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Kinetics of Photosynthate Translocation Donald Boyd Fisher Iowa State University

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Kinetics of Photosynthate Translocation Donald Boyd Fisher Iowa State University Iowa State University Capstones, Theses and Retrospective Theses and Dissertations Dissertations 1965 Kinetics of photosynthate translocation Donald Boyd Fisher Iowa State University Follow this and additional works at: https://lib.dr.iastate.edu/rtd Part of the Biochemistry Commons, and the Botany Commons Recommended Citation Fisher, Donald Boyd, "Kinetics of photosynthate translocation" (1965). Retrospective Theses and Dissertations. 4085. https://lib.dr.iastate.edu/rtd/4085 This Dissertation is brought to you for free and open access by the Iowa State University Capstones, Theses and Dissertations at Iowa State University Digital Repository. It has been accepted for inclusion in Retrospective Theses and Dissertations by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. This dissertation has been micro&hned exactly as received ® ® ® ^ FISHER, Donald Boyd, 1935- KINETICS OF PHOTOSYNTHATE TRANS­ LOCATION. Iowa State University of Science and Technology, Ph.D., 1965 Botany University Microfilms, Inc., Ann Arbor, Michigan KINETICS OF PHOTOSYNTHATE TRANSLOCATION by Donald Boyd Fisher A Dissertation Submitted to the Graduate Faculty in Partial Fulfillment of The Requirements for the Degree of DOCTOR OF PHILOSOPHY Major Subject: Biochemistry Approved : Signature was redacted for privacy. Signature was redacted for privacy. fieao. oi I'lajor ueparument Signature was redacted for privacy. D of Graduate College Iowa State University Of Science and Technology Ames, Iowa 1965 il TABLE OF CONTENTS Page I. INTRODUCTION MD LITERATURE REVIE'/J 1 II. ANATOMIC OBSERVATIONS 12 A, Observations on the Leaf Structure 12 B, Observations on the Phloem 18 III. ISOTOPIC EXPERIMENTS 23 A. Materials and Methods 23 1. Plant material 23 2. General feeding and sampling procedures 24 3. Extraction 26 4. Chromatography of water soluble materials 29 5. Chromatography of polar lipids 32 6. Identification of water soluble compounds 37 7. Identification of lipids 39 8. Quantitative analysis of sugars 44 9. Radioactivity determinations 46 10. Starch hydrolysis 48 B. Results 59 1. Progression of the translocation profile down the conducting tissue 59 a. Experiments with soybean 59 b. Experiments with barley 63 2. Carbon-l4 kinetics in the soybean leaf during steady state labelling: An exploratory experiment 66 3. Quantitative behavior of the sucrose pool size " 72 a. Daily variations in the sucrose pool in a soybean leaf 72 b. The effect of excision on the sucrose pool size in a soybean leaf 73 4. The kinetics of l^C accumulation in the petioles of soybean and kidney bean leaves following pulse labelling 78 ill Page 5. Carbon-l4 kinetics in the soybean leaf following pulse-labelling 79 a. Carbohydrates 81 . b. Lipids 90 c. Amino acids and organic acids 93 d. Total activity 97 6. Carbon-l4 kinetics in soybean leaf following pulse-labelling, with special reference to the specific activity of sucrose during short times 99 7. Carbon-l4 kinetics in the soybean leaf during steady state labelling IO5 a. Carbohydrates 107 b. Lipids 116 c. Amino acids and organic acids 118 d. Total activity 118 8. Translocation in soybean plants following pulse-labelling 122 a. Gross distribution of radio­ activity between leaf, stem and root 125 b. Distribution of total ethanol- soluble radioactivity in the stems 127 c. Distribution of ethanol- insoluble radioactivity in the stems 130 d. Distribution of non-sucrose ethanol-soluble radioactivity in the stems harvested at 75 and 125 minutes 137 e. Carbon-l4 kinetics in the leaves l44 f. Sucrose concentrations and specific activities in the leaves and petioles 149 9. The effect on translocation of excising various plant parts 152 a. Excision of both leaf and root 152 b. Excision of leaf or root 153 THEORETICAL CONSIDERATIONS OF TRANSLOCATION 157 A. Mathematical Models for the Effects of Leaf Size, Shape, and Source Pool Kinetics on the Efflux of Radioactive Translocate from leaves 157 iv Page 1. Model for a linear, parallel-veined leaf 158 2. Model for a rectangular leaf l66 3. Model for a peltate leaf " I69 4. Comparison of the effects of leaf size and shape I7I B. Source Pool Kinetics I78 C. Carbon-l4 Kinetics in the Soybean Stem and Petiole 192 D. Application of the Models to Willow and Sugar Beet I98 E. An Estimate of the Pressure Drop in Soybean Sieve Tubes 206 P. The Relationship between Pulse Labelling and Steady State Labelling 210 V. DISCUSSION 214 VI. sumiARY 225 VII. LITERATURE CITED 229 VIII. APPENDIX A. LIST OF SYMBOLS 239 IX. APPENDIX 3. EXACT VALUES FOR THE TURÎTOV^R TIMES USED TO DESCRIBE COMPARTMENTAL MODELS 242 X. APPENDIX C. DERIVATION OF THE EQUATIONS DESCRIBING THE EFFECTS OF LEAF SIZE, SHAPE AND SOURCE POOL KINETICS ON THE RATE OF TRACER EFFLUX FROM LEAVES 243 A. Equations for a Linear