Karban started off as a cicada researcher, studying how trees cope with the plague of sap-sucking bugs that descends upon them every 17 years. Back then, the assumption was that plants survived by being tenacious, adapting their physiology to hunker down and suffer through droughts, infestations and other abuse. But in the early 1980s, the University of Washington zoologist David Rhoades was finding evidence that plants actively defend themselves against insects. Masters of synthetic biochemistry, they manufacture and deploy chemical and other weapons that make their foliage less palatable or nutritious, so that hungry bugs go elsewhere. For Karban, this idea was a thrilling surprise — a clue that plants were capable of much more than passive endurance.
How does one leaf know it’s being eaten, and how does it tell other parts of the plant to start manufacturing defensive chemicals? To prove that electrical signals are at work, Ted Farmer’s team placed microelectrodes on the leaves and leaf stalks of Arabidopsis thaliana (a model organism, the plant physiologist’s equivalent of a lab rat) and allowed Egyptian cotton leafworms to feast away. Within seconds, voltage changes in the tissue radiated out from the site of damage toward the stem and beyond. As the waves surged outward, the defensive compound jasmonic acid accumulated, even far from the site of damage.
The genes involved in transmitting the electrical signal produce channels in a membrane just inside the plant’s cell walls; the channels maintain electrical potential by regulating the passage of charged ions. These genes are evolutionary analogues to the ion-regulating receptors that animals use to relay sensory signals through the body. “They obviously come from a common ancestor, and are deeply rooted,” Farmer said. “There are lots of interesting parallels. There are far more parallels than differences.”
What Rhoades found next was even more surprising — and controversial. He was looking at how the Sitka willow altered the nutritional quality of its leaves in response to infestation by tent caterpillars and webworms. In the lab, when he fed the insects leaves from infested trees, the worms grew more slowly. But their growth was also stunted when he fed them leaves from undamaged willows that lived near the trees being eaten.
The same biochemical change seemed to be happening in both groups of trees, and Rhoades’ conclusion, published in 1983, was that the untouched willows were getting a message from those under attack. That same year, Ian Baldwin and Jack Schultz from Dartmouth University found that seedlings of poplar and sugar maple began pumping out anti-herbivore phenols when placed in a growth chamber next to saplings with shredded leaves. They described it as plant communication. “People were really excited,” said Karban. “The popular press went wild with this.”
That reception made many scientists nervous. The 1979 film “The Secret Life of Plants” (after a 1973 book of the same name) had wowed audiences with time-lapse photography that made plants seem to writhe with vitality as they unfurled their leaves and pushed out roots. The film claimed that science had proven that plants were conscious and could sense human emotions. “It made people think the whole field was hokey,” said Farmer.
Then, in 1984, both talking tree papers were picked apart by the eminent ecologist John Lawton (who was later knighted). Lawton said that Baldwin’s study was poorly designed and that Rhoades must have accidentally spread an insect disease that slowed the bugs’ growth. His criticism nearly stopped the research dead in its tracks. Rhoades, whom Karban calls the “unheralded father of the field,” couldn’t get funding to replicate his studies and eventually quit science to run a bed and breakfast. People stopped talking about plant communication; the field went dark.