The nucellus and chalaza in monocotyledons: structure and schematics.
The significance of certain ovular characters (number of integuments and nucellus type) in higher-level systematics of angiosperms has long been noted, especially for dicotyledons (e.g., van Tieghem, 1898; Young & Watson, 1970; Philipson, 1974; Dahlgren, 1975). Indeed, ovular and embryological characters, together with pollen apertures, wood anatomy, and certain chemical characters, are proving important in the determination of wider relationships between angiosperm families. Evaluating structures as character states in the context of independently derived phylogenies increases our understanding both of the homology and evolution of the structures concerned and of relationships between taxa. Analysis of rbcL data in a broad range of angiosperm taxa (Chase et al., 1993) provided support for division of the eudicots (dicotyledons with triaperturate pollen) into two major groups: (1) tenuinucellate/sympetalous (asterids) and (2) not tenuinucellate/polypetalous (rosids). Furthermore, most tenuinucellate dicotyledons are also unitegmic, as Dablgren (1975) noted, whereas the majority of "primitive" dicotyledons and monocotyledons have bitegmic ovules (Endress, 1990, 1994; Dahlgren & Clifford, 1982).
In monocotyledons, on the other hand, earlier assessments (e.g., Dahlgren & Clifford, 1982; Stevenson & Loconte, 1995; Chase et al., 1995b) have indicated that both number of integuments and nucellus type lack systematic significance at the family level. The plesiomorphic conditions in monocotyledons are generally considered to be bitegmic and crassinucellate (e.g., Palser, 1975). Other nucellar and chalazal structures, such as hypostase, perisperm, and chalazosperm, are regarded as being of some systematic significance in monocotyledons and are used as characters in analyses. However, their terminology is confused and their homologies require testing. Part of the confusion in terminology arises from the fact that ovule and seed structures are not static; they may initiate, proliferate, or degenerate at different stages of development (primordium, mature ovule, or seed). Ovular structures and seed structures are often given different names although they may relate to the same tissues at different stages of development. Confusion between chalaza and nucellus originates from the general practise of referring to the (proximal) part of the nucellus nearest the chalaza as the "chalazal region of the nucellus," or "chalazal nucellus." Other confusion stems inevitably from literature in different languages.
In light of recent assessments of monocot relationships (e.g., Chase et al., 1995b; Stevenson & Loconte, 1995), a review of nucellar and chalazal characters in monocotyledons is timely. Strictly comparative data are needed for the different monocot groups. Batygina and Yakolev (1990) reviewed embryological structures in monocotyledons (using Takhtajan's system), and Batygina (1994) summarised embryological terminology and concepts, both in the Russian language. This paper reviews the systematic significance of nucellar and chalazal ovular especially in the lily groups (Asparagales and Liliales), with examples both from new data and the literature.
III. Nucellus and Chalaza
The nucellus arises from the apex and body of the ovule primordium. It is ultimately enclosed by one or two integuments, which develop from around the primordium base and encircle its apex, forming the micropyle. The archespore, usually a single cell, arises from within the nucellus. Since the archespore ultimately gives rise to the megagametophyte (embryo sac), the nucellus is the part of the sporophyte that encloses the megagametophyte, separating it from the inner integument, although some of the nucellus may have degenerated at floral anthesis. The chalaza is the region of the ovule where the nucellus, integuments, and funicle merge, and therefore usually encompasses a vascular bundle. The interface between chalazal and nucellar tissues is more or less on a line drawn between the ventral and dorsal limits of the inner integument, where it emerges from the chalaza (Fig. 1) (Rudall et al., in press). In a young ovule this line is approximately at the base of the megasporocyte (megaspore mother cell), but in some taxa the nucellus later proliferates, so that it may eventually lie below the ends of the integuments (e.g., in pachychalazal ovules: see below). Such varying differentiation of different parts of the ovule accounts for the occasional confusion of anatropous and campylotropous ovules.
