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Pesticide Resistance: Strategies and Tactics for Management. 1986. National Academy Press, Washington, D.C. Plant Pathogens S. G. GEORGOPOULOS Heritable variation for sensitivity to many of the protestant fun- gicides has not been demonstrated in plant pathogenic fungi, and the electiveness of these chemicals has not changed. The remaining Protestants, together with the systemics, can be classified into two groups, depending on whether resistance is controlled by a major gene or a number of interacting genes. Field populations in the former give a bimodal and in the latter a unimodal distribution for sensitivity. Resistance to benzimidazoles, carboxamides, acylalanines, and the protein synthesis inhibitors develops by modification of the sen- sitive site. Changes in membrane transport systems have been shown responsible for resistance to polyoxins and the inhibitors of ergos- terol biosynthesis. Finally, resistance to dihydrostreptomycin and to pyrazophos may result from a change in the ability to metabolize the chemical. INTRODUCTION The main causes of infectious plant diseases are fungi, bacteria, and vi- ruses. At present, effective antiviral agents to control plant viruses in agri- culture are not available. Current chemical control of plant pathogenic bacteria and other prokaryotes is based only on copper and the antibiotics streptomycin and oxytetracycline (Jones, 19821. A large variety of chemicals, however, are available against fungi. My discussion will deal mainly with resistance to fungicides, although resistance in bacteria will be mentioned. (For dis- cussion on preventing and managing resistance, see Dekker in this volume.) 100

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PLANT PATHOGENS 101 Earlier treatments of the subject include those of Georgopoulos (1977; 1982) and Dekker (1985~. Fungi are eukaryotic organisms with well-defined nuclei, each bounded by an envelope that remains intact during mitosis. The vegetative pathogenic phase of most fungi is characterized by haploid nuclei, with the exception of the members of Oomycetes, in which meiosis takes place in the oogonia and the antheridia, so that the organism is diploid throughout the asexual stages of its life cycle (Fincham et al., 19791. In haploid fungi, resistance mutations are subject to immediate selection because they may not be shielded by dominance. Complications arise, however, because many fungi can carry two or more genetically unlike nuclei in a common cytoplasm. In the As- comycetes, this condition, known as heterokaryosis, often permits changes in the proportions of different nuclei in response to selection (Davis, 19661. By contrast the heterothallic Basidiomycetes are characterized by a stable dikaryon, with each cell containing two nuclei. The dikaryon is genetically equivalent to a diploid, but is more flexible. In heterothallic species each cell of the dikaryon contains two nuclei of different mating type. Bacteria as well as mycoplasmal- and rickettsial-like plant pathogens do not contain typical nuclei. The genetic information in a bacterium is contained in the chromosome and in a variable number of plasmids, which carry genes for their own replication in bacterial host cells and for their transmissibility from cell to cell (and often also genes conferring a new phenotype on their hosts). Most of the antibiotic resistance found in bacteria that cause disease in humans and animals is plasmid determined (Datta, 19841. GENETIC CONTROL OF RESISTANCE Fungi are highly variable and adaptable organisms. Plant breeders are particularly conscious of this in their attempts to achieve disease control by developing resistant varieties of crop plants. The ability of fungi to render fungicides ineffective varies greatly, however, depending mainly on the fun- gicide (Georgopoulos, 19841. Appropriate Variability Apparently Unavailable The effectiveness of most protectant agricultural fungicides has remained unchanged after decades of use. Mutational modification of fungal sensitivity to practically any of these fungicides has not been demonstrated in the lab- oratory. The variability required to break down the effectiveness of these chemicals apparently is unavailable to the target fungi. The multisite activity of most protectant fungicides is undoubtedly important but is not always sufficient to explain the inability for resistance to develop. Copper fungicides, for example, have been used for 100 years against

