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Orbicules in angiosperms: morphology, function, distribution, and relation with tapetum types.

II. Introduction

Orbicules, or Ubisch bodies, were discovered more than a century ago by Rosanoff(1865). Up to now these minute structures, covering the inner surface of most secretory tapeta, remained enigmatic and therefore highly attractive to botanists concerned with anther structure, pollen development, and sporopollenin synthesis.

In a recent overview Pacini and Franchi (1993) listed 33 species from 22 angiosperm families with secretory tapetum and orbicules (references from 1971 to 1993). From the early days of orbicule research two other lists of taxa with presence/absence of orbicules were published. Von Ubisch (1927) investigated 20 taxa from 14 families and Kosmath independently reported in the same year on 69 taxa from 35 families.

The lack of any recent summary about the distribution of orbicules throughout the angiosperms encouraged us to review the literature from the very first report (Rosanoff, 1865) until December 1996. Papers published since 1970 were traced by a literature search in BIOSIS on the keyword "orbicule?". Earlier articles and additional papers (e.g., sometimes the term "Ubisch bodies" was used instead of "orbicules") were found mainly by unraveling reference lists. The extensive bibliography of stamen morphology and anatomy (Lynch & Gregory, 1996) proved to be a useful source of additional references. All papers under "Tapetum" in the subject index were checked for information about orbicules.

We restricted this review to the angiosperms; for information on gymnosperms (e.g., Ueno, 1960a, 1960b; Yamazaki & Takeoka, 1962; Audran, 1981; Rowley & Walles, 1987) and lower plants (ferns: e.g., Lugardon, 1981; mosses: e.g., Zajac, 1995) we refer to specialized literature.

The aim of the present paper is threefold: (1) to give a concise state of knowledge about tapetum and orbicules, (2) to enumerate the taxa where orbicules were reported to be present or certified absent, and (3) to visualize the systematic distribution of orbicules throughout the angiosperms by plotting the information on a dahlgrenogram. We also document the oft-suggested correlation between the presence of orbicules and tapetum types by comparing this dahlgrenogram with the distribution of tapetum types.

III. Tapetum

The anther tapetum is a highly specialized tissue. It is the innermost cell layer of the anther wall in all Spermatophyta and it plays a crucial role in the development of both microspores and orbicules. We only mention some basic points here that are necessary for a better understanding of what follows on orbicules.

A. TYPES

Since Goebel (1901) two main tapetal types are recognized: the secretory (a.k.a. parietal, glandular, or cellular non-syncytial) tapetum and the amoeboid (a.k.a. syncytial invasive or periplasmodial) tapetum. In secretory tapeta the cells remain in situ until their degeneration, while in amoeboid tapeta the tapetal protoplasts move into the loculus, forming a periplasmodium that is in direct contact with the developing microspores. The distinction between these two main types has become less evident (e.g., Rowley et al., 1992). Many subtypes have been recognized (Pacini et al., 1985) and transitional types have been described (for references, see Hesse & Hess, 1993). Secretory tapeta are believed to be the most primitive type from which all other types, tending toward more efficient nutrition, are derived (Sporne, 1973; Pacini et al., 1985).

B. DEVELOPMENT

The tapetum is essentially of parietal origin, irrespective of the type of anther wall formation (Davis, 1966). Periasamy and Swamy (1966), however, suggested the dual origin of tapetum in angiosperms: from the parietal layer in the outer regions of the locules and from the connective tissue toward the inner half of the locules. Other studies suggest that tapetum could arise from the sporogenous tissue as well (Bhandari, 1971).

Tapetal cells pass through a number of cycles of secretory activity and redifferentiation, which is rather unusual for plant cells (Rowley, 1993). The behaviour and ultrastructure of tapetal cells through their lifetime is quite variable for different species and of course determined by the type of tapetum. References of ontogenetic studies of tapetum can be found in, e.g., Bhandari, 1984, and Suarez-Cervera & Seoane-Camba, 1986.

C. FUNCTIONS

Tapetal cells have an essential nutritive role for the developing microspores. Several other functions were suggested by Pacini et al. (1985), such as the production and release of callase to dissolve the callosic envelope around the tetrads, the production of other sporophytic proteins, the formation of sporopollenin precursors, the formation of tryphine, pollenkitt, and viscin threads. Secretory tapeta in addition produce orbicules and the locular fluid (Pacini et al., 1985).

D. GENERAL DISTRIBUTION IN ANGIOSPERMS

Secretory tapeta are characteristic of 175 (+ 15 presumably) angiosperm families, 88% of which are dicots. Amoeboid tapeta have been found in 32 angiosperm families, of which 14 are dicots. Both types of tapetum occur together in 12 families. Surprisingly, the tapetum type of ca. 177 families is still unknown (Pacini et al., 1985, after Davis, 1966, with modifications). According to Davis (1966), there are 21 families where both tapetum types occur together. A current review of tapetum information in the monocotyledons, is forthcoming from Furness and Rudall (this issue).

The distribution of the two main tapetum types in angiosperms was shown on dahlgrenograms: for dicots by Dahlgren (1991), and for monocots by Dahlgren and Clifford (1982) and Dahlgren et al. (1985).

