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Insect resistance to biopesticides


Mechanisms of insecticide resistance in insects.

Use of biopesticides or non-chemical pesticides is encouraged as a part of integrated pest management (IPM) for environmental and human safety and to reduce the risk of insecticide resistance.  With the increase in biopesticide use in both organic and conventional cropping systems, it is a good time to review the potential of insect resistance to botanical and microbial pesticides. 

Insects and mites develop resistance to chemical pesticides through genetic, metabolic, or behavioral changes resulting in reduced penetration of toxin, increased sequestration or excretion, reduced binding to the target site, altered target site that prevents binding of the toxin, or reduced exposure to the toxin through modified behavior.  When the active ingredient is a toxic molecule and has the mode of action similar to that of a chemical compound, regardless of the plant or microbial origin, arthropods are more likely to develop resistance through one or more of the abovementioned mechanisms.  When the mode of action is infection by a microorganism, rather than a toxin, arthropods are less likely to develop resistance.  Under natural circumstances, plants, insects, natural enemies, and beneficial or harmful microbes continuously co-evolve and adapt to changing environment.  When there is a higher selection pressure, such as indiscriminate use of chemical pesticides, increased mutagenesis can lead to resistance issues.  A good understanding of insect resistance to biopesticides will help minimize potential risks and improve their efficient use in IPM.

Resistance to botanical pesticides

            Nicotine, an alkaloid from Nicotiana spp., is one of the earlier botanical pesticides known.  Although nicotine is not currently used as an insecticide, its synthetic alternatives – neonecotinoids – are commonly used against several pests.  Botanical insecticide pyrethrum, extracted from the flowers of Chrysanthemum cinerariaefolium, contains insecticidal pyrethrins (synthetic pyrethrins are referred to as pyrethroids).  Although insect resistance to pyrethrum or pyrethroid compounds has been known (Whitehead, 1959; Immaraju et al., 1992; Glenn et al., 1994), they have been effectively used against a number of pests through careful placement in IPM, organic, or conventional management strategies.  Additionally, pyrethrin products have been effectively used along with piperonyl butoxide, which acts as a synergist and resistance breaker (Gunning et al. 2015).

Another botanical insecticidal compound, azadirachtin, is a tetranortriterpenoid limonoid from neem (Azadirachta indica) seeds, which acts as an insecticide, antifeedant, repellent and insect growth regulator.  While neem oil, which has a lower concentration of azadirachtin, has been used in the United States as a fungicide, acaricide, and insecticide for a long time, several azadirachtin formulations in powder and liquid forms have become popular in recent years and were found effective in managing important pests (Dara 2015a and 2016).  Feng and Isman (1995) reported that the green peach aphid, Myzus persicae developed resistance to pure azadirachtin under artificially induced selection pressure after 40 generations, but did not develop resistance to a refined neem seed extract.  They suggested that natural blend of azadirachtin compounds in a biopesticide would not exert selection pressure that could lead to resistance.  Additionally, Mordue and Nisbet (2000) discussed that azadirachtin can play a role in insecticide resistance management because it reduces the detoxification enzyme production as a protein synthesis inhibitor.  Azadirachtin also improved the efficacy of other biopesticides in multiple studies (Trisyono and Whalon, 2000; Dara, 2013 and 2015b).

Insects feeding on plant allelochemicals can develop cross-resistance to insecticides (Després et al., 2007).  For example, overproduction of detoxification enzymes such as glutathione S-transferases and monooxygenases in the fall armyworm, Spodoptera frugiperda,when it fed on corn and cowpea, respectively, imparted cross-resistance to various chemical pesticides.  It is important to keep this in mind when botanical pesticides are used to detect potential resistance issues.

Resistance to bacterial biopesticides

            Bacillus thuringiensis (Bt)is a gram-positive soil bacterium, which contains crystalline toxic protein that is activated upon ingestion by an insect host, binds to the receptor sites in the midgut, and eventually causes insect death.  Since the mode of action involves a toxin rather than bacterial infection, several insects developed resistance to Bt pesticides or transgenic crops that contain Bt toxins (Tabashnik et al., 1990; McGaughey and Whalon, 1992; Tabashnik, 1994; Iqbal et al., 1996).  However, Bt pesticides are still very popular and used against a variety of lepidopteran (Bt subsp. aizawai and Bt subsp. kurstaki), dipteran (Bt subsp. israelensis and Bt subsp. sphaericus), and coleopteran (Bt subsp. tenebrionis) pests.