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102 MECHANISMS OF RESISTANCE TO PESTICIDES several of the major fungal pathogens of plants, with no decline in their effectiveness or isolation of resistant mutants of plant pathogenic fungi. Yet mechanisms for copper resistance do exist. In several species of higher plants, tolerance of high concentrations of copper can be achieved by mutations of chromosomal genes (Bradshaw, 19841. In the yeast Saccharomyces cerevis- iae, copper resistance of naturally occurring resistant strains is mediated by a single gene. Sensitive strains cannot grow on media containing 0.3 mM CuS04, while resistant mutants are not inhibited at concentrations up to 1.75 mM. Enhanced resistance levels, up to 12.0 mM CuS04, reflect gene am- plification (Fogel and Welch, 19824. Unlike fungi, bacterial plant pathogens have evolved copper resistance. In Xanthomonas campestris pv. vesicatoria, copper-resistant isolates exist in nature and are not controlled by the amount of Cu + + available from fixed copper fungicides. The genetic determinant of this resistance is located in a conjugative plasmid. A gene for avirulence (inducing a hypersensitive re- sponse) to certain lines of pepper is located on the same plasmid (Stall et al., 19841. Copper fungicides probably have retained the same effectiveness in con- trolling plant pathogenic fungi, because the genes conferring resistance to copper are not available to these fungi. Similarly, no genes substantially affect the sensitivity of fungi to sulfur, dithiocarbamates, phthalimides, qui- nones, chlorothalonil, or any of a few other, less important protectant fun- gicides. Mutants with well-defined resistance to any fungicide of this group have never been obtained. Variations in sensitivity seem to be neither her- itable nor of considerable importance in practice. One-Step Pattern In some of the specifically acting systemic fungicides, one-step major changes in sensitivity of plant pathogenic fungi are obtained with single-gene mutations. One mutation is sufficient to achieve the highest level of resistance possible. If more loci control sensitivity a mutant allele at one locus is epistatic over wild-type alleles at other loci. All sensitive fungi appear to have the genes required for major, one-step changes in sensitivity to fungicides of this group. In nature, sensitive and resistant populations are distinct, and controlling resistant populations by increasing the dose rate of the fungicides or shortening the spray interval is not possible. Such complete loss of ef- fectiveness has not been experienced with fungicides where development of resistance does not follow this one-step pattern. The best known examples of this type of genetic control of sensitivity have been provided by studies on the benzimidazole fungicides, introduced in 1968. At least 50 species of fungi have developed resistance to benzimida- zoles; all attempts to obtain resistance to these fungicides in any sensitive

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PLANT PATHOGENS 103 species have succeeded. In some fungi, for example, Aspergillus nidulans, in addition to the locus for high resistance to benzimidazoles, a few other loci may be involved in smaller decreases of sensitivity. Mutant genes at different loci, however, do not interact, and a stepwise increase of resistance does not occur (Hastie and Georgopoulos, 19711. In other species, for ex- ample, Venturia inaequalis, polymorphism in a single gene causes different resistance levels, and a second locus does not seem to be involved in sen- sitivity to benzimidazole fungicides (Katan et al., 19831. Similar one-step development of resistance in fungi has been recognized with several other systemics and with the aromatic hydrocarbon and dicar- boximide group, most of which do not show systemic activity. Major genes have been identified for carboxamides (Georgopoulos and Ziogas, 1977), kasugamycin (Taga et al., 1979), and aromatic hydrocarbons and dicarbox- imides (Georgopoulos and Panopoulos, 19661. Similar genes are undoubtedly involved in the development of resistance to acylalanines and to polyoxin. Although genetic studies have not demonstrated this yet, the bimodal sen- sitivity distribution found in field populations indicates a one-step change. As with