Feature: Epigenetics helps plants weather winter

It’s a privileged plant that has access to a steady stream of sunlight, consistent temperatures and ample hydration. Many have to endure extremes of one or another, or even all three. Yet plants are far from defenceless against the ravages of a fickle environment. It’s been the mission of Dr Jean Finnegan and her colleagues at CSIRO Plant Industry in Canberra to find out how plants use epigenetics to cope with changing environmental conditions that they have no choice but to endure.

Most of Finnegan’s work has been done in the ubiquitous plant model, Arabidopsis, and the condition she studies is prolonged cold, “like during winter in Canberra for instance,” Finnegan says. To this end, the group at CSIRO has long been interested in an adaptation response in plants called vernalization.

First described in the 1800s, this is the phenomenon whereby germinated plants that are exposed to extreme cold temperatures for long periods will flower much earlier once the days get longer and warmer compared to counterparts that have not experienced the same cold conditions. This response is seen mostly in Northern hemisphere species and is very important for agricultural plants that have to survive harsh winters followed by short growing seasons, as it allows them to flower early so there is plenty of time to set seed ready for the winter again. In fact, varieties of wheat, barley and canola exist that will not flower unless they go through extreme cold.

According to Finnegan, this mechanism has been used in agriculture for a long time, and is also important for Australia where we need to use particular crop varieties more suited to the generally warmer growth conditions. In fact, early European settlers nearly starved as their crops failed year after year, simply because it was not cold enough for the plants to trigger flowering.

One of the first big clues to the molecular basis of vernalization came about 10 years when Finnegan’s colleague, Candice Sheldon, identified a key gene regulating flowering in all Brassica plants (like canola, broccoli etc). This gene, called Flowering Locus C (FLC), represses flowering and, not surprisingly, also proved crucial for the vernalization response.

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Setting seed while the sun shines

FLC expression is turned off when a plant is exposed to long periods of extreme cold, thus removing the block to flowering. So, when the temperature comes back up in spring, flowering occurs straight away. This effect was also found to be gradual and quantitative – that is, the longer the plant is in the cold, the more FLC is repressed, and the sooner it will flower when things heat up, which seems like a clever way to ensure successful seed development even with long winters and short springs.

The epigenetic nature of the FLC response was only realised with evidence that the progeny of a vernalization-competent plant does not undergo the same response until it too has been in the cold, meaning it has to be ‘broken in’ by a harsh winter before being ready to flower early.

“So, the seeds of these cold-hardened plants have FLC switched on during the first cold snap, thus ‘forgetting’ the gene was switched off in the parent. This mitotic memory but meiotic reset proved it was an epigenetic phenomenon.”

So, how do these plants ‘know’ it is so cold for so long? To address this intriguing question, Finnegan first asked how FLC is regulated. She and colleagues subsequently showed that a particular marker of gene activity present on the chromatin around the FLC gene gets removed under cold conditions and is replaced by a repressive mark called H3 trimethyl-lysine 27 (K27me3).

“We also found that this gene marker redistributes across the entire FLC locus once the warm conditions return, and that this ‘spread’ is the thing needed to keep FLC from working and to allow rapid flowering,” says Finnegan.

More clues upstream of the action

More recently, Finnegan went looking for answers further up the FLC signalling pathway and is now studying a crucial gene called VIN3 (Vernalization Insensitive 3), which is essential for vernalization.

“Like FLC, VIN3 expression also changes quantitatively in response to the cold, but it gets induced rather than repressed,” says Finnegan. “Also, VIN3 induction is needed to get the changes in FLC. So now we are trying to work out the basis of the VIN3 gene response and how it all works quantitatively in synchrony with FLC.”

The network regulating FLC is so complex and new regulators are being identified all the time, according to Finnegan. “It makes sense because flowering is so important to a plant’s success and so must be very finely tuned.”

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Then, just as it seemed the main suspects were rounded up, very recent work by Finnegan has turned up a surprising new piece of evidence for the network of intrigue that is vernalization.

“The fascinating thing about the VIN3 gene upstream of FLC is that plants grown in warm conditions also have FLC chromatin heavily marked by the K27me3 repressor,” i.e., they also show epigenetic changes. “But we now find, to our surprise that when these warm-weather plants are subjected to extreme cold that mark is not removed and the plant is somehow overriding the repression when it activates VIN3 expression. This is the first time that such a phenomenon has been described and we now think that K27me3 might act to modulate the rate of VIN3 induction and expression.”

Whatever the case, Finnegan is certain of one thing: “There is definitely something quite exquisite happening with the expression of this gene that we do not yet understand.”

Nailing the mechanisms and molecules underlying epigenetic regulation in plants clearly has huge practical implications, particularly as pressures on crop success, efficiency and flexibility increase with an ever-changing climate. “Ideally, we could target epigenetic modifications to a particular gene whose expression is critical for adapting to certain environmental conditions. For example, although the climate is generally getting warmer, events like late frosts due to less water vapour in the atmosphere are increasingly problematic for agriculture. We need to maintain productivity… especially as the population continues to grow and land for agriculture doesn’t.”