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Nondispersive Protein Bodies in Sieve Elements: a Survey and Review of Their Origin, Distribution and Taxonomic Significance

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Nondispersive Protein Bodies in Sieve Elements: a Survey and Review of Their Origin, Distribution and Taxonomic Significance 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 Downloaded from Brill.com10/07/2021 05:44:19AM via free access 144 IAWA Bulletin n.s., Vol. 12 (2),1991 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. Downloaded from Brill.com10/07/2021 05:44:19AM via free access Behnke - Nondispersive protein bodies in sieve elements 145 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
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