Seasonal shift in timing of vernalization as an adaptation to extreme winter

Abstract

The requirement for vernalization, a need for prolonged cold to trigger flowering, aligns reproductive development with favorable spring conditions. In Arabidopsis thaliana vernalization depends on the cold-induced epigenetic silencing of the floral repressor locus FLC. Extensive natural variation in vernalization response is associated with A. thaliana accessions collected from different geographical regions. Here, we analyse natural variation for vernalization temperature requirement in accessions, including those from the northern limit of the A. thaliana range. Vernalization required temperatures above 0°C and was still relatively effective at 14°C in all the accessions. The different accessions had characteristic vernalization temperature profiles. One Northern Swedish accession showed maximum vernalization at 8°C, both at the level of flowering time and FLC chromatin silencing. Historical temperature records predicted all accessions would vernalize in autumn in N. Sweden, a prediction we validated in field transplantation experiments. The vernalization response of the different accessions was monitored over three intervals in the field and found to match that when the average field temperature was given as a constant condition. The vernalization temperature range of 0–14°C meant all accessions fully vernalized before snowfall in N. Sweden. These findings have important implications for understanding the molecular basis of adaptation and for predicting the consequences of climate change on flowering time.Plants are not able to move around and so they need to be able to adapt their growth and development to seasonal changes in their environment. For example, prolonged exposure to cold temperatures during winter can prime some plants to flower when temperatures increase in the spring—a process called vernalization. In these plants, extended periods of cold temperatures lead to lower activity of a gene called FLC, which normally inhibits flowering.In the plant Arabidopsis thaliana, vernalization requires several months of exposure to temperatures between 0–6°C. Recently, A. thaliana plants from southern Europe were found to vary in the temperature requirements for vernalization, responding to temperatures higher than 6°C. This suggested that plants from northern Europe might vernalize preferentially at lower temperatures. Here, Duncan et al. compared vernalization in a collection of A. thaliana plants (or ‘accessions’) sampled from different regions of Sweden and the UK.The experiments show that all the accessions needed temperatures above 0°C to vernalize and that vernalization still worked relatively well at temperatures as high as 14°C. The optimal temperature range for vernalization differed between the accessions, but plants from more northern areas did not necessarily vernalize at lower temperatures. For example, for one particular accession from northern Sweden, the temperature that is optimum for vernalization was 8°C, a notably higher temperature than expected.Historical local climate records suggested that this accession would vernalize before the first snowfall of the winter in North Sweden. Duncan et al. confirmed this proposal with field experiments. Plants were grown in natural field sites in September and then moved into a greenhouse. The experiments show that the plants complete vernalization by November, which strongly suggests that FLC is silenced during autumn rather than during winter, as previously thought. This changed temperature response is due, in part, to a small number of tiny genetic differences in regions of the FLC gene that do not code for protein.These findings have important implications for future studies of vernalization and flowering time, and for understanding how plants will adapt to on going and future climate change. The next step is to understand what causes these changed temperature responses at a molecular level, which should enable selective breeding for flowering and harvest date in a range of crops.