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Sexuality in the Cellular Slime Mold Dictyostelium Giganteum (Meiosis/Mating Types/Self-Incompatibility/Macrocysts) GREGORY W

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Sexuality in the Cellular Slime Mold Dictyostelium Giganteum (Meiosis/Mating Types/Self-Incompatibility/Macrocysts) GREGORY W Proc. Nat. Acad. Sci. USA Vol. 72, No. 3, pp. 970-973, March 1975 Sexuality in the Cellular Slime Mold Dictyostelium giganteum (meiosis/mating types/self-incompatibility/macrocysts) GREGORY W. ERDOS, KENNETH B. RAPER, AND LINDA K. VOGEN Departments of Bacteriology and Botany, University of Wisconsin, Madison, Wisc. 53706 Contributed by Kenneth B. Raper, December 23, 1974 ABSTRACT By pairing of strains of Dictyostelium MATERIALS AND METHODS giganteum in various combinations this species was shown to be heterothallic. Four mating types were iden- Most of the cultures of Dictyostelium giganteum were obtained tified. Some strains could not be assigned a mating type from Mr. John Sutherland, formerly of this laboratory, and and others showed no mating reaction. No self-compatible were isolated by him from various prairie habitats in Wiscon- strains were found. Mutations were introduced in several strains and genetic crosses were performed. The results of sin. Others were obtained from the collection of cellular slime these crosses show that mating and macrocyst formation molds assembled and maintained in this laboratory. Stock are controlled by a single locus-multiple allele incom- cultures were maintained on phosphate-buffered 0.1% lactose/ patibility system. The results also support the view that 0.1% peptone agar, pH 6 (7) in association with the food the myxamoebae that emerge upon germination of the Forty-two different macrocysts are the products of meiosis. bacterium, Escherichia coli strain B/r. isolates were tested for their mating type by pairing them in In the cellular slime molds the macrocyst is a developmental various combinations according to the procedure described in alternative to the sorocarp. Macrocyst formation begins with earlier studies (4). Three isolates were selected for further the development of a large cell that increases in size as it genetic analysis: WS-588, WS-589, WS-606. Mutations were ingests surrounding myxamoebae (1, 2). Prior to their in- induced in these strains by means of N-methyl-N'-nitro-N- gestion the associated myxamoebae have formed the loose, nitrosoguanidine according to the method described by Weber fibrillar primary wall. The ingested myxamoebae are con- and Raper (8). After exposure to the mutagen myxamoebae tained in vacuoles of the enlarging macrocyst protoplast. were resuspended in liquid medium (9) and allowed to grow When ingestion is complete, the single large cell forms a rigid to a concentration of 106 cells per ml. They were then spread secondary wall and a more flexible, trilaminar tertiary wall on solid media containing 250 /Ag/ml of cycloheximide at (2). As the macrocyst matures the ingested amoebae are concentrations of 103 to 106 cells per plate. Resistant strains fragmented into smaller and smaller bodies until they are arose as plaques in the lawn of concurrently inoculated completely digested, giving the cyst a homogeneous ap- bacteria. Cells were also spread on nonselective media at 10 to pearance. After an appropriate period of maturation, the time 20 cells per plate and clonal isolates were tested for tempera- varying with the species, the protoplast of the macrocyst ture sensitivity at 270. cleaves into myxamoebae which escape when the walls break Mutant strains were crossed among themselves and with (3). wild-type strains. Crosses were made by techniques previously described for macrocyst formation in D. discoideum (4). s adgeinth celllar sim mldomeirom a ultrastructural Germination of the macrocysts was attempted after 5-6 weeks studyofsuch cyn oetI,where late of incubation. The macrocysts were removed from the plates in development meiotic chromosomes were observed (2). It and washed three times in a solution containing 250 ,g/ml of was also shown that the large cell of the nascent macrocyst was streptomycin sulfate. They were then resuspended in sodium at first binucleate but became uninucleate by the time in- dodecyl sulfate (0.0125%) and shaken for 2 hr, after which the gestion of the adjacent myxamoebae began. These facts in- cysts were again washed three times in the streptomycin solu- dicated that the macrocyst protoplast arose from the fusion of tion followed by 2 hr shaking in 0.7% EDTA. After three two cells followed by nuclear fusion and subsequent meiosis,\ more washes in streptomycin solution the macrocysts were thus making the giant cell a zygote. \\ spread on nonnutrient agar containing 250 ,/g/ml of strepto- It has been shown that there ar heterothaliic as ie 1 as mycin sulfate. This method was devised (10) to eliminate homothallic forms. This was first demonstrated in Dictyo- contamination of the germination plates by