benzimidazoles, resistance can make any of these fungicides inef- fective. In practice this does not always happen, where the mutant gene adversely affects fitness (Georgopoulos, in press). Development of resistance to streptomycin, mediated either by chromosomal or plasmid-borne genes, also appears to follow the same one-step pattern (Schroth et al., 1979; Yano et al., 1979). Multistep Pattern The genetic control of resistance to a third category of fungicides is more complicated. Single gene mutations may have measurable effects on the phenotype, although they are generally small. High level resistance requires positive interaction between mutant genes and is acquired in a multistep fashion, for example, to dodine (Kappas and Georgopoulos, 1970) and to the ergosterol biosynthesis inhibitors (van Tuyl, 1977~. The involvement of several resistance genes and of modifiers maintains a unimodal sensitivity distribution in field populations even after many exposures. Mean sensitivity may gradually decrease, but effectiveness is not completely lost and an increase in fungicide dosage improves disease control (Georgopoulos, in press). The most resistant members of field populations cannot become pre- dominant, because the required accumulation of several resistance genes apparently affects fitness. Similar selection of less sensitive forms and some decrease in effectiveness with time has been noticed with the 2-aminopyrimidine fungicides, fentin, and the phosphorothiolates. Differences in sensitivity to these fungicides, which are found in nature, either have not been studied genetically or cannot

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104 MECHANISMS OF RESISTANCE TO PESTICIDES [it N+C-O-C H3 carbendazim :(CH3 5 1C-N carbox in (B-tubulin ~(succinic dehydrogenase complex) CH3 1 3 ^_N,C-C OOCH3 By< VCH2-OCH3 CH3 o melalaxyl Fit NA poly merase- tempt a [e complex H OOC- 11-40H HO OH kasugamycin ~ ribosome) FIGURE 1 Structural formulas of fungicides to which resistance develops by modification of the sensitive site (indicated in parentheses). be attributed to specific genes (Hollomon, 19811. Variation within popula- tions however, is continuous, and no discrete classes can be distinguished for sensitivity, excluding the possibility of involvement of major genes. Resistance to the above fungicides probably develops in a stepwise manner. RESISTANCE MECHANISMS The few biochemical studies on fungicide resistance indicate that resistance mutations either modify the sensitive site or the membrane transport systems involved in influx and efflux of the fungicidal molecule, or they affect the ability for toxification or detoxification. Examples illustrating the operation of these mechanisms follow. Modification of Sensitive Site The benzimidazole fungicides, such as carbendazim (Figure 1), inhibit mitotic division by preventing tubulin polymerization. In the nonpathogen Aspergillus nidulans, a major gene for resistance to these fungicides codes for p-tubulin, one of the subunits of the tubulin molecule. Mutational mod- ifications of this subunit can be recognized electrophoretically and by the tubulin's ability to bind benzimidazole fungicides (this ability is inversely correlated to resistance) (Davidse, 19821. The genes for carbendazim resis- tance and for carbendazim extra-sensitivity are allelic and are 16 nucleotides apart (van Tuyl, 19771. Tubulin modifications that lower affinities for ben- zimidazole fungicides increase affinity for N-phenyl carbamate compounds, some of which possess antimitotic activity in higher plants (Kato et al.,

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PD4NT PATHOGENS 105 19841. Other modifications, however, may cause resistance to benzimida- zoles and to N-phenyl carbamates. The carboxamide fungicides, such as carboxin (Figure 1), inhibit respi- ration by preventing the transport of electrons from succinate to coenzyme Q. In the corn smut pathogen, Ustilago maydis, two allelic mutations modify the succinic dehydrogenase complex (SDC, succinate-CoQ oxidoreductase), resulting in moderate and high resistance of mitochondrial respiration to carboxin and to most carboxamides (Georgopoulos and Ziogas, 1977~. Some specific structural groups of carboxamides, however, are selectively active against one or the other type of mutated SDC (White and Thorn, 19801. Apparently the gene controlling resistance codes for a component of SDC and, when