Annual Reviews
www.annualreviews.org/aronline
Annu.R ev. P hytopathol.1993.31:127-50
Copyright©1993by AnnualReviewsInc. All rights reserved
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
FUNGAL VEGETATIVE
COMPATIBILITY
John F. Leslie
Department
of Plant Pathology,Throckmorton
Hall, KansasState University,
Manhattan, Kansas66506-5502
KEYWORDS:ascomycetes,
fungal genetics,
heterokar~ns, parasexual cycle
INTRODUCTION
Heterokaryonformation betweendifferent fungal individuals is an important
componentof manyfungal life cycles and mayserve as the first step in the
parasexual cycle and the transmission of hypovirulent factors such as dsRNAs.
Heterokaryosis also is a means by which normally haploid fungi mayenjoy
the benefits of functional diploidy, such as complementation
or heterosis. In
plant pathogenic fungi, the entity that emergesfollowing heterokaryosis may
differ from its constituents in aggressiveness or host range; someof these
aspects have been reviewedin previous volumesin this series (9, 28, 45, 62,
72, 112, 114, 117, 143, 154, 158, 160). In most heterothallic fungi, the
formation of a heterokaryonbetweentwo genetically different haploid strains
is an essential part of the life cycle. Suchheterokaryonsmaybe quite stable
and persist vegetatively for an indefinite period of time or maylast only long
enoughfor the componenthaploid nuclei to fuse and then immediatelyundergo
meiosis.
In manyfungi, sexual and vegetative heterokaryons are quite distinct from
one another. Strains capable of forminga successful sexual heterokaryonmay
be unable to form a successful vegetative heterokaryonand vice versa. Strains
that are capable of forming these types of heterokaryons are referred to as
"sexually" or "vegetatively" compatible, respectively. Strains that are vegetatively compatible with one another are frequently described as membersof
the same vegetative compatibility group, or VCG.Sexual compatibility is
usually governed by one or more mating-type loci that mayhave two or more
alleles (58, 62). Vegetative compatibility maybe governedby the mating-type
loci in somefungi, e.g. manybasidiomycetes, but there also are examplesin
which a separate set of genes controls the formation and stability of these
vegetative heterokaryons.
127
0066-4286/93/0901-0127$02.00
Annual Reviews
www.annualreviews.org/aronline
128
LESLIE
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
Genetic systems governing vegetative
compatibility
have been reported in
many different
fungi (for examples, see Table 1). The formal interactions
these systems vary greatly.
Conceptually,
the simplest systems are those in
which strains that are identical at a particular set of loci are capable of forming
a stable heterokaryon, while those that differ at any of these loci are incapable
of forming a vegetatively
stable heterokaryon.
This type of interaction
is
usually referred to as allelic compatibility.
Nonallelic interactions
also may
occur in which alleles at one locus interact
with alleles at a second locus to
block the formation of a stable heterokaryon. One of the best-studied
examples
of nonallelic
interaction
occurs in Podospora anserina (Table 1). An even
more complex nonallelic
interaction
has been described
in Heterobasidion
annosum by Chase & Ullrich (26, 27). The molecular bases for all of these
interactions
are all but unknown, and are probably quite varied.
To the extent that vic (for vegetative
incompatibility)
genes represent
means for discriminating
self from nonself,
they represent
a recognition
mechanism that is carried
throughout
much of the biological
world, e.g.
Thompson & Kirch (153). Fungi have served as excellent
model systems for
the study of many phenomena in higher organisms (122), but it is not evident
whether fungal recognition
systems resemble those of other eukaryotes.
Table 1 Literature citations to somefungal systems in which vegetative
compatibility has been reported
Organism
Citation(s)
Aspergillus spp.
Ceratocystis spp.
Cochliobolus heterostrophus
Colletotrichum spp.
Cryphonectria parasitica
Cryptostroma spp.
Diaporthe phaseolorum
Fusariurn spp.
7, 22, 24, 38, 40-43, 77, 78, 116
14, 52
96
15
3-5, 92, 108, 144
155
133
2, 10, 11, 29, 31, 33, 39, 46, 53, 55, 64,
65, 76, 80-82, 100, 101, 130, 137139, 141, 142, 149
69, 145
163
1
134
159
44, 49, 59-62, 71, 98, 106, 107, 120,
121, 125, 127, 128, 161, 162
24
8, 56, 93, 156
89, 90
111
151
79, 113, 135, 140, 157
Hypoxylon spp.
Leptographiurn wagneri
Leucostoma persoonii
Leucocytospora kunzei
Morchella esculenta
Neurospora spp.
Penicillium spp.
Podospora anserina
Sclerotinia sclerotiorum
Septoria nodorum
Trichoderma spp.
Verticillium spp.
Annual Reviews
www.annualreviews.org/aronline
FUNGALVEGETATIVECOMPATIBILITY
129
Myobjective in this review is to describe our current understandingof the
allelic vegetative compatibility reactions in four different ascomycetefungi,
Aspergillus, Cryphonectria, Fusarium, and Neurospora. These fungi have
served as modelsfor the basic study of the genetic mechanismscontrolling
vegetative compatibility, and they can be used to illustrate someof the ways
vegetative compatibility maybe used in the study of fungal populations.
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
GENERAL
PROPERTIES
Vegetativecompatibilitysystemsgenerally act to restrict the transfer of nuclear
and cytoplasmic elements during growth. In each of these four fungi, hyphal
fusion usually occurs normally, even betweenstrains that carry vegetatively
incompatible nuclei. However,after an incompatible fusion occurs, a killing
reaction follows that leads to death of the heterokaryotic cell. The incompatibility systems in these fungi are all allelic in nature, and field populations
usually are quite polymorphic. Throughoutthis review I use the symbol vic
to refer to loci that governvegetative compatibility. 1 use the term vegetative
compatibility group(VCG)to refer to strains that can form a stable vegetative
heterokaryon, implying identity of alleles at every vic locus. This is the
terminology that is usually employedwith Fusariumspp., but is somewhat
different from that used with some other fungi. I have noted equivalences
where appropriate.
Most studies of vegetative compatibility have focused on the fusion
(anastomosis) of hyphaerather than the fusion of protoplasts or spheroplasts.
The workdone with fused protoplasts is quite interesting, however,since the
heterokaryons formedfollowing protoplast fusion appear to be significantly
different from those formedfollowinghyphal anastomosis(2, 151). The killing
of heterokaryotic cells composedof incompatible nuclei that occurs following
hyphal anastomosis may not occur in some instances following protoplast
fusion (40, 57, 105, 118). These data may be interpreted to mean that
cell-membrane components or materials in the space between the cell
membraneand the cell wall are responsible for at least someof the killing
reactions. Suchan interpretation could also be used to explain the survival of
heterozygous partial diploids in Neurospora(see below) that carry both vic
alleles at the samelocus.
Neurospora
Vegetativecompatibility has beenstudied most intensively in the heterothallic
Neurosporacrassa. Most of this work has focused on the number, location,
and phenomenologyof the different loci and alleles. The loci governing
vegetative compatibility are usually termedhet loci. In Neurosporavegetative
compatibility has been studied by examiningheterokaryons for prototrophic
growth (59) and barrage formation (67, 68), by microscopic examination
heterokaryoticcells (61), and throughthe formationof partially disomicstrains
Annual Reviews
www.annualreviews.org/aronline
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
130
LESLIE
that are heterozygous at one or morevic loci (106, 120). Ten different vic
loci have been identified to date and these have been mappedto five of the
seven chromosomes;
others are presumedto exist but have yet to be identified.
Preliminary evidence is available for multiple alleles at two of these loci,
het-C (D. D. Perkins, personal communication)and her-8 (98). All of the vic
loci in Neurosporahave been identified using the partial disomic method(see
below), but only somehave been tested for their ability to block heterokaryon
formation per se. Heterozygosityat the het-i locus (128) does not lead to the
cytoplasmickilling reaction, but can lead to the loss of one of the components
through unbalanced growthor nuclear division. In a limited study of strains
from three sites in Louisiana, Mylyk(107) showedthat no two of fifteen
strains were identical to one another and that heteromorphism
for at least five
genes occurred amongthe five isolates examinedfrom one site.
The mating-type locus can act as a vegetative compatibility locus in N.
crassa, but the incompatibility reaction associated with mating type can be
suppressedby a recessive allele at the unlinkedtol locus (109). The tol locus
is not knownto suppress the heterozygous reaction at either het-C or her-E,
but whether it affects other vic genes is unknown(121). Differences
vegetative compatibility loci mayenhance sexual fertility (49). In the
pseudohomothallic N. tetrasperma, which normally grows as a heterokaryon
containing nuclei of opposite matingtype, a recessive allele is present at the
tol locus (73).
The molecular mechanism(s) by which any of these loci function is not
known.Wilsonet al (I 62) have shownthrough microinjection studies that the
agent responsible for the killing reaction is labile to proteases but not to RNAse
or DNAse.These studies were extended by Williams & Wilson (161) who
found evidence for the involvement of an RNA-associatedcomponentto the
killing reaction, and showedthat the molecular weight of the active complex
was approximately 200,000 daltons. They also suggested, based on killing
kinetics and the geometryof the microinjection process, that saturation of a
receptor is a prerequisite for killing and that the cell membranes
(and more
specifically damageto them) was involvedin the killing reaction. Considerable
effort is now being devoted to the cloning of the genes that govern the
vegetative compatibility response in N. crassa, and manyof these questions
should be more easily approached once that has been accomplished.
