The path of least resistance: Inserting genes into plants could protect crops from pests, at least till the latter become immune, says Simon Hadlington

THE arable farmer's ongoing battle with crop pests could soon enter a new phase. Modern molecular biology will enable genes to be inserted into plants, rendering them resistant to specific pests.

Field trials using such 'transgenic' crops are already under way. In the United States, the gene from a bacterium has been inserted into cotton plants. The gene's product is specifically toxic to the larvae of the moth Heliothis, an economically important cotton pest. If these and other tests prove successful, transgenic pest-resistant crops could be commercially available within a few years.

Proponents of this gene technology point to a new, environmentally clean era in pest control, free from the need to spray chemicals that can drift on the wind into places where they may be harmful to wildlife or humans. But one persistent problem will need to be addressed if the technology is to displace conventional systems. Virtually all crop pests eventually become resistant to a given pesticide. Because genetic engineering technology is so expensive to develop, it is imperative pests do not become resistant quickly.

This effort to prolong the useful life of genetically engineered crops could have profound implications for farming practices.

One study, for example, suggests arable farmers could find themselves cultivating a paradox: transgenic insect-resistant crops could rapidly lose their insecticidal properties unless they are planted next to fields of completely untreated crops, where insect pests are allowed a free rein.

Such a regime might be difficult to enforce but would be necessary to prevent the pests from rapidly evolving resistance to the insecticide manufactured by the plant.

The study, by two geneticists, has found that a system of providing 'refuges' for insect pests could be more effective than cheaper, more logistically - and politically - simple options.

The scientists suggest governments might have to provide incentives, or even legislate, for farmers to adopt such a strategy, given that the untreated crops could fail. The refuges could be one use for surplus agricultural land, they say.

The problem of resistance became apparent in the early days of chemical pest control. The more often a population of organisms is exposed to a harmful chemical, the faster resistance evolves. The mechanism of this evolution of resistance is in essence Darwinian natural selection.

Within a large population of pests exposed to a toxin, a small number of individuals will not be susceptible to the toxin to the same degree as the rest. These are more likely to survive, mate among themselves and produce a proportion of resistant offspring.

Because the bulk of the population has been wiped out, conditions are very favourable for the resistant minority, and within a few generations a new, resistant population will have established itself.

The onset of resistance could be particularly rapid for crops that produce their own insecticide. This is because the plant will continue to produce the toxin even when the pest population is so low that it does not warrant treatment.

Using conventional pest control techniques, no pesticide would be applied during such times. This periodically allows the resistant genes within the population to become diluted, delaying the onset of resistance. But with the transgenic crop the pests will be continually exposed to the toxin, allowing resistance to evolve.

Dr James Mallet, a lecturer in genetics at University College, London, has, with Dr Patrick Porter, of Mississippi State University, compared the likely efficacy of the two favoured strategies for delaying the onset of resistance.

'Given the amount of money that has been spent developing these crops, it is important that their insecticidal properties last a reasonable length of time,' Dr Mallet says.

A number of options exist. The first is to identify new genes that can be inserted into the crop to give it resistance, much in the same way that new insecticides are developed when the old ones become ineffective. This is an expensive solution.

It might also be possible to adopt 'pyramiding', in which more than one gene is used to produce a cocktail of toxins. It would take a long time for a given pest to evolve resistance to several toxins simultaneously. This is a technologically complex achievement. The remaining options involve enabling the pests to be exposed to the toxin only partially, giving them some respite from its effects. In these conditions it might be supposed that evolution of resistance would be slower, as there would be less 'selection pressure' for the resistant genes because the environment would be less extreme.

There are three ways this might be done. One is to programme the foreign gene to be expressed only in the vulnerable tissue of the plant - in cotton, for example, this would be the flower. The population of pests would therefore be exposed to the toxin only when it ate the appropriate tissue.

The cheapest, most simple solution would be to sow a mixture of transgenic and unmanipulated seeds. The resulting field of crop would therefore contain both toxic and non-toxic plants, effectively achieving the same result as using tissue-specific gene expression.

The final option would be to plant completely toxic fields next to completely untreated ones - creating 'refugia' for the insects.

What Dr Mallet and Dr Porter have shown, using a simple genetic model, is that the seed mixture option, which seems the most attractive, could be seriously flawed and, in some circumstances, could speed up the rate of evolution of resistance compared with a pure stand of toxic crop. The model, published in the Proceedings of the Royal Society in 1992, requires two prerequisites: that during the different stages of its life cycle, an insect might have differing degrees of resistance; and that the insect can move between plants.

Put simply, the model says that if a partially resistant insect were exposed throughout its life to the toxin, it would not survive. But if it happened to be feeding on the toxic plant during its resistant stage, before moving to a nontoxic plant, its chances of survival would increase.

Dr Mallet believes that if pest movement is sufficiently common, it could be better to have a crop of entirely toxic plants, which would wipe out all but the most resistant of the pests.

In order to 'dilute' these surviving resistance genes, the farmer would have to plant nearby a stand of untreated crop. Here a population of pests could survive without any 'selection pressure' and the genes conferring resistance would be rare.

The chances of a surviving resistant individual from the toxic field meeting and mating with a similar resistant individual from the unexposed population would be small. Dr Mallet does not suggest the seed mixture strategy would be dangerous in all circumstances, but says that to formulate a successful policy, it will be necessary to take into account a whole host of considerations about the biology of the pest in question. By making some simple and plausible assumptions, he and Dr Porter have shown that the whole matter needs careful forethought.

He also acknowledges that a policy of planting refugia could be fraught with political difficulties. 'Seed companies can hardly expect farmers to plant refugia for resistance management if short-

term economic considerations dictate planting a pure-line transgenic crop,' he says. 'Although refugia might be in the public interest, it is hard to imagine farmers or industry voluntarily creating them if they are competing against other farmers or companies not promoting such strategies.'

Dr Mallet contends that there would be a case for legislation to compel the planting of refugia, which could take the form of an expanded 'set aside' programme. 'Pure, toxin-free seed would be grown on a fraction of cropland, which would provide a sufficient refugium of insect susceptibility to reduce selection. The programme would be enhanced if broadcast pesticide use were prohibited on this land, and pest control should be only by ecologically sustainable means.'

(Photograph omitted)