鈥淎 DISEASE can go through the whole field within 48 hours,鈥� says Kevin
Littleboy, who farms mainly wheat and potatoes in North Yorkshire. 鈥淚f I didn鈥檛
control diseases, I wouldn鈥檛 have a crop.鈥� Though it鈥檚 livestock epidemics such
as BSE and foot and mouth that grab headlines, plant diseases quietly wipe out
10 per cent of crop yields worldwide. That鈥檚 in spite of the $6-billion
worth of fungicides that get sprayed on crops around the world each year.
This chemical warfare being waged in our fields might suggest that the plants
have no defences of their own against disease. Not so. In addition to a plethora
of genes that target specific pathogens, plants have a generalised,
immune-system-like defence that can help combat a wide range of diseases. But
surprisingly, plants use this latter defence system only half-heartedly.
Researchers have recently discovered that altering a single gene can overcome
the plants鈥� reticence. Could this open the way to giving crops a helping hand
against disease?
This underused weapon, called 鈥渟ystemic acquired resistance鈥� or 鈥渋nducible
resistance鈥�, is a generalised, vaccination-like response that plants can deploy
when attacked by any of a wide range of bacteria, fungi or viruses. Biologists
have known for 40 years that a virus will cause less damage to a plant if that
plant has been inoculated with a mild dose of the pathogen a few days earlier.
What鈥檚 more, inoculated plants prove to be better equipped at resisting
unrelated diseases. This inducible resistance can be triggered by a wide range
of pathogens and provides protection lasting for weeks or months.
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Until now, crop breeders have paid little attention to inducible resistance.
Instead, they have focused on a much more tempting target, the so-called
鈥渞esistance鈥� or R genes. R genes code for receptor proteins that recognise
individual strains of pathogen and then direct infected cells to commit suicide.
This deprives the pathogen of its hosts and stops the infection in its tracks.
鈥淲hen you have an R gene you can have complete resistance,鈥� says John Mundy, a
researcher at Copenhagen University. 鈥淚t means [the genes] are much more
attractive for breeding purposes.鈥�
But like the flu jab, R genes can be rendered useless if a pathogen mutates
into a slightly modified form. If this happens, a variety of wheat, say, that
has been bred to resist a particular disease can become effectively ungrowable
in as little as three years. So crop breeders must race to develop varieties
with the right R genes before new disease strains render existing varieties
useless. When the breeders fall short, a disease can ravage farmers鈥�
crops鈥攁s happened in the summer of 1988, when barley growers in Britain
and northern Europe saw their previously resistant crops suddenly succumb to
devastating mildew infections.
Inducible resistance, by contrast, gives less absolute protection but should
be much more robust. It depends on a broad array of internal defences, such as
physical blocks to invading fungi and the production of a range of different
anti-microbial compounds, so pathogens find it difficult to evolve ways to evade
it. 鈥淚t won鈥檛 give you as much resistance as the R genes,鈥� says Mundy, 鈥渂ut when
you haven鈥檛 got the right R genes, then what can you do?鈥�
Unfortunately, as Littleboy鈥檚 experience shows, most crops don鈥檛 show enough
inducible resistance to make much difference in the field. In the lab, however,
scientists are beginning to find out why. Three years ago, a group led by Roger
Innes at Indiana University in Bloomington discovered mutants of the laboratory
weed Arabidopsis that induce their defences much more strongly than
normal. For example, powdery mildew鈥攁 major disease of cereal
crops鈥攊nitially spreads across leaves of both normal Arabidopsis
and these mutant plants. The mutants, however, switch on their inducible
defences more quickly, and to approximately four times the normal level. This
slows the mildew鈥檚 spread, allowing the plants to grow new leaves faster than
the disease can infect them. These mutant plants eventually outgrow the
infection.
The difference between the mutants and normal plants, Innes found, is that
the mutants lack a gene called EDR1. This year, his group showed that
EDR1鈥檚 role is to weaken a plant alarm signal called salicylic acid, a
close chemical relative of aspirin that is produced by cells in diseased parts
of the plant and orchestrates the plant鈥檚 defences against the infection
(Proceedings of the National Academy of Sciences, vol 98, p 373). 鈥淲e think that
EDR1acts as a brake,鈥� says Innes. Plants that lack this brake end up
with a hair-trigger response to infection, which helps them to snuff out a
smouldering infection before it catches.
