Vernalisation. Control of Vernalisation through the Floral Repressor FLC

Many plant species will not flower unless they have experienced winter cold. Avoidance of unfavourable conditions in this way maximises reproductive success. It implies that an individual plant retains a memory of a stress exposure. Vernalisation shows a time course very different from that of cold acclimation. The latter is triggered by comparatively brief cold exposure of minutes to hours. Vernalisation, in contrast, usually requires several weeks of cold. In fact, early physiological experiments showed that the memory of cold exposure can remain intact for many months.

When a plant with a flowering behaviour that is dependent on the day length and vernalisation is exposed to cold and then cultivated for a long time under a day/night cycle that represses flowering, it will flower when shifted to the permissive day length. Thus, the memory does not fade during the growth in the “wrong” day/night cycle. The memory of cold survives even when meristematic cells give rise to a new individual in tissue culture, that is, through vegetative propagation. The new individual behaves as if it had experienced the winter itself, not just the mother plant it is derived from.

How does this reliable memory work without a brain? Friedrich Laibach observed that there are winter annual accessions of A. thaliana that require vernalisation and there are summer annual accessions that do not. Genetic analyses of this difference led to the identification of Flowering Locus C (FLC). When the underlying gene was cloned it became clear that in winter annual accessions, the expression of FLC is gradually repressed during vernalisation (Fig. 2.35) (Amasino 2010). FLC acts as a repressor of flowering (Fig. 2.31) and has to be inactivated before the transition into the reproductive phase can occur. FLC inactivation proceeds through epigenetic changes.

Fig. 2.35. Control of vernalisation through the floral repressor FLC. In winter annual accessions of Arabidopsis thaliana (note that the flower morphology and petal colour in the figure are not representative of A. thaliana), flowering occurs late unless winter conditions have been experienced. The FRIGIDA (FRI)- dependent expression of FLC suppresses the transition to flowering. Prolonged exposure to cold gradually inactivates FLC via histone modifications, that is, through an epigenetic mechanism. Plants acquire a mitotically stable memory of winter and flower earlier

Chromatin at the FLC locus changes from an active state, allowing transcription of the gene to an inactive state. This change is associated with alterations in the post-translational modification of histones. The DNA thread is wrapped around histones and, depending on the molecular appearance of the histones, other proteins are recruited that either promote or suppress gene activity. Histone modifications represent one of the classic epigenetic mechanisms (see molecular biology textbooks).

When cells undergo mitosis and divide, the information—that is, the pattern of histone modification—is passed onto the daughter cells. In this way the memory is maintained over long periods of time. After sexual reproduction, however, the vernalisation has to be reset, otherwise the next generation would not be able to adequately respond to its environment; for example, the plants would flower without experiencing a winter first, which could clearly be disastrous. Therefore, the epigenetic mark at the FLC locus is erased during the formation of gametes in meiosis.

The summer annual habit of some A. thaliana accessions arose through defects in the genes underlying the vernalisation requirement. Loss-of-function mutations in either the FLC gene itself or the gene FRIGIDA (FRI), which activates FLC (Johanson et al. 2000), can turn A. thaliana into a rapid cycler that no longer needs exposure to winter conditions. These mutations represent an early documented example of how a loss of gene function can lead to a dramatic change in a life history trait that may confer a potential competitive advantage in particular habitats.

The key role of FLC is not restricted to annual plants. As is the case for CO and FT, different life history traits and strategies are mediated by variations in the same factors. The crucifer Arabis alpina is perennial, that is, it goes through repeated cycles of vegetative and reproductive growth. The FLC orthologue in A. alpina (PEP1, for Perpetual floweringl) controls this behaviour as well. In contrast to the annual plant A. thaliana, the inactivation of FLC by epigenetic changes during long cold exposure is only transient in A. alpina (Wang et al. 2009). The plants “forget” the winter experience after a while and are again ready to respond to the next seasonal cycle.