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Review Cite This: J. Agric. Food Chem. 2018, 66, 7553−7561

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Interaction of Chemical Pesticides and Their Formulation Ingredients with Microbes Associated with Plants and Plant Pests Stephen O. Duke*,† †

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USDA-ARS, Natural Products Utilization Research Unit, P.O. Box 1848, University, Mississippi 38677, United States of America ABSTRACT: Chemical pesticides and their formulation ingredients can have unintended effects on microbes associated with plants and plant pests. These effects can be due to direct effects on the microbes or to effects on crops or weeds that subsequently affect the microbes. In addition to fungicides, some insecticides, herbicides, and formulation compounds are toxic to plant pathogenic microbes, as well as to potentially beneficial microbes, such as those that infect insect pests. These chemicals, especially herbicides, can also indirectly affect microbes through their effects on crops and weeds. For example, glyphosate strongly impairs shikimic acid pathway-based plant defenses to microbial diseases in glyphosate-susceptible plants, significantly increasing its efficacy as an herbicide. Some herbicides induce plant defenses against plant pathogens. For a complete understanding of integrated pest management and overall cost/benefit of pesticide use, much more information is needed on microbial/pesticide interactions. KEYWORDS: biocontrol, fungicide, herbicide, insecticide, microbe, plant pathogen

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INTRODUCTION Synthetic pesticides have been the most used technology for management of agricultural pests for more than 70 years. Despite this heavy reliance, relatively little research has been conducted on the influence of these chemicals on nontarget microorganisms. Such microbes can be beneficial to crop production (e.g., microbial biopesticides, many endophytes, and growth-promoting rhizosphere bacteria) or detrimental (e.g., some plant pathogens), and depending on the dose, effects of pesticides can be either beneficial or harmful to these individual microbes and can alter the microbial community. Furthermore, the effect of the pesticides on the microbe can be either indirect (e.g., through effects on the plant response to the microbe) or direct. Formulation ingredients used with many pesticides can also have profound effects on microbes, and much of the literature is confounded by not separating effects of the pesticide from its formulation ingredients. Thus, this general topic is quite complex, with many potential interactions, most of which have not been studied in any detail, if at all. Studying these interactions can provide a better understanding of integrated pest management and the benefits and costs of pesticide use. This area of research was of great interest to the late Jack Altman, who edited a book on pesticide interactions in agriculture in 1993 (reprinted but not revised in 2017),1 several of the chapters of which overlap with this review. For example, there is a chapter on effects of pesticides on soilborne plant pathogens.2 Since this book was published, there have been few reviews on topics related to pesticide effects on nontarget microbes. Exceptions are the reviews of Hoagland,3 Duke et al.,4 and Gressel5 on the interactions of synthetic herbicides with plant pathogens and microbial bioherbicides and those of Kortekamp6 and Sanyal and Shrestha7 on side effects and direct effects of herbicides on plant-pathogen interactions. More focused reviews are available on the effects of the most used pesticide, glyphosate, on plant pathogens.8−10 © 2018 American Chemical Society

There is also a recent review on microbiome microbe involvement in pesticide resistance,11 a topic that this review will not cover. In the past decade, many crop growthstimulating microbes have been patented and developed, and some of these are being used commercially.12,13 The market for these products is rapidly increasing.13 Yet, very little is known of the compatibility of these products with chemical pesticides. An objective of this review is to provide a critical, updated review of chemical pesticide effects on nontarget microbes, but not to provide an encyclopedic discussion of all of the literature on this topic. A second objective is to make readers aware of the importance of pesticide/formulation ingredient interactions with nontarget microbes in agriculture and to point out some of the many unanswered questions in this research area.

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DIRECT EFFECTS OF FORMULATED AND UNFORMATED PESTICIDES As mentioned earlier, much of the literature on effects of pesticides on microbes, like much of the toxicological literature, is confounded by using only a commercial pesticide which can contain formulation ingredients that have their own toxicity profiles (see Formulation Ingredients section below). Even if the formulation ingredients are nontoxic, they can synergize the effects of the pesticide on the intended pest as well as other organisms, the reason that they are used. Thus, to realistically determine the effect of a pesticide on microbes in the field, formulated products as used by farmers must be used. Even when a pure pesticide is used, the researchers often add a formulation ingredient of their own to get the pesticide in solution and/or to improve uptake. In much of what is Received: Revised: Accepted: Published: 7553

