DeVine is used in Florida citrus groves against the alien invasive weed stranglervine. Plants produce a wide variety of secondary metabolites that deter herbivores from feeding on them. Some of these can be used as biopesticides. They include, for example, pyrethrins, which are fast-acting insecticidal compounds produced by Chrysanthemum cinerariaefolium [ 41 ]. They have low mammalian toxicity but degrade rapidly after application. This short persistence prompted the development of synthetic pyrethrins pyrethroids. The most widely used botanical compound is neem oil, an insecticidal chemical extracted from seeds of Azadirachta indica [ 42 ].
Two highly active pesticides are available based on secondary metabolites synthesized by soil actinomycetes. They fall within our definition of a biopesticide but they have been evaluated by regulatory authorities as if they were synthetic chemical pesticides. Spinosad is a mixture of two macrolide compounds from Saccharopolyspora spinosa [ 43 ]. It has a very low mammalian toxicity and residues degrade rapidly in the field. Farmers and growers used it widely following its introduction in but resistance has already developed in some important pests such as western flower thrips [ 44 ].
Abamectin is a macrocyclic lactone compound produced by Streptomyces avermitilis [ 45 ]. It is active against a range of pest species but resistance has developed to it also, for example, in tetranychid mites [ 46 ]. A semiochemical is a chemical signal produced by one organism that causes a behavioural change in an individual of the same or a different species.
The most widely used semiochemicals for crop protection are insect sex pheromones, some of which can now be synthesized and are used for monitoring or pest control by mass trapping [ 47 ], lure-and-kill systems [ 48 ] and mating disruption. Worldwide, mating disruption is used on over ha and has been particularly useful in orchard crops [ 49 ].
Biopesticides have a range of attractive properties that make them good components of IPM. Most are selective, produce little or no toxic residue, and development costs are significantly lower than those of conventional synthetic chemical pesticides [ 8 ]. Microbial biopesticides can reproduce on or in close vicinity to the target pest, giving an element of self-perpetuating control.
Biopesticides can be applied with farmers' existing spray equipment and many are suitable for local scale production. The disadvantages of biopesticides include a slower rate of kill compared with conventional chemical pesticides, shorter persistence in the environment and susceptibility to unfavourable environmental conditions.
Because most biopesticides are not as efficacious as conventional chemical pesticides, they are not suited for use as stand-alone treatments. However, their selectivity and safety mean that they can contribute meaningfully to incremental improvements in pest control [ 50 ].
A good example is the entomopathogenic fungus B. Spider mites are routinely managed using regular releases of predators, but there are often periods in the season when control breaks down. In the past, growers relied on conventional pesticides as a supplementary treatment but this has become ineffective because of pesticide resistance and it can have knock-on effects on other insect natural enemies.
Beauveria bassiana is effective against spider mites, has a short harvest interval, and is compatible with the use of predators [ 51 ].
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So it works well as an IPM component and is now the recommended supplementary treatment for spider mite on greenhouse crops across Europe. Worldwide there are about biopesticide products being sold [ 52 ]. The EU biopesticides consist of 34 microbials, 11 biochemicals and 23 semiochemicals [ 53 ], while the USA portfolio comprises microbials, 52 biochemicals and 48 semiochemicals [ 54 ]. To put this into context, these biopesticide products represent just 2.
However, the market may need to increase substantially more than this if biopesticides are to play a full role in reducing our overreliance on synthetic chemical pesticides. Companies will only develop biopesticide products if there is profit in doing so. Similarly, the decision for a farmer whether or not to adopt a novel technology can be thought of in economic terms as a cost-benefit comparison of the profits to be made from using the novel versus the incumbent technology. A number of features of the agricultural economy make it difficult for companies to invest in developing new biopesticide products and, at the same time, make it hard for farmers to decide about adopting the new technology:.
These factors mean that using conventional synthetic chemical pesticides applied on a calendar basis can be difficult to replace in favour of an IPM portfolio of alternative tactics including biopesticides. Chemical pest control may then become locked into the system until such a time that it fails, for example, if pesticide resistance becomes widespread, as in the greenhouse crops industry. In the case of biopesticides, the products that have been most successful so far, such as microbial Bt, are very similar to chemical pesticides. It is important to stress that chemical pesticides are and will remain a vital part of crop protection.
