Cold is known to markedly inhibit rates of photosynthesis, via both its kinetic effects on protein activity and membrane fluidity. Rapid increases in soluble sugars also contribute to an inhibition of photosynthesis through feedback inhibition and down-regulation of nuclear-encoded photosynthetic gene expression. Extended cold-treatment of pre-existing leaves can also result in photodamage; low temperature slows the consumption of ATP and NADPH by the Calvin cycle and the resulting over-reduction of the photosynthetic electron transport chain may cause oxidative damage to the light-harvesting machinery. A further (and important) limitation is the exhaustion of chloroplastic orthophosphate (Pi) required for ATP regeneration and maintenance of the thylakoid membrane proton gradient, which in turn drives the chloroplastic electron transport chain. Calvin cycle turnover also decreases (explaining the observed decline in carbon assimilation) as this relies on ATP to drive the regeneration of ribulose-1,5-bisphosphate (RuBP) reduction.
Recovery of photosynthesis occurs during cold acclimation via an increase in the export of chloroplastic triose phosphates across an antiporter that exchanges these Calvin cycle intermediates for cytosolic Pi. As Pi is produced in the cytosol during sucrose synthesis, the recovery of sucrose metabolism via increases in the abundance and activity of SPS and cytosolic fructose 1,6 bisphosphatase (cFBPase) is an important step in the restoration of photosynthetic function during cold acclimation, and has also been suggested to be partly responsible for the decrease in sensitivity to photoinhibition that occurs following cold acclimation. Also contributing to the recovery of photosynthesis is the increase in the abundance and activity of several proteins directly involved in photosynthesis.
The photosynthetic phenotype of cold-developed leaves has been suggested to be distinct from that of pre-existing leaves. Cold-developed leaves exhibit marked physical changes compared to warm-grown leaves (Figure 14.23). Leaves developed in the cold tend to be thicker, with a higher leaf mass per area and higher nitrogen and protein concentrations than leaves developed at warmer temperatures.
Figure 14.23. (A) Warm-grown (left), 10-day cold-treated (centre) and cold-developed (right) shoot phenotypes of Arabidopsis thaliana. Warm-grown plants experienced 25/20°C day/night temperatures, whereas cold-treated and cold-developed plants were exposed to constant 5°C. (B) and (C) show transverse sections of representative warm-grown and cold-developed leaves, respectively (Source: Atkin et al. 2006).
Cold developed leaves can accumulate soluble sugars without the suppression of carbon assimilation typically associated with an abundance of photosynthates, and the transcript and protein abundance of most of the Calvin cycle enzymes have been found to be greatly increased in these leaves. The abundance of ribulose-1,5-bisphosphate carboxylase oxygenase (Rubisco) increases, whereas the other Calvin cycle enzymes tend to decline with cold acclimation relative to Rubisco. Further recovery of sucrose synthesis in cold developed leaves assists in the recovery from cold stress and photoinhibition; SPS transcript abundance, protein and the activity of the enzyme increases relative to the Calvin cycle and starch synthesis during acclimation. Associated with the increase in photosynthetic capacity in cold developed leaves is a change in electron transport capacity relative to carboxylation capacity, and an alleviation of triose phosphate utilization (TPU) limitation. Alleviation of TPU limitation during acclimation to low temperatures has been ascribed to increasing activity and transcription of SPS and cFBPase, and the redistribution of inorganic phosphate between cellular compartments. The net result of these changes is an increase in photosynthetic capacity in newly developed, relative to pre-existing, leaves. This phenomenon may therefore optimise the function of these new leaves to their environment.