it mutates, the component's affinity for a given carboxamide increases or decreases, depending on the structure and on the mutation. The binding site of carboxin in animal mitochondria is formed by two small peptides, CII,_3 and CI1_4 (Ramsey et al., 1981~. The acylalanines, such as metalaxyl (Figure 1), are fungicides selectively active against Oomycete fungi. These fungicides inhibit RNA synthesis by interfering with the activity of a nuclear, a-amanitin-insensitive RNA po- lymerase-template complex. Nuclei isolated from a metalaxyl-sensitive strain of the pathogenic Phytophthora megasperma f. sp. medicaginis contained RNA polymerase activity that could be partially inhibited by metalaxyl. By contrast, nuclei isolated from a resistant strain did not contain metalaxyl- sensitive polymerase activity (Davidse, 19841. Resistance, therefore, results from mutational change of one of the RNA polymerases. Many antifungal antibiotics act on protein synthesis (Siegel, 1977), but most are not used to control plant diseases. Cycloheximide binds to the 60-S ribosomal subunit and inhibits the transfer of amino acids from ami- noacyl tRNA to the polypeptide chain, preventing also the movement of ribosomes along the mRNA. In the nonpathogen Neurospora crassa, mod- ifications of protein components of the 60-S subunit create cycloheximide resistance. Single gene-controlled configurational changes of the ribosomes appear to not interfere with normal ribosome functioning. In double mutants, however, where positive interactions result in higher cycloheximide resis- tance, the presence of two mutant ribosomal components disturbs vital func- tions of the ribosomes (Vomvoyanni and Argyrakis, 19791. Kasugamycin (Figure 1) is more important than cycloheximide in plant disease control, particularly against the rice blast pathogen, Pyricularia ory- zae. This antibiotic inhibits protein synthesis in both 80-S and 70-S ribo- somes. Kasugamycin interacts with the 30-S subunit of ribosomes from sensitive strains, but it does not bind to ribosomes from resistant strains of bacteria. Resistance mutations either inactivate an RNA methylase or alter a ribosomal protein (Cundliffe, 19801. In P. oryzae, kasugamycin inhibits protein synthesis, probably by preventing the binding of aminoacyl-tRNA to

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106 MECHANISMS OF RESISTANCE TO PESTICIDES the r~bosome. In a cell-free system with r~bosomes from a resistant mutant, protein synthesis is not inhibited, indicating that mutations modify some component of the r~bosome (Misato and Ko, 19751. Membrane Transport Systems Polyoxins, for example, polyoxin D (Figure 2), block the biosynthesis of chitin, acting as competitive inhibitors for ur~dine diphosphate-N-acetylglu- cosamine in the chitin synthesis reaction. The presence of polyoxin leads to a pronounced accumulation of the normal metabolite. In strains of Alternaria kikuchiana, a pathogen of Japanese pear, polyoxin sensitivity and chitin synthesis inhibition correlate in viva but not in vitro, indicating that the site of action of the antibiotic remains equally sensitive. Polyoxin resistance is associated with a very ineffective system for dipeptide uptake. Sensitive strains are capable of high active uptake of polyoxin in media without di- peptides, but not in media containing glycyl-glycine. In contrast, polyoxin uptake is very low in resistant strains, whether dipeptides are present or absent Whorl et al., 19771. Thus, reduced activity of dipeptide perrnease appears to be responsible for polyoxin resistance. Resistance to ergosterol biosynthesis-inhibiting fungicides such as fenar- imol (Figure 2), however, is not related to fungicide influx, which is passive. In wild-type strains of the nonpathogen Aspergillus nidulans, passive fen- ar~mol influx results in considerable accumulation that induces an efflux activity that is energy-dependent. In strains of the same organism carrying a mutation for fenar~mol resistance, the efflux activity appears to be consti- tutive, preventing initial fungicide accumulation within the cells. When efflux H (COOH HOOC on O=C-N-~ I H2N-$H HE-OH ~ OH OH-CH CH2-O-~-N H2 o polyoxin D chitin biosynthesis - ~C] it, fenarimol ~ ergos tero! biosynthesis ~ FIGURE 2 Structural formulas of fungicides to which resistance develops by modification of membrane transport systems (mechanism of action indicated in parentheses).