When used appropriately they can give excellent control with minimal adverse effects. The use of chemical pesticides should therefore be promoted within an IPM framework so that they are used sparingly to minimize the evolution of resistance in target pest populations. However, IPM will only work if farmers have access to a range of crop protection tactics together with the knowledge on how to integrate them. Biopesticides encompass a very wide range of living and non-living entities that vary markedly in their basic properties, such as composition, mode of action, fate and behaviour in the environment and so forth.
They are grouped together by governments for the purposes of regulating their authorization and use. These regulations are in place: firstly, to protect human and environmental safety; and secondly, to characterize products and thereby ensure that manufacturers supply biopesticides of consistent and reliable quality. The EU also requires that the efficacy of a biopesticide product is quantified and proved in order to support label claims.
Only authorized biopesticide products can be used legally for crop protection. The guidance of the OECD is that biopesticides should only be authorized if they pose minimal or zero risk. The biopesticide registration data portfolio required by the regulator is normally a modified form of the one in place for conventional chemical pesticides and is used by the regulator to make a risk assessment. It includes information about mode of action, toxicological and eco-toxicological evaluations, host range testing and so forth.
This information is expensive for companies to produce and it can deter them from commercializing biopesticides, which are usually niche market products. Therefore, the challenge for the regulator is to have an appropriate system in place for biopesticides that ensures their safety and consistency but which does not inhibit commercialization. Until very recently, it is true to say that government regulators—with the probable exception of the USA—were unfamiliar with biologically based pest management and were therefore slow to appreciate the need to make the regulatory process appropriate for biopesticides rather than treat them in the same way as synthetic chemical pesticides.
The decision whether or not to authorize a biopesticide product is made on the basis of expert opinion residing within the regulatory authority. When the regulators lack expertise with biopesticides, they tend to delay making a decision and may request the applicant to provide them with more data. There is also a risk that the regulator—using the chemical pesticide registration model—requests information that is not appropriate. Some regulatory authorities, the UK, for example, have acknowledged that basing the regulatory system for biopesticides on a chemical pesticides model has been a barrier to biopesticide commercialization [ 69 ].
A key question is whether the regulator, having recognized a problem, is able to do something about it. This can lead to systemic problems and stand in the way of introducing innovations into the regulatory system. This is not to say that regulatory innovation is not possible, and where there is sound evidence that a particular group of biopesticides presents minimal risk, the regulators have modified the data requirements. Other innovations are also being developed, which we discuss in the following sections.
IPM principles do not become mandatory until , but member states have been encouraged to use rural development programmes funded under the Common Agricultural Policy to provide financial incentives to farmers to start implementing IPM before this date. In the Commission's view, further research is still needed to develop successful crop-specific strategies for the deployment of IPM and this should include multidisciplinary research.
Although such services can be provided privately and their quality guaranteed by a system of certification, it may be that countries that have retained state extension services, such as Denmark, have an inherent advantage in providing IPM advice in a cost-effective way. This directive provided for a two-tier system of regulation involving the Community and member state levels.
However, it quickly became evident that mutual recognition between different member states was not working, hence undermining the functioning of the EU internal market and deterring the development of biopesticides and other innovative products. This proposal proved controversial during the passage of the legislation. It was eventually achieved with northern, central and southern zones and an EU-wide one for greenhouses. The new legislation gives a specific status to non-chemical and natural alternatives to conventional chemical pesticides and requires them to be given priority wherever possible.
Biopesticides should generally qualify as low-risk active substances under the legislation. Low-risk substances are granted initial approval for 15 years rather than the standard A reduced dossier can be submitted for low-risk substances but this has to include a demonstration of sufficient efficacy. One requirement for low-risk substances, that is still to be elaborated, is that their half-life in the soil should be less than 60 days and this may cause problems for some microbial biopesticides, such as rhizosphere-competent antagonists of soil-borne plant pathogens.
The new European legislation does not give the biopesticides industry all that it may have hoped for, but it does give biopesticides legislative recognition and opens up the potential for faster authorization processes and effective mutual recognition. This will require sustained work by those interested in the wider use of biopesticides. Many of the details of how mutual recognition in ecozones will operate in practice remain to be resolved, for example, how member states will interact with one another during the process.
