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in Pinophyta

G. S Paliwal

Paliwal GS 1992. Phloem in Pinophyta. Palaeobotanist 41 : 114·127.

The gymnospermous phloem shows major differences from those of the cryptogams on one hand and the angiosperms on the Other. These include both the type of conducting cells as well as the cellular composition. Even more important is the degree and nature of functional inter· relationship between the conducting and parenchyma cells. The following evolutionary trends have been suggested: Increase in the amount of axial parenchyma; Decrease in the number of albuminous cells in the rays; Increase in the axial albuminous cells: Increase in the fibres; Increase in the regular arrangement. of cells The work on the fossil taxa does prOVide variable suppOrt to these suggestions. It is generally believed that the cryptogamic sieve element arose from a parenchyma cell and all the phloem produced in the fossil lycopods, Sphenopsida and ferns is primary in origin. Here the phloem consists of either sieve elements only or the sieve elements with scattered parenchyma cells. There is no definite relationship between the conducting elements and the parenchyma cells as seen in the . Additional parenchyma is often present in the form of a sheath separating the ,-ylem from the narrow phloem tissue. The typical cryptOgamic sieve elements are identical to the elongate parenchyma cells. These are relatively small in diameter, longer than the parenchyma cells but shorter than the gymnospermous sieve cells. In some taxa, the sieve elements are of twO sizes: large (up to 600 /lm) and small (between 100·1,500 /lm). The end walls of the cryptogamous sieve elements are horizontal or slightly oblique and the sieve areas are small and vary markedly in their outline. The sieve pores occur in the sieve areas as well as scattered on the vertical walls. The callose deposition has been found in Psi/otum, lycopods and the ferns. Key-words-Evolution, Phloem, Pinophyta, .

G. 5. Paliwal, Developmental Botany Laboratory, Department of Botany, H.N.B. Garbwal University, Srinagar 246 174, Pauri, India.

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Essays in Evolutionary Biology Edlro,..: B. S Vcnkatachala, David L. Dilcher & Hari K. Mahcshwarl Publisher: Bltbal Sahnl InStitute of Palaeobotany, Lucknow PALIWAL-PHLOEM IN PINOPHYTA 115

THE sieve elements in gymnosperms have been Available data are based mainly on two species~ investigated since the early part of the 18th century. Cycas circinalis Strasburger 1891 and Microcycas The studies chiefly concern secondary phloem, calocoma Chrysler 1926. mostly of Pinatae. Recently, Gnetatae has also been The axial system of the secondary system worked out in fairly good details. Kollmann· (1964, contains sieve elements, parenchyma ceils, and 1%8): Esau (1969), Behnke (1971) and fibres. The sieve elements are relatively long with Panhasarathy (1975) have reviewed the phloem inclined end walls, and their faces merge with the structure and ontogeny. Behnke (1974) has provided radial lateral walls. The sieve areas are variable in a survey of the types in the sieve cells of shape and occur on end walls, and the radial faces of gymnosperms. lateral walls. In the present article an attempt has been made Parenchyma cells are of two kinds~those to bring together the present state of available containing starch, and sometimes druses of calcium information on the structure of this complex tissue. oxalate, and the albuminous cells. In the non­ It would be seen that more and more investigators functioning phloem, the starch-containing cells have concentrated their attention on the Pinicae remain intact, and the albuminous cells collapse. (taking both the stem and the needle), and despite Chrysler (1926) also noted pits in the walls between its importance as a distinct line of the seed plants, adjacent parenchyma cells and believed them to be only limited research has been done on the identical in shape and distribution to the sieve areas Cycadicae and Gneticae (where the leaves have been in the sieve elements. the chief object of analysis), although a beginning Apparently, in the cycads the primary phloem of had been made by Mettenius as early as 1861. the leaf is devoid of fibres. In the older petioles and stems, the prolO-phloem is cn..lshed. Metaphloem CYCADICAE' tissue contains wide sieve elements and narrower parenchyma cells. Parenchyma also separates the The phloem of cycads is rather poorly known. tracheids from the sieve elements. The genera investigated are listed in Table 1. Within the transfusion tissue located on the

Table I-Phloem in Pinophyta (Gymnosperms)

TAXON/GROUP SPECIES OR GROUP AUTHORS OPTICAL EM YEAR INVEST!GATED

A. Cycadicae Medulossa sp. Smoot, E. L. + 1984 Cycas circinalis Strasburger, E. + 1891 Cycas revolufa Mellenius, G. + 1861 Dioon edule Dippel, L. + 1869 Microcycas calocoma Chrysler, M. A. - + 1926 Zamia Parthasarathy, M. V. - + 1975

B. Pinicae 1. Ginkgoatae Ginkgo biloba Bertrand, C. E. + 1874 Seward, A. C. & Gowan, J. + 1900 Chauv~aud,G • 1903 Sprecher, A. + 1907 Gunckel, J. E. & + 1946 Wetmore, R. H. Srivastava, L. M. + - 1963 Dute, R. R. + + 1983

2. Pinaceae Abies conocolor Wilson, B. F. 1963 A. pindrow Chauveaud, G. + - 1902b A. procera WilcOX, H. + - 1954 A. sachalinensis Shimaji, K. + - 1964 Abies sp. Grillos & Smith + 1959 Dacrydium sp. !lese, W. & Malle, V. 1962 Knudson, L. + 1913 TimeJI, T. E. + 1973 Brudarmann, G. & - 1973 Koran, Z.

·Terminology after CronqUist e/ al. (1966). Con/do 116 THE PAlAEOBOTANIST

Table l-Contd.

TAXON/GROUP SPECIES OR GROUP AUTI-IORS OPTICAL EM YEAR l1\TVESTIGATED

Pinus nigra Sauter, T T., Dorr, I. & + 1976 Kollmann, R. P. pinea Wooding, F. B. P. + 1966 P. pinea Wooding, F. B. P. + 1.968 P. pinaster Carde, J. P. + + 1973, 1974 P. radiara Mahmood, A. 1965 P. radiata Barnen, J. R. + 1971a P. radiaia Singh, A. P. 1984a, b P. radiata Barnett, J. R. + 1974 P. resinosa Campbell, R. +C 1972 P. resinosa Neuberger, D. S. + 1973 P. resinosa Neuberger, D. S. & + 1974, 1975 Evert, R. F. P. resinosa Neuberger, D. S. & + 1976 Evert, R. F. P. rigida Brown, H. P. + -C 1912 P. sabiniana Alosi, M. C. & Park, R. B. 1983 P. strobus Brown, H. P. + 1915 P. strobus Abbe, L. B. & + 1939 Crafts, A. S. P. strobus Evert, R. F. & + 1965 Alfieri, F. J. P. strobus Murmanis, L. & + 1966 Evert, R. F. P. strobus Srivastava, L. M. & + 1966b O'Brien, T. P. Murmanis, L. & + 1967 Evert, R. F. P. strobus Srivastava, L. M. + 1969 P. strobus Murmanis, L. + 1970, 1972 P. strobus Chafe, S. C. & + 1972 Doohan, M. E. P. strobus Murmanis, L. + 1974 P. sylvestris Hill, A. W. + + 1901 P. sylvestris Parameswaran, N. & + 1970 liese, W. P. sylvestris Parameswaran, N. + 1971 Preston, R. D. + 1963 Thaine, R. M. C. + + 1964 Parker, B. C. + 1965 P. sylvestris Warmbrodt, R. D. & -m 1985 Eschrich, W. Pinus sp. Wooding, F. B. P. & + 1965b Nonhcote, D. H. Pinus sp. Alfieri, F. J. & + 1968a, b Even, R. F. Pinus sp. Mahmood, A. 1968 Pinus sp. Schulz, A., Alosi, A. C, -C ]989 Sabnis, D. B. & Park, R. B. taxijolia Sterling, C + 1947 P. taxijolia Braun, H. J. & + 1965 Den Outer, R. W. P. menziesii Gourret, T. P. & + + 1974 Strullu, D. G. Abietineae Chrysler, M. A. + ]913 Pinaceae Barghoorn, E. S. + 1941 Pinaceae Muhlethaler, K. - + 1950 m·mycorriza Pinaceae Roelofsen, P. + 1959, 1965 Pinaceae Srivastava, L. M. + ]96~ Contd. PALIWAL-PHLOEM IN PINOPHYTA 117

Table l-Contd.