IV. Orbicules

A. DISCOVERY AND EARLY DAYS OF ORBICULE RESEARCH

The historical literature, from the first report in 1865 by Rosanoff up to the 1920s, concentrates mainly on anatomy and morphology of the anther, and often more specifically the tapetum.

Rosanoff (1865: 447) observed a granular membrane completely enveloping the mature massulae in the Mimosaceae. Between this membrane and the microspores is an empty space with more granules, or "Kornchen und Tropfchen" (grains and droplets), as Rosanoff called them. Rosanoff also found out that these granules are resistant to concentrated sulfuric acid and thus give the same reaction as cuticula.

In his carefully illustrated study on anther anatomy of many species from different plant families, Chatin (1870) distinguished three layers in the anther wall, of which the innermost may reduce to granules. Chatin's figures indicate that these granules most likely correspond to orbicules.

In the 1920s, several botanists studied the anther tapetum. Their attention was drawn to the minute particles between tapetum and pollen grains. Mascre (1922) reported for Boraginaceae that tapetal cells are cutinised towards the locule. It seems that the cutinised layer by Mascre corresponds to orbicules arranged between the tapetal cells and the pollen grains. Schnarf (1923) mentioned the presence of "kugelige Verdickungen" (spherical thickenings) on the adaxial side of the secretory tapetum cells in Lilium martagon. These structures remained intact even after total destruction of the tapetal cells.

The first paper illustrated with light microscopic pictures was written by Krjatchenko (1925). He studied the activity of mitochondria and described the development of granules on the inner surface of the tapetal cells in Lilium croceum. Krjatchenko suggested that they develop from lipid droplets secreted by the tapetal cells, and that the droplets possibly originate from mitochondria.

Von Ubisch (1927) and Kosmath (1927) independently published a list of taxa with and without orbicules; the structures were called "Plattchen" (plates) by von Ubisch (1927) and "kutikulaahnliche Tapetumzellmembran" (cuticula like tapetal cell membrane) by Kosmath (1927). Both scientists did experiments with several chemicals and stains to elucidate the nature of the structures. Since these particles showed the same reaction as the pollen exine and because they developed synchronously with the pollen wall, von Ubisch concluded that they must be homologous with the exine. Both authors stressed that these particles are restricted to and a general feature of secretory tapeta. Von Ubisch observed a cavity in the center of the particles and Kosmath reported interspecific size differences.

B. DEFINITION AND TERMINOLOGY

Contrary to what the literature says, Kosmath (1927) did not coin the term "Ubisch granules" because of the contribution of von Ubisch. As far as we could trace, it was Rowley (1962) who introduced the term "Ubisch body." The term "orbicules," proposed by Erdtman and coworkers (1961: 9), was defined as "small granules spread over the exine surface in certain gymnosperms." In Japanese literature they are often called "con-peito-grains," referring to star-shaped cookies made for special occasions (J. Rowley, pers. comm.). In his first papers on the topic, Heslop-Harrison (1968a, 1968b) used the term "plaques." Later, in 1971, he rejected "Ubisch bodies" in favor of "orbicules" since they were not discovered by von Ubisch.

Another, carefully formulated early definition was presented by Rowley (1963). He defined Ubisch bodies as extra-exinous objects having a role in exine establishment. This definition is consistent with the previously published ideas of Rowley et al. (1959), Chambers and Godwin (1961), and Heslop-Harrison (1962). Form and perhaps also origin of orbicules was reported to be variable.

Skvarla and Larson (1966: 1123) referred in their definition to the parallelisms with the exine: "Ubisch bodies are small bodies of sporopollenin resembling the form of pollen exines of the species in which they occur."

Other authors distinguished between Ubisch bodies and orbicules (Madjd & Roland-Heydacker, 1978; Abadie & Hideux, 1979). According to them, Ubisch bodies are hollow and have a surface structure comparable to the respective pollen exine, while orbicules are massive spherical structures that can deform; both do consist of sporopollenin. In the present paper the two terms are considered synonyms.

C. MORPHOLOGY AND COMPOSITION

Orbicules are most variable in both shape and size. Size is ranging from 0.14 [[micro]meter] in Rondeletia odorata (Rubiaceae; Huysmans et al., 1997) and 0.15 [[micro]meter] in Saxifraga cymbalaria var. huetiana (Saxifragaceae; Abadie & Hideux, 1979) to 15 [[micro]meter] in Quararibea (Bombacaceae; Nilsson & Robyns, 1974). Generally they are less than 5 [[micro]meter] in diameter.

Frequently, remarkable similarities between the surface structure of orbicules and the respective pollen exine have been reported (grasses: Rowley et al., 1959; Quararibea: Nilsson & Robyns, 1974; Sorghum: Christensen et al., 1972; Triticum: El-Ghazaly & Jensen, 1986; Lilium: Clement & Audran, 1993a; Platanus acerifolia: Suarez-Cervera et al., 1995), although this is not always true (El-Ghazaly & Nilsson, 1991; Huysmans et al., 1997).

