IAWA Bulletin n.s., Vol. 12 (2),1991: 143-175

NONDISPERSIVE PROTEIN BODIES IN SIEVE ELEMENTS: A SURVEY AND REVIEW OF THEIR ORIGIN, DISTRIBUTION AND TAXONOMIC SIGNIFICANCE

by

H..Dietmar Behnke Zellenlehre, Universitat Heidelberg, 1m Neuenheimer Feld 230, D-69oo Heidelberg, Germany

Summary Nondispersive protein bodies present in but has not been found in sieve elements of the sieve elements in addition to dispersive other plant classes. In the young nucleate P-protein are characteristic features of many sieve element, P-protein is first discernible woody dicotyledons; their origin may be nu• with the light microscope as small accumula• clear or cytoplasmic. While nuclear nondis• tions named P-protein bodies (earlier: 'slime persive protein bodies are found in only two bodies'). While in most angiosperms these families, the Boraginaceae and Myristicaceae, bodies disperse during the differentiation of bodies of cytoplasmic origin are present in 39 the sieve elements, some taxa are known to of the more than 350 families screened. These retain nondispersive P-protein bodies (cf. results were obtained from 228 dicotyledons Cronshaw & Sabnis 1990). studied with the electron microscope and data As early as 1886 Fischer depicted "some• of additional species from the literature. The thing in the shape of a small disk ... occur• terminology, origin, form and distribution of ring in almost all active sieve tubes of Urtica nondispersive protein bodies are discussed. . .. and by its reactions to be regarded as Their ultrastructural composition is described slime." He interpreted this body as a remnant as being predominantly spindle-shaped, com• of the not completely dissolving nucleus, but pound-spherical, rod-shaped and rosette-like. admitted: "I cannot decide definitely that this Based on the data accumulated from over 450 is a remnant of the nucleus. I was led to this species (of about 3000 screened) it is evident supposition by the shape of the thing in ques• that their taxonomic range is confined to a few tion" (Fischer 1886: 303, translated from Ger• dicotyledon superorders. Compound-spheri• man). Lecomte (1889) observed "globules cal nondispersive protein bodies are charac• des matieres albuminoides" in mono- and di• teristic of most of the Malvanae/Violanae; cotyledons, most of which turned out to be spindle-shaped forms are restricted to the identical with P-type sieve-element plastids Fabaceae (Rutanae). Rosanae-Proteanae• (see Behnke 1972). However, under the Myrtanae and the Magnolianae are the only heading of albuminous globules Lecomte also other superorders that contain nondispersive described that "each sieve tube of linden al• protein bodies in several of their families. ways contains at least one voluminous gran• Evolutionary trends and possible taxonomic ule (up to 4 ~m in diameter), ... and that in consequences implied in this distribution are "Rubus each tube contains a granule even discussed. much greater than those of linden" (Lecomte Key words: P-protein bodies, nuclear crys• 1889: 287, translated from French). tals, sieve elements, phloem. At about the same time Strasburger (1891) found a peculiar slime body in the sieve ele• Introduction ments of Robinia and Wisteria. He described P-protein (= phloem protein, Esau & Cron• its structure as elipsoidal, polygonal, spindle• shaw 1967; = 'slime' in earlier literature) is a or barrel-shaped and pointed out in particular characteristic component of angiosperm sieve that each body seemed to be suspended in the elements and is also occasionally present in middle of the cell lumen, the suspension be• companion and phloem-parenchyma cells, ing effected by means of a thin thread which

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extends from both ends of the body towards was open to a reinvestigation. Deshpande & the sieve plates (Strasburger 1891: 193). The Evert (1970) concluded that the persistent subsequent description by Baccarini (1892), spherical inclusion bodies in the sieve ele• Staritz (1893) and Mrazek (1910) of such ments of PopUlus, Quercus, Salix and TWa suspended slime bodies in more than 80 spe• did not have any connection with nucleoli. cies of the Fabaceae (but not in Caesalpinia• Oberhiiuser and Kollmann (1977) cytochemi• ceae or Mimosaceae) marked the distinction cally characterised the 'extruded nucleolus' of of a specific form of P-protein body that is Passiflora as protein inclusion, with no known to be restricted to the Fabaceae: the similarities to a nucleolus. Esau (1978a) in an spindle-shaped crystalline P-protein bodies. ultrastructural study of the differentiation of Crafts (1939) mentioned that "peculiarly the sieve elements of Gossypium found intact sculptured spherical bodies" are "common in nuclei with nucleoli next to and independent the sieve-tube elements of many angiosperms" from inclusion bodies and reevaluated the and "have been recognised in species of the formerly described 'extruded nucleoli' as following genera: Casuarina, Eucalyptus, spheroidal bodies related to P-protein. Gossypium, Melicytus, Populus, and Titia" Ultrastructural research provided the tools (Crafts 1939: 390-391). Salmon (1946) re• necessary to describe yet another category of ported on slime bodies in a great many of inclusion bodies in sieve elements: Esau & angiosperms, including tailed ("flagelloide") Magyarosy (1979a, b) detected protein crys• bodies in several Fabaceae and - most not• tals of nuclear origin in Amsinckia (Boragi• ably - a spheroidal body in Passiflora as well naceae) and traced their development from the as spiny forms ("ursiniforme") in Althaea, beginning of sieve-element differentiation Castanea and Urtica. through the enucleate condition. Subsequent Another category of sieve-element inclu• screening of other species in the family (Esau sion bodies was established by Esau (1947) & Thorsch 1982; Fisher et al. 1989) confirm• who reinvestigated Rubus, Gossypium and ed that nuclear protein crystals are a charac• Eucalyptus. In Rubus, Engard (1944) had teristic feature of the Boraginaceae (see also described the origin of inclusion bodies as an Behnke & Barthlott 1983). Among the many extrusion of nucleoli, but named them slime angiosperms studied, only one other family, bodies. Esau (1947) confirmed Engard's re• the Myristicaceae, was hitherto documented port, described an extrusion of nucleoli in to also contain nuclear crystals in their sieve sieve elements of Gossypium and Eucalyptus, elements (Behnke 1988, 1991). Previously, renamed them "extruded nuclei", and men• crystalloids derived from nuclei have been tioned their characteristic sculpturing and per• found in mature sieve elements of the fern sistence until the final breakdown of the sieve Platycerium bifurcatum (Evert & Eichhorn element. Eventually, Esau (1947) also reinter• 1974). - Tubular and filamentous protein preted the spherical bodies described earlier aggregates occurring in sieve-element nuclei by Crafts (1939) as extruded nucleoli. Zahur had previously been observed in TWa (Evert (1959) listed 41 species from twelve different & Deshpande 1970) and Gossypium (Esau families as containing extruded nucleoli (see 1978a). In contrast to the nuclear crystals, Table 1), and, finally, Kollmann (1960a, b) however, this protein is morphologically not described the extrusion phenomenon in Pas• distinct enough to trace it among the P-pro• siflora and was able to disclose the ultra• tein dispersed within the lumen of the enu• structural composition of the body. Other cleate sieve-element. early electron micrographs published showed The aim of this paper is to describe the dif• 'extruded nuclei' in TWa (Evert & Murmanis ferent forms of nondispersive protein bodies 1965) and Salix (Mishra & Spanner 1970). present in sieve elements and observed by the In the subsequent period of a more general author during his EM studies of more than application of electron microscopy (EM) to 2500 angiosperms and to give an annotated sieve elements, with its potentials to resolve review of all nondispersive protein bodies more details of their ontogeny and structure, hitherto described with light and electron the origin of the different inclusion bodies microscopy.

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Materials and Methods 228 species from 39 dicotyledon families 1970; Ilker & Currier 1975; Esau 1978a; (family delimitation after Dahlgren 1989) Nehls et al. 1978), crystalline P-protein were investigated. Results from 169 species bodies (Cronshaw 1975; Behnke 1981a; are reported for the first time (see Table 1 for Evert 1984, 1990; Cronshaw & Sabnis identification and origin of material). 1990), nondispersive or persistent P-protein Living material- recently removed from bodies (Behnke & Barthlott 1983; Behnke the plant or shipped within a few days under 1989a, b), paracrystalline protein or inclusion special care - is a prerequisite for a fixation bodies (Parameswaran 1983), nondispersing of sieve elements and the eventual investi• protein body (Esau & Cheadle 1984; Thorsch gation of their ultrastructural characters with & Esau 1988), and 'extruded nucleoli'. the transmission electron microscope. Thin Contrary to this, the non dispersive protein hand sections were made with a razor blade bodies of the Fabaceae have almost un ani• from young shoots or end parts of tree momdy been named crystalline P-protein or branches less than 1 cm in diameter. The P-ptbtein crystals (Wergin & Newcomb sections were immersed into Karnovsky's 1970; Palevitz & Newcomb 1971; Cronshaw (1965) fixing solution (containing sodium 1975; Lawton 1978a, b; Behnke & Pop cacodylate buffered formaldehyde and glu• 1981; Evert 1984, 1990; Cronshaw & Sabnis taraldehyde), kept therein for 3 to 24 hrs, 1990). Prior to the definition of P-protein washed in 0.1 M sodium cacodylate buffer other terms were used, e. g. irregular bodies (1 hr), postfixed in 1% buffered osmium (Bouck & Cronshaw 1965), fibrous slime tetroxide (1 hr), dehydrated through stepwise body (Wark & Chambers 1965), flagelloid or increasing concentrations of acetone, em• flagellate inclusions (Salmon 1946; Lafleche bedded in an Epon-Araldite-mixture and after 1966), "crystalline" inclusion body (Zee polymerisation processed according to stan• 1968), mucoid body (Gerola et al. 1969). dard methods. Nondispersive protein bodies of nuclear Material made available by collections origin were referred to as crystalline (nuclear) from original locations was sent to Heidel• inclusions (Esau & Magyarosy 1979a, b) or berg either fresh (causing a delay of up to a nuclear crystalloids (Esau & Thorsch 1982; week between sampling and start of fixation) Thorsch & Esau 1983; Fisher et al. 1989; or as fixed hand sections (causing an equally Behnke 1991). long delay between primary and postfixa• Proposal: In an attempt to standardise the tion). description of all proteinaceous inclusion Collections from botanical gardens or field bodies not bound by membranes and found collections by the author are represented by in enucleate sieve elements (Le. those protein 'Sieve-element plastid Vouchers' (SV, see bodies not dispersed during their ontogeny), Table 1) which are presently stored with the it is proposed to use the collective term author at Heidelberg, but will later be placed nondispersive protein bodies and add, where in the HElD herbarium. SV contain a sample necessary, specific epithets explaining their of the specimen collected, electron micro• origin (e.g., 'nuclear') or form and substruc• graphs of its typical plastid and other sieve• tural composition (e. g., 'compound-spheri• element characters, and an embedded block cal'). of the respective fixation used. Origin and diversity Only in a few species has the development Results and Discussion of nondispersive protein bodies been traced back to young nucleate, close to meristematic Terminology sieve elements. Ultrastructural studies introduced a con• The origin of nuclear nondispersive pro• fusing terminology as regards the protein tein bodies in the intact nucleus is undisputed bodies of mature sieve elements: inclusions and frequently demonstrated (Esau & Magya• or inclusion bodies (Deshpande & Evert rosy 1979a; Esau & Thorsch 1982; Behnke

