Interaction of Chemical Pesticides and Their Formulation Ingredients

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Interaction of Chemical Pesticides and Their Formulation Ingredients with Microbes Associated with Plants and Plant Pests Stephen O. Duke J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.8b02316 • Publication Date (Web): 05 Jul 2018 Downloaded from http://pubs.acs.org on July 7, 2018

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Journal of Agricultural and Food Chemistry

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Interaction of Chemical Pesticides and Their Formulation Ingredients

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with Microbes Associated with Plants and Plant Pests

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Stephen O. Duke†

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†

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Mississippi, 38677, United States of America

USDA-ARS, Natural Products Utilization Research Unit, P. O. Box 1848, University,

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ABSTRACT: Chemical pesticides and their formulation ingredients can have unintended

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effects on microbes associated with plants and plant pests. These effects can be due to direct

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effects on the microbes or to effects on crops or weeds that subsequently affect the microbes.

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In addition to fungicides, some insecticides, herbicides, and formulation compounds are toxic

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to plant pathogenic microbes, as well as to potentially beneficial microbes, such as those that

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infect insect pests. These chemicals, especially herbicides, can also indirectly affect microbes

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through their effects on crops and weeds. For example, glyphosate strongly impairs shikimic

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acid pathway-based plant defenses to microbial diseases in glyphosate-susceptible plants,

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significantly increasing its efficacy as a herbicide. Some herbicides induce plant defenses

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against plant pathogens. For a complete understanding of integrated pest management and

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overall cost/benefit of pesticide use, much more information is needed on microbial/pesticide

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interactions.

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KEYWORDS: biocontrol, fungicide, herbicide, insecticide, microbe, plant pathogen

ACS Paragon Plus Environment


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INTRODUCTION

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Synthetic pesticides have been the most used technology for management of agricultural pests

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for more than 70 years. Despite this heavy reliance, relatively little research has been conducted

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on the influence of these chemicals on non-target microorganisms. Such microbes can be

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beneficial to crop production (e.g., microbial biopesticides, many endophytes, and growth-

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promoting rhizosphere bacteria) or detrimental (e.g., some plant pathogens), and, depending on

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the dose, effects of pesticides can be either beneficial or harmful to these individual microbes

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and can alter the microbial community. Furthermore, the effect of the pesticides on the microbe

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can be either indirect (e.g., through effects on the plant response to the microbe) or direct.

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Formulation ingredients used with many pesticides can also have profound effects on microbes

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and much of the literature is confounded by not separating effects of the pesticide from its

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formulation ingredients. Thus, this general topic is quite complex, with many potential

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interactions, most of which have not been studied in any detail, if at all. Studying these

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interactions can provide a better understanding of integrated pest management and the benefits

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and costs of pesticide use.

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This area of research was of great interest to the late Jack Altman, who edited a book on

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pesticide interactions in agriculture in 1993 (reprinted but not revised in 2017),1 several of the

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chapters of which overlap with this review. For example, there is a chapter on effects of

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pesticides on soil-borne plant pathogens.2 Since this book was published, there have been few

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reviews on topics related to pesticide effects on non-target microbes. Exceptions are the reviews


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of Hoagland,3 Duke et al.,4 and Gressel5 on the interactions of synthetic herbicides with plant

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pathogens and microbial bioherbicides and those of Kortekamp,6 and Sanyal and Shrestha7 on

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side effects and direct effects of herbicides on plant-pathogen interactions. More focused

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reviews are available on the effects of the most used pesticide, glyphosate, on plant pathogens.8-

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topic that this review will not cover. In the last decade, many crop growth-stimulating microbes

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have been patented and developed, and some of these are being used commercially.12,13 The

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market for these products is rapidly increasing.13 Yet, very little is known of the compatibility of

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these products with chemical pesticides. An objective of this review is to provide a critical,

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updated review of chemical pesticide effects on non-target microbes, but not to provide an

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encyclopedic discussion of all of the literature on this topic. A second objective is make readers

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aware of the importance of pesticide/formulation ingredient interactions with non-target

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microbes in agriculture and to point out some of the many unanswered questions in this research

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area.

There is also a recent review on microbiome microbes involvement in pesticide resistance,11 a

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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

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the toxicological literature, is confounded by using only a commercial pesticide which can

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contain formulation ingredients that have their own toxicity profiles (see formulation ingredient

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section below). Even if the formulation ingredients are non-toxic, they can synergize the effects

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of the pesticide on the intended pest as well as other organisms, the reason that they are used.



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Thus, to realistically determine the effect of a pesticide on microbes in the field, formulated

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products as used by farmers must be used. Even when a pure pesticide is used, the researchers

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often add a formulation ingredient of their own to get the pesticide in solution and/or to improve

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uptake. In much of what is discussed below, I try point out whether the authors used technical

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grade pesticides alone or formulated versions of the pesticide. Unfortunately, there are few paper

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that examine the effects of technical grade, unformulated pesticides on microbes or have the

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proper formulation blank controls.

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Fungicides. Since the function of agricultural fungicides is to kill or manage fungal pathogens

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of crops, it is expected that they may have effects on fungal microbes other than crop pathogens.

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For example, Wyss et al.14 found several commercial, formulated fungicides (benomyl, copper

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hydroxide, chlorothalonil, fosetyl-Al, iprodione, maneb, mancozeb, and vinclozolin) used to

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control crop diseases to be highly inhibitory to the fungal weed biological control plant pathogen

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Phomopsis amaranthicola. None of the fungicides that they tested were compatible with P.

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amaranthicola. Although they tested only a few fungicides, it is clear that the simultaneous use

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of fungicides for crop disease control and mycopesticides for pest management is problematic.

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Fungicides can antagonize microbes such as Trichoderma viride, which is used for biological

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control of soil and seed-born plant pathogens. The mycelial growth of this biological control

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agent is strongly inhibited by the commercial fungicides hexaconazole, copper oxychloride, and

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benomyl and was found to be incompatible with the seed treatment with commercial, formulated

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fungicides mancozeb, captan, and carbendazim.15 Similarly, the commercially formulated

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fungicides hexaconazole, propiconazole, triflumizole, tebuconazole, and tridemorph were found


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to completely inhibit mycelial growth of Trichoderma harzianum at 10, 25, 50, 200, and 300 mg

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L-1, respectively.16

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Conversely, some fungicides can act additively or even synergistically with certain

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biocontrol microbes. For example, when treatments of the commercially formulated fungicide

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iprodinone or the microbial biofungicide T. harzianum that each reduced Botrytis cinerea

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infection of cucumber by about 50% were combined, the disease incidence and severity were

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reduced almost entirely.17 Use of fungicide-resistant mutants of biocontrol microbes can make

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the biocontrol organism compatible with fungicides that complement their activity.e.g., 18 An

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example is the use of benomyl-resistant T. viride with benomyl in the control of Fusarium

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oxysporum in Chrysanthemum morifloium.19

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Fungicides inhibit the germination and growth of entomopathogenic fungi that can be used as

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bioinsecticides. For example, two (mancozeb and metiram) of four commercially formulated

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fungicides tested were fungitoxic to the entomopathogenic fungus Beauveria bassiana.20 In a

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more extensive study, nine fungicides (zineb + copper oxychloride, mancozeb, tradimefon,

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copper oxychloride, metalaxyl, sufur, sulfur + nitrothal-isopropyl, and hymexazol) had generally

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toxic effects on eight different entomopathogenic fungi: Beauveria bassiana, Conidiobolus

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coronatus, C. thromboides, Metarhizium anisopliae, Paecilomyces farinosus, P. fumosoroseus,

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Scopulariopsis brevicaulis, and Verticillium lecanii.21 Commercial formulations of benomyl,

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metalaxyl, mancozeb, and captafol were inhibitory to Entomophthora planchoniana in vitro.22

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This fungus infects and sometimes controls green peach aphid. In the field, aphid numbers in

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potatoes were highest when metalaxyl, mancozeb, or captafol were applied, indicating that this

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entomopathogenic fungus was negatively affected by these fungicides.



