DEVELOPMENT AND DISPERSAL OF P-PROTEIN IN THE PHLOEM OF COLEUS BLUMEI BENTH.

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1 J. Cell Sci. 4, (1969) 155 Printed in Great Britain DEVELOPMENT AND DISPERSAL OF P-PROTEIN IN THE PHLOEM OF COLEUS BLUMEI BENTH. M. W. STEER AND E. H. NEWCOMB Department of Botany, University of Wisconsin, Madison, Wisconsin, U.S.A. SUMMARY The development of P-protein (slime) in the phloem of Coleus stem apices has been studied electron microscopically using material fixed in glutaraldehyde followed by osmium tetroxide. In phloem parenchyma cells the earliest-appearing groups of tubular P-protein commonly are seen in close association with clusters of ' spiny' vesicles similar to those reported in Phaseolus phloem (Newcomb, 1967). The vesicles break down as the P-protein masses enlarge, and are assumed to contribute to P-protein formation. Subsequently the groups of tubules are consolidated into a single spindle-shaped body aligned longitudinally in each phloem parenchyma cell or sieve element. The microtubules observed frequently in the vicinity of the young P-protein body may play a role in its consolidation or in the longitudinal alignment of its constituent tubules. Some P-protein bodies acquire a highly organized structure in which the tubules are arranged hexagonally around lightly staining centres. Disaggregation of the P-protein body occurs during disintegration of the cytoplasm and nucleus, and results initially in the presence of swirls of packed fibrils. During disaggregation, the tubules of the mature P-protein body, which are about 200 A in diameter, are converted to fibrils about 70 A in diameter in a process apparently with several intermediate stages. In longitudinal view the fibrils exhibit alternate electron transparent and dense bands that impart a striated appearance to the mass. During maturation of the sieve element the swirls of fibrillar masses separate into individual fibrils which become dispersed through the cell lumen. INTRODUCTION Several recent papers have considerably expanded our knowledge of the fine structure of slime bodies in a wide range of plants (Lafleche, 1966; Northcote & Wooding, 1966; Tamulevich & Evert, 1966; Wooding, 1967; Cronshaw & Esau, 1967; Northcote & Wooding, 1968). There now seems general agreement that in many cases the slime body is composed of a mass of tubules approximately 200 A in diameter (Northcote & Wooding, 1966; Tamulevich & Evert, 1966; Wooding, 1967; Cronshaw & Esau, 1967). It has been reported that in the maturing sieve elements these tubules are transformed into a system of fibrils, each having a characteristic alternate light- and dark-staining band along its length (Northcote & Wooding, 1966; Cronshaw & Esau, 1967; Wooding, 1967). Although their dimensions are somewhat dissimilar, the fibrils of the above studies probably represent similar stages in the different plants used. The origin of the slime bodies has not been determined, although Wooding (1967) observed dense vesicles adjacent to developing tubules. Work in this laboratory has provided evidence that 'spiny vesicles' (vesicles bearing small tubular projections) may be involved in the formation of slime bodies in root apices of Phaseolus vulgaris (Newcomb, 1967). The present paper is part of an overall