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& Barthlott 1983; Thorsch & Esau 1983; to the crystalline P-protein bodies have been Fisher et al. 1989; Behnke 1991; see also depicted by the previous authors and were Figs. 1 & 2). In Amsinckia (Esau & Magya• discussed by Palevitz & Newcomb (1971) as rosy 1979a) and Echium (Esau & Thorsch evidence for their involvement in crystal de• 1982) their appearance in cells recently deriv• velopment, while Cronshaw (1975) as the ed from procambium was shown to serve result of an ontogenetic study of the sieve as one of the earliest markers for sieve ele• elements of Phaseolus vulgaris reports: "Ag• ments. gregates of tubular P-protein develop into In the primary phloem of hypocotyledon P-protein bodies, these are usually distinct or young internodal areas of several Faba• and appear to be unrelated to the crystalline ceae, the earliest recognisable sieve elements P-protein." were found to be devoid of spindle-shaped Compound-spherical nondispersive pro• (crystalline) nondispersive protein bodies tein bodies found in other dicotelydon fami• (Lafleche 1966; Wergin & Newcomb 1970; lies appear "before any other features iden• Palevitz & Newcomb 1971). Lafleche (1966) tifying the cell as a differentiating sieve recorded the presence of a "flagellate inclu• element become evident" (Esau 1978a: Gos• sion" in sieve elements located between 1 and sypium), are present in the earliest discernible 3 mm from the apex of Phaseolus vulgaris. sieve element (Behnke & Kiritsis 1983: Palevitz & Newcomb (1971) found small Drymis), and represent "the first outstanding thin crystals in young internodes and hypo• feature that identifies a differentiating sieve cotyls of Desmodium canadense and dis• element" (Thorsch & Esau 1988: Euphorbia). cussed their formation "by a rapid synthesis Although the earliest stages of nondispersive or condensation in sieve elements at a stage protein bodies were identified in future sieve when the elements still have thin cell walls elements just derived from a procambial and undifferentiated sieve plates." Using cell - and still incompletely separated from seedlings of Glycine max, Wergin & New• sister cells not containing such bodies (Esau comb (1970) described the formation of the 1978a), their exact origin, i. e., site and crystals as a conversion from tubular P-pro• conditions of protein synthesis, is not yet tein which originates from granular material settled. synthesised in the young sieve element. Tubular P-protein in close spatial association (text continued on page 159)

Legends of Figures 1-8 (pages 147-148):

~ Figs. 1 & 2. Nuclear nondispersive protein bodies in Horsfieldia sp. (Myrlsticaceae) -1: Young sieve element, x 5,000. - 2: Enucleate sieve element, x 20,000. - Figs. 3 & 4. Spindle-shaped nondispersive protein bodies. - 3: Securinega securidaca (Fabaceae), longitudinal section of enucleate sieve element, x 5,000. - 4: Lupinus polyphyl/us (Fabaceae), oblique cross section of nucleate sieve element with nondispersive protein body, x 10,000. - m = mitochondrium; n = nucleus; nc = nucleolus; p = plastid; pp = dispersed P-protein; star marks nuclear protein; arrows point to sieve pores; bars = 1 ~m. ~~ Fig. 5. Compound-spherical nondispersive protein body in nucleate sieve element of Xylotheca kraussiana (Flacourtiaceae), x 5,000. - Fig. 6. Globular/ovoid body in enucleate sieve element of Austrobaileya scandens (Austrobaileyaceae), x 3,000. - Fig. 7. Irregular bodies in nucleate sieve element of Elaeagnus angustifolius (Elaeagnaceae), x 15,000. - Fig. 8. Rod-cluster body in enucleate sieve element of Palmeria scandens (Monimiaceae), x 15,000. - ce = companion cell; m = mitochondrium; n = nucleus; p = plastid; PC = phloem-parenchyma cell; SE = sieve element; v = vacuole; arrows point to sieve pores; bars = 1 ~m.

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Figs. 5-8. See legend on page 146.

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Figs. 9-13. Nondispersive protein bodies in the Magnolianae. - 9: Compound-spherical body in Bubbia semecarpoides (Winteraceae). - 10: Rod-shaped body in Galbulimima baccata (Hi• mantandraceae). - 11-13: Compound-spherical bodies of Monimiaceae. - 11: Tetrasynandra loxiflora. - 12: Matthaea calophyUa. - 13: Xymalos monospora. - p = plastid; bars = 1 ).lill.

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Figs. 14-17. Compound-spherical nondispersive protein bodies in the Malvanae 1. - 14: Ster• culia cf. conwsa (Sterculiaceae), x 10,000. - 15: Modiola multifida (Malvaceae), x 20,000. - 16: Colona scabra (Tiliaceae), x 20,000. - 17: Bombax ellipticum (Bombacaceae), x 20,000. - pp = dispersed P-protein; arrows point to sieve pores; bars = 111m.

-t Figs. 18-22. Compound-spherical nondispersive protein bodies in the Malvanae II. - 18: Arto• carpus integrifolia (Moraceae), x 20,000. - 19: Coussapoa schottii (Cecropiaceae), x 20,000.- 20: Pteroceltis tatarinowii (Ulmaceae), x 18,000. - 21: Acalypha wilkesiana (Euphorbiaceae), x 20,000. - 22: Dichapetalum guineense (Dichapetalaceae), x 20,000. - m = mitochondrium; pp = dispersed P-protein; arrows point to sieve pores; bars = 111m.

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24

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Figs. 23-25. Compound-spherical nondispersive protein bodies in the Violanae I. - 23: Smeath• mannia pubescens (Passifloraceae), x 14,000. - 24: Erythrospermum phytolaccoides (Flacour• tiaceae), x 14,000. - 25: Jdesia polycarpa (Flacourtiaceae), x 50,000. - arrows point to sieve pores; bars = 1 fl.m. - Figs. 26-29. Compound-spherical nondispersive protein bodies in the Vio1anae II. - 26: Doryalis caffra (F1acourtiaceae), x 7,000. - 27: Turnera ulmifolia (Turnera• ceae), x 20,000. - 28: Hymenanthera dentata (Violaceae), x 30,000. - 29: Melicytus ramijlorus (Violaceae), x 50,000. - pp = dispersed P-protein; arrows point to sieve pores; bars = 111m.

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Figs. 30-33. Nondispersive protein bodies in the Rosanae I. - 30: Rod-cluster body in Tetra• centron sinense (Tetracentraceae), x 20,000. - 31: Barrel-shaped body in Nothofagus ob/iqua (Nothofagaceae), x 10,000. - 32: Compound-spherical body in Lithocarpus densiflora (Faga• ceae), x 30,000. - 33: Compound-spherical body in Casuarina equisetifolia (Casuarinaceae), x 30,000. - pp = dispersed P-protein; arrows point to sieve pores; bars = 1 ~m.

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Figs. 34-37. Nondispersive protein bodies in the Proteanae I. - 34: Irregular body in EZaeag• nus angustifolius (Elaeagnaceae), x 20,000. - 35-37: Rosette-like bodies in Proteaceae. - 35: Stenocarpus salignus, x 20,000. - 36: Banksia baxteri, x 20,000. - 37: Lomatia illicifolia, x 20,000. - er = endoplasmic reticulum; bars = 1 Jl.m.

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Figs. 40-42. Nondispersive protein bodies in the Rosanae ll. - 40: Compound-spherical body in Cunonia capensis (Cunoniaceae), x 20,000. - 41: Compound-spherical body in Crataegus dippeli• ana (Malaceae), x 20,000. - 42: Rod-shaped body in Exochorda giraldii (Amygdalaceae), x 6,000. - Fig. 43. Compound-spherical body in Agonisflexuosa (Myrtaceae), x 30,000. - p = plasid; pp = dispersive P-protein body; w = nacreous wall; arrows point to sieve pores; bars = 1 j.l.m. f- Figs. 38 & 39. Nondispersive protein bodies in the Proteanae II. - 38: Leucadendron tortum (Proteaceae), x 50,000; bar = 1 j.l.m. - 39: Substructural composition of protein body in Protea punctata (Proteaceae), x 100,000.

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- 46

Figs. 44-46. Compound-spherical nondispersive protein bodies in different taxa. - 44: Strom• bosia ceylanica (Olacaceae), x 5,000. - 45: Goupia sp. (Celastraceae), x 20,000. - 46: Perilla Jrutescens (Lamiaceae), x 20,000. - Arrows point to sieve pores; bars = 1 ~m.