TAXON/GROUP SPECIES OR GROUP AUTI-IORS OPTICAL EM YEAR INVESTIGATED

Pinaceae Harris, W. M. + 1972

3. Taxodiaceae Metasequoia Kollmann, R. & + 1961 giyptostroboldes Schumacher, W. M. glyptostroboides Kollmann, R. & + 1962a Schumacher, W. M. glyptostroboides Kollmann, R. & + 1962b Schumacher, W. M. glyptostroboides Kollmann, R. & + 1963 Schumacher, W. M. glyptostroboides Bacher, T. W. + 1964 M. glyptostroboides Kollmann, R. & + 1964 Schumacher, W. M. glyptostroboides Kollmann, R. + 1965 M. glyptostroboides Willenbrink, J & 1966 Kollmann, R. M. glyptostroboides Kollmann, R. 1967 Metasequoia sp. Schumacher, W. + 1967 M. glyptostroboides Hebant, c. -C 1975 Sequoiadendron giganteum Hebant, c. -C 1975 Sequoia sempervirens Isenberg, I. + 1943 S. sempervirens Sterl ing, C. + 1946

4. Callitris sp. Bamber, R. K. + 1959 Chamaecyparis obtusa Pesacreta, T. C. & + + 1986 Parthasarathy, M. V. JUniperus communis Kollmann, R. & Dorr, I. + 1966 Thuja orientalis Chauveaud, G. + 1902 Pinicae Abbe, L. B. & Crafts, A. S. + 1939 Huber, B. & Graf, E. + 1955

Gneticae Ephedra Thompson, W. P. + 1912 Hepton, C. E. L. & + 1960 Preston, R. D. £. americana Nosi, Margaret, C. + 1972 & Alfieri, F. J £. cali/ornica Alfieri, F. J & + 1983 Mottola, P. M. Welwitschia bainesii Evert et at. + 1973 Gnetaceae Bertrand, E. E. + 1874 Gnetaceae Boodle, L. A. & + 1894 Worsdell, W. C. Gnetaceae Strasburger, E. + 1891 Gnetum and angiosperms Thompson, W. P. + 1919 Gnetum Mltheshwari, P. & + 1961 Vasil, Vimla Gnetum gnemon and Behnke, H. D. & + 1973 Ephedra campylopoda Paliwal, G. S. Gnetum gnemon Paliwal, G. S. & + 1973 Behnke, H. D. PINOPHYTA Bertrand, C. E. + 1874 Moeller, J + 1882 Feustel, H. + 1921 Holdheide, W. + 1951 Chang, Y. P. + 1954a, b Behnke, H. D. + 1974 C=Chemical analysis; m=Mycorriza.

flanks of the bundle, the parenchyma cells next to suggested that these cells serve as intermediate cells the phloem are rich in cytoplasmic contents and comparable to the albuminous cells. have rather large nuclei. Strasburger (1891) had The ultrastructure of sieve elements of Zamia 118 THE PALAEOBOTANIST pseudoparasitica reveals that the ontogeny is PINACEAE identic;!l to that of the Pinaceae (Panhasarthy, 197'5). However, unlike the necrotic nuclei reponed by Srivastava (1963b) presented a comprehensive various authors, here the nuclei have been observed study of Pinaceae with regard to different cell types, at various stages of degeneration. P-protein is their distribution, origin of the tissue component in lacking, as 10 other gymnosperms. The other cell the cambium, and the problem of proper organelles also exhibit a similar behaviour during interpretation of the albuminous cells covering 13 differentiation. Aggregates of ER that normally occur species. Evert and Alfieri (1965) studied five species on both sides of sieve areas in the mature sieve cells of Pinaceae. and appear to be interconnected by elements of ER The first detectable change in the cambial traversing the sieve pores, have also been noticed. derivative, destined to become the sieve cell is the marked increased in cell volume, accompanied primarily by radial expanSion. Soon afterwards, it GINKGOATAE begins to deposit secondary wall thickening which is characteristic to this family and is lamellar in Bertrand (1874) was the first to examine the appearance. Older cells have more lamellae in their secondary phloem of Ginkgo biloba, Salisburia walls than the younger ones, a fact which indicates adjantifolia in which he found the sieve elements that the deposition of the wall material continues for (cellules grillagees) to be wider as compared to sometime Throughout these changes, the cytoplasm those of He distinguished fibres, retains the usual compliments of organelles. Rough parenchyma cells, and sieve elements in the phloem ER is evident in the form of cisternae and vesicles of stems and noticed the enlargement of and the ground substance is rich in free ribosomes. parenchyma cells in the older phloem. Strasburger In some instances, fine fibrillar material can be (1891) discussed cenain features of the secondary detected in the vesicles of the rough ER. phloem, especially the albuminous cells in this Mitochondria and dictyosomes are abundant and the taxon. conex of the cell contains microtubules which are Although comparatively less homogeneous in usually oriented parallel to the long axis of cell. appearance, the precursory phloem elements in The also undergo changes. These Ginkgo are similar to those of the Pinatae. The sieve accumulate a few electron dense bodies in the elements differentiating at a later stage have rather stroma, SOme of which reach a size of 1-2 iLm in distinct sieve areas. Srivastava (1963a), too found the older sieve lements (Srivastava & O'Brien, 1966; secondary phloem to be similar to that of Pinatae in Barnett, 1974). These crystals are thought to be being composed of sieve elements, parenchyma proteinaceous and show weak refrigence under strands, and fibres in the axial system and rays in the polarized light. Their origin and significance is not radial system. He, however, did not confirm the known but these may have developed from the presence of fibres in the secondary phloem of shon osmiophilic intralamellar inclusions in the plastids shoots which had abundant druses as reported by of cambial initials. Similar inclusions have been seen Seward and Gowan (1900), Sprecher (1907), and in the sieve elements of cenain dicotyledons also, Gunckel and Wetmore (] 946). e.g., Datura (Hohl, 1960), Pisum (Bouck & The albuminous cells associated with the sieve Cronshaw, 1965), and Avena (O'Brien & Thimann, cells lack starch, and get crushed in the old phloem. 1967); although in the last two instances it has not These are connected to the sieve cells by one-sided been shown that these bodies have been derived sieve areas. As callose was not present in sufficient from plastids. It is to be noted here that Wooding quantity, lateral connections between sieve elements (1966) has described in ray plastids the and al buminous cells remained untraced. These accumulation of granules, comparable in staining to cells also have plastids but do not store normal, the starch grains. detectable starch. The second stage of differentiation involves The fibres are elongated, tapering elements that drastic changes in the organ~lIesand membrane are flattened tangentially. These are non-septate as systems of the cell. The cisternae of rough ER observed in the macerated tissue. They have a vesiculate funher, lose their ribosomes, and then the narrow lumen and thick, distinctly lamellated walls vesicles disappear. Simultaneously, a new reticulum which appear to be composed of cellulose. These do is formed, composed of large cisternae which in not give positive staining with phloroglucinol and several instances occur close to the wall. Bouck and HCI and are strongly birefringent under polarized Cronshaw (1965) refer it as the 'sieve tube light. reticulum' (STR), since these also occur in the sieve PAUWAL-PHLOEM IN PINOPHYTA 119

