Low temperature interrupts circadian regulation of transcriptional activity in chilling-sensitive plants

Impaired chloroplast function is responsible for nearly two-thirds of the inhibition to net photosynthesis caused by dark chilling in tomato (Lycopersicon esculentum Mill.), yet it has not been possible to localize the dysfunction to specific chloroplast reactions. We report here on an effect that low-temperature exposure has in tomato on the expression of certain nuclear-encoded chloroplast proteins, which may be directly related to the chilling sensitivity of photosynthesis. Transcriptional activity of genes for both the chlorophyll a/b binding protein of photosystem II (Cab) as well as for ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) activase was found to be controlled by an endogenous rhythm. For Cab this rhythm was also visible at the level of newly synthesized protein, indicating that the circadian control of transcriptional activity normally ensures that this protein is synthesized only during daylight hours. However, low-temperature treatment suspended the timing of the rhythm in tomato so that, upon rewarming, the circadian control was reestablished but was displaced from the actual time of day by the length of the chilling exposure. In addition, we found that the normal turnover of Cab and Rubisco activase mRNA was suspended during the low-temperature treatment, but, upon rewarming, this stabilized message was not translated into protein. We believe that the low-temperature-induced mistiming of gene expression together with its effect on the translatability of existing transcripts may be an important clue in unraveling the basis for the chilling sensitivity of photosynthesis in tomato.