in daylength, including both transient and gradual changes observed in realistic light intervals across a year, due to weather and seasons. By analyzing published gene expression data, we found that the dynamics produced by the eS6-P control circuit can be observed in the expression profiles of a large number of genes. Our work provides mechanistic insights into the complex dynamics of a ribosomal protein, and it proposes a previously underappreciated function of the circadian clock which not only prepares organisms for normal diel cycles but also helps to detect both transient and seasonal changes with a predictive power. Author summary Circadian clocks provide animals and plants with internal rhythmic dynamics that anticipate light-dark cycles in a consistent fashion. Many genes in plants are controlled by both the circadian clock and light-dark cycles through independent pathways. One paradigm for the interaction between clock and light signaling pathways is expressed in the ‘external coincidence’ model, which explains the seasonal flowering of plants in response to daylength. However, it is unclear how many different such paradigms can be encoded in the light-and-clock signaling network. Based on a recent observation that circadian rhythms and light-dark cycles drive the phosphorylation of ribosomal protein eS6 with opposing phases, we built a mathematical model for the eS6 phosphorylation (eS6-P). We found that these observations can be explained by a feedforward circuit describing a clock-independent light pathway and a clock-dependent pathway that influences eS6-P dynamics across the day. This circuit has the remarkable feature of detecting the daylength variations at the beginning of a day by integrating the signals from the clock and the light-dark cycles in a phase-sensitive manner. We used realistic photoperiod data to show that the circuit can detect both transient (weather) and long-term (seasonal) changes in daylength variations. These results show rich dynamic information from clock-light signal integration and suggest a new property of the circadian clock in robustly detecting changes in light conditions.