Leaf 243 B. Equations for a Rectangular Leaf 246 C. Equations for a Peltate Leaf 248 D. Fortran Statements for the Leaf Models 25O 1. Program for a linear leaf model 25O 2. Program for a rectangular leaf model 251 3. Program for a peltate leaf model 252 V Page E. Derivation of Dimensionless Equations for a Linear Leaf 252 XI. APPENDIX D. DERIVATION OP EQUATIONS FOR COMPARTMENTAL MODELS 25^ XII. APPENDIX E. DERIVATION OP THE EQUATION DESCRIBING THE DISTRIBUTION OF RADIOACTIVITY IN THE TRAl^SLOCATION STREAM IN THE STEM 257 XIII. ACKNOWLEDGMENT 259 1 I. INTRODUCTION AND LITERATURE REVIEW The transport of substances in plants takes place largely- through two sets of conducting tissues, the xylem and the phloem. The non-living nature of the conducting cells in the xylem and their obvious tubular form resulted in a more ready understanding of transport in that tissue than has been the case with phloem. In the phloem the question of how and where materials are transported is greatly complicated by the fact that all of the cells involved are maintained in a living state, and must remain alive in order for solute transport to occur (28). A number of mechanisms have been proposed to account for transport in the phloem, and a myriad of experiments have been performed to test those proposals. In the work to be presented here, the main interest has been concerned with those experiments which have employed radioactive tracers, and their mathematical interpretations according to one transport mechanism or another. One of the most attractive hypotheses offered as an explanation for phloem transport has been Munch's theory of mass flow between tissues of different osmotic pressures (72). The modern version of this theory envisions a solution of high sugar concentration being contributed to sieve tube endings in the leaf by the secretory activity of the cells in the vein 2 endings. At points of sugar utilization in the other parts of the plant, the loss of sugar from the sieve tubes causes a decreased osmotic pressure. The sugar solution is forced through the connecting sieve tubes along the pressure gradient caused by the difference in osmotic pressure. The.principal difficulty with this mechanism is the question of whether there is an adequate pressure gradient generated to cause the observed flow rates (27, 5^). Spanner (90) has advanced a theory which also calls for the bulk flow of a solution in the sieve tubes. In this model, however, the motivating force is electroosmosis, caused by the cyclic pumping of potassium ions through the sieve plates in the direction of flow. On the basis of their work with the cotton plant. Mason and Maskell (67) and Mason and Phillis (68) proposed that move­ ment takes place by a process of ''activated diffusion" through a stationary cytoplasm. To account for the transport rates observed, the apparent diffusion coefficient of sucrose must be about 40,000 times that of the usual coefficient. They did not suggest how this might be achieved. Van den Honert (99) proposed that materials might be transported along a diffusion gradient at an interface in the sieve tube. He proposed that the tonoplast was the site of this interface, but sieve cells apparently do not have a tonoplast (e.g., 38), and the location of the proposed inter­ 3 face Is presently a matter of conjecture. Several workers have suggested that protoplasmic stream­ ing plays a key role in phloem transport. Curtis (30) suggested that cyclosis in the sieve elements accompanied by diffusion of sugar across the end-walls of adjacent sieve elements might account for the transport. However, streaming of the type he hypothesizes has not been observed in mature sieve elements (28), and the commonly observed translocation rates (about 1 cm min ^) are an order of magnitude greater than cytoplasmic streaming rates in higher plants (59). " Thaine (95, 9^) proposed a translocation model based on his observations of cytoplasmic tubules which, he says, traverse the sieve element lumen from one sieve plate to the other. The contents of some of the strands move up the sieve element while those of the others move down carrying carbohy­ drates which are in a dynamic equilibrium with sucrose in the sieve element vacuoles. This model is quite similar to one proposed by Canny (19)> also based on Thaine's observations. These observations have been disputed by Esau et aJL. (36) and, although strands within sieve tubes have been described by others (27, 3^» 39» 78), they often seem to be quite different from those described by Thaine. According to Evert and Derr (39)J they are more fibrillar in nature, and he has not seen any motion associated with them. A recent description of streaming in phloem fibers (69) resembled the descriptions 4 made by Thaine but motion pictures of the streaming showed more bulk movement of protoplasm than Thaine reported. Also, Thaine did not observe reversal of streaming, but this was clearly demonstrated in the case of the fibers.
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