The achievement of real gains is very sensitive to the detailed implementation of the new procedures. What is clear is that the considerable variations in the levels of resource available to regulatory authorities in different member states will be a constraint on effective delivery. In the EU, having a system of mutual recognition of plant protection products means that it is possible for one member state to engage in regulatory innovation and gain a first mover advantage over other member states. In relation to biopesticides, it is arguable that Britain has taken such a position.
Concern about the lack of availability of biopesticides in the UK led to the introduction in June of a pilot project to facilitate their registration. Its aim was to increase the availability of biopesticides by improving knowledge and raising awareness of the requirements of the UK government regulator at the time, the government regulator was the Pesticides Safety Directorate PSD but it has subsequently become the Chemicals Regulation Directorate CRD.
In April , the pilot project was turned into a fully fledged biopesticides scheme. Prior to the introduction of the scheme, just four products had been approved between and Following the introduction of the pilot project, seven products were guided to approval. In April , five products were at various stages of evaluation and several other companies were discussing possible applications with PSD. Two products were approved in and several were at various stages of the registration process. In order to better operate the scheme, the regulator provides specialist training on biopesticides to members of its pesticide approvals group and has assigned a biopesticides champion.
PSD thought it desirable to involve as many people in their pesticide approvals group in this work as possible, rather than having a unit that only dealt with biopesticides and which would probably have insufficient work. Trained staff members are able to participate in pre-submission meetings with applicant biopesticide companies. Particularly if they are held early in the process, they can help applicants to plan the acquisition of the data they need for registration and also avoid the compilation of any material that would be superfluous.
A number of such meetings were observed on a non-participant basis as part of our research. The meetings enabled the identification of gaps in the application dossier and mutually helpful discussions of how these could be filled, for example, by using data published in the scientific literature.
CRD intends to continue to operate the biopesticides scheme with reduced fees. The scheme has had to face a number of challenges. From a CRD perspective, the biopesticides scheme was seen as a pathfinder in Europe and it could make it the preferred regulation authority for such products providing it is able to maintain the process of regulatory innovation. Governments are likely to continue imposing strict safety criteria on conventional chemical pesticides, and this will result in fewer products on the market. Perhaps the biggest advances in biopesticide development will come through exploiting knowledge of the genomes of pests and their natural enemies.
Researchers are already using molecular-based technologies to reconstruct the evolution of microbial natural enemies and pull apart the molecular basis for their pathogenicity [ 74 — 76 ]; to understand how weeds compete with crop plants and develop resistance to herbicides [ 77 ]; and to identify and characterize the receptor proteins used by insects to detect semiochemicals [ 78 ]. This information will give us new insights into the ecological interactions of pests and biopesticides and lead to new possibilities for improving biopesticide efficacy, for example, through strain improvement of microbial natural enemies [ 79 ].
As the genomes of more pests become sequenced, the use of techniques such as RNA interference for pest management is also likely to be put into commercial practice [ 80 ]. We stated earlier that biopesticide development has largely been done according to a chemical pesticides model that has the unintended consequence of downplaying the beneficial biological properties of biopesticides such as persistence and reproduction [ 67 ] or plant growth promotion.
The pesticides model still has much to offer, for example, in improving the formulation, packaging and application of biopesticides. For example, biologists are only just starting to realize the true intricacies of the ecological interactions that occur between microbial natural enemies, pests, plants and other components of agroecosystems [ 81 ]. Take entomopathogenic fungi for instance. We now know that species such as B. This creates new and exciting opportunities for exploiting them in IPM, for example, by inoculating plants with endophytic strains of entomopathogenic fungi to prevent infestation by insect herbivores.
There are opportunities also to exploit the volatile alarm signals emitted by crop plants so that they recruit microbial natural enemies as bodyguards against pest attack [ 83 — 85 ] and to use novel chemicals to impair the immune system of crop pests to make them more susceptible to microbial biopesticides [ 86 , 87 ]. The biopesticide products that will result from new scientific advances may stimulate the adoption of different policies in different countries.
