PROTOPLASMIC INCOMPATIBILITY AND CELL LYSIS IN
PODOSPORA ANSERZNA. I. GENETIC INVESTIGATIONS ON
MUTATIONS O F A NOVEL MODIFIER GENE THAT SUPPRESSES
CELL DESTRUCTION
JACQUES LABARERE
AND
JEAN BERNET
Laboratoire de Gine'tique, Universiti de Bordeaux 11,
A U e des Facultis, 33405 Talence, France
Manuscript received February 22, 1977
Revised copy received June 15, 1977
ABSTRBCT
In Podospora anserina, protoplasmic incompatibility (a phenomenon that
prevents heterokaryon formation because of the destruction of the fused cells)
can be studied in homokaryotic strains that combine nonallelic incompatibility
genes or carry mutations at the lys loci. In these strains cell destruction occurs
early in development and is associated with an arrest of growth.-From the
self-lysing strains ZysA(1) and RI.' ( R and V are nonallelic incompatibility
genes) mutations have been selected that suppress the self-lysing trait, i.e.,
that prevent cell destruction and remove growth inhibition. Some of them were
derived from a novel modifier locus, modC, located near the mating-type
locus.-In C / D and C / E iccompatibility systems, modC mutations, which per
se have no obvious effect, were considered i n addition to mutations i n the previously identified modifier loci, modA and modB. The demonstration of a
functional interdependence among the three mod genes suggested that modC
is not the structural gem for the protease associated with cell lysis, but is
involved, like modA and modB, in its control.-All three modC mutant strains
investigated exhibit defects i n the formation of protoperithecia, suggesting that
the modC gene function is essential to the occurrence or development of the
female organs. This is the third argument that supports the hypothesis
(BOUCHERIE,BBCUERET
and BERNET1976) that protoplasmic incompatibility
and female organ formation might be related phenomena.
I N Podospora anserina protoplasmic incompatibility due to the interaction
between nonallelic incompatibility genes is accompanied by the synthesis of
novel proteins, especially two proteolytic enzymes, proteases I11 and IV, suspected of being responsible for the phenomenon of cell destruction following the
fusion of cells of unlike genotypes (BBGUERET1972,1973; BBGUERETand BERNET
1973). Five nonallelic incompatibility systems were found in this fungus, of
which three, CJD, CJE and R/V, came from an investigation of 16 geographical
races (BERNET
1965,1967). Two additional systems, F/G and K J L , were derived
from mutations induced in a wild-type strain (DELETTRE
and BERNET
1976).
Protoplasmic incompatibility can be observed in the homokaryotic strains CD;
CE and RV that combine nonallelic incompatibility genes. In these strains proGenetics 87: 249-257 October, 1977.
250
J. LABARERE A N D J. BERNET
tease deregulation is expressed in the form of an arrest of growth early in development and in the phenomenon of cell destruction that spreads into the thallus
(BERNET1965). Self-lysing (SL) strains, similar to the previous ones, were
obtained from defective mutations in two genes, ZysA (B~GUERET
and L A B A R ~ R E
1971) and ZysB (DELETTRE
and BERNET1976).
SL strains were the sources of mutations called mod mutations, selected on the
basis of the suppression of the self-lysing trait. Mutations of the gene modA
were screened by growth restoration of SL strains (BELCOURand BERNET1969).
SL genotypes to which are added the mutation modA(1) exhibited a continuous
growth and displayed the so-called MSL (“modified self-lysing”) phenotype.
They differ from the wild type in their inability to grow at 11O , a cold-sensitivity
phenomenon that was shown to be the result of the synthesis of a protease
(BOUCHERIE,
DELETTRE
and BERNET1976). The mutations of the modifier gene
modB (BERNET1971) were screened by suppression of the cold sensitivity in
MSL strains (BOUCHERIE
and BERNET1974).
Investigations carried out on the modA and modB genes led us to postulate
that they were not the structural genes f o r protease I11 and IV. The gene modA,
whose product was shown to be dihydrostreptomycin sensitive (BERNET,
BBGUERET and LABAR~RE
1973), was postulated to be a ribosome associated
factor essential for the synthesis of protease 111 (BOUCHERIE.
