Development of Arabidopsis thaliana leaves at low temperatures releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates

Abstract

Arabidopsis thaliana plants were grown at 23°C and changes in carbohydrate metabolism, photosynthesis and photosynthetic gene expression were studied after the plants were shifted to 5°C. The responses of leaves shifted to 5°C after development at 23°C are compared to leaves that developed at 5°C. Shifting warm developed leaves to 5°C lead to a severe suppression of photosynthesis that correlated with a rapid and sustained accumulation of hexose phosphates and soluble sugars. Associated with the suppression of photosynthesis and the accumulation of soluble sugars was a reduction in the amount of transcript for genes encoding photosynthetic proteins (cab and rbcS). In contrast, leaves that developed at 5°C showed an increase in photosynthesis and control levels of photosynthetic gene expression. This recovery occurred even though leaves that developed at 5°C maintained large pools of soluble sugars. Leaves that developed at 5°C also showed a strong upregulation of the cytosolic pathway for soluble sugar synthesis but not of the chloroplastic pathway for starch synthesis. This was shown at the level of both enzyme activity and the amount of transcript. Thus, development of Arabidopsis leaves at 5°C resulted in metabolic changes that enabled them to produce and accumulate large soluble sugar pools without any associated suppression of photosynthesis or photosynthetic gene expression. These changes were also associated with enhanced freezing tolerance. We suggest that this reprogramming of carbohydrate metabolism associated with development at low temperature is essential to the development of full freezing tolerance and for winter survival of over‐wintering herbaceous annuals.

Cold acclimation of Arabidopsis thaliana results in incomplete recovery of photosynthetic capacity, associated with an increased reduction of the chloroplast stroma

“…This is similar to the acclimation response reported for cereals (Hurry et al , 1994(Hurry et al , 1995Savitch et al 1997Savitch et al , 2000a. However, in contrast to cereals, neither cold stress nor cold acclimation of Arabidopsis plants was associated with a decrease in ATP or in the ATP/ADP ratios (Strand et al 1997;Hurry et al 2000) or in the amount of metabolically accessible Pi (Strand et al 1999;Hurry et al 2000).…”

“…The recovery of photosynthetic activity in Arabidopsis leaves that developed at 5°C has been shown to be associated with a strong increase in the activity of enzymes of the Calvin cycle and of the sucrose biosynthetic pathway. These acclimative changes also result in a pronounced shift in partitioning of newly ®xed carbon into sucrose (Strand et al 1997(Strand et al , 1999Hurry et al 2000). This is similar to the acclimation response reported for cereals (Hurry et al , 1994(Hurry et al , 1995Savitch et al 1997Savitch et al , 2000a.…”

“…2, Table 1). Previous reports have shown that the complete recovery of photosynthetic activity at 5°C and the growth irradiance is associated with an increase in the activity of Calvin cycle enzymes and enzymes of the sucrose biosynthetic pathway (Strand et al 1997(Strand et al , 1999Hurry et al 2000). In this report we show that the development of new leaves at 5°C results in a strong but incomplete recovery of light-saturated photosynthetic CO 2 assimilation and in vivo PSII activity, and with a full recovery of PSI photooxidation (P700 + ) capacity (Table 1, Fig.…”

“…Photosynthesis is also strongly inhibited in Arabidopsis leaves shifted to low temperature and this inhibition is associated with the reduced expression of nuclear-encoded photosynthetic genes (Strand et al 1997). The recovery of photosynthetic activity in Arabidopsis leaves that developed at 5°C has been shown to be associated with a strong increase in the activity of enzymes of the Calvin cycle and of the sucrose biosynthetic pathway.…”

The xanthophyll cycle and acclimation of Pinus ponderosa and Malva neglecta to winter stress

“…Increases in PSII eciency correlated with a reconversion of Z+A to V in both species, but in P. ponderosa, these changes were not accompanied by changes in ATP/ADP. Although there was an elevated absolute level of ATP+ADP in the needles collected predawn in winter relative to summer (see also Hurry et al 1995c;Strand et al 1997), this should not, however, be sucient to reverse the direction of ATPasecatalyzed reactions. The evidence presented here is therefore not consistent with ATP-fueled reverse proton pumping as an underlying mechanism for maintenance of (Z+A)-dependent energy dissipation in overwintering pine needles.…”