Interference with the biosynthesis of antimicrobial compounds can also be a means for plant pathogens to be resistant to biocontrol agents. Fusaric acid, a toxin produced by the plant pathogenic fungus F. This repressive effect may affect the performance of biocontrol bacteria that are sensitive to fusaric acid. A plant pathogen can also reduce the antibiotic production of a biocontrol agent, by altering its chemical environment. For example the plant pathogenic fungus Gaeumannomyces graminis var tritici acidifies the environment, thus disturbing the activity of the antagonistic bacterium P.
Finally, natural plasmid transfer between bacteria was also shown to provide a possible mechanism for plant pathogens to become resistant to biocontrol agents. This was the case for example for the soilborne bacterium A. The resistance resulted from the fact that this plasmid carries both the gene coding for the production of agrocin 84, the antibiotic responsible for the activity of the biocontrol agent, and the gene involved in the resistance to this antibiotic. It was suggested that the establishment of large populations of Agrobacterium carrying plasmid pAgK84 could threaten the effectiveness of A.
To minimize the risk of transfer of this plasmid by A. The judicious use of biocontrol agents and particularly of the new strain K should minimize the risk of pAgK84 transfer into pathogenic Agrobacterium strains and thus help to preserve the effectiveness of A.
Most biocontrol agents acting by hyperparasitism produce enzymes such as chitinases and glucanases. Specific mechanisms can help plant pathogens to protect themselves against these cell wall degrading enzymes. For example, the synthesis of melanin polymers could help microorganisms to protect against microbial enzymes Bell and Wheeler, The formation of chlamydospore-like structures and vacuolated portions in mycelium allows the pigeonpea wilt pathogen Fusarium udum to maintain a slow growth and the production of conidia in presence of the hyperparasitic bacterium Bacillus subtilis AF1 Harish et al.
Another possible mechanism implies the repression of the synthesis of enzymes produced by the biocontrol agent. For instance, the mycotoxin DON, produced by Fusarium culmorum and Fusarium graminearum represses the expression of genes coding for chitinases in the biocontrol strain Trichoderma atroviride P1 Lutz et al.
The induction of resistance in plants involves the synthesis and the activation of plant defense compounds as the result of activity of an elicitor. This induction leads to rapid production of reactive oxygen species, modifications of cuticle thickness, cell wall appositions, accumulation of phenolic compounds and production of phytoalexins and pathogenesis-related proteins rendering the plants more resistance to pathogen attack Wiesel et al.
To survive and become established in a resistance-induced plant, plant pathogens have to overcome these induced host defense chemicals. Plant pathogens may evolve a combination of strategies to colonize and survive in this environment. Such strategies could include transporting toxic chemicals out of the cell or sequestrating them in cellular organelles, detoxifying host defense compounds by converting or modifying them and interfering with host signaling Morrissey and Osbourn, A way for plant pathogens to cope with host defense chemicals is to secrete them out of the cells as in the case of antimicrobial compounds produced by biocontrol agents see section above.
For example, ABC transporter activity has been implicated in the tolerance of Nectria haematococca to pisatin, a phytoalexine of Pisum sativum Denny et al. Similarly, a recent study on Grosmannia clavigera , a fungal pathogen of pine trees, showed that this fungus can survive and become established in pine tissues by the induced expression of an efflux ABC transporter GcABC-G1 Wang et al.
This allows the fungus to cope with intracellular levels of monoterpenes, which are among the most abundant antimicrobial pine defense chemicals. ABC transporters are potentially involved in the virulence and aggressiveness of fungal plant pathogens, by decreasing the toxic effect of phytoalexins Del Sorbo et al.
Botrytis cinerea is for instance able to detoxify the alpha-tomatine, a phytoanticipin found in tomato plants Quidde et al.
In this study, 12 out of 13 isolates of B. The ability of B. A correlation between the ability of eight isolates of B. Some plant pathogens, like the fungus Microcyclus ulei , are tolerant to hydrocyanic acid, a volatile compound produced by plants in response to various damages Osbourn, This tolerance might be due to cyanide-resistant respiration. Other fungi could also detoxify this compound by converting it to formamide, via cyanide-hydratases.
Some plant pathogens are then able to degrade defense compounds and thus might be able to overcome the effect of biocontrol agents acting through plant defense induction. The hypersensitive reaction HR involves the production of reactive oxygen species that leads to cell death and it is generally consider as a signal to induce the synthesis of antimicrobial compounds like phytoalexins. It usually prevents the fungal penetration into host tissue but it has been shown that HR facilitates the colonization of the plants by necrotroph fungal pathogens like B.
