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Biological Research

versión impresa ISSN 0716-9760

Biol. Res. v.33 n.1 Santiago  2000 

Characterization and mapping of an informational suppressor in Aspergillus nidulans


State University of Maringá, Department of Cell Biology and Genetics, Maringá, Paraná, Brazil


The present work was undertaken to characterize a suppressor gene present in a mutant strain of A. nidulans obtained with NTG (N-Methyl-N'-Nitro-N-Nitrosoguanidine). Analyses of this mutant have shown that this suppressor, designated suO1, induces phenotypic co-reversion of several auxotrophic mutations and makes the strain sensitive to aminoglycoside antibiotics and lower temperatures. suO1 has shown to be on linkage group VIII. The vegetative growth of the mutant strain is very unstable because the suppressor gene induces the production of prototrophic mitotic sectors. The strains bearing the suO1 gene produce cleistothecia containing a reduced number of viable ascospores during the sexual cycle. The segregation of the genetic markers has also been observed in the mutant strain self crossed. From the above results it may be concluded that suO1 is an informational suppressor.

Key words: Aspergillus nidulans, barren cleistothecia, informational suppressor, paromomycin.


Mutations in genes that codify the macromolecules participating in the process of protein synthesis may impair the fidelity of the translation process, changing the expression of any other gene in the genome of the cell (10, 27, 33). Such mutations are defined as informational suppressors since they may recover the cell's wild type phenotype when present in the genome with other mutations in structural genes (4, 12, 13, 19).

Previous papers have shown that the ribosomes are involved in the gene suppression event because they are completely involved in assuring the fidelity of the translation process (6,11). Ribosomal mutations may hinder the linking of tRNA to the functional ribosome or may weaken the codon-anticodon association during translation (17). Both alterations lead to mistakes in the reading of the mRNA triplets, thereby allowing the occurrence of gene suppression (6, 15).

In S. cerevisiae, proteins S28 and S4 of the smaller ribosomal subunit interact to control translation fidelity. Mutations in genes that codify these proteins lessen translation fidelity and give strains sensitivity to paromomycin (26).

Informational suppressors were described in prokaryotes and in many lower eukaryotes: Podospora anserina (29), Coprinus lagopus (25), Aspergillus nidulans (14, 31), Saccharomyces cerevisiae (22) and Neurospora crassa (23). A high percentage of these suppressors codify altered ribosomal proteins that develop alternative possibilities to translate the same triplet (1,8, 16, 26).

On the other hand, mutations in genes that codify proteins associated with ribosomes may imitate the effects of an informational suppressor (35). Gene Sup35, described in S. cerevisiae, codifies a 76.5 KD protein (Sup35p), whose C-terminal domain shows similarity to the EF-1a elongation factor (7). Mutations in this gene and its super-expression reduce translation fidelity and show the effect of an omnipotent suppressor (24).

In Podospora anserina, genes su1 and su2 codify proteins homologous to proteins eRF3 and eRF1 of S. cerevisiae respectively. Gene su1 deletion is lethal in P. anserina. Reduction of its expression confers upon the strains the ability to suppress nonsense mutations, while its over-expression leads to an anti-suppressor phenotype (9).

In A. nidulans, ribosomal suppressors were identified by their effects on the growth and morphology of colonies and because suppressed strains showed a great sensitivity to aminoglycoside antibiotics (21). In these mutants blockage of sexual reproduction and the reduction of viability of asexual spores were related to the presence of ribosome suppressors in the genome of the cells (3).

Paromomycin is an aminoglycoside antibiotic that causes in vitro (5) and in vivo (28) mistranslation. Auxotrophic mutants of A. nidulans bearing ribosome suppressors exhibit hypersensitivity to paromomycin (20). These strains also show growth sensitivity at 20º C. These mutants could also be defective in ribosome assembly (3).

This research reports the identification of a new suppressor mutation (suO1) in A. nidulans, which was obtained after NTG (N-metil-N'-nitro-N-nitrosoguanidine) treatment of the A288 master strain. The suppressor strain showed co-reversion of alleles in physiologically unrelated genes. The susceptibility of the suO1 mutant to paromomycin and cold temperature and the ability of suppressor strain to form barren cleistothecia have been reported. Data suggest that suO1 is an informational suppressor, probably associated with the control of translation fidelity.