B~GUERET
and
RERNET 1976). The gene modB was proposed to be a repressor gene controlling
and BERNET
the translation of the protease IV messenger (BOUCHERIE,DELETTRE
1976). Thus, the selection of mutations by growth restoration from self-lysing
strains provides a powerful means of investigating the genetic factors involved in
protease regulation.
Extensive selection for mod mutations has been performed on the self-lysing
strains CD, CE and RI/ (BELCOUR
1969; B~GUERET
1973). This paper deals with
mod mutatians screened from the SL strain RI/ and ZysB(1) that reveal a novel
locus, modC, whose function has been investigated in comparison with that
already demonstrated for the genes modA and modB.
MATERIALS A N D M E T H O D S
Podospora anserina is an heterothallic Ascomycete whose life cycle closely resembles that of
Neurospora crassa. Asci contain fcur spores that include the two products of a half tetrad.
Binucleated spores provide the heterokaryotic strains used for dominance and complementation
tests. In about five percent of the asci, one spore is replaced by two uninucleated spores that give
rise to the homokaryotic sei€-sterile (+or -) strains needed to perform appropriate crosses and
for F, genetic analysis. For details see ESSER(1969).
“Barrage” and protoplasmic incompatibility: The term “barrage” designates an unpigmented
area formed on the confrontation line between tw9 strains. In the barrage area, mixed cells
formed by the fusion of hyphae from different strains are deqtroyed by a lysis reaction (RIZET
and SCHECROUN
1959; BERNET1963) called protoplasmic incompatibility.
lncompztibility genes, nomenclature: In the R/V nonallelic incompatibility system, incompatibility genes are represented by capital letters because only m e incompatibility gene is
known at both the r and U loci. At the c, d and e loci, which give rise to the C / D and C / E
systems, studies of 16 geographical races called ( A ) , ( B ) , (C), etc., revealed allelic series
(BERNET
1965, 1967) : c(s), d ( A ) and e ( F ) designate genes c, d and e from the geographic races
CELL LYSIS IN
25 1
Podospora anserina
(s), ( A ) and ( B ) . To simplify nomenclature, capital letters, C, D and E are used only when
incompatibility genes are involved in nonallelic intcractions.
Self-lysing ( S L ) strains: In SL strains, growth stops early in development and the cells lyse
as the consequence of the presence of incompatibility genes (strains CD, RV, etc.) or of a mutation in the genes ZysA and ZysB (BERNET1965; BBCUERET
and L A B A R ~ 1971;
R E DELETTRE
and
BERNZT1976).
Modified self-lysing ( M S L ) strains: They are SL strains in which the self-lysis trait is suppressed by the mutation modA(1) of the modifier gene modA (BELCOUR
and BERNET1969). MSL
strains exhibit a continuous growth, but are distinguishable from normal or wild-type strains
because of (1) the absence of protoperithecia, ( 2 ) defects i n the pigmentation pFocess, ( 3 ) cold
sensitivity, and (4)the presence of a barrage in canfrontation with normal strains, whatever the
genotype of the latter (BELCOUR
1969; BZRNET,BBGUERET
and ~ B A R ~ R1973).
E
Heterokaryons: For balanced heterokaryons two complementing riboflavine-requiring mutations ribA(1) and ribB(1) were used. Heterokaryotic strains result from the germination of
binucleated spores or are formed by anastomosis of homokaryons.
Selection procedure: The self-lysing strains RV and lysB(1) were cultured on cellophane pads
deposited on natural medium supplemented with dihydrostreptomycin. This antibiotic confers conRE
After 48
tinuous growth to SL strains and suppresses cell lysis (BERNETand L A D A R ~1969).
hr of culture, mycelias were UV mutagenized and returned 12 h r later to standard medium on
which grawth completely stops and most of the cells lyse Revertant strains were isolated from
sectors i n which growth resumes.
