Martin Howard is a Professor at the John Innes Centre, one of a small cluster of research institutes in Norwich. In the fourth of our Celebrating Basic Plant Science series, he explains how he uses mathematical modelling to understand how plants remember winter cold and respond to it throughout the year.
How do plants ‘know’ the correct time to flower? Getting this timing right is vital for reproductive success; flowering in the middle of winter is unlikely to be optimal! Many factors are integrated together to make this critical decision, including the day length.
We have been studying one aspect of this question: How the plant Arabidopsis thaliana perceives and then remembers exposure to winter cold. This fundamental mechanism ensures that flowering doesn’t occur until winter has passed. Interestingly, this memory is quantitative – a longer winter means flowering is faster once it starts (see the image below). This process is a very nice example of what’s called an epigenetic phenomenon, as the plants store information about winter cold exposure even after the environmental stimulus (cold) has been removed.
So how is this information about cold stored? In Arabidopsis, this is centred on a gene called FLC (Flowering Locus C). When the plant is cold, the FLC gene is turned off. The products of this gene prevent flowering, so turning it off actually stimulates the plant to flower. Over recent years, we have learned a great deal about the operation of FLC and associated genes through genetics and biochemistry, in large part through the work of my experimental collaborator, Caroline Dean. However, despite all this knowledge it was still not clear overall how the epigenetic memory system worked. This was partly due to feedback among the different components, which made arriving at an intuitive understanding a very difficult task. For these reasons, we began to model the dynamics of FLC mathematically in the hope of making sense of these interactions and, we hoped, revealing some underlying simplicity in how the system operated.
Mathematical modelling turned out to be very informative and suggested that FLC gene silencing occurred in an all or nothing fashion inside each cell. This silencing was mediated by chemical modifications to proteins called histones that package DNA. The fact that each cell was silenced either completely or not at all meant that the information about winter cold is effectively stored digitally inside each cell. As is the case for computers, such a mechanism is extremely stable and means that the information can be robustly remembered over many weeks or months, as the plant grows after winter.
To test these theoretical ideas we examined the pattern of FLC expression at the level of single cells in Arabidopsis roots and indeed observed a spotty, all or nothing expression pattern. Such a pattern can also explain the quantitativeness of the phenomenon, with a greater duration of cold leading to a greater fraction of cells in the plant with FLC switched off.
Although we still have an enormous amount to learn about how plants remember winter, combining mathematical modelling with genetics, biochemistry and, increasingly, single cell imaging has certainly paid dividends. Modelling has allowed us to dissect the underlying dynamics, and come up with experimentally testable hypotheses, much more rapidly than would otherwise have been the case.
Some words of caution, however: even getting started on the modelling required a great deal of prior data, without which we would have had no firm foundations for our theories. Moreover, our modelling philosophy was to extract only the barest of essentials from this data to try to tease out the underlying mechanism. In my view, this is the only approach that is sensible: constructing over-complex mathematical models that try to incorporate too many details often fails to provide the desired insights. Nevertheless, it seems to me that the combination of modelling and experiments is a powerful solution, perhaps the only solution, to understanding increasingly complex, interlocked, biology.
Overall, the FLC system has been an excellent example of how plants are driving fundamental research that is relevant to all of biology. The mechanisms involved in epigenetic memory are conserved across a very wide range of organisms from plants to flies to humans. So we hope that our hard-won, fundamental insights from FLC will apply very widely indeed.
If you want to read more about vernalisation, the process by which plants remember and react to cold temperatures, try this free-to-access review article: Song et al. 2012, J. Cell Science 25:3723. Martin presented some of his other work on how plants perfectly calculate use of their resources overnight at our 2013 conference on synthetic biology and you can see his presentation slides here.
Image credits: Crocus by Swirus71 via Stock.xchng. Image of Arabidopsis plants courtesy of Martin Howard.