We have seen this already with genetically modified GM crops. In Europe, by contrast, there has been widespread resistance among consumers to GM crops and the EU excludes them from the biopesticide regulatory process. Another complex issue surrounds the regulation of biopesticides that have multiple modes of action. For example, species of the fungus Trichoderma , which are used as biopesticides against soil-borne plant pathogenic fungi, are able to parasitize plant pathogenic fungi in the soil; they also produce antibiotics and fungal cell wall degrading enzymes, they compete with soil-borne pathogens for carbon, nitrogen and other factors, and they can also promote plant growth by the production of auxin-like compounds [ 89 , 90 ].
Some Trichoderma products have been sold on the basis of their plant growth promoting properties, rather than as plant protection products, and so have escaped scrutiny from regulators in terms of their safety and efficacy. In general, the adoption of IPM tactics is correlated with farmer education and experience and the crop environment with IPM being adopted more on horticultural crops [ 91 ]. We have mentioned previously that biocontrol-based IPM has been adopted widely by the greenhouse crops industry but is not used much by growers of broad-acre crops.
Greenhouses represent intensively managed, controlled environments that are highly suitable for IPM. Biocontrol adoption was undoubtedly helped by the fact that greenhouse crop production is labour intensive and technically complex, and thus growers already had a high level of knowledge and were used to technological innovation. How IPM and alternative technologies such as biopesticides can be taken out to broad-acre crops and the wider rural environment—where human capital is spread thinly and where the ecological environment is far more complex and less stable than in a greenhouse—is an interesting question, and one where public policy is likely to play an important role.
The total systems approach is based: firstly, on managing the agroecosystem to promote pest regulating services from naturally occurring biological control agents, for example, by providing refugia and alternative food sources for natural enemies within the crop and in field margins; and secondly, on making greater use of crop varieties bred with tissue-specific and damage-induced defences against pests [ 92 ]. Biopesticides would have an important role as back-up treatments in this system, although some biopesticides could also be used as preventative treatments, e. To make IPM work in the total system concept, institutional arrangements would be required that: provide a market for natural pest regulation as an ecosystem service; promote biopesticides and other environmentally benign technologies in agriculture; value human and natural capital in rural areas; and synthesize knowledge on natural science, economics, and the social dimension of agriculture and the rural environment see, for example, [ 93 ].
Such a holistic system for pest management would require far better integration of the existing policy network [ 94 ]. This may seem like an ambitious proposition, but it is becoming increasingly necessary. One area that certainly warrants greater consideration for the future is the attitude of the public and the food retailers to biopesticides and other alternative pest management tools.
There is concern among the public about pesticide residues in food but there is little public debate about the use of alternative agents in IPM. In our research, we have found that the major food retailers have done little to engage in discussions about making biological alternatives to synthetic chemical pesticides available to farmers and growers.
PMID: Bailey , 2 G. Grant 3. Alastair S. Mark Tatchell. Wyn P. This article has been cited by other articles in PMC. Abstract Over the past 50 years, crop protection has relied heavily on synthetic chemical pesticides, but their availability is now declining as a result of new legislation and the evolution of resistance in pest populations. Keywords: biopesticide, Integrated Pest Management, adoption, regulation.
Agriculture and the environment - OECD
However, the use of synthetic pesticides is becoming significantly more difficult owing to a number of interacting factors: — The injudicious use of broad-spectrum pesticides can damage human health and the environment [ 5 , 6 ]. Worldwide, over species of arthropod pests have resistance to one or more insecticides [ 8 ], while there are close to species of herbicide-resistant weeds [ 9 ].
However, the rate at which new, safer chemicals are being made available is very low. This is caused by a fall in the discovery rate of new active molecules and the increasing costs of registration [ 12 ]. These concerns are voiced despite the fact that pesticides are among the most heavily regulated of all chemicals. Integrated pest management There is an urgent requirement for alternative tactics to help make crop protection more sustainable.
The main IPM tactics include: — Synthetic chemical pesticides that have high levels of selectivity and are classed by regulators as low-risk compounds, such as synthetic insect growth regulators.
These include the calculation of economic action thresholds, phenological models that forecast the timing of pest activity, and basic pest scouting. These tools can be used to move pesticide use away from routine calendar spraying to a supervised or targeted programme. Biopesticides Biopesticides are a particular group of crop protection tools used in IPM. Examples of some commercially available biopesticides. Open in a separate window. Biopesticide commercialization Worldwide there are about biopesticide products being sold [ 52 ].