,@phenyl pyruvic acid (MERCK), a protease inhibitor, was used to protect the cells of SL
strains against destruction at a dose (0.C2 M ) that does not affect growth of a normal strain
(B~GUERET
1973). It was shown that ,&phenyl pyruvic acid inhibits proteases I11 and IV that
are suspected of being responsible for cell disintegration (DELETTRE
1976).
RESULTS
A. Mutations at the modC locus
The mutations were screened on the basis of growth restoration to self-lysing
strains of genotype RV and lysB(1) after two days of culture on dihydrostreptomycin supplemented medium and mutagenesis by UV light.
1 . Mutations derived from thE RV strain: Revertant strains recovered from the
strain RV were studied for the presence of a barrage and the formation of a stable
heterokaryon in combination with three reference strains : the normal strains
TABLE 1
Main features of the revertnnt strains recovered b y growth restoration from the
self-lysing RV strain
Number of strains
Class 1
Class 2
Class 3
947
73
2
Presence of a barrage’ and formation
of a heterokaryon+ with strains of genotype
rV
Ru
RV modA(1)
N,Het+
1,HetI, Het-
1,Het
1,HetI, Het-
&Het
N,Het+
N, H e t
Mutated gene
R
modA
modx
* The presence o r the absence of a barrage in strain confrontation is indicated by the letters I
(Incompatibility) and N (Normal confrontation line).
The functional allelism of the mutation restoring growth was determined by the formation
of a prototrophic mycelium resulting from the mixing of a revertant strain auxotrophic because
of the mutation ribA(1) and the reference strains that carried the mutation ribB(1). Het+ o r
Het- indicated whether the heterokaryon succeeded o r failed.
+
252
J. LABARERE A N D J. BERNET
rV and Rv and the MSL strain, RV modA(1). On the basis of these observations,
the mutant strains can be separated into three classes (Table 1 ) . In class 1,
mutations conferring growth were mutations in the gene R. In class 2, the
revertants exhibited MSL phenotype and were compatible with the MSL strain
RV modA(l), both in strain confrontation (absence of a barrage) and in the
formation of a stable heterokaryon. It was clear that they arose from a mutation
in the gene modA. The two mutant strains in class 3 were MSL strains since a
barrage was formed only when they were confronted with the normal strains
rV and Rv. They differed from strains in class 2 because they failed to f o r m an
heterokaryon when they were mixed with the MSL strain RV modA(1). From
these results it might be postulated that the two revertant strains MSL 1 and
MSL 2 in class 3 arose from recessive mutations in one or two genes modx
different from modA.
In order ta investigate these hypothetical modx mutations, strains MSL 1 and
MSL 2 were crossed with a reference strain rV. SL strains were found in the
progeny of each cross, in addition to strains exhibiting the parental MSL phenotype and carrying the mating type allele of the strains MSL l and MSL 2. This
suggested that the mutations modxl and modx2 responsible for the phenotypes
MSL 1 and MSL 2 were linked to the mating-type locus. Half of the normal
strains in both progeny exhibited female sterility due to a complete absence of
protoperithecia. Since most of the female sterile strains displayed the mating
type of the MSL parent, it was deduced that female-sterile strains carried the
mutant gene modxl o r modx2.
The results in Table 2 also suggested that the mutations modxl and modx2
were allelic because both mutations were linked to the mating-type locus. Since,
as seen above, modxl and modx2 were recessive mutations, allelism can be determined by testing for the formation of a stable heterokaryon including MSL 1 and
MSL 2 nuclei. Indeed, a prototrophic heterokaryon was formed by combination,
on minimal medium, of the homokaryotic auxotrophic strains RV m d x l ribA ( I )
and RV m d x 2 ribB(1). This indicated that the m d x mutations derived from a
single gene, which we called mode. Henceforth, modxl and modx2 are designated modC(1) and modC(2).
TABLE 2
Results from the crosses between the reuertant strains M S L I and M S L 2 (RV modx)
carrying the mating-type allele (+)and a standard strain rV (-)
Wild type
Mating type
MSL 1
MSL 2
Genotypes
(+)
(-1
3 4 5
2
58
rV modx+
Female sterile
(+)
51
45
(-)
2
3
rV modx
MSL strains.