Aspergillus
Numerous Aspergillus species have been examined for the presence of
vegetative compatibility. Since formation of a stable vegetative diploid is a
prerequisite for the parasexual cycle, vegetative compatibility has long been
an importanttopic relative to this genus. Theworkin Aspergillus is relatively
well-balanced betweenfundamentalstudies of the vic loci and implications of
the workfor population studies. At least eight vic loci (termed het loci) are
Annual Reviews
www.annualreviews.org/aronline
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
FUNGALVEGETATIVE
COMPATIBILITY
131
knownin the homothallic A. nidulans (38), and multiple alleles are known
be present at at least two loci (37). Vegetative compatibility maybe scored
directly or through the use of a chromosome
assay systemthat uses protoplast
fusion to form an appropriate heterozygous diploid and then uses pairs of
haploid segregants to mapthe heterozygous vic loci (4143). Studies of VCGs
(termed h-c groups) has revealed that these groups are widely dispersed in the
United Kingdom(38), and that genetic diversity is greater between groups
than within groups (17-19). Antibiotic production mayalso be restricted
particular VCGs(38).
Cryphonectria
Vegetative compatibility workin this genus has been limited to Cryphonectria
parasitica. Interest has focused on the role of vegetative compatibility in the
transfer of double-stranded RNA
(dsRNA)from one strain to another. Strains
carrying this dsRNAare hypovirulent and do not cause severe chestnut blight
(5, 92, 112). Natural spread of this dsRNA
could lead to sustainable biological
control of this disease. At least 5-7 loci (termedv-c loci) havebeenidentified
in C. parasitica and strains that differ only at a single locus are known(4).
Mutantsat vic loci have been recovered followingmutagenesiswith ultraviolet
light in a laboratory context (144).
Vegetative compatibility in C. parasitica is usually scored by barrage
formation between strains that are not compatible with one another (3).
electron microscopestudies, fusion cells betweenvegetatively incompatible
hyphae have been shownto degenerate in a mannersimilar to that observed
in N. crassa (108). DsRNAs
can be transferred between strains that are
different VCGs(5, 92). As the numberof heterozygousvic loci increases the
efficiency of transfer of the dsRNAdecreases. The dsRNAparticles are
transferred moreefficiently than are mitochondria(63).
Fusarium
Heterokaryosis, barrages, and perhaps complementation or other types of
mycelial interactions have been recognizedin the genus Fusariumfor at least
100 years (104, 115, 152). With the work of Puhalla (139) and Puhalla
Spieth (141-142), these observations of hyphal interactions were mergedwith
genetic theory developed for modelgenera Aspergillus and Neurospora.This
merger has been used primarily in population studies of the imperfect F.
oxysporum(see below) in an attempt to develop new diagnostic techniques.
A few basic studies have been done, however,and there is evidence for genetic
segregation of vic loci in both the heterothallic F. moniliforme(perfect stage
Gibberella fujikuroi) (141) and the homothallicF. graminearum
(perfect stage
Gibberella zeae) (12). In F. moniliformeone vic locus (vicl) has been mapped,
and there are strains that are knownto differ at only this locus. Basedon the
segregation of different VCGtypes from a cross, at least ten vic loci are
Annual Reviews
www.annualreviews.org/aronline
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
132
LESLIE
expected in F. moniliforme. Mutantswith a novel phenotype,i.e. inability to
fuse properly to form a heterokaryon, have been described and termed
heterokaryonself-incompatible (32, 74). Researchers characterizing Fusarium
populations with VCGsshould be aware of the existence of these mutant
strains and the difficulties that they could pose for the interpretation of
population data (see belowfor moredetail on this mutantclass). In general,
population studies using VCGshave been quite extensive in this genus, but
muchremains to be done to understand the basic biology of the vic loci that
are responsible for the VCGphenotypes.
TECHNIQUES
The methodsused to identify vic loci are important. Three basic types of
"techniques have been used: direct assessment of heterokaryon formation
(usually by complementationof recessive auxotrophic or pigmentation markers); direct assessment of inability to form a heterokaryon (usually through
barrage formation); and, finally, throughgrowthcharacteristics of strains that
are partial diploids and are heterozygousat one or more vic loci. I discuss
each of these basic techniques, consider a complicating phenomenon
(heterokaryonself-incompatibility) that can lead to misdiagnosisof vegetative
compatibility, and describe potential mutagenesisand cloning strategies for
these loci.
Direct Heterokaryon Formation
Direct tests of heterokaryonformation usually involve the establishment of a
stable prototrophic heterokaryonunder conditions in whichneither of the two
auxotrophiccomponents
could survive. Thesetests are a direct test of vegetative
(heterokaryon) compatibility. In principle, any genetic markers whosedefect
can be remedied by complementation can be used to detect heterokaryon
formation. In practice, auxotrophor pigmentationmarkersare usually preferred
because of the ease of distinguishing the heterokaryotic colony from its
components. The mutants used may originate from any source. If forcing
markersmust be introduced by a typical mutant hunt procedure, then the labor
required will preclude any extensive screening of populations, and simpler
methodsmust be applied. The introduction of nitrate nonutilizing (nit) mutants
has provided such a solution. Whena heterokaryon is forced between
auxotrophicstrains in the sameVCG,then a prototrophic heterokaryonresults.
If the strains are in different VCGs,then no prototrophic growthoccurs.
Puhalla (139, 142) adapted to Fusariuma technique developed by Cove
(35, 36) for Aspergillus. Spontaneous nit mutants can be recovered as
chlorate-resistant sectors at a sufficiently high frequencythat they can be used
for population studies in Fusariurnand Aspergillus. In Fusariutn the technique
has been well-characterized (11, 31, 32, 46, 50, 84, 85, 87, 99). Many
the tests can be done on 24-well (86) or even 96-well (C. Campbell&J.
Annual Reviews
www.annualreviews.org/aronline
FUNGALVEGETATIVECOMPATIBILITY
133
Leslie, unpublished)microtiter plates, and tests of hundredsto thousands of
isolates for diagnostic and/or tracking purposes are nowfeasible (7, 83).
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
Barrage
The barrage phenomenonis conceptually the opposite of a prototrophic
vegetatively compatible heterokaryon. Barrages occur between vegetatively
incompatible strains in manyfungi, including Podospora(56), Neurospora
(68), and Cryphonectria, but the ease with which they can be identified
depends upon environmental conditions. A barrage mayresult when hyphae
of incompatible strains grow into each other and interact in an antagonistic
manner.The barrage region occurs wherethe two colonies contact one another
and may be sharply delimited. The barrage phenomenonrequires hyphal
fusion, and in the barrage region numerouslethal hyphal fusions will occur.
The barrage phenomenonforms the main basis for scoring vegetative
compatibility and assigning strains to VCGsin C. parasitica (3). In
parasitica, whenstrains in different VCGs
are paired on a plate they will grow
until they meet and then form a barrage. The barrage consists of a central
region that contains dead or dying cells of the type described by Newhouse
& MacDonald(108). A dark layer of pigment mayalso be deposited in this
region. Oneither side of this central region the myceliaforma higher, thicker
layer of growth that maybe accompaniedby the formation of perithecia.
Vegetatively compatible strains do not interact in this manner, but instead
they simply grow into each other without altering their morphology.
Partial
Diploids
Partial chromosome
duplications in Neurosporaare structural duplications of
segmentsof the fungal genome.If the duplicated region carries a vic locus,
then it is possible to construct strains that are heterozygousfor particular loci.
Unlike heterokaryons, these heterozygous partial diploids enclose both vic
alleles in the samenucleus and ensure that a 1:1 ratio is maintained.The major
advantageoffered by this technique is that it allows one or a few vic loci to
be studied without havingto construct strains that differ at only one vic locus.
If these duplications breakdowninto a euploidconfiguration, then it is possible
to obtain strains that differ only in the duplicated region. This approachhas
been used to obtain strains that differ only at het-5 or het-8 (107).
In Neurospora segmental chromosomeduplications can be generated in
crosses between certain types of chromosomerearrangements and normal
sequence strains (123). Duplication strains that are heterozygous for
contained vic gene are phenotypically quite aberrant with abnormalgrowth,
pigmentation, and morphology(98,106, 110, 120). The pigmentation reaction
may be intensified by supplementing the mediumwith phenylalanine and
tyrosine (119). Amongthe vic loci in N. crassa, all but het-i have been
examinedusing this technique. The strength of the incompatibility reaction
Annual Reviews
www.annualreviews.org/aronline
134
LESLIE
amongthe progeny can vary with the strains used in the cross (98, 106).
Whetherthis difference in reaction intensity is attributable to the individual
alleles at the locus or to the genetic backgroundof the individuals involved
in the cross has not been determined. An updated list of strains carrying
rearrangementsthat can be used to identify the alleles at different vic loci in
N. crassa has recently been published (124).
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
Mutagenesis
and Cloning Strategies
Mutagenesis and cloning strategies carry with them unspoken assumptions
regarding the modeof action of vic genes. These assumptionswill affect the
methodsthat are chosen to select for mutants or transformants. For example,
if alleles are not nearly isosequential, then it probablywill not be possible to
convert one discriminatory allele into another. Similarly, the effect of null
mutations are generally unknown: should such mutants be expected to be
compatible or incompatible with all other strains? Finally, are vic genes
essential? If they encode an essential componentof the cell membrane,for
example, then it maynot be possible to completely inactivate these genes
unless conditional mutants are made. The cloning of the S/s alleles in P.
anserina suggests that the alleles at at least someof the vic loci are nearly
isosequential and that neutral alleles exist that are compatiblewith both of the
discriminatoryalleles (156).
Mutantsat vic loci have been successfully selected in C. parasitica and F.
oxysporum. In both cases some of the findings were unexpccted and need to
be repeated and confirmed. In C. parasitica, Rizwana& Powell (144) were
able to induce changes from one VCGtype to another using ultraviolet light;
the mutants they recovered were unstable, and continued to change their VCG
type as they grew. Rizwana & Powell (144) suggested that this observed
instability could form the basis for muchof the variability observed with
respect to VCG
in field populations of C. parasitica. In F. oxysporumf. sp.
lycopersici, Kroon & Elgersma (91) obtained simultaneous change of both
pathogenic race and VCG.They suggested that one (or perhaps more) of the
vic loci might be involvedin the recognition of the host plant, and that changes
in vic genotypecould also result in changesin pathogenicity. Elias &Schneider
(53) found that this same pathogen group could be subdivided into numerous
VCGs, and that members of the same VCGcould belong to different
pathogenic races. In this context, the findings of Kroon&Elgersmaneed to
be repeated and carefully checked to control unrelated problems, such as
accidental cross-contamination, before the hypothesis that vic loci themselves
can affect pathogenicity is accepted.