Strains. The A. nidulans strains were derived from Utrecht stock (UT448, UT196) and FGSC (A610, A288, G351). The M-15 mutant strain was derived from the A288 master strain after NTG (N-metil-N'-nitro-N- nitrosoguanidina) treatment. The methA strain is a mitotic segregant derived from the UT448//UT196 diploid strain.

Genotypes of the mutant and master strains

M-15: wA3 (II), white conidia; adE20 (I), yA2 (I); pyroA4 (IV); nicB8 (VII); riboB2 (VIII), with requirements for adenine, pyridoxine, nicotinamide and riboflavin, respectively; sB3 (VI) with sulphate transport impairment; galA1 (III), facA303 (V), unable to grow on galactose and ammonium acetate as the sole carbon source; suA1adE20, suppressor of adE20 (specific for this ad allele); suO1 (VIII), informational suppressor.

G351: fwA1 (VIII), fawn conidia, pabaA1(I), with requirements for p-aminobenzoic acid; alx4 (III), lack of utilization of allantoin as nitrogen source; suaA101 (III) allele specific suppressor; sB3 (VI), sulphate transport impairment; alcR125(VII) lack of utilization of ethanol as sole carbon source.

A610: yA1 (I) yellow conidia; pabaA1 (I), with requirement for p-aminobenzoic acid.

UT448: wA2 (II) white conidia; riboA1, pabaA124, biA1 (I), with requirements for riboflavin, p-aminobenzoic acid and biotin, respectively; AcrA1 (II) resistant to acriflavin.

UT196: yA1 (I) yellow conidia; methA17 (II), pyroA4 (IV), with requirements for methionine and pyridoxine, respectively.

methA: yA1 (I) yellow conidia; methA17 (II), with requirement for methionine.

A288: wA3 (II), white conidia; adE20 (I), yA2 (I); pyroA4 (IV); nicB8 (VII); riboB2 (VIII), with requirements for adenine, pyridoxine, nicotinamide and riboflavin, respectively; sB3 (VI) with sulphate transport impairment; galA1 (III) and facA303 (V), unable to grow on galactose and ammonium acetate as the sole carbon source; suA1adE20, suppressor of adE20 (specific for this ad allele).

Culture Media. The complete medium (CM) and minimal medium (MM) were used as described by Van de Vate and Jansen (34). The selective medium (SM) was supplemented MM according to the requirements of each strain. The solid medium contained 1.5% agar. Incubation was performed at 37º C.

Mutagenesis. 5 x 106 conidia/mL of the A288 strain were added to small vials containing NTG solution to give a final concentration of 1.0 mg NTG/mL. The suspension was shaken at 37º C for 2 h before plating. A control was prepared with the same conidial concentration. Samples of both suspensions (control and treatment) were collected to determine the number of viable conidia through dilution.

Mutant selection. Mutagenized suspension at appropriated dilution was spread on CM and the colonies grown after 48 h of incubation at 37º C were transferred to supplemented MM, each time separately, without riboflavin, pyridoxine, sodium sulphate and nicotinamide. They were also transferred to supplemented MM containing galactose or ammonium acetate as the sole carbon source.

Aminoglycoside treatment. Conidia from the M-15 mutant and from their mitotic segregants were inoculated into the center of six Petri plates containing CM plus paromomycin (2.0 mM). The plates were incubated at 37º C for five days. Colony diameters were measured daily for five days and the values observed after treatment were taken as a percentage of the control (growth in antibiotic-free medium). Data were compared by Student's t test at P < 0.05.