May 2, 2018 July 1, 2018 July 5, 2018 July 5, 2018 DOI: 10.1021/acs.jafc.8b02316 J. Agric. Food Chem. 2018, 66, 7553−7561

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Journal of Agricultural and Food Chemistry

control could alleviate some of the adverse interactions.19 However, this strategy could be complicated by the number of commercial fungicides with many different modes of action used in agriculture. Furthermore, the potential for gene flow of fungicide resistance genes to crop pathogens would have to be considered. Herbicides. Many herbicides are directly toxic to microbes. Table 1 provides some examples of direct inhibitory effects of herbicides on plant pathogens. For example, Wyse et al.14 reported strong reductions in sporulation of the plant pathogen Phomopsis amaranthicola by a range of herbicides used at their highest approved rate for application (Table 1). An issue with many of the papers listed in Table 1 is that most of the studies listed used commercial formulations of herbicides (see

discussed below, I try point out whether the authors used technical grade pesticides alone or formulated versions of the pesticide. Unfortunately, there are few papers that examine the effects of technical grade, unformulated pesticides on microbes or have the proper formulation blank controls. Fungicides. Since the function of agricultural fungicides is to kill or manage fungal pathogens of crops, it is expected that they may have effects on fungal microbes other than crop pathogens. For example, Wyss et al.14 found several commercial, formulated fungicides (benomyl, copper hydroxide, chlorothalonil, fosetyl-Al, iprodione, maneb, mancozeb, and vinclozolin) used to control crop diseases to be highly inhibitory to the fungal weed biological control plant pathogen Phomopsis amaranthicola. None of the fungicides that they tested were compatible with P. amaranthicola. Although they tested only a few fungicides, it is clear that the simultaneous use of fungicides for crop disease control and mycopesticides for pest management is problematic. Fungicides can antagonize microbes such as Trichoderma viride, which is used for biological control of soil and seed-born plant pathogens. The mycelial growth of this biological control agent is strongly inhibited by the commercial fungicides hexaconazole, copper oxychloride, and benomyl and was found to be incompatible with seed treatment with commercial, formulated fungicides mancozeb, captan, and carbendazim.15 Similarly, the commercially formulated fungicides hexaconazole, propiconazole, triflumizole, tebuconazole, and tridemorph were found to completely inhibit mycelial growth of Trichoderma harzianum at 10, 25, 50, 200, and 300 mg L−1, respectively.16 Conversely, some fungicides can act additively or even synergistically with certain biocontrol microbes. For example, when treatments of the commercially formulated fungicide iprodinone or the microbial biofungicide T. harzianum that each reduced Botrytis cinerea infection of the cucumber by about 50% were combined, the disease incidence and severity were reduced almost entirely.17 Use of fungicide-resistant mutants of biocontrol microbes can make the biocontrol organism compatible with fungicides that complement their activity.18 An example is the use of benomyl-resistant T. viride with benomyl in the control of Fusarium oxysporum in Chrysanthemum morifloium.19 Fungicides inhibit the germination and growth of entomopathogenic fungi that can be used as bioinsecticides. For example, two (mancozeb and metiram) of four commercially formulated fungicides tested were fungitoxic to the entomopathogenic fungus Beauveria bassiana.20 In a more extensive study, nine fungicides (zineb + copper oxychloride, mancozeb, tradimefon, copper oxychloride, metalaxyl, sufur, sulfur + nitrothal-isopropyl, and hymexazol) had generally toxic effects on eight different entomopathogenic fungi: Beauveria bassiana, Conidiobolus coronatus, C. thromboides, Metarhizium anisopliae, Paecilomyces farinosus, P. f umosoroseus, Scopulariopsis brevicaulis, and Verticillium lecanii.21 Commercial formulations of benomyl, metalaxyl, mancozeb, and captafol were inhibitory to Entomophthora planchoniana in vitro.22 This fungus infects and sometimes controls green peach aphids. In the field, aphid numbers in potatoes were highest when metalaxyl, mancozeb, or captafol were applied, indicating that this entomopathogenic fungus was negatively affected by these fungicides. Genetically modifying microbes used for biocontrol of weeds or insects to be resistant to fungicides used for crop pathogen