            Spinosad is a mixture of macrocyclic lactones, spinosyns A and spinosyns D, derived from Saccharopolyspora spinosa, an actinomycete gram-positive bacterium, and is used against dipteran, hymenopteran, lepidopteran, thysanopteran, and other pests. Spinosad products, while naturally derived are registered as chemical pesticides, not as biopesticides. Insect resistance to spinosad later led to the development of spinetoram, which is a mixture of chemically modified spinosyns J and L.  Both spinosad and spinetoram are contact and stomach poisons and act on insect nervous system by continuous activation of nicotinic acetylcholine receptors.  However, insect resistance to both spinosad (Sayyed et al., 2004; Bielza et al., 2007) and spinetoram (Ahmad and Gull, 2017) has been reported due to extensive use of these pesticides.  Cross-resistance between spinosad and some chemical insecticides has also occurred in some insects (Mota-Sanchez et al., 2006; Afzal and Shad, 2017).

Resistance to viral biopesticides

            Baculovirus infections in lepidoptera have been known for centuries, especially in silkworms.  Currently, there are several commercial formulations of nucleopolyhedroviruses (NPV) and granuloviruses (GV).  When virus particles are ingested by the insect host, usually lepidoptera, they invade the nucleii of midgut, fatbody, or other tissue cells and kill the host.  Baculoviruses are generally very specific to their host insect species and can be very effective in bringing down the pest populations.  However, variations in the susceptibility of certain insect populations and development of resistant to viruses has occurred in several host species (Siegwart et al., 2015).  Resistance to different isolates of Cydia pomonella granulovirus (CpGV-M, CpGV-S) in codling moth (Cydia pomonella) populations is well known in Germany and other parts of Europe (Sauer et al., 2017a & b).

Resistance to fungal biopesticides

            There are several fungi that infect insects and mites.  Fungal infection starts when fungal spores come in contact with an arthropod host.  First, they germinate and gain entry into the body by breaching through the cuticle.  Fungus later multiplies, invades the host tissues, kills the host, and emerges from the cadaver to produce more spores.  Entomophthoralean fungi such as Entomophthora spp., Pandora spp., and Neozygites spp. can be very effective in pest management through natural epizootics, but cannot be cultured in vitro for commercial scale production.  Hypocrealean fungi such as Beauveria bassiana, Isarea fumosorosea, Metarhizium brunneum, and Verticillium lecanii,on the other hand, can be mass-produced in vitro and are commercially available.  These fungi are comparable to broad-spectrum insecticides and are pathogenic to a variety of soil, foliar, and fruit pests of several major orders.  Since botanical, bacterial, and viral biopesticides have insecticidal metabolites, proteins, or viral particles that have specific target sites and mode of action, insects have a higher chance of developing resistance through one or more mechanisms.  Although fungi also have insecticidal proteins such as beauvericin in B. bassiana and I. fumosorosea and dextruxin in M. anisopliae and M. brunneum, their mode of action is more through fungal infection and multiplication and arthropods are less prone to developing resistance to entomopathogenic fungi.  However, insects can develop resistance to entomopathogenic fungi through increased melanism, phenoloxidase activity, protease inhibitor production, and antimicrobial and antifungal peptide production (Wilson et al., 2001; Zhao et al., 2012; Dubovskiy et al., 2013).  It appears that production of detoxification enzymes in insects against fungal infections can also impart resistance to chemical pesticides.  Infection of M. anisopliae in the larvae of greater wax moth, Galleria mellonella, increased dexotification enzyme activity and thus resistance to malathion (Serebrov et al., 2006).

            These examples show that insects can develop resistance to biopesticides in a manner somewhat similar to chemical pesticides, but due to the typically more complex and multiple modes of action, at a significantly lesser rate depending on the kind of botanical compound or microorganism involved.  Resistance to entomopathogenic fungi is less common than with other entomopathogens. Since biopesticide use is not as widespread as chemical pesticides, the risk of resistance development is less for the former.  However, excessive use of any single tool has the potential for resistance or other issues and IPM, which uses a variety of management options, is always a good strategy.

Acknowledgements: Thanks to Pam Marrone for reviewing the manuscript.

References

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Posted on Wednesday, December 6, 2017 at 8:43 AM

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