Genetic Techniques. The general methodology used was that of Pontecorvo et al. (31). Diploid strains were prepared by Roper's method (32). Mitotic haploidization was carried out spontaneously by growing the diploid strains in plates containing CM for seven days. Two processes were used to select the haploid mitotic segregants for the mapping of the suppressor gene. One was mitotic stability: the sectors isolated from the diploid M-15 // methA strain were inoculated into CM after purification and incubated at 37º C for six days. Only segregants that did not originate new mitotic sectors in CM, exhibiting vegetative stability, were considered as haploid and selected for analysis. The other process used was the exhibition of the pleiotropic effects induced by the suppressor gene: the selected segregants that showed reduced growth and sensitivity to paromomycin and cold temperature were considered suppressor strains. For the analysis of the sexual cycle, the heterokaryons were prepared in liquid MM plus 2.0% CM. Hybrid and self cleistothecia were obtained after transference of the heterokaryons to sealed Petri dishes containing solid supplemented MM in accordance with the requirements of the crossed strains. The plates were incubated for 21 days at 37º C.

Ascospore and conidial viabilities. The number of ascospores per cleistothecium or conidia per mL was determined by counting in a haemocytometer. Ascospore or conidia suspensions at appropriate dilutions were spread on CM and the number of colonies observed after 48 h of incubation at 37º C was compared with the number of ascospores or conidia counted in the haemocytometer at the same dilution.

Cold Sensitivity Assay. Conidia from the M-15 mutant strain and from their mitotic segregants were inoculated in the center of six Petri dishes containing CM. The plates were incubated at 20o C. Colony diameters were measured once a day for four days.


Characterization of M15 mutant

The M-15 mutant was obtained by treating the A288 strain with NTG. The mutant strain is isogenic with the parental strain A288, but shows phenotypic co-reversion of the nutritional mutations of the A288 strain. The M-15 mutant is mitotically unstable and spontaneously produces yellow sectors (y, w+) visible from colonies grown in CM (Fig. 1). These sectors are haploid mitotic variants derived from M-15 mutant and show phenotypic co-reversion of the w (conidial color) and nutritional mutations of M-15. Their phenotypes are w+ (II), galA+ (III); pyroA+ (IV); facA+ (V); sB+ (VI); nicB+ (VII) and riboB+ (VIII).

Figure 1. Mitotic instability of M-15 mutant. Conidia of the mutant strain were inoculated in Petri dishes containing Complete Medium. The plates were incubated at 37º C for four days. The M-15 mutant produces white conidia (y,w), it may spontaneously originate yellow (y, w+) mitotic sectors (arrow). These sectors are produced by phenotypic suppression of w mutation.

Macroscopically, the M-15 mutant forms colonies with many aerial hyphae in their central regions and brown pigment on their backsides.

The mutant strain also shows reduced growth at 37º C and low viability of asexual spores when compared with the A288 parental strain (Figs. 2 and 3). Impairment of the sexual cycle of mutant M-15 was shown by production of cleistothecia with a reduction of viable ascospores in an M-15 x M-15 self cross (Table I). Analyses of self-crossed cleistothecia of the M-15 mutant showed the segregation of the w gene and all their nutritional markers among viable ascospores (Table II).

Figure 2. Growth at 37º C of strains M-15, A288 (control), and mitotic segregants derived from diploid M-15 // methA (strains 1-7). Ordinates, diameter of colonies (mm). Abcissas, time (hours). Height of column represents the mean ( SEM of 6 experiments.
* Significantly different from control at P<0.05 (Student's t test).

Figure 3. Conidial viability (%) of M-15, A288, G351 and 520 strains. Height of column represents the mean SDM of 6 experiments.



Total number of viable ascospores per cleistothecium
Cleistothecia M-15 x M-15 A288 x A288 UT196 x UT196

1 10 2,500 15,3000
2 01 4,380 3,150
3 1650 1,870 3,075
4 19 2,420 6,775
5 3080 2,850 6,000
6 12 1,500 10,2250

Table II

Meiotic segregation of mutant M-15 markers in the M-15 x M-15 cross. Results include analysis of viable progenies of four cleistothecia obtained by crossing.

