Below are the first 10 and last 10 pages of uncorrected machine-read text (when available) of this chapter, followed by the top 30 algorithmically extracted key phrases from the chapter as a whole.
Intended to provide our own search engines and external engines with highly rich, chapter-representative searchable text on the opening pages of each chapter.
Because it is UNCORRECTED material, please consider the following text as a useful but insufficient proxy for the authoritative book pages.
Do not use for reproduction, copying, pasting, or reading; exclusively for search engines.
OCR for page 100
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
OCR for page 101
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
OCR for page 102
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
OCR for page 103
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
OCR for page 104
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.,
OCR for page 105
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
OCR for page 106
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).
OCR for page 107
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
OCR for page 108
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.
OCR for page 109
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.)
OCR for page 110
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.
Representative terms from entire chapter:
fungicide resistance