ce lis, whereas Srivastava and 0 'Brien (1966) have from the two sides may join after following a path. termed it as sieve element reticulum (SER). During The 'pores' in the walls of dead sieve elements are these changes in the ER, ribosomes and dictyosomes certainly much wider than the plasmodesmata. become infrequent and are no longer deteCted in Barnett (1974) has critically analysed this aspect of the cytoplasm. the sieve cells of . He did not record Even and Alfieri (] 965) have reponed the any simple pits in the radial walls of the cambium. presence of necrotic nuclei in the mature sieve cells Gradually, the wall thickness increases in these Muramanis and Even (] 966), Srivastava and O'Brien regions, although these are devoid of the lamellar (]966), \Xiooding (1966, 1968) and Neuberger appearance like the rest of the walls. In an almost (J 973) have identified ~omparablestages of nuclei mature sieve area, the difference in the structure in the mature sieve elements. In the elements between the cell wall and the material of which the immediately adjacent to the crushed phloem, the cell plate is made is more obvious. Usually a sieve vesicular masses, nuclear remnants, and plate is homogeneous, staining evenly, but the mitochondria associated with longitudinally remaining cell wall is lamellar in structure. ThiS is stranded material persist along the wall, and the the stage when communication channels begin to lumen of sieve elements appear completely empty develop between the cells. Later these widen until The inclusions of the sieve element plastids these have become large enough for entire disappear by the time it is mature, and they contain organelles to pass through them. The pores in the only granules resembling starch in their staining wall are lined by plasmalemma (Srivastava & behaviour (Pinus pinea; Wooding, 1966, Wooding O'Brien, 1966), but Wooding (1966) observed them & Nonhcote, 1965b). In Pinus radiata and p to be lined by callose as revealed by fluorescence strobus the crystalline inclusions change to a fibrillar microscopy. form. Callose-Some authors believe that the callose The mature sieve elements of have a thick, is scanty or lacking in the functional sieve element lamellated secondary wall, separated from the and that the relatively large amount of callose seen cytoplasm by a persistent plasmalemma. The in the sieve element is an artefact of fixation and peripheral cytoplasm is composed of an elaborate' sectioning (Zimmermann, 1960; Craft & Currier, system of smooth ER in the form of long cisternae ]963; Eschrich, 1963; Evert & Derr, 1964). Others, Somewhat abnormal mitochondria are often though not denying the earlier postulate yet, enmeshed between these cisternae Plastids are maintain that callose does occur naturally and lines present in various stages of breakdown, along\vith the sieve pores (Esau & Cheadle, 1965; Esau et aI., the starch grains and prOtein crystalloids The 1962; Engleman, 1966a; Srivastava & O'Brien, 1966). ground substance is composed of a fine fibrillar material, derived either from the stroma of Cell wall-Srivastava (1969) advanced a degenerated plastids, from the rough ER, or both. somewhat unorthodox concept of microfibrillar Degenerating nuclei are mostly present, but the orientation for the sieve cell walls of white pine. He vacuolar membranes, dictyosomes, and ribosomes enVisaged a wall composed of lamellae in which are absent. Microtubules may be present at maturity microfibrils are aligned at an angle to or at both the but they are difficult to distinguish with certainty. horizontal and venical axis of the cell. This suggests Plasmalemma seems to be maintained even in the that not only are the microfibrils subtending the advanced stages of sieve element differentiation, but horizontal axis at an angle as seen in the surface the initial, three-layered structure is ruled out at this (tangential) view, but also at an angle to the vertical stage (Srivastava & O'Brien, 1966). Barnen (1974) axis when the wall is viewed in sectional planes. has recorded stacks of hexagonally packed tubules Chafe and Doohan (1972) demonstrated that, in the lumen of sieve elements of P. radiata. contrary to Srivastava's (J 969) concept, the The earliest detectable change in the initiation microfibrils are always oriented parallel to the cell of the sieve area has been noticed soon after the cell wall and they describe'S' or 'z' helices around the wall formation has begun. The formation of sieve cell wall. Obselvations with polarized light suggest pores, i.e., whether the sieve areas arise from the pit that the orientation of most microfibrils is higher fields in the fusiform initials from which the sieve than 45 0 with respect to the cell axis. Oblique cells have been derived or whether their origin is de sections through the cell wall indicate an orientation novo, needs explaining. Srivastava and O'Brien of moderately low helical pitch perhaps 50-60 0 or (1966) explained that some boring of the wall more from the cell axis. Therefore, these authors occurs, because a cavitymedian nodule is formed held that the observations of Srivastava (1969) may where none existed before. Furthermore, strands be due to oblique sectioning of the walls. 120 THE PALAEOBOTANIST

The microtubules play an important role in the resemblance to the slime. Neuberger (1973) and regulation of wall synthesis among the later Neuberger ar'd Evert (1974) indicated that P­ angiospermous taxa (Ledbetter & Porter, 1963; protein is absent in Pinus. Interestingly enough, Hepler & Newcomb, 1964; Cronshaw, 1965; Thaine (1964) had reported discrete strands running Cronshaw & Bouck, 1965). Srivastava (1969) in the sieve elements, between the sieve pores in observed microtubules in the sieve cell cortices and which material is translocated. their persistence in the later stages of differentiation Parenchyma Cells-It has been pOinted out that in Pinus strobus also. This led him to conclude that the organelle component of the parenchyma cells these may serve more than one function in the and the other cells are similar. Srivastava and . Wooding (1966) and Barnett (1974), O'Brien (1977) found the cytoplasm of the however, could not confirm their association with albuminous cells of Pinus strobus to be rich in the process of cell wall formation. On the other mitOchondria and rough ER. Traditionally, the hand, in the initial stages of development of the cell, companion cells of the angiosperms have been large number of golgi bodies were found to be implicated as a likely centre of energy supply for at present together with the microtubules close to the least some of the processes involved in the transport plasmalemma. of solutes. Plastids- The sieve cell plastids are among the first organelles to indicate structural changes during TAXODIACEAE cell differentiation. Crystalloids, starch granules, Moeller (1882) described the arrangement, filamentous material or osmiophilic globules may be types of crystals, and their distribution in a few formed in the plastids depending upon the species. species, such as Cunninghamia sinensis, Podocmpus For example, all the four types of inclusions may be thunbergii, Sequoia gigantea, Taxodium distichum found in the sieve cell plastids of Pinus species and Taxus baccata. Strasburger (1891) reported the (Srivastava & O'Brien, 1966; Murmanis & Evert, 1966; presence of albuminous cells in Taxodiaceae. Wooding, 1966; Parameswaran & Liese, i970; Holdheide (1951) gave a description of the phloem Parameswaran, 1971; Barnett, 1974; Sauter, 1974) of Taxus baccata. and Picea abies (Timell, 1973). As the differentiation of the sieve elements begins, the plastids undergo Sieve cell protoplast and sieve plate interesting changes. They accumulate a few electron differentiation dense bodies in the stroma. Some of these reach a Kollmann and Schumacher (1964) observed in size of 1-2 J..Lm in the older sieve elements. These Metasequoia a remarkable though temporary, have been referred to as 'crystalloids'. It has been increase and expanSion of the endoplasmic suggested that they may arise from the osmiophilic reticulum throughout the cell lumen of the sieve intralamellar inclusions present in the plastids of elements during development. Plastids also begin cambial initials (Srivastava & O'Brien, 1966). Similar differentiation simultaneously. structures have been seen in the sieve elements of Nuclear disintegration in Metasequoia sieve Datura (Hohl, 1960) and Avena (O'Brien & cells appears to be preceded by a coarsening of the Thimann, 1967). Recently, Behnke (1974) has internal structure of the swollen nucleus which is reviewed the organization of sieve element plastids plainly visible under the electron microscope. The of gymnosperms and concludes that all the Pinaceae nuclear substance is particularly conspicuous examined possess p-type plastids, characterized by a (Kollmann & Schumacher, 1961). Later, there is a peripheral, ring-shaped bundle of protein filament, general loosening of internal Structure of the an additional protein crystalloid and several starch nucleus accompanied by remarkable changes in the grains. The latter are mostly club-shaped. nuclear envelope (Kollmann, 1961a). The P-protein-Structures referable as 'slime' or 'P­ endoplasmic reticulum may play a part in the protein' have been observed in the sieve elements of subsequent resorption of the nuclear substance different species of Pinaceae (Srivastava, 1963; Evert (Kollmann, 1960). The nucleus in Metasequoia & Alfieri, 1965). Abbe and Crafts (1939) commented (though of a changed shape) is seen in sieve on their .'transitOry' nature. Observations of sieve elements near the cambium with well-developed elements with electron microscope have produced plasmatic connections (Kollmann,1961 a; Kollmann & conflicting results with regard to P-protein in Pinus. Schumacher, 1961). This is in contrast to the reports However, Srivastava and O'Brien (1966) and Barnett in Cucurbita maxima, where the nuclei disintegrate (1974) documented the origin of this fibrillar in the differentiating sieve elements before the sieve protein from the plastid matrix and doubted its pores develop (Esau et al, 1962). PALIWAL-PHLOEM IN PINOPHYTA 121