Table 1. Direct Inhibitory Effects of Formulated and Unformulated Herbicides on Plant Pathogens, Biological Control Agents, and Plant Growth-Promoting Microorganisms herbicide atrazine bentazon bromoxynil clethodim diclofop-methyl diquat diuron glufosinate

glyphosate

imazapyr linuron MCPP oxyfluorfen paraquat pendimethalin pyrithioc sodium quizalofop ethyl sethoxydim trifluralin 2,4-D

microbe

reference

Trichoderma viride Colletotrichum truncatum Rhizoctonia cerealis Pseudocercosporella herpotrichoides Phomopsis amaranthicola C. truncatum Cercospora rodmanii P. amaranthicola A. flavus R. solani Sclerotinia homeocarpa Puccinia lagenophora Dreschlera teres Dactylaria higginsii Calonectria crotalariae Pythium ultimum Fusarium nivale F. solani R. solani T. viride Azotobacter vinelandii Bradyrhizobium japonicum Pseudomonas oxyzihabitans Burkholderia gladioli F.m culmorum F. oxysporum P. amaranthicola P. amaranthicola P. amaranthicola D. higginsii D. teres T. viride T. viride T. viride P. amaranthicola F. solani P. lagenophora C. rodmani

15a 23 24a 24a 14a 23 25 14a 26a 27 27 28a 29a 30a 31a 32 33 34a 34a 15a 35a 36 37a 37a 38a 38a 14a 14a 14a 30a 29a 15a 15a 15a 14a 39 28a 25

a

The authors used either commercial products which contain ingredients in addition to the herbicide, formulated technical grade herbicide with other ingredients, or the paper did not divulge whether the herbicide was technical grade or a formulated product.

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DOI: 10.1021/acs.jafc.8b02316 J. Agric. Food Chem. 2018, 66, 7553−7561

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Journal of Agricultural and Food Chemistry footnote), making it impossible to determine whether the effects shown are due to the herbicide, the formulation ingredients, or both. Pesticide formulation ingredients can have profound effects on microbes (see Formulation Ingredients section below). In two of the papers listed in Table 1, technical grade herbicide was compared with the formulated, commercial herbicide.33,39 After 24 h of treatment, there was little difference in the effect of technical grade and formulated trifluralin on germtube growth Fusarium solani.39 But, formulated trifluralin inhibited mycelia growth after 12 days at concentrations of nonformulated trifluralin that stimulated growth. Early work on glyphosate by Grossbard33 reported that, although pure glyphosate is toxic to a variety of fungi, the formulation ingredients alone can be even more fungitoxic. Determination of the role of formulation ingredients of commercial pesticide products in the toxicity to microbes is difficult, because obtaining these ingredients as they are formulated in a commercial product is usually not possible, as formulations are often trade secrets. However, comparisons can be made of the pure pesticide with the formulated product on the basis of the same concentration of the pesticide.39 The most heavily utilized herbicide worldwide, glyphosate,40 is toxic to many bacteria and fungi (Table 1).41 Presumably, glyphosate acts by the same mode of action on these microbes as it does in plants, by inhibition of the shikimate pathway enzyme 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS), which is present in plants, fungi, and bacteria.42 However, not all microbes are inhibited by glyphosate, and some microbial forms of EPSPS are resistant to glyphosate. In fact, the most used transgene to produce glyphosate-resistant (GR) crops is the CP4 gene from Agrobacterium sp., which encodes a GR form of EPSPS.43 Some microbes can even benefit from glyphosate. For example, the plant growthpromoting rhizobacterium Enterobacter cloacae degrades glyphosate and can use it as a phosphorus source.44 Endophytic microbes are known to provide some level of herbicide tolerance to some plants by metabolically degrading some herbicides taken up by the plant or by inducing higher levels of metabolic degradation by the plant.11,45 However, even though some plants metabolize glyphosate, there is no clear evidence that glyphosate degradation is a mechanism of tolerance or resistance to this herbicide.46 There may be beneficial aspects of the fungitoxic effects of some herbicides. For example, crops that have been made completely resistant to a particular herbicide47 can directly benefit from the use of that herbicide on the resistant crop due to the fungicidal or antibiotic effect of the herbicide. Indeed, infection by several plant pathogens has been found to be reduced in both glyphosate- and glufosinate-resistant crops sprayed with the herbicides.27,41,48−56 An example of glyphosate reduction of wheat rust in GR wheat is provided in Figure 1. Some diseases can be partially controlled in nonGR plants, with sublethal applications of glyphosate. For example, leaf area infected by the rust Puccinia psidii in Eucalyptus grandis was reduced by sublethal glyphosate applications.57 Glyphosate has even been patented for disease control in GR crops.58 In the case of glyphosate reduction of Asian soybean rust (Phakospora pachyrhizi) in GR soybeans, there is good evidence that the effect is through a direct effect on the EPSPS of this pathogen.41 The most dramatic direct effects of a herbicide on a plant pathogen in vivo are those of glyphosate on rusts. But, the beneficial effects are not as robust as those of commercial fungicides, and timing of the glyphosate