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Genetically modifying microbes used for biocontrol of weeds or insects to be resistant to

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fungicides used for crop pathogen control could alleviate some of the adverse interactions.e.g., 19

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Although this strategy could be complicated by the number of commercial fungicides with many

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different modes of action used in agriculture. Furthermore, the potential for gene flow of

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fungicide resistance genes to crop pathogens would have to be considered.

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Herbicides. Many herbicides are directly toxic to microbes. Table 1 provides some examples of

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direct inhibitory effects of herbicides on plant pathogens. For example, Wyse et al.14 reported

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strong reductions in sporulation of the plant pathogen Phomopsis amaranthicola by a range of

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herbicides used at their highest approved rate for application (Table 1). An issue with many of

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the papers listed in Table 1 is that most of the studies listed used commercial formulations of

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herbicides (those in reference numbers in bold), making it impossible to determine whether the

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effects shown are due to the herbicide, the formulation ingredients, or both. Pesticide

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formulation ingredients can have profound effects on microbes (see formulation section below).

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In two of the papers listed in Table 1, technical grade herbicide was compared with the

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formulated, commercial herbicide.33, 39 After 24 h of treatment there was little difference in the

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effect of technical grade and formulated trifluralin on germtube growth Fusarium solani.39 But,

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formulated trifluralin inhibited mycelia growth after 12 days at concentrations of non-formulated

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trifluralin that stimulated growth. Early work on glyphosate by Grossbard33 reported that

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although pure glyphosate is toxic to a variety of fungi, the formulation ingredients alone can be

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even more fungitoxic. Determination of the role of formulation ingredients of commercial

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pesticide products in the toxicity to microbes is difficult, because obtaining these ingredients as

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they are formulated in a commercial product is usually not possible, as formulations are often


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trade secretes. However, comparisons can be made of the pure pesticide with the formulated

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product on the basis of the same concentration of the pesticide.e.g., 39

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The most heavily utilized herbicide worldwide, glyphosate,40 is toxic to many bacteria and

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fungi (Table 1).41 Presumably glyphosate acts by the same mode of action on these microbes as

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it does in plants, by inhibition of the shikimate pathway enzyme 5-enolpyruvylshikimate-3-

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phosphate synthase (EPSPS), which is present in plants, fungi, and bacteria .42 However, not all

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microbes are inhibited by glyphosate, and some microbial forms of EPSPS are resistant to

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glyphosate. In fact, the most used transgene to produce glyphosate-resistant (GR) crops is the

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CP4 gene from Agrobacterium sp., which encodes a GR form of EPSPS.43 Some microbes can

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even benefit from glyphosate. For example, the plant growth-promoting rhizobacterium

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Enterobacter cloacae degrades glyphosate and can use it as a phosphorus source.44 Endophytic

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microbes are known to provide some level of herbicide tolerance to some plants by metabolically

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degrading some herbicides taken up by the plant or by inducing higher levels of metabolic

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degradation by the plant.11, 45 However, even though some plants metabolize glyphosate, there is

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no clear evidence that glyphosate degradation is a mechanism of tolerance or resistance to this

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herbicide.46

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There may be beneficial aspects of the fungitoxic effects of some herbicides. For example,

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crops that have been made completely resistant to a particular herbicide47 can directly benefit

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from the use of that herbicide on the resistant crop due to the fungicidal or antibiotic effect of the

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herbicide. Indeed, infection by several plant pathogens has been found to be reduced in both

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glyphosate- and glufosinate-resistant crops sprayed with the herbicides.27, 41, 48-56 An example of

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glyphosate reduction of wheat rust in GR wheat is provided in Figure 1. Some diseases can be



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partially controlled in non-GR plants, with sub-lethal applications of glyphosate. For example,

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leaf area infected by the rust Puccinia psidii in Eucalyptus grandis was reduced by sub-lethal

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glyphosate applications.57 Glyphosate has even been patented for disease control in GR crops.58

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In the case of glyphosate reduction of Asian soybean rust (Phakospora pachyrhizi) in GR

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soybeans, there is good evidence that the effect is through a direct effect on the EPSPS of this

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pathogen.41 The most dramatic direct effects of a herbicide on a plant pathogen in vivo are those

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of glyphosate on rusts. But, the beneficial effects are not as robust as those of commercial

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fungicides, and timing of the glyphosate application for weed management in GR crops is not

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likely to coincide with the best time for application of a fungicide. Furthermore, there is little

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evidence of beneficial effects of glyphosate against diseases other than rusts, even though some

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of these pathogens are sensitive to glyphosate in vitro. In these cases the doses needed for a

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reduction in crop disease are likely higher than those needed for weed management. Glyphosate

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has strong effects on plant defenses to plant pathogens in glyphosate-sensitive plants. This is

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discussed in detail in the Indirect Interactions section.

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Some crops have been made resistant to the acetolactate synthase (ALS) inhibiting herbicide

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imazapyr by mutation breeding and to 2,4-D by transgene technology.47 Because some plant

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pathogens are inhibited by these herbicides (Table 1), there could be some as yet unreported

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benefits of using these herbicides on these crops. Conversely, these same herbicides, as well as

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glyphosate and glufosinate, may also reduce disease (either natural infestations or mycoherbicide

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use) in weeds that have evolved high levels of resistance to these herbicides through target site

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modifications or other mechanisms.


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An almost totally unexplored area of research is the effect of herbicides for herbicide-resistant

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crops on endophytes in those crops. There are herbicide-resistant crops resistant to glyphosate,

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glufosinate, 2,4-D, and ALS inhibitors, and, as mentioned above, there are microbes sensitive to

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all of these herbicides, probably because the molecular target sites of these herbicides are found

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in many microorganisms. Stuart et al.59 found changes in endophytic fungi associated with

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imazapyr-resistant sugarcane that was treated with this ALS inhibitor herbicide. The changes

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were qualitative and quantitative and persisted for at least eight months after herbicide treatment.

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Unfortunately, the authors did not report any effects on crop growth or yield. Glyphosate

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applied to GR cotton caused transient effects on rhizobacterial communities.60 Again, the authors

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did not measure effects on plant health, growth, or yield. Endophytes are believed to be generally

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beneficial to plants, so there could be indirect damaging effects of a herbicide to a herbicide-

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resistant crop via such indirect effects. However, most evidence indicates that the herbicide has

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no effects on yield of GR crops that is independent of weed managment.e.g., 61-63

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Insecticides. There is much less recent information available on direct effects of insecticides

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than on fungicide and herbicide effects on microbes of agricultural interest. Bollen2 reviewed

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most of what had been done up until 1992. Much of the more recent literature is on the effects of

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insecticides on insect biocontrol microbes. Exceptions, such as the studies of Zhang et al.64, 65

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that found that commercially formulated cypermethrin application increased bacterial abundance

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and changed bacterial community composition of pepper plant leaves are rare. Leaf bacterial

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community composition can affect susceptibility to plant pathogen infection. Other non-

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biocontrol-related findings since 1992 are that hexaflumuron has direct fungitoxic effects on the

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plant pathogen Rhizoctonia solani,66 and that formulated pyrethroid insecticides cause



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morphological changes in colonies of the plant pathogenic bacterium Pseudomonas syringae.67

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Formulated chlorpyrifos and lindane were found fungitoxic to several plant pathogens.68 But, the

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effects could have been due to formulation ingredients. Triazophos significantly reduced soil

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populations of bacteria and fungi at only 10 mg L-1 a week after application.69

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The commercially formulated miticide dicofol completely inhibited the mycelial growth of

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the biocontrol microbe T. harzianum at 200 mg L-1, and several insecticides (endosulfan,

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fenpropathrin, propargite, and quinolphos) reduced growth more than 50% at 300 mg

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L-1.16 Three commercially formulated neonicotinoid insecticides inhibited the in vitro mycelia

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growth of two entomopathogenic fungi (Beauveria bassiana and Metarhizum anisopliae) used

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for insect biocontrol.70 However, these insecticides stimulated growth of Paecilomyces sp.