To our knowledge, orbicules have almost never been found in taxa with an amoeboid tapetum, Gentiana acaulis being the only exception (Lombardo & Carraro, 1976b). Most angiosperms with a secretory tapetum produce orbicules, mainly on the inner tangential, and to a lesser extent on the radial walls of tapetal cells (e.g., El-Ghazaly & Jensen, 1986; Huysmans et al., in prep.). Sometimes, however, orbicules are found all around the tapetal cell membranes (e.g., in Primula obconica: Stevens & Murray, 1981).

Orbicules are resistant to acetolysis and react similarly to the exine with different histochemical stains, thus providing ample evidence for sporopollenin composition of the orbicule wall. El-Ghazaly and Jensen (1987) found for both orbicule walls and pollen exines of Triticure aestivum an intense staining for acidic and neutral polysaccharides and for unsaturated lipids, while the structures stained moderately for proteins. Suarez-Cervera et al. (1995), working on Platanus acerifolia, showed that the central part of the orbicules stains positively for lipids, glycoproteins, and acidic and neutral polysaccharides during all stages of maturation. A detailed cytochemical investigation of Lilium orbicules was published by Clement and Audran (1993a, 1993b).

D. ORIGIN AND DEVELOPMENT

There have always been questions about tapetal cells being the site of origin for orbicules and about which organelles in the tapetal cells could give rise to pro-orbicules. A concise review of the origin of orbicules is provided by Bhandari (1984).

According to Krjatchenko (1925), in Lilium croceum "une substance graisseuse" (a granular substance) is formed at tetrad stage by the mitochondria of the tapetal cells and is excreted through the plasmalemma to form a dented locule surface. Heslop-Harrison (1962) adopted this idea in his paper on the origin of tapetal particles in Silene pendula and Cannabis sativa. Organelles that have the dimensions of mitochondria and show "occasionally sufficient evidence of cristae" were believed to be the site of origin for orbicules (Heslop-Harrison, 1962: 1069). This interpretation was reconsidered by Heslop-Harrison and Dickinson (1969) on the basis of evidence from other studies (Carniel, 1967; Rowley & Erdtman, 1967; Echlin & Godwin, 1968a). Rowley and Erdtman (1967), for instance, thought the word "mitochondria" in Krjatchenko (1925) should read as "lysosomes" to explain the source of orbicules.

Skvarla and Larson (1966) interpreted orbicules to represent sporopollenin deposition upon membranes aggregated at the tapetal surface. They believed that these membranes are derived from ruptured microspores since in Zea mays cytoplasmic organelles and cytomembranes are always suspended in the locular fluid. One year later, however, Camiel (1967: 500) gave evidence for an intracellular development of Ubisch bodies in Oxalis: "Contrary to the current opinion they are not located on the outside of the inner cell wall but on its inside." In 1971 Carniel stressed in his work on Eleocharis that only mature Ubisch bodies become free as a result of tapetal protoplast degeneration.

The endoplasmic reticulum of tapetal cells as site of origin for orbicules was first mentioned by Echlin and Godwin (1968a). This has been confirmed for Allium cepa (Risueno et al., 1969). Risueno et al. (1969) observed endoplasmic reticulum elements, dispersed through the cytoplasm from the nuclear membrane to areas in the vicinity of the plasmalemma, producing electron-dense bodies with characteristics similar to those of the central core of the sporopollenin granules.

Risueno et al. (1969) discussed the three hypotheses published at that time about the origin of orbicules. These hypotheses can be summarized as follows:

1. They are formed both in the cells of the tapetum and in the locule of the pollen sac (Rowley et al., 1959).

2. They originate solely in the tapetum through modification of certain cytoplasmic organelles (Heslop-Harrison, 1962).

3. They are formed exclusively in the locule without invoking tapetal cell regulation, from membrane complexes derived from abortive microspores (Skvarla & Larsson, 1966).

In our opinion, Risueno et al. (1969) did not distinguish consistently between the formation of the pollen exine and Ubisch bodies. They assumed Ubisch bodies to be a main source of sporopollenin precursors for the exine (as we discuss in greater detail in the next section).

Tapetal endoplasmic reticulum as site of origin for orbicules has since then also been proposed by Reznickova and Willemse (1980), Herich and Lux (1985) for Lilium, El-Ghazaly and Jensen (1986) for Triticum aestivum, Chen et al. (1988) for Anemarrhena asphodeloides, and el-Ghazaly and Nilsson (1991) for Catharanthus roseus.

The development of orbicules is studied mostly in the shadow of pollen ontogenetic investigations. In few papers on the subject, pro-orbicules were believed to appear between the tapetal plasmalemma and the degenerating walls of the tapetal cells (Homer & Lersten, 1971; Christensen et al., 1972; Steer, 1977). In Avena (Steer, 1977) and Sorghum (Christensen et al., 1972), lipid droplets appear on tapetal plasmalemma depressions after loss of the cell wall of the inner facing tapetal cell surfaces. No morphological evidence was found for the intracytoplasmic formation of pro-orbicules. The timing of pro-orbicule formation varies slightly between the different species: from early stages of meiosis II in Avena (Steer, 1977) to late tetrad stage in Sorghum (Christensen et al., 1972) to microspore release from the tetrads in Citrus (Homer & Lersten, 1971).

