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The Respiration of the Pea Plant. Oxidation of Hexose

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The Respiration of the Pea Plant. Oxidation of Hexose 34 PLANT PHYSIOLOGY nostic foliaire a l'arachide. Oleagineux 6: 329-337. 19. THOMAS, W. Foliar diagnosis; principles and prac- 1951. tice. Plant Physiol. 2: 571-599. -1937. 18. PREVOT, P., OLLAGNIER, M. and GiLLIER, P. Diag- 20. ULRICH, A. Physiological bases for assessing the nostic foliaire de l'arachide et equilibre des fumu- nutritional requirements of plants. Ann. Rev. of res (Senegal 1951). Oleagineux 4: 185-194. 1952. Plant Physiol. 3: 207-228. 1952. THE RESPIRATION OF THE PEA PLANT. OXIDATION OF HEXOSE PHOSPHATE AND PENTOSE PHOSPHATE BY CELL-FREE EXTRACTS OF PEA LEAVES1'2'3 MARTIN GIBBS DEPARTMENT OF BIOLOGY, BROOKHAVEN NATIONAL LABORATORY, UPTON, LONG ISLAND, NEW YORK Evidence for the presence of the Embden-Meyerhof- by the method of LePage and Mueller (17) and found Parnas pathway in higher plants has accumulated to contain 31% Co II and to be free of Co I. TPN rapidly in the last few years (23). The major out- (80%) purchased from the Sigma Chemical Co. was standing difference reported between the glycolytic also used. The barium salts of the phosphate esters pathway in the green tissues of higher plants and in were converted into potassium salts by dissolving in yeast, animal tissue and microorganisms is the pres- 1 N HCl, adding a slight excess of 10% K2SO4 and re- ence in green tissues of a glyceraldehyde phosphate moving the resulting BaSO4 by centrifugation. The dehydrogenase linked not only to diphosphopyridine supernatant solution was neutralized with 1 N KOH nucleotide but also to triphosphopyridine nucleotide and diluted to make the final substrate concentration (1, 13). either 0.1 M or 0.05 M. Preliminary evidence has also been gathering that PREPARATION OF PEA LEAF EXTRACT: Pisum sativum an alternate pathway of glucose-6-phosphate metabo- variety Alaska (Rogers Brothers Seed Co., Idaho lism characterized in yeast (6, 9, 10), animal tissue Falls, Idaho) was used throughout this investigation. (11, 15, 16) and microorganisms (8, 12), and termed The seeds were soaked overnight in tap water, then the " hexosemonophosphate shunt " may also be op- transplanted to tanks containing gravel in the green- erating in leaves (3, 13), roots (13) and other tissues house. Nutrient solution (14) .was poured over the (5, 7) in higher plants. gravel once during the period of growth. The present investigation was undertaken to estab- It is in order to note that cell-free preparations of lish whether the enzymes of the "hexosemonophos- leaves obtained from plants grown in the winter (No- phate shunt" are present in pea leaves and, if so, vember through March) were unsatisfactory for ma- (1) whether the pathway is the same as in tissue of nometry, although solar radiation was supplemented other organisms and (2) whether it is connected with with artificial light, total radiation being 300-800 fc. the glycolytic pathway. Leaves of 11-15 day plants were used. A typical batch of plants had 4-5 sets of leaves, weighed about MATERIALS AND METHODS 2 gm, and disregarding the cotyledons, the weight was Fructose-1,6-diphosphate (FDP), fructose-6-phos- approximately evenly divided among the leaves, stems phate (F-6-P), and adenosine triphosphate (ATP) and roots. In general, about 70 gm of leaves, sepa- were purchased from the Schwarz Laboratories. Glu- rated from the stems, were ground with an equal cose-6-phosphate (G-6-P) and 6-phosphogluconate weight of acid-washed, cold, sharp sand and 20 ml of (6-PG) were prepared by the methods of Seegmiller ice-cold 0.5 M KHCO3 in a cold mortar. This opera- and Horecker (21). Ribose-5-phosphate (R-5-P) was tion and subsequent ones in the preparation of the kindly supplied by Dr. R. DeMoss. Ribonic acid-5- cell-free extracts were carried out at 0-40C. The ex- phosphate prepared from ribose-5-phosphate by the tract was strained through 4 thicknesses of cheesecloth hypoiodite oxidation procedure of Moore and Link and centrifuged at 18,000 x g for 20 minutes. On occa- (19) was kindly supplied by Dr. L. M. Paege. Coen- sion the supernatant material was passed through glass zyme I (diphosphopyridine nucleotide, DPN) was ob- wool to remove fat particles. The solution had a dark tained from the Schwarz Laboratories. Analysis green color, its volume was 50-75 ml and its pH showed that it contained 61% DPN. Coenzyme II varied from 6.8 to 7.5. The pH was brought to 7.2 (triphosphopyridine nucleotide, TPN) was prepared with either ice-cold 1 N KOH or 2 N acetic acid. This preparation