Plant resistance to insects consists of inherited genetic qualities that result in a plant being less dam- aged than another (susceptible one) that is subject to the same conditions but lacks these qualities. Plant resistance is a relative concept, as spatial and temporal variations in the environment influence its expres- sion and/or effectiveness. Generally, the production of plants resistant to particular insect pests is accom- plished by selective breeding for resistance traits. The three functional categories of plant resistance to insects are:
1 antibiosis, in which the plant is consumed and adversely affects the biology of the phytophagous insect;
2 antixenosis, in which the plant is a poor host, deterring any insect feeding;
3 tolerance, in which the plant is able to withstand or recover from insect damage.
Antibiotic effects on insects range from mild to lethal, and antibiotic factors include toxins, growth inhibitors, reduced levels of nutrients, sticky exudates from glan- dular trichomes (hairs), and high concentrations of indigestible plant components such as silica and lignin.
Antixenosis factors include plant chemical repellents and deterrents, pubescence (a covering of simple or glandular trichomes), surface waxes, and foliage thick- ness or toughness – all of which may deter insect colonization. Tolerance involves only plant features and not insect–plant interactions, as it depends only on a plant’s ability to outgrow or recover from defoliation or other damage caused by insect feeding. These cate- gories of resistance are not necessarily discrete – any combination may occur in one plant. Furthermore, selection for resistance to one type of insect may render a plant susceptible to another or to a disease.
Selecting and breeding for host-plant resistance can be an extremely effective means of controlling pest insects. The grafting of susceptible Vitis viniferaculti- vars onto naturally resistant American vine rootstocks confers substantial resistance to grape phylloxera (Box 11.2). At the International Rice Research Institute (IRRI), numerous rice cultivars have been developed with resistance to all of the major insect pests of rice in southern and south-east Asia. Some cotton cultivars are tolerant of the feeding damage of certain insects, whereas other cultivars have been developed for their chemicals (such as gossypol) that inhibit insect growth.
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sent, control measures are necessary if crops are to be grown successfully.
Insecticides effectively controlled the Colorado potato beetle until it developed resistance to DDT in the 1950s.
Since then the beetle has developed resistance to each new insecticide (including synthetic pyrethroids) at pro- gressively faster rates. Currently, many beetle popula- tions are resistant to all traditional insecticides, although new, narrow-spectrum insecticides became available in the late 1990s to control resistant populations. Feeding can be inhibited by application to leaf surfaces of antifeedants, including neem products (Box 16.3) and certain fungicides; however, deleterious effects on the plants and/or slow suppression of beetle populations has made antifeedants unpopular. Cultural control, via rotation of crops, delays infestation of potatoes and can reduce the build-up of early-season beetle populations.
Diapausing adults mostly overwinter in the soil of fields where potatoes were grown the previous year and are slow to colonize new fields because much post- diapause dispersal is by walking. However, populations of second-generation beetles may or may not be reduced in size compared with those in non-rotated crops. Attempts to produce potato varieties resistant to the Colorado potato beetle have failed to combine useful levels of resistance (either from chemicals or glandular hairs) with a commercially suitable product.
Even biological control has been unsuccessful because known natural enemies generally do not reproduce rapidly enough nor individually consume sufficient prey to regulate populations of the Colorado potato beetle effectively, and most natural enemies cannot survive the cold winters of temperate potato-growing areas.
However, mass rearing and augmentative releases of certain predators (e.g. two species of pentatomid bugs) and an egg parasitoid (a eulophid wasp) may provide substantial control. Sprays of bacterial insecticides can produce effective microbial control if applications are timed to target the vulnerable early-instar larvae. Two strains of the bacterium Bacillus thuringiensisproduce toxins that kill the larvae of Colorado potato beetle. The bacterial genes responsible for producing the toxin of B. thuringiensisssp. tenebrionis (=B. t.var. san diego) have been genetically engineered into potato plants by inserting the genes into another bacterium, Agrobac- terium tumefaciens, which is capable of inserting its DNA into that of the host plant. Remarkably, these transgenic potato plants are resistant to both adult and larval stages of the Colorado potato beetle, and also produce high-quality potatoes. However, their use has been restricted by concerns that consumers will reject transgenic potatoes and because the Bt plants do not deter certain other pests that still must be controlled with insecticides. Of course, even if Bt potatoes be- come popular, the Colorado potato beetle may rapidly develop resistance to the “new” toxins.
Leptinotarsa decemlineata(Coleoptera: Chrysomelidae), commonly known as the Colorado potato beetle, is a striking beetle (illustrated here, after Stanek 1969) that has become a major pest of cultivated potatoes in the northern hemisphere. Originally probably native to Mexico, it expanded its host range about 150 years ago and then spread into Europe from North America in the 1920s, and is still expanding its range. Its present hosts are about 20 species in the family Solanaceae, especially Solanumspp. and in particular S. tuberosum, the cultivated potato. Other occasional hosts include Lycopersicon esculentum, the cultivated tomato, and Solanum melongena, eggplant. The adult beetles are attracted by volatile chemicals released by the leaves of Solanumspecies, on which they feed and lay eggs.
Female beetles live for about two months, in which time they can lay a few thousand eggs each. Larvae defoliate potato plants (as illustrated here) resulting in yield losses of up to 100% if damage occurs prior to tuber formation. The Colorado potato beetle is the most important defoliator of potatoes and, where it is pre-
In general, there are more cultivars of insect-resistant cereal and grain crops than insect-resistant vegetable or fruit crops. The former often have a higher value per hectare and the latter have a low consumer tolerance of any damage but, perhaps more importantly, resistance factors can be deleterious to food quality.