Figure 1. Effect of glyphosate treatment on severity of wheat leaf rust (Puccinia triticina) in GR wheat. (A) No glyphosate at 13 days after innoculation with wheat rust. (B) Treated with glyphosate at 0.84 kg ae ha−1 14 days before innoculation and photographed 13 days after innoculation. (C) Glyposate treatment 1 day before innoculation. Reproduced with permission from ref 48. Copyright National Academy of Science, USA, 2005.

application for weed management in GR crops is not likely to coincide with the best time for application of a fungicide. Furthermore, there is little evidence of beneficial effects of glyphosate against diseases other than rusts, even though some of these pathogens are sensitive to glyphosate in vitro. In these cases, the doses needed for a reduction in crop disease are likely higher than those needed for weed management. Glyphosate has strong effects on plant defenses to plant pathogens in glyphosate-sensitive plants. This is discussed in detail in the Indirect Interactions section. Some crops have been made resistant to the acetolactate synthase (ALS) inhibiting herbicide imazapyr by mutation breeding and to 2,4-D by transgene technology.47 Because some plant pathogens are inhibited by these herbicides (Table 1), there could be some as yet unreported benefits of using these herbicides on these crops. Conversely, these same herbicides, as well as glyphosate and glufosinate, may also reduce disease (either natural infestations or mycoherbicide use) in weeds that have evolved high levels of resistance to these herbicides through target site modifications or other mechanisms. An almost totally unexplored area of research is the effect of herbicides for herbicide-resistant crops on endophytes in those crops. There are herbicide-resistant crops resistant to glyphosate, glufosinate, 2,4-D, and ALS inhibitors, and as mentioned above, there are microbes sensitive to all of these herbicides, probably because the molecular target sites of these herbicides are found in many microorganisms. Stuart et al.59 found changes in endophytic fungi associated with imazapyrresistant sugar cane that was treated with this ALS inhibitor herbicide. The changes were qualitative and quantitative and persisted for at least eight months after herbicide treatment. Unfortunately, the authors did not report any effects on crop growth or yield. Glyphosate applied to GR cotton caused transient effects on rhizobacterial communities.60 Again, the authors did not measure effects on plant health, growth, or yield. Endophytes are believed to be generally beneficial to 7555


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of their own, but they can increase the activity of the pesticide in many ways, such as improving movement of the pesticide into the pest, slowing evaporation of spray droplets, spreading spray droplets after landing, and/or increasing the pesticide half-life. However, these “inert” ingredients can have biological activity on various microbes of importance in agriculture. For example, Morjan et al.75 found the formulation ingredients of a commercial glyphosate product to be very inhibitory to three entomopathogic fungi, whereas glyphosate alone had little or no effect. Formulation ingredients were also fungitoxic with or without glyphosate. Similarly, as mentioned earlier, Grossbard found the effects of glyphosate formulation ingredients to be slightly more fungitoxic than glyphosate.33 As discussed above, reports of the effects of formulated, commercial pesticides on microbes are impossible to interpret unless they are accompanied by parallel studies with technical grade pesticide, the formulation blank, or preferably both. For example, the study by Przemieniecki et al.38 found formulated glyphosate to act additively in the biocontrol activity of a Pseudomonas species against Fusarium plant pathogens. The biocontrol microbe was affected little by the formulated glyphosate. How much of the observed effects on Fusarium were due to the formulation components was impossible to determine. Wyss et al.14 tested the effects of 20 adjuvants and formulation ingredients on the germination of the spores of the mycoherbicide Phomopsis amaranthicola. Seventeen of them were inactive or weakly active, but two (nonooxyol and alkylaryl polyethoxylate/sodium salt of alkylsulfonated alkylate) were very inhibitory, and one (polyalkyleneoxidemodified heptamethyltrisiloxiane) completely inhibited germination. Weaver et al.76 found several spray adjuvants to enhance the activity of the mycoherbicide Myrothecium verrucaria; however, they provided evidence that formulation ingredients of several, but not all, commercial glyphosate products were very toxic to the spores of this fungus. It cannot be assumed that if the active ingredient of a formulated product has no effect on a particular microbe, there will be no effect of the commercially formulated product itself. Also, one cannot assume that a product with a particular trade name will be safe for a particular microbe because it has been proven to be safe at one time or from one source. This is because formulations of a product can differ between regions and can be altered at a later time. There is relatively little information on interactions of formulation ingredients with microbes important in agriculture.