To date, the cloning of vic genes from any of these fungi has not been
reported, but one vic gene (S/s) in the allelic series in P. anserina has been
cloned (156). Several groups are attempting to clone vic loci in other fungi,
and future reviews of this area will undoubtedly contain a great deal of
Annual Reviews
www.annualreviews.org/aronline
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
FUNGALVEGETATIVECOMPATIBILITY
135
information on this aspect of vic gene biology. Direct selection for
transformants is possible in systems where barrages can be observed if a
successful transformation event results in a changefrom one VCG
to another.
Transformants maythen be identified by the barrage they form with their
neighbors on the transformation plate. A more difficult problem maybe to
identify transformants if they are heterozygous for a vic locus and are not
growingas well as their counterparts with only a single copy of a vic allele.
To the extent that these strains resemblethe partial diploids described above,
they will be at a selective disadvantage on the transformation plates. With
single clones it maybe possible to transform strains that differ at a vic
locus, e.g. vicx a and vicxb. If DNAcontaining the vicxa allele is used for
transformation, then a vicxa recipient strain should be transformedat a normal
rate. If the recipient strain carries the vicxb allele, then the heterozygous
transformants should grow poorly, or not at all. It should be possible to
determine if an individual DNAclone carries a particular vicx allele by
comparingthe relative efficiency with which the two recipients are transformed. This identification
technique is not immediately amenable to
sib-selection or to transformation with manydifferent cloned fragments,
since the desired transformants may be dead, weak, or morphologically
abnormal, depending upon the strength of the resulting incompatibility
interaction. The greater the numberof DNA
types put into the transformation,
the more difficult it will be to discern if there is a significant difference
betweenthe vicx a and the vicx~’ recipients. Direct selection of such poorly
growing strains, which would allow the use of sib-selection and related
techniques, might be possible if the pigmentation phenotypethat results in
somestrains carrying partial duplications (106, 110, 120) can be adapted
to transformation protocols.
HeterokaryonSelf-Incompatibility (HSI)
In the four genera discussed in this review, incompatiblestrains form to fuse
a heterokaryon,and it is only after cell fusion that the vegetative incompatibility reaction occurs. Strains carrying mutationsthat prevent themfrom fusing
to form heterokaryons, even with themselves, have been identified in field
populations of F. oxysporurn (10, 74, 76), F. moniliforme (21, 32, 85), and
F. subglutinans (30). These strains can lead to an incorrect diagnosis
vegetative incompatibility since they will usually not form heterokaryonswith
any other strains. It is important to identify such strains to prevent the
overestimation of the numberof VCGswithin a population.
In F. moniliforme (32), naturally occurring HSI (heterokaryon self-incompatible) mutant strains cultured under laboratory conditions form 2-16%
of the hyphal fusions formedby heterokaryon self-compatible (HSC)strains,
which can form heterokaryons normally. Hyphal branching per se does not
appear to be affected. Meiotic progeny from a cross betweenan HSCand HSI
Annual Reviews
www.annualreviews.org/aronline
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
136
LESLIE
strain segregate 1:1 for the HSIphenotype,suggesting that this trait is under
the control of a single nuclear gene (hsil). Crosses betweentwo HSIstrains
cannot be madesince the HSIstrains examinedto date are all female sterile.
Since heterokaryonsof F. moniliformeare limited to the cells that participated
in the fusion event, i.e. the nuclei do not migrate following heterokaryon
formation (16, 136), for an observable prototrophic heterokaryonto be formed,
there must be a sufficient numberof fusions so that the heterokaryotic cells
can cross-feed their neighbors. SomeHSIstrains can form weakheterokaryons
with HSCstrains (21, 76), however, so the HS1strains appear to have only
a diminishedcapacity to makea heterokaryonrather than a completeinability.
The 1-2%frequency at which HSI isolates are recovered from field populations, and their widespreadgeographic distribution, argues that mutations to
self-incompatibility are not uncommon
and that they are not subject to intense
selection pressure. Thesefindings, combinedwith the limited reproduction of
the heterokaryotic cells, suggest that heterokaryonformation, at least under
field conditions, is not of crucial importancein these Fusariumspp.
POPULATIONS
Studies of populations using VCGsas a means to measure diversity have
becomewidespread in recent years. The multiple-locus base for the VCG
subdivisions meansthat with one test the relationship at multiple loci is being
assessed. The resulting subdivisionspermit us to determineidentities relatively
quickly (e.g. 25, 47), but VCGsare not useful in determining the degree
relatedness if the two isolates are not identical. In Fusariummuchof the work
with VCGsis the result of two advances: The developmentof nit mutants as
forcing markersfor heterokaryontests, and the insightful proposal by Puhalla
(139) that pathogenic subgroupsmight be limited to one or a few VCGs.Work
with both biometric (17, 19) and molecular markers (10, 66, 76) has shown
that isolates within a VCG
tend to be moresimilar than isolates in different
VCGs.There are exceptions tc~ this rule, however,and although the assumption that strains within a VCGare clonally related appears to be generally
true, it should be madewith caution.
Isolates within a VCGare potentially capable of exchanging genetic
information via a parasexual process. The importanceof this ability depends
upon the structure of the population and the numberof partners with which a
strain could exchange information. Correlations between VCGsand other
characters such as pathogenicity could lead to useful diagnostics (6, 10, 34,
76, 103), and the VCGsthemselves are useful tools for tracking isolates that
are found or that have been released into the population (7, 83). VCGsmay
also be useful as a biological containment for cloned genes, especially if
coupled with traits such as heterokaryonself-incompatibility (see above) that
limit heterokaryonformation and sexual fertility.
Annual Reviews
www.annualreviews.org/aronline
FUNGALVEGETATIVECOMPATIBILITY
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
Population
137
Structure
VCGsserve as a natural meansto subdivide fungal populations. The vic loci
and alleles that define VCGs
are presumedto be selectively neutral with respect
to traits such as pathogenicityand vegetative viability per se. If selection acts
to maintain a large numberof VCGswithin a population, perhaps due to the
values of individualism such as those described by Rayner(143) or to reduce
spread of infectious agents (23, 71), then frequency-dependentselection may
be reflected in the frequencies of individual vic genes and VCGs,and the
numberof VCGsthat are maintained in the population.
Expectations for the types of subdivisions induced by VCGs
within a sexual
population are quite different from those expected for an asexual population.
If 10 vic loci with two alleles per locus are segregating in a population, then
offspring can be produced that belong to over 1000 different VCGs.If the
population reproduces sexually moreoften than selection and/or genetic drift
can eliminate the different VCGtypes from the population, then there will
always be a large numberof VCGsrepresented in the population. In general,
then, a sexually reproducing population would be expected to have a high
level of VCG
diversity. Thus, if a character (such as pathogenicity or race)
is determined by one or a few genes, there probably will be no correlation
between race and VCG.Since some transfer of mitochondria can occur
betweenstrains in different vegetative compatibility groups, the subdivisions
discerned in a population using VCGsmay not correspond 1:1 with those
discerned using mtDNA
polymorphisms (66).
In an asexual population, differences at the vic loci are assumed to
effectively limit the exchangeof genetic informationto those individuals that
belong to the same VCG.Since sexual recombination does not occur, members
of each VCGwill form a genetically isolated subpopulation that will be
subjected to standard population genetic forces such as selection, mutation,
migration, and drift (70). At their simplest, each VCGcan be thought of
a series of clones of a single parental strain (although in reality each VCG
will be composedof isolates that fortuitously possess the same set of vie
alleles). As time passes, if all membersof the clone are equally fit, then
members
of the clone will be lost by chanceto randomgenetic drift. Similarly,
if each VCG
is equally fit, then VCGswill be lost by chanceto genetic drift,
and the population will becomeless diverse. In each geographicarea different
VCGswill be lost by chance, and it is unlikely that any one VCGwould~be
retained at every site. If one (or a few) VCG
is selectively morefit than most
of the others, then membersof this group will tend to predominate in the
population at different geographiclocations.
Supposethat selection in such an asexual population occurs on the basis of
virulence. Underthese conditions, strains that can attack a particular host will
multiply in the presenceof that host, while strains that cannot attack the host
should be found in lesser numbers,if at all. Althoughthe genetic alterations
Annual Reviews
www.annualreviews.org/aronline
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
138
LESLIE
that give rise to newpathogenic races are not known,new races mayresult
from a single gene mutation, and for simplicity I will makethis assumption.
If the initial populationcontains no host-specific pathogenicstrains, then any
strain in which a mutation to pathogenicity occurs will be at a selective
advantage. Soil populations of some phytopathogenic fungi are extremely
diverse with respect to VCG(33, 64, 65, 81), and thus, if mutations occur
independently and at random, two mutants that are the result of different
independent mutation events wouldbe expected to occur in isolates that are
vegetatively incompatible. In contrast, isolates that are clones of each other
wouldbe expected to be in the same VCG.Thus, pathogenic strains that are
vegetatively compatible are presumedto have originated from the same clone
evenif they are geographicallyisolated fromone another. Conversely,isolates
with similar pathogenic capabilities that are vegetatively incompatible are
assumednot to be clones, but to have developedtheir pathogenic capabilities
independently. Distinctions such as these can enable investigators to distinguish betweenpathogenic strains that have arisen locally and those that have
been imported from another location.