[Figure 1 ILLUSTRATION OMITTED]
Prior to formation of the archespore, the ovule primordium is organised into either two or three distinct zones defined by orientation of cell division, as in the vegetative shoot apex (Bouman, 1984). The trizonate type is by far the most common, the dizonate type being a reduced form, which has probably evolved many times. The outermost (dermal) layer undergoes mainly anticlinal divisions at first, although it may later proliferate at the micropylar end to form a nucellar cap, and sometimes may also proliferate around and below the embryo sac. The archespore forms in the subdermal layer (of the trizonate type), immediately subtended by the central zone. The central zone forms the hypostase and other proximal nucellar structures, such as the postament and Zuleitungsbahn (conducting passage: see below).
IV. Distal (Micropylar) Region of Nucellus
The most widely used classification of the nucellus relates to the position of the megasporocyte. This was initially developed by van Tieghem (1898) and later Asplund (1920) (see Dahlgren, 1927; Maheshwari, 1950; Bouman, 1984), and is based largely on comparative work in dicotyledons. In the tenuinucellate condition the megasporocyte is hypodermal rather than deep-seated; the hypodermal archespore gives rise directly to the megasporocyte without first forming parietal tissue (Figs. 2A, 3A). However, in some tenuinucellate taxa, rapid and complete degeneration of micropylar megaspores and pressure from adjacent tissue soon results in a continuous subdermal nucellus layer at the micropyle. It is therefore essential to examine the megasporocyte stage to correctly determine this character condition. In tenuinucellate ovules the archespore and megasporocyte are indistinguishable.
[Figures 2-3 ILLUSTRATION OMITTED]
The converse condition is the crassinucellate one. In crassinucellate ovules (Figs. 2B, C, 3B-D, 4A-C) the megasporocyte is separated from the epidermis by one or several parietal layers (Bouman, 1984). The parietal tissue is derived from the archespore, which divides to form a proximal megasporocyte and a distal parietal cell (which may or may not divide further) (e.g., Davis, 1966), although in practice this cell division is rarely observed. In crassinucellate ovules the nucellus is therefore a sporangiophore-sporangium complex (Herr, 1995). Campbell (1900) reported a highly unusual instance in Dieffenbachia (Araceae) where the distal derivative formed the megasporocyte. In rare cases (e.g., Xanthorrhoea: Fig. 5), the archespore is apparently initially deep-seated, not hypodermal. Davis also used the term "pseudocrassinucellate" for a condition in which the megasporocyte is hypodermal (i.e., tenuinucellate), but the nucellar epidermis later further divides to form a nucellar cap, so that the megagametophyte becomes deep-seated.
[Figures 4-5 ILLUSTRATION OMITTED]
Following the earlier literature and current conventions, Dahlgren and Clifford (1982) identified two characters relating to the micropylar region of the nucellus in monocotyledons: (1) presence or absence of parietal cell (sometimes called "tapetal cell," or Deckzellen) and (2) presence or absence of a multiseriate nucellar cap derived from cell divisions in the nucellar epidermis. In their definition the nucellar cap is always multiseriate, in contrast to that of Tilton (1980a) where it may be either uniseriate or multiseriate (see below). The first character relates to the position of the megasporocyte, the second generally to the position of the megagametophyte (whether deep-seated or not), since cell divisions in the nucellar epidermis normally occur after the megasporocyte stage.
The majority of monocotyledons are crassinucellate, including many early-branching taxa (sensu Chase et al., 1995a, 1995b), such as Tofieldia (Oho, 1929), Pleea (Browne, 1961), and many Araceae, although in Araceae both crassinucellate and tenuinucellate conditions are present (Grayum, 1991). In Acorus the megasporocyte is two cell layers from the surface (Fig. 4D). Most early-branching ("primitive") dicotyledons are also crassinucellate (e.g., Chloranthaceae: Endress, 1987).
Wiegand (1900) described early development in three crassinucellate monocotyledons: Convallaria majalis (Convallariaceae), Potamogeton foliosus (Potamogetonaceae), and Canna indica (Cannaceae). In Convallaria and Canna the archesporial cell divides into a proximal megasporocyte and a distal parietal cell, which then repeatedly divides anticlinally to form a single layer of cells between the megasporocyte and the nucellar epidermis. In Potamogeton the parietal cell divides both anticlinally and periclinally to form four cell layers between the megasporocyte and the nucellar epidermis. The occurrence of periclinal divisions in parietal tissue may well constitute a different character state, although this requires further review.