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PLANT PATHOGENS R=CH2OH H O~N1'(N~ o 0~ H3C~ N -2 O NHCH3 CH~H OH a inactivated dibydrostreplomycin ~ ribosomes ~ C2H5O-C ~ S H3C=O-~-OC2HS oc2Hs pyrazophos 107 CC13 capran protein thiol s C2H5O~' H3C ~OH toxic metabol ite of pyrazophos ( mechanism no' known) FIGURE 3 Structural formulas of dihydrostreptomycin 3'-phosphate, captan, pyrazophos, and the toxic metabolite 2-hydroxy-5-methyl-6-ethoxycarbonylpyrazolo (1-5-a)-pyr~ dine (information on the mode of action given in parentheses). activity is inhibited by respiration or phosphorylation inhibitors, net fungicide uptake by the mutant strains may be as high as that by the wild type. Mutant genes, therefore, affect the efficiency of fungicide excretion from the my- celium (de Waard and Fuchs, 19821. Detoxification or Nontoxipcation Streptomycin resistance in the fireblight pathogen Erwinia amylovora is believed to result from a chromosomal mutation modifying the ribosome (Schroth et al., 19791. In Pseudomonas lachrymans (the bacterium causing cucumber angular leaf spot), however, resistance to dihydrostreptomycin is plasmid mediated; the antibiotic is detoxified by phosphorylation. From re- sistant isolates, one can obtain a cell-free system that can inactivate the antibiotic in the presence of ATP. The product of the enzymatic inactivation is dihydrostreptomycin 3'-phosphate (Figure 31. The antibiotic can be re- generated by alkaline phosphatase treatment (Yang et al., 1978b). A difference in captan sensitivity (Figure 3) between two isolates of Bo- trytis cinerea could be correlated with the rate of synthesis of reduced glu- tathione in response to the fungicide (Barak and Edgincton, 19841. Increased

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108 MECHANISMS OF RESISTANCE TO PESTICIDES amounts of nonvital soluble thiolic compounds may inactivate fungicides reacting with thiol, thus preventing the damage to cellular protein thiols. Widespread occurrence of this type of resistance to multisite fungicides, however, has not been reported. The systemic fungicide pyrazophos (Figure 3) is toxic to fungi that convert it to 2-hydroxy-5-methyl-6-ethoxycarbonylpyrazolo (1-5-a)-pyrimidine (PP) (Figure 3), which has a much broader fungitoxic spectrum than pyrazophos. In Ustilago maydis, a fungus incapable of this toxification, mutants with resistance to PP could not be obtained. Pyrazophos resistance in Pyricularia oryzae comes from mutational loss of the ability to metabolize the fungicide and to produce the toxic product (de Waard and van Nistelrooy, 1980~. Apparently, resistance develops more easily by loss of ability for toxification than by modification of the siteLs) of action of the toxic product. CONCLUSION Research is greatly needed to increase our understanding of the genetic and biochemical mechanisms of resistance to chemicals used to control plant diseases. Unfortunately methods for such research are either unavailable or time-consuming. At the same time, the study of resistant mutants has con- tr~buted considerably to our understanding of the action of several selective antifungal substances and of some basic cellular processes. Although a better knowledge of the genetics and biochemistry of plant pathogenic microor- ganisms will facilitate future efforts to understand fungicide resistance, sci- entists must not overweigh present difficulties to achieve their goals. REFERENCES Barak, E., and L. V. Edgincton. 