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(Charophyceae)I Received for Publication November 20, 1987 and in Revised Form January 15, 1988

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(Charophyceae)I Received for Publication November 20, 1987 and in Revised Form January 15, 1988 Plant Physiol. (1988) 87, 78-82 0032-0889/88/87/0078/05/$01 .00/0 Two Class I Aldolases in the Green Alga Chara foetida (Charophyceae)I Received for publication November 20, 1987 and in revised form January 15, 1988 SIGRID JACOBSHAGEN AND CLAUS SCHNARRENBERGER* Institut far Pflanzenphysiologie, Zellbiologie und Mikrobiologie, Freie Universitat Berlin, Konigin-Luise- Str. 12-16a, D-1000 Berlin 33 (West) ABSTRACT E. gracilis; however, experimental support for a cytosolic class I aldolase, which is different in its properties from the chloroplast Aldolase activity of Chara foetida (Braun) could be separated into a class I aldolase, was not achieved (see also "Discussion"). Very minor (peak I) and a major peak (peak I) by ion-exchange chromatog- early reports claim both class I and class II aldolases being cy- raphy on DEAE-cellulose. Affinity chromatography on P-cellulose re- tosolic (5) or the class II aldolase being plastidic (23). sulted in highly purified aldolase preparations with specific activities of During the course of our studies on aldolases of Chara foetida 3.2 and 4.8 units per milligram protein and molecular subunit masses of we discovered for the first time and describe here two distinct 37 and 35 kilodalton, as shown by SDS-PAGE, for the aldolase of peak class I aldolases in a green alga. This situation is similar to the I and peak II, respectively. Both aldolases belong to class I aldolase since cytosol and chloroplast specific class I aldolases of higher plants. the activity is not inhibited by 1 millimolar EDTA. The Km (fructose-1,6- Since increasing evidence derived from fine structure (16, 20) bisphosphate) values were 0.64 and 13.4 micromolar, respectively. The and sequence homology of 5S rRNA (7) implies a very close aldolase of peak I showed a 6.7 times stronger crossreaction with a specific evolutionary relationship of Charophyceae with higher plants our antiserum against the cytosol aldolase of spinach than with an antiserum finding of two class I aldolases in C. foetida may give a valuable against the chloroplast aldolase of spinach. On the other hand the aldolase clue to the evolutionary origin of higher plant aldolases from the of peak II showed a 5.1 times stronger cross-reaction with the a-plastid- tribe of Charophyceae. aldolase antiserum than with the ar-cytosol-aldolase antiserum. For algae this is the first separation of two class I aldolases. They are similar to the MATERIALS AND METHODS cytosol and chloroplast aldolases in higher plants, but different from a reported class I (Me2+ independent) and class II (Me2+ dependent) al- Plant Material. The green alga Chara foetida (Braun) was dolase in other algae. taken from an open-air culture in the Botanical Garden of Berlin and cleaned from macroscopic debris. Microscopic control showed only a minor contamination with other microorganisms. Separation of Isoenzymes by Chromatography on DEAE-Cel- lulose. Between 10 and 37 g of wet algal material was homoge- nized in three volumes of buffer A (20 mM Tris-HCl [pH 8.6], 10 mM j-mercaptoethanol) for 2 min in an icebath using a Virtis Aldolases from different biological sources are either depend- "45" homogenizer. The homogenate was centrifuged for 15 min ent on divalent ions for activity (class II aldolases) or not (class at 43,000g at 4°C. The supernatant was readjusted to pH 8.6 and I aldolases) (19, 23). Class I aldolases are present in animals and immediately applied to a column (3 x 11 cm) of DE 32-cellulose in higher plants including ferns and mosses (2, 15, 23). Higher (Whatman, Springfield Mill, Maidstone, Kent/England) equili- plants contain even two class I aldolases, one being compart- brated with buffer A. The column was washed with 50 ml of mented in the cytosol and the other in chloroplasts (1, 12, 14). buffer A. The proteins were eluted by a linear gradient of 0 to Class II aldolases occur in fungi and procaryotes (6, 23). In some 0.4 M KCl in buffer A of twice the column volume and subse- procaryotes, such as Escherichia coli, an additional class I type quently by 80 ml of 1.0 M KCl in buffer A. Fractions of 2 ml aldolase can be developed upon growth on pyruvate or lactate were collected, assayed for aldolase activity, and measured for (26). On the other hand, algae appear to have both a class I and KCl concentration by conductimetry. For further a class II aldolase (2, 5, 8, 15, 18, 21-23). In the green algae Affinity Chromatography on Phosphocellulose. pu- Chlamydomonas reinhardii and C. mundana and the eugleno- rification