2 156 M. W. Steer and E. H. Newcomb investigation to confirm this observation and clarify the fine structural changes ocurring in the developing sieve element. It will describe the formation and breakdown of slime bodies in the stem apices and leaf primordia of Coleus blumei Benth. Slime body formation has been studied both in phloem parenchyma and in sieve elements undergoing differentiation. At the level of the light microscope, phloem development in this material has been followed by Jacobs & Morrow (1958, 1967). Esau & Cronshaw (1967) have proposed that the slime body components be referred to as 'P-proteins', and subsequently (Cronshaw & Esau, 1967) have designated the tubules as 'P-i protein' and the banded or striated fibrils as 'P-2 protein'. In our opinion the terms 'slime' and 'slime body' are badly in need of replacement, and ' P-protein' as a class designation is brief, convenient, and suggestive. We are therefore adopting it in this paper. However, the results reported herein as well as the evidence from other work in our laboratory and from recent publications in the field suggest that considerable variability of form exists in P-protein both within and among species, and that different types of P-protein may be interconvertible. We feel, therefore, that it would introduce confusion if we were to attempt to assign 'P-numbers' to our components, at least at this time. Much more information is needed on the range in form and dimensions, the interrelationships, and interconvertibilities of the P-proteins at different stages in the same plant and in a variety of plant species before the validity of distinctive P-numbers can be assessed. MATERIALS AND METHODS Stem apices were dissected from greenhouse specimens of Coleus blumei Benth. and immediately immersed in 3 % glutaraldehyde containing M phosphate buffer at ph 6-8. After fixation in the glutaraldehyde for 3-5 h at room temperature the apices were washed for 1 h in four changes of M phosphate buffer and postfixed in 2 % osmium tetroxide in buffer of the same molarity for 3 h. They were then dehydrated in an acetone series and embedded in Araldite-Epon (Mollenhauer, 1964). Sections were cut on a Servall MT-2 Ultramicrotome with a diamond knife. Thick sections ( /*) were routinely dried on to glass slides and stained with toluidine blue for examination in the light microscope. Thin sections were collected on 300 x 75 mesh copper grids, stained with aqueous 2% uranyl acetate followed by lead citrate (Reynolds, 1963), and viewed in a Hitachi HU-11A microscope at 75 kv with a 30/t objective aperture. OBSERVATIONS Spiny vesicles similar to those first reported from Phaseolus (Newcomb, 1967) are found in young phloem cells in the stem apices of Coleus. Although the 'spines' on the vesicles in Coleus are similar in size to those reported from Phaseolus, it has not been possible to resolve clearly their tubular nature. There is some indication that they are not as well preserved by fixation in Coleus as in Phaseolus. Clusters of spiny vesicles are observed frequently in young phloem parenchyma cells of Coleus; however, they

3 F'-Protein in the phloem of Coleus 157 are smaller and less striking than those encountered in Phaseolus root tips. Since unequivocal evidence for the presence of spiny vesicles in sieve elements undergoing differentiation has not yet been obtained, the following description of P-protein formation from spiny vesicles is based on observations made on phloem parenchyma cells. The description of the subsequent stages is based on observations made on sieve elements and sieve tubes as well as phloem parenchyma. In the earliest observed stages of the formation of tubular P-protein (P1-protein of Cronshaw & Esau, 1967), only a few tubules are present. Frequently these are seen to be intimately associated with a cluster of spiny vesicles, many of which appear indistinct as though undergoing dissolution. An example of a cell at a somewhat later stage is illustrated in Fig. 1, which shows the developing tubules running out from a localized cluster of disintegrating spiny vesicles. Both longitudinal and transverse sections of similar cells have shown that the spiny vesicles are interspersed among the tubules throughout a large part of the cytoplasm. The spiny vesicles in the clusters appear to break down completely; no trace has been found of a possible stage where the vesicles persist after losing their spines. These cells also contain an extensive system of endoplasmic reticulum with associated polysomes. A darkly staining fibrous material, similar in appearance to that observed in Phaseolus (Newcomb, 1967), is present in the phloem parenchyma cells and sieve tubes. Larger accumulations are regularly observed in phloem cells of the stem below the apex and occasionally in the sieve elements of the leaf primordia. The origin and ultimate fate of this material in Coleus have not been determined. In some micrographs it can be seen in association with the spiny vesicles and developing P-protein tubules, suggesting that it may contribute to formation of the latter. The tubules of P-protein are A in diameter, with an inner electrontransparent core about 50 A across. The wall (70-85 A thick) is not uniformly electrondense in longitudinal section. The staining pattern in transverse sections was examined be means of the Markham rotational reinforcement method (Markham, Frey & Hills, 1963); a definite radially repeating structure could not be demonstrated. The aggregation and orientation of the tubules in the sieve elements follows a consistent sequence of development from association of tubules with spiny vesicles to the formation of the completed P-protein body. Initially the tubules appear randomly arranged, but they soon form groups, within each of which they are oriented parallel to one another (Fig. 1). These groups merge to form a single large P-protein body in the parenchyma cell or sieve element (Fig. 2). Clusters of spiny vesicles are not found associated with the larger P-protein bodies in the parenchyma cells, although scattered individual spiny vesicles are occasionally observed around their edges and amongst the tubules. In transversely sectioned sieve elements, developing P-protein bodies are circular to ellipsoidal in outline. Frequently the arrangement of the tubules suggests that the bodies have a definite twist about their long axes. Microtubules are often seen running from the plasmalemma into or alongside the developing P-protein body. Conceivably they may be involved in the longitudinal alignment of the P-protein body in the sieve element. The completed tubular P-protein body is characteristically spindle-shaped in longi-