Conventional methods of obtaining host-plant resistance to pests are not always successful. Despite more than 50 years of intermittent effort, no com- mercially suitable potato varieties resistant to the Colorado potato beetle (Chrysomelidae: Leptinotarsa decemlineata) have been developed. Attempts to pro- duce potatoes with high levels of toxic glycoalkaloids mostly have stopped, partly because potato plants with high foliage levels of glycoalkaloids often have tubers rich in these toxins, resulting in risks to human health.
Breeding potato plants with glandular trichomes also may have limited utility, because of the ability of the beetle to adapt to different hosts. The most promising resistance mechanism for control of the Colorado potato beetle on potato is the production of genetically modified potato plants that express a foreign gene for a bacterial toxin that kills many insect larvae (Box 16.5).
Attempts to produce resistance in other vegetables often have failed because the resistance factor is incom- patible with product quality, resulting in poor taste or toxicity introduced with the resistance.
16.6.1 Genetic engineering of host resistance and the potential problems
Molecular biologists have used genetic engineering techniques to produce insect-resistant varieties of a number of crop plants, including corn, cotton, tobacco, tomato, and potato, that can manufacture foreign antifeedant or insecticidal proteins under field condi- tions. The genes encoding these proteins are obtained from bacteria or other plants and are inserted into the recipient plant mostly via two common methods: (i) using an electric pulse or a metal fiber or particle to pierce the cell wall and transport the gene into the nucleus, or (ii) via a plasmid of the crown-gall bac- terium,Agrobacterium tumefaciens. This bacterium can move part of its own DNA into a plant cell during infec- tion because it possesses a tumor-inducing (Ti) plasmid containing a piece of DNA that can integrate into the chromosomes of the infected plant. Ti plasmids can be modified by removal of their tumor-forming capacity, and useful foreign genes, such as insecticidal toxins,
can be inserted. These plasmid vectors are introduced into plant cell cultures, from which the transformed cells are selected and regenerated as whole plants.
Insect control via resistant genetically modified (transgenic) plants has several advantages over insecticide-based control methods, including con- tinuous protection (even of plant parts inaccessible to insecticide sprays), elimination of the financial and environmental costs of unwise insecticide use, and cheaper modification of a new crop variety compared to development of a new chemical insecticide. Whether such genetically modified (GM) plants lead to increased or reduced environmental and human safety is cur- rently a highly controversial issue. Problems with GM plants that produce foreign toxins include complica- tions concerning registration and patent applications for these new biological entities, and the potential for the development of resistance in the target insect populations. For example, insect resistance to the tox- ins ofBacillus thuringiensis(Bt) (section 16.5.2) is to be expected after continuous exposure to these proteins in transgenic plant tissue. This problem might be over- come by restricting expression of the toxins to certain plant parts (e.g. the bolls of cotton rather than the whole cotton plant) or to tissues damaged by insects. A specific limitation of plants modified to produce Bt toxins is that the spore, and not just the toxin, must be present for maximum Bt activity with some pest insects.
It is possible that plant resistance based on toxins (allelochemicals) from genes transferred to plants might result in exacerbation rather than alleviation of pest problems. At low concentrations, many toxins are more active against natural enemies of phytophagous insects than against their pest hosts, adversely affecting biological control. Alkaloids and other allelochemicals ingested by phytophagous insects affect development of or are toxic to parasitoids that develop within hosts containing them, and can kill or sterilize predators. In some insects, allelochemicals sequestered whilst feed- ing pass into the eggs with deleterious consequences for egg parasitoids. Furthermore, allelochemicals can increase the tolerance of pests to insecticides by select- ing for detoxifying enzymes that lead to cross-reactions to other chemicals. Most other plant resistance mech- anisms decrease pest tolerance to insecticides and thus improve the possibilities of using pesticides selectively to facilitate biological control.
In addition to the hazards of inadvertent selection of insecticide resistance, there are several other environ- mental risks resulting from the use of transgenic plants.
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First, there is the concern that genes from the modified plants may transfer to other plant varieties or species leading to increased weediness in the recipient of the transgene, or the extinction of native species by hybri- dization with transgenic plants. Second, the transgenic plant itself may become weedy if genetic modification improves its fitness in certain environments. Third, non-target organisms, such as beneficial insects (pollin- ators and natural enemies) and other non-pest insects, may be affected by accidental ingestion of genetically modified plants, including their pollen. A potential haz- ard to monarch butterfly populations from larvae eating milkweed foliage dusted with pollen from Bt corn attained some notoriety. Milkweeds, the host plants of the monarch larvae, and commercial cornfields com- monly grow in close proximity in the USA. Following detailed assessment of the distance and Bt content of pollen drift, the exposure of caterpillars to corn pollen was quantified. A comprehensive risk assessment con- cluded that the threat to the butterfly populations was low.
Crop plants engineered genetically for resistance to herbicides may impact deleteriously on non-target insects. For example, the widespread use of weed con- trol chemicals in fields of herbicide-resistant corn in the mid-western USA is leading to the loss of milkweeds used by the larvae and flowering annuals used as nectar sources by the adults of the monarch butterfly.
The monarch has received much attention because it is a charismatic, flagship species (section 1.7), and sim- ilar effects on populations of numerous other insects are unlikely to be noticed so readily.