Organ specificity in the plant circadian system is explained by different light inputs to the shoot and root clocks

Abstract

Summary Circadian clocks allow the temporal compartmentalization of biological processes. In Arabidopsis, circadian rhythms display organ specificity but the underlying molecular causes have not been identified. We investigated the mechanisms responsible for the similarities and differences between the clocks of mature shoots and roots in constant conditions and in light : dark cycles.We developed an imaging system to monitor clock gene expression in shoots and light‐ or dark‐grown roots, modified a recent mathematical model of the Arabidopsis clock and used this to simulate our new data.We showed that the shoot and root circadian clocks have different rhythmic properties (period and amplitude) and respond differently to light quality. The root clock was entrained by direct exposure to low‐intensity light, even in antiphase to the illumination of shoots. Differences between the clocks were more pronounced in conditions where light was present than in constant darkness, and persisted in the presence of sucrose. We simulated the data successfully by modifying those parameters of a clock model that are related to light inputs.We conclude that differences and similarities between the shoot and root clocks can largely be explained by organ‐specific light inputs. This provides mechanistic insight into the developing field of organ‐specific clocks.

Circadian Clock and Photoperiodic Flowering in Arabidopsis: CONSTANS Is a Hub for Signal Integration

“…In addition, micrografting experiments demonstrated that the clock in the shoot apex can affect circadian rhythms in root tissues, although the actual nature of the systemic signaling component for rhythm coupling remains unknown . It is noteworthy that mathematical modeling suggests that the difference in clock properties between the shoot and root can be explained by light sensitivity of clock entrainment in each tissue (Bordage et al, 2016). Supporting this idea, tissue-specific clock properties, such as phase variation in clock genes, or different sensitivity to temperature signals, has been reported in intact Arabidopsis plants (Thain et al, 2002;Michael et al, 2003;Yakir et al, 2011).…”

Spatiotemporal Analysis of Localized Circadian Arrhythmias in Plant Roots

“…Plant cells act as self-sustained oscillators, with their own circadian clocks that regulate interactions with surrounding cells. Phase waves in leaves and roots (Fukuda et al, 2007;Wenden et al, 2012;Ukai et al, 2012;Fukuda et al, 2012), differences in inherent periods between tissues (Endo et al, 2014;Takahashi et al, 2015;Bordage et al, 2016), and spatiotemporal analytical data (Fukuda et al, 2007;James et al, 2008;Wenden et al, 2012;Fukuda et al, 2013) suggest that the cellular oscillator network involves nonlinear phenomena. It was also reported that growth and developmental processes in roots exhibit marked spatiotemporal patterns, such as striped waves resulting from strong phase resetting in the elongation-differentiation (ED) region of the root tip.…”

Caracterização do relógio biológico e seu impacto no metabolismo da cana-de-açúcar

“…A novidade neste estudo foi dissecar os diferentes órgãos e detectar em qual estava a dominância de expressão dos genes do oscilador central, especulando sobre a possibilidade de uma sinalização de longa distância sincronizar o funcionamento dos relógios nos órgãos afastados do meristema apical (Takahashi et al, 2015). Embora tenha sido sugerido que o sinal sincronizador entre órgãos seja um metabólito da fotossíntese (James et al, 2008;Haydon et al, 2013;Takahashi et al, 2015), há evidências de que a luz possa ser percebida pelos órgãos e ser o elemento sincronizador entre os relógios dos órgãos de Arabidopsis (Bordage et al, 2016).…”

“…Ou talvez a luz possa ser o fator de sinalização neste caso. Um estudo recente mostrou que em Arabidopsis, a raiz exposta à luz de baixa intensidade é percebida pelo oscilador deste órgão, regulando-o de forma semelhante à exposição a açúcar (Takahashi et al, 2015;Bordage et al, 2016).…”

“…Isto deveria ser considerado importante, pois muitos estudos sugerem que a expressão de genes do oscilador central varia entre órgãos, de modo que há uma influência maior de alguns órgãos sobre outros na regulação da oscilação circadiana (James et al, 2008;Endo et al, 2014;Takahashi et al, 2015). Além disso, as variáveis ambientais, como luz, são percebidas diferentemente pelos relógios dos órgãos de Arabidopsis (Bordage et al, 2016). Estes dados abrem um precedente para hipóteses sobre se a influência do relógio biológico sobre os transcritos é a mesma em todos os órgãos.…”