the two aldolases separated by chromatography on phyta Euglena gracilis the class I aldolase appears to be predom- DEAE-cellulose were pooled separately and dialyzed against imidazole 10 mM inant in photoautotrophically grown cells and the class II aldolase buffer B (20 mM [pH 6.5], 8-mercaptoethanol onto a in mixo- or heterotrophically grown cells (2, 5, 18, 21, 22). Only or dithiothreitol). Each aldolase was loaded P-cellulose buffer B. The column in a very early investigation (23) the occurrence of class I and P 11 (Whatman) column equilibrated with x class II aldolase activity was found in the opposite way. The sizes were 2 x 10 cm and 3 12 cm for the aldolase eluting evaluation of the intracellular compartmentation of class I and first and second from DEAE-cellulose, respectively. The col- class II aldolase in algae appears contradictory because of dif- umns were washed each with two column volumes of buffer B ficulties in cell fractionation. The most convincing data suggest and eluted with 0.1 mM fructose-1,6-bisphosphate in buffer B. were is a enzyme (10, 18) and Fractions containing aldolase activity pooled, dialyzed against that the class I aldolase chloroplastic 10 and the class II aldolase a cytosolic enzyme (18). In another paper buffer C (20 mm imidazole [pH 7.0], mM dithiothreitol), (2), some preliminary evidence was achieved for an additional used for enzyme characterization. class I aldolase activity in the cytosol of autotrophically grown Protein was determined with Coomassie brilliant blue G-250 as described by Sedmak and Grossberg (25). I Supported by a grant of the Deutsche Forschungsgemeinschaft. Enzyme Assay. Fructose-bisphosphate aldolase (EC 4.1.2.13) 78 TWO CLASS I ALDOLASES IN CHARA FOETIDA 79 was measured spectrophotometrically at 22°C according to Wu If this method is applied to proteins of C. foetida (Fig. 1) a and Racker (28). One ml of reaction mixture contained 50 mM chromatographic aldolase pattern similar to that of higher plants Tris-HCl (pH 7.5), 4.5 mM MgCl2, 1 mm EDTA, 1 unit each of is obtained, i.e. a small aldolase peak (peak I) preceding a larger triosephosphate isomerase and glycerol-3-P dehydrogenase, 210 aldolase peak (peak II). The activity in peak I represented about /LM NADH, and 2 mm fructose-1,6-bisphosphate trisodium salt 10% and the activity in peak II about 90% of the total activity (Boehringer, Mannheim, FRG). In order to test for class II (average of two experiments). activity the aldolases were incubated in either 1 mm EDTA or The two aldolases were further purified by affinity chroma- 0.1 mm zinc sulfate plus buffer C for 10 min at 37°C and the tography on phosphocellulose up to a specific activity of 3.2 units activity determined subsequently in the above reaction mixture (mg-1 protein) for the peak I aldolase and of 4.8 units (mg-' without both MgCl2 and EDTA. The enzyme activity of 1 unit protein) for the peak II aldolase (Table I). SDS-PAGE showed corresponds to the cleavage of 1 ,umol substrate per min. single protein bands for the two aldolases (Fig. 2). If more protein Immunotitration of Aldolase. The method of immunotitration was applied to the gel, additional minor bands became visible was carried out according to Kessler (9) and as described pre- (not shown). We consider the purity of peak I aldolase to be at viously (12). A constant amount of aldolase activity and 20,ul least 90% and of peak II aldolase to be at least 50%. The mo- of antiserum or dilutions of it were incubated for 5 min. Then, lecular subunit masses were estimated to be 37 and 35 kD for 5 Al of a 12% suspension of protein A-coated Staphylococcus the aldolase of peak I and II, respectively. These molecular aureus Cowan I cells were added. After incubation for 2 min the masses are similar to those of the cytosol and chloroplast aldolase suspension was centrifuged at 14,000g for 1 min in a Biofuge A from higher plants (12, 14). (Heraeus Christ) and the activity in the supernatant was deter- The activity of both aldolases from C. foetida was resistant to mined. For the aldolase of peak I 80 ,l of enzyme were used incubation in 1 mM EDTA. Also, the activity was not increased for incubation with the antisera and 90 ,tl of the supernatant by incubation with 0.1 mm zinc sulfate (Table II). Similarly, an were used for activity measurements. Accordingly, 30 ,ul of en- even higher concentration of 10 mm EDTA had no inhibitory zyme from peak II were used for incubation and 43 Al of the effect on either aldolase. Finally, after incubation with 1 mM supernatant used for activity measurements. The antisera con- EDTA, the activity in the presence of less than 0.1 mm EDTA tained a small amount of aldolase activity that was corrected for was not increased by an excess of 0.5 mM zinc sulfate.
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