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QUANTITATIVE STUDIES of Rdna in AMPHIBIANS

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QUANTITATIVE STUDIES of Rdna in AMPHIBIANS J. Cell Set. 24, 109-118 (1977) 109 Printed in Great Britain QUANTITATIVE STUDIES OF rDNA IN AMPHIBIANS M. VLAD Department of Biological Sciences, University of Warwick, Coventry CV4. 7AL, England SUMMARY The proportion, of the genome that is complementary to 18 and 28 s has been determined for 12 species of amphibians. The group of species chosen for the experiment includes 5 related species belonging to the same genus {Plethodon) as well as species belonging to distant taxonomic groups whose C-values range from 3 to 62 pg. Hybridization of rRNA (18S + 28S) to whole chromosomal DNA to saturation level indicates that the proportion of rDNA decreases with increasing DNA content. The results presented in this paper do not support the hypothesis of Nardelli, Amaldi & Lava-Sanchez that the number of ribosomal cistrons in various amphibians can always be expressed as a power of 2. INTRODUCTION North-American salamanders of the family Plethodontidae which comprises a large number of related species have the same general morphology and similar karyotypes, yet they have widely different C-values (amount of DNA per haploid genome). Classical taxonomical studies based on morphological characters and evolution of the family have shown that those species that are considered to be the most primitive have relatively small genomes and they are found East of the Great Plains of the United States. The species that are considered to be most advanced have the largest genomes of the family and are found in the Pacific North-West of the United States. Therefore, it is likely that in the course of evolution Western genomes have grown larger whereas Eastern ones have remained more or less constant (Wake, 1966; Kezer, unpublished observations; Macgregor & Horner, unpublished obser- vations; Mizuno & Macgregor, 1974). Studies of the lampbrush chromosome karyotypes from plethodontid salamanders have shown that the increase in C-value is accompanied by a considerable increase in the absolute length of chromosomes, although their relative dimensions remained unchanged (Macgregor, Mizuno & Vlad, 1974; Vlad & Macgregor, 1975). If the growth of the genome is achieved through a balanced increase in the moderately repetitive fraction, as has been suggested by Mizuno & Macgregor (1974) then one would expect that organisms with larger genomes would have more copies of a specific gene complex than those with smaller genomes. The best known moderately repetitive sequence in the eukaryotic genome is that which codes for ribosomal RNA (rRNA). Ribosomal cistrons (one cistron = 18 s + 28 s + spacer) are tandemly arranged no M. Vlad and clustered in one or more nucleolus organizers per haploid genome. Their number can be measured by quantitative hybridization (Ritossa & Spiegelman, 1965) of labelled 18 s and 28 s rRNA to whole chromosomal DNA from the species in question. In this study I have determined the proportion of the genome that is complementary to 18 and 28 S rRNA in 5 species of plethodontid salamanders and 7 species of other amphibians covering a wide range of C-values, in order to see whether genome size and the number of ribosomal cistrons per genome are related. I also wished to re-examine certain aspects of the model put forward by Nardelli, Amaldi & Lava- Sanchez (1972), who suggested that the number of ribosomal cistrons in various amphibians can always be expressed as a power of 2. MATERIALS AND METHODS The animals used in this study were: Xenopus laevis (Daudain), Rana esculenta (Linne), Bufo bufo (Laurenti), Triturus cristatus carnifex (Laurenti), Plethodon cinereus cinereits (Green), Plethodon glutinosus (Green), Plethodon vehiculum (Cooper), Plethodon durmi (Bishop), Plethodon elongatus (Van Denburgh), Oedipina uniformis (Kegerstein), Ambystoma opacum (Gravenhorst), and Rhyacotriton olympicus (Gaige). R. esculenta, B. bufo and T. c. carnifex were supplied by Gerrard & Haig Ltd., East Preston, Sussex. P. c. cinerus, P. glutinosus and A. opacum were collected in New Jersey, U.S.A. P. vehiculum, P. dimni and P. elongatus were collected in Oregon and California, U.S.A. R. olympicus was collected in the Olympic Peninsula of Washington, U.S.A. and O. uniformis was collected in Costa Rica. X. laevis came from the stock kept in the University of Leicester. All American salamanders were collected and sent to our laboratory by Dr J. Kezer of the University of Oregon, or by Dr R. Nussbaum of Oregon State University. The source of DNA was carcases from degutted fresh or frozen animals from which the gonads had been removed. Two or three carcases were homogenized in o-i M EDTA and 005 M Tris (pH 84) with a Silverson Mixer - Emulsifier Blender. DNA was extracted by a simple detergent-phenol procedure as described by Macgregor & Kezer (1971). The procedure included incubation with Sarkosyl (Ciba-Geigy) and pronase, extraction with phenol, precipitation with ethanol, digestion with ribonuclease A and T1 and a-amylase, and centrifugation on a CsCl gradient (Flamm, Bond & Burr, 1966). Approximately 30 fractions were collected by puncturing the bottom of the centrifuge tube. The optical density at 260 nm was determined for each fraction and all but the first and the last 5 fractions were combined. Samples of radioactive DNA from 4 species were prepared by injecting doses of 25 /tCi of ["CJthymidine into the abdominal wall. Each animal received a total of 15 fid over a period of 2 weeks. The radioactive DNA was extracted following the procedure described above. In all cases the specific activity of 14C-DNA after purification was 120-170 cpm/fig. 3H-RNA was prepared from cultures of Xenopus kidney cells grown for 7 days in a medium containing PHJuridine (1 mCi/20 ml of culture medium). The rRNA was prepared as described by Pardue, Gerbi, Eckhardt & Gall (1970), including the following steps: short incubation at room temperature (23 °C) in o-i M acetate buffer (pH 5) with Sarkosyl, pronase and polyvinyl sulphate (PVS), extraction with cold phenol, precipitation with ethanol, digestion with deoxyribonuclease and centrifugation on a 5-20 % sucrose gradient. Fractions containing 18 and 28 S rRNA were detected by scintillation counting, combined and the RNA reprecipitated with ethanol. The precipitate was redissolved in 2 x SSC (SSC = 015 M NaCl +0-015 M sodium citrate, pH 7) and its specific activity determined. Ribosomal RNA in this condition was used for hybridization. Whole somatic DNA from each species was denatured with 007 N NaOH in 6 x SSC and filtered through nitrocellulose filters (Sartorius Membrane filter, 25 mm diameter, 045 /tm pore size). Each filter was loaded with 20 /tg of DNA. Blank filters received the same treatment apart from the absence of DNA. A series of incubation vials were set up, each containing a different concentration of'H-rRNA in 2 x SSC. rRNA concentrations ranged from 0-3 /ig/ml rDNA in amphibians in to 28 /tg/ml (Figs, i, 2). Two filters from each species were placed in each vial together with two blank filters. Filters were incubated together for 8-10 h at 67 °C. After incubation filters were treated essentially as described by Gillespie & Spiegelman, 1965. They were washed in 6 x SSC at room temperature, treated with ribonuclease A (50 /tg/ml in 2 x SSC) at 37 CC for 1 h and washed again in 6 x SSC, rinsed in 70% ethanol, dried at 65 °C for 10 min and counted in a liquid scintillation counter. The retention of DNA on nitrocellulose filters, monitored by using 14C-DNA, was 88-907 % (Table 1). The melting temperatures of rRNA/DNA hybrids were estimated by measuring the counts of 3H-rRNA eluted from filters in 1 x SSC at 5 °C temperature intervals from 25 to 90 °C (McCarthy, 1967). The 3H-rRNA eluted at each temperature point was precipitated with 20 % trichloroacetic acid, trapped on GF/C Whatman filters and counted in a liquid scintillation counter. Table 1. DNA retention on nitrocellulose filters No. of No. 0//o counts put of counts of counts Species on filter retained retained Xenopus laevis 2952 2679 907 Rana escidenta 3288 2893 880 Triturus cristatus 2544 2255 89-0 Piethodon vehiculum 2880 2612 907 fP. cinereus z ,?. e/ongatus QO =1. O . 0. uniform is - R. olympicus -P. g/utinosus ~P. vehiculum -P. dunni 1-4 2-8 5 6 14 28 RNA,//g/ml incubat'on mixture Fig. 1. Saturation curves for 7 species of salamanders obtained by annealing increasing amounts of 3H-rRNA (18 s + 28 s) from Xenopus cell culture to 20 fig of whole, somatic DNA trapped on nitrocellulose filters. The specific activity of the 3H-rRNA was 450153 x io6 cpm//ig. RESULTS Saturation curves were constructed by plotting the counts bound per filter against the concentration of the incubation mixture. At least 3 separate saturation curves were constructed for each species. Each experiment was carried out with DNA prepared in the same way from different batches of animals and different samples of rRNA. For the same batch of DNA the results were identical. DNA from different batches of animals gave slightly different results (compare Figs. 1 and 2). In one experiment all 12 species were treated together and the results are shown in Fig. 2. Apparently the saturation values are distributed randomly over a wide range, that 112 M. Vlad X. laevis - T.c. ctrnifex R. esculents B. bufo P. c/nereuj P. glutinosus A. opacurn P. vehiculum P. elongatus P. dunni 0. uniformis R. olympicus 20 RNA, //g/ml incubation mixture Fig. 2. Saturation curves for 12 species of amphibians obtained by annealing increasing amounts of 'H-rRNA (i8s + 28s) from Xenopus cell culture to 20 fig of whole, somatic DNA from each species trapped on nitrocellulose filters. The specific activity of the 'H-rRNA was 3-22670 xio' cpm/fig.
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