Bugging the line: Aphids help us spy on plant communication
“It is impossible not to be struck with the resemblance between the foregoing movements of plants and many of the actions performed unconsciously by the lower animals... ...the most striking resemblance is the localisation of their sensitiveness, and the transmission of an influence from the excited part to another...” from The Power of Movement In Plants (1880) by Charles Darwin (1809-1882)
In his astonishingly detailed “The Power of Movement In Plants”, Charles Darwin noted the incredible resemblance between how plants and animals perceive their environment and respond to it. He proposed that plants possess a mechanism, like our nervous system, to transmit information about external stimuli from one part of the plant to another. Research suggests that Darwin was not far off in his proposition. Experiments are revealing that plants do, in fact, possess an internal communication network. Recently, tiny insects, aphids, have allowed us to spy on these internal communications.
Like miniature spies, aphids tap into plants’ internal conversations. Just like wiretappers listening in on telephone calls, aphids connect with plants’ internal communication network. Recent research published in New Phytologist, enlisting aphid wiretappers, reveals that signalling from one part of the plant to another shares striking similarities with our nervous system. The findings point to the importance of this system in protecting plants from attack by insect pests.
Aphids are specialised insects that feed on plants. They have a mouthpart, called a stylet, which is syringe-like. The stylet penetrates deeply into the plant, tapping directly into the plant’s plumbing system.
Plants have two major components to their internal plumbing, the xylem and the phloem. The xylem transports water and dissolved nutrients obtained by roots up to the aerial tissues of the plants. The xylem is largely a collection of dead cells that function like capillaries – tiny pipes through which the liquid is drawn. By contrast, the phloem is made up of living cells – active tubes that transport a syrupy sap that is rich in sugars made by photosynthesis in the leaves. The living cells of the phloem transport the sap throughout the plant, where is will be used to build the growing plant body.
Aphids tap into the phloem, because it is so full of nutrients. The stylet functions like a long straw, drawing the syrupy phloem sap into the aphid’s mouth. As long as there aren’t too many aphids, this isn’t overly harmful to the plant, as the volume the aphid drinks is tiny. In fact, it is in the aphid’s interest to ensure that the plant remains healthy, so that there is still plenty of syrup to be had.
When aphids connect with the phloem, they are not just connected with the plant’s internal plumbing. They are also connected with the plant’s internal wiring.
In the 1980s, scientists discovered that phloem cells also function as a communication system through which electrical signals travel. Just as electrical signals are transmitted through the neurons in your nervous system, electrical signals are transmitted through the plant’s body via phloem cells. In plants, it is as though the nervous system and the circulatory system are brought together within one tissue – the phloem – simultaneously transporting materials throughout the body, while transmitting electrical signals.
In both plants and animals, electrical signals function in an analogous manner. They transmit information from one location to another. If you wound your hand, an electrical signal travels from your skin, up your arm, to your brain, to let you know you have been wounded, and to draw your hand away. When a plant is wounded, a similar electrical signal is generated - but instead of travelling to a centralised brain, the electrical signal travels to other parts of the body, to inform them that wounding has occurred.
In plants, wounding means danger. Normally the danger comes from herbivores. Wounding is generally a prelude to becoming somebody’s meal.
The ability of a wounded part of the plant to let other parts know that wounding has occurred can allow the other plant parts to prepare a defence against herbivores. Plants have a suite of sophisticated defences that they can bring to bear to protect themselves from herbivores. These defences work best if they are readied in advance of the predator.
Some herbivores don’t wound so much as they nibble. Nibbling may escape the detection of the plant. This could have dire consequences, as lot of nibbling can be every bit as fatal as a big bite. Consequently, it is interesting to know if plants might be able to detect nibbling, and transmit a warning signal, in the same manner as wounding does.
In new research by Vicenta Salvador-Recatalà, Freddy Tjallingii, and Edward Farmer, aphids provided novel insights into the role of the phloem network in the response to the nibbling feeding of caterpillars.
Normally it is difficult to record electrical signals travelling in the phloem. Phloem is located within the stem, under other plant cells. Botanists generally have to use specialised, tiny electrodes to record electrical signals in the phloem. These electrodes are very fragile, damaging to the plant, overly sensitive to vibrations, and difficult to handle and use.
In contrast to miniaturised electrodes, aphid stylets firmly tap into the phloem, are not easily dislodged, and don’t break. Living aphids that are attached to the phloem can then be converted into electrodes themselves, simply by connecting them to one end of an electrical circuit. With the other end of the circuit embedded in the soil, the electrode circuit can sensitively, and robustly, detect electrical signals transmitted through the plant body without concerns for vibration from or damage to the plant.
Using this aphid phloem-tapping system, Vicenta Salvador-Recatalà and colleagues investigated the transmission of electrical signals in response to caterpillar feeding. They found that even the nibbling of caterpillars could induce electrical signals, on a smaller scale, but akin to those transmitted by wounding.
The electrical signals travelled through the plants like waves. The waves travelled most rapidly to leaves that were closest to the site of caterpillar feeding, and slower to other regions of the plant. When the waves were rapid, a wound response was activated in those leaves – even though the caterpillar was nibbling on a different leaf.
The nibbling-induced electrical waves travelled through plants in a manner analogous to the way that electrical signals travel through neurons in animals.
In neurons, electrical waves are transmitted by virtue of changes in the way charged atoms, ions like calcium, flow into and out of the cell. The flow of ions is controlled by protein channels embedded in the membrane of neurons. In the absence of a signal, the channels are closed. When a neuron receives the right signal, these channels open, allowing the ions to flow out through the channel. This induces a change in ion concentrations inside the cell, and thereby creates the electrical wave.
Plants make protein channels that are similar to those found in neurons. They also open and close in response to appropriate signals, and, when open, allow ions, especially calcium, to flow. When Vicenta Salvador-Recatalà and colleagues looked at plants where the function of some of these channels was impaired, they found that caterpillar feeding no long produced the electrical waves.
These findings suggest that plants respond to caterpillar nibbling using an electrical signalling network that functions fundamentally like neurons do. Clearly, plants don’t have neurons. Instead, they make use of similar molecular building blocks to construct a response network to an adverse stimulus that bares striking parallels to neurotransmission.
While aphid spies do have their drawbacks – after all, they are also feeding on the plant – these little masters of espionage are providing profound insights into how their host plants function. Their wiretapping capabilities are likely to uncover other secrets encoded in plant responses to a variety of threats, especially insect pests. As such, they are important agents in helping us in the ongoing effort to protect the plants we rely upon from pests and pathogens.
Fromm J, & Lautner S (2007) Electrical signals and their physiological significance in plants. Plant, Cell & Environment 30: 249-257
Salvador‐Recatalà V, Tjallingii WF, & Farmer EE (2014) Real‐time, in vivo intracellular recordings of caterpillar‐induced depolarization waves in sieve elements using aphid electrodes. New Phytologist. DOI: 10.1111/nph.12807