VCG Stability
The usefulness of VCG
markers for population studies is dependentupontheir
stability. Theavailable data indicate that most VCGs
studied are stable through
time and space, including laboratory manipulation. A possible exception to
this general rule has recently been reported in C. parasitica, where mutants
with altered vegetative compatibility were induced with UVlight (144). Some
of these mutants were unstable with respect to their VCG-phenotype,but it
is unclear from the data presented whetherthe instability is due to a mutator
gene that was activated during the mutagenesisprocess or to an instability in
the alleles at one (or more)of the vic loci. Theseresults are quite different
from those reported by Anagnostakis (3), whofound no evidence for mitotic
instability of VCGsin C. parasitica. In one study using N. crassa, changes
in VCG
appear to be associated with gross genomicreorganization rather than
with simple mutation of one allelic form to another (127). There are instances
in F. oxysporumin which the VCGphenotypes differ but the strains have
identical mtDNA
RFLPphenotypes and race designations (66, 76, 129).
Changessuch as these could result from sexual recombination, but no sexual
stage is knownin F. oxysporurn, and Gordon& Okamotohave suggested that
exchangeof mitochondriacan occur betweenstrains that are in different VCGs
but that differ at only one or a fewvic loci.
Parasexuality
Parasexuality has been proposed as a widespreadevent in somefungi, but this
phenomenon
requires the establishment of a stable heterokaryon in which the
parasexual cycle of diploidization~haploidization can occur. The relative
Annual Reviews
www.annualreviews.org/aronline
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
FUNGALVEGETATIVECOMPATIBILITY
139
frequency of heterokaryon formation under natural conditions and the frequencyof subsequent parasexual recombinationhas been the subject of much
speculation, and additional experimentationwill be required to relate existing
claims [usually based on prototrophic recombinants recovered following
selection (e.g. 20, 48, 105, 117, 146-148, 150)] to heterokaryon formation
under field conditions. Parasexual recombinationis potentially an important
mechanism
in the life cycle of somefungi since it provides an alternative to
meiosis for the reassortment of the organism’sgenome.It is not clear whether
the transitory heterokaryons formed following fusion of two vegetatively
incompatible strains are sufficient for parasexual genetic exchangeto occur,
even though exchangeof at least somecytoplasmic constituents can occur.
Distinguishing
between true recombinants and grossly unbalanced
heterokaryonsis a difficult technical problem,even with the use of molecular
markers. At present, I would expect to see nuclear recombination under
nonselective conditions only between isolates that belong to the same VCG.
APPLICATIONS
VCGsand their constituent vic loci have a numberof potential applications
in addition to providing insights into the cellular and population biology of
these organisms.Suggestedapplications are primarily in the area of population
analysis and mirror the discussion of populations presented above. Applications of the vic gene phenotypes to questions in molecular and cell biology
will becomemore apparent once we have enough knowledgeabout these genes
to ask meaningfulquestions.
Diagnostics
The most useful application of vegetative compatibility for manyplant
pathologists is the potential use of VCGsas a diagnostic tool. This application
rests on the hypothesis (139) that strains in the samepathogenicgroup, e.g.
forma specialis, race, etc, are in one or only a few VCGs.The pathogen is
then identified through placementinto a particular VCG
rather than through
the muchmore laborious pathogenicity tests against a series of standard
cultivars. Muchof the population work with VCGsin Fusarium has been
concerned with testing this concept (6, 29, 30, 46, 51, 54, 65, 80-82, 94,
95, 102, 137, 139). The usefulness of the VCGsin this endeavor has varied
greatly. It has been very useful, with tight correlations, within F. oxysporurn
f. sp. apii (34, 138), F. oxysporumf. sp. conglutinans (10), andF. oxysporum
f. sp. tnelonis (74-76). VCGsand pathogenic groups have been moderately
well-correlated within F. oxysporumf. Sp. cubense (13,129-132). There have
been no obvious correlations, however, in F. oxysporumf. sp. asparagi (55)
and F. oxysporumf. sp. lycopersici (53).
In developing VCGsas a diagnostic tool, it is important to rememberthat
Annual Reviews
www.annualreviews.org/aronline
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
140
LESLIE
VCGs,as with other genetic and molecular tools such as RFLPs, RAPDs,
and isozymes, are correlative in nature, and that correlation does not imply
cause and effect. Most work to date has focused on subgroups of F.
oxysporum, and this fungus is extremely widespread in cultivated and
agricultural soils worldwide. Thus, it is important to complete Koch’s
postulates to test the correlation betweenVCG
and pathogenicity with isolates
being used. Twotypes of error are possible if such tests are not madesince
nonpathogenicstrains maybe recovered from diseased plants. In the first type
of error, if a nonpathogenicstrain(s) is in the same VCG
as the pathogenic
strain, then the VCG
test could detect artificially high levels of the pathogen.
Based on somework with strains from nominally nonpathogenicsources (34,
64, 65), I expect this type of problemto be relatively rare. In the secondtype
of error, strains apparently belonging to the same pathogenic subgroupwould
belong to manyVCGs.In such a case manydifferent nonpathogenic strains
maybe accompanyingone or a few pathogenic strains in their attack on the
plant. Both types of errors can be eliminated by repeating Koch’spostulates
with representative strains from each of the VCGsthat contains pathogenic
strains.
The usefulness of VCGsas a diagnostic tool can be strengthened if the
strains contained within the VCGcan be shownto be related to one another,
using a technique other than vegetative compatibility. Since VCGsare based
on the constitution of the organismat a set of vic loci, twostrains maybelong
to the same VCGbut yet not be asexual clones of a commonparent (21).
the pathogenic strains within a VCG
are all closely related or identical by
other measuresof genetic variability, e.g. RFLPsor RAPDs,then these data
wouldgreatly strengthen the idea that these strains are all derived from a
common
progenitor. In at least one case it has been possible to observe genetic
differentiation within a single VCGof F. oxysporumf. sp. cubense (129).
The usefulness of VCGsas a diagnostic tool could also be improvedif the
need to generate nit mutants in all of the field isolates to be examinedcould
be relieved. At present, these mutants can be generated sufficiently rapidly to
enable research level investigations to proceed, but it is not practical to use
this process on a commercialscale because of the amountof processing that
is required for each field isolate.
Analternative is to create a specific tester strain for each VCG
that needs
to be detected. The tester strain wouldhave one recessive marker that could
be selected against and one dominantmarker that could be selected for. In
the context of F. oxysporum the recessive marker would probably be an
auxotroph that requires a growth substance such as amino acid, vitamin, or
nucleic acid that the funguscould ordinarily synthesize for itself. This marker
wouldprobably be induced using a mutagenicagent such as ultraviolet light,
x-rays, or a chemical mutagen. The dominant marker would probably be a
drug-resistance marker, although the ability to utilize an exotic compound
or
Annual Reviews
www.annualreviews.org/aronline
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
FUNGALVEGETATIVE
COMPATIBILITY
141
other dominanttrait could also be used. This marker could be introduced by
recombinant DNA-mediated
transformation or by mutagenesis. Available drug
resistance markers include, but are not limited to, acriflavin, benomyl,
hygromycin, and methyltryptophan resistance, and exotic compoundscould
include acetamide. This strain could not grow by itself on the minimalmedium
commonlyused for screening F. oxysporumbecause of its recessive auxotrophy.
The tester strain would be incorporated into Komada’smediumthat had
been amended with the appropriate drug or exotic compound. (Komada’s
mediumis a commonlyused minimal mediumthat enriches for the Fusarium
propagulesin field samples.) If testing for several different VCGs
wasdesired,
then several different tester strains could be incorporated into the sametest
medium.Material containing the field isolates wouldbe distributed onto the
agar surface using established techniques for the material being examined.
Thedrug to whichthe tester strain is resistant wouldprevent the field strains
from growing by themselves.
Field strains and tester strains that are in the sameVCG
could fuse to form
stable complementaryheterokaryons. These heterokaryons wouldbe resistant
to the incorporated drug (fromthe markerin the tester strain) and able to grow
without unusual supplementation (from the prototrophic allele in the field
isolate that wouldcomplementthe tester strain’s defect). The heterokaryons
would appear as rapidly growing, vigorous colonies against a backgroundof
inhibited growthof either the tester strain or field strains that belongin different
VCGsand are unable to makea viable heterokaryon with the tester strain.
The numberof heterokaryotic colonies can be used as a direct measureof the
numberof fungal propagules of a particular VCG
present in the material being
sampled.
Tests
of Genetic Homogeneity
VCGsare a convenient tool for determining if field isolates are clones of a
common
progenitor. Suchidentifications can be important in determining the
numberof genetically distinct individuals within a population. VCGanalyses
can also be used to determine if strains with unusual variants have a clonal
origin. Such analyses have been used in Fusariummoniliforme to determine
if the strains carrying mutations at the pall (25) andfuml(47) loci were
clonal origin. In both cases, the strains examinedwere from distinct VCGs
and therefore were not clones. Thesedata are insufficient to prove that the
mutants are of independent origin, however, since sexual reproduction may
lead to progenythat carry the samemutation but are in different VCGs.
VCGscan also provide evidence for genetic nonhomogeneity.For example,
nonpathogenicpopulations of F. oxysporumare quite diverse with respect to
VCGsand similar to F. moniliforme in the amount of variability. In F.
moniliforme, which has a knownsexual stage, the relatively large numberof
Annual Reviews
www.annualreviews.org/aronline
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
142
LESLIE
VCGshas been attributed to sexual reproduction. This suggests that sexual
reproduction maybe occurring covertly in F. oxy~porumeven though no sexual
stage is knownfor this fungus. Here weseemto have a bullet hole in a target
without the "smoking gun" that is usually required to prove that sexual
reproduction is occurring. Similar situations are knownin other organismsas
well, e.g. the amoebaNaegleria lovaniensis (126).