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Morphology and distribution among angio• ceae, e.g. Amsinckia, contain compound sperms crystals, i.e. composed of dense and loose Whatever the origin of the different non• parts (Esau & Magyarosy 1979a, b; Fisher et dispersive protein bodies and however di• al. 1989), the dense parts resembling other verse their ultrastructural morphology turn crystals in the family whereas the loose parts out to be, their restriction to sieve elements are composed of tubular units which after and persistence in enucleate cells are common disintegration of the nucleus are dispersed but features supporting the concept of a unifying stay distinct from dispersive P-protein (Esau nomenclature. Moreover, for several differ• & Magyarosy 1979b). Some of the cross• ent forms it has been demonstrated by histo• sectioned nuclear crystals of Amsinckia chemical staining (Ilker & Currier 1975) and closely resemble views from developing digestion with proteolytic enzymes (Ober• spindle-shaped bodies depicted in young hauser & Kollmann 1977; Nehls et al. 1978; sieve elements by Wergin and Newcomb Thorsch & Esau 1983; Behnke 1986b) that (1970). nondispersive protein bodies are composed A reinvestigation of Uncarina and other of proteins only. The sizes of nondispersive Pedaliaceae did not reveal persistent nuclear protein bodies range from about 1 J.LII1 to more crystals in their sieve elements. The lamellate than 30 J.LII1. crystals depicted in sieve-element nuclei of Structural details of the protein crystals Uncarina (Behnke & Barthlott 1983) were revealed with the electron microscope are not present in enucleate mature sieve ele• generally explained as fine striations showing ments. a periodicity of about 12 nm (Figs. 29 & 39; Several species of the Proteaceae investi• see also Lafleche 1966; Wergin & Newcomb gated by the author contain rosette-like crys• 1970; Palevitz & Newcomb 1971; Lawton tals (Figs. 35-37 and Table 1) that may look 1978a) or less (Behnke 1991). Proposals of like nuclear crystals. However, their nuclear their substructural organisation have only origin could not been shown so far. rarely been published. A tubular composition The crystalline nondispersive protein bod• was first disclosed by Kollmann (1960b) in ies of the Fabaceae are generally referred to the "extruded nucleolus" of Passiflora (see as being spindle-shaped. In most species the also Oberhauser & Kollmann 1977). Nehls et body is composed of a central part, that is al. (1978) describe the compound-spherical elongate in longitudinal section (Fig. 3) and body of Salix to be composed of hexagonal• square or rectangular in cross section (Fig. ly, densely arranged 18 nm wide tubules and 4), and in general two tails, one inserted at explain the appearance of two different sizes each end of the central part, suspending the of striations in a model. Tightly packed 'four• body in the enucleate sieve element (cf. Stras• sided' tubules in transections and parallel burger 1891). Not all of the investigated spe• striations in longitudinal sections were also cies have tails: Mrazek (1910) lists several detected in nuclear crystals of Boraginaceae species that lack tails, Lawton (1978a) pro• (Esau & Magyarosy 1979a; Esau & Thorsch poses a general distinction between tailed and 1982). tailless bodies. Different shapes of the central Nuclear nondispersive protein bodies are part, i. e. other than spindle-shaped, have distinct by their specific forms resembling to been recognised and named barrel- or rod• some extent inorganic crystals and having shaped (Strasburger 1891; Staritz 1893; Mra• sharp edges. Elongate solitary crystals that zek 1910). are rectangular in cross sections and extend Ultrastructural studies depict the central through the entire length of a nucleus are part as composed of striated filaments or found in many Boraginaceae (Esau & Thorsch tubules that are in connection to the like• 1982; Behnke & Barthlott 1983; Fisher et at. wise structured tails (Lafleche 1966; Wergin 1989). Crystal aggregates in the form of ro• & Newcomb 1970; Palewitz & Newcomb sette-like crystals are found in other Boragin• 1971). In enucleate sieve elements the central aceae and are typical of Myristicaceae (Figs. part often disintegrates into loosely arranged 1 & 2; cf. Behnke 1991). A few Boragina- filaments (see e.g. figures in Lafleche 1966,

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Wergin & Newcomb 1970, Behnke 1981b) 27), Violaceae (Figs. 28 & 29) and Salica• which, however, do not disperse in the ceae (Table 1), the Sterculiaceae (Fig. 14), sieve-element lumen. Fisher (1975) and Malvaceae (Fig. 15), Bombacaceae (Fig. 17), Lawton (1978b) have demonstrated that the Tiliaceae (Fig. 16), Moraceae (Fig. 18), Ce• spindle-shaped protein bodies do not dis• cropiaceae (Fig. 19), Urticaceae (Table 1), perse in uninjured sieve elements. Dichapetalaceae (Fig. 22) and Euphorbiaceae Reports by Baccarini (1892) and Zahur (Fig. 21), the Myrtaceae (Fig. 43), Malaceae (1959) on the presence of nondispersive pro• (Fig. 41) and Rosaceae (Table 1). In the Fa• tein bodies and Poinciana (= Delonix) and gaceae (Fig. 32; see also Deshpande & Evert Cassia (both Caesalpiniaceae) were not con• 1970; Parameswaran 1983) and Casuarina• firmed in ultrastructural studies nor corrobor• ceae (Fig. 33), in some Flacourtiaceae (Figs. ated by other genera tested in the Caesalpinia• 25, 26) and in some Passifloraceae (e.g., ceae (Behnke & Pop 1981) and therefore Passiflora, Oberhiiuser & Kollmann 1977) may have been a result of wrongly determin• the core is less densely packed and appears to ed material. On the other hand, the finding of be composed of the same type of aggregates tailed spindle-shaped nondispersive protein that form the mantle. bodies in the sieve elements of Swartzia Less regularly arranged nondispersive pro• (formerly Caesalpiniaceae) adds support to tein bodies were found in Rhus (Anacardia• include this genus in the Fabaceae (cf. Behn• ceae) and described as stellate by Deshpande ke 1981b). & Evert (1970). Similar aggregates were ob• served in some species of Monimiaceae (Fig. Nondispersive protein bodies found in 11), Proteaceae (Figs. 38, 39) and Wintera• other dicotyledon families are of different ceae (Fig. 9; see also Behnke 1981a). Since it shapes and were mostly referred to as spher• cannot presently be ruled out that exact serial oidal or spherical. Our present EM-study sectioning may eventually reveal a core, these distinguishes mainly between compound• bodies are filed among the compound• spherical, rod-shaped and rosette-like bodies spherical. (Table 1). A new category of nondispersive protein Compound-spherical bodies are the most bodies was observed in several species of the common form found among dicotyledons Proteaceae (see Table 1) and is named rosette• (Table 1, cs) and conform to many nondis• like. Several to many protein crystals with persive protein bodies described in light sharp edges are gathered into a compound microscopy (see Table 1). Although some body that shows similarities to a rosette or variations exist, compound-spherical bodies druse crystal (Figs. 35-37). are generally composed of a core and a struc• Large rod-shaped nondispersive protein tured mantle. The mantle is preferentially bodies are found in a few genera, mostly composed of rod-like or similarly shaped within families that also contain other non• protein crystals (Figs. 13, 32, 33, 43, 46). dispersive bodies, e. g. in Fagus (Schulz & The core may consist of one (occasionally Behnke 1987), Exochorda (Fig. 42), Galbu• few) densely packed protein crystal(s) (see limima (Fig. 10). A few genera, e.g., Pal• Figs. 28, 29) from which the rods radiate or me ria (Fig. 8) and Tetracentron (Fig. 30), of a rather homogeneous mass (Figs. 13). contain nondispersive protein bodies that are Rarely, the mantle lacks a crystalline sub• composed of parallel rods (rod-cluster). structure (Fig. 20) but may be composed of Nondispersive protein bodies with shapes filaments or tubules, a modification that is that did not fit into any of these categories found in some Urticales and has previous• were observed in a few other taxa: bodies ly been named 'globular' (Behnke 1981a, with globular or ovoidal outlines and homo• 1989b). geneous, non-crystalline contents were de• Families that typically contain compound• scribed in Austrobaileya (Fig. 6 and Behnke spherical nondispersive protein bodies in• 1986a, b); barrel-shaped bodies in Nothofa• clude the Flacourtiaceae (Figs. 5, 24-26), gus (Fig. 31); and irregular bodies in Elae• Passifloraceae (Fig. 23), Turneraceae (Fig. agnaceae (Figs. 7, 34).

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Table 1. Dicotyledon taxa found to contain nondispersive protein bodies.

Family =families recognised in Dahlgren (1989); SV =sieve element plastid voucher; Herb. = heroarium where other vouchers are deposited; LM = form of bodies reported in light microscopic study; EM = form shown in electron microscopic study. Abbreviations: ba =barrel-shaped; cs =compound spherical; dis =discoid; exn =extruded nucleolus; fla =fla• gellar; gl =globular; ir = irregular; ma = gelatinous masses; nc = nuclear crystal; nde = not defined; ndp = nondispersing protein body; ov =ovoid; rc = rod-cluster; rd =rod-shaped; ro =rosette-like; sli - slime; sp = spindle-shaped; sph =spherical/spheroidal; st =stellate; urs =spinous (ursinifonne). Fig. =illustrations present in this paper (numbers) or in reference given (#); * in References refers to data published here for the first time; Origin of material by collector or botanical garden (BG, abbreviations of cities after Index Herbariorum).