4 158 M. W. Steer and E. H. Newcomb tudinal section (Fig. 3). In transverse section many of the tubules appear to be arranged in hexagonal patterns around small, central, lightly staining structures. Although this arrangement is observed in earlier stages where the tubules are not all parallel to the long axis of the cell, greater regularity is found in later stages where most of the tubules are parallel as illustrated in Fig. 5. Occasionally fine lines are seen radiating from the tubules (Fig. 5, inset). The possibility that these are interconnecting strands between the tubules has been mentioned by Cronshaw & Esau (1967). Several authors (Northcote & Wooding, 1966; Cronshaw & Esau, 1967; Wooding, 1967) have recorded the conversion of similar P-protein tubules to striated or banded fibrils (P2-protein of Cronshaw & Esau, 1967). Some further details of this conversion have come to light in our observations on Coleus. Accompanying this conversion is the breakdown of the P-protein body. The early stages of the disaggregation of the large spindle-shaped P-protein body occur before extensive disintegration of the cytoplasm and nucleus has taken place. As seen in transverse section the outermost portions of the P-protein body spread outward in a centrifugal manner, so that commonly the cytoplasm is almost filled with large swirls of P-protein. An early stage in this process is shown in Fig. 4. The cytoplasm disintegrates leaving the lumen of the sieve tube largely filled with individual P-protein fibrils and fibrillar aggregates (Figs. 6,7). The latter eventually break down to form uniformly dispersed fibrils. Alteration of structure in~the tubules occurs as the P-protein body disintegrates. Initially, as noted previously, the diameter of the tubules is A and that of the central core 50 A. However, the diameter of the tubules at the earliest recorded stages of P-protein body disaggregation is 170 A and that of the central core is only 30 A. This is illustrated in Fig. 4, where a mass of fibrils has separated from the main body of tubules. At later stages still smaller tubules, with a diameter of about 100 A (central core 25 A), as well as fibrils about 70 A in diameter, can be found together in the same sieve element. These fibrils sometimes appear to have a more lightly staining core, an observation which will be discussed later. Initially, the fibrils to which the tubules give rise are in aggregates. Transverse sections of these aggregates reveal that the fibrils are packed into rows, each row being staggered with respect to the next so that the fibrils are separated from one another by a A electron-transparent space (Fig. 6). In longitudinal section each fibril shows a characteristic structure, consisting of alternating light and dark bands, each approximately 60 A in width. The bands on neighbouring fibrils are coincident, imparting a transversely striped appearance to the aggregates (Fig. 4). Some of these aggregates also have a longitudinal, darkly staining band giving rise to a pattern of squares (Fig. 7). This is believed to result from sectioning the rows of fibrils at right angles. As stated above, these aggregates disperse to form the individual banded fibrils. DISCUSSION The original suggestion that spiny vesicles in Phaseolus root tips contribute to formation of the P-protein tubules (Newcomb, 1967) is further supported by the present