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Nevertheless, the negative effects were not sufficient to expect significant incompatibility of

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these products. The pyrethroid insecticide permethrin not only had no effect on the efficacy of

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two fungal entomopathogens (B. bassiana and M. anisopliae) on the Anopheles gambiae

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mosquito, but it was claimed to be synergistic with these biocontrol microbes.71 Likewise,

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synergism was claimed between formulated imidaclorprid and the same two entomopathogenic

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fungi on larvae of the citrus root weevil (Diaprepes abbreviates).72 A commercial neem (a.i.,

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azadirachtin) insecticide preparation was found to be fungitoxic to several entomopathogenic

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fungi as well as to some plant pathogens,73 Crude neem products contain numerous compounds

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other than azadirachtin that could be fungitoxic. In vitro growth of the soil pathogen biocontrol

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microbe Trichoderma harzianum was inhibited by formulated carbosulfan and quinolphos, as

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well as a formulation of profenfos plus cypermetrin.74 Deltamethrin, monocrotophos, and

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dimethoate did not inhibit growth. In summary, before combining insect biocontrol microbes


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with chemical insecticides, compatibility should be tested, as some insecticides and/or their

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formulation ingredients are toxic to these beneficial microbes.

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Formulation ingredients. Commercial pesticides are normally combined with formulation

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ingredients such as surfactants, stabilizers, spreaders, adjuvants, and other chemicals to enhance

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their efficacy. These formulation additives are supposed to have little or no pesticidal activity of

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their own, but they can increase the activity of the pesticide in many ways, such as improving

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movement of the pesticide into the pest, slowing evaporation of spray droplets, spreading spray

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droplets after landing, and/or increasing the pesticide half life. However, these ‘inert’

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ingredients can have biological activity on various microbes of importance in agriculture. For

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example, Mojan et al.74 found the formulation ingredients of a commercial glyphosate product to

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be very inhibitory to three entomopathogic fungi, whereas glyphosate alone had little or no

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effect. Formulation ingredients were also fungitoxic with or without glyphosate. Similarly, as

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mentioned earlier, Grossbard found the effects of glyphosate formulation ingredients to be

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slightly more fungitoxic than glyphosate.33 As discussed above, reports of the effects of

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formulated, commercial pesticides on microbes are impossible to interpret unless they are

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accompanied by parallel studies with technical grade pesticide, the formulation blank, or

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preferably both. For example, the study by Przemieniecki et al.38 found formulated glyphosate to

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act additively in the biocontrol activity of a Pseudomonas species against Fusarium plant

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pathogens. The biocontrol microbe was affected little by the formulated glyphosate. How much

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of the observed effects on Fusarium were due to the formulation components was impossible to

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determine.



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Wyss et al.14 tested the effects of 20 adjuvants and formulation ingredients on the

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germination of the spores of the mycoherbicide Phomopsis amaranthicola. Seventeen of them

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were inactive or weakly active, but two (nonooxyol and alkylaryl polyethoxylate/sodium salt of

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alkylsulfonated alkylate) were very inhibitory and one (polyalkyleneoxide-modified

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heptamethyltrisiloxiane) completely inhibited germination. Weaver et al.76 found several spray

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adjuvants to enhance the activity of the mycoherbicide Myrothecium verrucaria, however they

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provided evidence that formulation ingredients of several, but not all, commercial glyphosate

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products were very toxic to the spores of this fungus. It cannot be assumed that if the active

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ingredient of a formulated product has no effect on a particular microbe there will be no effect of

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the commercially-formulated product itself. Also, one cannot assume that a product with a

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particular trade name will be safe for a particular microbe because it has been proven to be safe

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at one time or from one source. This is because formulations of a product can differ between

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regions and can be altered at a later time. There is relatively little information on interactions of

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formulation ingredients with microbes important in agriculture.

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INDIRECT INTERACTIONS Most indirect interactions of pesticides with agriculturally important microbes involve direct

253 effects on crops or weeds that translate into indirect effects on microbes associated with plants. 254 The vast majority of documented indirect effects involve herbicides because they have profound 77

255 effects on plants, even at subtoxic doses.

Herbicides can have strong effects on plant

256 susceptibility to plant pathogens by either inducing or inhibiting disease resistance mechanisms, 257 depending on the herbicide and its dose. Some fungicides (e.g., benzothiodiazole BTH,


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258 probenazole, tiadinil, laminarin, fosetyl-Al, and extract of giant knotweed (Reynourtria 259 sachalinensis)) designed for crops act indirectly by inducing pathogen resistance mechanisms in 78

260 the plant.

By similar means, they can affect non-target microbes, although this is poorly

261 documented compared to indirect effects of herbicides. Some insecticides can influence plant 262 biochemistry,79 but I am unaware of cases of indirect effects of insecticides on microbes through 263 indirect effects on plants. An indirect effect of herbicides that will not be covered here is the 264 suppression of plant pathogen populations of crops by killing weeds that harbor these 265 pathogens. 266

e.g., 80, 81

Gressel5 reviewed the topic of synergy between herbicides and plant pathogens in detail,

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and before that review, Hoagland3 reviewed improving the efficacy of microbial bioherbicides

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with chemicals, mostly herbicides.

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The most heavily used herbicide in the world, glyphosate, is well known for reducing some

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plant defenses to pathogens.9, 10, 61 It is a specific inhibitor of EPSPS, a key enzyme in the

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shikimate pathway from which aromatic amino acids (phenylalanine, tyrosine, and tryptophan)

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are derived.41,42 Lignin, a physical barrier to infection and disease spread, and antimicrobial

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phytoalexins are derived from aromatic amino acids. Thus, glyphosate reduces production of

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these plant defenses to pathogens, making the plant more susceptible.9, 10 In fact, it has long

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been known that glyphosate is much more effective in the presence of plant diseases, because,

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with reduced plant defenses, the disease aides the herbicide in killing the plant.10, 82-84 A good

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example of this is shown in Figure 2. This effect can vary with weed species and whether or not

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it is glyphosate-resistant.82 This phenomenon was the basis for the synergism found between

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microbial bioherbicides and glyphosate.85 Glyphosate has been found to synergize numerous



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microbial bioherbicides, including Colletotrichum graminicola and Gloeocercospora sorghi on

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shattercane (Sorghum bicolor);86 Myrothecium verrucaria for kudzu (Pueraria lobata),

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redvine (Brunnichia ovata), and trumpetcreeper (Campsis radicans) control;87,

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for green foxtail (Setaria viridis).90 However, glyphosate and at least some of its formulation

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ingredients being toxic to some plant pathogens (see above), the synergism works best when

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the weed is sprayed first with glyphosate and later with the pathogen.e.g., 86

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Colletotrichum truncatum for hemp sesbania (Sesbania exaltata);89 and Pyricularia setariae

One can speculate that in GR crops treated with glyphosate, the disease levels in surviving

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weeds in the same fields should be high because of the reduced disease resistance of the weeds.

