Swedish University of Agricultural Sciences, Department of Plant Biology & Linnean Center for Plant Biology, PO-Box 7080, SE-75007 Uppsala, Sweden
Strolling through gardens and nature in March, one sees signs of spring everywhere. It is less the fresh green of young leaves but rather the colour of first flowers that attract the attention of the eye. Naturally – plants flower in spring. Although this sounds like a trivial statement, do we know how plants tell time? Admittedly, we know a lot: day length (photoperiod) is a mighty signal of spring and coming summer, often promoting floral activators such as the florigen FT. Rising temperatures are similarly effective to stimulate the earliest plants of the year to flower. Gardeners observed that climate change with milder early springs brings typical bulbous spring flowers to blossom earlier than they used to. Many plants, however, flower only later in the year and possibly not at all within their first year. Requiring weeks or even months of winter cold to permit subsequent flowering is common to vernalization-dependent plants (Chouard, 1960). Much research has focused on molecular mechanisms of vernalization, and in the model Brassicaceae Arabidopsis it is well established that the main responsibility to prevent or delay flowering before the winter lies with the repressor FLC, which keeps FT inactive (van Dijk, 2015). Winter cold in turn stably switches off expression of the repressor clearing the stage for flowering. Chromatin-based (epigenetic) mechanisms ensure that FLC remains switched off long after the cold of winter has passed. A protein complex that contains the Polycomb group proteins VRN2 converts chromatin at the FLC locus into a repressive local wall (Zografos et al., 2012).
Many molecular mechanisms and pathways are widely conserved in nature – FT, for instance, is an activator of flowering in all flowering plants. In contrast, vernalization pathways are not conserved. It is thought that as plant families spread from warmer into winter-cold regions, vernalization evolved multiple times independently. Many plants do not even carry an FLC gene. Not surprisingly, temperate grasses establish flowering after cold very differently to Arabidopsis. Cold regulates grass FT but homologs of Arabidopsis FLC or VRN2 are not involved (Fjellheim et al., 2014). Also sugar beet, where vernalization is of great economic relevance, has its unique way to detect winter. It uses a pair of FT paralogs differentially regulated by cold but as far as we know no FLC or VRN2 homologs (Pin et al., 2010). Recent work from the Putterill group now shows that the legume Medicago has yet another way to respond to winter (Jaudal et al., 2016).
In Arabidopsis, the main function of VRN2 is to repress FLC after winter. Like some other plants, Medicago has a VRN2 gene but no FLC. But does MtVRN2 affect flowering?
Yes it does! Jaudal and colleagues show that plants lacking MtVRN2 loose the requirement for vernalization. They flower early under inductive long days even without a cold treatment. This early flowering is accompanied by increased expression of the FT homolog FTa1. Loss of FTa1 abolishes the early flowering of Mtvrn2 mutants. Thus, the function of VRN2 differs between Arabidopsis and Medicago: Arabidopsis VRN2 represses a floral repressor after vernalization and vrn2 mutants flower late. Medicago VRN2 represses a floral activator before vernalization and Mtvrn2 mutants flower early. It is not known repression of FTa1 by MtVRN2 is direct or mediated by another protein. Initial chromatin immunoprecipitation experiments failed to strongly support a direct role (Jaudal et al., 2016). Given that FTa1 may be expressed only in a few cells, direct regulation of FTa1 by MtVRN2-mediated chromatin modifications remains, however, fully consistent with the reported data.
Together, vernalization responses have often evolved to repress FT homologs in the absence of vernalization but the molecular details differ greatly between species. It is difficult to extrapolate from current knowledge to novel species and further work in additional models is needed. Now that spring brings new energy to nature, researchers should become inspired and decipher more ways how to feel that the cold is gone.
Chouard P. 1960. Vernalization and its relations to dormancy. Annual Review of Plant Physiology 11, 191-238.
Fjellheim S, Boden S, and Trevaskis B. 2014. The role of seasonal flowering responses in adaptation of grasses to temperate climates. Frontiers in Plant Sciences 5, 431.
Jaudal M, Zhang L, Che C, Hurley DG, Thomson G, Wen J, Mysore KS, and Putterill J. 2016. MtVRN2 is a Polycomb VRN2-like gene which represses the transition to flowering in the model legume Medicago truncatula. Plant Journal. DOI: 10.1111/tpj.13156
Pin PA, Benlloch R, Bonnet D, Wremerth-Weich E, Kraft T, Gielen, JJ, and Nilsson O. 2010. An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet. Science 330, 1397-1400.
van Dijk A-J. 2015. Cold kick-start for flowering. Flowering Highlights.
Zografos BR and Sung S. 2012. Vernalization-mediated chromatin changes. Journal of Experimental Botany 63, 4343-4348.