Sieve areas in presumably active sieve cells have cells of Taxodiaceae. Although albuminous cells are an extensive median nodule which is about 3 J..'m in present in the phloem, not all of them are connected diameter and is represented by a lens-shaped cavity with the sieve cells (Schumacher, 1967). in the region of the middle lamella and the primary walls of the sieve area containing dense cYtoplasmic CUPRESSACEAE structures. From this median nodule, many protoplasmic strands, about 50-80 (max. 350) J..'m in Differentiation of the sieve cells is similar to diameter, pass to the protoplast of both adjacent that of the Pinaceae although in contrast to the latter sieve cells. the sieve elements do not have secondary walls but Sieve areas in the sieve cells are localized possess numerous small crystals in the middle mainly on the radial tapering end walls, each lamella of the radial walls of all the cell types. Such measuring 4-5 square micron and containing about 7 crystals are absent at the sieve areas and the primary sieve pores per square micron. The diameter of the pit fields (Evert & Alfieri, 1965). Perhaps the crystals sieve pores vary between 50-500 J..'m. Connecting encountered in this study are similar to the granules, strands of about 270 J..'m are observed with sufficient Chang (1954a, b) had reported for this plant. Slime frequency (Kollmann & Schumacher, 1962). bodies were described in young sieve elements. A comparative study of the fine structure of Internal strands traversing from one cell to another, cytoplasmic strands in the sieve areas and pit-fields through the sieve area pores, have also been seen in give best support to the common concept that the both fresh and PAA-fixed tissue. Srivastava (1963) connecting strands are highly differentiated interpreted these as 'slime'. The plastids (Behnke, plasmodesmata. Kollmann (1964) postulated that 1974) of Calocedrus decurrens, Chamaecyparis the sieve elements should be considered as nootkatensis, Jumperus fragrans, and Thuja plicata functional from the moment the differentiated are of the P-type. connect1ng strands join the adjacent protoplast, which are established in the very early stage of sieve GNETICAE element development. In that case all the changes which fake place later in the cytoplasmic fine Maheshwari and Vasil (1961) compiled structur'e and which ultimately lead to the information on the phloem of Gnetum. During the degeneration of the sieve cell, might be considered past few years the phloem of this taxon together not to' be a prerequisite to, but rather a result of the with the other two genera has been investigated physiological functions peculiar to the conducting both with the light as well as electron microscopes. element. Well-differentiated plastids occur in sieve cells EPHEDRACEAE whose protoplast is still intact. These have an internal matrix with numerous vesicles, occasional The secondary phloem of the genus Ephedra electron dense tubules and a few stroma membranes comprises sieve elements, two kinds of axial which are continuous with the layer of limiting parenchyma cells, and multiseriate parenchymatic membrane. During spring and summer, the plastids rays, reported to be absent in Gnetaceae. The older form many starch grains within the stroma. In the phloem contains fibre·sclereids as a real cell type. dormant phloem, the starch is only rarely found but Sieve elements bear sieve areas on the radial walls in later stages the internal structure of the plastid is and on the walls common with the albuminous cells. greatly reduced and many starch grains are stored. Within the sieve area, pores are generally combined Finally when the sieve element has become fully in groups; the latter have been termed as sieve fields differentiated, the plastids have poorly organized (Russow, 1882; Strasburger, 1887; Hill 1901; Evert & internal matrices and are almost completely filled Alfieri, 1965). Each pore, whether in a lateral sieve with starch grains of different shapes and sizes. Their or on the overlapping end wall, measures matrices become more and more electron approximately 0.8 J..'m. Sieve areas have not been transparent as cell differentiation progresses. recorded on the transverse walls between sister Behnke (1974) reports only S-type plastids in the cells, whether they be two sieve cells or a sieve cell sieve elements of other members of Taxodiaceae, and an albuminous cell (Alosi & Alfieri, 1972). viz., Cryptomeria japonica, Sequoiadendron Callose occurs as only a narrow layer of the sieve giganteum and Taxodium distichum. elements. The starch·containing-parenchyma cells P-protein is absent in the sieve elements of may maintain their integrity or develop secondary Metasequoia glyptostroboides (Koll mann, 1964). walls and become fibre-sclereids. Strasburger (1891) Scanty information is available on the parenchyma stated that albuminous cells are found in the axial 122 THE PALAEOBOTANIST system and form continuous files or are dispersed in Mature sieve elements have blunt to tapering the same row with starch-containing cells. These are ends. Their waJls remain thin with no nacreous or generally half the length of sieve cells (Alosi & secondary thickening. The sieve elements faJl intO Alfieri, 1971). tWO categories based on their length: those about Ray cells accumulate calcium oxalate in the 400 /-Lm long and other measuring only 220 /-Lm. The middle lamella in the form of rod-shaped crystals, former are the direct derivatives of the fusiform similar to the crystals seen in the phloem cell waJls initials whereas the latter arise after a transverse of Juniperus (Evert & Alfieri, 1965). division in their precursors. Alosi and Alfieri (1972) have described the stranded and thread-like Ontogeny of the secondary sieve element composition of the slime-body and have shown The ontOgeny of pholem in Ephedra calijornica intracellular sieve area connections through these and E viridis has been observed by Alosi and Alfieri thread-like structures. However, this information (1972). Behnke and Paliwal (1973) have recorded needs further confirmation, especiaJly because toe some features of the sieve cells and parenchyma occurrence o"f P-protein has been contradicted by cells of E. campylopoda. Behnke and Paliwal (1973). Phloem initials look very similar to the cambial Albuminous cells have connections with the initials from which these have been derived. They smaJl sieve areas of adjoining cells. An ovoid body, possess long, thin, granular nuclei with several about 3 /-Lm in diameter appears just after transverse nucleoli, delicate cell walls with primary pit fields, divisions of the phloem mother cells and lies near small radial diameter, very oblique end walls, and the newly constituted daughter nucleus. Because of lightly staining cellular COntents. However, an ovoid its positive reaction with Ponceau S, this body has body appears in the differentiating cell. It is often been referred to as slime-body as in the located near the nucleus and resembles in shape and angiospermous sieve elements. Ultrastructural staining the largest nucleolus observed. Some of the studies by Behnke and Paliwal (1973), however, fusiform phloem derivatives undergo a transverse failed to confirm this inference. The albuminous division before developing into shorter sieve cells cells have dense protoplasm, rich in elongated (Alosi & Alfieri, 1973) These divisions are similar to mitochondria, plastids, granular ER, free ribosomes those described by Esau and Cheadle (1955) and and a prominent nucleus, and are connected to the Zahur (1959) in some dicoryledonous taxa. This sieve cells by branched plasmodesmata on their shortening of sieve elements has been considered as side, fusing with a sieve pore on the sieve cell side. an advanced character. The two daughter cells formed after a transverse The nucleus flattens and in some cells appears division in the sieve element precursor may not to curl around the periphery of the cell in a bracelet­ necessarily differentiate into sieve elements, but one like fashion. It may be irregular in outline, but of these may differentiate into the sieve cell whereas maintains itS granular character and chromaticiry. No the other may form the parenchymatOUS albuminous evidence of the degeneration of the nuclear cell (Alosi & Alfieri, 1972). Cells that appear to be membrane has been observed. Necrotic nuclei, transitional between sieve cells and albuminous preViously described for Pinatae, are also frequent in cells have been observed in Ephedra. The fact that the mature sieve cells of Ephedra. an albuminous cell of Ephedra is formed directly Smaller and less distinct slime bodies have been from a single division of a fusiform mother cell recorded to appear later than the larger slime bodies distinguishes it from the albuminous cells of most (Alosi & Alfieri, 1972). These authors further other gymnosperms and correlates the two groups inferred tnat th'e smaller slime bodies anastOmose with specialized parenchyma cells, including and then disperse. The dispersed slime may become companion cells of higher plants. deposited at the site of the future sieve area. Finally, it forms a thin parietal film and may become WELWITSCHIACEAE collected near the differentiating sieve areas. Differentiation of the sieve area begins very Strasburger (1891) found the vascular bundles early and the progress is rapid in developing sieve in the ieaf of Welwitschia mirabilis to be similar to elements, as in Cucurbita (Frey-Wyssling & those in Gnetum, with the sieve elements somewhat Muhlethaler, 1957; Buvat, 1963). The time of narrower and appearing to have swollen waJls. complete perforation of sieve areas could not be Electron microscopic observations indicate that discerned but it is complete at the time the element most of the xylem and phloem elements in becomes functional (Alosi & Alfieri, 1972; see also Welwitschia are arranged in the radial rows or files Evert et al, 1970). in both primary as well as the secondary phloem PALIWAL-PHLOEM IN PI NOPHYf A J23