Genetic Markers
Cleistothecia w ribo pyro sB3 nic gal fac Segregants

1 + + + - + + + 01
  + + + + + + + 01
  + + - + - + + 06
  + - - - + + + 01
  - - - + + + + 02
  - + + + + + + 01
2 + - + - + + + 02
  + - - - + + + 01
  + + + - + + + 01
  - - + + + + + 01
  - - - + + + + 01
3 + + - - + + + 01
  + + - - - + - 43
  - + - + + + + 02
  - + - + - + - 02
  - + - + - - - 01
4 + - - - + + + 04
  + + + - + + + 02
  + + + + + + + 03
  + + - - + + + 01
  + - + - + + + 01
  - + + + + + + 03
  - + - + + + + 02
  - - - + + + + 01
  - - + + + + + 03

When crossing the M-15 mutant with the A288 parental strain, the 1:1 Mendelian segregations were observed for the gal, fac, sB, nicB, and ribo markers. These results suggest that the phenotypic alterations shown by the M-15 mutant result from a change in a single nuclear gene (Table III). The phenotypic co-reversion of all auxotrophic mutations of the M-15 strain in the M-15 x M-15 cross (Table II) could be explained if the M-15 mutant bore a suppressor gene. In the M-15 x UT448 cross approximately 1/4 of the offspring showed the mutant phenotype of M-15 strain for markers facA303, nicB8 and pyroA4. These results lend considerable weight to our premise that the M-15 mutant is a suppressor strain. On the other hand, the absence of suppression of some nutritional markers in the M-15 x M-15 and M-15 x A288 crosses (Tables II and III) and the production of more than 1/4 auxotrophic progeny for the galA and biA genes in the M-15 x UT448 cross (Table III) demonstrate the low efficiency of the suppressor gene. These results and the sensitivity of the M-15 mutant to paromomycin and growth at 20º C (Figs. 4 and 5) suggest the informational character of the suppressor gene, which was named suO1.


Segregation of markers of M-15 mutant in the M-15 x A288 and M-15 x UT448 crosses. The sB3, riboA1 and riboB2 markers were not analyzed in the M-15 x UT448 cross.

Genetic Markers Number of Segregants
  M-15 x A 288 M-15 x UT448

w+ 31 04
w 53 1240
bi+ 84 31
bi 0 97
gal+ 35 87
gal 49 41
pyro+ 0 1050
pyro 84 23
fac+ 39 97
fac 45 31
sB3+ 44 0-
sB3 40 0-
nic+ 40 99
nic 44 29
ribo+ 46 0-
ribo 38 0-

(-) These markers could not be analyzed in this cross.

The pleiotropic effects induced by suO1 (reduced growth and sensitivity to paromomycin and cold temperature) were also observed among the haploid mitotic segregants derived from M-15 // methA diploid strain (Figs. 4 and 5). These segregants were obtained by spontaneous haploidization of the diploid strain in Complete Medium (see Materials and Methods).

Figure 4. Inhibition of growth (%) by paromomycin 2mM of strains M-15, A288 (control) and mitotic segregants derived from the diploid M-15 // methA strain (strains 1-7). Height of column represents the mean ± SEM of 6 experiments.
* Significantly different from control at P<0.05 (Student's t test).

Figure 5. Growth at 20º C of strains M-15, A288 (control) and mitotic segregants derived from the M-15 // methA diploid strain (strains 1-7). Ordinates, diameter of colonies (mm). Abcissas time (hours). Height of column represents the mean ±± SDM of 6 experiments.
* Significantly different from control at P<0.05 (Student's t test).

Recessiveness of suppressor suO1

The suO1 mutation was recessive both in the diploid and in the heterokaryons formed by the mutant M-15 and the master strain UT196. Both were incapable of growth in the absence of pyridoxine.

Mapping by parasexual cycle

Diploid M-15 // methA was haploidized spontaneously in CM, and the mitotic segregants were analyzed phenotypically for the mapping of the suppressor gene (suO1) (Table IV). Analysis of diploid M15 // A610, heterozygous for the pabaA gene was undertaken to analyze chromosome I segregation (Table V).


Phenotypic analysis of the mitotic segregants derived from the M-15 // methA diploid strain.



w meth gal pyro fac sB3 nic ribo

+ - + - + - + - + - + - + - + -
20 03 05 18 11 12 20 03 19 04 16 07 11 12 23 0

Table V

Mitotic segregation of chromosomes I and II from the M-15 // A610 diploid strain.