In most papers, however, pro-orbicule formation is considered to be intra-tapetal (e.g., Echlin & Godwin, 1968a; El-Ghazaly & Jensen, 1986). Suarez-Cervera et al. (1995) believed the so-called "grey bodies" in the tapetal cytoplasm to be the progenitors of the Ubisch bodies (references are given for different species). The next question, then, is how they pass the tapetal plasmalemma. In Triticum it is shown that a membrane is formed around the pro-orbicule as it approaches the plasmalemma. After fusion of these membranes, the pro-orbicules are released (El-Ghazaly & Jensen, 1986).

1. Determination of Sporopollenin Deposition on Pro-orbicules

Sporopollenin accumulation in higher plants essentially takes place simultaneously in the primexine of developing microspores and on the surface of the pro-orbicules (e.g., Christensen et al., 1972; El-Ghazaly & Jensen, 1986). Rowley and Skvarla (1974: 445) stated that "the specific form of the Ubisch body wall, which is identical with the pollen exine surface, is determined by a plasma membrane-glycocalyx."

In monocots the orbicular wall seems to develop on a specific reticulate pattern (= glycocalyx). For example, Rowley and Skvarla (1974) reported a plasma membrane glycocalyx on pro-orbicules of Phleum pratense, El-Ghazaly and Jensen (1985) in Triticum, and Reznickova and Willerase (1980) and Clement & Audran (1993a) in Lilium. The coat of the proorbicules, which appears to guide the deposition of sporopollenin, stains positively for polysaccharides and proteins, similar to the pollen wall (Rowley, 1976; Rowley & Dahl, 1982; E1Ghazaly & Jensen, 1987).

E. FUNCTION

Why should the (secretory) tapetum develop any sporopollenin wall at all and why should it form mainly on the inner tangential surface of the tapetal cells? Echlin (1971) and Bhandari (1984) reviewed the early literature on the different hypotheses that have been proposed to attribute a function to orbicules. We summarise these views here and report on additional findings in the past 20 years. The list of suggested possible functions of orbicules is long, and none of them is satisfactorily proved.

1. Orbicules as a Transport Mechanism for Sporopollenin

Orbicules represent a transport mechanism for sporopollenin between the tapetum and the developing microspores and thus take active part in sporoderm formation. The idea that orbjoules might contribute to the development of the exine was first raised by Maheshwari (1950). Protoplasmic strands were observed in Poa annua by Rowley (1962) extending from the tapetum to the spinules on the pollen exine. Banerjee and Barghoorn (1971) showed in some grasses that spinules of orbicules are in contact with those on the pollen exine through strands of sporopollenin, indicating a track for the possible transfer of substrate from the tapetal cells to the exine. In Triticum, microfilaments are observed occasionally connecting orbicule spinules with the microspore wall (El-Ghazaly & Jensen, 1986). Banerjee and Barghoorn (1971:127) found in some grasses, immediately prior to anther dehiscence, some depolymerisation of the mature sporopollenin, "possibly caused by secretion from the centrum of the Ubisch bodies." In the same study it is observed that a large number of new spinules are produced at pollen maturity, apparently by the orbicules. This would suggest an important role for orbicules in sporoderm formation in grasses.

This idea is shared by Risueno et al. (1969) for Allium cepa. They observed that orbicules become part of mature exines and thus actively take part in the formation and development of the pollen exine. In Soja some orbicules become nail-shaped and are found in the tectum perforations of the pollen grains (Madjd & Roland-Heydacker, 1978). The authors carefully suggested a possible participation of the orbicules in the construction of the pollen exine. Robertson (1984) mentioned that orbicules of Rhigozum trichotomum (Bignoniaceae) become intimately bound to the exine after being released into the thecal fluid. He added that the orbicules are stripped of the osmiophilic layers which appear to be incorporated into the sporoderm. Polowick and Sawhney (1993) indicated that in Lycopersicon esculentum (Solanaceae) the orbicule surface may also provide material for the exine. Abadie et al. (1981) mentioned contact between orbicules and exine in Turgenia latifolia and Hydrocotyle mexicana (Apiaceae). An additional argument to strenghten this hypothesis might be the observation that the exine initially develops on the side facing the tapetum, and thus facing the orbicules (Gorczynski, 1935).

A number of authors follow a hypothesis that is in contradiction to the former one namely, that there is no direct relationship between orbicules and exine development (Carniel, 1967; Rowley & Erdtman, 1967; Heslop-Harrison & Dickinson, 1969). A fact corroborating this idea is that sporopollenin synthesis associated with the tapetum begins before sporopollenin accumulation in the exine in Silene pendula, Lilium longiflorum, and Oxalis spp. Furthermore, orbicules are not universally present, not even in all taxa with secretory tapeta (see Table II) so they cannot have such a general function as exine construction.

2. Temporary Packaging of Sensitive Material for Transport through Locular Sap

This hypothesis was suggested by Rowley and Walles (1987) in their work on Pinus sylvestris. The locular fluid probably contains exocellular enzymes (see Herdt et al., 1978) against which the sporopollenin wall of the orbicules forms an effective barrier.

3. By-products of Tapetal Cell Metabolism

Some researchers hold that orbicules have no specific function; they are nothing more than a by-product of tapetal cell metabolism. Heslop-Harrison (1968b) stated that orbicules cannot be considered to act as a temporary storage of sporopollenin material because they are neither eliminated nor eroded during exine growth after callose dissolution. Heslop-Harrison (1968b) simply regarded orbicules as by-products of the tapetum (see also Echlin & Godwin, 1968a; Dickinson & Bell, 1972).

