HSP90, ZTL, PRR5 and HY5 integrate circadian and plastid signaling pathways to regulate CBF and COR expression.

Abstract

The circadian clock synchronizes a wide range of biological processes with the day/night cycle, and correct circadian regulation is essential for photosynthetic activity and plant growth. We describe here a mechanism where a plastid signal converges with the circadian clock to fine-tune the regulation of nuclear gene expression in Arabidopsis (Arabidopsis thaliana). Diurnal oscillations of tetrapyrrole levels in the chloroplasts contribute to the regulation of the nucleus-encoded transcription factors C-REPEAT BINDING FACTORS (CBFs). The plastid signal triggered by tetrapyrrole accumulation inhibits the activity of cytosolic HEAT SHOCK PROTEIN90 and, as a consequence, the maturation and stability of the clock component ZEITLUPE (ZTL). ZTL negatively regulates the transcription factor LONG HYPOCOTYL5 (HY5) and PSEUDO-RESPONSE REGULATOR5 (PRR5). Thus, low levels of ZTL result in a HY5-and PRR5-mediated repression of CBF3 and PRR5-mediated repression of CBF1 and CBF2 expression. The plastid signal thereby contributes to the rhythm of CBF expression and the downstream COLD RESPONSIVE expression during day/night cycles. These findings provide insight into how plastid signals converge with, and impact upon, the activity of well-defined clock components involved in circadian regulation. In a wide range of organisms, the circadian clock synchronizes biological processes with the time of day. The circadian oscillator provides a robust internal rhythm that anticipates daily changes and optimizes the usage of resources with day/night cycles. In Arabidopsis (Arabidopsis thaliana), the clock consists of a repressilator with a series of transcription-translation feedback loops (Pokhilko et al., 2012), and up to 70% of the chloroplast and 36% of the nuclear genomes have been shown to be subject to circadian regulation (Harmer et al., 2000; Schaffer et al., 2001; Michael and McClung, 2003; Michael et al., 2008). Correct circadian regulation in plants is important for photosynthetic activity and growth by synchronizing gene expression, protein modification, and stomatal opening with the light/dark cycle (Hennessey and Field, 1991; Green et al., 2002; Dodd et al., 2005). The mechanisms and signaling pathways that connect the circadian clock with the regulation of photosynthetic activity in the chloroplasts are not well known; however, there are some suggested mechanisms by which the cir-cadian oscillator can communicate timing information to the chloroplast (Dodd et al., 2014). For example, the core subunits of the plastid-encoded polymerase are encoded by the chloroplast genome, but the nucleus-encoded sigma factors are required for promoter specificity and the initiation of transcription (Schweer et al., 2010). The nuclear genome in Arabidopsis encodes six sigma factors (SIG1-SIG6), and their expression is circadian regulated; it was suggested that the circadian timing of the nucleus-encoded sigma factors in turn controls the timing of transcription of the photosynthesis genes encoded in the chloroplast (Noordally et al., 2013). This regulatory control of transcription could provide a way to communicate timing to the chloroplast. Furthermore, it has been suggested that the chloroplast itself is involved in the regulation of the circadian clock and that chloroplast retrograde signals can alter circadian rhythms (Hassidim et al., 2007). Thus, the close interaction between the circadian clock and chloroplast retrograde signaling systems could provide fine-tuning of photosynthetic gene expression and photosynthetic activity during the day. Expression of the nucleus-encoded C-REPEAT BINDING FACTOR (CBF) transcription factors, CBF1, CBF2, and CBF3, is circadian regulated with a peak at the middle of the light period (Bieniawska et al.,