was used immediately or placed in the 1 Received March 16, 1953. deep freeze until the next day. The frozen material 2A preliminary report was given at the meetings of the American Institute of Biological Science, Ithaca, when thawed the next morning formed a heavy pre- N. Y., September, 1952. cipitate which was removed 'by centrifugation at 3 Research carried out at Brookhaven National Labo- 18,000 x g for 20 minutes. The removal of this pre- ratory under the auspices of the U. S. Atomic Energy cipitate did not affect the activity of the extract. In Commission. some of the experiments, the extract was dialyzed 6 GIBBS-RESPIRATION OF PEA 35 hours against 10 liters of 0.02 N NaHCO3 or 0.02 N TABLE I NaHCO3 containing, 47 mM cysteine* HCl. The pH of the dialyzing mixture was EFFECT OF BOILED PEA LEAF EXTRACT ON THE OXIDATION 7.5. OF On occasion, extracts were prepared in the usual GLUCOSE-6-PHOSPHATE BY PEA LEAF EXTRACT manner with 150 mg of sodium versenate (pH 7.4) added to protect the sulfhydryl-containing enzymes. REACTANTS * (AL/111O02 UPTAKEMIN) Extracts prepared in this manner were inactive for manometry, presumably due to the removal of co- Undialyzed P.L.E., G-6-P, TPN .......... 232 factors. Dialyzed P.L.E., TPN ......... ............ 67 Oxygen uptake was determined manometrically at Dialyzed P.L.E., G-6-P ........ ............ 42 370 with air as the Dialyzed P.L.E., TPN, G-6-P+ 0.2 ml B.P.L.E. + 33 gas phase. The main compart- Dialyzed P.L.E., TPN, G-6-P+ 0.5 ml B.P.L.E. 58 ment of each Warburg vessel usually contained 1.0 ml Dialyzed P.L.E., TPN, G-6-P+ 1.0 ml B.P.L.E. 118 of dialyzed enzyme solution, 0.1 ml of 0.2 M MgC12, 0.05 ml riboflavin (1 mg/ml), and 0.05 ml of 0.25 M * 1.0 ml pea leaf extract dialyzed against NaHCO3, 0.5 ATP, or undialyzed enzyme solution, 1.0 ml, and water, mg TPN, 0.2 ml 0.05 M glucose-6-phosphate. Total vol- 0.45 ime 2.5 ml. ml. The side arm contained 0.05 ml TPN solu- t P.L.E.-pea leaf extract. tion (1 mg/ml) and 0.2 ml of 0.05 M substrate. The t B.P.L.E.-undialyzed pea leaf extract heated 2 min- center well contained 0.2 ml 20% KOH as CO2 ab- utes at 100°C. sorbent or in experiments with cyanide a suitable contains the entire KOH-KCN mixture. After the endogenous level had complement of enzymes necessary for the transfer of electrons from the substrate to subsided (usually 60-90 minutes), the reaction was After initiated by tipping in the TPN and substrate. oxygen. dialysis, the pea leaf extract loses its For capacity to oxidize hexose and pentose phosphate, each point on the curves, duplicates were run. the The rate of reduction of TPN was followed at 340 however, oxidizing activity of the dialyzed prep- in 1 cm aration is restored by the addition of pea leaf extract m/A cells in a Beckman spectrophotometer, heated at 100°C for 2 model DU, at 23-25°. The cell contained 1.5 ml minutes (table I). These heat- veronal buffer, pH 8.0, 0.05 ml enzyme solution, 0.05 TABLE II ml TPN (1 mg/ml) and 0.1 ml of 0.05 M substrate. EFFECT OF Water was added to make a total volume of 3 ml. COFACTORS ON THE OXIDATION OF FRUCTOSF-1,6- Blanks omitting TPN were used. DIPHOSPHATE By DIALYZED PEA LEAF EXTRACT RESULTS ADDITIONADDITION 02 UPTAKE Figure 1 indicates that the cell-free preparation ~~(AL1120 MIN) contains enzymes capable of oxidizing fructose-1,6- FDP, riboflavin, ATP, TPN ............. 370 diphosphate, fructose-6-phosphate, glucose-6-phos- Riboflavin, ATP, TPN .................. 112 phate, 6-phosphogluconate and ribose-5-phosphate. FDP, ATP, TPN ........................ 201 The following materials are not oxidized: glucose, FDP, riboflavin, TPN ................... 199 gluconic acid, ribose, ribonic acid-5-phosphate, hy- FDP, riboflavin, ATP ................... 117 droxypyruvic acid and formic acid. When formic acid See methods section for protocol. Extract dialyzed was used as substrate DPN was also added; however, against NaHCO3. it had no effect. It is also apparent from figure 1 that the extract stable cofactors are also present in boiled yeast juice. Of the various likely cofactors tested, a mixture of TPN, ATP and riboflavin or riboflavin phosphate in- creases the oxygen uptake when any of the hexose or pentose phosphates is employed as substrate (tables II, III, IV). With some extracts the rate of oxidation of FDP TABLE III EFFECT OF ADENOSINE TRIPHOSPHATE ON THE OXIDATION OF FRUCTOSE-1,6-DIPHOSPHATE BY PEA LEAF EXTRACT MICROMOLES OF ATP 02 UPTAKE (T,L/50 MIN) 0 50 MINUTES 5 90 FIG. 1. Oxidation of hexose and pentose phosphate by 10 117 pea leaf extract. Extract 1.0 ml; 0.5 mg TPN and 15 117 0.2 ml 20 132 0.05 M substrate.
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