Video: Light effects illustrate how plants react to airborne warning messages from their threatened neighbors using Ca2+ signals. © Masatsugu Toyota/Saitama University
A caterpillar attack is in the air! Researchers have gained new insights into the mysterious ability of plants to “smell” threats from neighbors and then arm themselves accordingly. They were able to document which volatile substances convey these warnings using a luminous detection method. This also showed in detail how the signal transmission takes place in the recipient plants, which leads to the activation of armament measures against the impending attacks.
They seem helpless – but plants are also not defenseless against their enemies and can react to threats, studies have shown: Some produce toxic and bitter substances or develop hardened tissue structures when they are attacked by caterpillars and the like. These reactions are based on the spread of calcium ions (approx2+) as messenger substances in the plants when a pest bites a leaf. But the sophistication of plant defense systems goes even further, as was first discovered in 1983: Plants release volatile organic compounds into the air when damaged. Neighbors who have not yet been affected can then “smell” these substances and use them as danger signals to initiate defensive measures against impending threats. This form of communication has now been documented in many plant species. However, the exact mechanisms underlying perception and the triggering of defenses have so far remained unclear.
Plant communication literally illuminates
The study by researchers led by senior author Masatsugu Toyota from the University of Saitama now closes this gap. For their experiments they used the model plant of science – the thale cress Arabidopsis thaliana. Breeding lines were used that were genetically engineered to have a special property: these test plants develop certain protein sensors in their tissues that react to calcium ions with a fluorescent glow. This made it possible to see how these plant messenger substances are formed and spread in the plants.
First, the scientists examined how the test plants react to air that was sucked out from plants infested by caterpillars. The fluorescence images documented how calcium ion signal transductions were triggered in the plants within seconds after they “got wind” of the pest infestation. But which chemical messenger is crucial? First of all, it became clear again that the plants apparently do not “smell” the caterpillars themselves. “Volatile substances released from manually crushed leaves also dissolved Ca2+signals in undamaged neighboring plants,” says Toyota. The team then investigated the question of exactly which substances these are. The observations of the florescence reactions when administering different compounds revealed: Two representatives from the aldehyde group released when leaves are damaged are crucial, at least in Arabidopsis.
Signal transmission activates armor mechanisms
By examining the gene activities in the test plants, the researchers were then able to further confirm the significance of the two “warning substances”: They responded to the substances by upregulating hereditary traits, which are already known to have functions in plant defense. In order to precisely demonstrate the relationship between signal propagation and defense reactions, the scientists then treated some test plants with substances that block the calcium ion system. As a result, defense activation no longer occurred. It is now clear: the two aldehydes trigger the defense reactions to a Ca2+-dependent manner.
As the detailed images also documented, the so-called stomata play an important role in the plants’ “sense of smell”. “Plants do not have noses, but these stomata serve as entry points for air into the spaces in the leaf tissue,” says Toyota. It was shown that the bean-shaped guard cells of the stomata were the first to respond with a release of calcium ions within a minute of exposure. Then the mesophyll cells and finally the lower epidermis cells attack.
Toyota concludes: “We have finally revealed the complicated story of when, where and how plants respond to airborne warnings from their threatened neighbors. This etheric communication network, which remains hidden from our view, plays an important role in the defense system of the plant world,” says the scientist.
Source: Saitama University, specialist article: Nature Communications, doi: 10.1038/s41467-023-41589-9