IAWA Bulletin n.s., Vol. 7 (1),1986 47
STORIED STRUCTURE OF THE SECONDARY PHLOEM
by
R. W. den Outer Vakgroep Plantencytologie en -morfologie, Landbouwhogeschool, Arboretumlaan 4, 6703 BD Wageningen, The Netherlands
Summary The anatomy of the secondary phloem with cambium the initials are not arranged in hori• a storied structure of 49 species of woody dico• zontal tiers, their ends overlap, they are long, tyledons from the Ivory Coast, West Africa, has and their length may vary considerably. The been studied. They belong to the families Bixa• non-storied cambium is considered to be phylo• ceae (I species), Bombacaceae (3 species), Cae• genetically more primitive than the storied one. salpiniaceae (4 species), Papilionaceae (18 spe• The storied pattern of fusiform cells can be dis• cies), Sterculiaceae (16 species), and Tiliaceae rupted as a consequence of pseudo transverse di• (7 species). In the Bixaceae and Sterculiaceae visions and elongation (Zagorska-Marek, 1984). only the axial system is storied whereas in the Both the axial cells and rays of secondary four other families usually both the ray and phloem and xylem derived from a storied cam• axial systems are storied. bium may remain storied or the stratification Anatomical features accompanying storied may be present only in the axially elongated structure in the secondary phloem are describ• cells. In this last case a partiy storied structure is ed, viz.: sieve-tube elements are generally short present. Within a species, even within a single with slightly oblique to transverse sieve plates; sample of a tree the storied structure can change sieve areas in the side walls of the sieve-tube from very conspicuous to hardly discernible. elements are sparse, poorly developed, unequal• Therefore the development of storeys must be ly spaced or diffuse, or entirely absent; com• dependent on several factors (Philipson et aI., panion cells are similar in length to the sieve• 1971). tube elements they accompany, one per sieve A storied structure is usually accompanied by element or are septated to form a strand of other anatomical features in both the secondary cells; in the conducting secondary phloem, pa• phloem and xylem. For the secondary xylem renchyma strands are nearly always composed they have already been described by J ansso• of at the most four cells; phloem fibres, multi• nius (1931), Reinders and Reinders-Gouwentak seriate rays and crystal cells are always present; (1961) and others in the following way: an arrangement of similar elements in tangen• tial layers often occurs. Though storied struc• I. fusiform parenchyma cells often occur; pa• ture itself is considered to be an advanced fea• renchyma strands are usually composed of ture, the component elements of the secondary only two cells, or at the most four cells (at a phloem itself can be specialised, intermediate distance of more than two cells from the ves• or even primitive according to standards given sels); by Zahur (1959). 2. alllibriform fibres within a certain area of the Key words: Ivory Coast, sieve tubes, companion tree are approximately of the same length. cells, phloem parenchyma, phloem fibres, They have usually a wide middle part with phloem rays, evolutionary advancement. the length of the fusiform initials and sud• denly narrowing pointed ends placed uni• laterally on the middle part like a bayonet; Introduction 3. wood with storied structure lacks fibre• The arrangement of cambial cells in tangen• tracheids; tial view shows two basic patterns: storied and 4. perforation plates in the vessels are (usually) non-storied. In a storied (storeyed, stratified) simple; cambium the fusiform initials occur in horizon• 5. when storied structure is present in one spe• tal tiers with the ends of the cells of one tier cies of a family, one finds characteristics asso• appearing at the same level. The initials are ciated with storied structure in all the other short, with little variation in length. They occur species of the same family. Conversely, if in highly specialised dicotyledons (Beyer, 1927; some species of a family possess these char• Esau, 1977; Chavan & Shah, 1983; Metcalfe & acteristics, one can find species with actual Chalk, 1983, and others). In the non-storied storied structure in this family.
