Plant early-warning system alerts leaves to insect attack

It might appear that plants just sit there, but don't be fooled by that calm exterior. Plants can't simply up sticks and move when the going gets tough, so, to survive and grow, they need to be able to sense the world around them and respond accordingly.

Studies suggest that at least one type of plant can "hear" insect feeding vibrations, and can buzz messages internally to sound the alarm if leaves are attacked.

Plants are good at sensing, but their modes of sensing don't look like those of animals, says Dr Heidi Appel of the University of Missouri. She and her colleague Rex Cocroft have discovered that Arabidopsis thaliana (thale cress) plants can pick up the vibrations caused by Pieris rapae caterpillars chewing on leaves, and the plants respond by boosting bitter-tasting defensive chemicals to ward those hungry predators off.

“Rex had been studying how insects use plants as substrates to transmit vibrations they use to communicate with each other on the same plant. I had been studying how plants recognise insect herbivores and mount appropriate chemical defences,” says Appel.

“When Rex mentioned that insect chewing vibrations were a real nuisance when he was trying to measure vibrational signalling among insects, we both realised that maybe, just maybe, plants could use these chewing vibrations to recognise insect herbivores.”

The researchers created a library of feeding vibrations caused by caterpillars and played them to undamaged leaves so they moved as if they were being eaten, even though no caterpillars were present, says Appel.

When they later set the caterpillars loose on the leaves, they found that plants that had experienced the mimicked feeding vibrations responded more strongly to the attack, even in “distal” (faraway) leaves that had not been exposed directly to the acoustics. “Sure enough, plants that had received the feeding vibrations made more [defensive] mustard oils than those receiving silence,” says Appel.

But could the plants tune into the specific vibes of caterpillar feasts? Appel and Cocroft next experimented with vibrations caused by wind and by calls of another insect, the treehopper. "Once again, the plants experiencing chewing vibrations made more chemical defences in response to later caterpillar attack than plants experiencing silence, and they did not respond in this way to wind or to treehopper calls," says Appel of the study, published last year in the journal Oecologia.

“This tells us that the plant not only detected feeding vibrations, but could respond selectively to them in an ecologically relevant way. Our work provides a reason for plants to detect vibrations, and shows that they have impressive selectivity in their ‘hearing’.”

So if plants can "hear" when insects attack, how do they raise the alarm? Prof Ted Farmer at the University of Lausanne found Arabidopsis thaliana uses electricity to buzz a warning signal to other parts of the plant when a leaf is cut or wounded.

The finding came as something of a surprise, he says. It started when his lab measured the time between a leaf being wounded and other, distal leaves on the same plant making jasmonate, a chemical compound involved in defending the plant against being an insect’s lunch.

“The synthesis of this defence compound, which is quite complex, was happening far more quickly than we had anticipated,” says Farmer, who has worked in the field of plant signalling since the 1980s.

“And when we studied the speed at which it accumulated in the wounded and distal leaves, we saw the signal travelled at about 8cm per minute; too slow to be a pressure signal and too fast for transport of that little molecule jasmonate from one leaf to another.”

The researchers placed electrodes on the plants and mapped electrical activity at the wounded and unwounded leaves. To their amazement, the electrical changes correlated with jasmonate being made. Could it be that an electrical signal was “telling” the faraway leaves to prime for attack?

To seal the deal, the scientists injected currents into the plants, he says. “We investigated different currents and we found one that could itself set off the plant-produced electrical current that then caused the production of jasmonate.”

Using genetic knockouts, Farmer’s lab worked out that two particular molecules were needed for this signal buzz to happen, thus sparking another intriguing insight.

"The two genes we had identified are closely related to important genes in human synapses in the nervous system," says Farmer of the finding, which was published in the journal Nature in 2013. "We already knew those genes existed in the plant – that wasn't a surprise – but to find a role in electrical signalling is interesting."

His hunch is that two systems are involved: phloem, which transports sugars; and xylem, which transports water and minerals. “We believe phloem and xylem are working together somehow [to convey electrical signals],” he says. “It’s very tricky to know which roles either of those cell types play, but it’s great fun to try and find out.”

APHID SPIT: STEALTHY SALIVA OF SMALL ATTACKERS

Could the secrets of healthier crops lie in aphid spit? Aphids attack a wide range of plants, including barley, wheat, orchard trees and glasshouse crops. Dr Tom Wilkinson, a senior lecturer at the school of biology and environmental science in UCD, is trying to understand more about the molecular tricks these insects play as they tap into the plants’ food supplies.

“Most aphids feed by inserting their mouth parts into the plant tissue to tap into a sugar-rich and relatively nitrogen-rich diet in the phloem tissue inside the plant,” he says.

As the insects dig in, they secrete a “gelling” saliva that hardens. Then when they hit the phloem, the saliva changes to a more watery version, says Wilkinson.

His lab has rigged up a feeding system to “fool” the aphids into secreting these saliva types, although it takes about 40,000 insects to produce enough spit for a single sample for analysis.

Working with Dr Jim Carolan at Maynooth University, the researchers have identified a handful of proteins in these hard-won samples, and Wilkinson says some could be involved in stopping plants from raising the alarm.

“A lot of plant defences are triggered by a release of calcium,” he says. “We think some of these saliva proteins could be acting like a cloaking device at a molecular level; they mop up the calcium that would normally tell the plant that it is being eaten.”

There’s plenty left to find out, and other researchers are starting to dig more deeply into the roles of these aphid proteins too, says Wilkinson, who sees ultimate applications in managing crop damage. “If you can come up with a way of targeting the saliva in some way, it would make a good specific method of controlling these notorious pests,” he says.