Family / Species SV Hero. LM EM Fig. References/Origin of material

Amygdalaceae Exochorda giraldii Hesse + rd 42 * /BG-HEID Anacardiaceae Rhus glabra cs(st) # Deshpande & Evert 1970 AustrobaiJeyaceae Austrobaileya maculata C.T. White + gl/ov # Behnke 1986a, b Austrobaileya scandens C.T. White WU gl/ov 6 * / R. Tracey (Australia) Betulaceae Betula papyrifera Sukatsch. + cs(gl) Behnke 1989b Betula verrucosa sph # Salmon 1946 Bombacaceae Bombax ellipticum H.B.K. cs 17 * /BG-B Ceiba pentandra sph Deshpande 1983 Durio zebethinus exn Zahur 1959 Montezuma cubensis Urb. + cs * /BG-C Boraginaceae Amsinckia douglasiana A. DC. nc # Esau & Magyarosy 1979a, b Amsinckia intermedia F. & M. nc # Thorsch & Esau 1983; Amsinckia mensiesii (Lehm.) [Fisher et aI. 1989 Nels. & Macbr. nc # Fisher et aI. 1989 Amsinckia spectabilis nc # Fisher et aI. 1989 Anchusa azurea Mill. nc Fisher et aI. 1989 Anchusa hybrida Ten. nc Fisher et aI. 1989 Borago officinalis L. nc Fisher et aI. 1989 Cerinthe glabra Mill. nc Fisher et aI. 1989 Cerinthe major L. nc Fisher et aI. 1989 Cerinthe minor L. nc # Fisher et aI. 1989 Cordia lutea Lam. nc Fisher et aI. 1989 Cryptantha maritima Greene nc Fisher et aI. 1989 Cynoglossum columnare Bivona nc Fisher et aI. 1989 Cynoglossum creticum Mill. nc Fisher et aI. 1989 Cynoglossum gennanicum Jacq. nc # Fisher et aI. 1989 Cynoglossum nervosum Benth. + nc * IBG-HEID Cynoglossum officinale L. nc Fisher et aI. 1989 Cynoglossum wallichii G. Don. nc Fisher et aI. 1989 Echium acanthocarpum Svent, nc Fisher et aI. 1989 Echium aculeatum Poir. nc Esau & Thorsch 1982 Echium angustifolium Mill. nc # Esau & Thorsch 1982 Echium benthencourtii A. Santos nc # Esau & Thorsch 1982 Echium decaisnei Webb & Berth. nc Esau & Thorsch 1982 Echium fastuosum Jacq. nc Esau & Thorsch 1982 Echium giganteum L. f. nc # Esau & Thorsch 1982 Echium handiense Svent. nc Esau & Thorsch 1982 Echium judaeum Lacaita nc # Esau & Thorsch 1982

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Family / Species SV Herb. LM EM Fig. References/Origin of material

(Boraginaceae continued) Echium lusitanicum L. nc Fisher et al. 1989 Echium onosmifolium Webb. & Berth. nc Fisher et al. 1989 Echium pininiana Webb. & Berth. nc # Fisher et al. 1989 Echium plantagineum L. nc Esau & Thorsch 1982 Echium rosulatum Lange nc Esau & Thorsch 1982 Echium russicum J.F. Gme!. nc Fisher et al. 1989 Echium sabulicola Pomel nc # Esau & Thorsch 1982 Echium simplex DC. nc Esau & Thorsch 1982 Echium strictum L. f. nc # Esau & Thorsch 1982 Echium tuberculatum Hoffm. & Link nc Fisher et al. 1989 Echium virescens DC. nc Esau & Thorsch 1982 Echium vulgare L. nc Fisher et al. 1989 Echium wildpretii H. Pearson ex Hook. f. nc # Esau & Thorsch 1982 Eritrichium rupestre Bunge nc Fisher et al. 1989 Heliotropium curassavicum L. nc Fisher et al. 1989 Lappula deflexa Garcke nc Fisher et al. 1989 Lappula myosotis Moench. nc # Fisher et al. 1989 Lindelofia longiflora (Benth.) Baill. + nc * /BG-HEID Lindelofia macrostyla (Bunge) Popov. nc Fisher et al. 1989 Lithodora diffusa (Lag.) 1. M. Johnsl nc Fisher et al. 1989 Lithospermum officinale L. nc Fisher et al. 1989 Myosotis latifolia Poir. nc # Fisher et al. 1989 Nonnea lutea (Desr.) DC nc Fisher et al. 1989 Omphalodes linifolia Moench. nc Fisher et al. 1989 Omphalodes cappadocica (Willd.) DC. nc Fisher et al. 1989 Onosma stellatum Waldst. & Kit. nc # Fisher et al. 1989 Plagyobothrys undulatus (Piper) 1.M. Johnst. nc Fisher et al. 1989 Pulmonaria mollis Wolff. + nc # Behnke & Barthlott 1983 Symphytum orientale L. nc Fisher et al. 1989 Trichodesma scotti Balf. f. nc Fisher et al. 1989 Casuarinaceae Casuarina cunninghamii Miq. cs Behnke 1989b Casuarina equisetifolia L. cs 33 Behnke 1989b Casuarina sp. sph Crafts 1939 Casuarina stricta Dryand cs Behnke 1989b Cecropiaceae Coussapoa schottii Miq. + cs(gl) 19 Behnke 1989b Celastraceae Goupiasp. + MO cs 45 * / B. Nelson (Brasil) Cunoniaceae Cunonia capensis L. + cs 40 * /BG-HEID Weinmannia parviflora exn Zahur 1959 Dichapetalaceae Dichapetalum guineense (DC.) Keay + cs 22 * /BG-BR Ehretiaceae Ehretia anacua 1.M. Johnst. nc Fisher et al. 1989 Elaeagnaceae Elaeagnus angustifolius L. + ir 7, 34 * /BG-HEID Euphorbiaceae Acalypha sp. exn Zahur 1959 Acalypha wilkesiana Muel!. Arg. + cs 21 * /BG-HElD Bischofia javanica exn Zahur 1959 Euphorbia pulcherrima ndp/cs # Thorsch & Esau 1988 Jatropha sp. rd * /BG-HEID Joannesia princeps VeIl. cs * /BG-K

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Family I Species SV Herb. LM EM Fig. References/Origin of material

(Euphorbiaceae continued) Macaranga gIlIIIdifoIia exn Zahur 1959 Macaranga sp. exn Zahur 1959 Fabaceae Abrus precatorius L. sp • I O.S. Paliwal (India) Adesrnia rnuricata DC. sp • I BO-C Alhagi pseudoalhagi (M.B.) Desv. sp • IO.S. Paliwal (India) Amicia zygorneris rd # Mrazek 1910 Amorpha fragIllllS rna Baccarini 1892 Amorpha fruticosa rna Baccarini 1892 AnarthrophyUurn elegans Phil. f. Cat. MO sp • I BO-MO Andira stipuIacea Benth. + sp • I BO-RB (K. Kubitzki) AnthyIIis tetraphylla rna Baccarini 1892 AnthyIIis vuIneraria L. rna Baccarini 1892; + sp • I BO-HEID Apios americana Medik. sp # Baccarini 1882; Staritz 1893; (= tuberosa Moench) sp # Behnke & Pop 1981 Arachis hypogaea rna Baccarini 1892 Astragalus cicer L. sp # Behnke & BarthIolt 1983 Astragalus falcatus Lam. ba # Staritz 1893; sp • I BO-HEID Astragalus glycyphyllos rd # Mrazek 1910 Astragalus sesameus rna Baccarini 1892 Astragalus sp. rna Baccarini 1892 Baptisia australis R. Br. ov # Staritz 1893; sp • I BO-HEID BiserruIa pelecinus rna Baccarini 1892 Bolusanthus speciosus Harms sp • lBO-Fro Butea rnonosperma Kuntze sp • IO.S. Paliwal (India) Calycotorne spinosa Link sp • I BO-C Canavalia ensiformis (L.) DC. sp • lBO-BONN Caragana decorticans sp Zahur 1959 Carmichaelia australis sp Zahur 1959 Castanospermum austtaIe sp Zahur 1959 Christia vespertilionis (L. f.) Bakh. f. sp • lBO-BONN Cicer arietinurn rna sp Baccarini 1892; Arsanto 1982 Clitoria temata L. sp # Behnke & Pop 1981 Coronilla coronata L. sp • I BO-HEID Coronilla scorpioides rna Baccarini 1892 Coronilla stipuIaris rna Baccarini 1892 Coronilla valentina rna Baccarini 1892 Coronilla varia rd Mrazek 1910; sp # Palevitz & Newcomb 1971 Coronilla vera rna Baccarini 1892 CrotaIaria juncea L. sp • I raised from seeds Cytisus adami sp Mrazek 1910 Cytisus albus Hacq. sp ,. I BO-HEID Cytisus candicans sp # S taritz 1893 Cytisus hirsutus IXle # Salmon 1946 Cytisus purpureus ba # Mrazek 1910 Dalbergia sisso Roxb. ex DC. sp ,. I O.S. Paliwal (India) Dalea frutescens A. Oray + sp ,. I Texas (Behnke & Eifert) Desmodium canadense sp # Palevitz & Newcomb 1971 Desrnodiurn gyrans rna # Baccarini 1892 Desrnodiurn iIIinoense sp Palevitz & Newcomb 1971 Desrnodium penduIifIorurn rna/ba # Baccarini 1892; Staritz 1893 Desrnodiurn uncinatum DC. sp ,. I BO-C

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Family / Species SV Herb. LM EM Fig. References/Origin of material