5 F'-Protein in the phloem of Coleus 159 study of Coleus stem apices. Groups of tubules in the earliest stages of formation are seen lying at the edges of clusters of apparently disintegrating spiny vesicles; as the tubular groups enlarge and consolidate, the vesicles disappear. It seems reasonable to assume, therefore, that spiny vesicles contribute some or all of the material required for tubule synthesis, at least in some of the differentiating cells of the procambial strand. Most of this material is presumably proteinaceous, since protein is the major component of P-protein bodies (e.g. see Cronshavv & Esau, 1967). A mechanism must exist for transferring the protein from its site of synthesis on the ribosomes to the spiny vesicles. Some observations that appear relevant to this problem are that in Phaseolus the spiny vesicles are closely associated physically with both endoplasmic reticulum and dictyosomes (Newcomb, 1967), and in Coleus a conspicuous group of cisternae of endoplasmic reticulum is commonly observed lying near the spiny vesicles and developing tubules. Jamieson & Palade (1967 a, b) have reported that in certain animal systems proteins produced by the ribosomes are transferred to the endoplasmic reticulum and thence to the dictyosomes, and are subsequently released in vesicles. It may be suggested that the P-protein is transferred from the endoplasmic reticulum to the dictyosomes similarly, and is then incorporated into the structure of the spiny vesicles. On the other hand, it is possible that the spiny vesicles arise directly from the endoplasmic reticulum. The P-protein may be localized in the spines, since they constitute the unique feature of these vesicles. However, since the entire vesicle structure appears to break down during formation of the P-protein tubules, the fate of the remainder of the vesicle is also in question. The hexagonal arrangement of the tubules in the P-protein bodies may be a peculiarity of the Coleus phloem since it has not been reported from other plants. Also the electron-dense 'centres' around which many of the tubules are arranged have not been reported previously. These centres appear to be an integral part of the P-protein body since they are observed consistently in the later stages of its formation. It is not possible to determine whether the centres persist when the P-protein body disaggregates since they would not be distinguishable from the fibrils in transverse sections of the fibrillar aggregates. The conversion of tubules to fibrils has been investigated in Acer by Northcote & Wooding (1966). Fibrils A in diameter were observed apparently fraying out directly from tubules A in diameter. They suggested that fibrils are formed initially, and that these then associate to form tubules during P-protein body development. These tubules apparently disaggregate to form the original fibrils when the sieve element matures. A subsequent study by Wooding (1967) on the same material has provided further support for this process of disaggregation. In Coleus there does not appear to be a stage at which the tubules are converted suddenly to fibrils; rather, there is a gradation of intermediate forms which are recognizable in thin sections as tubules of progressively smaller diameter. Initially, as the diameter of the tubule decreases from 200 A, the thickness of the wall is only slightly reduced. Later the wall thickness is markedly reduced, since tubules A in diameter can be found alongside fibrils with a diameter of 70 A (Fig. 6). We have been unable to observe the precise manner of formation of fibrils from tubules. The thick-

6 160 M. W. Steer and E. H. Newcomb ness of the tubule wall before P-protein body disaggregation occurs is similar to the diameter of the fibrils formed subsequently (70 A), so that the simple disaggregation process envisaged by Northcote and Wooding would be quite feasible. However, this leaves unexplained the observation of tubules of intermediate dimensions in Coleus. Cronshaw & Esau (1967) have suggested that in sieve elements of Nicotiana the tubules may be converted to fibrils as a result of changes induced in the cytoplasm by the vacuolar contents following breakdown of the tonoplast. Such a mechanism does not appear to occur in Coleus since the tonoplast is still intact when the first fibrils are formed. A possibly related difference between the two species is that in Coleus, tubules are not observed to persist in mature sieve tubes, as reported for Nicotiana. In Acer (Northcote & Wooding, 1966; Wooding, 1967) the alternating lightly and darkly staining bands of the fibrils impart a striated appearance to the fibrillar aggregates. A similar staining pattern has also been observed in the fibrils of Nicotiana and their aggregates by Cronshaw & Esau (1967). It should be emphasized that in Coleus the fibrillar aggregates are derived directly from the P-protein body and that subsequently they disaggregate to give free, individual fibrils. In the aggregates many of the fibrils appear to have a more lightly staining core in transverse section, suggesting a tubular structure. However, this may be due to an uneven staining pattern, as can be seen in longitudinal sections of the fibrils. It appears that there is considerable variation in the form of P-protein even in the relatively few_species of plants so far examined in detail. The sequence followed in its development in Coleus seems to resemble the general pattern of development previously reported for Nicotiana and Acer. However, Phaseolus, in which a large crystalline P-protein body is produced (Lafleche, 1966), and Cucurbita, in which several darkly staining spherical bodies are formed in each sieve element (Esau & Cheadle, 1965; Evert, Murmanis & Sachs, 1966), are two examples of species having apparently quite different patterns of development. Thus the pathway of P-protein differentiation seems to be variable among different species of plants, suggesting that a detailed study of this in a wide range of materials will be required before any general conclusions can be reached. Of particular interest is the form that the P-proteins take in the mature and presumably actively transporting sieve tubes. It is interesting to note, in light of the current view that they may participate in the translocation process, that in the three species (Acer, Nicotiana and Coleus) for which sufficiently detailed observations are available the P-proteins of the mature sieve tubes are quite similar in appearance. This work was supported in part by Grant GB-6161 from the National Science Foundation. REFERENCES CRONSHAW, J. & ESAU, K. (1967). Tubular and fibrillar components of mature and differentiating sieve elements. J. Cell Biol. 34, ESAU, K. & CHEADLE, V. I. (1965). Cytologic studies on phloem. Univ. Calif. Publ. Bot. 36, ESAU, K. & CRONSHAW, J. (1967). Tubular components in cells of healthy and tobacco-mosaic virus infected Nicotiana. Virology 33, EVERT, R. F., MURMANIS, L. & SACHS, I. B. (1966). Another view of the ultrastructure of Cucurbita phloem. Ann. Bot. N.S. 30,

