Heat Shock–Induced Fluctuations in Clock and Light Signaling Enhance Phytochrome B–Mediated Arabidopsis Deetiolation

Abstract

ORCID ID: 0000-0001-6525-8414 (J.J.C.).Moderately warm constant ambient temperatures tend to oppose light signals in the control of plant architecture. By contrast, here we show that brief heat shocks enhance the inhibition of hypocotyl growth induced by light perceived by phytochrome B in deetiolating Arabidopsis thaliana seedlings. In darkness, daily heat shocks transiently increased the expression of PSEUDO-RESPONSE REGULATOR7 (PRR7) and PRR9 and markedly enhanced the amplitude of the rhythms of LATE ELONGATED HYPOCOTYL (LHY) and CIRCADIAN CLOCK ASSOCIATED1 (CCA1) expression. In turn, these rhythms gated the hypocotyl response to red light, in part by changing the expression of PHYTOCHROME INTERACTING FACTOR4 (PIF4) and PIF5. After light exposure, heat shocks also reduced the nuclear abundance of CONSTITUTIVE PHOTOMORPHOGENIC1 (COP1) and increased the abundance of its target ELONGATED HYPOCOTYL5 (HY5). The synergism between light and heat shocks was deficient in the prr7 prr9, lhy cca1, pif4 pif5, cop1, and hy5 mutants. The evening element (binding site of LHY and CCA1) and G-box promoter motifs (binding site of PIFs and HY5) were overrepresented among genes with expression controlled by both heat shock and red light. The heat shocks experienced by buried seedlings approaching the surface of the soil prepare the seedlings for the impending exposure to light by rhythmically lowering LHY, CCA1, PIF4, and PIF5 expression and by enhancing HY5 stability.

HY5, a positive regulator of light signaling, negatively controls the unfolded protein response inArabidopsis

“…In fact, our qRT-PCR data suggest that the tolerance of the hy5 mutant to ER stress conditions was due to the elevated expression of UPR marker genes in these plants. In conclusion, these results are consistent with those of recent studies suggesting that HY5 is a critical component in the integration of light signaling with different defense responses against stress conditions, an important event for plant survival under adverse conditions (10,31,32).…”

“…Previous studies also suggest that the abundance of HY5 protein is regulated by either low temperature or short heat shock through the 26S proteasomemediated degradation system (10,31). The proteosomal degradation of HY5 and proteolytic cleavage of bZIP28 fine tunes the balance between the two proteins to compete for binding the ERSE motifs and in turn regulate UPR genes.…”

Rapid Decline in Nuclear COSTITUTIVE PHOTOMORPHOGENESIS1 Abundance Anticipates the Stabilization of Its Target ELONGATED HYPOCOTYL5 in the Light

“…The nuclear fluorescence of YFP-COP1 was measured by using confocal microscopy as described (Karayekov et al, 2013). The fluorescence signal caused by nuclear YFP-COP1 followed an exponential decay with a half-life of 2.4 6 0.5 h (mean 6 SE; Fig.…”

PIFs: Systems Integrators in Plant Development

“…Seedling deetiolation also requires integration with the clock, as mutants in several clock components show phy-mediated deetiolation phenotypes, but the mechanism is not well understood (Ito et al, 2007). Interestingly, during deetiolation, daily heat shocks in etiolated seedlings gate hypocotyl growth upon exposure to R light, enhancing hypocotyl inhibition (Karayekov et al, 2013). The proposed mechanism in part involves heat induction of LHY and CCA1 rhythms, which in turn cause oscillations of PIF4 and PIF5 to modulate the seedling ability to respond to light (Karayekov et al, 2013).…”

“…Interestingly, during deetiolation, daily heat shocks in etiolated seedlings gate hypocotyl growth upon exposure to R light, enhancing hypocotyl inhibition (Karayekov et al, 2013). The proposed mechanism in part involves heat induction of LHY and CCA1 rhythms, which in turn cause oscillations of PIF4 and PIF5 to modulate the seedling ability to respond to light (Karayekov et al, 2013). In the case of cold, the circadian clock regulates the expression and gates the cold induction of the C-repeat binding factors CBF1, 2, and 3, a pathway with a major role in plant cold acclimation and freezing tolerance.…”