plants, so there could be indirect damaging effects of a herbicide to a herbicide-resistant crop via such indirect effects. However, most evidence indicates that the herbicide has no effects on yield of GR crops that is independent of weed managment.61−63 Insecticides. There is much less recent information available on direct effects of insecticides than on fungicide and herbicide effects on microbes of agricultural interest. Bollen2 reviewed most of what had been done up until 1992. Much of the more recent literature is on the effects of insecticides on insect biocontrol microbes. Exceptions, such as the studies of Zhang et al.64,65 that found that commercially formulated cypermethrin application increased bacterial abundance and changed bacterial community composition of pepper plant leaves, are rare. Leaf bacterial community composition can affect susceptibility to plant pathogen infection. Other nonbiocontrol-related findings since 1992 are that hexaflumuron has direct fungitoxic effects on the plant pathogen Rhizoctonia solani,66 and that formulated pyrethroid insecticides cause morphological changes in colonies of the plant pathogenic bacterium Pseudomonas syringae.67 Formulated chlorpyrifos and lindane were found fungitoxic to several plant pathogens.68 But, the effects could have been due to formulation ingredients. Triazophos significantly reduced soil populations of bacteria and fungi at only 10 mg L−1 a week after application.69 The commercially formulated miticide dicofol completely inhibited the mycelial growth of the biocontrol microbe T. harzianum at 200 mg L−1, and several insecticides (endosulfan, fenpropathrin, propargite, and quinolphos) reduced growth more than 50% at 300 mg L−1.16 Three commercially formulated neonicotinoid insecticides inhibited the in vitro mycelia growth of two entomopathogenic fungi (Beauveria bassiana and Metarhizum anisopliae) used for insect biocontrol.70 However, these insecticides stimulated growth of Paecilomyces sp. Nevertheless, the negative effects were not sufficient to expect significant incompatibility of these products. The pyrethroid insecticide permethrin not only had no effect on the efficacy of two fungal entomopathogens (B. bassiana and M. anisopliae) on the Anopheles gambiae mosquito, but it was claimed to be synergistic with these biocontrol microbes.71 Likewise, synergism was claimed between formulated imidaclorprid and the same two entomopathogenic fungi on larvae of the citrus root weevil (Diaprepes abbreviates).72 A commercial neem (a.i., azadirachtin) insecticide preparation was found to be fungitoxic to several entomopathogenic fungi as well as to some plant pathogens.73 Crude neem products contain numerous compounds other than azadirachtin that could be fungitoxic. In vitro growth of the soil pathogen biocontrol microbe Trichoderma harzianum was inhibited by formulated carbosulfan and quinolphos, as well as a formulation of profenfos plus cypermetrin. 74 Deltamethrin, monocrotophos, and dimethoate did not inhibit growth. In summary, before combining insect biocontrol microbes with chemical insecticides, compatibility should be tested, as some insecticides and/ or their formulation ingredients are toxic to these beneficial microbes. Formulation Ingredients. Commercial pesticides are normally combined with formulation ingredients such as surfactants, stabilizers, spreaders, adjuvants, and other chemicals to enhance their efficacy. These formulation additives are supposed to have little or no pesticidal activity

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INDIRECT INTERACTIONS Most indirect interactions of pesticides with agriculturally important microbes involve direct effects on crops or weeds that translate into indirect effects on microbes associated with plants. The vast majority of documented indirect effects involve herbicides because they have profound effects on plants, even at subtoxic doses.77 Herbicides can have strong effects on plant susceptibility to plant pathogens by either inducing or inhibiting disease resistance mechanisms, depending on the herbicide and its dose. Some fungicides (e.g., benzothiodiazole BTH, probenazole, tiadinil, laminarin, fosetyl-Al, and extract of giant knotweed (Reynourtria sachalinensis)) designed for crops act indirectly by inducing pathogen resistance mechanisms in the plant.78 By similar means, they can affect nontarget microbes, although this is poorly documented compared to indirect effects of herbicides. Some insecticides can influence plant biochemistry,79 but I am 7556