(Even et al, 1973). Two types of cells have been parenchyma cells (usually referred to as 'companion described in the phloem of this taxon, sie\'e cells aIII I cells') are in direct association with the former, parenchyma cells. The structure of the former is occasionally the laticifers (which occur in some similar to that of Gnetum and Ephedra. In a manner species of Gnetum, e.g., G gnemon and are in close similar to what has been observed in Pinatae and association with the sieve elements) and the fibre Gnetum, the plastids in \¥Ielwitscbia sieve cells also sclereids invariably develop secondary walls after undergo remarkable changes such as the formation the sieve elements cease to function. In the early of starch grains, proliferation of internal membranes, secondary phloem the sieve elements tend to form and decrease in the denSity of the matrix. homogeneous radial files alternating with radial Osmiophilic globules continue to be present in the rows of parenchyma cells. Thompson (1919) plastids but disappear from the cytoplasm. These depicted such a tissue at a level where parenchyma plastids differ from those of Pinus in that they lack cells appear narrow and occupy the corners crystalline inclusions and fibrillar material at all delimited by four sieve cells. Although, he stages of differentiation. The starch grains in them considered that the sieve cells, and the parenchyma are also club·shaped like those in Gnetllm. cells are not sister cells, he chose to call the latter as In contrast to the spatial relationship between companion cells. The recent study of Paliwal and pyconotic nucleus and endoplasmic reticulum Behnke (1973), however, indicates that although reported in some angiosperms and pteridophytes ontogenetically unrelated these are placid close to (Bouck & Cronshaw, 1965; Northcote & Wooding, each other. Moreo\'er. they could demonstrate that the 1966; Liberman-Maxe, 1966; Esau & Gill, 1971; Esau, sieve cells and phloem parenchyma cells do not 1972), Pinus strobus (Murmanis & Evert, 1966) and originate from a common mother cell by radial Gnetum gnemon (Behnke & Paliwal, 1973), only a di\'isions, as is true fm angiosperms. E\'iclently, resemblance of this has been reported between the therefore, the two types of cells have an nuclear envelope and mitochondria in Welwitscbia independent origin. Thus, by virtue of their mirabilis (Evert et aI., 1973). Portions of the inner independent origin, plasmatiC connections, and membrane of the nuclear coat develop protrusions densely staining contents, the phloem-parenchyma into the nuclear matrix, so that in some profiles part cells of Gnetum fit the definition of albuminous of the nucleus appears to be perforated. cells originally proVided by Strasburger (1891). Sieve cells of \¥Ielwitscbia have much in Coupled with this are the findings of ontogenetically common with those of Pinatae. In addition to related parenchyma cells, but not the companion nucleus, mitOchondria and ER, the mature, cells in members of the Calycanthaceae (Cheadle & plasmalemma lined sieve cell contains plastids with Esau, 1958), and in Luffa cylindrica (Shah & Jacob, starch granules. In contrast to plastids of immature 1969). Srivastava's (1969) work on the secondary sieve cells, those of mature sieve cells lack internal phloem of Austrobaileya scandens, a recognizedly membranes and their matrices are hyaline (vel)' primitive angiosperm (reported to lack companion clear) in appearance. The mitochondria undergo no cells by Bailey & Swamy, 1949), led him to post the apparent structural modification. The sieve cells lack idea that a clear distinction between all these ribosomes, dictyosomes, and microtubules. The different cells that are cytologically and vacuoles of young sieve cells and lumen of mature physiologically related to the sieve elements is ones sometimes contain a coarse fibrous substance, difficult. Further, in view of the great similarity similar in appearance to that found in the vacuoles between the companion cells of angiosperms and of parenchymatous cells of the leaf. The nature of the albuminous cells of gymnosperms including this substance has been determined but it should their being the same cell type and in haVing not be confused with slime or P-protein which is originated through the adaptation of some totally absent. During maturation the tonoplast, parenchyma cells to assist the sieve elements in long which delimits the vacuolar contentS from the distance transport, Srivastava also proposed to cytoplasm in young cells, ceases to be identifiable abandon the term albuminous cells and retain only and the sieve cell then appears to contain one large companion cells both for gymnosperms and central cavity, angiosperms (see also Behnke, 1986). Behnke and Paliwal (1973) have indicated that a similar situation GNETACEAE occurs in Gnetum gnemon and hence the term The first information on the phloem tissue in parenchyma cells should be used for describing this group is perhaps that of Strasburger (1891) these albuminous cells. Here the phloem contains sieve elements with sieve In the crushed condition the primary phloem areas on the lateral walls and thus the adjacent gets delimited by a massive accumulation of the wall 124 THE PAlAEOBOTANIST

material. The ray cells have thick walls except those present. Plastids may have ovoid, hemispherical, or few that differentiate into sclereids. Ray cells or elongated profiles. These contain thylakoids, a sclereids contain starch and CIystals. In contrast to dense matrix, and accumulate varying quantities of the ray cells of Ephedra, those of enetum starch. The nucleus persists for the entire life of accumulate calcium oxalate in the lumen not in the these cells. Cell sap is retained in several small wall. Strasburger found it remarkable that the ray vacuoles, which generally fuse to form a central cells containing crystals had no less starch than the cavity. They are deVOid of proteinaceous substance crystal-free cells. In the active phloem, the in contrast to the reports of Strasburger (1891), but parenchyma cells are filled with starch but in the are identical to those described by Liberman-Maxe older phloem these become empty and crushed like (1971) in Polypodium vulgare in this respect (see the sieve elements. Maxe, 1966). Internally their structure undergoes The above description would lead us to simplication, the thylakoids become disorganized conclude that the studies on the phloem tissue in and the matrix materials also decrease. Starch is Pinophyta had begun in the last century and have present in them from the earliest stage of sieve cell continued to invite the attention of a host of differentiation, the number of starch grains researchers till date. Of course, with the availability increasing gradually. Some of these are always club­ of the new tOols and techniques now, more and shaped, a feature that seems to be characteristic of more details have come to light pertaining to the enetum and some members of the Taxodiaceae structure of the sieve cells/elements and the nature (Behnke, 1974). of the connections between these and the associated The changes in the ER during sieve cell parenchyma/albuminous cells. For instance, we now differentiation are more significant. The granular ER, know that a differentiating sieve element in enetum present in the young sieve cells tends to be modi­ gnemon is discernible from Its neighbouring fied by a swelling of interacisternal spaces. After the parenchymatOus cell by its very long nucleus with loss of ribosomes, the ER assumes a more tubular densely stained patches of chromatin, partly attached structure; tubules spreading throughout the cell to the inside of the nuclear envelope by lumen but have a tendency to form aggregates. mitOchondria often in close vicinity to the outside of Within the aggregates, the ER tubules lie parallel to the nuclear envelope, by starch-containing plastids, each other but may also become twisted altogether. and a less dense cytoplasmic matriX, containing Frequently the ER complexes are associated with the some ER aggregates. On the other hand, the nucleus degenerati ng nuclei or with the plastids. Various of the parenchyma cell ·extends partly into a opinions have been expressed for this association of cytoplasmic bridge, passing through the vacuole. ER (most of all close to the sieve areas), and its Moreover, the albuminous cells of the three genera functional' significance, if any. Dictyosomes and of the Gneticae (as well as the parenchyma cells) microtubules also disappear. Finally ER, plastids, are interconnected through plasmodesmata and mitochondria represent the only organelles left occurring in groups and united in the region of the in the living protOplast, an arrangement which is middle lamella by the median cavities. The perhaps the characteristic condition of the mature connections to the sieve elements are intermediate sieve cell in gymnosperms. The central cell sap between a sieve area and a plasmodesmata I field. cavity sometimes contains fibrillar material that This also shows the growth of our knowledge since mixes with and disappears within the protOplast the publications of de Bary (1884) or even Coulter after tOnoplast degeneration. P-protein has not been and Chamberlain 0917; Behnke & Sjolund, 1990). detected either by light or electron-microscopy in young or mature sieve elements (Paliwal & Behnke, REFERENCES 1973) Parenchyma cell (of all the types including Abbe LB & Crafts AS 1939. Phloem of while pine and Olher coni­ those associated with the sieve cells) differentiation, ferous species. Bol Gaz. 100: 695· 722. Alfieri FJ & Even RF 1965. Seasonal phloem developmem in revealed featu~eswhich are quite similar to those of Pinus slrobus. Am I Bal. 52 : 626-627. the companion cells in angiosperms. The most Alfieri FJ & Even RF 1968a. Observations on albuminous cells in remarkable change in the cambial initial destined to Pinus. Planta (Berlin) 78 : 95·97. become' a parenchyma cell is that it becomes rich in Alfieri FJ & Even RF 1968b. Seasonal developmem of the secon­ cellular organelles. The ribosomes become dary phloem in Pinus. Am. j. Bal. 55: 518-528. abundantly distributed in the cytoplasm and are Alfieri FJ & MOllola PM 1983. Seasonal changes in the phloem of Ephedra cali/arnica Wats. Bal. Gaz. 144 : 240-246. ER. deposited on the Microtubules, dictyosomes and Alosi MC & Alfieri FJ 1972. Omogeny and structure of the secon- mitochondria, with well-defined cisternae are also dary phloem in Ephedra. Am. I Bal. 59 818-827. PALIWAL-PHLOEM IN PINOPHYTA 125

