Limited light intensity and low temperature: Can plants survive freezing in light conditions that more accurately replicate the cold season in temperate regions?

Abstract Plants in temperate regions have evolved mechanisms that enable them to survive sudden temperature drops. Experiments with plants grown in long-day conditions, in which they are most sensitive to freezing stress, indicate that the cold acclimation mechanism is light-dependent and does not fully operate under low light intensity. However, winter annuals like Arabidopsis thaliana Col-0 germinate in the fall, overwinter as rosettes, and thus must acclimate under short photoperiods and low irradiance. Thus, we have analysed effects of variations in light intensity in plants grown under short-day photoperiod at the 1.14 growth stage (14 rosette leaves). Plants were acclimated at 4 °C for seven days under control and limited-light conditions: 100 and 20 μmol m-2s-1 photosynthetic photon flux density (PPFD), respectively. All cold-acclimated plants accumulated molecular markers reportedly associated with acquired freezing tolerance, including proline, sucrose, cold-responsive gene transcripts, dehydrins and low temperature-induced proteins. Observed changes (and similarity of freezing stress survival rates of plants in both light conditions) indicate that low PPFD did not inhibit the cold acclimation process. The molecular analysis identified distinct PPFD-specific adaptation mechanisms manifested in contrasting contents of anthocyanins, cytokinin conjugates, photosystem proteins, and enzymes involved in protein, energy, and reactive oxygen species metabolism. Finally, the results identify putative proteins and metabolite markers correlating with susceptibility to freezing stress of non-acclimated plants grown under low PPFD. Our data show that Arabidopsis plants grown under short-day photoperiods can be fully cold-acclimated under limited light conditions, employing standard and PPFD-specific pathways.