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

Abstract

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 H (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.Many plant species that are evolutionarily adapted to warm habitats are very susceptible to injury by low-temperature exposure. Brief exposures to low (00C < T < 10TC), but above freezing, temperatures can have profound effects on seasonlong growth and productivity even though there may be no outward signs of damage. For many chill-sensitive species, an important element of the low temperature-induced injury is an inhibition of photosynthesis.Low-temperature exposure in combination with high irradiance causes rapid inhibition of photosynthesis in a broad range of plants including tomato (1), cucumber (2), and maize (3). Several elements contributing to the inhibition have been identified. Damage to the reducing side of photosystem II is well documented (4-6) and, for moderately sensitive species such as maize, may be the major cause of impaired whole plant photosynthesis following chilling. However, in the most chill-sensitive species, such as tomato (Lycopersicon esculentum), impaired reductive activation of the stromal bisphosphatases appears to be the dominating factor limiting carbon assimilation following chilling in the light (7).Low temperature at night can also cause severe reductions in CO2 fixation on the day following the chill. Like the inhibition caused by chilling in the light, it is clear that the primary loss of activity arises due to direct impairment of chloroplast function (8), but i...

Catalase Is Encoded by a Multigene Family in Arabidopsis thaliana (L.) Heynh

“…CAT2 mRNA is most abundant in leaves and is found in all green (photosynthesizing) organs. CAT2 also exhibits a circadian rhythm in mRNA abundance with peak abundance during the early subjective morning (Zhong et al, 1994), as is seen with photosynthetic genes such as CAB (Kay and Millar, 1993;Piechulla, 1993;McClung and Kay, 1994), RBCS (McClung, 1993), and RCA (Martino-Catt and Ort, 1992;Pilgrim and McClung, 1993;Watillon et al, 1993). Photosynthetic capacity itself peaks in the subjective morning (Sweeney, 1987).…”

Chilling Delays Circadian Pattern of Sucrose Phosphate Synthase and Nitrate Reductase Activity in Tomato1

“…In tomato, low-temperature treatment delays the progress of the circadian clock regulating the transcription of certain nuclear-encoded genes, including cab (chlorophyll a/b binding) and rca (Rubisco activase) (Martino-Catt and Ort, 1992). The clock stops for the duration of the chilling treatment and resumes upon rewarming, but the affected rhythms are then out of phase with the actual time of day.…”

“…Thus, although the inhibition of net photosynthesis by dark chilling in plants such as tomato and cucumber can be quite large, the underlying causes are subtle and are likely to involve disruption of the coordination among the component reactions of photosynthesis rather than direct inhibition of the reactions themselves. An intriguing effect of low temperature on the circadian regulation of transcription (Martino-Catt and Ort, 1992) indicates that the low-temperature-induced inhibition of photosynthesis in tomato may result from the loss of coordination in the expression of critical enzymes controlling photosynthetic metabolism.In tomato, low-temperature treatment delays the progress of the circadian clock regulating the transcription of certain nuclear-encoded genes, including cab (chlorophyll a/b binding) and rca (Rubisco activase) (Martino-Catt and Ort, 1992). The clock stops for the duration of the chilling treatment and resumes upon rewarming, but the affected rhythms are then out of phase with the actual time of day.…”

“…Thus, although the inhibition of net photosynthesis by dark chilling in plants such as tomato and cucumber can be quite large, the underlying causes are subtle and are likely to involve disruption of the coordination among the component reactions of photosynthesis rather than direct inhibition of the reactions themselves. An intriguing effect of low temperature on the circadian regulation of transcription (Martino-Catt and Ort, 1992) indicates that the low-temperature-induced inhibition of photosynthesis in tomato may result from the loss of coordination in the expression of critical enzymes controlling photosynthetic metabolism.…”

Alteration of Gene Expression Associated with Abscisic Acid-Induced Chilling Tolerance in Maize Suspension-Cultured Cells

“…Ort et al (1989) suggested that the synthesis of the 35 Mr protein is not correlated with chilling tolerance, but rather, correlated with the chilling sensitivity of photosynthetic system in chillingsensitive plants. Martino-Catt and Ort (1992) found that chilling interrupts circadian regulation of the transcriptional activity in tomato, and they proposed that chilling-induced mistiming of gene expression is a central factor underlying the chilling sensitivity of photosynthesis in chilling-sensitive plants. The induction of a thiol protease in tomato fruits has been shown to require less chilling in a chilling-sensitive variety than in a less chilling-sensitive one Fischer, 1988, 1990).…”