Alosi MC & Park RB 1983. Fractionation and polypeptide analysis of the thickened sieve cell walls in Pinus strobus L. of phloem tissue of Doug!. Planta 157 Protoplasma 75 : 67· 78. 298·306. Chang yP 1954a. Bark structure of North American conifers. Bailey 1W & Swamy BGL 1949. The morphology and relationship US.DA_ Tech. Bull. (1095). of Austrobaileva I Arnold Arbor. 30 : 222·226. Chang yP 1954b. Anatomy of common North American pulpwood Bamber RK 1959. The anatomy of the barI< of 5-species of barks. Tappi Monogr. Ser. (14). Callitris Vent. Proc. Linn Soc. NS. W. 84 375· 381 Chauveaud G 1902a. De l'existence d'elements precurseurs des Barghoorn ES 1941. Origin and development of uniseriate rays in tube cribles chez des Gymnosperms. C. R. Acad. Sci. 134 the Coniferae. B ul/. Torrey bot. Club 67 303- 328. 1605-1606. Barnell JR 1971. Electron-microscope preparation technique Chauveaud G 1902b. Developpement des elements precurseurs applied to the light microscopy of the cambium and its des tubes cribles dans Ie Thuja orientalis. Bull Mus. derivatives in Pinus mdiata 0 Don. j. Microsc. 94 : 175- 180. Hist. Nat. 8 447-454. Barnett JR 1974. Secondary phloem in Pinus radiata D. Don, 1 Chauveaud G 1903. Recherches sur Ie mode deformation des Structure of differentiating sieve cells. N Z. J. Bot. 12 tubes cribles dans la racine des cryptogames vascul­ 245·274. aires et des Gymnospermes. Ann Sci Nat. Bot_ 18 : 165­ Behnke HD 1971. Zusammenschau der Feinstrukturforschung an 277 Stoff-Ieitgewebe wahrend der Jahre 19601972 In Merxmuller Cheadle VI & Esau K 1958. Secondary phloem of the Calycan- H et al (editors)-Fortschrltte del' Botanik: 45-52. Springer­ thaceae. Univ Calif. Pubis Bot. 29 397-510. Verlag, Berlin. Chrysler MA 1913. The origin of the erect cells in the phloem of Behnke HD 1974. Sieve element plastids of gymnospermae : their Abietineae. Bot. Gaz. 56 : 36-50. ultrastructure in relation to systematics. Plant Syst_ Evol. Chrysler MA 1926. Vascular tissue of Microcycas calocoma. Bot. 123 1-12. Gaz 82 233- 252. Behnke HD 1986. Sieve element characters and the ;systemaric Coulter JM & Chamberlain CJ 1917. Morphology of the gymnos· position of Austrobaileya (Austrobaileyaceae)-with com­ perms Chicago. ments to the distinction and definition of sieve cells and Craft AS & Currier HB 1963. On sieve tube function. Protoplasma sieve-tube members. Plant Syst. Evol. 152 101-121. 57 188- 202. Behnke HD & Paliwal GS 1973. Ultrastructure of phloem and its Cronquist A, Takhtajan A & Zimmermann W 1966. On the higher development in Gnetum gnemon with some observations of taxa of Embryobisita. Taxon 15 129-134. l:.phedra campylopoda. Protoplasma 78 305-319. Cronshaw J 1965. In "Cellular ultrastructure of woody plants" Behnke HD & Sjolund RD (ed.) 1990. Sieve elements. compara Syracuse, NY tive structure, induction and development. Springer-Verlag, de Bary A 1884. Comparative anatomy of the vegetative organs of Heidelberg. the phanerogams and ferns. Oxford. Bertrand CE 1874. Anatomie comparee des tiges et des Feuilles Dippel L1869. Des Mikriscope und seine An wendung-Zweiter Teil chez les Gnetaceeis et les coniferes Am. Sci Nat. Bot. 20 : 5­ Anwendung des Mikroscopes auf die Histologie del' gewachse 153 Braunschweig. Friedrich Verlag, Berlin. Bocher 1W 1964. Morphology of the vegetative body of Meta- Dute RR 1983. Features of sieve-element ontogeny in Ginkgo sequoia glyptostroboides Dansk. bot. Ark. 24 1-70. biloba. Am J. Bot. 70 19. Boodle lA & Worsdell WC 1894. On the comparative anatomy of Eames AJ & MacDaniels LH 1947. An introduction to plant the Casuarinaceae with special reference to the Gnetaceae anatomy. New York. and Cupuliferae. Ann. Bot. Land. 8 : 231-264. Engleman EW 1965. Sieve elements of Impatiens sultanii. I. Bouck GB & CronshawJ 1965 The fine structure of differentiating Wound reaction Ann Bot Land. 29 83-101. sieve elements_ J. Cell BioI. 25 79-96. Esau K 1960. Anatomy of the seed plants. New York_ Braun HJ & Den Outer RW 1965_ Uber die tertrien Wachstums Esau 1965. Plant anatomy. New York. Vorgange im bast von Pseudotsuga taxiflora (Sic.) (Poir) Esau K 1969. The Phloem. In Zimmermann W, Ozenda P & Wulff Britton. AI/g. forst-U jagdztg 136 101-105. HD (editors) Encyclopaedia of plant anatomy. Vol. 5 Brown HP 1912. Growth studies in forest . I. pt (2). Berlin. Mill. Bot. Gaz 54 : 386-403 Esau K & Cheadle VI 1955. Significance of cell divisions in Brown HP 1915. Growth studies in forest trees. II. Pinus strobus. differentiating phloem. Acta Bot. neerl. 4 : 348·357. Bot. Gaz 59 197-241. Esau K & Cheadle VI 1958. Wall thickeninj! in sieve elements. Brudermmann G & Koran Z 1973. Tissue volume change in black Proc natn. Acad Sci. US.A 44 545·553. phloem (Picea mariana). Can. I Bot. 51 : 1649-1653. Esau K & Cheadle VI 1965. Cytological studies on phloem. Univ. Buvat R 1963. Les infrastructure et la differentiation de cellules Calif. PubIs Bot. 36 253- 344. cribles de Cucurblta pepo. Portugal. Acta Bioi ser. A 7 Esau K, Cheadle VI & Risley EB 1962. Development of sieve plate 249-299 pores. Bot Gaz. 123 233-243. Campbell R 1972. Electron microscopy of the development need­ Esau K & Gill RH 1970a. Observations of spiny vesicles and les of var. maritima. Ann. Bot Land. 36 : 711­ P-protein in Nicotiana tabaccum. Protoplasma 69 : 373- 388. 720_ Esau K & Gill RH 1970b. A spiny cell component in the sugarbeel. Carde JP 1973. Le tissue de transfert (=cellules de Strasburger) J. Ultrastruct. Res. 31 444-455. dans la aiguilles du Pin maritime ( Ait.)_ Esau K & Gill RH 1971. Association of endoplasmic reticulum and I. Etude histologique et infrastructurale du adulte. J. its relation to the nucleus in a differentiating sieve element. Microsc. 17 : 65- 88. J. Ultrastmct. Res. 34 144-158. Carde JP 1974. Le tissue de transfert (=cellules de Strasburger) Eschrich W 1963a. Beziehungen zwischen dem Auftreten der dans la aiguilles du Pin maritime (Pinus pinaster Ail.) II. Callose und des primaren Phloem bei Cucurbila ficljolia. Caracteres eytochimiques et infrastructuraux de la paroi Planta 60 : 243-261. et des plasmodesmes. J. Microsc. 20 : 51-72. Eschrich W 1963b. Der Phloemsaft von Cucurbita ficifolla. Planta Chafe SC & Doohan ME 1972. Observations on the ultrastructure 60 216-224. 126 THE PALAEOBOTANIST