A more careful examination of F. oxysporumfor a sexual stage may be
warranted. To the extent that previous workers examinedonly strains from
the same pathogenic and/or geographic origin, pairings mayhave been made
primarily between isolates belonging to the same VCGand sexual recombination would not be expected to occur. In some mating populations of
Gibberellafujikuroi(88) femalefertile strains are relatively rare. Thus, sexual
recombination, if it occurs, probably wouldnot be frequent but could occur
sufficiently often to maintain a large numberof VCGswithin the population.
Isogenization
and Genetic
Mapping
Genetically defined isogenic strains are a key underlying componentin most
genetically tractable systems. The construction of isogenic lines is usually a
tedious time-consumingtask that requires at least ten generations of backcrossing to a recurrent parent to achieve reasonable isogeneity (97). With
relatively quick generation time of 4-6 weeks, such a project wouldrequire
nearly a year just for the crosses, and longer if markers must be scored and
evaluated before the next set of backcrosses can be started. Even at the end
of such a process, a region of approximatelyten mapunits on either side of
the inbred locus (and appropriate mating-type loci) wouldremainheterozygous
(strictly speaking allozygous).
Differences at the vic loci can be used to select "near-isogenic" lines
following a single cross. The methodologyrelies on the fact that numerous
vic loci are dispersed throughout the genome,and that allelic identity is
required at all vic loci for stable heterokaryonformation. Whenbackcrossing
to a fixed parent, someof the progenyin the first backcrosswill be as isogenic
with the "recurrent" parent, as are the averageprogenyof the tenth (or later)
backcrosses. The problemis to identify these near-isogenic progeny, since all
of the progenywill be phenotypically identical. In the randombackcrossing
approach, all of the progeny become"near-isogenic" through the laws of
probability. If the two strains differ at numerousvic loci, however, then
homozygosityat all of the vic loci (as assessed by heterokaryon formation
betweensomeof the progenyand the recurrent parent) can be used to identify
near-isogenic lines following a single cross. If strains are marked with
appropriate auxotrophs (the nit mutants described above work quite well),
then the near-isogenic progenycan be selected directly on a suitable medium.
The process requires less time than the more traditional backcrossing procedure, but its efficiency depends upon the number and location of the
Annual Reviews
www.annualreviews.org/aronline
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
FUNGALVEGETATIVE
COMPATIBILITY
143
heterozygousvic loci. If the markerbeing brought into the constant genetic
backgroundis closely linked to one of the vic loci then more progenywill
needto be analyzedthan if the vic loci and the inbred markerare moreloosely
linked.
Asa corollary to this isogenization process, it is also possible to count and
to mapvic loci in systems where a sufficiently detailed genetic mapwith
molecularmarkersexists. In essence, the two strains are crossed and a set of
progenythat are vegetatively compatiblewith one of the parents is identified.
The molecular markers segregating in the cross are then scored. Each
heterozygousvic locus should sit at the heart of a region that is characterized
by no crossing over within this highly selected progeny set. The numberof
such regions should provide an estimate of the numberof heterozygous vic
loci in the cross and the linked markersshould provide a starting place for
the chromosomewalks needed to clone these genes.
CONCLUSIONS
AND PROBLEMS
REMAINING
Detailed molecular genetic investigations of mechanismsof vegetative compatibility are just beginning. Thesegenes governthe phenomenon
of self-recognition and are not biochemical"housekeeping"loci, in the same sense that
most biosynthetic genes are. Theseloci probably also play a critical role in
fungal life cycles. Anunderstanding of their role in cellular and population
terms should lead to newinsights as to howfungal cells and the populations
to whichthey belong are organized. Someof the problemsof interest remaining
listed below.
1,
2.
3.
4.
5.
6.
Howmanydifferent types of vegetative compatibility interactions exist?
Are vic genes essential?
Howmanydiscriminatory alleles are there per vic locus?
Whatrole, if any, do the vic genes play in the sexual cycle?
Whatother genes, if any, are involved in vic gene expression?
What is the molecular basis of the recognition and killing reactions
associated with vegetative compatibility?
7. Howsimilar are the different vic loci within a fungus to one another, or
to loci with similar functions in other fungi and other organisms?
8. Howimportant are the vic loci in delimiting fungal individuals?
9. Howimportant are the vic genes as blocks to genetic exchangeunder field
conditions?
10. Whatis the significance of the VCGsubdivisions within populations?
11. Howstable are VCGsin nature?
I suspect that progress in the area of vegetative compatibility, especially
the molecularand cellular aspects, will be rapid. The vegetative compatibility
phenomenon
provides a simple modelfor self/nonself recognition and inter-
Annual Reviews
www.annualreviews.org/aronline
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
144
LESLIE
action, a commonproperty of biological systems. An understanding of the
basic underlying biology should further the implementation of biological
control measures that rely on the transfer of cytoplasmic hypovirulence factors,
and perhaps provide new insights into the means that these organisms use to
recognize other inhabitants of their environment.
Population questions are already being addressed in some fungi using
vegetative compatibility. The amount of variability present in some populations may determine the usefulness of VCGsas a diagnostic tool. At present
there is no general rule about correlation between pathogenicity and VCG,
with some systems showing useful correlation between VCGand pathogenicity, while others show little or no correlation. The alleles at the vic loci may
be subject to frequency-dependent selection, and once molecular probes for
different alleles becomeavailable direct studies of allele frequencies should
be possible. An important constraint to many population studies is the lack
of suitable theoretical models to test with the data that are rapidly becoming
available. Development of these models will be as important to the interpretation of the population data as the development of the molecular tools
necessary to obtain the data.
Further studies of vegetative compatibility should lead to new insights into
the organization, composition, and function of fungal individuals and populations. Answers to the numerous remaining population and cellular/molecular
questions should complement one another and increase our understanding of
how fungi distinguish self from nonself and why they might wish to do so.
ACKNOWLEDGMENTS
Contribution no. 93-251-J from the Kansas Agricultural Experiment Station,
Manhattan. Research in my laboratory is supported by the Kansas Agricultural
Experiment Station, the Kansas State Board of Agriculture (Kansas Corn
Commission), and the Sorghum/Millet Collaborative Research Support Program (INTSORMIL) AID/DAN-1254-G-00-0021-00 from the US Agency for
International
Development, Washington, D.C. Portions of this manuscript
were completed while I was on sabbatical leave in the laboratory of David
D. Perkins, Department of Biological Sciences, Stanford University, Stanford,
CA, and supported in part by US Public Health Service Research grant AI
01462 to Dr. Perkins.
Literature Cited
1. Adams,G., Hammar,S., Proffer, T.
1990. Vegetative compatibility in
Leucostomapersoonii. Phytopathology
2.
80:287-91
Adams, G., Johnson, N., Leslie,
J.
F., Hart, L, P. 1987. Heterokaryons
of Gibberella zeae formed following
3.
4.
hyphal anastomosis or protoplast fusion.
Exp. Mycol. 11:339-53
Anagnostakis, S. L. 1977. Vegetative
incompatibility in Endothia parasitica.
Exp. Mycol. 1:306-16
Anagnostakis,
S. L. 1982. Genetic
analyses of Endothia parasitica: Link-
Annual Reviews
www.annualreviews.org/aronline
FUNGAL VEGETATIVE
5.
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
age data for four single genes and
three vegetative compatibility types.
Genetics 102:25-28
Anagnostakis, S. L., Waggoner, P. E.
1981. Hypovirulence, vegetative incompatibility, and the growthof cankers
of chestnut blight. Phytopathology71:
1198-202
Baayen, R. P., Kleijn, L. 1989. The
Elegansfusaria causing wilt disease of
carnation. II. Distinction of vegetative
compatibility groups. Neth. J. Plant
Pathol. 95:185-94
Bayman, P., Cotty, P. J. 1991. Vegetative compatibility and genetic diversity in the Aspergillusflavus population
of a single field. Can. J. Bot. 69:170711
Bernet, J. 1967. Les syst~mes
d’incompatibilities chez le Podospora
anserina. C. R. Acad. Sci. Paris 265:
1330~33
Boone, D. M. 1971. Genetics of Venturia inaequalis. Annu.Rev. Phytopathol.
9:297-318
Bosland, P. W., Williams, P. H. 1987.
An evaluation of Fusarium oxysporum
from crucifers based on pathogenicity,
isozyme polymorphism, vegetative
compatibility, and geographic origin.
Can. J. Bot. 65:2067-73
Bowden, R. L., Leslie, J. F. 1992.
Nitrate non-utilizing
mutants of
Gibberella zeae (Fusarium graminearum) and their use in determining
vegetative compatibility. Exp. Mycol.
16:308-15
Bowden, R. L., Leslie, J. F. 1992.
Evidencefor outcrossing in Gibberella
zeae (Fusarium graminearutn). Phytopathology 82:1065 (Abstr.)
Brake, V. M., Pegg, K. G., Irwin,
J. A. G., Langdon, P. W. 1990.
Vegetative compatibility groups within
Australian populations of Fusariumoxysporum f. sp. cubense, the cause of
Fusarium wilt of bananas. Aust. J.
Agric. Res. 41:863-70
Brasier, C. M. 1983. A cytoplasmically
transmitted disease of Ceratocystis
ulmi. Nature 305:220-23
Brooker, N. L., Leslie, J. F., Dickman,
M. B. 1991. Nitrate non-utilizing mutants of Colletotrichum and their use
in studies of vegetative compatibility
and genetic relatedness. Phytopathology
81:672-77
Bumett, J. H. 1975. Mycogenetics: An
Introduction to the General Genetics
of Fungi. NewYork: Wiley. 375 pp.
Butcher, A. C. 1968. The relationship
between sexual outcrossing
and
heterokaryon incompatibility in Aspergillus nidulans. Heredity 23:443-52
COMPATIBILITY
145
18. Butcher, A. C. 1969. Non-allelic interactions and genetic isolation in wild
populations of Aspergillus nidulans.