Christensen et al. (1972) mentioned that the orbicule wall formation could be regarded as a vestigial capacity of the tapetum because, phylogenetically, this layer once was active sporogenous tissue. Hesse (1986) also referred to the homology between the sporogenous tissue and the anther tapetum to explain the highly similar genetic information for formation of sporopollenin in both tissues. Indeed, analogies between orbicules and the respective ektexine are not restricted to few unrelated species but are, in fact, common in higher plants.

4. Associated with Pollen Dispersal

Heslop-Harrison (1968a, 1968b) was the first researcher to suggest that orbicules are associated with pollen dispersal forming a non-wettable locule surface from which pollen can easily detach. Keijzer (1987b) tested Heslop-Harrison's hypothesis on anthers of Lilium hybrid cv. 'Enchantment'. He removed the pollen grains and pollenkitt from a dehisced anther and then detached the tapetal membranes on the inner tangential endothecium wall together with the orbicules. Afterwards pollen and pollenkitt was reattached to this reduced pollen sac. Under extremely wet circumstances (98% relative humidity), most of the pollen did fall out of the anther whereas intact anthers did not lose their pollen. Both types of dehisced anthers reclosed under these wet conditions. In our opinion this is not a proof of the validity of the hypothesis. On the contrary, this experiment only proves that the removal of orbicules changes the sticking properties of the pollen to the locule wall - or perhaps that, as formulated in an abstract by the same author (Keijzer, 1984), in natural circumstances the lack of orbicules leads to the removal of the pollen grains by rain.

An observation in favor of this hypothesis is that during the shrinkage of the locule wall at dehiscence, the orbicules approach each other, creating a more continuous layer. This was also observed by Heslop-Harrison and Dickinson (1969) in Lilium longiflorum.

5. Role in Degradation of Tapetal Cells

The idea that orbicules might actively participate in lysis and degradation of tapetal cells has been suggested by Rowley and Erdtman (1967). They mentioned that orbicules are probably incidental in a tapetal digestive system that uses acid hydrolases. Herich and Lux (1985) observed in Lilium henryi that the orbicules get connected with the tapetal plasmalemma and then become lytically active. They could not elucidate which part of the orbicules is lytically active and enzymatic studies were promised.

6. As Prevention against Osmosis and Collapse of Developing Microspores

In some species, material (sporopollenin precursors) passing from the secretory tapetum to the microspores is generally deposited on the pro-orbicules to form the sporopollenin wall of the orbicules. Polymerisation of this excess of material will decrease the risk of high concentrations of sporopollenin precursors in contact with the developing microspores (ElGhazaly & Jensen, 1986; El-Ghazaly & Nilsson, 1991).

F. A DISTINCTIVE MICROMORPHOLOGICAL CHARACTER?

The possible taxonomic value of orbicules has been repeatedly stressed (Heslop-Harrison, 1962; Rowley, 1963; Banerjee, 1967; Carniel, 1971). Banerjee (1967) argued for the use of orbicules as a criterion in the taxonomy of grasses since their size, shape, and abundance vary by species. Despite this awareness, few studies have been published where the systematic importance of orbicule characters was investigated. The work of Ueno (1959, 1960a, 1960b) in gymnosperms was pioneering in this respect. To our knowledge, the combined pollen and orbicule morphological investigation in Bombacaceae (Nilsson & Robyns, 1974) was the first of its kind in angiosperms. Later the taxonomic applicability of orbicules has been demonstrated in Chloanthaceae, generally included in the Verbenaceae (Raj & El-Ghazaly, 1987) and in the genus Euphorbia (El-Ghazaly, 1989; El-Ghazaly & Chaudhary, 1993). In many cases pollen morphological similarity between species is also reflected in their orbicules. However, conflicting results may occur. In a recent paper (Huysmans et al., 1997) character states of orbicules were delimited in the Cinchonoideae - Rubiaceae on the basis of SEM observations. Evidence is given that, at least in this group, orbicule characteristics are systematically useful on generic or tribal level.

Striking analogies between orbicules and the respective sexine seem to be common in higher plants (Hesse, 1986). The similarities are not only macromorphological but also in the finest micromorphological characters of the structural elements in orbicules and the respective sexines (e.g. Rowley & Skyarla, 1974; El-Ghazaly & Jensen, 1986, 1987). These parallelisms are explained by Hesse (1985) as being rooted in the homology of tapetum and sporogenous tissue.

G. INTRASPECIFIC VARIATION

The occasionally observed intraspecific variation in orbicules contradicts the above-mentioned possible taxonomic value of these structures. Two main types of intraspecific variation can be distinguished: (1) different kinds of orbicules in one species or (2) not all specimens of the same species produce orbicules.