Evert RF & Alfieri FJ 1965. Ontogeny and structure of coniferous Kollmann R 1964. On the fine structure of sieve element pro- sieve cells. Am. j. BOI. 52 : 1058-1066. toplast. Phylomorphology 14 247-264. ' Evert RF, Bormann CH, Butler V& Gilliland MG 1973a. Structure Kollmann R 1965 Zur Lokalisierung der funktionostuchtigen and development of sieve·cell protoplasts in leaf veins of siebzellen im sekunoaren phloem von Melasequoia glYPlos- Welwilschia. PrOloplasma 76 : 1-21. Iroboides. Planla 65 173-179. Evert RF, Bormann CH, Butler V& Gilliland MG 1973b. Structure Kollmann R 1967. Autoradiographischer Nachweis der Assimilat­ and development of sieve areas in the leaf veins of Wei· transportbahn im secundaren phloem von Melasequoia wilschia. PrOloplasma 76 23-44. glYPlOslroboides. Z Pjlanzenphysiol 56 401-409. Evert RF, Davis JD, Rucker CM & Alfieri FJ 1970. On the occurrence Kollmann R \968 Funktionalla Morphologie des COll/jeren of nuclei in mature sieve tube elements. Planla 95 : 281· Phloem. Berlin. 296. Kollmann R& Dorr I 1966. Lokalisierung funktionstuchtigen Evert RF & Derr WF 1964. Slime substance and strands in sieve siebzellen bei juniperus communis mit hilfe von Aphiden. Z. elements. Am. j. BOI. 51 875-880. Pjlanzenphysiol. 55 131·141. Feustel H 1921. Anatomie und Biologie der gymnospermen· Kollmann R& Schumacher W 1961 Uber die Feinstruktur des bEitter. Beil BOI Cent. 38.: 177- 257. phloem von Melasequoia glYPloslroboides. und seine Jahresz Frey·Wyssling A& Muhlethaler KR 1957. Submicroscopic eitlichen Ver·anderungen. I. Mitt. Das Ruhephloem. Planta differentiation of plasmodesmata and sieve plate in Cucur· 57 583·607. bila. j. Ullras/ruet Res 1 38·48. Kollmann R& Schumacher W 1962a. Uber die Feinstruktur des Gourret JP & Strullu DG 1974. Evolution des proteoplasts du phloem von Melasequoia glYPloslroboides und seine phloeme de Pseudolsuga menziesii Mirb (Abietacees) au Jahreszeitlichen Veranderugen. II Mitt. Vergleichende Un­ cours de la differenciation des elements cribIes. j. Mierosc. tersuschungen du plasmatischen verbindungsbruchen in 20 73-82. phloemparenchym zellen und Siebzellen. Planta 58 366­ Grillos SJ & Smith FH 1959. The secondary phloem of Douglas . 386 For. Sci 5 377-388. Kollmann & Schumacher W 1962b. Uber die Feinstruktur des Gunckel JP & Wetmore RH 1946. Studies of development in long von Melasequoia glYPloslroboides und seine shoots and shon shoots of Gil7kgo bi/oba L. 11. Phyllotaxis Jahreszeitlichen Veranderungen. III. Mitt. die Reaktivierung and the organisation of the primary vascular system: primary der Phloemzellen in Frllhjahr. Planta 59 195-221. phloem and primary xylem. Am j. BOI. 33 532- 543. Kollmann R& Schumacher W 1963. Uber die Feinstruktur des Harris WM 1972. Ultrastructural observations on Pinaceae leaf phloems von Melasequoia glyptoslrob9ides und seine Jahres­ phloem. New Phytol. 71 169·173. zeitlichen Veranderungen. rv Mitt. Weitere Beobachtungen Hebant, C 1975- Lack of incorporation of tritiated uridine by zum Feinbaus der Plasmabrucken in den Siebellen. Plal1la nuclei of mature sieve elements in Metasequoia glYPloslro­ 60 360·389 bOides and Sequoiadendrol7 giganteum. Planla 126: 161-163­ Kollmann R& Schumacher W 1964. Uber die Feinstruktur des Hemenway AF 1913. The evolurion of the sieve tubes. Bot. Gaz. phloems von Melasequoia glYPloslroboides und seine Jahres­ 55 236- 243 zeitlichen Veranderungen, V. Mitt. die Differenzierung der Hepler PK & Newcomb EH 1964. Microtubules and fibrils in the siebzellen in Verlaufe einer Vegetationsperiode. Plal1la cytoplasm of Coleus cells undergOing secondary wall 63: 155·190. deposition j. Cell Bioi 20 529-533- ledbetter MC & Porter KR 1963· A "microtubule" in plant cell Hepron CEL & Preston RD 1960. Electron microscopic observa­ fine structure. j. Cell Bioi 19 239246. tions of the structure of sieve connections in the phloem Liberman-Maxe M 1917. Etude cytologique de la dim~renciation of angiosperms and gymnosperms j. expml/ Bot. 11 381­ des cellules criblees de Polypodium vulgare. (Polypodiacee). 394. j. Microsc 12 271·288. Hill AW 1901a. The distribution and character of connecting Maheshwari P& Vasil V 1961 Gnelum. CSIR, New Delhi. threads in the tissues of Pinus sylveSlris and Mahmood A 1965. Secondary walls in the phloem of Pinus radiala other allied species. Phil. Trans. R Soc. 8 194 83- 125 D.Don Nalure Lond 207 : 657-658. Hill AW 1901 b. The histology of the sieve tubes of Pinus. Ann. Mahmood A 1968. Cell grouping and primary wall generations in BOI Lond 15 575-611. the cambial zone, xylem and phloem in Pinus. AUSlralian Hohl HR 1960 Uber die submikroskopische Struktur normaler j. BOI 16 177-196. und hyperplastischer Gewebe von Dalura slramonium L. I. Maxe M 1966. Etude de la degenerescence nucleaire dans les Normalgewebe. Ber schweiz. BOI. Ges. 70 395-439. cellules criblees de Polypodium vulgare (Polypodiacee). Holdheide W 1951. Anatomie Mitteleuropaischer Geholzrinden. C. R. Acad. Sci. Paris 262 2211-2214. In Freund 1-1 (Editor)-Handbuch des Mikroskopie in der Mettenius G 1861. Beitrage zur AnatOmie der Cycadeen. Abh. Technik. 5 : 193·367 Malh-Phys. Cl. Kon. Sachs Ges. Wiss. 5 : 567-608. Huber B & Graf E 1955. Vergleichende Untersuchungen uber die Moeller J 1882. Anatomie der Baumrinden. Berlin. Geleitzellen der Siebrohren. Ber. dl. BOI Ges. 68 313-3· Muhlethaler K 1950. Elektronenmikroskopische Untersuchungen Isenberg IH 1943. The anatomy of the redwood bark. Madrono 7 uber den Feinbau und das wachstum der Zellmembranen in 85·91 Mais und Hafer Koleoptilen. Ber schweiz. BOI. Ges 60 Klinken J 1914. Uber das gleitende Wachstum der 1nitialen 614-624 im Kambium der Koniferen und der Markstrahlenverlauf in Murmanis l 1970. Locating the initial in the vascular cambium of ihr& sekundaren Rinde_ Bib/. BOI. (BioI.) 19 1·41. Pinus slrobus L by electron microscopy. Wood Sci Tech. Knudson l 1913. Observations on the inception, season and 4 1-14. duration of cambium development in the American Murmanis l 1972. Filamentous components (slime) in coniferous (Lalix laricina (DUROl Koch.). Bull. Torrey bOI. Club 40 Sieve elements (Abstr.). Proc. 30th Eleclron microscopy 271-293. socielY, U.S.A. Kollmann R 1961a. Zur Feinstruktur des Phloem. Ber. dl. bOI. Murmanis L 1974. Filamentous components of secondary phloem Ges. 74 54-55. sieve elements in Pinus slrobus L. Ann. BOI. Lond 38 PALIWAL-PHLOEM IN PINOPHYTA 127