+ - + -
29 05 09 25

Among the 23 ribo+ mitotic segregants derived from diploid M15 // methA, seven showed pleiotropic effects that characterize the presence of suO1 in their genome: reduced growth and sensitivity to paromomycin and to cold temperature (Figs. 2, 4 and 5). Results determined the segregation of the suppressor in approximately 3 su+: 1 su among the mitotic segregants. Results mapped the suppressing mutation in chromosome VIII (Tables IV and V). The phenotypic segregations of the methA, galA and nicB genes among the mitotic segregants analyzed in Table IV may be justified by the low efficiency of suO1 in suppressing these mutations.


The characteristics of an informational ribosomal-assumed suppressor have been described above. It was named suO1 and isolated by co-reversion of several physiologically unrelated mutations. The suppressor strains were shown to be more sensitive to paromomycin than the su+ parental strain. Assuming that paromomycin is active to stimulate mistranslation in cell-free systems (5), the mode of action of suO1 might be similar to this antibiotic.

Aminoglycoside antibiotics have a particularly important role in informational suppression studies. Two classes of informational suppressors have been characterized in A. nidulans: tRNA suppressor and ribosomal suppressor (19). The tRNA suppressors do not alter the growth rates of the suppression strains; they are semi-dominant in diploids and behave like wild-type control strains in the presence of aminoglycoside antibiotics. On the other hand, the ribosomal suppression strains have altered morphologies and reduced growth rates. Ribosomal suppressors are also recessive in heterozygous diploid strains and render the strains hypersensitive to aminoglycoside antibiotics (19).

The recessive mutations described in A. nidulans and characterized as ribosomal suppressors (suaA and suaC) render the strains cold-sensitive. This effect has been associated with the participation of the product of the suppressor gene in a multimere aggregate (3, 31).

The suppressor strains studied here (M-15 and the mitotic segregants derived from the M-15 // methA diploid strain) exhibited cold-sensitivity, reduction of the growth rates and higher growth inhibition in the presence of paromomycin than in its absence (Figs. 2, 4 and 5). These results make suO1 a putative ribosomal suppressor. The hypersensitive basis of the of M-15 mutant to paromomycin may be the additive effect of two agents, the suO1 mutation and the presence of aminoglycoside, which increase error levels during protein synthesis.

The production of different phenotypic classes in the M-15 x M-15 cross and the lack of phenotypic suppression of some mutations observed among the segregants obtained in the M-15 x UT448 and M-15 x A288 crosses could be due to insufficient synthesis of the gene product. It demonstrates the low efficiency of the suO1 mutation (Tables II and III). These results are in accordance with Gorini (10), who suggested that a viable ribosomal suppressor should have a very low efficiency because it mistranslates a great number of codons. The absence of pyro+ segregants among the progeny of M-15 x A288 cross indicates that the efficiency of the suppression is not the same for the studied markers (Tables II and III).

Experiments thus suggest that the recessive suppressor mutation suO1, mapped in the VIII chromosome of the M-15 mutant, encodes for a component involved in the translation of proteins. The product of suO1 might be a ribosomal protein or a regulatory enzyme that modifies ribosomal proteins (3, 18, 26).

The study of ribosome suppressors in A. nidulans is justified as the fungus shows typical eukaryotic reactions to aminoglycoside antibiotics and since there is a similarity between the translation factors of the fungus and those of mammals (2,21). Further studies of this mutant will prove necessary to provide information about the constitutional or regulatory part of the protein coded by the suppressor gene with regard to the control of translation fidelity.


We are much indebted to Mrs. Luzia A. S. Regasse and Mrs. Sonia A. de Carvalho for their technical assistance. Financial support was provided by CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico). MGM Franzoni is the recipient of a CNPq fellowship. We are especially thankful to God.

Corresponding author: Dra. Marialba Avezum Alves de Castro-Prado. Universidade Estadual de Maringá. Departamento de Biologia Celular e Genética. Av. Colombo 5790. 87020-900. Maringá, Paraná, Brazil. e-mail:

Received: November 4, 1999. Accepted in revised versions: June 7 2000


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