SL strainst
(+)
(+)
45
42
(--)
I
0
RV modx
3
(-)
56
2 4 4
RV m&+
* Normal strains and MSL strains were distinguished on the basis of a barrage formation in
confrontation with wild type and MSL strains (see MATERIALS AND METHODS).
) T h e mating type of the self-lysing strains was determined at 32", a t which temperature
the RV strains exhibit the wild-type phenotype (LABAR~RE
1973) and produce microconidia.
CELL LYSIS IN
253
Podospora anserina
2. Mutatiorrs derived from the self-lysing strain lysB (1) : The mutant strain
ZysB(1) was the only self-lysing strain in which growth restoration at 26'
required, in addition to m o d A ( l ) , a mutation in the gene modB (DELETTRE
and
BERNET1976). Most of the revertant strains that we screened by growth restoration from the strain ZysB(1) exhibited a wild phenotype, indicating that they
arose from a true reversion or an additional mutation at the ZysB locus. One
revertant strain, of more than five hundred examined, displayed the MSL phenotype. The results in Table 3 indicate that this MSL strain resulted from the
mutation of a single gene that is closely linked to the mating-type locus. This
modx3 mutation was clearly responsible for a reduction in the number of protoperithecia to 150 protoperithecia per cm2 as compared with more than 1000 for
a normal strain.
These results suggested that the modx3 mutation might be a third mutation
of the gene modC. This was demonstrated by the formation of a prototrophic
heterokaryotic strain between the MSL strain ZysB(1) modx3 carrying the auxotrophic mutation ribB(1) and the MSL strain RV modC(1) ribA(1). Under the
same conditions, no heterokaryon was formed when the second strain was the
MSL strain RV modA(1) ribA(1). These results showed that m o h 3 is a recessive mutation of the gene modC, which we henceforth call modC(3).
It was not possible to investigate the effect of the first two mutations, modC(1)
and modC(2), on the self-lysing mutation ZysB(1). The double mutant strain
modC ZysB could not be made because the strains carrying the mutations modC
or the mutations Zys were female sterile. The mutation modC(3), derived from
the reversion of lysB(1) was tested for its effect on the R/V system. It showed no
obvious effect since strain RV modC(3) exhibited the SL phenotype.
B. The modC mutations in the C/D and C/E systems
Each m d C mutation was investigated in an attempt to determine whether its
suppressing effect on protoplasmic incompatibility induced by the R/V interaction (or by the ZysB(1) mutation) also extended to the C/O and C / E incompatibility systems. Crosses were performed in order to introduce the mutations
modC into three referenced self-lysing genotypes: c(s) d ( A ) for the C / D system
and c ( A ) e ( F ) and c(s) e ( A ) for the C / E system.
TABLE 3
Progeny of the cross between the revertant M S L strain recosuered b y growth restoration
from the self-lysing strain lysB(1) and a normal strain ( l y B + )
Normal strains
Strains with reduced
female fertility
Wild type
Mating type
Number of strains
Genotypes
(+I
(-)
1
32
lysBf modxf
(f)
(-)
38
2
LysBf modx
MSL strains'
(-1
29
3
lysB(1) modx
(+I
SL strainst
(+I (-1
2
34
lysB(1) m o d d
* Parental MSL strain was of the (+)mating type.
-f The mating type was determined after growth cm dihydrostreptomycin supplemented
medium.
