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The Use of DNA Probes for Taxonomic Study of Dictyostelium Wild Isolates

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The Use of DNA Probes for Taxonomic Study of Dictyostelium Wild Isolates Copyright 0 1988 by the Genetics Society of America The Use of DNA Probes for Taxonomic Study of Dictyostelium Wild Isolates William B. Evans, Joanne E. Hughes and Dennis L. Welker Molecular BiologylBiochemistry Program, Department of Biology, Utah State University, Logan, Utah 84322-5500 Manuscript received October 9, 1987 Revised copy accepted March 3, 1988 ABSTRACT The classification of 27 wild isolatesassigned to Dictyostelium discoideum on the basis ofmorphological criteria was reexamined using probes specific for DNA sequences cloned from the type strain NC4. These probes included ones specific for ribosomal spacer DNA regions and for a ribosomal RNA coding sequence, as well as probes for two chromosomal gene families (actin and discoidin) and for the DIRS-1 transposable element. Four isolates (AC4, WS526,WS584 and ZASA)which had previously been shown to have unusual mating characteristics were distinctly different from other isolates. We interpret these differences as indicating that the four atypical isolates represent species other than D. discoideum. Probes for the ribosomal spacer DNA either did not hybridize to the DNA of these four isolates or had decreased levels of hybridization to EcoRI restriction fragments of different lengths to that observed with the type strain. With the discoidin probe, all isolates had DNA fragments that hybridized but AC4, WS526, WS584 and ZASA lacked a pair of fragments that were conserved in NC4 and other isolates. With the actin probe, AC4, WS526, WS584 and ZASA lacked numerous fragments that the other isolates shared with NC4. The DIRS-1 probes showed strong hybridization with ZASA and weak hybridization to the other threeisolates; however, the major EcoRI fragment in WS526 and WS584 was smaller than that in NC4 while ZASA and AC4 had fragments of similar size to that in NC4. The asexual isolates WS526 and WS584 were closely related to each other and appearto be isolates of the same species although there were some differences in the overall pattern of EcoRI restriction fragments from high copy number sequences and of restriction fragments hybridizing to the actin and discoidin gene probes. The homothallic isolates AC4 and ZASA appear to represent two additional species; ZASA, and possibly AC4, are more closely related to D. discoideum than the species represented by WS526 and WS584. Overall it appears that the four atypical isolates (AC4, ZASA, WS526 and WS584) are less distantly related to D. discoideum than are isolates of D.purpureum and D. mucoroides. HE cellular slime mold Dictyosteliumdiscoideum the wild isolate mustbe crossed toa genetically T has been studied for many years by develop- marked haploidtester strain to producea diploid mental biologists. This organism differentiates dur- from which segregant haploids arethen obtained ing asexual fruiting body formation into only two (WELKER,HIRTH and WILLIAMS 1985;GRANT, major cell types, spores and stalk cells (LOOMIS 1982; WELKERand WILLIAMS 1985;WELKER et al. 1986). In SPUDICH 1987).Molecular genetic analyses involving order to facilitate such studies wild isolates must be transformation,insertional mutagenesis, antisense properly assigned to their respective species. Like- RNA, and amplified gene expressionare now possible wise, it is important to know that plasmid-bearing (NELLEN,SILAN and FIRTEL 1984; KNECHT and isolates are properlyidentified; particularly in the LOOMIS1987; DELOZANNE and SPUDICH 1987; REY- construction and use of transformation vectors based MOND, NELLENand FIRTEL 1985;REYMOND et al. on endogenous plasmids, so that the host range of 1986). Molecular approaches arealso being employed the plasmids can be defined and problems associated to expand the genetic linkage map of D. discoideum with it understood. (GRANT, WELKERand WILLIAMS,1985; WITKE et al. In thepast, morphological featuresof the amoebae, 1986; WELKERet al. 1986; DINGERMANNet al. 1987) asexualfruiting bodies and sexual structures have and to study nuclearplasmid DNAs (METZet al. 1983; been used for classification in the Dictyostelids (RAPER NOEGELet al. 1985; NOEGEL,METZ and WILLIAMS 1984).However, increased knowledge of the wild 1985). Many of the recent genetic studies use either isolates has made it apparent that there arelimitations proteinpolymorphisms or restriction fragment associated withclassification based solely on mor- length polymorphisms (RFLPs). Mostof the poly- phology, since it is known that morphological char- morphisms utilized have been identified by compar- acteristics are dependent to some extent on various ison of different wild isolates. For linkage analyses, aspects of culture conditions (RAPER 1984). Nucleic Genetics 119: 561-569 (July, 1988). 