Downloaded from Brill.com10/02/2021 07:10:07AM via free access ~ Table I. Secondary phloem characters of the investigated species with a storied structure. 00
sieve tube companion axial phloem cell parenchyma rays
.... ':l'" 0 .... ------.... ",-0 t::~'" ~t:: ~E C ..t:: E l:: '" "'-'" ::l~ E o
Downloaded fromBrill.com10/02/2021 07:10:07AM Duboscia viridiflora (K. Schum.) Mildbr. 578 III 350 c B + 360 6 + He II + Grewia carpinifolia Juss. 289 III 260 c B + 275 4 + He II + Grewia malacocarpa Mast. 264 II 420 b B + 435 8 + + Hell + Grewia mollis Juss. 298 III 205 c B + 205 4 + He II + Nesogordonia papaverifera (A. Chev.) R. Capuron 243 III 305 c B + 305 4 + He II +
Legend: + = present; - = absent. Sieve tube type I = sieve tubes over 500 J..UtIlongwith very oblique sieve plates with 10 or more sieve areas, sieve pores small, diameter sieve tube about equal to that of parenchyma cells; type III = sieve tubes less than 300 J..UtIlongwith slightly oblique to transverse, simple sieve plates, diameter less than that of parenchyma cell; type II = intermediate between types I and III. Sieve area type b = sieve areas present on side walls, poorly developed; type c =sieve areas absent from side walls or very obscure. Companion cell type B = cells as long as sieve tubes; type C =cells in septate strands; place * = companion cells parallel to the sieve tube against its ra- dial wall; ** = companion cells seemingly cut off from corner of sieve tube. Phloem rays: he =heterogeneous, composed of upright and procumbent cells; ho =homogeneous, via freeaccess composed entirely of upright or procumbent cells; type I =rays uni- and multiseriate with long uniseriate tails; type II = rays uniseriate and multiseriate with short uniseriate tails; type III = rays uniseriate only. Bast type 4m =repeated sequence of four layers: fibres (crystalliferous cells), parenchyma, sieve tubes, parenchyma. ~ '" 50 IAWA Bulletin n.s., Vol. 7(1),1986
In general the secondary xylem with a storied (175-)233(-390) j..lm; Sterculiaceae (230-) structure is considered to be specialised. Yet 311( -405) j..lm and Tiliaceae (205-)313( -420) the composing elements do not always show j..lm. The diameter of the sieve tubes is smaller advanced characteristics. In the secondary xy• than that of the axial parenchyma cells (see lem of some Piperaceae, for instance, storied also Esau, 1977, and Metcalfe & Chalk, 1979; axial parenchyma and scalariform intervascular all species). pits make an unusual combination of specialised 2) Sieve areas in the side walls of the sieve• and primitive features (Patel & Bowles, 1980). tube elements are usually poorly developed and The characteristics of the secondary phloem in a small number, unequally spaced or diffuse with a storied structure are only partly known. (type b; 42 species); only in a few cases entire• In our investigation we tried to analyse these ly absent or obscure (type c; 7 species). characters. In this respect the arrangement of 3) Companion cells are of similar length to the cells must be studied in the conducting sec• the sieve-tube elements they accompany (type ondary phloem, since changes in the noncon• B; 25 species), or also septated to form a strand ducting phloem may obscure the possible exis• of cells (type C; 24 species). There is nearly al• tence of the stratification. ways one long companion cell, or one strand of companion cells per sieve-tube element. The Materials and Methods companion cells belonging to successive sieve• Bark samples of woody dicotyledons from tube elements of a sieve tube are usually not in the Ivory Coast, West Africa, are from the Ver• direct contact with each other. The companion steegh and Den Outer collection (1969). The cells more often appear as though cut out of collection is housed at the Department of Plant the corner of the sieve tube (32 species) than Cytology and Morphology, Agricultural Univer• lying against the radial wall of the sieve tube sity, Wageningen, the Netherlands. All material (17 species). studied is accompanied by herbarium vouchers. 