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Differential Activity Staining Proc. Nat. Acad. Sci. USA Vol. 72, No. 12, 4914-4917, December 1975 Biochemistry Differential activity staining: Its use in characterization of guanylyl- specific ribonuclease in the genus Ustilago (gel electrophoresis/nucleic acid-dye interaction/fungal taxonomy/agrostology/phytopathology) A. BLANK AND CHARLES A. DEKKER Department of Biochemistry, University of California, Berkeley, Calif. 94720 Communicated by Howard K. Schachman, October 8, 1975 ABSTRACT Guanylyl-specific ribonuclease can be iden- eight other members of the genus, including six parasites of tified by a novel technique employing electrophoresis in major food crops (12). We have developed a novel method polyacrylamide slabs followed by differential activity stain- ing. The technique requires as little as 7 ng of enzyme which for identification of these enzymes in unfractionated culture may be grossly admixed with contaminants, including other media; the method, involving differential activity staining ribonucleases. following polyacrylamide gel electrophoresis, permits estab- Upon electrophoresis and activity staining, a variety of ri- lishment of their base specificity without prior purification. bonucleases can be visualized as light or clear bands in a col- ored background formed by toluidine blue complexed with EXPERIMENTAL PROCEDURE oligonucleotide substrate. Guanylyl-specific ribonuclease, which is detectable when using an oligonucleotide substrate Materials. Cultures of U. avenae, U. bullata, U. hordei,- of random base sequence, does not yield a band when using U. kolleri, U. nigra, U. nuda, and U. tritici were the gra- oligonucleotides bearing guanylyl residues at the 3'-termini cious gift of Dr. Jens Nielsen. U. maydis, U. halophiloides, only and containing, therefore, no susceptible internucleo- and U. cynodontis were germinated from teliospores ob- tide bonds; in contrast, a ribonuclease with a different base specificity or no base specificity yields a band with either tained from Dr. Richard Mower. U. sphaerogena was substrate. This differential activity staining method for es- cloned from a culture provided by Dr. J. B. Neilands. U. vio- tablishing guanylyl specificity permits estimation of the ex- laceae was obtained from Mr. M. Baird. RNases T1, T2, and tent of nonspecific cleavage of internucleotide linkages by a U2 were Sankyo products. RNase N1 and RNase A (5X crys- putatively guanylyl-specific enzyme and is at least as sensi- tallized) were obtained from Sigma. RNases U1 (13) and U4B tive as conventional procedures for determination of base (14) were prepared in this laboratory. Union Carbide seam- specificity. With this new technique guanyloribonuclease has been less cellulose tubing (1 inch diameter), boiled just prior to identified in the unfractionated culture medium of 10 organ- use, was employed for dialysis. isms belonging to the phytopathogenic fungal genus Ustila- Assays. Ribonuclease activity was measured in our stan- go. It is suggested that guanylyl-specific ribonuclease is dard assay (11) in which RNase U1 has a specific activity of widely distributed among Ustilago species; its electrophoret- 300,000 units/mg dry weight (13). ic properties may be revealing of phylogenetic relationships Electrophoresis. Electrophoresis was carried out in 12.5% among these plant parasites and among their hosts. The general technique of differential activity staining, de- polyacrylamide slabs at 30 mA for 90 min at 40 as described veloped for determination of the base specificity of ribonuc- by Ames (15) except that sodium dodecyl sulfate and mer- leases, may be widely applicable to analysis of enzymes cata- captoethanol were omitted from all solutions. For electro- lyzing depolymerization reactions. phoresis of RNase A only, a low pH acetate-3-alanine buffer system (16) was employed. Since discovery of the classic RNase T1, guanylyl-specific ri- Differential Activity Staining. Following electrophoresis, bonucleases have been found in bacteria, in the three classes gel slabs were sliced into a right and left half, each half of fungi, and in a slime mold (1-5). Most of these enzymes bearing identical samples. Activity staining was carried out are extracellular proteins of molecular weight about 11,000; at room temperature at pH 7.0 using 0.1 M Tris-HCl, or at the amino-acid composition of six (1-4) and the amino-acid pH 5.0 using 0.1 M sodium acetate. Gels were incubated for sequence of two of them (1, 6) have been reported. Although 5 min in buffer, for 15 min in buffer containing oligonucleo- they are most widely known as an analytical tool for deter- tide substrate (50 A260 units*/ml, about 35 ml total volume), mination of nucleotide sequence in RNA (1, 7), the guany- for 2 min in buffer, for 5 min in 0.2% Toluidine Blue 0 lyl-specific ribonucleases are highly interesting in their own (Eastman) in 0.5% acetic