1984. Glutathione synthesis in response to captan: A possible mechanism for resistance of Botrytis cinerea to the fungicide. Pestic. Biochem. Physiol. 21:412- 416. Bradshaw, A. D. 1984. Adaptation of plants to soils containing toxic metals a test for conceit. Pp. 4-19 in Origins and Development of Adaptation. Ciba Found. Symp. 102. London: Pitman. Cundliffe, E. 1980. Antibiotics and prokaryotic ribosomes: Action, interaction and resistance. Pp. 555-581 in Ribosomes: Structure, Function, and Genetics, G. Chambliss, G. R. Craven, J. Davies, K. Davis, I. Kahan, and M. Nomura, eds. Baltimore, Md.: University Park Press. Datta, N. 1984. Bacterial resistance to antibiotics. Pp. 204-218 in Origins and Development of Adaptation. Ciba Found. Symp. 102. London: Pitman. Davidse, L. C. 1982. Benzimidazole compounds: Selectivity and resistance. Pp. 60-70 in Fungicide Resistance in Crop Protection, J. Dekker and S. G. Georgopoulos, eds. Wageningen, Netherlands: Centre for Agricultural Publishing and Documentation. Davidse, L. C. 1984. Antifungal activity of acylalanine fungicides and related chloroacetanilide herbicides. Pp. 239-255 in Mode of Action of Antifungal Agents, A. P. J. Trinci and J. F. Ryley, eds. Cambridge: British Mycological Society. Davis, R. H. 1966. Heterokaryosis. Pp. 567-588 in The Fungi: An Advanced Treatise, Vol. 2, G. C. Ainsworth and A. S. Sussman, eds. New York: Academic Press.

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PLANT PATHOGENS 109 Dekker, J. 1985. The development of resistance to fungicides. Prog. Pestic. Biochem. Toxicol. 4: 165-218. de Waard, M. A., and A. Fuchs. 1982. Resistance to ergosterol biosynthesis inhibitors II. Genetic and physiological aspects. Pp. 87-100 in Fungicide Resistance in Crop Protection, J. Dekker and S. G. Georgopoulos, eds. Wageningen, Netherlands: Centre for Agricultural Publishing and Documentation. de Waard, M. A., and J. G. M. van Nistelrooy. 1980. Mechanism of resistance to pyrazophos in Pyricularia oryzae. Neth. J. Plant Pathol. 86:251-258. Fincham, J. R. S., P. R. Day, and A. Radford. 1979. Fungal Genetics, 4th ed. Oxford: Blackwell. Fogel, S., and J. W. Welch. 1982. Tandem gene amplification mediates copper resistance in yeast. Proc. Natl. Acad. Sci. 79:5342-5346. Georgopoulos, S. G. 1977. Development of fungal resistance to fungicides. Pp. 439-495 in Anti- fungal Compounds, Vol. 2, M. R. Siegel and H. D. Sister, eds. New York: Marcel Dekker. Georgopoulos, S. G. 1982. Genetical and biochemical background of fungicide resistance. Pp. 46- 52 in Fungicide Resistance in Crop Protection, J. Dekker and S. G. Georgopoulos, eds. Wag- eningen, Netherlands: Centre for Agricultural Publishing and Documentation. Georgopoulos, S. G. 1984. Adaptation of fungi to fungitoxic compounds. Pp. 190-203 in Origins and Development of Adaptation. Ciba Found. Symp. 102. London: Pitman. Georgopoulos, S. G. In press. The development of fungicide resistance. in Populations of Plant Pathogens: Their Dynamics and Genetics, M. S. Wolfe and C. E. Caten, eds. Oxford: Blackwell. Georgopoulos, S. G., and N. J. Panopoulos. 1966. The relative mutability of the cnb loci in Hypomyces. Can. J. Genet. Cytol. 8:347-349. Georgopoulos, S. G., and B. N. Ziogas. 1977. A new class of carboxin resistant mutants of Ustilago maydis. Neth. J. Plant Pathol. (Suppl. 