(Fabaceae continued) Desmodium viridif10rum rna Boccarini 1892 Dichilus lebeckoides DC. PRE sp */BG-MO Dolichos jacquinianus rna Boccarini 1892 Dolichos lablab rna Baccarini 1892; sp Palevitz & Newcomb 1971 Dolichos lignosus rna # Boccarini 1892 Dorycnium herbaceum ViiI. + sp * /BG-HEID Dorycnium suffruticosum ba # Staritz 1893 Ebenus cretica rna Boccarini 1892 Erythrina coraJloides Moe. & Sesse ex DC. sp * /BG-BONN Erythrina cristagalli ma/ba # Baccarini 1892; Staritz 1893 Erythrina insignis rna Boccarini 1892 Erythrina monosperma sp Zahur 1959 Erythrina viarum rna Boccarini 1892 Galega officinalis rna # Baccarini 1892: Staritz 1893 Genista aetnensis rna Boccarini 1892 Genista radiata (L.) Scop. + sp * /BG-HEID Genista sibirica ov # Staritz 1893 Glycine max (L.) Merr. sp # Wergin & Newcomb 1970; sp * /BG-C Glycine soja Sieb. et Zucco sp * /BG-C Glycyrrbiza echinata L. + sp * /BG-BONN Glycyrrhiza glabra rna # Boccarini 1892 Gonoeytisus angulatus (L.) Spach MO sp * /BG-MO HaJimodendron halodendron (pall.) Voss ba # Staritz 1893; Zahur 1959 (= argenteum DC.) sp * /BG-C Hebestigma cubense Urb. sp * /BG-FfG Hedysarum capitatum rna Boccarini 1892 HedYsarum coronarium rna # Boccarini 1892 Hedysarum flexuosum L. sp * /BG-C Hippocrepis unisiJiquosa rna Boccarini 1892 Hovea longifolia (R. Br.) Ait. sp * /BG-BONN Hymenocarpus circinnatus rna Boccarini 1892 Inoearpus edulis Forst. sp Zahur 1959; sp * / Waimea Arboretum Kennedia pubescens rna Boccarini 1892 Kennedia rubicunda (Schneev.) Vent. MO sp * /BG-MO Laburnum anagyroides Medik. rd/sp # Staritz 1893; Mrazek 1910; (= Cytisus laburnum) fla Salmon 1946; + sp * /BG-HEID Lathyrus c1ymenum rna Boccarini 1892 Lespedeza crytobotrya sp Zahur 1959 Lespedeza thunbergii (DC.) Nakai sp */BG-BONN Liparia splendens sp * / BG-Kirstenbosch (Gold- Lonchoearpus sp. sp * /Venezuela (Behnke) [blatt) Lotus americanus Bisch. sp * /BG-C Lotus comiculatus rna Boccarini 1892 Lotus creticus rna Boccarini 1892 Lotus edulis rna Boccarini 1892 Lotus omithopoides rna Baccarini 1892 Lotus tetragonolobus rna # Boccarini 1892 Lupinus angustifolius sp # Mrazek 1910 Lupinus luteus sp # Mrazek 1910 Lupinus polyphyllus Lindl. + sp 4 * /BG-HEID Maackia chinensis Takeda MO sp */BG-MO

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Family / Species SV Herb. LM EM Fig. References/Origin of material

(Fabaceae continued) Medicago maritima rna Baccarini 1892 Medicago orbicularis rna Baccarini 1892 Medicago sativa ba # Mrazek 19lO; sp Palevitz & Newcomb 1971 Medicago scutellaris rna Baccarini 1892 Melilotus alba rna Baccarini 1892 Melilotus messanensis rna Baccarini 1892 Melilotus sulcata rna Baccarini 1892 Millettia thonningii Baker + sp * /BG-K Mucuna deeringiana (Bort.) Merr. sp * / raised from seeds Onobrychis sp. sp * / L. Pop (near Besan~on) Ononis hircina sp-ba # S taritz 1893 Ononis sp. rna Baccarini 1892 Ononis spinosa L. sp * /BG-HEID Ormosia desycarpa sp Zahur 1959 Ornithopus compressus rna Baccarini 1892 Oxylobium lanceolatum Druce MO sp * /BG-MO Pericopsis mooniana Thw. sp * / Waimea Arboretwn Petteria ramentacea (Sieber) K.B. Presl. sp * /BG-C Phaseolus caraca1la rna Baccarini 1892 Phaseolus coccineus L. (= multiflorus Lam.) sp sp # Mrazek 19lO;Lawton 1978a,b Phaseolus lunatus sp # Mrazek 1910 Phaseolus vulgaris L. ma/sp # Baccarini 1892; Salmon 1946; fla # LaFleche 1966; Gerola et aI. 1969; sp # Palevitz & Newcomb 1971; sp # Cronshaw 1975; Esau 1978b Piscidia erythrina sp Zahur 1959 Pisum sativum L. sp/nde Mrazek 1910; Salmon 1946; sp # Bouck & Cronshaw 1965; sp # Wark & Chambers 1965; sp # Zee 1968; Schulz 1986 Pongamia glabra sp Zahur 1959 Psoralea bituminosa rna Baccarini 1892 Psoralea onobrychis Nutt. sp * /BG-C Pterocarpus indicus sp Zahur 1959 Pueraria phaseoloides Benth. + sp * /BG-K Pueraria sp. fla # Salmon 1946 Rbynchosia precatoria ov # S taritz 1893 Rhynchosia pyramidalis Urb. sp */BG-BONN Robinia hispida sp Mrazek 1910 Robinia pseudoacacia L. (incl. monophylla) sp/fla # Strasburger 1891; Salmon 1946; sp Zahur 1959; + sp # Behnke 1981a Robinia viscosa Vent. sp * /BG-C Sarothamnus scoparius sp Mrazek 1910 Scorpittrus subvillosa rna Baccarini 1892 Securigera securidaca Dalla Torre & Sarnth. + sp 3 * /BG-K Sesbania platycarpa Pers. sp * / raised from seeds Sophora chrysophylla sp Zahur 1959 Sophora japonica sp Zahur 1959 Sophora tetraptera sp Zahur 1959

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Family / Species SV Herb. LM EM Fig. References/Origin of material

(Fabaceae continued) Spartium junceum L. MO sp * /BG·MO Strongylodon lucidum sp Zahur 1959 Strongylodon sp. sp * / Waimea Arboretum Sutherlandia frutescens rna Baccarini 1892 Swartzia crocea Benth. sp # Behnke 1981b Templetonia retusa R.Br. MO sp * /BG·MO Thermopsis fabacea (pall.) DC. + sp * /BG·HEID Trifolium pratense sp Mrazek 1910 Trifolium sp. rna Baccarini 1892 Trigonella foenum·graecum rna Baccarini 1892 Vicia faba sp # Mrazek 1910 Vicia sativa sp Mrazek 1910 Vicia sp. rna # Baccarini 1892 Vicia unijuga A. Br. + sp * /BG·HEID Wisteria sinensis (Sims) Sweet + sp/fla # Strasburger 1891; Salmon 1946; sp * /BG·HEID Fagaceae Castanea sativa Mill. + cs # Behnke 1989b Castanea sp. urs # Salmon 1946 Castanopsis bomeensis King cs # Parameswaran 1983 Fagus sylvatica L. + rd # Behnke & Schulz 1987; Behnke 1989b Lithocarpus densiflora Rehder cs 32 Behnke 1989b Quercus alba cs # Deshpande & Evert 1970 Quercus edulis Makino (= Pasania) cs Behnke 1989b Quercus glauca Thunb. (= Cyc1obalanopsis) cs Behnke 1989b Quercus robur L. (= Pseudoaegilops) + cs # Behnke 1989b Trigonobalanus verticillata Forman cs Behnke 1989b Flacourtiaceae Aheria gardneri exn Zahur 1959 Azara microphylla Hook. cs * /BG·HEID Casearia sylvestris Sw. + cs * /BG·BO Doryalis caffra (Harv. et Sond.) Warb. + cs 26 * /BG·HEID Erythrospermum phytolaccoides Gardn. + cs 24 * /BG·BO Flacourtia cataphracta exn Zahur 1959 Flacourtia inermis exn Zahur 1959 1desia polycarpa Maxim. cs 25 * /BG·HEID Kiggelaria africana L. + cs * /BG·HEID Oncoba spinosa Forsk. cs * /BG·MJG Poliothyrsis sinensis Hook. cs # Behnke & Barthlott 1983 Xylosma congestum cs # 1lker & Currier 1975 Xylosma hillebrandii exn Zahur 1959 Xylosma sp. exn Zahur 1959 Xylotheca kraussiana Hochst + cs 5 * / G. Merz et al. Himantandraceae (Ivory Coast) Galbulimima baccata Bailey rd 10 * / R. Tracey (Australia) Lamiaceae Perilla frutescens (L.) Britt. + cs 46 * /BG·HEID Malaceae Crataegus x dippeliana Lange + cs 41 * /BG·HEID Pyracantha coccinea M.J. Roem. + cs * /BG·HEID Malvaceae Althaea officinalis L. + urs # Salmon 1946; cs * /BG·HEID

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Family / Species SY Herb. LM EM Fig. References/Origin of material

(Malvaceae continued) Fugosia hakeaefolia Hook. cs * /BG-K Gossypium hirsutum L. sph/exn cs # Crafts 1939; Esau 1947, 1978a Hibiscadelphus giffordianus exn Zahur 1959 Hibiscadelphus hualalaiensis exn Zahur 1959 Hibiscus amottianus exn Zahur 1959 Hibiscus kokio exn Zahur 1959 Hibiscus rosa-sinensis exn Zahur 1959 Hibiscus tiliaceus exn Zahur 1959 Modiola multifida Moench cs 15 * /BG-HEID Napaea dioica L. cs * /BG-C Pavonia praemorsa Cay. cs * /BG-HEID Sida meyeniana exn Zahur 1959 Thespesia acutiloba (Bak. f.) Exell & Mendosa + cs * /BG-K Thespesia populnea exn Zahur 1959 Monimiaceae Hedycarya angustifolia A. Cunn. + cs * / J. Jacobs (Australia) Levieria beccariana Perk. L cs * / Philipson 3661 Matthaea calophylla Perkins + cs 12 Behnke 1988 Mollinedia sp. ex aff. M. floribunda Tu!. WU cs * /Morawetz 12-91280 Mollinedia sp. nov. ined. ex aff. M. widgrenii A. DC WU cs * /Morawetz 22-15381 Palmeria pulchra Perk. L rc * / Philipson 3667 Palmeria scandens F. Muel!. rc 8 * / R. Tracey (Australia) Peumus boldus Mol. + rc * /BG-DUSS Tambourissa purpurea A. DC. MO cs(st) # Behnke 1981a Tetrasynandra longipes Perkins BRI cs * / Webb & Tracey 11051 Tetrasynandra loxiflora Perkins cs 11 * / Irvine & DOrr (Australia) Xymalos monospora Baill. + cs 12 * / R. Pretorius (Lowveld BG) Moraceae Artocarpus integrifolia L. cs 18 Behnke 1989b Brosimum alicastrum Sw. + cs Behnke 1989b Castilla ulei Warb. + cs Behnke 1989b Myrtaceae Agonis flexuosa (Willd.) Lind!. cs 43 * /BG-K Angophora cordifolia Cav. cs * /BG-K Callistemon phoeniceus Lind!. + cs * /BG-HEID Calothamnus rupestris Schau. cs * /BG-MJG Eucalyptus rostrata Schlecht. exn # Esau 1947 Eucalyptus sp. sph/exn Crafts 1939; Zahur 1959 Eucalyptus viminalis Labill cs * /BG-HEID Eugenia edulis Yell. (= Hexachlamys) cs * /BG-MJG Eugenia jamboIana exn Zahur 1959 Eugenia moluccana exn Zahur 1959 Eugenia sp. exn Zahur 1959 Eugenia uniflora exn Zahur 1959 Kunzea ambigua (Sm.) Hochr. cs * /BG-K Leptospermum laevigatum (Gaertn.) F. Mue1!. + cs * /BG-HEID Leptospermum sp. exn Zahur 1959 Lophomyrtus obcordata (Raoul) Burret + cs * /BG-U (= Myrtus obcordata) exn Zahur 1959 Melaleuca acuminata F. Muell. cs * /BG-HEID Metrosideros polymorpha exn Zahur 1959

