Acclimation of photosynthesis allows plants to adjust the composition of their photosynthetic apparatus to adapt to changes in the environment, and is important in maintaining fitness. Dynamic acclimation refers to acclimation of fully developed leaves, after developmental processes have ceased. Rates of photosynthesis fluctuate with environmental change, and this requires metabolic adjustments. It has previously been shown that acclimation requires the chloroplastic glucose 6-phosphate/ phosphate translocator GPT2. Using label-free proteomics we characterised the acclimation deficient gpt2 mutant. High light acclimation involves changes in the composition of the photosynthetic proteome and increases in many other metabolic enzymes, but in gpt2 plants, a reduced ability to alter protein composition, and enhanced stress responses were seen. Using a combined transcriptomics and proteomics approach we also analysed acclimation to low temperature. We show that photosynthetic acclimation requires the cytosolic fumarase, FUM2. In fum2 mutants, an enhanced transcriptional response to low temperature was seen, which was impaired at the level of the proteome, relative to the WT. We also identified a protein encoding a β-Amylase, BAM5, that strongly responded to high light acclimation. The role of this protein was further characterised, and we show a nonchloroplastic location. Furthermore, suppression of this gene resulted in plants that were unable to acclimate, and had a reduced sugar content. This research highlights novel and diverse roles for proteins in acclimation, and provides a comprehensive proteomic profiling of high light and low temperature acclimation that has previously been lacking.