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There is no effect of glyphosate on the shikimate pathway in GR crops, so their shikimate pathway-mediated defenses against microbes are not compromised. Diseases in GR crops treated with glyphosate are generally less severe or the same as for conventional crops, depending on the disease.9,61,62,91,92 Glyphosate has been shown to increase susceptibility of the weed Cassia obtusifolia to the bioherbicide microbe Alternaria cassia,93 glyphosate-susceptible soybeans to the plant pathogens Phytophthora megasperma and Pseudomonas syringae,94−96 alfalfa to the pathogen Verticillium albo atrum,97 and field beans to the pathogen Colletotrichum lindemuthianum.98 In each case, the effect correlated with glyphosate-caused reductions in a shikimate pathway-derived phytoalexin. Similarly, glyphosate reduced lignin production in roots of field beans, thereby making the plants more susceptible to disease caused by Pythium spp..99 Other herbicides, such as bentazon, chlorimuron, diclofop, imaziquin, and oryzalin, have been reported to be compatible with or to increase the severity of diseases caused by plant pathogens.23,100,101 The magnitude of the effect is dependent on the dose of the herbicide. A plant injured by a herbicide may be more susceptible to a pathogen. Certain subtoxic doses of a herbicide can stimulate plant growth and other physiological parameters, a phenomenon called hormesis.102 Hormetic effects could increase resistance of crops and weeds to plant pathogens. Adjuvants and other formulation ingredients can also enhance the virulence of microbial bioherbicides, apparently by alteration of the plant surface and/or creating an appropriate microenvironment for the pathogen. For example, Weaver et al.76 found several formulation ingredients to improve the efficacy of mycoherbicide Myrothecium verrucaria on sicklepod. They speculated that these compounds altered the plant cuticle in a way that was conducive to infection. Some herbicides can enhance plant disease resistance. In particular, herbicides that cause mild oxidative stress can induce plant defenses to plant pathogens. For example, herbicides that inhibit the protoporphyrinogen oxidase (PPO) cause oxidative stress by causing accumulation of the photosensitizing pigment protoporphyrin IX (PPIX).103 Low doses of acifluorfen, a diphenylether PPO inhibitor, induce production of the phytoalexins pisatin, glyceollins, hemigossypol, and phaseolin in peas, soybeans, cotton, and beans, respectively.104 Acifluorfen can also increase production of the phytoalexin camalexin in Arabidopsis thaliana.105 This phenomenon is the reason that at least one PPO inhibitor herbicide, lactofen, has a claim on the label for use to suppress Sclerotinia sclerotiorum (white mold) in soybeans.4 At the recommended application rate, lactofen causes no damage to soybeans but will cause some PPIX production and therefore mild oxidative stress. As the application rate of lactofen increases, the glyceolin level goes up dramatically, with concomitant decreases in lesion diameter caused by white mold infection.106,107 In a more detailed study of the effect of lactofen on synthesis of glyceolin-related compounds, Landini et al.108 found levels of the isoflavones glyceollin, genistein, daidzein, and daidzin as well at the 7-O-glycosyl-6″-Omalonate of daidzein to be increased by lactofen, while levels of 7-O-glycosyl-6″-O-malonate of genistein decreased in soybean cotyledons. The levels of 7-O-glycosyl-6″-O-malonate of daidzein increased as much as 2 μmol per gram of fresh weight, while the maximal increase of the other compounds approached 0.5 μmol per gram of fresh weight. They found