Hesse (1986) pointed out that different kinds of orbicules can occur in a single species. In Delonix elata, for instance, large, elongated, curved, and sculptured orbicules are found together with tiny, globular, or ovoid orbicules. In Euphorbia palustris, Hesse (1986) distinguished type A and B orbicules, respectively with and without central core. Shape and size is variable in both types. A and B orbicules occur together in time and space. We feel hesitant to accept this delineation because tangential sections on the periphery of orbicules with a central core will also appear as coreless. Hesse (1986) concluded that, at least in Euphorbia, they represent another orbicule generation; the different orbicule-characters are presumably due to different gene expressions during the stages of microsporogenesis. Cerceau-Larrival et al. (1981) found in Saxifraga cymbalaria both disc-shaped and spherical orbicules. The spherical orbicules originate later in the ontogeny than the disc-shaped ones.

Fusion of single orbicules (= derived from one pro-orbicule) may occur forming "complex" orbicules. These complex orbicules may be composed of few single orbicules as in Helleborus foetidus (Echlin & Godwin, 1968a), Euphorbia (Hesse, 1986), Cinchona pubescens, and Luculia pinceana (Huysmans et al., 1997). In the latter two rubiaceous species, the orbicule cores seem to remain intact (Huysmans et al., 1997). In Lilium some sporopollenin globules fuse, forming "a second generation of orbicules" (Reznickova & Willemse, 1980).

In Turgenia latifolia and Hydrocotyle mexicana (Apiaceae) a double orbicular secretion is observed (Abadie et al., 1981). The secretory tapetum of Turgenia latifolia produces micro-orbicules (0.25 [[micro]meter]) and macro-orbicules (5 [[micro]meter]) that are without central core. Orbicules in Hydrocotyle mexicana have a lipidic core and macro-orbicules also exhibit a nonsporopollenin body surrounded by an acetolysis-resistant sheath. The tapetum of Hydrocotyle mexicana is of the intermediary type.

Examples of species where not all specimens produce orbicules are found only in the vast amount of literature on both genetic and cytoplasmic male sterility (see reviews by, inter alia, Edwardson, 1970; Laser & Lersten, 1972; Kaul, 1988). Many authors report irregularities in the tapetum. Ontogenetic disturbance in the structure and/or function of the tapetum leads to male sterile pollen (Gifford & Foster, 1989: 566).

Few examples are given to illustrate the possible differences between orbicules in fertile and sterile lines of the same species. In a comparative study on the tapetal behaviour in male fertile and male sterile Iris pallida, Lippi et al. (1994) found no orbicules at all in the sterile clone. In the male fertile line the inner anther surface was completely covered by orbicules. The same pattern was observed for Zea mays (Colhoun & Steer, 1981) and Beta vulgaris (Hoefert, 1971).

Moussel et al. (1992) worked on Vicia faba and found for the fertile line that 14 out of 30 stamens had membranous formations (MFs) that give rise to pro-orbicules. In the other 16 stamens orbicules were not formed but the MFs moved in the anther cavity and became fixed on the ectoaperture edges of the microspores. In the sterile line only eight stamens on 26 produced orbicules and the number of MFs formed was more abundant. Exine formation was characterized by an exaggerated development of the different pollen wall layers. The authors advanced the following model to explain the observations: the MFs participate either in pro-orbicule synthesis in the tapetal glycocalyx or in building the rectum ornamentation by moving through the anther cavity loaded with sporopollenin. In male sterile lines many of the MFs are used for the abundant exine development, thus restricting the orbicule number.

Male sterility can affect orbicule formation in other ways too, such as through differences in size or wall ornamentation.

Keijzer and Cresti (1987) compared anther tissue development in male sterile Aloe vera and male fertile Aloe ciliaris. In the sterile line tapetal development and breakdown were normal; one of the visible deviations, however, was the presence of some large orbicules, which is in conflict with the model proposed by Moussel et al. (1992). Young et al. (1979) studied anther and pollen development in male sterile intermediate wheat-grass plants. They found different expressions of male sterility including orbicular wall malformations. De Vries and Ie (1970) noted that male sterility did not necessarily affect orbicule formation. They looked at anther tissue and pollen grains of cytoplasmic male sterile and fertile wheat (Triticum aestirum) for possible differences in cytoplasmic structures. Orbicules were observed in the anthers of both male sterile and fertile plants, with no visible differences.

El-Ghazaly and Jensen (1990) and El-Ghazaly (1990) studied the effect of a gametocide on the development of the pollen wall and noted that the orbicules were smaller in size and with thinner walls than those in untreated anthers.

H. ORBICULES IN THE FOSSIL RECORD

Spores with adhering orbicules are known from as early as the Devonian (Emsian; [+ or -]370 million years ago) (Taylor, 1990). Most accounts on fossil orbicules are from Mesozoic (Cretaceous) seed plants (e.g., Taylor & Alvin, 1984; Osborn et al., 1991; Serbet & Stockey, 1991; Archangelsky & Taylor, 1993). Fossil orbicules are also found in pteridosperm pollen organs (e.g., Taylor, 1976; Stidd, 1978). A comparison between fossil orbicules and tapetal membrane systems and those of extant plants can be found in Taylor, 1976.

On the basis of presence of orbicules in lycopods and bryophytes, Pacini et al. (1985) regarded the secretory tapetum as the most primitive. This hypothesis is corroborated by the presence of orbicules early in the fossil record.