562 W. B. Evans, J. E. Hughes and D. L. Welker acid and protein homologieshave been useful for FRANCIS(University of Delaware). Isolates of the other species identification and phylogenic studies in other specieswere obtained from K. B. RAPER (University of organisms. Phylogenic work based on DNA includes Wisconsin), D. FRANCIS(University of Delaware), D. WAD- DELL (Bergische Universitat, Wuppertal), J. C. CAVENDER determinationsof sequences, hybridization studies, (Ohio University), G. W. ERDOS (University ofFlorida), D. and analyses of RFLPs. DNA sequences present in H. O'DAY(University of Toronto) and the American Type multiplecopies per cell haveoften been utilized. Culture Collection. Strains were grownat 21" in association These include mitochondrial DNA, kinetoplast DNA, with Escherichia coli B/r on DM medium (PODGORSKIand repetitive DNA, and, in particular, the DNA encodingDEERINC 1980) or with Klebsiella aerogenes on SM medium (WELKER1986; SL'SSMAN1966). The geographicalorigins ribosomal RNA (DUTTA1986; AVISE, LANSMANand and sexual mating characteristicsof the D.discoideum isolates SHADE 1979; MOREL et al. 1980;BORST et al. 1980; are given as part of Table 1. JEFFREYS, WILSONand THEIN1985; APPELSand Dvo- DNA isolation: DNAs were isolated using a modification RAK 1982; MATTHEWSand DEBONTE1985; WOESE of previously published techniques (WELKERet al. 1986). 1987). Genes encoding ribosomal RNAs are highly DNA isolated from bacteriallygrown cells was extracted with phenol and chloroform, ethanol precipitated and then conserved because of the ubiquitous requirement for further purified using cesium chloride density gradients. these nucleic acids, hence their sequences can be used After recovery from the gradients the DNA was spool- to determine the phylogenic relationships of groups precipitated with ethanol, dried, and dissolved in TE (10 that have been separate for long periods oftime. mM Tris, 1 mM EDTA, pH 7.5). DNA sequence analysisof a ribosomal RNA gene Slot blots, electrophoresis and hybridization: The Schleicher and Schuell Minifold I1 slot blot apparatus was indicates that D.discoideum diverged early from other used for slot blots; genomicDNA (1 kg/slot) was pretreated eukaryotes (MCCARROLLet al. 1983). Characterization and loaded according to the manufacturer's instructions. of theless highly conserved spacerDNA surrounding Following application of the DNA, the nitrocellulose mem- the ribosomal RNA genes by sequencing, hybridiza- brane was rinsed in 5 X SSC, baked for 2 hr, then tion or RFLP analysis provides information on more prehybridized, hybridized, and hybridization detected ac- cording to standard techniques. DNA samples for gels were recently separated species. digested with restriction enzymes and separated on 0.8% The DNAencoding the ribosomal genes in D. agarose gels using a Tris phosphate running buffer (36 discoideum has been studied extensively. This rDNA mM Tris, 30 mM NaH2P04,1 mM EDTA). The separated is present in extrachromosomal palindromic dimers DNA fragments were blotted to nylon membranes (Zeta- of 88 kb (COCKBURN,TAYLOR and FIRTEL1978). Each bind, Bio-Rad) using the alkaline transfer protocol (REED and MANN 1985) or to nitrocellulose (Nitroplus 2000, cell contains about 90 dimers allowing easy visualiz- Micron Separations) by the SOUTHERN(1975) protocol. For ationof restriction fragments from the rDNA on useas probe DNA, E. coli plasmidswith inserts of D. agarose gels stained with ethidium bromide. Cloned discoideum DNA were nick translated using either 92P-dATP DNA is available for much of the coding and spacer or biotinylated dUTP. Biotin-labeled probe DNA was de- DNA on the rDNA palindromes (NESS et al. 1983; tected using kits and protocols supplied by Bethesda Re- search Laboratories. The probes were: pCTl (EMERYand EMERYand WEINER198 1); RFLPs affecting this DNA WEINER1981), pEcoIV and pEcoVII (NESS et al. 1983), have been identified (WELKER,HIRTH and WILLIAMS pDd812 (DEVINE,TSANG and WILLIAMS1982), ACTIN-8 1985). Hence we chose to investigate whether or not (ROMANSand FIRTEL1985), GM45A (CHUNG,ZUKER and wild isolates designated as D. discoideum on the basis LODISH1983), pB41-6 (ZUKERand LODISH1981). Probes pCTl and pEcoIV are of ribosomal spacer DNA, pEcoVII of morphological criteria were closely related based is of ribosomal gene-coding DNA; pDd812is a cDNA clone on (1) the ability oftheir DNA tohybridize with of a discoidin I gene; ACTIN-8 contains a genomicse- probes derived from the rDNA of the D. discoideum quence encoding an actin gene; GM45A and pB41-6 con- type strain NC4 and (2) where hybridization to the tain the DIRS-I internal EcoRI fragment and terminal rDNA probes occurred, on the presence of RFLPs. repeat, respectively. We also utilized probes for two protein-coding gene families (actin and discoidin) and the DIRS-1
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