From leaf growth to flower: daylength and on-off switches

I think now is the time to explain briefly, in layman's terms, your work on the physiology of flowering, one of the two principal lines of research which brought you international recognition and acclaim. Before this interview you wrote to me that 'questions about how plants sense and respond to daylength and the messages sent from the leaves that perceive it to the shoot apex that reacts to it, and how the apex shifts from leaf to flower formation' have dominated your life in science. Could you now tell us a little bit more about that?

Well, I found a suitable test plant, Lolium temulentum, which I am still working on. It is just an ordinary grass, darnel, the 'tares' of the Bible. It is a weed of wheat crops. It flowers at about the same time as the wheat crop and its seeds are about the same size as wheat seeds so it gets propagated along by being sown with the next lot of seed. But they may carry a fungal disease (not ergot) which can cause blindness and madness in people. In biblical times you separated the tares from the grain, and people in the Middle Ages knew that they needed to pick the seeds of tares out of the wheat samples before they made a loaf of bread or something like that. This old plant, well known in biblical times, has been a wonderful experimental plant for me.

For the first five to six weeks we grow our plants in short days, going into darkness at 4 pm, and they remain vegetative. But keeping the light on till midnight tonight, say, is enough to make this plant flower. Chailakhyan's explanation was that the leaf makes a long day floral hormone which goes off down to the shoot apex and switches it on. But there is an alternative explanation, that the leaf, in short days, is making something that stops the plant from flowering, and as soon as you give it a long day, away it can go. Flowering physiologists had not resolved which alternative was correct.

One of my early experiments in Canberra, even before I got set up with the phytotron and had more space, was to test those alternatives. So I would have a plant with one leaf out getting the long day, and at the same time all the other leaves wrapped up for the night in aluminium foil, which involved a lot of labour. Then I could cut off the one leaf, or the other leaves, at various times and see what the result was. The conclusion from the experiment was clearly that both processes operated. There was a message from the long-day leaf to the shoot apex, switching it on, and there was a message from the short-day leaves that reduced the flowering response or would stop it, in the absence of any positive stimulus.

I got into hot water with the high priest of flowering physiology, Anton Lang – a good friend of mine and colleague but we traded punches quite a lot – who 'gave me the works' in his criticism. But subsequently, 15 years later when he had convinced himself that my finding was correct, he was gracious enough in defeat to send me a postcard saying, 'In hindsight I should have done the anti-florigen grafts at the same time as we did the pro-florigen grafts.' His approach was not my kind of experiment but to graft different plants together, grafting the leaves from one plant that had had short days onto a plant that had not, or vice versa.

That was one question. We then were able to consider how fast this message moved. By cutting the sheaths at different heights and so on, we could work out when it arrived at the shoot apex. So that was the time when we should look for changes at the minute shoot apex. That work has been very productive. I have had a lot of colleagues in it – in all my work, really – but particularly all through that.

Defining the hormone messenger

The next question was what the messenger is, what it is that switches on the shoot apex to make leaves instead of flowers, and as I have said, we are getting towards that now.

In fact, Anton Lang was the person who set me on that trail. In 1956, just before I left America, he did an experiment with a small sample of a newly available plant hormone, gibberellic acid, which he put on his favourite experimental plant. The plants flowered in short days, and he was so excited that he called me over to see them in the glasshouse. I got so excited that on my way to Australia I visited ICI in England and they gave me a small sample – it was unobtainable otherwise. As soon as I could I tried it out on my Lolium, and it made them flower in short days. But there are now 150 different gibberellins and only a few of them cause the plant to flower. That is partly what we are working on at the moment, and that is where in recent years I have had a lot of very fruitful collaboration with Lew Mander, who is the world's authority on running up different gibberellins.

Does he make them, or just isolate them?

He makes them. If you want an exotic one he'll think hard – he's still thinking about some of the ones we have asked him for – but mostly after a while he's been able to supply us with all sorts of them, including some artificial ones.

So you have some idea of which ones work and which don't?

Well, around 1990, about the time I retired, we were concentrating on defining which parts of the molecule are important. It is quite a complex molecule, with four rings and various hydroxyl groups attached here and there. It depends very much on where the hydroxyl groups are. For example, if it is a hydroxyl group on carbon 2, no flowering. On carbon 3 and not on carbon 2, very good flowering. So Lew has been able to present us with all sorts of opportunities for defining the important elements of the structure.

There are various things we couldn't explain. For example, the two gibberellins that are most effective for making the plant elongate, GA1 and GA4, are not effective for making it flower. That is what we have been working on recently. We think a paper by a Japanese group has given us a key to why some of these gibberellins work, when some that we would expect to work don't work. That is just the way it often happens in science: there was an incidental observation to which the Japanese did not attach any significance in their paper because they were looking at other things. As Rod King, my colleague in all this work, and I read the paper – independently – we each thought immediately, 'Ah! That would be very helpful for us if the same thing applies in Lolium.'

Focus questions

• Scientists often look for competing alternatives which could explain natural phenomenon. Evans discussed two possible explanations as to how plants begin to flower, both of them involving chemical messengers. How do his two explanations differ?
• Animals also use chemical messengers to control life processes. Can you name some of these and how they influence animal biology?