This would all be of merely academic interest if EDR1was found only
in Arabidopsis. But the gene is also present in the genome of unrelated species
such as rice and barley, so it probably exists in most flowering plants. Could
knocking out this single gene, then, be a simple way to boost inducible defences
across the board? 鈥淭hat鈥檚 the $64,000 question,鈥� says Innes.
It鈥檚 probably too early to chill the champagne, however. Innes says it鈥檚
unlikely to be an accident that EDR1muffles the salicylic acid alarm:
鈥淭his gene is highly conserved and so it must serve an important function in the
wild.鈥� Most likely, he thinks, it helps ensure that plants don鈥檛 waste resources
by overreacting to minor infections that pose no real threat. Innes fears that
without EDR1, crops could spend too much on defence.
Innes鈥檚 worry is not an idle one. Last December, Mundy and his colleagues
reported they had found Arabidopsis mutants that lack a gene called
MPK4 and as a result make salicylic acid constantly, even when totally
disease-free, so that their inducible defences are always on. Compared with
normal plants, however, the mutants are stunted. 鈥淭hey are probably about a
sixth to an eighth the normal size,鈥� says Mundy.
Turning on the inducible defence system might have another drawback, too. An
excess of salicylic acid may weaken the plant鈥檚 response to a second alarm
signal, jasmonic acid, which triggers defences against insects and some
diseases. 鈥淭he plants are super-resistant against some pathogens but
super-susceptible to others,鈥� says Mundy.
But these problems aren鈥檛 putting anyone off. The general feeling is that,
compared with their wild relatives, crops are raised in relative luxury and may
have resources to spare for tougher inducible resistance. In fact, the first
commercial means of inducing disease resistance in crops is already available.
In 1999, Novartis (now Syngenta) began selling a salicylic acid mimic called
acibenzolar-S-methyl as a spray under the name of Bion in Europe and Actigard in
the US. Though it works against powdery mildew on wheat, it is mainly used now
by tomato, tobacco and banana growers.
鈥淚t slows down disease and gives an overall increase in yield,鈥� says Urs
Neuenschwander at Syngenta鈥檚 labs in Basel, Switzerland. 鈥淚n banana, we
recommend use once a month, so there are several applications. In other crops,
there are just one or two applications.鈥� However, Neuenschwander stresses that
farmers should not overuse Bion, since it could make the plants spend too much
on their own defence. 鈥淔or farmers, it鈥檚 normally: `In case of disease, use
more,鈥� but with Bion, if you use more you may have negative effects,鈥� says
Neuenschwander.
Upping the ante rather more, last year Huub Linthorst and his colleagues at
Leiden University in the Netherlands genetically modified plants so that they
always produced salicylic acid, just like Mundy鈥檚 mutants that lack
MPK4. The altered plants showed increased resistance against both viruses
and fungi and, surprisingly, did not appear to pay too high a price. 鈥淭he plants
look very healthy and grow very well,鈥� says Linthorst. Mundy suggests that the
difference between Linthorst鈥檚 plants and his own may be that deleting
MPK4 might activate other pathways as well as causing an overproduction of
salicylic acid.
Whatever the case, Linthorst鈥檚 results show that even a permanent deployment
of inducible resistance may be a viable option as long as it is done in
moderation. Certainly, the genes used by Linthorst and his colleagues are in
high demand. 鈥淧eople around the world are trying to put the genes into their own
plants,鈥� he says, 鈥渂ut I haven鈥檛 heard if any of them have succeeded yet.鈥�
Given the similarity between salicylic acid and aspirin, Linthorst is quick
to point out that crops with increased salicylic acid levels shouldn鈥檛 do any
harm to people eating them. 鈥淭he amounts of salicylic acid you need in plants to
have these effects are so low in comparison to what humans use [when taking
aspirin] that there wouldn鈥檛 be any problems,鈥� he says. Of course, that isn鈥檛
true for all plants. Aspirin itself was manufactured to mimic the painkilling
effect of chewing willow bark, which is loaded with salicylic acid and its
derivatives. Presumably, willows have evolved genetic 鈥渆arplugs鈥� for the
salicylic-acid alarm, enabling them to produce such high levels without putting
their defences on permanent red alert.
If Innes, Linthorst and others do eventually manage to create crops with more
vigorous inducible resistance, farmers will inevitably measure their value by a
stark standard鈥攚hether such crops cost less to keep healthy. 鈥淚f you have
a disease in the crop, you need to get in there immediately and spray to stop it
before it spreads,鈥� says Littleboy. How much better it would be if the crops
themselves can keep the disease at bay in the first place.