unaware of cases of indirect effects of insecticides on microbes through indirect effects on plants. An indirect effect of herbicides that will not be covered here is the suppression of plant pathogen populations of crops by killing weeds that harbor these pathogens.80,81 Gressel5 reviewed the topic of synergy between herbicides and plant pathogens in detail, and before that review, Hoagland3 reviewed improving the efficacy of microbial bioherbicides with chemicals, mostly herbicides. The most heavily used herbicide in the world, glyphosate, is well-known for reducing some plant defenses to pathogens.9,10,61 It is a specific inhibitor of EPSPS, a key enzyme in the shikimate pathway from which aromatic amino acids (phenylalanine, tyrosine, and tryptophan) are derived.41,42 Lignin, a physical barrier to infection and disease spread, and antimicrobial phytoalexins are derived from aromatic amino acids. Thus, glyphosate reduces production of these plant defenses to pathogens, making the plant more susceptible.9,10 In fact, it has long been known that glyphosate is much more effective in the presence of plant diseases, because, with reduced plant defenses, the disease aides the herbicide in killing the plant.10,82−84 A good example of this is shown in Figure 2. This effect can vary with weed species and whether or

Figure 2. Effects of different doses of glyphosate on the glyphosatesusceptible weed Ambrosia trifida grown in sterile and nonsterile field soil 21 days after glyphosate application. Reproduced with permission from ref 82. Copyright Weed Science Society of America, 2012.

not it is glyphosate-resistant.82 This phenomenon was the basis for the synergism found between microbial bioherbicides and glyphosate.85 Glyphosate has been found to synergize numerous microbial bioherbicides, including Colletotrichum graminicola and Gloeocercospora sorghi on shattercane (Sorghum bicolor);86 Myrothecium verrucaria for kudzu (Pueraria lobata), redvine (Brunnichia ovata), and trumpetcreeper (Campsis radicans) control;87,88 Colletotrichum truncatum for hemp sesbania (Sesbania exaltata);89 and Pyricularia setariae for green foxtail (Setaria viridis).90 However, with glyphosate and at least some of its formulation ingredients being toxic to some plant pathogens (see above), the synergism works best when the weed is sprayed first with glyphosate and later with the pathogen.86 One can speculate that in GR crops treated with glyphosate, the disease levels in surviving weeds in the same fields should be high because of the reduced disease resistance of the weeds. 7557


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(4) Duke, S. O.; Wedge, D. E.; Cerdeira, A. L.; Matallo, M. B. Interactions of synthetic herbicides with plant disease and microbial herbicides. In Novel Biotechnologies for Biocontrol Agent Enhancement and Management; Vurro, M., Gressel, J., Eds.; Springer: Dordrecht, The Netherlands, 2007; pp 277−296. (5) Gressel, J. Herbicides as synergists for mycoherbicides, and vice versa. Weed Sci. 2010, 58, 324−328. (6) Kortekamp, A. Unexpected side effects of herbicides: modulation of plant-pathogen interactions. In Herbicides and Environment; Kortekamp, A., Ed.; Intech: Rijeka, Croatia, 2011; pp 85−104. (7) Sanyal, D.; Shrestha, A. 2008. Direct effect of herbicides on plant pathogens and disease development in various cropping systems. Weed Sci. 2008, 56, 155−160. (8) Martinez, D. A.; Loening, U. R.; Graham, M. C. Impacts of glyphosate-based herbicides on disease resistance and health of crops: a review. Environ. Sci. Eur. 2018, 30, 2. (9) Hammerschmidt, R. How glyphosate affects plant disease development: it is more than enhanced susceptibility. Pest Manage. Sci. 2018, 74, 1054−1065. (10) Lévesque, C. A.; Rahe, J. E. Herbicide interactions with fungal root pathogens, with special reference to glyphosate. Annu. Rev. Phytopathol. 1992, 30, 579−602. (11) Gressel, J. 2018. Microbiome facilitated pest resistance: protential problems and uses. Pest Manage. Sci. 2018, 74, 511−515. (12) du Jardin, P. Plant biostimulants: Definition, concept, main categories and regulation. Sci. Hortic. 2015, 196, 3−14. (13) Calvo, P.; Kloepper, J. W.; Nelson, L. Agricultural uses of plant biostimulants. Plant Soil 2014, 383, 3−41. (14) Wyss, G. S.; Charudattan, R.; Rosskopf, E. N.; Littell, R. C. Effects of selected pesticides and adjuvants on germination and vegetative growth of Phomopsis amaranthicola, a biocontrol agent for Amaranthus spp. Weed Res. 2004, 44, 469−482. (15) Madhavi, G. B.; Bhattiprolu, S. L.; Reddy, V. B. Compatability of biocontrol agent Trichoderma viride with various pesticides. J. Hort Sci. 2011, 6, 71−73. (16) Sarkar, S.; Narayanan, P.; Divakaran, A.; Balamurugan, A.; Premkumar, R. The in vitro effect of certain fungicides, insecticides, and biopesticides on mycelia growth of the biocontrol fungus Trichoderma harzianum. Turk. J. Biol. 2010, 34, 399−403. (17) Elad, Y.; Zimand, G.; Zaqs, Y.; Zuriel, S.; Chet, I. Use of Trichoderma harzianum in combination or alternation with fungicides to control cucumber grey mould (Botrytis cinerea) under commercial greenhouse conditions. Plant Pathol. 1993, 42, 324−332. (18) Papavizas, G. C.; Lewis, J. A. Physiological and biocontrol characteristics of stable mutants of Trichoderma viride resistant to MBC fungicides. Phytopathology 1983, 73, 407−411. (19) Locke, J. C.; Marois, J. J.; Papavizas, G. C. Biological control of Fusarium wilt of greenhouse-grown chrysanthemums. Plant Dis. 1985, 69, 167−169. (20) Loria, R.; Galaini, S.; Roberts, D. W. Survival of inoculum of the entomopathogenic fungus Beauveria bassiana as influenced by fungicides. Environ. Entomol. 1983, 12, 1724−1726. (21) Majchrowicz, I.; Poprawski, T. J. Effects in vitro of nine fungicides on growth of entomopathogenic fungi. Biocontrol Sci. Technol. 1993, 3, 321−336. (22) Lagnaoui, A.; Radcliffe, E. B. Potato fungicides interfere with entomopathogenic fungi impacting population dynamics of green peach aphid. Am. J. Potato Res. 1998, 75, 19−25. (23) Caulder, J. D.; Stowell, L. Synergistic herbicidal compositions comprising Colletotrichum truncatum and chemical herbicides. U.S. Patent 4,775,405A, 1988. (24) Kataria, H. R.; Gisi, U. Interactions of fungicide-herbicide combinations against plant pathogens and weeds. Crop Prot. 1990, 9, 403−409. (25) Charudattan, R. The role of pesticides in altering biocontrol efficacy. In Pesticide Interactions in Crop Production, Beneficial and Deleterious Effects; Altman, J., Ed.; CRC Press: Boca Raton, FL, 1993; pp 421−432.