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Family / Species SV Herb. LM EM Fig. References/Origin of material

(MyrtK:eae continued) Metrosideros rugosa exn Zahur 1959 Metrosideros scandens exn Zahur 1959 Myrceugenia luma I.M. Johnst. cs * /BG-MJG Myrtus bullata exn Zahur 1959 Pimenta racemosa (Mill.) J.W. Moore cs */BG-BONN Psidium cattleyanum exn Zahur 1959 Rhodamnia cinerea Jack. + cs * / Leila Forest Res. (Sabah) Syncarpia sp. exn Zahur 1959 Syzygium sp. exn Zahur 1959 Tristania conferta R. Br. + cs .. /BG-L Myristicaceae Compsoneura sprucei Warb. MO,CR nc # Behnke 1991 Horsfieldia glabra (Blume) Warb. + ne # Behnke 1991 Horsfieldia globuIaria Warb. + ne Behnke 1991 Horsfieldia iryaghedhi (Gaertn.) Warb. ne Behnke 1991 Horsfieldia sp. + ne 1,2 Behnke 1991 Horsfieldia sylvestris (Houtt.) Warb. + ne Behnke 1991 Iryanthera elliptica Ducke USM,G nc Behnke 1991 Knema glauca (Blume) Warb. + nc # Behnke 1991 Knema latericia Elmer subsp. ridleyi (Gandager) de Wilde + nc Behnke 1991 Knema laurina Warb. + nc # Behnke 1991 Myristica fatua Houtt. + nc Behnke 1991 Myristiea fragrans Houtl + nc # Behnke 1991 Myristica lancifolia Piret subsp. montana (Roxb.) de Wilde + ne # Behnke 1991 Myristica maxima Warb. + ne Behnke 1991 Myristica muelleri Warb. BRl ne Behnke 1991 Myristica sp. exn Zahur 1959 Osteophloeum platyspermum Warb. USM,G ne Behnke 1991 Virola calophylla Warb. USM,G nc Behnke 1991 Virola duckei A.C. Smith USM,G ne Behnke 1991 Virola surinamensis (Roland) Warb. ne # Behnke 1991 Nothoragaceae Nothofagus obliqua (Mirb.) Oerst. + ba (sp) 32 Behnke 1989b Olacaceae Ochanostachys amentacea Mast. + es * /BG-BO Strombosia ceylanica Gardn. + es 44 .. /BG-BO Ximenia americana L. + ETH es .. / Edwards 2994 Ximenia caffra Sond. + es .. / R. Pretorius (Lowveld BG) Passifloraceae Adenia keramanthus Harms + es Behnke & Barthlott 1983 Adeniasp. + es .. /BG-HEID Passiflora coerulea sph/exn # Salmon 1946; Kollmann 1960a, b; es # Oberhlluser & Kollmann 1977 Passiflora edulis Sims. + cs # .. /BG-HEID Passiflora laurifolia L. + cs .. /BG-L Smeathmannia pubescens Soland ex R. Br. + es 23 .. /BG-BR Pandaceae Galearia celebica Koord. + rd .. /BG-BO Galearia filiform is Boer!. + rd .. /BG-BO Proteaceae Aulax pinifolia Berg. ro .. /BG-BONN

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Family / Species SV Herb. LM EM Fig. References/Origin of material

(Proteoceae continued) Banksia baxteri R. Br. ro 36 */BG-K Dryandra formosa R. Br. ro */BG-K Grevillea robusta exn Zahur 1959 Isopogon tridens F. Muell. ro */BG-BONN Knightia excelsa R. Br. ro * /BG-E Leucadendron saxatile Salter cs(st) * /BG-HEID Leucadendron tortum R. Br. cs(st) 38 * /BG-HEID Leucospermum pluridens Rourke cs(st) * /BG-HEID Lomatia ferruginea R. Br. ro * /BG-E Lomatia ilicifolia R. Br. ro 37 * /BG-HEID Macadamia temifolia F. Muell. + exn Zahur 1959; ro * /BG-HEID Protea neriifolia R. Br. cs(st) .. /BG-HEID Protea punctata Meissn. cs(st) 39 .. /BG-HEID Serruria florida Knight + cs .. /BG-HEID Stenocarpus salignus R. Br. + ro 35 "/BG-HEID Xylomelum pyriforme Knight ro .. /NSW, Australia (Behnke) Ranunculaceae Clematis bonstedtii + cs .. /BG-HEID Clematopsis stanleyi Hutchins. + cs .. /BG-U Rosaceae Dryas suendermannii Siinderm. + rd .. /BG-HEID Rhodotypus scandeus (Thunb.) Mak. + rd .. /BG-HEID Rubus australis exn Zahur 1959 Rubus phoenicolasius Maxim. + cs .. /BG-HEID Rubus sp. sli Lecomte 1889; Engard 1944 exn # Esau 1947; Zahur 1959 Salicaceae Populus deltoides cs # Deshpande & Evert 1970 Populus sp. sph Crafts 1939 Salix caprea L. cs # Mishra & Spanner 1969 Salix matsudana Koidz. + cs .. /BG-HEID Salix sachalinensis Fr. Schmidt cs # Nehls et al. 1978

Sterculiaceae Brachychiton acerifolius F. Muell. exn Zahur 1959; cs .. /BG-K Commersonia echinata exn Zahur 1959 Commersonia platyphylla exn Zahur 1959 Guazuma tomentosa exn Zahur 1959 Heritiera littoralis Ail. exn Zahur 1959; + cs .. /BG-HEID Melochia vitiensis exn Zahur 1959 Pterygota brasiliensis F. Allem. cs .. / BG-RB (K. Kubitzki ) Sterculia cf. comosa Wall. + cs 14 .. /BG-BO Sterculia urens sph Deshpande 1983 Sterculia tragacantba Lind!. + cs .. /BG-K Tarrietia argyrodendron Bentb. cs */BG-K Theobroma cacao exn Zahur 1959 Tiliaceae Berria javanica Burret + cs * /BG-BO Brownlowia elata Roxb. + cs .. /BG-BO Brownlowia peltata Benth. + cs * /BG-BO Colona scabra Burr. + cs 16 * /BG-BO Grewia oppositifolia Buch.-Ham. ex Roxb. cs .. /BG-MJG

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Family / Species SV Herb. LM EM Fig. References/Origin of material

(Tiliaceae continued) Tilia americana exn # Zahur 1959; exn Evert & Murmanis 1965; cs # Deshpande & Evert 1970 THia platyphyllos Scop. + cs */BG-HEID Tilia silvestris rxk # Salmon 1946 THia sp. sph Lecomte 1889. Crafts 1939 Turneraceae Turnera ulmifolia L. + cs 27 * / BG-BONN. -BR Tetracentraceae Tetracentron sinense Oliv. rc 30 Behnke 1989b Ulmaceae Aphanantbe aspera Planch. in DC. cs(gl) Behnke 1989b Chaetacme aristata Planch. + cs(gl) Behnke 1989b Pteroceltis tatarinowii Maxim. cs(gl) 20 Behnke 1989b Trema amboiensis exn Zahur 1959 Trema guinensis Priemer cs(gl) Behnke 1989b Trema micrantha Blume + cs(gl) Behnke 1989b Trema orientaIis exn Zahur 1959 Tremasp. exn Zahur 1959 Ulmus fulva Michx. + cs(gl) Behnke 1989b Urticaceae Laportea moroides Wedd. cs # Behnke 1981a Urtica sp' dis/urs # Fischer 1886; Salmon 1946 Violaceae Anchietia parvifolia H. Hallier + cs * /BG-U Hybanthus communis Taub. + cs * /BG-BR Hymenantbera dentata R. Br. ex DC. + cs 28 */BG-BONN Melicytus grandiflorus exn Zahur 1959 Melicytus ramiflorus J. R. & G. Forst. cs 29 * /BG-MJG Melicytus sp. sph Crafts 1939 Rinorea lanceolata (Wall.) O. Kuntze + cs * /BG-BO Rinorea longicuspis Eng!. + cs * /BG-U Viola canina L. cs * /BG-HEID Viola hederacea Labil!. + rc * /BG-HEID Winteraceae Bubbia pauciflora (E.G. Baker) Dandy ndp Esau & Cheadle 1984 Bubbia cf. queensIandica NSW cs(st) * / P. Hind 80204 Bubbia semecarpoides ndp Esau & Cheadle 1984 (F. Muell.) B.L. Burtt BRI cs(st) 9 * / R. Tracey (Australia) Drimys lanceolata (poir.) Bail!. + cs(st) Behnke & Kiritsis 1983; ndp Esau & Cheadle 1984 Drimys piperita Hook. + cs(st) * / Kinabalu National Park (Sabah) Drimys winteri l.R. et G. Forst. + cs(st) # Behnke & Kiri tsis 1983; ndp Esau & Cheadle 1984 Exospermum stipitatum (Baill.) Van Tiegh. ndp Esau & Cheadle 1984 Pseudowintera axillaris cs(st) # Behnke & Kiritsis 1983; (J.R.&G. Forst) Dandy ndp Esau & Cheadle 1984 Pseudowintera colorata (Raoul) Dandy + cs(st) Behnke & Kiritsis 1983 Tasmannia insipida R.Br. ex DC. cs(st) # Behnke & Kiritsis 1983 Zygogynum baillonii Van Tiegh. ndp Esau & Cheadle 1984 Zygogynurn bicolor Van Tiegh. ndp Esau & Cheadle 1984 Zygogynum vinkii Sampson ndp Esau & Cheadle 1984

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Fig. 47. Distribution of nondispersive protein bodies among the orders and superorders in Dahlgren's (1989) system of the dicotyledons (cytoplasmic origin = hatched; nuclear origin = dotted). The amount of shading corresponds to the position and sizes of the respective families (as indicated in Dahlgren's figure 2).

