Science: The Day of the Aphids

Can a laboratory in York halt the march of the tiny pests that cause pounds 100m worth of damage every year?
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Angela Douglas is not like the rest of us. When she examines the underside of the leaves of her broad beans and discovers a teeming population of tiny aphids, she does not look aghast and instinctively reach for the insecticide gun. On the contrary, these aphids are being encouraged to thrive, because the broad beans are not in Dr Douglas's vegetable plot; they are being grown under carefully controlled conditions in a laboratory at the University of York.

Dr Douglas is leading a research team that is asking some fundamental questions about aphid biology. And the answers that are being unearthed could present new ways of tackling this major pest - which is not only the scourge of the gardener, but also causes an estimated pounds 100m of damage to commercial crops each year in the UK. The aphid is simply Britain's most economically destructive insect pest.

There are around 4,400 species of aphid worldwide, although the vast majority are in fact innocuous. In this country there is a handful of species which are a nuisance, and these become a problem to gardeners and farmers throughout the summer, from May onwards. Aphids damage plants first by feeding on the plant's sap and thereby taking away its nutrients, and secondly by transmitting viruses that attack plants.

Aphids feed on nutrients that travel around the plant in vessels called sieve-tubes. The aphid inserts specialised needle-like mouthparts - stylets - into the plant and plugs into a sieve-tube. Once in place, the aphid can remain for several days, imbibing the plant sap at its leisure.

For the York biologists it is at this point that things get interesting. Plant sap is nutritionally poor, consisting mainly of sucrose, a few amino acids and a small handful of minerals. In particular, the sap is deficient in the so-called essential amino acids. Amino acids are the building blocks of proteins, which form the machinery of every living cell. There are 20 amino acids; animals can synthesise 11 of them from raw ingredients. However, the remaining nine, the essential amino acids, cannot be synthesised; they must be obtained intact from another source.

Clearly, on its own, plant sap - the entomological equivalent of junk food - is insufficient to sustain an aphid. Nevertheless, it is all that the aphid eats. So the question is: how does the aphid make up for the sap's lack of essential amino acids?

Dr Douglas believes she knows the answer. And the key is this: when you kill an aphid you kill not just one organism but millions - because every species of aphid known has about 10 million bacteria crammed inside its body cavity.

These bacteria belong to the genus Buchnera. They are about two-thousandths of a millimetre across, are spherically shaped and cannot survive for any length of time outside the insect's body. They live inside relatively large cells of the aphid, called mycetocytes. A single mycetocyte may contain several thousand bacteria, each surrounded by a cell membrane. The mycetocytes are packed tightly into the insect's body cavity.

Remarkably, the bacteria are passed on from mother to offspring. Most female aphids reproduce parthenogenetically - that is, the eggs are not fertilised by males. As the egg develops within the mature female, bacteria are expelled from the mycetocyte cells by a process called exocytosis. They then migrate to the nearby egg cell where they are enveloped, or "endocytosed". In this way, each egg cell receives about 100 bacteria from the mother. So each aphid offspring emerges into the world ready- equipped with its own population of bacteria.

"Here at York we have been trying to establish whether the bacteria are important to the aphids' survival," says Dr Douglas. "And if they are, what role do they play?"

The first step was to eliminate the bacteria and see what happened to the adult aphids. "To do this we fed aphids with antibiotics the moment they were born," says Dr Douglas. "By examining the aphids under the microscope and testing them for the presence of bacterial DNA, we were satisfied that we had obtained bacteria-free insects."

These aphids were allowed to feed on plants and their growth and reproductivity were compared with a normal population.

"We found that the aphids without the bacteria grew very poorly," says Dr Douglas. "Many reached adulthood at less than one-fifth of their normal size. And whereas untreated insects produced between 50 and 80 offspring over three weeks, the aphids treated with antibiotic produced either no offspring at all, or stillborn offspring, or young that died after a day or two. It is quite clear that the aphids have an absolute requirement for the bacteria."

Dr Douglas hypothesised that the bacteria were providing their host with the essential amino acids that were absent from the plant sap. To test this, the researchers again used antibiotic-treated insects. They fed them with the raw ingredients they needed to synthesise amino acids, tagged with a radioactive label. After a period of time they analysed the contents of the aphids' bodies to see which amino acids were present.

"We found that aphids with bacteria contained the full range of amino acids, both essential and non-essential," says Dr Douglas. "On the other hand, the insects treated with antibiotics had no essential amino acids at all. It seems clear that the bacteria are synthesising essential amino acids for their host organism."

But the story of Buchnera's indirect role in maintaining the aphid's pest status does not end with its nutritional munificence. Aphids transmit viruses between plants; one class of economically important plant viruses spread by aphids is the luteoviruses. Virus particles are ingested by the aphid in plant sap. They travel into the gut, then are transported across the gut wall into the body cavity. Eventually, the virus comes into contact with cells of the aphid's salivary glands and gets transported into the salivary duct, becoming excreted with the saliva when the aphid feeds.

At the Research Institute for Plant Protection in Wageningen, in the Netherlands, Dr Hans van den Heuvel has discovered that luteoviruses bind to a particular protein inside the aphid's body, which enables them to survive the journey between one plant and another. This protein, it turns out, is produced by Buchnera. It is suspected that the bacterial protein somehow protects the virus particle from attack by enzymes inside the aphid's body.

When the bacteria are experimentally eliminated by antibiotics, the aphids are a much less efficient transmitter of the virus. One obvious question arising from both the British and the Dutch work is whether new aphicides can be developed based on the relationship between the bacteria and the insect. "Clearly, antibiotics could kill the insects, but that is self- evidently unacceptable as there are already too many antibiotics around," says Dr Douglas, who stresses that the work at York with antibiotics has been done under strictly controlled laboratory conditions.

However, Dr Douglas is convinced that detailed biochemical investigation of the membrane that surrounds the individual bacteria within the mycetocyte could well reveal a signalling system - a protein, say - unique to this partnership, which could provide a highly specific target for a pest- control agent.

That remains a research project for the future. In the meantime, those of us who wish to protect our roses will have to continue to rely on the more conventional methods of zapping these irritating, yet fascinating, pests. Or else hope that it is a good year for ladybirds.

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