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

Abstract

Overnight low-temperature exposure inhibits photosynthesis in chilling-sensitive species such as tomato (Lycopersicon esculentum) and cucumber by as much as 60%. In an earlier study we showed that one intriguing effect of low temperature on chilling-sensitive plants is to stall the endogenous rhythm controlling transcription of certain nuclear-encoded genes, causing the synthesis of the corresponding transcripts and proteins to be mistimed when the plant is rewarmed. Here we show that the circadian rhythm controlling the activity of sucrose phosphate synthase (SPS) and nitrate reductase (NR), key control points of carbon and nitrogen metabolism in plant cells, is delayed in tomato by chilling treatments. Using specific protein kinase and phosphatase inhibitors, we further demonstrate that the chilling-induced delay in the circadian control of SPS and NR activity is associated with the activity of critical protein phosphatases. The sensitivity of the pattern of SPS activity to specific inhibitors of transcription and translation indicates that there is a chilling-induced delay in SPS phosphorylation status that is caused by an effect of low temperature on the expression of a gene coding for a phosphoprotein phosphatase, perhaps the SPS phosphatase. In contrast, the chilling-induced delay in NR activity does not appear to arise from effects on NR phosphorylation status, but rather from direct effects on NR expression. It is likely that the mistiming in the regulation of SPS and NR, and perhaps other key metabolic enzymes under circadian regulation, underlies the chilling sensitivity of photosynthesis in these plant species.Most warm-climate plant species are sensitive to brief exposures to low, nonfreezing temperatures. Lowtemperature exposure in combination with high irradiance causes rapid, often very severe inhibition of photosynthesis in a broad range of plants, including maize (Baker et al., 1983), cucumber (Peeler and Naylor, 1988), and tomato (Lycopersicon esculentum) (Martin and Ort, 1985). Several elements that contribute to this inhibition have been identified and all may ultimately arise from the photosynthetic production of oxygen radicals (Wise, 1995). An inhibition of electron-transport capacity originating from damage to the reducing side of PSII is well documented (e.g. Powles et al., 1983;Kee et al., 1986; Percival et al., 1987) and, for moderately sensitive species such as maize, may be the major cause of impaired whole-plant photosynthesis after chilling. However, in the most severely chilling-sensitive species, such as domestic tomato, impaired reductive activation of the stromal bisphosphatases appears to be the dominating factor limiting carbon assimilation after chilling in the light (Sassenrath et al., 1990).Low temperature at night can also cause severe reductions in CO 2 fixation that persist on the day after the chill, even after optimal growth temperatures have been restored. Like the inhibition caused by chilling in the light, it is clear that the primary loss of activity is caused b...

Mutations in the Prokaryotic Pathway Rescue the fatty acid biosynthesis1 Mutant in the Cold

“…3 and 4); before this, they retain a substantial capacity for recovery (Wu et al, 1997). These findings and results from other studies of chilling-sensitive plants (Wu and Browse, 1995;Jones et al, 1998;Thakur et al, 2010) suggest that an elevated level of high-melting-point PG is one of several traits that evolved in tropical and subtropical plants (possibly conferring selective advantage) but that are incompatible with growth in periodically cold climates (Wu and Browse, 1995). It is important to note that our observation of elevated high-melting-point PG in fab1 does not establish this as the cause of damage and death of fab1 plants at 2°C.…”

Contrasting effect of dark-chilling on chloroplast structure and arrangement of chlorophyll–protein complexes in pea and tomato: plants with a different susceptibility to non-freezing temperature

“…Yet the mechanisms involved in dark-chilling are not clearly deWned. Short-term chilling treatments in the dark stalled the circadian rhythms in chlorophyll a/b binding protein and Rubisco activase mRNA expression (Jones et al 1998) and enhanced the abundance of Rubisco small subunit transcripts (van Heerden et al 2003a). Experiments with soybean grown for several days in a chillingnight/warm photoperiod cycle, showed susceptibility of both fructose-1,6-bisphosphatase and photochemistry to a dark-chilling treatment (van Heerden et al 2003a, b).…”

Field Testing of Tomato Chilling Tolerance under Varying Light and Temperature Conditions

“…Spooner, S. chilense (Dunal) Reiche and S. peruvianum L., recover rapidly after exposure to sub-optimal temperatures, which is expressed through greater growth capacity and decreased inhibition of photosynthesis (Brüggemann and Linger, 1994) or minor alterations in N metabolism (Jones et al, 1998). Wild species have been used for constructing genetic maps and identifying genes of agronomic importance.…”