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TRANSLOCATION in PLANTS Between Regions of Synthesis and Utilization. by CURTIS (22; Also 9 and 25); and MASON and PHILLIS Have

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TRANSLOCATION in PLANTS Between Regions of Synthesis and Utilization. by CURTIS (22; Also 9 and 25); and MASON and PHILLIS Have TRANSLOCATION IN PLANTS A. S. CRAFTS Introduction Elimination of certain untenable theories has nlarrowed recent research on translocation to a search for the mechanism of rapid longitudinal move- ment of foods through phloem. (For comprehensive bibliographies see 22, 48, and 51.) Present theories fall into two categories: (1) movement of solute molecules taking place in, through, or upon the surface of sieve-tube protoplasm, and which results from protoplasmic activity; (2) mass flow of solution through sieve tubes or phloem, related, at least indirectly, to activ- ity of photosynthetic tissues, and not dependent upon the activity of the sieve-tube protoplasm.1 Both mechanisms are based upon ringing experi- ments which demonstrate limitation of primary movement of foods to the phloem, and upon analytical data which indicate concentration gradients between regions of synthesis and utilization. Evidence for the protoplasmic streaming hypothesis has been reviewed by CURTIS (22; also 9 and 25); and MASON and PHILLIS have recently elabo- rated an activated diffusion theory (45, 46, 47, 48) to explain solute move- ment via the sieve-tube protoplasm. These workers postulate an indepen- dent movement of various solutes resulting from independent gradients; they call upon vital activities or surface phenomena to explain the accelera- tion required. This paper presents the case for mass flow, drawing attention to certain quantitative evidence and to cytological studies oni the activity of sieve-tube protoplasm. Concentration gradients of organic solutes in the phloem have been ade- quately demonstrated.2 That they cause an effective diffusional movement of the solutes is less certain. Physical aspects indicate that diffusion, over long distainees, is naturally a slow process; and acceleration of unilateral solute movement, to the required rates, independent of the solvent, would necessitate an immense expenditure of energy. MASON and PHILLIS (48) have recognized this fact. The mass-flow hypothesis involves a mechanism for transforming con- centration gradients into pressure differences. The essential features of this mechanism are apparently incorporated in the normal structure of plants (11, 50). Exudation studies (12, 15, 50, 51) indicate a maintained 1 HUBER has recently proposed a somewhat similar classification (HUBER, BRUNO. Hundert Jahre Siebr6hren-Forschung. Protoplasma 29: 132-143. 1937.). 2 See also HUBER, B., SCHMIDT, E., and JAHNEL, H. Untersuchungen iiber den Assimilatstrom. I. Tharandt F6rstl. Jahrb. 88: 1017-1050. 1937. 791 792 PLANT PHYSIOLOGY pressure gradient in the phloem; and studies on virus movement by BEN- NETT (2, 3, 4) and others, which indicate a marked parallelism between translocation of virus and organic foods, cast doubt on the independent movement of solvent and solutes. Those who favor mass-flow question the evidence for independent movement of various solutes; and they present anatomical, physiological, and cytological data which indicate (1) that the total phloem (or sieve-tube strand) is the unit of conduit, (2) that mature sieve-tube protoplasm is in a state of reduced activity, and (3) that phloem exudation occurs at rates sufficient to explain common phenomena of growth and storage. Since the perfect experiment for demonstrating which mechanism actu- ally functions in the phloem has not been devised, judgment must rest, for the present, upon a reconciliation of the recognized facts with known plant structure and behavior. With this in view, new observations on the proper- ties of sieve tubes will be presented, and an attempt made to interpret current research on food movement.' Phloem studies Many observations emphasize the important relation between ontogeny and function of the phloem. Previous studies (12, 13, 14, 15) have indi- cated the changes in form and physiology that take place as the sieve tube matures, passes through its functioning period, and is obliterated. Recent observations confirm these earlier reports. Young sieve-tube elements are spheroid or cylindrical and well rounded. Having nuclei, slime bodies, and cytoplasm in a high state of activity, they react to stains and plasmolyzing solutions as normal vacuolated living cells. Attending the nuclear disintegration, loss of slime bodies, and alteration of permeability that occurs with maturity, are morphological changes of pro- found significance (12, 13, 14, 15). At maturity the side walls of sieve tubes are slowly pressed in by surrounding cells so that the elements become funnel-shaped at each end, the transverse area in the center becoming pro- gressively smaller. Finally the walls are pressed together, and the lumen disappears completely; the only structures left at obliteration are the sieve plates, often found lodged between the phloem parenchyma cells. EsAU (26, 27, 29) has illustrated this process of sieve-tube obliteration in the for- mation of the bundle cap in sugar beet and celery. Though