Abstract

The E3 ubiquitin ligase COP1 (CONSTITUTIVE PHOTOMORPHOGENIC1) plays a key role in the repression of the plant photomorphogenic development in darkness. In the presence of light, COP1 is inactivated by a mechanism which is not completely understood. This leads to accumulation of COP1’s target transcription factors, which initiates photomorphogenesis, resulting in dramatic changes of the seedling’s physiology.Here we use a mathematical model to explore the possible mechanism of COP1 modulation upon dark/light transition in Arabidopsis thaliana based upon data for two COP1 target proteins: HY5 and HFR1, which play critical roles in photomorphogenesis. The main reactions in our model are the inactivation of COP1 by a proposed photoreceptor-related inhibitor I and interactions between COP1 and a CUL4 (CULLIN4)-based ligase. For building and verification of the model, we used the available published and our new data on the kinetics of HY5 and HFR1 together with the data on COP1 abundance. HY5 has been shown to accumulate at a slower rate than HFR1. To describe the observed differences in the timecourses of the “slow” target HY5 and the “fast” target HFR1, we hypothesize a switch between the activities of COP1 and CUL4 ligases upon dark/light transition, with COP1 being active mostly in darkness and CUL4 in light. The model predicts a bi-phasic kinetics of COP1 activity upon the exposure of plants to light, with its restoration after the initial decline and the following slow depletion of the total COP1 content. CUL4 activity is predicted to increase in the presence of light. We propose that the ubiquitin ligase switch is important for the complex regulation of multiple transcription factors during plants development. In addition, this provides a new mechanism for sensing the duration of light period, which is important for seasonal changes in plant development.

Highlights

  • Plants undergo massive changes in the transcriptional profiles of $ 20% of their entire genome upon first exposure to light, when their developmental program switches from skotomorphogenesis in darkness to photomorphogenesis in light (Jiao et al, 2005). This causes drastic changes in plant physiology, which includes shortening of hypocotyl, concomitant opening and expansion of cotyledon and differentiation of chloroplasts (Jiao et al, 2007; Khanna et al, 2006). These changes are driven by the massive accumulation of light-responsive transcription factors, such as HY5, HFR1 and others, which were shown to be the key positive regulators of photomorphogenesis (Jiao et al, 2007; Osterlund et al, 2000; Zhang et al, 2008)

  • COP1 is abundant in darkness and involved in degradation of light-inducible transcription factors, such as HY5, HFR1, LAF1, BIT1 and others (Duek et al, 2004; Hong et al, 2008; Osterlund et al, 2000; Saijo et al, 2003; Seo et al, 2003)

  • At the first step we considered a simple scheme of reactions with only one-sided negative regulation of CUL4 activity by active COP1 (Scheme 1 of Fig. 2A; model equations are presented in Appendix)

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Summary

Introduction

Plants undergo massive changes in the transcriptional profiles of $ 20% of their entire genome upon first exposure to light, when their developmental program switches from skotomorphogenesis in darkness to photomorphogenesis in light (Jiao et al, 2005). The model explained this fall by the restoration time, h. More recent studies demonstrated that the changes in SPA protein concentrations are relatively slow compared to the fast changes in the kinetics of COP1 targets (Zhu et al, 2008) This suggests that the fast changes in COP1/CUL4 system upon dark/light transitions are mainly determined by some other components of the system, such as CSN, CDD and CAND1. The model suggests a new mechanism of light perception by the ligase switch in plants

Experimental Methods
Simple mathematical model
Findings
Full mathematical model

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