These plant pathogenic fungi might therefore exploit particular defense mechanisms of the plant to overcome the induced resistance effect of a biocontrol agent. Moreover, many other plant pathogens can protect themselves against oxidative damage Duffy et al. Some plant pathogens can significantly slow down the growth of biocontrol agents by exploiting more rapidly the resources within their environment and then affecting their efficacy.
This was shown in a study conducted to evaluate the effect of several fungal root pathogens on the capacity of biocontrol strains P. For instance, in presence of some Pythium species, the population of P. In this case, the infection by Pythium tends to reduce the root surface available for bacterial colonization which, as a consequence, tends to limit the population of potential antagonists. In another study, the plant pathogenic oomycete P.
This population size reduction limits the competition in the rhizosphere for nutrients leaking from wounds caused by P. Competition may also occur on the phyllosphere where the microbial community is also important in number and diversity and where microorganism—microorganism interactions can occur Vorholt, This microbial community may also affect the efficacy of biocontrol agents. Knowledge about plant microbiome rhizosphere, phyllosphere, endosphere and the microbial interactions occurring on those niches should contribute to the improvement of biological control.
Despite the limited number of published studies dedicated to this topic, it is clear from this review that plant pathogens can display various including very low levels of sensitivity to biocontrol agents, regardless of the complexity of their mode of action. Certain pathogens also have the potential to adapt in a few generation to the selection pressure exerted by biocontrol agents.
Available information is sufficient to suggest that the assumption that durability of biological control is necessarily higher than that of chemical control may not always be justified. However, it is not sufficient to draw conclusions about the existence of specific traits related to the plant pathogen or related to the biocontrol agent that could explain the loss of effectiveness of a biocontrol agent in practice.
There is much need for further studies on issues related to this topic. Among them, the establishment of baseline sensitivity i. Such monitoring is carried out routinely for fungicide resistance in fungal plant pathogens world-wide Brent and Hollomon, It is a first step to evaluate the distribution and the potential impact of resistance in the field. Moreover, detection of partially resistant isolates may indicate a risk of developing a more severe resistance that subsequently may initiate a possible loss of control in the field.
Monitoring can be done at specific sites, for example to ascertain the implication of resistance in cases when loss of biocontrol effectiveness is observed in the field.
It can also be done at different dates to document the evolution of sensitivity following series of treatments with a given biocontrol agent and to monitor possible shifts in the natural populations of a plant pathogen, as suggested by Yang et al.
Finally, cross-resistance with other existing biocontrol agents or possibly fungicides may also be determined. In addition to the population approach described above, experimental evolution studies are also needed to evaluate the ability of plant pathogens to evolve under the selection pressure exerted by a biocontrol agent. This approach will result in identifying risk factors that can foster the selection of strains of plant pathogens resistant to biocontrol agents.
Various biocontrol agents and different plant pathogens must be tested in the future. This will result in identifying types of biocontrol agents with lower risk of efficacy loss, i.
Even though all biocontrol agents should create selection pressure on target populations of plant pathogen, some modes of action may present a clear opportunity for pathogens to evolve resistance. For example, a mechanism involving antibiosis would, by analogy with the fungicides, be considered a high risk to be overcome, whereas a multiple or a more complex mode of action would indicate relatively low risk.
This knowledge is essential to ensure a durable efficacy of biocontrol agents on target plant pathogens. Even if the data are too sparse to suggest general statement on the use of biocontrol agents in practice, this review highlights the necessity for careful management of their use once they become commercially available in order to avoid repeating the mistakes made with chemical fungicides.
For instance, we should consider alternating or combining biocontrol agents with different mechanisms of action. In addition to possibly ensure the durability of biological control, the combination of several biocontrol agents have shown to improve the efficacy and reduce the variability of efficacy Flaherty et al. The context of integrated pest management is probably an effective way to reduce the risk of resistance development but it necessitates to evaluate the compatibility of the biocontrol agents together with other protection methods.
The combined use of biocontrol agents together with pesticides requires that their efficiency is not altered when applied in conjunction or in alternation. Significant research efforts are also needed to anticipate the potential failure of biological control and integrate durability concerns in the screening procedure of new biocontrol agents. According to the results mentioned in this review, caution should be applied when screening and selecting isolates of biocontrol agents, to ensure a wide representation of the targeted plant pathogen population.
To test the efficacy of potential biocontrol agents or to screen for new biocontrol agents against plant diseases, most studies continue to use a single isolate or relatively few isolates. Innovative screening procedures based on the known mode of action have already been developed Schoonbeek et al.
We must go further by incorporating in the screening procedure, knowledge on the ability of plant pathogen to counteract these modes of action.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Ajouz, S. Comparison of the development in planta of a pyrrolnitrin-resistant mutant of Botrytis cinerea and its sensitive wild-type parent isolate. Plant Pathol.