859-863 et Kudo. I Jap. Forestry Soc. 46 199 204. Murmanis L & Evert RF 1966. Some aspects of sieve cell ultras­ Singh AP 1984a. Pinus radiata needle trace studies: fine tructure in Pinus strobus L. Am. I Bot. 53 1065-1078. structure of immature sieve cells in the primary phloem. Murmanis L & Even RF 1967. Parenchyma cells of secondary Cytologia 49 359- 384 phloem in Pinus strobus. Planta 73 301-318. Singh AP 1984b. Microfilamems in the phloem of Pin~radiata Neuberger DS 1973. Sieve·cell ultrastructure in the hypocotyl of coryledons. CylOlogia 49 385- 393. . Am. I Bot. 70 40/Abst. Smoot EL 1984. Phloem anatomy of the pteridos­ Neuberger OS & Evert RF 1974. Structure and development of the perm Medullosa and evolutionary trends in sieve element protoplast in the hypocoryl of Pinus resinosa. phloem. Bot. Gaz. 145 550-564. Am I BOI 61 360-374. Sprecher A 1907. Le Ginkgo biloba L. Geneva Neuberger DS & Evert RF 1975. Structure and development of Srivastava LM 1963a. Cambium and vascular derivatives of Ginkgo sieve areas in the hypocotyl of Pinus resinosa. Protoplasma biloba j. Arnold Arbor 44 165-192_ 84 109 125 Srivastava LM 1963b. Secondary phloem in Pinaceae. Univ Calif. Neuberger DS & Even RF 1976. Structure and developmem of the Pubis Bot. 36 1-142. sieve cells in the primary phloem of Pinus resinosa Pro­ Srivastava LM 1969. On the ultrastructure of cambium and its IOplasma 87 27· 37 vascular derivatives. III The secondary walls of the sieve Northcote DH & Wooding FBP 1966. Development of sieve tubes elemems of Pinus strobus. Am. j. Bot. 56 354·361. in Acer pseudoplatanus Proc. R. Soc. Land. B 163 : 524-537. Srivastava LM & O'Brien TP 1966. On the ultrastructure of cam­ O'Brien TP & Thimann KV 1967. Observations on the fine struc· bium and ilS vascular derivatives. II. Secondary phloem of lure of oal coleoptile. Ill. Correlated light and e·leclron Pinus strobus. PrOlOplasma 61 : 277-293. microscopy of the vascular tissues. PrOlOplasma 63 : 44}478. Steer MW & Newcomb EH 1969. Development and dispersal of P­ Paliwal GS & Behnke HD 1973. Light microscopic study of the protein in the phloem of Coleus blumei Benth. I Cell Sci. organization of phloem in the stem of Gnetum gnemon L. 4 155-169 PhylOmorphology 23 183-193. Sterling C 1946. Growth and vascular development in the shoot Parameswaran N 1971. Zur Feinstruktur der Assimilat leit bahnen apex of Sequoia sempervirens Lamb. End!. II. Cytological in der Nadel von Cytobiol. 3 70·88. aspects of vascularizalion. Am. I Bot. 33 35·45. Parameswaran N & Liese W 1970. Zur Cytologie de Strasburger· Strasburger E 1887. Das Botanische Prakticum. jena. zellen in Conifernadeln. Naturwiss. 57 45-46 Strasburger E 1891. Uber den Bau und die verreichtungen der Parker j 1965 Stains for strands in sieve tubes. Stain Techno. 40 : Leitungsbahnen in den Pflanzen. Histol. Beilr. Heft III. 223-225. jena. Parthasarathy MY 1975a. Ultrastructure of sieve cells in Cycads. Thaine R 1964. Proroplast structure in sieve tube elements. New 12th Int. Bot. Congress. Phytol. 63 : 236-243. Parthasarathy MY 1975b. Sieve elemem structure. In Zimmermann Thompson WP 1919. Companion cells in the bast of Gnetum and W (Ediror)-f1.Jloem transport. 212-280_ Berlin. , angiosperms_ Bot. Gaz 68 451-459. Pesacreta TC, Parthasarathy MY 1986 Microfilament bundles in Timell TE 1973· Ultrastructure of dormant and active cambium the roots of a , Chamaecyparis obtusa. Protoplasma zones and the dormant phloem associated with the formation 121 54-64. of normal and compression wood in Picea abies (L.) Karst. PreSIOn RD 1963. Ultrastructure and kinetic aspects of solute State Univ. Call. Environ. Sci. and For. Tech. Pub. 96 : 3-96. translocation in the stem of plams. Progr. Biophys. Malec. Warmbrodt RD & Eschrich W 1985. Studies on the of Bioch. 13 : 243-260. Pinus sylvestris L. produced in vitro with the basidiomycete Russow E 1882a. Uber den Bau und die Entwicklung der Sie­ vQ1-iegatus (SW. ex FR.) o. Kunlze. II. Ullras­ brohren und bau und EnrwickJung der Sekudaren Rinde truclural aspecls of the endoderm is and vascular cylinder of der Dicotylen und Gymnospermen. Sitzber. Naturf. Ges. the mycorrhizal rootlets. New Phytol. 100 : 403-418. Univ. Dorpat 6 257-327. Wilcox H 1954. Primary organisation of active and dormant roots Russow E 1882b. Sur La structure et Ie developpemem des tubes of noble fir, . Am. I BOI 49 : 221-236. cribrense. Ann. Sci. Natur. Bal. 14 167-215. Willenbrink j & Kollmann R 1966. Uber den Assimilat-transport in Sauter ] 1974. Structure and physiology of Strasburger cells. phloem von Metasequoia. Z. Pjlanzenphysiol. 55 42-53. Ber. dtsch. Bal. Ges. 87 327· 336. Wilson BF 1963. Increase in cell wall surface area during Sauter ], Dorr I & Kollmann R 1976. The u ltraslructure of enlargement of cambial derivatives in . Am. I Strasburger cells (=albuminous cells) in the secondary BOI 50 95- 102. phloem of Pinus nigra var. auslraca (Hoess) Badoux. Wooding FBP 1966. The development of the sieve cells of Pinus Proloplasma 88 31-49. pinea. Planta 69 230· 243. Schulz A, Alosi AC, Sabnis DO & Park RB 1989. A phloem-specific, Wooding FBP 1968. Fine structure of callus phloem in Pinus lectin-like protein is located in pine sieve-elemem plastids pinea. Planta 83 : 99·110. by immunocytOchemistry. Planta 179 : 506- 515. Wooding FBP & Northcote Dj 1965a. The fine structure and Schumacher WI967a_ Der Srofftransport zwischen parenchyma­ development of the companion cells of the phloem of Acer tischenzellen (Nahlranspon). Handbuch Pjlanzenphysiol. 13 pseudoplatanus. j. Cell BioI. 24 117-128. 3-16_ Wooding FBP & Northcote Dj 1965b. Association of the endop­ Schumacher W 1967b. Die Fernleitung der Sroffe in Pflanzenkor­ lasmic reticulum and the plastids in Acer and Pinus. Am. I per. Handbuch Pjlanzenphysiol. 13 61-177. Bar 52 526-531. Seward AC & Gowan jD 1900. The maiden-hair (Ginkgo Zahur MS 1959. Comparative study of secondary phloem of 423 biloba L.). Ann. Bal. Land. 14 109-154. species of woody dicoryledons belonging 10 85 families. Shah] & jacob R 1969. Developmem and structure of phloem Cornell Univ. Agric. exptl Station Mem. 358. in the petiole of Luffa cylindrica. Am. I Bot. 56 : 821-831. Zimmermann MH 1960. Longitudinal and tangential movements Shimaji K 1964. Structure and developmem of the inner bark within the sieve tube system of white ash (Fraxinus ameri­ tissue in Mast. var. Mayriana Miyabe cana L.). Beih Z. Sch. Forster. 30 : 289-300.