Interactions between Light and the Circadian Clock in the Regulation of CAT2 Expression in Arabidopsis

Abstract

In Arabidopsis seedlings germinated and grown in continuous light, CATZ mRNA abundance peaks 1 d after imbibition, consistent with the role of catalase in detoxifying HzOz generated during the 8-oxidation of fatty acids stored in the seed. A second peak of CATZ mRNA abundance, of lower amplitude than the initial peak, appears 6 d after imbibition and may be associated with the development of photosynthetic competence and induction of photorespiration. This second peak in steady-state CATZ mRNA abundance is regulated by light and is not seen in etiolated seedlings. CATZ mRNA accumulation is induced by exposure to high-fluence blue or far-red light but not by red light. In addition, light induction is unaffected by severa1 mutations that block blue light-mediated inhibition of hypocotyl elongation (blul, blu2, blu3, hy4), suggesting phytochrome involvement. When etiolated seedlings are transferred to continuous white light, CATZ mRNA rapidly (within 30 min) accumulates. It is interesting that in these seedlings CAT2 mRNA abundance undergoes pronounced oscillations with a circadian (24 h) periodicity, indicating control by the endogenous circadian clock. No such oscillations are detected in CAT2 mRNA abundance in etiolated seedlings prior to illumination. Control of CATZ expression by the circadian clock is also seen in 5-week-old plants grown in a light-dark cycle and transferred either to continu o u~ dark or to continuous light; in continuous light the circadian oscillations in CATZ mRNA abundance persist for at least five circadian cycles, indicating the robustness of this circadian rhythm.

Integrated Temporal Regulation of the Photorespiratory Pathway. Circadian Regulation of Two Arabidopsis Genes Encoding Serine Hydroxymethyltransferase

“…When etiolated seedlings were transferred into continuous light, SHM1 mRNA accumulated to a peak about 24 h after the onset of illumination and then declined slightly, which is reminiscent of the pattern observed with transcripts such as LHCB and CAT2, which are regulated by the circadian clock (Tavladoraki et al, 1989;Zhong et al, 1994Zhong et al, , 1998Millar and Kay, 1996). To directly assess whether a circadian clock controls SHM1 and SHM4 mRNA abundance, we measured mRNA abundance in whole seedlings germinated and grown for 7 d in 12-h light:12-h dark cycles and then released into continuous light.…”

“…Transcription of the RCA gene, which encodes Rubisco activase, a key regulator of Rubisco, is regulated by a circadian clock (Pilgrim and McClung, 1993;Liu et al, 1996). A circadian clock also regulates the mRNA abundance of the photorespiratory catalase gene CAT2 (Zhong et al, 1994), a peroxisomal component of the photorespiratory pathway. Moreover, a circadian clock gates the response of CAT2 to environmental stimuli such as light (Zhong et al, 1998).…”

“…In contrast, both phytochromes A and B contribute to the acute induction of Arabidopsis LHCB (CAB2) mRNA by light (Karlin-Neumann et al, 1988;Anderson et al, 1997). The transfer of etiolated seedlings into continuous white light induces circadian oscillations in LHCB (Tavladoraki et al, 1989;Millar and Kay, 1996) and CATALASE (Zhong et al, 1994(Zhong et al, , 1998 mRNAs. It is likely that the accumulation of SHM1 mRNA observed after 24 h of illumination with white, red, or blue light represents sampling during the peak of the circadian oscillation in SHM1 mRNA, because the phase of the oscillation of SHM1 mRNA is similar to the phases of the oscillations in LHCB and CATALASE 2 mRNAs, both of which peak about 24 h after the onset of illumination.…”

“…Light-regulated genes such as LHCB and CAT2 exhibit an acute response to light within about 4 h of the onset of illumination (Zhong et al, 1994(Zhong et al, , 1998Millar and Kay, 1996). In contrast, SHM1 did not exhibit an acute induction, suggesting that the accumulation of SHM1 mRNA in the light is an indirect response to illumination, and may represent a consequence of the stimulation of photosynthesis and photorespiration in the light.…”

“…The genes encoding the chloroplastic small subunit of Rubisco (RBCS) and Rubisco activase (RCA) exhibit oscillations in mRNA abundance that peak around dawn (Pilgrim and McClung, 1993). Similarly, the mRNA abundance of the peroxisomal photorespiratory catalase (CAT2) exhibits a maximum at the same circadian phase as RBCS and RCA (Zhong et al, 1994;Zhong and McClung, 1996).…”