4) In the conducting secondary phloem, pa• Samples were collected from stems at breast renchyma strands are nearly always composed height and immediately fixed in FAA. The col• of at most four cells (except chambered crys• lection comprises 749 V. and O. numbers. 449 talliferous cells) and as long or somewhat longer species were investigated, belonging to 26 fami• (up to 1.2 times as long) than the sieve-tube lies; of these families usually eight or more spe• elements. Mean parenchyma strand lengths pre• cies had been collected (444 species belonging ceded and followed by extreme values between to 24 families, Den Outer, 1983) except for the brackets are: Bixaceae 290 j..lm; Bombacaceae Bixaceae (I species) and Bom bacaceae (4 spe• (380-)453( -490) j..lm; Caesalpiniaceae (220-) cies). The investigated species are briefly de• 290(-320) j..lm; Papilionaceae (175-)247(-390) scribed in Den Outer (1972). j..lm; Sterculiaceae (260-)336(-435) J.I.Il1 and Anatomical features were studied in trans• Tiliaceae (205-)321(-435) j..lm. The axial paren• verse, radial and tangential sections and mace• chyma is not abundantly present and there is usu• rations; classification of phloem elements is ac• ally some enlargement of the cells in the inactive cording to Zahur (1959) and Den Outer (1983). phloem and some variation in cell size (type -). 5) Phloem fibres (type 3) and crystal cells are Results always present. Stone cells are often present A storied structure was found in only 49 (II (28 species); fibre-sclereids absent. On average %) of the 449 species investigated. They belong the phloem fibres are 5 times (Bombacaceae, to six families (see Table 1). Except for the Sterculiaceae and Tiliaceae) to 7 times (Bixa• family Bixaceae, all families either belong to ceae, Caesalpiniaceae and Papilionaceae) as long the order Malvales or to the Fabales. as the sieve-tube elements. The analysis of the characters associated with 6) Multiseriate rays always present, nearly al• storied structure for the secondary phloem is as ways with short (1-4 cells) uniseriate tails (43 follows: species). They are either homogeneous (only I) Sieve-tube elements are generally short procumbent or only upright cells are present; with slightly oblique to transverse simple sieve 21 species) or heterogeneous (procumbent and plates (type III, classification according to Za• upright cells are present; 28 species). hur, 1959, and Den Outer, 1983; 45 species); 7) An orderly sequence in a repeating series only in a very few cases with sieve plates with of four uni- or multiseriate tangential layers ar• 2 or 3 sieve areas (type II; 4 species). Mean sieve• ranged in a regular or irregular way as follows: tube lengths preceded and followed by extreme a tangential layer of fibres (crystalliferous cells), values between brackets are: Bixaceae 235 J.I.Il1; followed by a layer of axial-parenchyma cells, a Bombacaceae (295-)395(-470) j..lm; Cae sal• layer of sieve tubes, a layer of axial-parenchyma piniaceae (190-)262( -320) j..lm; Papilionaceae cells, often occurs (31 species).