Taxonomic significance The accumulated LM and EM data provide the foundation for a statement on the taxon• On the basis of his light microscopy omic distribution of nondispersive protein studies and the then known distribution of bodies which in Dahlgren's (1989) system nondispersive protein bodies (extruded nu• are confined to nine of the 25 superorders clei) Zahur (1959) makes the general state• recognised (Fig. 47). ment that their presence is largely restricted The most distinct shapes of nondispersive to more-primitive families. Zahur (1959) em• protein bodies are also the taxonomically phasises their occurrence in the closely relat• most isolated: the spindle-shaped bodies in ed Tiliaceae, Malvaceae, Sterculiaceae, Bom• the Fabaceae and the nuclear crystals in the bacaceae, Euphorbiaceae, and comments Boraginaceae. The restriction of the spindle• upon their presence in the Urticaceae as shaped bodies to the Fabaceae (or subfamily another indication that this family may be Faboideae) has been undisputed since Bacca• placed in vicinity to the former group. rini (1892) (see also Staritz 1893; Mrazek Since then ultrastructural studies extended 1910; Behnke & Pop 1981). Within the Ru• our knowledge of their distribution consider• tanae no other family is characterised by ably by adding new families to the list and by these or other forms of nondispersive protein almost tripling the number of spectes found bodies. The Boraginaceae (incl. Cordiaceae to contain nondispersive protein bodies. and Ehretiaceae) are the only taxon within From the 41 families listed in Table 1 Solananae to contain nondispersive protein nineteen represent new records and are the bodies and one of the only two families with• result of the present author's phloem inves• in all of the dicotyledons (the other being the tigations that cover the entire range of the Myristicaceae) to have nuclear nondispersive dicotyledons. protein bodies in their sieve elements.

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The MalvanaelViolanae represent the to mention relationships between families of taxonomically most homogeneous super• the Rosanae and the Fabaceae with its spin• orders with regard to the presence of non• dle-shaped bodies, the latter being sometimes dispersive protein bodies. The compound• placed in vicinity to the Rosanae, within its spherical bodies found in Sterculiaceae, Tilia• own order (Fabales: Cronquist 1981) or ceae, Bombacaceae, Malvaceae of the Mal• superorder (Fabanae: Takhtajan 1987). Also, vales, in Ulmaceae, Moraceae, Cecropiaceae, Santalales (with its positive family Olacaceae, Urticaceae of the Urticales, in Euphorbiaceae, Fig. 44) are filed by Takhtajan (1987) in Pandaceae, Dichapetalaceae of the Euphor• Rosanaean alliance, within his Celastranae biales, in Flacourtiaceae, Passifloraceae, Vio• (Goupia, Celastraceae, has also compound• laceae, Turneraceae of the Violales and in spherical bodies: Fig. 45). Salicaceae (Salicales) may certainly be re• The five families of the Magnolianae that garded as a characteristic feature of the entire contain nondispersive protein bodies repre• group. Nondispersive protein bodies have sent the entire range of forms: compound• not been identified thus far in other families spherical in the Monimiaceae and Wintera• of the five orders mentioned, leaving only a ceae, rod-cluster and rod-shaped in Monimia• few families not yet investigated. It is like• ceae and Hirnantandraceae, globular/ovoidal wise significant that none of the investigated in Austrobaileyaceae, and bodies of nuclear taxa of the Thymelaeales and Rhamnales origin in the Myristicaceae. Thus, the great (from Malvanae) and of the Tamaricales, number of forms of nondispersive protein Cucurbitales, Capparales, Tropaeolales and bodies found in the Magnolianae conforms to Salvadorales (from Violanae) contained non• the diversity of other characters in this super• dispersive protein bodies. However, a sepa• order that suggest a comparably basic posi• ration between positive and negative orders tion of this taxon. (with respect to nondispersive protein bod• Eventually, it should be mentioned that ies) seems unrealistic: practically all modern except for the Boraginaceae all families that systems align almost the same taxa within contain nondispersive protein bodies are these superorders, except for Thymelaeaceae woody (or basically woody) - a correlation (placed within the Myrtales by Cronquist that might add to the general syndrome of the 1981) and Rhamnales (in Rosanaean alliance primitive taxa. by Takhtajan 1987). A second centre of nondispersive protein Acknowledgements bodies is the Rosanae. This superorder, how• The ultrastructural study of the different ever, is rather heterogeneous, both with species was made possible through the gen• respect to the presence and to the form of erous help of my colleagues who collected nondispersive protein bodies. Compound• and sent fresh or fixed samples: Inge Dorr spherical bodies were found in some Faga• (Kiel, FRG), T.B.G. Egziabher ( Addis ceae, Betulaceae, Casuarinaceae, Cunonia• Abeba, Ethiopia), U. Eifert (Austin, Texas), ceae (Fig. 40), other forms in Trochoden• P. Goldblatt (St. Louis, Missouri), P. Hind draceae, Nothofagaceae, Fagus, Rosaceae, (Sydney, Australia), A. Irvine (Atherton, Aus• Malaceae, and Amygdalaceae. Nondispersive tralia), Janice Jacobs (Sydney, Australia), K. protein bodies could not be detected in mem• Kubitzki (Hamburg, FRG), G.Merz, H. Tehe bers of the Hamamelidales, Saxifragales, & A. Assi (Abidjan, Ivory Coast), W. Mora• Buxales, Droserales and a few other small wetz (Wien, Austria), B. Nelson (Manaus, orders of the Rosanae, but are present in Brazil), G.S. Paliwal (New Delhi, India), Myrtanae and Proteanae, two closely related W.R. Philipson (Christchurch, New Zea• superorders. Myrtaceae is the only family of land), R. Pretorius (Nelspruit, RSA), Rein• the Myrtanae that contains nondispersive pro• hild Tracey-Schreiner (Indooropilly, Aus• tein bodies (of compound-spherical form), tralia), K.R. Woolliams (Haleiwa, Hawaii). while in the Proteanae different forms are Other samples were collected by the author found in both its families, the Proteaceae and in botanical gardens, for which the directors Elaeagnaceae. Certainly, this is also the place gave permission. Marianne von der Decken,

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Doris Laupp and Liliana Pop (Heidelberg, & P.R. Crane), VoU: 105-128. Sys• FRG) gave invaluable technical help during tematics Ass. Spec. Vol. 40A, Clarendon the processing of the material from the fixa• Press, Oxford. tion to the micrograph. The Deutsche For• Behnke, H.-D. 1991. Sieve-element charac• schungsgemeinschaft gave travel and re• ters of Myristicaceae: nuclear crystals, search support for these investigations. My S- and P-type plastids, nacreous walls. sincere gratitude is extended to all the afore• Nord. J. Bot. 11 (in press). mentioned persons and institutions. Behnke, H.-D. & W. Barthlott. 1983. New evidence from the ultrastructural and mi• References cromorphological fields in angiosperm Arsanto, J.-P. 1982. Observations on P-pro• classification. Nord. J. Bot. 3: 43-66. tein in dicotyledons. Substructural and de• Behnke, H.-D. & U. Kiritsis. 1983. Ultra• velopmental features. Amer. J. Bot. 69: structure and differentiation of sieve ele• 1200-1212. ments in primitive angiosperms. I. Win• Baccarini, P. 1892. Intorno ad una particola• teraceae. Protoplasma 118: 148-156. rita dei vasi cribosi nelle Papilionacee. Behnke, H.-D. & L. Pop. 1981. Sieve-ele• Malpighia 6: 54-57. ment plastids and crystalline P(hloem)• Behnke, H.-D. 1972. Sieve-tube plastids in protein in Leguminosae: micromorpho• relation to angiosperm systematics - an logical characters as an aid to the circum• attempt towards a classification by ultra• scription of the family and subfamilies. In: structural analysis. Bot. Rev. 38: 155- Advances in legume systematics (eds. 197. R.M. Polhill & P.H. Raven): 707-715. Behnke, H.-D. 1981a. Sieve-element char• Academic Press, London acters. Nord. J. Bot. 1: 381-400. Bouck, G.B. & J. Cronshaw. 1965. The Behnke, H.-D. 1981b. Swartzia: Phloem ul• fine structure of differentiating sieve tube trastructure supporting its inclusion into elements. J. Cell BioI. 25: 79-95. Leguminosae-Papilionoideae. Iselya 2: Crafts, A.S. 1939. The protoplasmic proper• 13-16. ties of sieve tubes. Protoplasma 33: 389- Behnke, H.-D. 1986a. Sieve element charac• 398. ters and the systematic position of Austro• Cronquist, A. 1981. An integrated system of baileya (Austrobaileyaceae) - with com• classification of flowering plants. Colum• ments to the distinction and definition of bia Univ. Press, New York. sieve cells and sieve-tube members. PI. Cronshaw, J. 1975. P-proteins. In: Phloem Syst. Evol. 152: 101-12l. transport (eds. S. Aronoff et at.): 79-115. Behnke, H.-D. 1986b. Ultrastructure and Plenum Press, New York differentiation of sieve elements in primi• Cronshaw, J. & D.D. Sabnis. 1990. Phloem tive angiosperms. II. Primary phloem proteins. In: Sieve elements. Comparative sieve elements of Austrobaileya rnaculata. structure, induction and development Phytomorphology 36: 185-195. (eds. H.-D. Behnke & R.D. Sjolund): Behnke, H.-D. 1988. Sieve-element plastids, 257-283. Springer, Berlin, Heidelberg, phloem protein and evolution of flowering New York. plants. III. Magnoliidae. Taxon 37: 699- Dahlgren, G. 1989. The last Dahlgrenogram. 732. System of classification of the dicotyle• Behnke, H. -D. 1989a. Structure of the phlo• dons. In: The Davis and Hedge Fest• em. In: Transport of photoassimilates schrift (ed. K. Tan): 249-260. Edinburgh (eds. D.A. Baker & J.A. Milburn): 79- University Press, Edinburgh. 137. Longman, Harlow. Deshpande, B.P. 1983. On the protein inclu• Behnke, H.-D. 1989b. Sieve-element plas• sions in sieve elements of Sterculia urens. tids, phloem-proteins and the evolution of Ann. Bot. 52: 429-432. flowering plants. IV. Hamamelidae. In: Deshpande, B.P. & R.F. Evert. 1970. A re• Systematics, evolution and fossil history evaluation of extruded nucleoli in sieve of the Hamamelidae (eds. S. Blackmore elements. J. Ultrastr. Res. 33: 483-494.