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There is no effect of glyphosate on the shikimate pathway in GR crops, so their shikimate

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pathway-mediated defenses against microbes are not compromised. Diseases in GR crops

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treated with glyphosate are generally less severe or the same as for conventional crops,

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depending on the disease.9, 61, 62, 91, 92

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Glyphosate has been shown to increase susceptibility of the weed Cassia obtusifolia to the

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bioherbicide microbe Alternaria cassia,93 glyphosate-susceptible soybeans to the plant

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pathogens Phytophthora megasperma and Pseudomonas syringae,94-96 alfalfa to the pathogen

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Verticillium albo atrum,97 and field bean to the pathogen Colletotrichum lindemuthianum .98 In

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each case, the effect correlated with glyphosate-caused reductions in a shikimate pathway-

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derived phytoalexin. Similarly, glyphosate reduced lignin production in roots of field beans,

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thereby making the plants more susceptible to disease caused by Pythium spp..99

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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


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pathogens.23, 100, 101 The magnitude of the effect is dependent on the dose of the herbicide. A

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plant injured by a herbicide may be more susceptible to a pathogen. Certain subtoxic doses of a

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herbicide can stimulate plant growth and other physiological parameters, a phenomenon called

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hormesis.102 Hormetic effects could increase resistance of crops and weeds to plant pathogens.

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Adjuvants and other formulation ingredients can also enhance the virulence of microbial

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bioherbicides, apparently by alteration of the plant surface and/or creating an appropriate

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microenvironment for the pathogen. For example, Weaver et al.76 found several formulation

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ingredients to improve the efficacy of mycoherbicide Myrothecium verrucaria on sicklepod.

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They speculated that these compounds altered the plant cuticle in a way that was conducive to

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infection.

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Some herbicides can enhance plant disease resistance. In particular, herbicides that cause

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mild oxidative stress can induce plant defenses to plant pathogens. For example, herbicides that

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inhibit the protoporphyrinogen oxidase (PPO) cause oxidative stress by causing accumulation

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of the photosensitizing pigment protoporphyrin IX (PPIX).103 Low doses of acifluorfen, a

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diphenylether PPO inhibitor, induce production of the phytoalexins pisatin, glyceollins,

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hemigossypol, and phaseolin in peas, soybeans, cotton, and beans, respectively.104 Acifluorfen

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can also increase production of the phytoalexin camalexin in Arabidopsis thaliana.105 This

319

phenomenon is the reason that at least one PPO inhibitor herbicide, lactofen, has a claim on the

320

label for use to suppress Sclerotinia sclerotiorum (white mold) in soybean.4 At the

321

recommended application rate, lactofen causes no damage to soybean, but will cause some

322

PPIX production and therefore mild oxidative stress. As the application rate of lactofen

323

increases, the glyceolin level goes up dramatically, with concomitant decreases in lesion



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diameter caused by white mold infection.106, 107 In a more detailed study of the effect of

325

lactofen on synthesis of glyceolin-related compounds, Landini et al.108 found levels of the

326

isoflavones glyceollin, genistein, daidzein, and daidzin, as well at the the 7-O-glycosyl-6”-O-

327

malonate of daidzein to be increased by lactofen, while levels of 7-O-glycosyl-6”-O-malonate

328

of genistein decreased in soybean cotyledons. The levels of 7-O-glycosyl-6”-O-malonate of

329

daidzein increased as much as 2 µmoles per gram of fresh weight, while the maximal increase

330

of the other compounds approached 0.5 µmoles per gram of fresh weight. They found other

331

PPO inhibitors and rose bengal, a photosensitizer compound that acts like PPIX in causing

332

oxidative damage, to have similar effects, although the magnitude of the effects varied,

333

probably because of different levels of oxidative stress.

334

Sublethal doses of other herbicides can also stimulate production of phytoalexins, thereby

335

affecting plant pathogens. Pretilachlor and butachlor enhance production of the phytoalexins

336

momilactone A and sakurantetin in rice leaves.109 The dinitroaniline herbicides pendimethalin

337

and trifluralin can simulate production of the phytoalexin tomatine in tomato and fungitoxic

338

compounds in cotton, respectively.110, 111 The mechanisms of action these inductions were not

339

determined, but these cases might be caused by the hormetic influences of these herbicides.

340 341 342

SUMMARY Clearly, pesticides and their formulation ingredients can influence microbes associated with

343

crops and weeds in many ways. They can increase or reduce plant disease through direct or

344

indirect mechanisms. Even drift levels of some pesticides can have effects on some microbes.


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These effects can be critical to the success of microbial biopesticides used against insects,

346

weeds, and plant diseases. Likewise, they can have a range of effects on non-pathogenic

347

microorganisms associated with crops and weeds, such as endophytic, epiphytic, and

348

rhizophere microbial communities, many of which are being found to have greater roles in

349

plant health than previously thought.112-114 Discovery and commercialization of some of these

350

microbes to improve crop production is a growth industry,12,13 yet very little research is being

351

published on the potential impacts that may result from use of these products with pesticides

352

and their formulation ingredients. Future research should do a better job of differentiating

353

between effect of the pesticides and those of their formulation ingredients than much of the

354

previous work. This information could result in formulation changes that favor beneficial

355

pesticide/microbe interactions. For a complete understanding of integrated pest management

356

and the overall cost/benefit of pesticide use, much more information is needed on

357

microbial/pesticide interactions.

358 359

AUTHOR INFORMATION

360

Corresponding Author

361

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

362 363

ACKNOWLEDGEMENT

364

Erin Rosskopf provided helpful improvements to the manuscript.

365 366

Notes



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The author declares no competing financial interests.

368

369

370

371 372

REFERENCES (1) Altman, J. (ed.) Pesticide Interactions in Crop Production, Beneficial and Deleterious Effects 1993, CRC Press, Boca Raton, FL, USA, 579 pp.

373

(2) Bollen, G. J. Mechanisms involved in nontarget effects of pesticides on soil-borne

374

pathogens. In Pesticide Interactions in Crop Production, Beneficial and Deleterious Effects.

375

Altman, J., Ed., CRC Press, Boca Raton, FL, USA, 1993, pp. 281-301.

376 377 378

(3) Hoagland, R. E. Chemical interactions with bioherbicides to improve efficacy. Weed Technol. 1996, 10, 651-674. (4) Duke, S. O.; Wedge, D. E.; Cerdeira, A. L.; Matallo, M. B. Interactions of synthetic

379

herbicides with plant disease and microbial herbicides. In Novel Biotechnologies for Biocontrol

380

Agent Enhancement and Management. M. Vurro; Gressel, J., Eds., Springer, Dordrecht, The

381

Netherlands, 2007, pp 277-296.

382 383

(5) Gressel, J. Herbicides as synergists for mycoherbicides, and vice versa. Weed Sci. 2010, 58, 324-328.

384

(6) Kortekamp, A. Unexpected side effects of herbicides: modulation of plant-pathogen

385

interactions. In Herbicides and Environment, Kortekamp, A., Ed., Intech, Rijeka, Croatia,

386

2011, pp. 85-104.

387

(7) Sanyal, D.; Shrestha, A. 2008 . Direct effect of herbicides on plant pathogens and


Page 19 of 37


Duke - 19

388 389

disease development in various cropping systems . 2008, Weed Sci. 56, 155 – 160. (8) Martinez, D. A.; Loening, U. R.; Graham, M. C. Impacts of glyphosate-based herbicides

390

on disease resistance and health of crops: a review. Environ. Sci. Eur. 2018, 30, 2, doi:

391

10.1186/x12302-018-0131-7.