J. LABARERE A N D J. BERPU-ET
254
TABLE 4
Progeny of the crosses between the strain c(A) e(A) (-) used as female parent and c(F) e(F)
strains carrying the mutations modC (I), modC (2) or modC(3)
Wild type
Mating type
Cross involving
Genotypes
(+)
modC(1)
modC(2)
modC(3)
ce
modC
3
4
2
(-1
57
61
38
c(A) e(A)
0 ) e(F)
or c ( F ) e ( A )
modC+
Female sterile
(+)
50
68
41
(-)
4
5
2
c(A) e ( A )
c ( F ) e(F)
or c ( F ) e(A)
modC(x)
Growth on
dihydro- ,
strep tomycln
medium
( f ) (-)
1
2
0
18
28
12
No growth on
dihydrostrept.>mycin
medium
Undetermined
16
22
14
c(A) 4 F )
c(A) e(F)
modC+
modC(x)
The results were identical for all three interactions tested. For this, we present
the data drawn only from investigations in the c ( A ) / e ( F ) interaction. The
absence of MSL strains in the progenies reported in Table 4 indicated that the
three modC mutations did not have any obvious suppressing effect on the selflysing genotype c ( A ) e ( F ) . Nevertheless, it was observed that the SL strains,
which represented one-fourth of the progeny, displayed two phenotypes when
grown on dihydrostreptomycin-supplemented meha. Half of the SL strains
exhibited the expected phenomenon of growth restoration and cell lysis suppression produced by this drug on all the known SL strains (BERNETand
LABAR~R
1969;
E DELETTRE
and BERNET1976). These dihydrostreptomycinsensitive SL strains generally exhibited the mating type (-) of the wild-type
parent. Since modC was the only locus linked to the mating-type locus, it could
be concluded that the SL strains whose mating type could not be determined
were (+) strains, i.e., strains carrying the mutant alleles of modC. This suggested that the product of the gene modC participates in the dihydrostreptomycin
sensitivity of the self-lysing process.
Previous resutls showed that the m o d A gene product was responsible for the
dihydrostreptomycin dependence of SL strains (B~GUERET
1973; BERNET,
B~GUERET
and L A B A R ~ 1973).
RE
I n order to investigate a possible interaction
between the products of the genes m o d A and modC, strains C E m o d A ( 1 )
modC(x) were constructed f o r comparison with the SL strains CE or C E m o d C ( x )
and with the MSL strain CE modA(1). These four strains were obtained as
progeny of the cross 0 c ( A ) e ( A ) mcEdA(1) (-) x 8 c(F)e(F) modC(1) (+).
In the progeny, the MSL strains accounted for about one-sixteenth of the total
and predominantly (18 in 19) exhibited the mating type (-) of the modC+
parent. From this, it could be deduced that the MSL strains in the progeny carry
the wild-type gene mode+ and that the MSL phenotype resulted from the presence of the mutation m o d A ( I ) .
Thus, it might be suspected that the strains CE m o d A ( 1 ) modC(1) would
display the SL phenotype. This led us to examine carefully all the self-lysing
CELL LYSIS IN
255
Podospora anserina
TABLE 5
Self-lysing strains in the progeny of the cross
(-1 X d c(F)e(F) modC(1)
0 c(A)e(A) modA(1)
Clas3
Number
1
2
3
12
13
16
Growth on medium supplemented with
Dihydro-,
P-phenyl
Mating type
streptomycin
pyruvic acid
(+)
(-)
+-
-
-
'f
-
0
12
undetermined
15
1
(4-1
Genotypes
CE modA+ modC+
CE modA+ modC(1)
CE modA(1) modC(1)
strains in the progeny. These strains could be divided into three classes (Table 5 )
by culture on media supplemented with dihydrostreptomycin or with p-phenyl
pyruvic acid, a protease inhibitor. I n strains in class 1, dihydrostreptomycin
suppressed cell lysis and removed growth inhibition, and P-phenyl pyruvic acid
alone inhibited self-lysis without restoring growth. These are the typical traits
for self-lysing strains CE (LABAR~RE,
BBGUERETand BERNET1974). In class 2,
from the results reported in Table 4, SL strains carry only the mutation m o d e .
SL strains in class 3 exhibited a novel phenotype. They were insensitive to
dihydrostreptomycin and showed suppression by P-phenyl pyruvic acid both in
growth inhibition and in cell destruction. For these strains, the only possible
genotype was CE m o d A ( 1 ) modC(2). Since they produced microconidia on
,8-phenyl pyruvic acid-supplemented medium, it was possible to use them as male
parents and to demonstrate that they really were of the suspected genotype.
