System Identification of the Arabidopsis Plant Circadian System

Mathias Foo,David E. Somers,김판준 한국물리학회 2015 THE JOURNAL OF THE KOREAN PHYSICAL SOCIETY Vol.66 No.4

The circadian system generates an endogenous oscillatory rhythm that governs the daily activitiesof organisms in nature. It offers adaptive advantages to organisms through a coordination of theirbiological functions with the optimal time of day. In this paper, a model of the circadian systemin the plant Arabidopsis (species thaliana) is built by using system identification techniques. Priorknowledge about the physical interactions of the genes and the proteins in the plant circadian systemis incorporated in the model building exercise. The model is built by using primarily experimentallyverifieddirect interactions between the genes and the proteins with the available data on mRNAand protein abundances from the circadian system. Our analysis reveals a great performance of themodel in predicting the dynamics of the plant circadian system through the effect of diverse internaland external perturbations (gene knockouts and day-length changes). Furthermore, we found thatthe circadian oscillatory rhythm is robust and does not vary much with the biochemical parametersexcept those of a light-sensitive protein P and a transcription factor TOC1. In other words, thecircadian rhythmic profile is largely a consequence of the network’s architecture rather than itsparticular parameters. Our work suggests that the current experimental knowledge of the geneto-protein interactions in the plant Arabidopsis, without considering any additional hypotheticalinteractions, seems to suffice for system-level modeling of the circadian system of this plant and topresent an exemplary platform for the control of network dynamics in complex living organisms.

The Importance of the Plant Circadian Clock to Confer Heat Tolerance

( Tae Sung Kim ),( David E Somers ),( Yong Jin Park ) 한국육종학회 2014 Plant Breeding and Biotechnology Vol.2 No.4

Most eukaryotic organisms display specialized cellular and behavioral oscillations with a period of approximately 24 hours, which are called circadian rhythms. The biological clock generates a rhythm that conveys temporal information over a day. Through this system, most eukaryotic organisms appropriately respond to daily or seasonal environmental changes by regulating their physiology and development in a time-dependent manner, conferring the organism with an adaptive advantage. In plants, the endogenous timing system also controls many important physiological processes including flower opening, hormone synthesis, metabolic pathways and gene expression so that these sessile species may survive efficiently in changing environments. Temperature compensation (TC) is one of the defining features of the clock mechanism. Under this mechanism, the pace of the clock, or period, remains stable over a broad range of physiologically relevant temperatures, which is unlikely to happen in other biochemical reactions. Thus, this mechanism allows organisms to sustain their ordinary life in various thermal environments by providing an accurate measure of the passage of time, regardless of the ambient temperature. Considering the current global climate changes our planet is undergoing, understanding the fundamental mechanism underlying TC cannot be overemphasized. In this review, we discuss the molecular organization of the plant circadian clock and the concept of TC, as well as the significance of plant TC in conferring fitness under the current increasing thermal environments.

The importance of the natural variation in the plant circadian clock to enhance crop productivity under high temperature environments

Tae-Sung Kim,Yong-Jin Park,David E. Somers 한국육종학회 2014 한국육종학회 심포지엄 Vol.2014 No.07

Most eukaryotic organisms, including plants, display specialized cellular and behavioral rhythms with a period of approximately 24 hours. The circadian clock generates this rhythm to convey daily or seasonal basis of temporal information, coordinating the proper phasing of many important cellular processes. Temperature compensation (TC) is one of the defining features of the clock mechanism. Under this function, the speed of the clock or period remains relatively constant over physiologically relevant temperatures, unlike the biochemical reactions. Thus, TC allows organisms to sustain their life ordinarily in various thermal environments by providing an accurate measure of the passage of time regardless of surrounding temperatures. Previously, Edward and his colleagues performed a quantitative trait loci (QTL) study to find TC related natural variations in the recombinant inbred line (RIL) population from two Arabidopsis ecotypes, which are adapted to different thermal environments; one parent is Cvi accession (Cvi) which originates from the warm climate, Cape Verde Island, and the other is Ler accession (Ler) from Northern Europe. For the two most significant QTLs, the core clock components in Arabidopsis clock, GIGANTEA (GI) and ZEITLUPE (ZTL) are proposed as strong candidates. Moreover, the amino acid substitution leading to GICvi and ZTLCvi (Ler to Cvi) are suggested to be the causal factors for the TC QTLs respectively. However, precise molecular mechanisms of these natural variations on TC are still not understood well. Here, we elucidate the molecular impact of the natural variation shaping GICvi and ZTLCvi on TC function. GICvi and ZTLCvi post-translationally regulate ZTL stability in antagonistic way, resulting in the opposite period/clock effects mediated by ZTL protein abundance. However, if both GICvi and ZTLCvi are present, they mutually balance their own effect on ZTL, which in turn supports TC capacity of Cvi especially at high temperatures. Considering the amino acid residues in GI and ZTL, where the natural variations arise, are highly conserved across many important crop species including rice, corn, cabbage and etc., this research will give valuable insights into the TC related thermal adaptive processes in Arabidopsis as well as those important crop plants.