392 393 394 395 396 397 398 399 400 401 402

(9) Hammerschmidt, R. How glyphosate affects plant disease development: it is more than enhanced susceptibility. Pest Manag. Sci. 2018, 74, 1056-1065. (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 Manag. Sci. 2018, 74, 511-515. (12) du Jardin, P. Plant biostimulants: Definition, concept, main categories and regulation. Scientia Horticulturae 2015, 196, 3-14. (13) Calvo, P.; Kloepper, J. W. 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

403

pesticides and adjuvants on germination and vegetative growth of Phomopsis amaranthicola, a

404

biocontrol agent for Amaranthus spp. Weed Res. 2004, 44, 469-482.

405 406 407

(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

408

effect of certain fungicides, insecticides, and biopesticides on mycelia growth of the biocontrol

409

fungus Trichoderma harzianum. Turk. J. Biol. 2010, 34, 399-403.



Page 20 of 37

Duke - 20

410

(17) Elad, Y.; Zimand, G.; Zaqs, Y.; Zuriel, S.; Chet, I. Use of Trichoderma harzianum in

411

combination or alternation with fungicides to control cucumber grey mould (Botrytis cinerea)

412

under commercial greenhouse conditions. Plant Pathol. 1993, 42, 324-332.

413

(18) Papavizas, G. C.; Lewis, J. A. Physiological and biocontrol characteristics of stable

414

mutants of Trichoderma viride resistant to MBC fungicides. Phytopathology 1983, 73, 407-

415

411.

416 417 418

(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

419

fungus Beauveria bassiana as influenced by fungicides. Environ. Entomol. 1983, 12: 1724-

420

1726.

421 422 423 424 425 426 427 428

(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. Amer. J. Potato Res. 1998, 75, 19-25. (23) Caulder, J. D.; Stowell, L. Synergistic herbicidal compositions comprising Colletotrichum truncatum and chemical herbicides. US Patent 4,775,405A (1988). (24) Kataria, H. R.; Gisi, U. Interactions of fungicide-herbicide combinations against plant pathogens and weeds. Crop Protect. 1990, 9, 403-409.

429

(25) Charudattan, R. The role of pesticides in altering biocontrol efficacy. In Pesticide

430

Interactions in Crop Production, Beneficial and Deleterious Effects. Altman, J., Ed., CRC

431

Press, Boca Raton, FL, USA, 1993, pp. 421-432.


Page 21 of 37


Duke - 21

432 433

(26) Tubajika, K. M.; Damann, K. E. Glufosinate-ammonium reduces growth and aflatoxin B1 production by Aspergillus flavus. J. Food Prod. 2002, 65, 165-174.

434

(27) Liu, C.-A.; Zhong, H.; Vargas, J.; Penner, D.; Sticklen, M. Prevention of fungal

435

diseases in transgenic, bialaphos- and glufoinsate-resistant creeping bentgrass (Agrostis

436

palustris). Weed Sci. 1998, 46, 139-146.

437

(28) Wyss, G. S.; Müller-Schärer, H. Effects of selected herbicides on the germination and

438

infection process of Puccinia lagenophora, a biocontrol pathogen of Senecio vulgaris. Biol.

439

Control 2001, 20, 160-166.

440

(29) Tubia-Rahme, H.; Ali-Haimoud, D.-E.; Barrett, G.; Albertini, L. Inhibition of

441

Dreschleria teres scleroid formation in barley straw by application of glyphosate or paraquat.

442

Plant Dis. 1995, 79, 595-598.

443

(30) Yandoc, C. B.; Rosskopf, E. N.; Pitelli, R. L. C. M.; Charudattan, R. Effects of selected

444

pesticides on conidial germination and mycelia growth of Dactylaria higginsii, a potential

445

bioherbicides for purple nutsedge (Cyperus rotundus). Weed Technol. 2006, 20, 255-260.

446

(31) Berner, D. K.; Berggren, G. T.; Snow, J. P. Effect of glyphosate on Calonectria

447 448 449

crotalariae and red crown rot of soybean. Plant Dis. 1991, 75, 809-813. (32) Kawate, S. C.; Kawate, S., Ogg; A. G.; Kraft, J. M. Response of Fusarium solani f. sp. pisi and Pythium ultimum to glyphosate. Weed Sci. 1992, 40, 497-502.

450

(33) Grossbard, E. Effects of glyphosate on the microflora: with reference to the

451

decomposition of treated vegetation and interaction with some plant pathogens. In The

452

Herbicide Glyphosate. Grossbard, E.; Atkinson, D., Eds., Butterworths, London, 1985, pp. 159-

453

185.



Page 22 of 37

Duke - 22

454

(34) Black, B. D.; Russin, J. S.; Griffin, J. S. Herbicide effects of Rhizoctonia solani in vitro

455

and Rhizoctonia foliar blight of soybean (Glycine max). Weed Sci. 1996, 44, 711-716.

456

(35) Santos, A.; Flores, M. Effects of glyphosate on nitrogen fixation of free-living

457 458

heterotrophic bacteria. Lett. Appl. Microbiol. 1995, 20, 349-352. (36) Moorman, T. B.; Becerril, J. M.; Lydon, J.; Duke, S. O. Production of hydroxybenzoic

459

acids by Bradyrhizobium japonicum strains after treatment with glyphosate. J. Agric. Food

460

Chem.1992, 40, 289-293.

461

(37) Kuklinsky-Sobral, J.; Araújo, W. L.; Mendes, R.; Pizzirani-Kleiner, A. A.; Azevedo, J.

462

L. Isolation and characterization of endopyhytic bacteria from soybean (Glycine max) grown in

463

soil treated with glyphosate herbicide. Plant Soil 2005, 273, 91-99.

464

(38) Przemieniecki, S. W.; Kurowski, T. P.; Damszel, M. M.; Karwowska, A.; Adamiak, E.

465

Effect of Roundup 360 SL on survival of Pseusomonas sp. SP0113 strain and effective control

466

of phytopathogens. J. Agric. Sci. Tech. 2017, 19, 1417-1427.

467

(39) Yu, S.-M.; Templeton, G. E.; Wolf, D. C. Trifluralin concentration and the growth of

468

Fusarium solani f. sp. cucurvitae in liquid medium and soil. Soil Biol. Biochem. 1988, 20, 607-

469

612.

470 471

(40) Duke, S. O. The history and current status of glyphosate. Pest Manag. Sci. 2018, 74, 1029-1036.

472

(41) Dill, G. M.; Sammons, D.; Feng, C. C.; Kohn, F.; Kretzmer, K.; Mehrsheikh, A.;

473

Bleeke, M.; Honegger, J. L.; Farmer, D.; Wright, D.; Haupfear, E. A. Glyphosate: discovery,

474

development, applications and properties. In Glyphosate Resistance in Crops and Weeds:

475

History, Development, and Management. Nandula, V.K., Ed., John Wiley & Sons, Inc.,


Page 23 of 37


Duke - 23

476 477 478 479 480 481

Hoboken, NJ, 2010, pp. 1-33. (42) Kishore, G. M.; Shah, D. M. Amino acid biosynthesis inhibitors as herbicides. Annu. Rev. Biochem. 1988, 57, 627-663. (43) Green, J. M. Evolution of glyphosate-resistant crop technology. Weed Sci. 2009, 57: 108-117. (44) Kryuchkova, Y.; Burygin, G. L.; Gogoleva, N. E.; Gogoleve, Y. V.; Chernyshova, M.