Additional crosses were performed to demonstrate a possible interaction
between the products of the genes modC and modB. The first cross differed from
the cross represented in Table 4 by the presence of the mutation m o d B ( 1 ) in the
female parent c ( A ) e ( A ) . As in the preceding cross, no MSL strain was found in
the progeny. Therefore strains CE modB(2) modC(1) were SL strains like
CE modB(2) and CE modC(1).
The second cross differed from the cross reported in Table 5 in that the female
parent c ( A ) e ( A ) carried a mutation in the gene modB in addition to m o d A ( 1 ) .
MSL strains in the progeny exhibited both mating types, suggesting, in this case,
that half of them carried the mutant gene modC(1). Thus, these strains could be
expected to carry the genes CE m o d A ( 2 ) modC(1) modB(1). This was demonstrated by appropriate crosses. These results gave evidence of an interaction
between the products of the genes modC and modB.
DISCUSSION
Studies on the self-lysing strains RV and ZysB(1) have revealed that mutations
in a novel modifier gene m o d e , a gene closely linked to the mating-type locus,
suppressed the growth inhibition and the reaction of cell disintegration resulting
from the interaction of the nonallelic incompatible genes R and V or from the
mutation lysB(1).
None of the three modC mutations investigated suppressed protoplasmic
256
J. LABARERE A N D J. BERNET
incompatibility induced as the consequence of nonallelic interaction in the
incompatibility systems C / D or C/E. This results suggested that the gene m o d e
was not, in spite of the recessiveness of the “Emutations, the structural gene
f o r the protease responsible for cell destruction.
Previous results (LABAR~RE,
B~GUERET
and BERNET1974) showed that interaction between nonallelic incompatibility genes stopped protein (and RNA)
synthesis in addition to inducing the proteases mentioned above. Defective mutations in m o d A and m o d e reversed these two consequences, since in RV strains
they restored growth and suppressed cell destruction. These results lead us to
postulate that in the R/V system the genes m o d A and m o d e play, along with the
R/V interaction, the role of co-inhibitor in protein (and RNA) synthesis and
the role of co-factor in the induction of specific proteases. Differences between
m o d A and m o d e lie in the fact that the gene m o d A exerts such a role in all
nonallelic systems known until now (DELETTRE
and BERNET1976).
Investigations on m o d e mutant strains revealed defects in the process of
protoperithecia formation, defects that were responsible in two cases f o r complete
female sterility. This was the third observation supporting our previous hypothesis that there is a relationship between protoplasmic incompatibility and protoperithecia formation (BOUCHERIE,
B~GUERET
and BERNET1976). Mutant strains
m o d A or modB exhibit complete female fertility. Female sterility was observed
only in the double mutant strains m o d A m d B (BERNET1971). These results
suggested that the process of protoperithecia formation may be inhibited either
by a mutation in the m o d e gene or by a mutation in both genes m o d A and modB.
As mentioned above, the m o d e mutations, contrary to m o d A and modB mutations, exhibited no suppressing effect on the self-lysis reaction induced by nonallelic gene interactions in the C / D and C/E systems. The addition of a modC
mutation to the MSL genotype CE m o d A ( 1 ) resulted in a SL strain. Investigations on the SL strain CE m o d A ( 1 ) modC(1) showed that it differed from the
SL strains CE m o d C ( l ) , because the former and not the latter exhibited growth
on a &phenyl pyruvic acid-supplemented medium. This suggested that in a
strain CE m o d A ( 1 ) modC(I), arrest of growth was only a secondary effect that
might result from the activity of a protease induced by the C / E interaction. This
protease was under the control of the gene modB since the addition of the
modB(1) mutation to the genotype CE m o d A ( 1 ) modC(1) resulted in a MSL
strain. These results can be interpreted only if some kind of interaction is postulated between the products of the genes modC and modB.
Thanks are due to MRS.B. RICARD
for reading and correcting the translation of the manuscript. This work is partly supported by the Centre National de la Recherxhe Scientifique
(E.R.A. 485) and the Institut National de la SantC et de la Recherche Mkdicale.
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Corresponding editor: R. L. METZENBERG