Heredity 24:621-31
19. Butcher, A. C., Croft, J. H., Grindle,
M. 1972. Use of genotype environmentalinteraction analysis in the study
of natural populations of Aspergillus
nidulans. Heredity 29:263-83
20. Buxton, E. W. 1954. Heterocaryosis
and variability in Fusariumoxysporum
f. gladioli (Snyder &Hansen). J. Gen.
Microbiol. 10:71-84
21. Campbell, C., Farrokhi-Nejad, R., Leslie, J. F. 1992. Genetic diversity of
Fusarium moniliforme in seed from
two maize cultivars. Phytopathology
82:1082 (Abstr.)
22. Catch, C. E. 1971. Heterokaryon incompatibility in imperfect species of
Aspergillus. Heredity 26:29%312
23. Caten, C. E. 1972. Vegetative incompatibility and cytoplasmic infection in fungi. J. Gen. Microbiol.
72:221-29
24. Caten, C. E., Jinks, J. L. 1966.
Heterokaryosis: Its significance in wild
homothallic ascomycetes and fungi imperfecti. Trans. Br. Mycol. Soc. 49:8193
25. Chaisrisook, C., Leslie, J. F. 1990.
A maternally-expressed nuclear gene
controlling perithecial pigmentationin
Gibberella fujikuroi
(Fusarium
moniliforme). J. Hered. 81 : 189-92
26. Chase, T. E., UIIrich, R. C. 1990.
Genetic basis of biological species in
Heterobasidion annosurn: Mendelian
determinants. Mycologia 82:67-72
27. Chase, T. E., Ullrich, R. C. 1990.
Five genes determiningintersterility in
Heterobasidion annosum. Mycologia
82:73-81
28. Christensen, J. J., DeVay,J. E. 1955.
Adaptation of plant pathogen to host.
Annu. Rev. Phytopathol. 6:367-92
29. Correll, J. C. 1991. The relationship
between formae speciales, races and
vegetative compatibility groups in Fusarium oxysporum. Phytopathology 81:
1061-64
30. Correll, J. C., Gordon, T. R., McCain,
A. H. 1992. Genetic diversity in California and Florida populations of the
pitch canker fungus Fusarium subglutinans f. sp. pini. Phytopathology
82:415-20
31. Correll, J. C., Klittich, C. J. R.,
Leslie, J. F. 1987. Nitrate nonutilizing
mutants of Fusarium oxysporum and
their use in vegetative compatibility
tests. Phytopathology 77:164(~46
32. Correll, J. C., Klittich, C. J. R.,
Leslie, J. F. 1989. Heterokaryonself-
Annual Reviews
www.annualreviews.org/aronline
146
33.
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
LESLIE
incompatibility in Gibberella fujikuroi
(Fusarium moniliforme). Mycol. Res.
93:21-27
Correll, J. C., Puhalla, J. E., Schneider, R. W. 1986. Vegetative compatibility groups among nonpathogenic
root-colonizing strains of Fusariumoxysporum. Can. J. Bot. 64:2358-61
Correll, J. C., Puhalla, J. E., Schneider, R. W. 1986. Identification
of
Fusariumoxysporumf. sp. apii on the
basis of colony size, virulence and
vegetative compatibility. Phytopathology 76:396-400
Cove, D. J. 1976. Chlorate toxicity
in Aspergillus nidulans: Studies of mutants altered in nitrate assimilation.
Mol. Gen. Genet. 146:147-59
Cove, D. J. 1976. Chlorate toxicity
in Aspergillus nidulans: The selection
and characterization of chlorate resistant
mutants. Heredity 36:191-203
Croft, J. H., Dales, R. B. G. 1984.
Mycelial interactions and mitochondrial
inheritance in Aspergillus. In TheEcology and Physiology of the Fungal
Mycelium, ed. D. H. Jennings, A. D.
M. Rayner, pp. 433-50. London/New
York: Cambridge Univ. Press
Croft, J. H., Jinks, J. L. 1977. Aspects
of the populationgenetics of Aspergillus
nidulans. In Genetics and Physiology
of Aspergillus, ed. J. E. Smith, J. A.
Pateman, pp. 339-60. NewYork: Academic
Cullen, D., Smalley, E. B., Dimond,
R. L. 1983. Heterokaryosis in Fusarium
tricinctum and F. sporotrichioides. J.
Gen. Microbiol. 129:3035-41
Dales, R. B. G., Croft, J. H. 1977.
Protoplast fusion and the isolation of
heterokaryons and diploids from vegetatively incompatiblestrains of Aspergillus nidulans. FEMSMicrobiol. Lett.
1:201-4
Dales, R. B. G., Croft, J. H. 1983.
A chromosome assay method for the
detection of heterokaryonincompatibility (het) genes operating betweenmembers of different
heterokaryon
compatibility (h-c) groupsin Aspergillus nidulans. J. Gen. Microbiol. 129:
3643-49
Dales, R. B. G., Croft, J. H. 1990.
Investigation of the her genes that
control heterokaryonincompatibility between members of heterokaryon-compatibility
(h-c) groups A and G1
Aspergillus
nidulans.
J.
Gen.
Microbiol. 136:1717-24
Dales, R. B. G., Moorhouse,J., Croft,
J, H. 1983. The location and analysis
of two heterokaryon incompatibility
(het) loci in strains of Aspergillus
44.
45.
46.
47.
48.
49.
50.
51.
52.
53.
54.
55.
nidulans. J. Gen. Microbiol. 129:363742
Davis, R. H. 1966. Mechanisms of
inheritance. 2. Heterokaryosis. In The
Fungi: An Advanced Treatise, Vol. H,
The Fungal Organism, ed. G. C. Ainsworth, A. S. Sussman, pp. 567-88.
London/NewYork: Academic. 805 pp.
Day, P. R. 1960. Variation in phytopathogenic fungi.
Annu. Rev.
Microbiol. 14:1-16
Desjardins, A. E., Chfist-Harned, E.
A., McCormick,S. P., Secor, G. A.
1993. Population structure and genetic
analysis of field resistance to thiabendazole in Gibberella pulicaris from
potato tubers. Phytopathology 83:16370
Desjardins, A. E., Plattner, R. D.,
Shackelford, D. D., Leslie, J. F.,
Nelson, P. E. 1992. Heritability of
fumonisin B~ production in Gibberella
fujikuroi mating population A. Appl.
Environ. Microbiol. 58:279%805
Dhillon, T. S., Garber, E. D.,
Wyttenbach, E. G. 1961. Genetics of
fungi.
VI.
phytopathogenic
Heterokaryons involving Gibberella
fujikuroi and formae of Fusariumoxysporum. Can. J. Bot. 39:785-92
Doe, F. J. 1984. A role of vegetative
incompatibility genes in speeding the
onset of sexual reproduction in Neuro~pora. Neurospora Newsl. 31:14
(Abstr.)
Doe, F. J., Leslie, J. F. 1993. A
laboratory exercise for isolating and
characterizing microbial mutants with
metabolic defects. Am. Biol. Teach.
55:1n press
Dossa, C., Pandobahuon, A., Renard,
J. L., Boisson, C. 1991. Determination
of vegetative compatibility groups in
African Fusarium oxysporum strains
isolated from vascular wilt-infected oil
palms. Oleagineux 46:145-47
E1-Ani, A. S. 1981. Further studies
on heterokaryon compatibility
in
Ceratocystis radicicola. J. Elisha
Mitchell Sci. Soc. 97:136-38
Elias, K. S., Schneider, R. W. 1991.
Vegetative compatibility groups in Fusarium oxysporumf. sp. lycopersici.
P hytopathology 81:159-62
Elmer, W. H. 1991. Vegetative compatibility
groups of Fusarium proliferatum
from asparagus
and
comparisonsof virulence, growthrates,
and colonization of asparagus residues
amonggroups. Phytopathology 81:85257
Elmer, W. H., Stephens, C. T. 1989.
Classification of Fusarium oxysporum
f. sp. asparagi into vegetatively com-
Annual Reviews
www.annualreviews.org/aronline
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
FUNGAL VEGETATIVE
patible groups. Phytopathology 79:8893
56. Esser, K., Blaich, R. 1973. Heterogenic
incompatibility in plants and animals.
Adv. Genet. 17:107-52
57. Ferenczy, L., Szegedi, M, Kevei, F.
1977.Interspecific protoplast fusion and
complementation in Aspergilli. Experientia 33:184-86
58. Fincham,J. R. S., Day, P. R., Radford,
A. 1979. Fungal Genetics. Berkeley/Los Angeles: Univ. Calif. Press.
636 pp. 4th ed.
59. Garnjobst, L. 1953. Genetic control of
heterokaryosis in Neurospora crassa.
Am. J. Bot. 40:607-14
60. Garnjobst, L. 1955. Further analysis
of genetic control of heterocaryosis in
Neurospora crassa. Am. J. Bot. 42:
444-48
61. Garnjobst, L., Wilson, J. F. 1956.
Heterokaryosis and protoplasmic incompatibility in Neurospora crassa.
Proc. Natl. Acad. Sci. USA 42:61318
62. Glass, N. L., Kuldau, G. A. 1992.
Mating type and vegetative incompatibility in filamentous ascomycetes.
Annu. Rev. Phytopathol. 30:201-24
63. Gobbi, E., Martin, R. M,, Powell,
W. A., Van Alfen, N. K. 1990. Mitochondrial DNAof Cryphonectria
parasitica: Lack of migration between
vegetatively compatible strains. Mol.