482

P.; Makarov, O. E.; Fedorov, E. E.; Turkovskaya, O. V. Isolation and characterization of a

483

glyphosate-degrading rhizospere strain, Enterobacter cloaecae K7. Microbiol. Res. 2014, 169,

484

99-105.

485 486 487 488 489

(45) Tétard-Jones, C.; Edwards, R. Potential roles for microbial endophytes in herbicide tolerance in plants. Pest Manag. Sci. 2016, 72, 203-209. (46) Duke, S. O. 2011. Glyphosate degradation in glyphosate-resistant and -susceptible crops and weeds. J Agric. Food Chem. 2011, 59, 5835-5841. (47) Duke, S. O. Biotechnology: Herbicide-Resistant Crops. In: Encyclopedia of Agriculture

490

and Food Systems, Vol. 2, Van Alfen, N, Editor-in-chief, Elsevier, San Diego, CA, 2014, pp.

491

94-116.

492

(48) Feng, P. C. C.; Baley, G. J.; Clinton, W. P.; Bunkers, G. J.; Alibhai, M. F.; Paulitz, T.

493

C.; Kidwell, K. K. Glyphosate inhibits rust diseases in glyphosate-resistant wheat and soybean.

494

Proc. Natl. Acad. Sci. 2005, 102, 17290-17295.

495 496 497

(49) Feng, P. C. C.; Clark, C.; Andrade, G.; Balbi, M. C.; Caldwell, P. The control of Asian rust by glyphosate in glyphosate-resistant soybeans. Pest Manag. Sci. 2008, 64, 353-359. (50) Anderson, J. A.; Kolmer, J. A. Rust control in glyphosate tolerant wheat following



Page 24 of 37

Duke - 24

498 499

application of the herbicide glyphosate. Plant Dis. 2005, 89, 1136-1142. (51) Pankey, J. H.; Griffin, J. L.; Colyer, P. D.; Schneider, R. W.; Miller, D. K.

500

Preeemergence herbicide and glyphosate effect on seedling disease in glyphosate-resistant

501

cotton. Weed Technol. 2005, 19, 312-318.

502 503 504

(52) Samac, D.; Foster-Hartnett, D. Effect of glyphosate application on foliar diseases of glyphosate-tolerant alfalfa. Plant Dis. 2012, 96, 1104-1110. (53) Wang, Y.; Browning, B. A.; Ruemmele, B. A.; Bridger, A.; Chandlee, J. M.; Kausch,

505

A. P.; Jackson, N. Glufosinate reduces fungal diseases in transgenic glufosinate-resistant

506

bentgrasses (Agrostis spp.). Weed Sci. 2003, 51, 130-137.

507

(54) Uchimiya, H.; Iwata, M.; Nojiri, C.; Samarajeewa, P.K.; Takamatsu, S.; Ooba, S.;

508

Anzai, H.; Christensen, A. H.; Quail, P. H.; Toki, S. Bialaphos treatment of transgenic rice

509

plants expressing the bar gene prevents infection by the sheath leaf blight pathogen

510

(Rhizoctonia solani). Bio/Biotechnol. 1993, 11, 835-836.

511

(55) Pline, W. A.; Lacy, G. H.; Stromberg, V.; Hatzios, K. K. Antibacterial activity of the

512

herbicide glufosinate on Pseudomonas syrinage pathovar Glycinea. Pestic. Biochem. Physiol.

513

2001, 71, 48-55.

514

(56) Wang, Y.; Kausch, A. P. Chandlee, J. M.; Luo, H.; Ruemmele, B. A.; Browning, M.;

515

Jackson, N.; Goldsmith, M. R. Co-transfer and expression of chitinase, glucanase, and bar

516

genes in creeping bentgrass for conferring fungal disease resistance. Plant Sci. 2003, 165, 497-

517

506.

518 519

(57) Tuffi Santos, L. D.; Graça, R. N.; Alfenas, A. C.; Ferreira, F. A.; Melo, C. A.; Machado, M. S. Glyphosate reduces uredinospore development and Puccinia psidii disease


Page 25 of 37


Duke - 25

520 521 522 523

severity on Eucalyptus grandis. Pest Manag. Sci. 2011, 67, 876-880. (58) Baley, G. J.; Kohn, F. C.; Pitkin, J. W.; Rinehart, J.; Taylor, J. H. Method for disease control in MON89788. 2009, US7608761 B1. (59) Stuart, R. M.; Romão, A. S.; Pizzirani-Kleiner, A. A.; Azevedo, J. L.; Araújo, W. L.

524

Culturable endophytic filametous fungi from leaves of transgenic imidazolinone-tolerant

525

sugarcane and its non-transgenic isolines. Arch. Microbiol. 2010, 192, 307-313.

526 527 528

(60) Barriuso, J.; Mellado, R. P. Glyposate affects the rhizobacterial communities in glyphosate-tolerant cotton. Appl.Soil Ecol. 2012, 55, 20-26. (61) Duke, S.O.; Lydon, J.; Koskinen, W. C.; Moorman, T. B.; Chaney, R. L.;

529

Hammerschmidt, R. Glyphosate effects on plant mineral nutrition, crop rhizophere microbiota,

530

and plant disease in glyphosate-resistant crops. J. Agric. Food Chem. 2012, 60, 10375-10397.

531

(62) Williams, M. M.; Bradley, C. A.; Duke, S. O.; Maul, J. E.; Reddy, K. N. Goss’s wilt

532

incidence in sweet corn is independent of transgenic traits and glyphosate. HortScience 2015,

533

50, 1791-1794.

534

(63) Duke, S. O.; Rimando, A. M.; Reddy. K. N.; Cizdziel, J. V.; Bellaloui, N.; Shaw, D. R.;

535

Williams, M. M.; Maul, J. E. Lack of transgene and glyphosate effects on yield and mineral and

536

amino acid content of glyphosate-resistant soybean. Pest Manag. Sci. 2018, 74, 1168–1175.

537

(64) Zhang, B.; Bai, Z.; Hoefel, D.; Tang, L.; Wang, X.; Li, B.; Li, Z.; Zhuang, G. The

538

impacts of cypermethrin pesticide application on the non-target microbial community of the

539

pepper plant phyllosphere. Sci. Total Environ. 2009, 407, 1915-1922.

540 541

(65) Zhang, B.; Zhang, H.; Jin, B.; Tang, L.; Yang, J.; Li, B.; Zhuang, G.; Bai, Z. Effect of cypermethrin insecticide on the microbial community in cucumber phyllosphere. J. Environ.



Page 26 of 37

Duke - 26

542

Sci. 2008, 20, 1356-1362.

543

(66) Zhang, S.; Xiao, P.-Y.; Wen, G.-Y.; Cao, L.-M. Toxicity and mechanism of

544

hexaflumuron on Rhizoctonia solani AG-1 IA. Zhiwu Baohu Xuebao 2007, 34, 87-90.

545

(67) Patyka, V.; Buletsa, N.; Pasichnyk, L.; Zhitkevich, N.; Kalinichenko, A.; Gnatiuk, T.;

546

Butsenko, L. Specifics of pesticides effects on the phytopathogenic bacteria. Ecol. Chem. Eng.

547

2016, 23, 311-331.

548 549 550

(68) Bhonde, S. B.; Deshpande, S. G.; Sharma, R. N. Fungitoxicity of some insecticides. Curr. Sci. 1998, 74, 1039-1040. (69) Lakshimi, K. B.; Madhuri, T.; Indrani, V.; Suvarnalatha, D. P. Effect of triazophos-an

551

organophosphate insecticide on microbial population in paddy soils. Int. J. Cur. Res. Rev. 2015,

552

7, 64-67.