A number of features of the agricultural economy make it difficult for companies to invest in developing new biopesticide products and, at the same time, make it hard for farmers to decide about adopting the new technology: — Lack of profit from niche market products. The up-regulation of transporter genes during symbiosis indicated the action of transportation of useful compounds like amino acids, oligopeptides and polyamines through the symbiotic interface from one organism to other. Free living mycelium can take nitrate and ammonium from the soil.
Subsequently, these compounds reach the mantle and hartig net and are then transferred to the plants. Cysteine-rich proteins MISSP7 of fungus play an important role as effectors and facilitators in the formation of symbiotic interfaces [ ]. Many genes related to auxin biosynthesis and root morphogenesis showed up-regulation during mycorrhizal colonization [ 69 , , ]. Further, G. Bioactive compounds called Myc factors similar to Nod factors of Rhizobium are suggested to be secreted by mycorrhiza and Rhizobium and perceived by host roots for the activation of signal transduction pathway or common symbiosis SYM pathway [ , ].
The pathways that prepare plant for both AM and Rhizobium infection have some common points. The common SYM pathway prepares the host plant to bring about changes at the molecular and anatomical level with the first contact of fungal hyphae. Rhizobium leguminosarum biovar viciae can induce various genes in the plants like pea, alfalfa and sugar beet as evident from the microarray studies [ 40 ]. PGPR produce IAA which, in turn, induces the production of nitric Oxide NO , which acts as a second messenger to trigger a complex signaling network leading to improved root growth and developmental processes [ ].
Expression of ENOD11 and many defense-related genes and root remodelling genes get up-regulated during entry. Subsequently, this allows the formation of a pre-penetration apparatus or PPA [ ]. Though the biology behind the development of arbuscules is unknown, a gene called vapyrin when knocked down causes a decline in the growth of arbuscules [ ]. Many other genes including subtilisin protease 65, phosphate transporter 66 or two ABC transporters 67 are known to be involved in arbuscules formation [ , ].
Nitrogen-fixation genes are popularly used by scientists today to create engineered plants that can fix atmospheric nitrogen. The induction of nif genes in case of nitrogen fixing bacteria takes place under low concentration of nitrogen and oxygen in the rhizosphere [ 1 ]. Interestingly, sugarcane plantlets inoculated with a wild strain of G. Efficiency of nitrogen fixation is dependent on the utilization of carbon [ , ]. A bacterium like Bacillus subtilis UFLA can differentially induce genes in cotton plant as compared to control where no PGPR was supplied to the cotton plant [ 85 ]. Various differentially expressed genes were identified which include metallothionein-like protein type 1, a NODlike membrane integral protein, ZmNIP, a thionin family protein, an oryzain gamma chain precursor, stress-associated protein 1 OsISAP1 , probenazole-inducible protein PBZ1 and auxin and ethylene-responsive genes [ ].
The expression of the defense-related proteins PBZ1 and thionins were found to get repressed in the rice—H seropedicae association, suggesting the modulation of plant defense responses during colonisation [ ]. Among the PGPR species, Azospirillum was suggested to secrete gibberellins, ethylene and auxins [ ]. Some plant associated bacteria can also induce phytohormone synthesis, for example lodgepole pine when inoculated with Paenibacillus polymyxa had elevated levels of IAA in the roots [ ].
Rhizobium and Bacillus were found to synthesize IAA at different cultural conditions such as pH, temperature and in the presence of agro waste as substrate [ ]. Ethylene, unlike other phytohormones, is responsible for the inhibition of growth of dicot plants [ 69 ]. It was found by Glick et al. Interestingly, a model was suggested in which it was shown that ethylene synthesis from 1-aminocyclopropanecarboxylate ACC , an immediate precursor of ethylene, which is hydrolyzed by bacterial ACC-deaminase enzyme in the need of nitrogen and carbon source is also one of the mechanisms of induction of conditions suitable for growth.