acid, and for 30 min in several right. On-going studies of these enzymes include analysis of changes of 0.5% acetic acid. Incubations were carried out in their mechanism of action (1) and comparison, at a basic 14 cm glass petri dishes. Gels were stored in water at 20. level, with that of ribonuclease A (8); determination of struc- Preparation of Oligonucleotide Substrates. Oligonucleo- ture-function relationships among the various G-specific tides containing guanylyl residues only at the 3'-termini RNases and the related, purine-preferring RNase U2 (9); and were generated by exhaustive enzymatic digestion of high- investigation of their distribution, biological function, and molecular-weight wheat germ RNA prepared by a modifi- regulation (10, 11). cation of the procedure of Singh and Lane (17). RNA (330 Among known guanylyl-specific ribonucleases are two ex- A260 units/ml) was incubated 42 hr at room temperature creted by members of the phytopathogenic fungal genus Us- with 12 ,g/ml of RNase U1 in sterile 0.06 M Tris-HCl, pH tilago-RNase Ui from U. sphaerogena and an enzyme 7.5; a few drops of CHC13 were included; KOH was added from the corn smut U. maydis (1, 10). We report here that extracellular guanylyl-specific ribonuclease is produced by - * One A260 unit is that amount giving an A260 of 1 when dissolved Abbreviation: G-specific, guanylyl-specific. in 1 ml and the light path is 1 cm. 4914 Downloaded by guest on September 28, 2021 Biochemistry: Blank and Dekker Proc. Nat. Acad. Sci. USA 72 (1975) 4915 as necessary to maintain pH between 7 and 8. The digest Guanyloribonuclease Digest Alkaline Hydrolysate was dialyzed versus 4 liters of distilled water at 20 for 48 hr with one change of dialysis medium. Oligonucleotides having an average chain length (n) of 19.1 were prepared by dialysis, as described above, of 20 ml of sodium ribonucleate (Schwarz Bioresearch lot NHS 6402, about 30 mg/ml, titrated to pH 7.1 with KOH). Shorter oligonucleotides (n = 2.2-9.2) were prepared by partial al- kaline hydrolysis (18) of sodium ribonucleate (ICN-Nutri- tional Biochemicals lot 3990); the latter material too was oli- gomeric, having an average chain length after dialysis even lower than that of the Schwarz product. The starting materi- al was dissolved, with the aid of KOH, to give a 1% solution, pH 6.5-6.9. Aliquots were made 0.3 N in KOH and incubat- ed at 28° for 2-20 min. Following neutralization with ice- cold HCI04, or preferably with a premeasured amount of Dowex 50 X8(H+), 50-100 mesh (Bio-Rad Laboratories), hy- drolysates were Iyophilized. Fractions of various average lengths were obtained by chromatography of 5 ml of redis- FIG. 1. Differential activity staining of guanyloribonuclease. solved hydrolysate on a 2.6 X 12 cm column of Bio-Gel P2 Following electrophoresis the gel slab was sliced into a right and equilibrated with 0.1 M NH4HCO3, followed by left half bearing identical samples. Activity staining was carried (Bio-Rad) out at pH 5.0 to accommodate the acidic pH optima of RNases T2 Iyophilization. We have not determined whether the prod- and U2. The slab on the left was stained using oligonucleotides uct marketed by numerous suppliers as sodium ribonucleate from an exhaustive, dialyzed RNase U1 digest of RNA (A260 = is routinely composed of oligonucleotides; use of any partic- 49.5, average oligomer length = 5.6). The slab on the right was ular lot of such material for generation of oligomers of vari- stained using oligonucleotides generated by partial alkaline hy- ous average lengths should be initiated by determination of drolysis and gel filtration (A260 = 50.2, average oligomer length = and pilot alkaline hydrolyses (18) and fraction- 5.1). Samples are: 1, RNase T1 (10 ng); 2, RNase T1 (10 ng) and chain length, RNase T2 (0.1 units as specified by supplier); 3, RNase N1 (1 unit ation. as assayed in ref. 11); 4, RNase U1 (33 ng); 5, RNase U1 (33 ng) and For determination of average chain length, oligonucleo- RNase U2 (0.3 units as specified by supplier); 6, RNase U1 (33 ng) tide preparations (10-30 A260 units/ml in 0.05 M Tris-HCI, and RNase U4B (19 units as assayed in ref. 11). pH 9.0) were treated with bacterial alkaline phosphatase (Worthington, electrophoretically purified, 200 jg/ml) for 1 other cultures. After 5 days, activity in the U. nuda medium hr and for 2 hr. The preparations were then hydrolyzed with was too low to measure reliably (about 1 unit/ml); activity in 0.3 N KOH at 300 for 17 hr. Following neutralization with the U. tritic medium had reached 260 units/ml. Aliquots of HC04,-aliquots were chromatographed for 8 hr in 70% iso- culture medium, taken at the plateau of ribonuclease activi- propanol with 0.35 ml of NH3 per liter of air space (19) on ty, or at 5 days for U. bullata, U. nuda, and U. trtici, were Whatman 3MM paper prechromatographed in the same sol- applied to the gel shown in Fig.
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