I. DO ORBICULES CAUSE ALLERGY?

The allergenicity of pollen grains has long been the subject of extensive research. The question whether orbicules also contain allergens was first raised by Davis (1967). Orbicules of allergenic species dispersed into the atmosphere may act as a very effective vector to bring allergens to susceptible individuals. Indeed, the orbicules are often much more numerous than pollen grains and small enough to pass easily through the pores of most protective masks (Miki-Hirosige et al., 1994) and air-filters.

We give just some recent examples of immunocytochemical studies that pay attention to orbicules as well. For a detailed account we refer to the specialized biomedical literature. Intracellular localization of the two major allergens in rye-grass anthers (Lolium perenne) using specific monoclonal antibodies after anhydrous fixation showed no labeling on the orbicules or in the tapetal cells (Taylor et al., 1994). Yet, in a previous study on the same species, glycoproteins were found on the orbicules and in the anther locule (Vithanage et al., 1982). The major allergen responsible for Japanese cedar pollinosis is also found in the respective orbicules and on the tapetal materials remaining in the young anther, using both monoclonal and polyclonal antibodies produced from the protein (Miki-Hirosige et al., 1994). It is assumed that some of the allergenic protein is produced in the tapetum and localized in the orbicules and pollen wall during maturation, and that the rest of the allergenic protein is produced in the Golgi apparatus in the mature pollen grain (Miki-Hirosige et al., 1994). In a first paper on the possible allergenicity of Betula orbicules (El-Ghazaly et al., 1995), using the nitrocellulose membrane test on samples collected on Burkard tapes, it is shown that a large number of very small spots (ca. 4 [[micro]meter]) become visible on the nitrocellulose membrane. These are caused by small particles that cross-react with the polyclonal Bet v rabbit antibody. Because of their small size and since the time of appearance is simultaneous with the occurrence of pollen in the air, it is assumed that these small particles are orbicules.

V. Distribution of Orbicules in Angiosperms

A. PRESENCE OF ORBICULES

Our literature search resulted in a list of 314 species from 72 families reported to have orbicules (Table I). Although we aimed to search as exhaustively as possible, we realise that the present list is still incomplete because information is published in very diverse research fields, which complicates tracing. We would like to encourage readers to inform us about additional findings, either personal or from papers we overlooked.

Papers discussed in section IV.A are not included in Table I. Davis (1966: 14) listed 19 families in which orbicules have been recorded. Eleven of these are not in Table I: Amaranthaceae, Amaryllidaceae, Aristolochiaceae, Cuscutaceae, Cyclanthaceae, Linaceae, Molluginaceae, Olacaceae, Pedaliaceae, Portulacaceae, and Rhamnaceae. In the embryological descriptions of the respective families (Davis, 1966) only scarce information is given on orbicule occurrence. Since no specific references are given, this information is not included in Table I.

To visualise this information on a classification system, we have chosen to plot it on a dahlgrenogram (Dahlgren, 1989) [ILLUSTRATION FOR FIGURE 1 OMITTED]. Although we considered using the well-known "angiosperm-tree" by Chase et al. (1993) for this purpose, we ultimately decided that a convenient overview would be nearly impossible, given the fact that the tree with dicots and monocots on family level fills several pages. Moreover, information on presence or absence of tapetum types is so far only plotted on dahlgrenograms. All things considered, a dahlgrenogram was the obvious choice for presenting our data on orbicule distribution. We think the dahlgrenogram still is one of the most interesting tools for demonstrating the distribution of characters even if some classifactory insights are changed and evolutionary relationships are less univocal.

For localization of the families and assessment of their relative size, we followed Dahlgren (1989a, 1989b) for dicotyledons and Dahlgren and Clifford (1982) and Dahlgren et al. (1985) for monocotyledons.

[TABULAR DATA FOR TABLE I OMITTED]

B. SECRETORY TAPETA WITHOUT ORBICULES

Although it is generally accepted that orbicules are a general feature of secretory tapeta, few taxa have been traced with a secretory tapetum but without orbicules. Table II presents an overview of all negative observations we came across. We only mention references where the absence of orbicules is explicitly stated. The tapetum type of the respective species is also given, to enable the reader to interpret the information correctly. Nowhere is a hypothesis given to explain this absence.

C. WHY NO ORBICULES IN TAXA WITH AN AMOEBOID TAPETUM?

We found in the literature only one exception to the generally accepted rule that the presence of orbicules does not coincide with an amoeboid tapetum. According to Lombardo and Carraro (1976b), Gentiana acaulis has an amoeboid tapetum and also orbicules.

Bhandari (1984: 82) wrote the following about this question: "The lack of Ubisch bodies in the periplasmodial tapetum might also indicate the presence of some system of direct utilization of sporopollenin precursors during pollen wall formation."

[TABULAR DATA FOR TABLE II OMITTED]

The absence of orbicules in amoeboid tapeta indeed tests the hypothesis that implicates an active role for orbicules in the development of the pollen exine - an attributed function that awaits definitive proof.

