Severe cold, defined as a damaging cold beyond acclimation temperatures, has unique responses, but the signaling and evolution of these responses are not well understood. Production of oligogalactolipids, which is triggered by cytosolic acidification in Arabidopsis (Arabidopsis thaliana), contributes to survival in severe cold. Here, we investigated oligogalactolipid production in species from bryophytes to angiosperms. Production of oligogalactolipids differed within each clade, suggesting multiple evolutionary origins of severe cold tolerance. We also observed greater oligogalactolipid production in control samples instead of temperature-challenged samples of some species. Further examination of representative species revealed a tight association between temperature, damage, and oligogalactolipid production that scaled with the cold tolerance of each species. Based on oligogalactolipid production and transcript changes, multiple angiosperm species share a signal of oligogalactolipid production initially described in Arabidopsis, cytosolic acidification. Together, these data suggest that oligogalactolipid production is a severe cold response that originated from an ancestral damage response that remains in many land plant lineages and that cytosolic acidification may be a common signaling mechanism for its activation.

Internal cellular membranes must have their lipid composition remodeled for plants to survive low temperatures. One mechanism necessary for freezing tolerance of the chloroplast envelope membranes is well defined. An enzyme named “Sensitive to Freezing 2” (SFR2) changes monogalactolipid into oligogalactolipids at temperatures below freezing. Interestingly, SFR2 activity does not respond to initial cool temperatures, it only responds to barely tolerable freezing temperatures. Here, we show that SFR2 is post‐translationally regulated by modifications and changes to cytosolic acidification. We show that freezing increases cytosolic acidification and that proton pumps at both the plasma and vacuolar membranes participate in maintaining the acidification during low temperatures. Finally, quantitative measurements of SFR2’s product in a large number of plant species with diverse phylogenetic backgrounds shows that SFR2 is likely responding to membrane damage in some, if not all species. We conclude that plant low temperature sensing and response is likely a continuum rather than a switch, and that internal cellular membranes have systems set up to respond to damage in a diverse set of abiotic stresses.