1) 83:235-242. Hastie, A. C., and S. G. Georgopoulos. 1971. Mutational resistance to fungitoxic benzimidazole derivatives in Aspergillus nidulans. J. Gen. Microbiol. 67:371-374. Hollomon, D. W. 1981. Genetic control of ethirimol resistance in a natural population of Erysiphe graminis f. sp. hordei. Phytopathology 71:536-540. Hori, M., K. Kakiki, and T. Misato. 1977. Antagonistic effect of dipeptides on the uptake of polyoxin A by Alternaria kikuchiana. J. Pestic. Sci. 2: 139-149. Jones, A. L. 1982. Chemical control of phytopathogenic prokaryotes. Pp. 399-413 in Phytopath- ogenic Prokaryotes, Vol. 2, M. S. Mount and G. H. Lacy, eds. New York: Academic Press. Kappas, A., and S. G. Georgopoulos. 1970. Genetic analysis of dodine resistance in Nectria haematococca. Genetics 66:617-622. Katan, T., E. Shabi, and J. D. Gilpatrick. 1983. Genetics of resistance to benomyl in Venturia inaequalis isolates from Israel and New York. Phytopathology 73:600-603. Kato, T., K. Suzuki, J. Takahashi, and K. Kamoshita. 1984. Negatively correlated cross-resistance between benzimidazole fungicides and methyl N-(3,5-dichlorophenyl) carbamate. J. Pestic. Sci. 9:489-495. Misato, T., and K. Ko. 1975. The development of resistance to agricultural antibiotics. Environ- mental Qual. Sa. Suppl. 3:437-440. Ramsay, R. R., B. A. C. Ackrell, C. J. Coles, T. P. Singer, G. A. White, and G. D. Thorn. 1981. Reaction site of carboxanilides and of thenoyltrifluoroacetone in Complex II. Proc. Natl. Acad. Sci. 78:825-828. Schroth, M. N., S. V. Thompson, and W. J. Moller. 1979. Streptomycin resistance in Erwinia amylovora. Phytopathology 69:565-568. Siegel, M. R. 1977. Effect of fungicides on protein synthesis. Pp. 399-438 in Antifungal Compounds, Vol. 2, M. R. Siegel and H. D. Sisler, eds. New York: Marcel Dekker. Stall, R. E., D. C. Loshke, and R. W. Rice. 1984. Coniugational transfer of copper resistance and avirulence to pepper within strains of Xanthomonas campestris pv. vesicatoria. Phytopathology 74:797. (Abstr.)

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110 MECHANISMS OF RESISTANCE TO PESTICIDES Taga, M., H. Nakagawa, M. Tsuda, and A. Ueyama. 1979. Identification of three different loci controlling kasugamycin resistance in Pyricularia oryzoe. Phytopathology 69:463-466. van Tuyl, J. M. 1977. Genetics of fungal resistance to systemic fungicides. Meded. Landbouwho- gesch. Wageningen Ser. 77-2. Vomvoyanni, V. E., and M. P. Argyrakis. 1979. Pleiotropic effects of ribosomal mutations for cycloheximide resistance in a double-resistant homocaryon of Neurospora crassa. J. Bacteriol. 139:620-624. White, G. A., and G. D. Thorn. 1980. Thiophene carboxamide fungicides: Structure activity re- lationships with the succinate dehydrogenase complex from wild-type and carboxin-resistant mu- tant strains of Ustilago maydis. Pestic. Biochem. Physiol. 14:26-40. Yano, H., H. Fujii, and H. Mukoo. 1978a. Drug-resistance of cucumber angular leaf spot bacterium, Pseudomonas lachrymans (Smith et Bryan) Carsner. Ann. Phytopathol. Soc. Jpn. 44:334-336. Yano, H., H. Fujii, H. Mukoo, M. Shimura, T. Watanabe, and Y. Sekizawa. 1978b. On the enzymic inactivation of dihydrostreptomycin by Pseudomonas lachrymans, cucumber angular leaf spot bacterium: Isolation and structural resolution of the inactivated product. Ann. Phytopathol. Soc. Jpn. 44:413-419.