Nature as the inventive chemist (q.v. Alastair Fitter)

How do you link a meeting in America in late October of the Science Advisory Panel of the Environmental Protection Agency (EPA) with a recent letter in the Independent newspaper from the Country Landowners Association and a new agri-chemical with potentially extraordinary implications. The quick answer is natural chemicals used in defence mechanisms. The long answer is a bit complicated, but if you get to the end, you may understand just how dangerous the natural world is.

I start with the strange plant I noticed recently on wasteland in Montreal (Canada) whose unusual seed pods reminded me of the alien-containing pods in the classic film, The Invasion of the Bodysnatchers. The next day, I learnt about this plant in the Insectarium of the Montreal Botanical Gardens. It's a common weed in most of N. America called milkweed or Butterfly Weed (Asclepias spp.) and it is host to the offspring of that icon of the American natural world, the monarch butterfly. Monarchs are big butterflies - I know having had to duck out of the way of a low flier. They are also very colourful, migratory and have a tendency to swarm in dramatic drifts.

The monarch hit the headlines last year when there were reports that pollen from GM maize dusted onto the leaves of milkweed had reduced feeding and raised mortality in the larvae of the butterfly after they had eaten the leaves. The modification of the maize is carried out to include a gene which codes for a protein that is generally toxic to the larval stage of lepidoptera (butterflies and moths). Maize is attacked by the European corn borer, which bores holes into the stem of the corn, causing destruction of the plant. Thus the modification allows a systemic control of the corn borer larvae which ingest the toxic protein as they dine on the stem of the maize.

The origin of the toxic protein is familiar to organic growers because it derives from a bacteria (Bacillus thuringeniensis - Bt) which is commonly sprayed prophylactically onto the cabbage family to prevent damage from the caterpillars of the cabbage white butterfly. The larval stages ingest the toxin produced by the bacteria and are killed.

Another study last year showed that lacewing larvae fed on corn borer larvae that had been intoxicated with the new protein present in maize had a prolonged development time and elevated mortality. In subsequent experiments, the same scientists then cast doubt on the significance of those results. The toxicity could have been due to the decay of the corn borer larvae themselves. You can read all about these reports and the many, many more on the regulatory assessment of the use of incorporated Bt plant pesticides in the briefing papers for that meeting in October (see the EPA website). There is, however, only a cursory assessment of the ecological effects of using the Bt spray directly (mostly used in forestry situations in N. America). I particularly looked for this as I encourage wasps into my garden (figwort is good) because they eat cabbage white caterpillars. I wonder if wasps are harmed in any way in fields of organic cabbages sprayed with Bt?

Plants containing toxins are quite common in nature (think of the foxglove) and can be explained as a defence mechanism against being eaten. Take potatoes - the alkaloid solanin in potatoes is toxic and is produced in the tuber when it is exposed to light. Potato tubers grow below the surface, but could this be a mechanism for defence against being eaten if some of the tuber grows exposed above the soil? Other foods with toxins are psoralen in celery, lectins in kidney beans, tannins in tea and the classic cyanogenic glycosides in cassava. Which brings me back to milkweed.

The reason why the monarch lays its eggs on milkweed leaves is that the plant is poisonous. The larvae and caterpillars eat the leaves of the milkweed, but they are immune to the poison. Instead, they become poisonous themselves to any predator who wants to eat them. Full marks to the monarch butterfly for exploiting the defence mechanism of the milkweed. This leads me on to the letter in the Independent.

The Country Landowners Association wrote to encourage everyone to purge the UK of the common weed ragwort (Senecio spp.) because it is poisonous to livestock, particularly to horses. They wrote in reaction to previous letters that had praised the wildlife attraction of ragwort. (It grows in my garden, as its flowers are very good at attracting in hoverflies whose larvae are excellent predators of aphids. Lacewing larvae do the same job.) But ragwort has another distinction in that it is the host for the larvae of the cinnabar moth. Ragwort is not poisonous to the larvae, which stuff themselves with the alkaloid poison such that the adult moth becomes inedible to predators. Clever moth because not only has it learnt to protect itself, but also it has chosen to breed on a plant that few other species will eat. Briefly returning to the cabbage whites, they choose cabbages to host their larvae as they are immune to the mustard oils in cabbages that are poisonous to other insects. In fact, the butterflies are probably attracted to cabbages because of the smell of the mustard oil. (In improving wild cabbages, we have bred out much of the original high toxicity.)

Finally, I come to this new agri-chemical, which is probably a bit of a misnomer as it is a natural protein derived from bacteria, in the same way that the larval protein toxin is produced in Bt. This bacteria (Erwinia amylovora) is the cause of fire blight in apple and pear trees and many ornamentals in the rose family, leaving blackened branches, trunks, leaves, flowers and fruit. While the bacterial blight is ruinous for plants, its protein derivative is quite the opposite.

Agricultural scientists have long sought the chemical basis of a defence response in plants called the hypersensitive reaction. This develops in the few cells in direct contact with an invading pathogen in the plant's intercellular spaces and is essentially the suicide of those plant cells . By using a technique called molecular mutagenesis, scientists at Cornell University (USA) identified a number of hrp (pronounced "harp") genes of E. amylovora. These genes are involved both in fire blight infection, but also in the development of the hypersensitive response which thwarts the spread of the disease. The protein coded by the harp genes -called harpin - can be used to treat a plant before a pathogen attacks, and after a few days the plant's system mobilises its own defences against such things as bacterial wilts, and may acquire systemic resistance with no adverse effects.

Over 500 field trials of the protein have been carried out on about 45 crops in four countries. Growers found that harpin also accelerated ripening and improved yields on plants like cotton, citrus, peppers and tomatoes. While performing a field trial on pepper plants in 1996, it was noted that the harpin-treated plants were less damaged by insects than control plants not treated with the protein, suggesting the possibility that harpin induces resistance to insects as well.

The U.S. Environmental Protection Agency has granted conditional registration for the first commercial agricultural use of harpin under the name Messenger. Will it be just be another oddball discovery from the natural world, or will it revolutionise agricultural plant protection worldwide? And if it is the latter, will it be given the opportunity to prove its worth?

Mark Fisher, 5 October 2000