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Ogrodnick Classical biological control In many instances the complex of natural enemies associated with an insect pest may be inadequate. This is especially evident when an insect pest is accidentally introduced into a new geographic area without its associated natural enemies. Examples of introduced vegetable pests include the European corn borer, one of the most destructive insects in North America. To obtain the needed natural enemies, we turn to classical biological control. This is the practice of importing, and releasing for establishment, natural enemies to control an introduced exotic pest, although it is also practiced against native insect pests.
The first step in the process is to determine the origin of the introduced pest and then collect appropriate natural enemies from that location or similar locations associated with the pest or closely related species.
The natural enemy is then passed through a rigorous quarantine process, to ensure that no unwanted organisms such as hyperparasitoids are introduced, then reared, ideally in large numbers, and released. Follow-up studies are conducted to determine if the natural enemy successfully established at the site of release, and to assess the long-term benefit of its presence. There are many examples of successful classical biological control programs.
One of the earliest successes was with the cottony cushion scale, a pest that was devastating the California citrus industry in the late s.
A predatory insect, the vedalia beetle, and a parasitoid fly were introduced from Australia. Within a few years the cottony cushion scale was completely controlled by these introduced natural enemies. Damage from the alfalfa weevil, a serious introduced pest of forage, was substantially reduced by the introduction of several natural enemies. About 20 years after their introduction, the alfalfa acreage treated for alfalfa weevil in the northeastern United States was reduced by 75 percent.
A small wasp, Trichogramma ostriniae, introduced from China to help control the European corn borer, is a recent example of a long history of classical biological control efforts for this major pest. Many classical biological control programs for insect pests and weeds are under way across the United States and Canada. Classical biological control is long lasting and inexpensive.
Other than the initial costs of collection, importation, and rearing, little expense is incurred. When a natural enemy is successfully established it rarely requires additional input and it continues to kill the pest with no direct help from humans and at no cost. Unfortunately, classical biological control does not always work. It is usually most effective against exotic pests and less so against native insect pests. The reasons for failure are often not known, but may include the release of too few individuals, poor adaptation of the natural enemy to environmental conditions at the release location, and lack of synchrony between the life cycle of the natural enemy and host pest.
Augmentation This third type of biological control involves the supplemental release of natural enemies. Relatively few natural enemies may be released at a critical time of the season inoculative release or literally millions may be released inundative release. Pesticides are grouped into five main categories depending on the purpose they are usually applied for.
The first group are the fungicides, which are act against fungi. Then there are herbicides which are used against weeds. Herbicides are taken up by the leaves or the roots of the weed, causing it to die. Insecticides that, as the name suggests, destroy harmful insects, and then there are acaricides which protect plants from mites.
Finally there are nematicides to control nematodes that attack the plants. The use of chemical pesticides is widespread due to their relatively low cost, the ease with which they can be applied and their effectiveness, availability and stability. Chemical pesticides are generally fast-acting, which limits the damage done to crops. Chemical pesticides have some major drawbacks, but they are still widely sold and used.
We will discuss four of the disadvantages of chemical pesticides here. First, chemical pesticides are often not just toxic to the organisms for which they were intended, but also to other organisms.
Chemical pesticides can be subdivided into two groups: non-selective and selective pesticides. The non-selective products are the most harmful, because they kill all kinds of organisms, including harmless and useful species.
For example, there are herbicides that kill both broad-leaf weeds and grasses. This means they are non-selective since they kill nearly all vegetation. Selective pesticides have a more limited range. They only get rid of the target pest, disease or weed and other organisms are not affected. An example is a weed killer that only works on broadleaf weeds. This could be used on lawns, for example, since it does not kill grass. These days, a combination of several products is usually required to control several pests because almost all permitted products are selective and thus only control a limited range of pests.
Another disadvantage of chemical pesticides is resistance. Pesticides are often effective for only a short period on a particular organism. Organisms can become immune to a substance, so they no longer have an effect.
These organisms mutate and become resistant. This means that other pesticides need to be used to control them. A third drawback is accumulation. If sprayed plants are eaten by an organism, and that organism is then eaten by another, the chemicals are can be passed up the food chain. Animals at the top of the food chain, usually predators or humans, have a greater chance of toxicity due to the build-up of pesticides in their system.
Gradually, however, this effect is becoming less relevant because pesticides are now required to break down more quickly so that they cannot accumulate. If they do not, they are not permitted for sale. Accumulation, which is illustrated here, is one of the disadvantages of chemical pesticides. Animals or humans at the end of a food chain have a greater chance of damage or dying due to the build-up of pesticides in their system.
This drawback is becoming less important, however, because pesticides that do not break down quickly enough are no longer permitted.
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