Plant-Microbe Interact. 3:66-71
64. Gordon, T. R., Okamoto, D. 1991.
Vegetative compatibility groupings in
a local population of Fusarium oxysporum. Can. d. Bot. 69:168-72
65. Gordon, T. R., Okamoto, D. 1992.
Populationstructure and the relationship
between pathogenic and nonpathogenic
strains of Fusarium oxysporurn. Phytopathology 82:73-77
66. Gordon, T. R., Okamoto, D. 1992.
Variation in mitochondrial DNAamong
vegetatively compatibleisolates of Fusarium oxysporum, l£xp. Mycol. 16:
245-50
67. Griffiths, A. J. F. 1979. A Neurospora
experimentfor an introductory biology
course. Neurospora Newsl. 26:12
68. Griffiths, A. J. F., Rieck, A. 1981.
Perithecial distribution in standard and
variant strains of Neurosporacrassa.
Can. J. Bot. 59:2610-17
69. Griffin, D. H., Quinn, K. E., Gilbert,
G. S., Wang, C. J. K., Rosemarin,
S. 1992. The role of ascospores and
conidia as propagules in the disease
cycle of Hypoxylon mammatum.Phytopathology 82:114-19
70. Hartl, D. L., Clark, A. G. 1989.
Principles of Population Genetics. Sun-
71.
72.
73.
74.
75.
76.
77.
78.
79.
80.
81.
82.
83.
84.
COMPATIBILITY
147
derland, MA:Sinauer. 682 pp. 2nd
ed.
Hartl, D. L., Dempster, E. R., Brown,
S. W. 1975. Adaptive significance of
vegetative incompatibility in Neurospora crassa. Genetics 81:553-69
Isaac, I. 1967. Speciation in Verticilliurn. Annu. Rev. Phytopathol. 5:20122
Jacobson, D. J. 1992. Control of mating
type heterokaryon incompatibility by
the tol gene in Neurosporacrassa and
N. tetrasperrna. Genorne35:347-53
Jacobson, D. J., Gordon, T. R. 1988.
Vegetative compatibility and self-incompatibility within Fusarium oxysporurn f. sp. melonis. Phytopathology
78:668-72
Jacobson, D. J., Gordon, T. R. 1990.
Further investigations of vegetative
compatibility within Fusarium oxysporum f. sp. melonis. Can. J. Bot.
68:1245-48
Jacobson, D. J., Gordon, T. R. 1991.
Fusarium oxysporutn f. sp. melonis:
A case study of diversity within a
forma specialis. Phytopathology 81:
1064-67
Jinks, J. L., Catch, C. E., Simchen,
G., Croft, J. H. 1966. Heterokaryon
incompatibility and variation in wild
populations of Aspergillus nidulans.
Heredity 21:227-39
Jinks, J. L., Grindle, M. 1963. The
genetical basis of heterokatyon incompatibility in Aspergillus nidulans. Heredity 18:407-11
Joaquim, T. R., Rowe, R. C. 1990.
Reassessmentof vegetative compatibility relationships amongstrains of Verticillium
dahliae using nitratenonutilizing mutants. Phytopathology
80:1160-66
Katan, T., Hadar, E., Katan, J. 1989.
Vegetative compatibility of Fusarium
oxysporumf. sp. dianthi from carnation
in Israel. Plant Pathol. 38:376-81
Katan, T., Katan, J. 1988. Vegetative-compatibility groupingof Fusarium
oxysporumf. sp. vasinfectum from tissue and the rhizosphereof cotton plants.
Phytopathology 78:852-55
Katan, T., Zamir, D., Saffatti, M.,
Katan, J. 1991. Vegetative compatibility groups and subgroupsin Fusarium
oxysporumf. sp. radicis-lycopersici.
Phytopathology 81:255-62
Kedera, C. J., Leslie, J. F., Claflin,
L. E. 1992. Systemic infection of corn
by Fusariummoniliforme. Phytopathology 82:1138 (Abstr.)
Klittich, C. J. R., Correll, J. C.,
Leslie, J. F. 1988. Inheritance of sectoring
frequency
in Fusarium
Annual Reviews
www.annualreviews.org/aronline
148
85.
86.
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
87.
88.
89.
90.
91.
92.
93.
94.
95.
96.
LESLIE
moniliforme (Gibberella fujikuroi).
Exp. Mycol. 12:289-94
Klittich, C. J. R., Leslie, J. F. 1988.
Nitrate reduction mutants of Fusarium
moniliforme(Gibberella fujikuroi). Genetics 118:417-23
Klittich, C. J. R., Leslie, J. F. 1988.
Multi-well plates for complementation
tests of Fusarium. Fungal Genet.
Newsl. 35:21-22
Klittich, C. J. R., Leslie, J. F. 1989.
Chlorate-resistant, nitrate-utilizing mutants of Fusariummoniliforme (Gibberella fujikuroi). J. Gen. Microbiol.135:
721-27
Klittich, C. J. R., Leslie, J. F. 1992.
Identification of a second mating population
within
the
Fusarium
moniliforme anamorph of Gibberella
fujikuroi. Mycologia 84:541-47
Kohn, L. M., Carbone, I., Anderson,
J. B. 1990. Mycelial interactions in
Sclerotinia sclerotiorum. Exp. Mycol.
14:255-67
Kohn, L. M., Stasovski, E., Carbone,
I., Royer, J., Anderson, J. B. 1991.
Mycelial incompatibility and molecular
markersidentify genetic variability in
field populations of Sclerotinia
sclerotiorum. Phytopathology 81:48085
Kroon, B. A. M., Elgersma, D. M.
1991. Induction of mutants of Fusarium
oxysporumf. sp. lycopersici with altered virulence. Neth, J. Plan~Pathol.
97:409-16
Kuhlman, E. G., Bhattacharyya, H.
1984. Vegetative compatibility and
hypovirulence conversion amongnaturally occurring isolates of Cryphonectria parasitica. Phytopathology 74:
659-64
Labar~re, J., Bemet, J. 1977. Protoplasmic incompatibility and cell lysis
in Podosporaanserina. I. Genetic investigations on mutations of a novel
modifier gene that suppresses cell destruction. Genetics 87:249-57
LaMondia, J. A., Elmer, W. H. 1989.
Pathogenicity and vegetative compatibility amongisolates of Fusariumoxysporum and F. moniliforme colonizing
asparagus tissue. Can. J. Bot. 67:242024
Larkin, R. P., Hopkins, D. L., Martin,
F. N. 1990. Vegetative compatibility
within Fusarium oxysporum f. sp.
niveumand its relationship to virulence,
aggressiveness, and race. Can. J.
Microbiol. 36:352-58
Leach, J., Yoder, O. C. 1983.
Heterokaryon incompatibility in the
plant-pathogenic fungus Cochliobolus
heterostrophus. J. Hered. 74:149-52
97.
98.
99.
100.
101.
102.
103.
104.
105,
106.
107.
108.
109.
Leslie, J. F. 1981. Inbreeding for
isogeneity by backcrossing to a fixed
parent in haploid and diploid eukaryotes. Genet. Res. 37:239-52
Leslie, J. F. 1987. Heterokaryon incompatibility haplotypes on linkage
group VIL of Neurospora cra~’~’a.
Mycol. Soc. Am. Newsl. 38(1):35
(Abstr.)
Leslie, J. F. 1990. Genetic exchange
within sexual and asexual populations
of Fusarium. In Fusarium Wilt of Banana, ed. R. C. Ploetz, pp. 37-48.
St. Paul, MN:APS Press. 140 pp.
Leslie, J. F., Doe, F. J., Plattner, R.
D., Shackelford, D. D., Jonz, J. 1992.
Fumonisin BI and vegetative compatibility of strains from Gibberella
fujikuroi mating population ’A’ (Fusarium moniliforme). Myeopathologia
117:37-45
Leslie, J. F., Klittich, C. J. R., Correll,
J. C. 1988. Genetic exchange between
natural isolates of Fusariurn. Mycol.
Soc. Am. Newsl. 39(1):36 (Abstr.)
LOftier, H. J. M., Rumine, P. 1991.
Virulence and vegetative compatibility
of Dutch and Italian isolates of Fusarium oxysporumf. sp. lilii. J. Phytopathol. 132:12-20
Manicom, B. Q., Bar-Joseph, M.,
Kotze, J. M., Becker, M. M. 1990.
A restriction fragment length polymorphism probe relating vegetative compatibility groups and pathogenicity in
Fusarium oxysporum f. sp. dianthi.
Phytopathology 80:336-39
Miller, J. J. 1945. Studies on the
Fusariumof muskmelonwilt. I. Pathogenic and cultural studies with particular
reference to the cause and nature of
variation in the causal organism. Can.
J. Res. Sect. C 23:16-43
Moln~r, A,, Sulyok, L., Homok,L.
1990. Parasexual recombination betweenvegetatively incompatiblestrains
in Fusarium oxysporurn. Mycol. Res.
94:393-98
Mylyk, O. M. 1975. Heterokaryon
incompatibility genes in Neurospora
crassa detected using duplication-producing chromosome rearrangements.
Genetics 80:107-24
Mylyk, O. M. 1976. Heteromorphism
for heterokaryon incompatibility genes
in natural populations of Neurospora
crassa. Genetics 83:275-84
Newhouse, J. R., MacDonald, W. L.
1991. Theultrastructure of hyphalanastomoses between vegetatively compatible and incompatible virulent and
hypovirulent strains of Cyphonectria
parasitica. Can. J. Bot. 69:602-14
Newmeyer, D. 1970. A suppressor of
Annual Reviews
www.annualreviews.org/aronline
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
FUNGAL VEGETATIVE COMPATIBILITY
the heterokaryon-incompatibility associated with mating-type in Neurospora
crassa. Can. J. Genet. Cytol. 12:91426
110. Newmeyer, D., Taylor, C. W. 1967.
A pericentric inversion in Neurospora
with unstable duplication progeny. Genetics 56:771-91
111. Newton, A. C., Caten, C. E. 1988.
Auxotrophic mutants of Septoria
nodorumisolated by direct screening
and by selection for resistance to chlorate. Trans. Br. Mycol. Soc. 90:199207
112. Nuss, D. L., Koltin, Y. 1990. Significance of dsRNAgenetic elements in
plant pathogenic fungi. Annu. Rev.