bacteria, fungi, stelium discoideum (4), where three intercompatible mating and extraneous slime mold spores and myxamoebae that may types were identified. Later, other species were also shown to have remained. Plates were examined daily for contamination have heterothallic forms (5). The heterothallic nature of by myxamoebae that were not the product of germination. If Dictyostelium giganteum Singh (6) is the subject of this report. such contamination was found the plates were discarded. This species is a member of the Dictyostelium mucoroides com- After 3 days in a lighted incubator at 250 the macrocysts plex and is characterized by strongly phototropic sorocarps began to germinate. that have long sinuous stalks bearing large, white sori con- Progeny were recovered by using a sterile needle to pick sisting of propagative spores. The mating system of this up individual sorocarps that had arisen from single macro- species as well as some preliminary genetic analyses are cysts. (Each germinated macrocyst generally yields one small presented here. sorocarp.) The source of each sorocarp was confirmed micro- 970 Downloaded by guest on October 1, 2021 Proc. Nat. Acad. Sci. USA 72 (1976) Sexuality in Dictyodelium 971 TABLE 1. Macrocyst production from pairings of TABLE 2. Results of progeny analysis in crosses between single the four different mating types mutant strains and wild-type strains* WS-589 WS-606 WS-607 WS-588 Al cycD X A2 cycD+ Al tsgA + X AS tsgA Al AS AS A4 + WS-598 cycD cycD+ Total tsgA tsgA Total Al _ + + + Al 33 27 60 Al 26 19 45 WS-606 AS 21 28 49 AS 27 27 54 AS + - + + Total 54 55 109 Total 53 46 99 WS-607 x2 = 2.66, P = 0.5 (3 df) x2 = 1.8, P = 0.65 (3 df) AS + + - + for a 1:1:1:1 segregation. fo. a 1:1:1:1 segregation. WS-588 A4 + + + AS cycC+ X A4 cycC AS tsgA X A4 tsgA+ cycC+ cycC Total tsgA tsgA + Total scopically. The spores from each sorocarp were suspended in A2 32 39 71 AS 28 33 61 0.6 ml of a heavy bacterial suspension in distilled water. The A4 32 34 66 A4 29 25 54 spore suspension was divided equally among five tubes, each Total 64 73 137 Total 57 58 115 containing 2.5 ml of molten (450) growth medium with 0.7% XI = 0.95, P = 0.8 (3 df) x2 = 1.24, P 0.75 (3 df) agar. These were quickly agitated and poured over plates of for a :1:1:1 segregation. for a 1:1:1:1 segregation. solid growth media. Clonal isolates appeared after 3 days at 250 as clear areas in the soft agar where they had consumed * Numbers presented in table represent macrocysts analyzed. the bacteria. These isolates were then subcultured and tested df = degrees of freedom. for mating type and mutant characteristics. In later experi- ments (see Results) spores from sorocarps were subcultured clones that emerged from any one macrocyst were genetically directly without clonal isolation. alike but that among the total macrocyst progeny all possible RESULTS combinations of markers could be observed in each cross. For this reason clonal isolation was later abandoned and spores Of the 42 isolates tested, four mating types (Al, A2, AS, and from sorocarps were subcultured directly in order to determine A4) could be clearly identified among 17 of them. The mating the identity of a given macrocyst. In the accompanying tables types are self-incompatible and each one is cross-compatible each number represents macrocysts analyzed, their identity with any of the other three types (Table 1). Seven strains being established by either clonal isolation or direct subculture showed inconsistent or aberrant patterns in their mating re- methods. In all, some 1400 macrocysts have been germinated actions and could not be assigned to any of the four mating and analyzed; a portion of this analysis is the subject of this types. Neither did the results justify designation of additional report. mating groups to accommodate them. Sixteen strains showed The results of the crosses performed are presented in Tables no mating reaction under any of the circumstances investi- 2-4. In those crosses where only one of the parents carries a gated, nor were any self-compatible (homothallic) strains mutant marker (Table 2), random segregation of the mating of D. giganteum observed. type and the mutant gene is observed among the progeny in Three strains were selected for further genetic analysis: each case, and thus recombination between mating type and WS-589 (Al), WS-606 (A2), WS-588 (A4). With mutants mutant gene was established. These data are consistent with derived from these strains crosses were performed. Mutants the expectation that a typical meiotic process is operating. cycC and cycD are resistant to cycloheximide at 250 /Ag/ml in There is no evidence that mating type is closely linked to any solid media and are otherwise developmentally normal. The of the mutant loci studied. When these same mutant strains tsgA mutant is temperature sensitive in failing to grow at 270, are crossed with each other (Tables 3 and 4), mating type but it develops normally at 22.50.
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