Balanced Nucleocytosolic Partitioning Defines a Spatial Network to Coordinate Circadian Physiology in Plants

Kim, Y.,Han, S.,Yeom, M.,Kim, H.,Lim, J.,Cha, J.Y.,Kim, W.Y.,Somers, David E.,Putterill, J.,Nam, H.,Hwang, D. Cell Press 2013 Developmental cell Vol.26 No.1

Biological networks consist of a defined set of regulatory motifs. Subcellular compartmentalization of regulatory molecules can provide a further dimension in implementing regulatory motifs. However, spatial regulatory motifs and their roles in biological networks have rarely been explored. Here we show, using experimentation and mathematical modeling, that spatial segregation of GIGANTEA (GI), a critical component of plant circadian systems, into nuclear and cytosolic compartments leads to differential functions as positive and negative regulators of the circadian core gene, LHY, forming an incoherent feedforward loop to regulate LHY. This regulatory motif formed by nucleocytoplasmic partitioning of GI confers, through the balanced operation of the nuclear and cytosolic GI, strong rhythmicity and robustness to external and internal noises to the circadian system. Our results show that spatial and functional segregation of a single molecule species into different cellular compartments provides a means for extending the regulatory capabilities of biological networks.

ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light

Kim, Woe-Yeon,Fujiwara, Sumire,Suh, Sung-Suk,Kim, Jeongsik,Kim, Yumi,Han, Linqu,David, Karine,Putterill, Joanna,Nam, Hong Gil,Somers, David E. Nature Publishing Group 2007 Nature Vol.449 No.7160

The circadian clock is essential for coordinating the proper phasing of many important cellular processes. Robust cycling of key clock elements is required to maintain strong circadian oscillations of these clock-controlled outputs. Rhythmic expression of the Arabidopsis thaliana F-box protein ZEITLUPE (ZTL) is necessary to sustain a normal circadian period by controlling the proteasome-dependent degradation of a central clock protein, TIMING OF CAB EXPRESSION 1 (TOC1). ZTL messenger RNA is constitutively expressed, but ZTL protein levels oscillate with a threefold change in amplitude through an unknown mechanism. Here we show that GIGANTEA (GI) is essential to establish and sustain oscillations of ZTL by a direct protein–protein interaction. GI, a large plant-specific protein with a previously undefined molecular role, stabilizes ZTL in vivo. Furthermore, the ZTL–GI interaction is strongly and specifically enhanced by blue light, through the amino-terminal flavin-binding LIGHT, OXYGEN OR VOLTAGE (LOV) domain of ZTL. Mutations within this domain greatly diminish ZTL–GI interactions, leading to strongly reduced ZTL levels. Notably, a C82A mutation in the LOV domain, implicated in the flavin-dependent photochemistry, eliminates blue-light-enhanced binding of GI to ZTL. These data establish ZTL as a blue-light photoreceptor, which facilitates its own stability through a blue-light-enhanced GI interaction. Because the regulation of GI transcription is clock-controlled, consequent GI protein cycling confers a post-translational rhythm on ZTL protein. This mechanism of establishing and sustaining robust oscillations of ZTL results in the high-amplitude TOC1 rhythms necessary for proper clock function.