7 P-Protein in the phloem of Coleus 161 JACOBS, W. P. & MORROW, I. B. (1958). Quantitative relations between stages of leaf development and differentiation of sieve-tubes. Science, N.Y. 128, JACOBS, W. P. & MORROW, I. B. (1967). A quantitative study of sieve-tube differentiation in vegetative shoot apices of Coleus. Am. J. Bot. 54, JAMIESON, J. D. & PALADE, G. E. (1967a). Intracellular transport of secretory proteins in the pancreatic exocrine cell. I. Role of the peripheral elements of the Golgi complex..?. Cell Biol. 34, JAMIESON, J. D. & PALADE, G. E. (19676). Intracellular transport of secretory proteins in the pancreatic exocrine cell. II. Transport to condensing vacuoles and zymogen granules. J. Cell Biol. 34, 597-6i5- LAFLECHE, D. (1966). Ultrastructure et cytochimie des inclusions flagellees des cellules criblees de Phaseolus vulgaris. J. Microscopie 5, MARKHAM, R., FREY, S. & HILLS, G. T. (1963). Methods for the enhancement of image detail and accentuation of structure in electron microscopy. Virology 20, MOLLENHAUER, H. H. (1964). Plastic embedding mixtures for use in electron microscopy. Stain Technol. 39, NEWCOMB, E. H. (1967). A spiny vesicle in slime-producing cells of the bean root. J. Cell Biol. 35, C17-C22. NORTHCOTE, D. H. & WOODING, F. B. P. (1966). Development of sieve tubes in Acer pseudoplatanus. Proc. R. Soc. B 163, NORTHCOTE, D. H. & WOODING, F. B. P. (1968). The structure and function of phloem tissue. Sri. Prog., Oxf. 56, REYNOLDS, E. S. (1963). The use of lead citrate at high ph as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, TAMULEVICH, S. R. & EVERT, R. F. (1966). Aspects of sieve element ultrastructure in Primula obconica. Planta 69, WOODING, F. B. P. (1967). Fine structure and development of phloem sieve tube content. Protoplasma 64, (Received 20 March 1968) Cell Sci. 4

8 162 M. W. Steer and E. H. Newcomb Fig. i. A glancing longitudinal section of a differentiating phloem parenchyma cell in which P-protein tubules are apparently arising from clusters of disintegrating spiny vesicles. The circled cluster of vesicles is shown at higher magnification in the inset. Other spiny vesicles are also discernible at the edges of the tubular mass. A sieve tube (st) is present in the lower left, x 32000; inset, x

9 st P-Protein in the phloem of Coleus 163

10 164 M. W. Steer and E. H. Newcomb Fig. 2. Longitudinal section of a differentiating phloem parenchyma cell showing a stage in the aggregation of groups of tubules into a P-protein body, x Fig. 3. Longitudinal section of a fully developed P-protein body in a sieve element. Most of the tubules lie parallel to one another and approximately parallel to the long axis of the cell, x

11 P-Protein in the phloem of Cokus.* -^ jj^

12 166 M. W. Steer and E. H. Newcomb Fig. 4. Oblique section through a P-protein body in an early stage of disaggregation. Many of the fibrillar aggregates in the lower part of the figure exhibit a characteristic striated pattern in longitudinal section, x

13 # P-Protein in the phloem of Coleus ^

14 168 M. W. Steer and E. H. Newcomb Fig. 5. Transverse section of a sieve element containing a completed P-protein body. The regular hexagonal arrangement of the tubules around electron-dense centres is evident. The inset shows this at higher magnification. Fine lines can be seen radiating from some of the tubules, x 30000; inset, x Fig. 6. Transverse section of fibrillar aggregates formed at later stages of P-protein body disaggregation. A region can be seen where the rows of fibrils are staggered with respect to one another, x Fig. 7. A relatively uncommon square pattern seen in longitudinal sections of fibrillar aggregates. It is possible that this pattern results from sectioning an aggregate normal to the rows of fibrils, x

15 P-Protein in the phloem of Coleus

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