Phytopathol. 28:37-58
113. O’Garro, L. W., Clarkson, J. M. 1988.
Heterokaryon incompatibility and heterozygousdiploid production in Tomato
wilt isolates of Verticillium dahliae. J.
Gen. Microbiol. 134:2977-84
114. Ogoshi, A. 1987. Ecology and pathogenicity of anastomosis and interspecific groups of Rhizoctonia solani
Kiihn. Annu. Rev. Phytopathol. 25:
125-43
l lS. Page, O. T. 1961. Variation in the
banana-wilt pathogen Fusarium oxysporum f. cubense. Can. J. Bot.
39:545-57
116. Papa, K. 1986. Heterokaryon incompatibility
in Aspergillus flavus.
Mycologia 78:98-101
117. Parmeter, J. R. Jr., Snyder, W. C.,
Reichle, R. E. 1963. Heterokaryosis
and variability in plant pathogenic
fungi. Annu. Rev. Phytopathol. 1:5176
118. Peberdy, J. F., Ferenczy, L., eds.
1985. Fungal Protoplasts: Applications
in Biochemistry and Genetics. New
York: Dekker. 354 pp.
119. Perkins, D. D. 1972. An insertional
translocation in Neurosporathat generates duplications heterozygous for
mating type. Genetics 71:25-51
120. Perkins, D. D. 1975. The use of
duplication-generating rearrangements
for studying heterokaryon incompatibility genes in Neurospora. Genetics
80:87-105
121. Perkins, D. D. 1988. Main features
of vegetative incompatibility in Neurospora. Fungal Genet. Newsl. 35:4446
122. Perkins, D. D. 1992. Neurospora: The
organism behind the molecular revolution. Genetics 130:687-701
123. Perkins, D. D., Barry, E. G. 1977.
The cytogenetics of Neurospora. Adv.
Genet. 19:133-285
124. Perkins, D. D., Leslie, J. F., Jacobson,
125.
126.
127.
128.
129.
130.
131.
132.
133.
134.
135.
136.
149
D. J. 1993. Srains for identifying and
studying individual vegetative (heterokaryon) incompatibility loci in Neurospora crassa. Fungal Genet. Newsl.
40. In press
Perkins, D. D., Radford, A., Newmeyer, D., Bj6rkman, M. 1982. Chromosomalloci of Neurospora crassa.
Microbiol. Rev. 46:426-570
Pernin, P., Ataya, A., Cariou, M. L.
1992. Genetic structure of natural populations of the free-living amoeba,
Naegleria lovaniensis: Evidence for
sexual reproduction. Heredity 68:17381
Pittenger, T. H. 1964. Spontaneous
alterations of heterokaryoncompatibility factors in Neurospora. Genetics
50:471-84
Pittengcr, T. H., Brawncr, T. G. 1961.
Genetic control of nuclear selection in
Neurospora heterokaryons. Genetics
46:1645-63
Ploetz, R. C. 1990. Population biology
of Fusariurn oxysporumf. sp. cubense.
In Fusarium Wilt of Banana, ed. R.
C. Ploetz, pp. 63-76. St. Paul, MN:
APS Press. 140 pp.
Ploetz, R. C., Correll, J. C. 1988.
Vegetative compatibility amongraces
of Fusariumoxysporumf. sp. cubense.
Plant Dis. 72:325-28
Ploetz, R. C., Shepard, E. 1989. Fusarial wilt of banana in Florida. My¢ol.
Res. 93:242~45
Ploetz, R. C., Shepard, E. S., Crane,
J. H. 1988. Current importance of
fusarial wilt of banana in Dadecounty,
Florida and relationships amongand
the origins of isolates of the incitant,
Fusarium oxysporum f. sp. cubense
from Florida and other banana-growing
regions. Proc. Fla. State Hortic. Soc.
101:256-59
Ploetz, R. C., Shokes, F. M. 1986.
Evidence for homothallism and vegetative compatibility in southern
Diaporthe phaseolorum. Can. J. Bot.
64:2197-200
Proffer, T. J., Hart, J. H. 1988. Ve.getative
compatibility
groups m
Leucocytosporakunzei. Phytopathology
78:256-60
Puhalla, J. E. 1979. Classification of
isolates of Verticilliurn dahliae based
on heterokaryon incompatibility. Phytopathology 69:1186-89
Puhalla, J. E. 1981. Genetic considerations of the genus Fusarium. In
Fusarium: Disease, Biology and Taxonomy, ed. P. E. Nelson, T. A.
Toussoun, R. J. Cook, pp. 291-305.
University Park, PA: Penn. State Univ.
Press. 457 pp.
Annual Reviews
www.annualreviews.org/aronline
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
150
LESLIE
137. Puhalla, J. E. 1984. A visual indicator
of heterokaryosis in Fusarium oxysporumfrom celery. Can. J. Bot. 62:
541~45
138. Puhalla, J. E. 1984. Races of Fusarium
oxysporumf. sp. apii in California and
their genetic interrelationships. Can.J.
Bot. 62:546-50
139. Puhalla, J. E. 1985. Classification of
strains of Fusariumoxysporum on the
basis of vegetative compatibility. Can.
J. Bot. 63:179-83
140. Puhalla, J. E., Hummel, M. 1983.
Vegetative compatibility groups within
Verticillium dahliae. Phytopathology
73:1305-8
141. Puhalla, J. E., Spieth, P. T. 1983.
Heterokaryosis
in
Fusarium
moniliforme. Exp. Mycol. 7:328-35
142. Puhalla, J. E., Spieth, P. T. 1985. A
comparison of heterokaryosis and vegetative incompatibility amongvarieties
of Gibberella fujikuroi (Fusarium
moniliforme). Exp. Mycol. 9:39-47
143. Rayner, A. D. M. 1991. The phytopathological significance of mycelial
individualism. Annu. Rev. Phytopathol.
29:305-23
144. Rizwana, R., Powell, W. A. 1992.
Ultraviolet light-induced instability of
vegetative compatibility groups of
Cryphonectria parasitica. Phytopathology 82:1206--11
145. Sharland, P. R., Rayner, A. D. M.
1989. Mycelial interactions in outcrossing populations of Hypoxylon. Mycol.
Res. 93:187-98
146. Sidhu, G. S. 1983. Genetics of
Gibberella fujikuroi. I1. Natural occurrence and significance of heterokaryosis
in sorghumisolates. Can. J. Bot. 61:
331~--19
147. Sidhu, G. S. 1983. Genetics of
Gibberella fujikuroi. III. Significance
of heterokaryosis in naturally occurring
corn isolates. Can. J. Bot. 61:332025
148. Sidhu, G. S. 1983. Sexual and parasexual variability in soil fungi with
special
reference
to Fusarium
moniliforme. Phytopathology 73:95255
149. Sidhu, G. S. 1986. Genetics of
Gibberella fujikuroi. VIII. Vegetative
compatibility groups. Can. J. Bot. 64:
117-21
150. Sidhu, G. S., Webster, J. M. 1979.
A study of heterokaryosis and its sig-
15l~
152.
153.
154.
155.
156.
157.
158.
159.
160.
161.
162.
163.
nificance on virnlence in Fusarium
oxysporum. Can. J. Bot. 57:548-55
Stasz, T. E., Harman,G. E., Gullino,
M. L. 1989. Limited vegetative compatibility followingintra- and interspecific protoplast fusion in Trichoderma.
Exp. Mycol. 13:364-71
Stover, R. H. 1959. Studies on Fusarium wilt of bananas. IV. Clonal
differentiation amongwild type isolates
of F. oxysporum f. cubense. Can. J.
Bot. 37:245-55
Thompson,R. D., Kirch, H.-H. 1992.
The S locus of flowering plants: When
self-rejection is self-interest. Trends
Genet. 8:381-87
Tinline, R. D., MacNeill, B. H. 1969.
Parasexuality in plant pathogenicfungi.
Annu. Rev. Phytopathol. 7:147-70.
Todd, N. K., Rayner, A. D. M. 1980.
Fungal individualism. Sci. Prog. 66:
331-54
Turcq, B., Denayrolles, M., Begueret,
J. 1990. Isolation of the two allelic
incompatibility genes s and S of the
fungus Podospora anserina. Curr.
Genet. 17:297-303
Typas, M. A. 1983. Heterokaryon incompatibility and interspecific hybridization bctweenVerticilliurn albo-atrum
and Verticillium dahliae following protoplast fusion and microinjection. J.
Gen. Microbiol. 129:3043-56
Van Alfen, N. K. 1982. Biology and
potential
for disease control of
hypovirnlence of Endothia parasitica.
Annu. Rev. Phytopathol. 20:349-62
Volk, T. J., Leonard, T. J. 1989.
Experimental studies on the morel. I.
Heterokaryon formation between
monoascosporousstrains of Morchella.
Mycologia 81:523-31
Webster, R. K. 1974. Recent advances
in the genetics of plant pathogenic
fungi. Annu.R ev. P hytopathol. 12:33153
Williams, C. A., Wilson, J. F. 1966.
Cytoplasmic incompatibility reactions
in Neurospora crassa. Ann. NY Acad.
Sci. 129:853-63
Wilson, J. F., Garnjobst, L., Tatum,
E. L. 1961. Heterokaryon incompatibility in Neurosporacrassa microinjection studies. Am. J. Bot. 48:299-305
Zambino, P. J., Harrington, T, C.
1990. Heteroka~osis and vegetative
compatibility
~n Leptographium
wageneri. Phytopathology 80:1460-69
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.
Annu. Rev. Phytopathol. 1993.31:127-150. Downloaded from arjournals.annualreviews.org
by Washington State University on 02/25/09. For personal use only.