ACC-deaminase activity was also found in the bacteria such as Alcaligenes sp. The involvement of ACC deaminase in the indirect influence on the growth of plants was proved in Canola, where mutations in ACC deaminase gene caused the loss of effect of growth promoting Pseudomonas putida [ 29 ]. Gene encoding glucose dehydrogenase gcd involved in the DO pathway was cloned and characterized from Acinetobacter calcoaceticus and E.
Also a soluble form of gcd has been cloned from Acinetobacter calcoaceticus and G. Furthermore there are reports of site-directed mutagenesis of glucose dehydrogenase GDH and gluconate dehydrogenase GADH that has improved the activity of this enzyme. Mere substitution of SM provided thermal stability to E. The application of this technology was achieved by transferring genes involved in the DO pathway viz.
Hypothetical mechanism of action of biofertilizers in the root cell. The whole pathway involves receptor like kinases or other kinase related proteins like DMI and SYM71 to phosphorylate their substrates [ , ]. DM1 proteins play role in maintaining periodic oscillation of calcium ions inside and outside the nucleus. CCaMK is a calcium calmodulin-dependent protein kinase, which phosphorylate the product of CYCLOPS protein thus initiating activation of various genes involving formation of structures like nodule and PPA pre-penetration apparatus [ ].
Environmental stresses are becoming a major problem and productivity is declining at an unprecedented rate. Our dependence on chemical fertilisers and pesticides has encouraged the thriving of industries that are producing life-threatening chemicals and which are not only hazardous for human consumption but can also disturb the ecological balance.
Biofertilizers can help solve the problem of feeding an increasing global population at a time when agriculture is facing various environmental stresses. It is important to realise the useful aspects of biofertilizers and implement its application to modern agricultural practices. The new technology developed using the powerful tool of molecular biotechnology can enhance the biological pathways of production of phytohormones. If identified and transferred to the useful PGPRs, these technologies can help provide relief from environmental stresses. However, the lack of awareness regarding improved protocols of biofertiliser applications to the field is one of the few reasons why many useful PGPRs are still beyond the knowledge of ecologists and agriculturists.
Nevertheless, the recent progresses in technologies related to microbial science, plant-pathogen interactions and genomics will help to optimize the required protocols. The success of the science related to biofertilizers depends on inventions of innovative strategies related to the functions of PGPRs and their proper application to the field of agriculture.
The major challenge in this area of research lies in the fact that along with the identification of various strains of PGPRs and its properties it is essential to dissect the actual mechanism of functioning of PGPRs for their efficacy toward exploitation in sustainable agriculture. RKS supported the paper writing, data researching and revised the changes made to this paper. NT approved the changes made, and also with data researching and formatted the review. All authors read and approved the final manuscript.
National Center for Biotechnology Information , U. Journal List Microb Cell Fact v. Microb Cell Fact. Published online May 8. Author information Article notes Copyright and License information Disclaimer. Corresponding author. Deepak Bhardwaj: moc. Received Feb 25; Accepted Apr This article has been cited by other articles in PMC. Abstract Current soil management strategies are mainly dependent on inorganic chemical-based fertilizers, which caused a serious threat to human health and environment.
Keywords: Biofertilizer, Crop improvement, Environmental stress, Mode of action of biofertilizers, Sustainable agriculture. Introduction Conventional agriculture plays a significant role in meeting the food demands of a growing human population, which has also led to an increasing dependence on chemical Fertilizers and pesticides [ 1 ]. The microbiome: potential significance of beneficial microbes in sustainable agriculture The rhizosphere, which is the narrow zone of soil surrounding plant roots, can comprise up to 10 11 microbial cells per gram of root [ 11 ] and above 30, prokaryotic species [ 12 ] that in general, improve plant productivity [ 12 ].
Open in a separate window. Figure 1. Biofertlizers exploitation and nutrients profile of crops A key advantage of beneficial microorganisms is to assimilate phosphorus for their own requirement, which in turn available as its soluble form in sufficient quantities in soil.
Biofertilizers relevance and plant tolerance to environmental stress Abiotic and biotic stresses are the major constraints that are affecting the productivity of the crops. Mechanism of action of various biofertilizers Mycorrhiza is the association of fungus with the roots of higher plants. Figure 2. Conclusions Environmental stresses are becoming a major problem and productivity is declining at an unprecedented rate.
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