specific studies have been made on only a few species, this general behavior of sieve tubes is well known and has been observed by plant anatomists since the pioneer- ing studies of the past century. It apparently provides almost indisputable evidence that the sieve tube becomes permeable, loses turgor, and is finally collapsed by the pressure of surrounding phloem parenchyma cells (6, 27). ESAU (29), studying several plants, has noticed that when phloem tissues CRAFTS: TRANSLOCATION IN PLANTS 793 are killed by reagents which plasmolyze livilng cells, young sieve tubes always show shrinkage of the cytoplasm, indicating that they were plasmo- lyzed in the killing process before the tissue was sectioned. Mature sieve tubes, on the other hand, do not respond to these reagents in this way. As she has pointed out, STRASBURGER made the same observation years ago. Another unique feature of mature sieve tubes is that the plastids, in- stead of being associated with the peripheral cytoplasm, are free, floating in the vacuoles (13, 14). This fact aaain indicates an altered vitality of the cytoplasm, since in all normal living cells the plastids remain attached in some way. The separation of the plastids from the cytoplasm occurs at maturity, when the inner bounds of this layer appear to fade and become indefinite (13). These many observations, which involve intact as well as sectioned ma- terial and which in part date back to the earliest studies on phloem anat- omy, indicate with increasing conviction that sieve tubes undergo funda- mental changes in their osmotic relations as they reach maturity and are finally obliterated. According to the most logical interpretation, they lose their property of semipermeability and are slowly crushed by surrounding parenchyma cells that survive them by an appreciable period of time. Per- sistent differentiation and ontogeny of tissue are characteristic of the phloeim, and so long as life remains in a plant a certain number of maturing sieve tubes are available to serve their function in conduction. PHILLIS anid MASON (54) object that the highly permeable condition of the mature sieve tube may be an artifact resulting from sectioning. More recently, MASON and PHILLIS (48) state: "In order to insure plasmolysis of the sieve tube it is necessary to carry out the operation on the bark before it is citt and removed from the plant." They do not explain how they arrived at this conclusion; and, since the necessary microscopic observation would require some dissection, one cannot easily understand how the work could be done critically. To be certain of his observations one should carry out the plasmolysis under the microscope, where the condition of the sieve tube before and after treatment could be observed. Only in this way can one determine the ontogenetic state of the tube, its freedom from injury, and its reaction to the treatment. CURTIS objected, several years ago, stating that the permeable condi- tion of the mature sieve tube might be an artifact, but he was unable to substantiate his hypothesis by experiment. Although this point cannot be disregarded, one should remember that the living protoplasm of young sieve tubes an-d of phloem parenchyma cells is not seriously altered by the injury attendinog sectioning. Protoplasmic streaming, vital stain accumulation, and plasmolysis occur in these cells despite the sectioningf process. These cells are connected by protoplasmic connections as are mature sieve tubes. 794 PLANT PHYSIOLOGY There is at present no reason for assigning a special sensitivity to mature sieve tubes. Certainly the evidence indicates lowered rather than increased activity and responsiveness of these cells to injury or manipulation. Slime plugs in sieve tubes have been studied since the earliest investiga- tions of phloem and have been cited as evidence both for and against a mass flow. Recent observations have explained many of the difficulties in inter- preting the relation of slime plugs to translocation. According to a late paper (15), although such structures may be found lodged against the dis- tal sides of sieve plates for several centimeters from the cut end of a cucur- bit stem, removal of a thin slice 1 mm. or less in thickness would cause phloem exudation to be resumed. Slime plugs so located are particulate in structure and consist of the decomposition products of the slime bodies and nuclei. An earlier publication (12) cites instances where slime plugs were formed in different regions in sieve tubes by treatment with heat, al- cohol, and other coagulating agents. Such plugs are usually amorphous. They consist of the normal sieve-tube sap, which can be coagulated either inside or outside the sieve tube by the same agents. The particulate slime plugs therefore indicate a mass flow of solution through the sieve tubes, being composed of material filtered out at the plates. Studies on these structures and on the nearby sieve plates give no indica- tion of perforations within the protoplasmic strands traversing the plates. The amorphous plugs are composed of coagulated sieve-tube sap; and according to studies recently reported (15), this sap may continue to flow from cut stems for periods of 24 hours, coming from great distances along the stem.
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