553

(70) Neves, P. M. O. J.; Hirose, E.; Tchujo, P. T.; Miono, A. Compatibility of

554

entomopathogenic fungi with neonicotinoid insecticides. Neotrop. Entomol. 2001, 30, 263-

555

268.

556

(71) Farenhorst, M.; Knols, B. G. J.; Thomas, M. B.; Howard, A. F.; Takken, W.; Rowland,

557

M.; N’Guessan, R. Synergy in efficacy of fungal entomopathogens and permethrin against

558

West African insecticide-resistant Anopheles gambiae mosquitoes. PLOSone 2010, 5 (8),

559

e12081.

560

(72) Quintela, E. D.; McCoy, C. W. Synergistic effect of imidacloprid and two

561

entomopathogenic fungi on the behavior and survival of larvae of Diaprepes abbreviatus

562

(Coleoptera: Curculionidae) in soil. J. Econ. Entomol. 1998, 91, 110-122.

563

(73) Mietkiewski, R.; Ignatowicz, S.; Gorski, R. Comparative effects of BioNEEM and


Page 27 of 37


Duke - 27

564

some synthetic insecticides on the mycelia growth of entomopathogenic fungi in vitro.

565

Pestycydy 1996, (1), 15-24.

566

(74) Singh, V. P.; Srivastava, S.; Shrivastava, S.K.; Singh, H. B. Compatibility of different

567

insecticides with Trichoderma harzianum under in vitro conditions. Plant Pathol. J. 2012, 11,

568

73-76.

569

(75) Morjan, W. E.; Pedigo, L. P.; Lewis, L. C. Fungicidal effects of glyphosate and

570

glyphosate formulations on four species of entomopathogenic fungi. Environ. Entomol. 2002,

571

31, 1206-1212.

572

(76) Weaver, M. A.; Jin, X.; Hoagland, R. E.; Boyette, C. D. Improve bioherbicidal

573

efficacy by Myrothecium verrucaria via spray adjuvants or herbicide mixtures. Biol. Cont.

574

2009. 50, 150-156.

575 576

(77) Duke, S.O. Pesticide dose – A parameter with many implications. Amer. Chem. Soc. Symp. Ser. 2017, 1249:1-13.

577

(78) Fungicide Resistance Action Committee, FRAC Classification on Mode of Action

578

2018, http://www.frac.info/docs/default-source/publications/frac-mode-of-action-poster/frac-

579

moa-poster-2018.pdf?sfvrsn=e5694b9a_3, accessed June 18, 2018.

580 581 582

(79) Lichtenstein, E. P.; Millinton, W. F.; Cowley, G. T. Effect of various insecticides on growth and respiration of plants. J. Agric. Food Chem. 1962, 10, 251-256. (80) Reboud, X.; Eychenne, N.; Delos, M. Folcher, L. Withdrawal of maize protection by

583

herbicides and insecticides increases mycotoxin contamination near maximum thresholds.

584

Agron. Sustain. Devel. 2016, 36, 1-10.

585

(81) Wisler, G. C.; Norris, R. F. Interactions between weeds and cultivated plants as related



Page 28 of 37

Duke - 28

586

to management of plant pathogens. Weed Sci. 2005, 53, 914-917.

587

(82) Schafer, J. R.; Hallett, S. G.; Johnson, W. G. Response of giant ragweed (Ambrosia

588

trifida), horseweed (Conyza canadensis), and common lambsquaters (Chenopodium album)

589

biotypes to glyphosate in the presence of absence of soil microorganisms. Weed Sci. 2012, 60,

590

641-649.

591

(83) Schafer, J. R.; Hallett, S. G.; Johnson, W. G. Soil microbial root colonization of

592

glyphosate-treated giant ragweed (Ambrosia trifida), horseweed (Conyza canadensis), and

593

common lambsquaters (Chenopodium album) biotypes. Weed Sci., 2013, 61, 289-295.

594

(84) Descalzo, R.; Punja, Z. K.; Lévesque, C. A.; Rahe, J. E. Assessment of host specificity

595

among different species of glyphosate synergistic Phythium. Mycol. Res. 1996, 100, 1445-

596

1453.

597

(85) Christy, A. L.; Herbst, K. A.; Kostka, S. J.; Mullen, J. P.; Carlson, P. S. Synergizing

598

weed biocontrol agents with chemical herbicides. Amer. Chem. Soc. Symp. Ser. 1993, 524,

599

87-100.

600

(86) Mitchell, J. K.; Yerkes, C. N.; Racine, S.R.; Lewis, E. H. The interaction of two fungal

601

bioherbicides and a sub-lethal rate of glyphosate for the control of shattercane. Biol. Con.

602

2008, 46, 391-399.

603

(87) Boyette, C. D.; Hoagland, R. E.; Weaver, M. A.; Stetina, K. C. Interaction of the

604

bioherbicides Myrothecium verrucaria and glyphosate for kudzu control. Amer. J. Plant Sci.

605

2014, 5, 3943-3956.

606 607

(88) Boyette, C. D.; Hoagland, R. E.; Weaver, M. A.; Reddy, K. N. Redvine (Brunnichia ovata) and trumpetcreeper (Campsis radicans) controlled under field conditions by a


Page 29 of 37


Duke - 29

608

synergistic interaction of the Bioherbicide Myrothecium verrucaria and glyphosate. Weed Biol.

609

Manag. 2008, 8, 39-45.

610

(89) Boyette, C. D.; Hoagland, R. E.; Weaver, M. A. Interaction of a bioherbicides and

611

glyphosate for controlling hemp sesbania in glyphosate-resistant soybean. Weed Biol. Manag.

612

2008, 8, 18-24.

613 614 615

(90) Peng, G.; Byer, K. N. Interactions of Pyricularia setariae with herbicides for control of green foxtail (Setaria viridis). Weed Technol. 2005, 19, 589-598. (91) Lee, C. D.: Penner, D.; Hammerschmidt, R. Glyphosate and shade effects of

616

glyphosate-resistant soybean defense response to Sclerotinia sclerotiorum. Weed Sci. 2003,

617

51, 294-298.

618

(92) Kandel. Y. R.; Bradley, C. A.; Wise, K. A.; Chilvers, M. I.; Tenuta, A. U., Davis, V.

619

M.et al., Eﬀect of glyphosate application on sudden death syndrome of glyphosate-resistant

620

soybean under field conditions. Plant Dis. 2015, 99, 347–354.

621

(93) Sharon, A.; Amsellem, Z.; Gressel, J. Gyphosate suppression of an elecited response.

622

Increased susceptibility of Cassia obtusifolia to a mycoherbicide. Plant Physiol. 1992, 98,

623

654-659.

624

(94) Keen, N. T.; Holliday, M. J.; Yoshikawa, M. Effects of glyphosate on glyceollin

625

production and the expression of resistance to Phytophthora megasperma f. sp. glycinea in

626

soybean. Phytotpathology 1982, 72, 1467-1470.

627

(95) Ward, E. W. B. Suppression of metalaxyl activity by glyphosate. Evidence that host

628

defence mechanisms contribute to metalaxyl inhibition of Phytophthora megasperma f. sp .

629

glycinea to soybeans. Physiol. Plant Pathol. 1984, 25, 381-386.



Page 30 of 37

Duke - 30

630

(96) Holliday, M. J.; Keen, N. T. The role of phytoalexins in the resistance of soybean

631

leaves to bacteria: Effect of glyphosate on glyceollin accumulation. Phytopathology 1982, 72,

632

1470-1474.

633

(97) Latunde-Dada, A. O.; Lucas, J. A. Involvement of the phytoalexin medicarpin in the

634

differential response of callus lines of lucerne (Medicago sativa) to infection by Verticillium

635

albo atrum. Physiol. Plant Pathol. 1985, 26, 31-42.