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Engard, C.J. 1944. Organogenesis in Rubus. Fischer, A. 1886. Neue Beitrage zur Kennt• Univ. Hawaii Res. Publ. 21: 231 pp. nis der Siebrohren. Ber. Verh. Kg!. Sachs. [cited after Esau 1947]. Ges. Wiss. Math.-Phys. Kl. 37: 291- Esau, K. 1947. A study of some sieve-tube 336. inclusions. Amer. J. Bot. 34: 224-233. Fisher, D.B. 1975. Structure of functional Esau, K. 1978a. The protein inclusions in soybean sieve elements. Plant Physiol. sieve elements of cotton (Gossypium 56: 555-569. hirsutum L.). J. Ultrastr. Res. 63: 224- Fisher, D.D., J. Thorsch & K. Esau. 1989. 235. Inclusions in nuclei and plastids of Bora• Esau, K. 1978b. Developmental features of ginaceae and their possible taxonomic sig• the primary phloem in Phaseolus vulgaris nificance. Can. J. Bot. 67: 3608-3617. L. Ann. Bot. 42: 1-13. Gerola, F.M., G. Lombardo & A. Catara. Esau, K. & V.I. Cheadle. 1984. Anatomy of 1969. Histological localization of citrus the secondary phloem in Winteraceae. infectious variegation virus (CVV) in IAWA Bull. n.s. 5: 13-43. Phaseolus vulgaris. Protoplasma 67: 319- Esau, K. & J. Cronshaw. 1967. Tubular 326. components in cells of healthy and tobac• Ilker, R. & H.B. Currier. 1975. Histochem• co mosaic virus-infected Nicotiana. Virol• ical studies of an inclusion body and ogy 33: 26-35. P-protein in phloem of Xylosma conges• Esau, K. & A.C. Magyarosy. 1979a. A tum. Protoplasrna 85: 127-132. crystalline inclusion in sieve element Kamovsky, M.J. 1965. A formaldehyde• nuclei of Amsinckia. I. The inclusion in glutaraldehyde fixation of high osmolality differentiating cells. J. Cell Sci. 38: 1- for use in electron microscopy. J. Cell 10. BioI. 27: 137A-138A. Esau, K. & A.C. Magyarosy. 1979b. A Kollmann, R. 1960a. Untersuchungen tiber crystalline inclusion in sieve element nu• das Protoplasma der Siebrohren von Pas• clei of Amsinckia. II. The inclusion in siflora coerulea. I. Mitteilung: Lichtopti• maturing cells. J. Cell Sci. 38: 11-22. sche Untersuchungen. Planta 54: 611- Esau, K. & J. Thorsch. 1982. Nuclear crys• 640. talloids in sieve elements of species of Kollmann, R. 1960b. Untersuchungen tiber Echium (Boraginaceae). J. Cell Sci. 54: das Protoplasma der Siebrohren von Pas• 149-160. siflora coerulea. II. Mitteilung: Elektro• Evert, R.F. 1984. Comparative structure of nenoptische Untersuchungen. Planta 55: phloem. In: Contemporary problems in 67-107. plant anatomy (eds. R.A. White & W.C. Lafleche, D. 1966. Ultrastructure et cytochi• Dickison): 145-234. Academic Press, mie des inclusions flagellees des cellules New York. criblees de Phaseolus vulgaris. J. Micro• Evert, R.F. 1990. Dicotyledons. In: Sieve scopie 5: 493-510. elements. Comparative structure, induc• Lawton, D.M. 1978a. Ultrastructural com• tion and development (eds. H.-D. Behnke parison of the tailed and tailless P-protein & R.D. Sjolund): 103-137. Springer, Ber• crystals respectively of runner bean (Pha• lin, Heidelberg, New York. seolus multiflorus) and garden pea (Pisum Evert, R.F. & B.P. Deshpande. 1970. Nu• sativum) with tilting stage electron micro• clear P-protein in sieve elements of Tilia scopy. Protoplasma 97: 1-11. americana. J. Cell BioI. 44: 462-466. Lawton, D.M. 1978b. P-protein crystals do Evert, R.F. & S.E. Eichhorn. 1974. Sieve• not disperse in uninjured sieve elements in element ultrastructure in Platycerium bi• roots of runner bean (Phaseolus multiflo• furcatum and some other polypodiaceous rus) fixed with glutaraldehyde. Ann. Bot. ferns: The nucleus. Planta 119: 301-318. 42: 353-361. Evert, R.F. & L. Murmanis. 1965. Ultra• Lecomte, H. 1889. Contribution a l'etude du structure of the secondary phloem of Tilia liber des angiospermes. Ann. Sci. nat., americana. Amer. J. Bot. 52: 95-106. Ser. 7, Bot. 10: 193-324.

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Mishra, U. & D.C. Spanner. 1970. The fine Staritz, C. 1893. Uber einen neuen Inhalts• structure of the sieve tubes of Salix caprea korper der Siebrohren einiger Legumi• (L.) and its relation to the electroosmotic nosen. In: Festschrift zur 250jahrigen theory. Planta 90: 43-56. Jubelfeier des Gymnasiums St. Maria Mrazek, A. 1910. Uber geformte eiweiB• Magdalena Breslau: 181-199. Breslau. artige Inhaltskorper bei den Leguminosen. Strasburger, E. 1891. Uber den Bau und Osterr. Bot. Z. 60: 198-201 + 218-230 die Verrichtungen der Leitungsbahnen in + 312-321. den Pflanzen. Histologische Beitrage 3. Nehls, R., G. Schaffner & R. Kollmann. Fischer, Jena. 1978. Feinstruktur des Protein-Einschlus• Takhtajan, A. 1987. Systema Magnoliophy• ses in den Siebelementen von Salix sacha• torum. Nauka, Leningrad [in Russian]. linensis Fr. Schmidt. Z. Pflanzenphysiol. Thorsch, J. & K. Esau. 1983. Nuclear crys• 87: 113-127. talloids in sieve elements of Boraginaceae: Oberhauser, R. & R. Kollmann. 1977. Cyto• a protein digestion study. J. Cell Sci. 64: chemische Charakterisierung des soge• 37-47. nannten Freien Nucleolus als Protein• Thorsch, 1. & K. Esau. 1988. Ultrastructur• korper in den Siebelementen von Passi• al aspects of primary phloem. Sieve ele• flora coerulea. Z. Pflanzenphysiol. 84: ments in Poinsettia (Euphorbia pulcher• 61-75. rima, Euphorbiaceae). IAWA Bull. n. s. Palevitz, B.A. & E.H. Newcomb. 1971. 9: 363-373. The ultrastructure and development of tu• Wark, M.C. & T.C. Chambers. 1965. Fine bular and crystalline P-protein in the sieve structure of the phloem of Pisum sativum. elements of certain papilionaceous leg• I. The sieve element ontogeny. Aust. J. umes. Protoplasma 72: 399-426. Bot. 13: 171-183. Parameswaran, N. 1983. Crystalline protein Wergin, W.P. & E.H. Newcomb. 1970. bodies in the sieve element of Castanop• Formation and dispersal of crystalline sis borneensis. Beitr. BioI. Pflanzen 58: P-protein in sieve elements of soybean 413-419. (Glyxine max L.). Protoplasma 71: 365- Salmon, J. 1946. Differenciation des tubes 388. cribIes chez les Angiospermes: Recher• Zahur, M.S. 1959. Comparative study of ches cytologiques. Rev. Cytol. et Cyto• secondary phloem of 423 species of physiol. veget. 9: 55-168. woody dicotyledons belonging to 85 Schulz, A. 1986. Wound phloem in transi• families. Corn. Univ. Agric. Exp. Stat. tion to bundle phloem in primary roots of Mem. 358: 160 pp. Pisum sativum L. II. The plasmatic con• Zee, S.-Y. 1968. Ontogeny of cambium and tact between wound-sieve tubes and regu• phloem in the epicotyl of Pisum sativum. lar phloem. Protoplasma 130: 27-40. Aust. 1. Bot. 16: 419-426. Schulz, A. & H.-D. Behnke. 1987. Feinbau und Differenzierung des Phloems von Buchen, Fichten und Tannen aus Wald• schadensgebieten. Kernforschungszen• trum Karlsruhe, PEF 16: 95 pp.

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