In their work on the development of the amoeboid tapetum in Tradescantia, Tiwari and Gunning (1986b) found membrane-bound granules during tetrad stage which they considered to be analogous to the tapetal pro-orbicules in secretory tapeta. Since their amount and dimensions were not so obvious as in secretory tapeta, Tiwari and Gunning (1986b: 112) suggest "that in the plasmodial tapetum the machinery for transferring tapetally-synthesized sporopollenin to the spore-wall is efficient enough to limit the extent of formation of orbicules as by-products." The same authors posed the question of whether the limited occurrence of the granules is a manifestation of the amoeboid tapetum's capacity to overproduce sporopollenin or an evolutionary relic of the secretory tapetum (if the amoeboid type is considered to be more evolved than the secretory type, see section III.A.). Comparable structures were not yet reported for other amoeboid tapeta.

Experiments with colchicine treatments on anthers from species with an amoeboid tapetum yielded very interesting results concerning orbicules. Microtubules next to the tapetal plasma membrane were observed in different stages of development (Pacini & Keijzer, 1989; Tiwari & Gunning, 1986a, 1986c, 1986d). When the formation of these microtubules was blocked by colchicine treatments in anthers of Tradescantia virginiana, a species with an invasive syncytial tapetum, the plasmodium formation was inhibited (Tiwari & Gunning, 1986c). The spatial regulation of sporopollenin deposition was disrupted, which resulted in the formation of orbicules on the outside of the plasma membranes of tapetal cells. Similar effects of colchicine treatments were observed in the anthers of Canna, which has a nonsyncytial invasive tapetum normally without orbicules (Tiwari & Gunning, 1986). This work provided an experimental basis for the observation that sporopollenin polymerisation in an ordered form only takes place on extracellular lipidic surfaces. In the invasive amoeboid tapetum of T. virginiana, cell fusion during normal development indeed removes all such surfaces.
Table III

Summary of Tables I and II: number of families and species with and
without orbicules.

 Orbicules present Orbicules absent

Dicots Families 53 13

 Species 275 24

Monocots Families 19 3

 Species 39 4

Total Families 72 16

 Species 314 28


VI. Comments on Dahlgrenogram

In Table III we summarize the information of Tables I and II and Figure 1.

Fig. 1 demonstrates that the presence of orbicules is not restricted to a particular subclass or any other higher-level systematic group. The families with orbicules are spread over the system without a clear distribution pattern. Remarkably, the presence and absence of orbicules sometimes occur in the same family (Annonaceae, Berberidaceae, Fabaceae, Lamiaceae, Rubiaceae).

Suarez-Cervera et al. (1995: 81) speculated: "Perhaps their presence [orbicules] together with pollen grains, especially anemophilous, will also allow us to relate them with a system for a better dispersion of these pollen grains by the wind." From Figure 1 no such correlation with certain pollination syndromes could be deduced.

A. CORRELATION WITH TAPETUM TYPES

When we superimpose our dahlgrenogram on dahlgrenograms showing the distribution of tapetum types - namely, those of Dahlgren (1991) for dicots and Dahlgren and Clifford (1982) and Dahlgren et al. (1985) for monocots - there is indeed a very strong correlation: Orbicules do not occur in families with a dominant occurrence of an amoeboid tapetum. We found only two exceptions to this rule: Bignoniaceae and Alismataceae.

Both the Bignoniaceae and Alismataceae were shown to have an amoeboid tapetum; Davis (1966) confirms this. However, in Bignoniaceae four species are known to have orbicules, and in Alismataceae one. A recent study of tapetal development in Echinodorus cordifolius (Alismataceae) (El-Ghazaly & Rowley, in press), however, showed that tapetal cells remain secretorical until microspores are released from the callose envelope. At that time tapetal cells start to intrude into the locules and surround the microspores. Orbicules were clearly observed at tetrad stages only. This again illustrates that developmental studies are necessary to determine the true nature of the tapetum.

VII. Future Research

Many questions about origin, function, and morphological variation of orbicules remain. Only little of our knowledge is based on proven facts, the rest is based on hypotheses. Progress in understanding these fascinating structures can only be made by applying advanced techniques, assuring a more reliable fixation of the delicate tapetal tissues (e.g., rapid freeze-substitution). By autoradiography and isotope labeling, sporopollenin precursors can be traced and their route and destination can be determined during development.

The orbicule wall has the same biochemical composition as the pollen wall and is also ultrastructurally very similar. It is therefore a model to study sporopollenin biosynthesis in comparison with the pollen exine since orbicules are acellular structures, independent of cytoplasmic control (Clement & Audran, 1993b).

Any interpretation involving the control of exine morphology must also explain or be compatible with orbicule formation. Since orbicules are tapetal in origin, their existence severely tests models involving direct mediation of pollen wall form from the gametophyte (Rowley & Skvarla, 1974).

To make progress on the possible taxonomic value of orbicules it is necessary to have an idea about the overall morphological variation on a high systematic level. With the information available today it appeared impossible to recognize orbicule types on angiosperm level. More detailed SEM-observations of orbicules in situ are needed to reach this goal.

VIII. Acknowledgments

The first author holds a grant from the IWT and her research is financially supported by the research project N [degrees] G.0143.95 from the Fund for Scientific Research (F.W.O.). A travel grant from F.W.O. enabled S. Huysmans to discuss the final manuscript in Stockholm with G. El-Ghazaly and also with John Rowley, whose enthusiasm and expertise greatly stimulated finalisation of the paper. Thanks are due to Louis Ronse De Craene for translating the French abstract.

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