636

(98) Johal, G. S.; Rahe, J. E. Glyphosate, hypersensitivity, and phytoalexin accumulation

637

in the incompatible bean anthracnose host-parasite interaction. Physiol. Mol. Plant Pathol.

638

1988, 32, 267-281.

639

(99) Liu, L.; Punja, Z. K.; Rahe, J. E. Altered root exudation and suppression of induced

640

lignification as mechanism or predisposition by glyphosate of been root (Phaseolus vularis L.)

641

to colonization by Phythium spp. Physiol. Mol. Plant Pathol. 1997, 51, 111-127.

642 643

(100) Caulder, J. D.; Stowell, L. Synergistic herbicidal compositions comprising Alternaria cassiae and chemical herbicides. 1988, U.S. Patent 4,776,873.

644

(101) Graham, G. L.; Peng, G.; Bailey, K. L.; Holm, F. A. Interaction of Colletotrichum

645

truncatum with herbicides for control of scentless chamomile (Matricaria perforata) Weed

646

Technol. 2006, 20, 877-884.

647 648 649

(102) Belz, R. G.; Duke, S. O. Herbicides and plant hormesis. Pest Manag. Sci. 2014, 70, 698-707. (103) Dayan, F. E.; Romagni, J. G.; Duke, S. O. Protoporphyrinogen oxidase inhibitors. In

650

Handbook of Pesticide Toxicology 2nd Edition, Vol. 2. Agents., R.I. Kriegr, J. Doull, D.

651

Ecobichon, D. Gammon, E. Hodgson, L. Reiter, and J. Ross, eds., 2001, Academic Press. San


Page 31 of 37


Duke - 31

652 653 654 655

Diego, CA., pp. 1529-1542. (104) Kömives, T.; Casida, J. E. Acifluorfen increases leaf content of phytoalexins and stress metaboloites in several crops. J. Agric. Food Chem. 1983, 31, 751-755. (105) Zhao, J.; Williams, C. C.; Lasta, R. L. Induction of Arabidopsis tryptophan pathway

656

enzymes and camalexin by amino acid starvation, oxidative stress, and an abiotic elicitor.

657

Plant Cell 1998, 10, 359-370.

658 659 660

(106) Dann, E. K.; Diers, B. W.; Hammerschmidt, R. Suppression of Schlerotinia stem rot of soybean by lactofen herbicide treatment. Phytopathology 1999, 89, 598-602. (107) Nelson, K. A.; Renner, K. A.; Hammerschmidt, R. Cultivar and herbicide selection

661

affects soybean development and the incidence of Sclerotinia stem rot. Agron. J. 2002, 94,

662

1270-1281.

663 664

(108) Landini, S.; Graham, M. Y.; Graham, T. L. Lactofen induces isoflavone accumulation and glyceollin elicitation competency in soybean. Phytochemistry 2003, 62, 865-874.

665

(109) Tamogami, S.; Kodam, O.; Hirose, K.; Akatsuka, T. Pretilachlor [2-chloro-N-(2,6-

666

diethyphenyl)-N-(2-propoxyethyl)acetamide]- and butachlor [N-(butoxymethyl)-2-chloro-N-

667

(2,6-diethylphenyl)acetamide]-induced accumulation of phytoalexin in rice (Oryza sativa)

668

plants. J. Agric. Food Chem. 1995, 43, 1695-1697.

669

(110) El-Raheem, A.; El-Shanshoury, R.; El-Sououd, S. M.; Swadalla, O. A., El-Bandy, N.

670

B. Formation of tomatine in tomato plants infected with Streptomyces species and treated with

671

herbicides, correlated with reduction of Pseudomonas solanacearum and Fusarium oxysporum

672

f. sp. lycopersici. Acta Microbiol. Polonica 1995, 44, 255-266.

673

(111) Grinstein, A.; Lisker, N., Katan, J.; Eschel, Y. Herbicide-induced resistance to wilt



Page 32 of 37

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674 675 676 677 678 679 680

diseases. Physiol. Plant Pathol. 1984, 24, 347-356. (112) Busby, P. E.; Ridout, M.; Newcombe, G. Fungal endophytes: modifiers of plant disease. Plant Molec. Biol. 2016, 90, 645-655. (113) Santoyo, S.; Moreno-Hagelsieb, G.; Orozco-Mosqueda, M.C; Glick, B. R. Plant growth-promoting bacterial endophytes. Microbiol. Res. 2016, 183, 92-99. (114) Bacon, C. W.; White, J. F. Functions, mechanisms and regulation of endophytic and epiphytic microbial communities of plants. Symbiosis 2016, 68, 87-98.

681


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682

Table 1. Direct inhibitory effects of formulated and unformulated herbicides on plant pathogens,

683

biological control agents, and plant growth-promoting microorganisms. In the references in

684

bold, the authors used either commercial products which contain ingredients in addition to the

685

herbicide, formulated technical grade herbicide with other ingredients, or the paper did not

686

divulge whether the herbicide was technical grade or a formulated product.

687

Herbicide

Microbe

Reference

688

Atrazine

Trichoderma viride

15

689

Bentazon

Colletotrichum truncatum

23

690

Bromoxynil

Rhizoctonia cerealis

24

Pseudocercosporella herpotrichoides

24

691 692

Clethodim

Phomopsis amaranthicola

14

693

Diclofop-methyl

C. truncatum

23

694

Diquat

Cercospora rodmanii

25

695

Diuron

P. amaranthicola

14

696

Glufosinate

A. flavus

26

698

R. solani

27

699

Sclerotinia homeocarpa

27

Puccinia lagenophora

28

701

Dreschlera teres

29

702

Dactylaria higginsii

30

703

Calonectria crotalariae

31

697

700

Glyphosate



Page 34 of 37

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704

Pythium ultimum

32

705

Fusarium nivale

33

706

F. solani

34

707

R. solani

34

708

T. viride

15

709

Azotobacter vinelandii

35

710

Bradyrhizobium japonicum

36

711

Pseudomonas oxyzihabitans

37

712

Burkholderia gladioli

37

713

F.m culmorum

38

714

F. oxysporum

38

715

Imazapyr

P. amaranthicola

14

716

Linuron

P. amaranthicola

14

717

MCPP

P. amaranthicola

14

718

Oxyfluorfen

D. higginsii

30

719

Paraquat

D. teres

29

720

Pendimethalin

T. viride

15

721

Pyrithioc sodium

T. viride

15

722

Quizalofop ethyl

T. viride

15

723

Sethoxydim

P. amaranthicola

14

724

Trifluralin

F. solani

39

725

2,4-D

P. lagenophora

28

C. rodmani

25

726 727


Page 35 of 37


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728

729 730 731

Figure 1. The effect of glyphosate treatment on severity of wheat leaf rust (Puccinia triticina) in

732

GR wheat. A. No glyphosate at 13 days after innoculation with wheat rust. B. Treated with

733

glyphosate at 0.84 kg ae ha-1 14 days before innoculation and photographed 13 days after

734

innoculation. C. Glyposate treatment 1 day before innoculation. Reproduced with permission

735

from Ref. 48 (National Academy of Science, USA, 2005).

736



Page 36 of 37

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737 738 739

Figure 2. Effects of different doses of glyphosate on the glyphosate-susceptible weed Ambrosia

740

trifida grown in sterile and non-sterile field soil 21 days after glyphosate

741

application Reproduced with permission from Ref. 82 (Weed Science Society of America,

742

2012).


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Interaction of Chemical Pesticides and Their Formulation Ingredients

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