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Discussion structure is present in one species of a family, The presence of a storied structure is consid• one finds storied structure characteristics in all ered to be a specialised feature. In the second• other species of the same family and conversely. ary phloem, however, this does not mean that The composition of the Ivory Coast flora may all characteristics of the composing elements have exerted an important influence on the ob• and the tissue structure are necessarily also spe• tained results. The storied species all belong to cialised. If one uses Zahur's (1959) standards only two orders and one family. So it is not sur• (see also Esau, 1977, and Den Outer, 1983), it prising if character associations occur with for appears that the arrangement and structure of instance typical characters of the Malvales. The the axial parenchyma and mechanical tissue in trends reported here for secondary phloem may species with a storied structure, often must be be valid only for species from the Ivory Coast classified as not advanced. Sieve-tube elements and not for all species with a storied structure. and companion cells of storied species possess advanced characters bu t also characters that are References intermediate to primitive can occur; however, Beyer, 1.1. 1927. Die Vermehrung der radial en no primitive features (sieve-tube type I, sieve• Reihen im Cambium. Rec. Trav. Bot. Neerl. area type a, companion-cell type A) were found. 24: 631-786. In the axial system of the secondary phloem Chavan, R. R. & 1. 1. Shah. 1983. Statistical ap• (storied and non-storied) both advanced com• proach for the understanding of secondary panion-cell type (type C) and advanced sieve• phloem in 125 tropical dicotyledons. Proc. tube type (type III) are associated and there• Indian natl. Sci. Acad. B49: 28-36. fore correlated with a primitive axial-paren• Esau, K. 1977. Anatomy of seed plants. Ed. 2. chyma type (type -) and mechanical tissue Wiley, New York. type (type 3). The reverse correlation is also Janssonius, H.H. 1931.Die Verteilung des Stock• present (Den Outer, 1983). Since the secondary werkartigen Aufbaues im Holz der Diko• phloem with a storied structure possesses an ad• tylen. Rec. Trav. Bot. Neerl. 28: 97-106. vanced sieve-tube type associated with an inter• Metcalfe, C.R. & L. Chalk. 1979. Anatomy of the mediate or advanced companion-cell type, it is dicotyledons. Ed. 2. Vol. I. Systematic anat• clear that here too a primitive (or intermediate) omy of the leaf and stem, with a brief his• axial parenchyma type must be present togeth• tory of the subject. Clarendon Press, Oxford. er with a primitive mechanical tissue type. - & - 1983. Ditto. Ed. 2. Vol. II. Wood struc• Of the investigated species of the Ivory Coast ture and conclusion of the general introduc• the fusiform initial lengths and its derivatives are tion. Clarendon Press, Oxford. rather long in comparison with standards given Outer, R. W. den. 1972. Tentative determination by Zahur (1959). Sieve-tube element length key to 600 trees, shrubs and climbers from proved to be a dependable marker of phylo• the Ivory Coast, Africa, mainly based on geny of secondary phloem (Chavan & Shah, characters of the living bark, besides the 1983). Longer sieve-tube elements indicate here rhytidome and leaf. I. Meded. Landbouw• also a slightly more intermediate position of the hogeschool Wageningen 72-18: 1-73. secondary phloem. So in contradistinction to the - 1983. Comparative study of the secondary secondary xylem where storied structure is usu• phloem of some woody dicotyledons. Acta ally associated with advanced features, the sec• Bot. Neerl. 31: 29-38. ondary phloem as a whole is less advanced. These Patel, R.N. & A.Bowles.1980.Wood anatomy of deviations of the advanced construction pattern the dicotyledons indigenous to New Zealand. in the secondary phloem may be produced be• Piperaceae. New Zeal. J. Bot. 18: 507-514. cause the influence of the constan tJy changing Philipson, W.R., J.M. Ward & B.G. Butterfield. external factors is greater than in the secondary 1971. The vascular cambium. Chapman & xylem. Hall, London. It is also possible that the arrangement of sec• Reinders, E. & C.A. Reinders-Gouwentak.1961. ondary phloem characters determined by Zahur Handleiding bij de plantenanatomie. Van de O. c.) needs revision with regard to the axial-pa• Garde NV, Zaltbommel. renchyma and mechanical-tissue types; that is, Zagorska-Marek, B. 1984. Pseudotransverse di• these types have to change places from primitive visions and intensive elongation of fusiform to specialised and vice versa. In that case no prim• initials in the storeyed cambium of Tilia. itive characters are present in the secondary tis• Canad. J. Bot. 62: 20-27. sues (both phloem and xylem) of the investigated Zahur, M. S. 1959. Comparative study of sec• species. From our material alone it is not possi• ondary phloem of 423 species of woody ble to verify the statement made by other inves• dicotyledons belonging to 85 families. Cor• tigators (introduction: point 5) that, if storied nell Univ. Agr. Exp. St. Mem. 358: 1-160.
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