other PPO inhibitors and rose bengal, a photosensitizer compound that acts like PPIX in causing oxidative damage, to have similar effects, although the magnitude of the effects varied, probably because of different levels of oxidative stress. Sublethal doses of other herbicides can also stimulate production of phytoalexins, thereby affecting plant pathogens. Pretilachlor and butachlor enhance production of the phytoalexins momilactone A and sakurantetin in rice leaves.109 The dinitroaniline herbicides pendimethalin and trifluralin can simulate production of the phytoalexin tomatine in tomato and fungitoxic compounds in cotton, respectively.110,111 The mechanisms of action these inductions were not determined, but these cases might be caused by the hormetic influences of these herbicides.

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SUMMARY Clearly, pesticides and their formulation ingredients can influence microbes associated with crops and weeds in many ways. They can increase or reduce plant disease through direct or indirect mechanisms. Even drift levels of some pesticides can have effects on some microbes. These effects can be critical to the success of microbial biopesticides used against insects, weeds, and plant diseases. Likewise, they can have a range of effects on nonpathogenic microorganisms associated with crops and weeds, such as endophytic, epiphytic, and rhizophere microbial communities, many of which are being found to have greater roles in plant health than previously thought.112−114 Discovery and commercialization of some of these microbes to improve crop production is a growth industry,12,13 yet very little research is being published on the potential impacts that may result from use of these products with pesticides and their formulation ingredients. Future research should do a better job of differentiating between effect of the pesticides and those of their formulation ingredients than much of the previous work. This information could result in formulation changes that favor beneficial pesticide/microbe interactions. For a complete understanding of integrated pest management and the overall cost/benefit of pesticide use, much more information is needed on microbial/pesticide interactions.

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AUTHOR INFORMATION

Corresponding Author

*Tel.: +1 662 915 1036. Fax: +1 662 915 1035. E-mail: [email protected]. ORCID

Stephen O. Duke: 0000-0001-7210-5168 Notes

The author declares no competing financial interest.

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ACKNOWLEDGMENTS Erin Rosskopf provided helpful improvements to the manuscript. REFERENCES

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