The tenuinucellate condition is sparsely but widely distributed in monocotyledons (Dahlgren, 1927), and both conditions may sometimes occur within the same genus or even species (e.g., in Hemerocallis: Dahlgren, 1927; Lomandra: Rudall, 1994; Polygonatum and Smilacina: Bjornstadt, 1970; Amaianthium: Eunus, 1951; Nephthytis: Campbell, 1905). However, there is sometimes congruence between this character and existing monocot topologies at higher levels (e.g., Chase et al., 1995a, 1995b; Stevenson & Loconte, 1995). For example, among Asparagales, most taxa are crassinucellate (i.e., with parietal cells), including Agapanthus (Stenar, 1933) and Amaryllidaceae. Brodiaea, Dipterostemon, Dichelostemma, and Muilla (formerly Alliaceae, now Themidaceae) are also crassinucellate (Berg, 1978, 1996), whereas all members of Alliaceae lack parietal cells (Stenar, 1932). Recent analysis of rbcL and morphological data has resulted in these taxa and related genera being referred to a separate family, Themidaceae (Fay & Chase, 1996). The tenuinucellate condition is an apomorphy for the remaining genera of Alliaceae, although Ashurmetov and Yengalycheva (in press) reported a "mediocrinucellate" type for Allium, somehow intermediate between the crassinucellate and tenuinucellate types. The tenuinucellate condition also links the orchids with their probable sister family, Hypoxidaceae (both tenuinucellate), but not with other putatively linked taxa, such as Blandfordia or Astelia, which are crassinucellate (see Rudall et al., submitted). Stevenson and Loconte (1995) considered Hypoxidaceae close to Velloziaceae on this basis. Tenuinucellate ovules are also recorded in two closely related American genera of Iridaceae: Gelasine (Kenton & Rudall, 1987) and Eleutherine (Venkateswarlu et al., 1980), and in some Phormiaceae sensu lato (Chase et al., 1996): Dianella, Stypandra, Phormium, and Hemerocallis (Cave, 1955, 1975).
Among Liliales, there is good congruence for this character with rbcL data (Chase et al., 1995a) at the family level. Some lilioid families require recircumscription following recent analyses; for example Melanthiaceae is now widely regarded as a polyphyletic assemblage of several families (Stevenson & Loconte, 1995; Chase et al., 1995a, 1995b), some of them in Liliales (lilioid). The majority of lilioids are crassinucellate (e.g., Melanthiaceae-Narthecieae: Table I). If the rbcL topology is correct (Chase et al., 1995a), there are apparently two tenuinucellate lineages (Table I)--(1) Alstroemeriaceae, Luzuriagaceae, some Uvulariaceae (Disporum, Uvularia), and Colchicaceae; (2) Liliaceae and other Uvulariaceae (Tricyrtis: Fig. 6A)--although, judging from morphological data, and with further taxa added to the molecular analysis, these may represent a single tenuinucellate lineage.
[Figure 6 ILLUSTRATION OMITTED]
Table I Micropylar nucellar structures in some families of Liliales
Family Genus Alstroemeriaceae Alstroemeria, Bomarea Calochortaceae Calochortus Campynemataceae Campynema, Campynemanthe Colchicaceae Androcymbium, Colchicum, Gloriosa, Iphigenia Liliaceae Erythronium, Fritillaria, Gagea, Lilium, Tulipa Melanthiaceae - Chionographis Chionographideae Melanthiaceae - Amaianthium, Veratrum, Melanthieae Zygadenus Melanthiaceae - Heloniopsis, Metanarthecium Narthecium Narthecieae Philesiaceae Lapageria, Philesia Smilacaceae Ripogonum Smilax Trilliaceae Paris, Trillium Uvulariaceae Clintonia, Disporum, Streptopus, Trcyrtis, Uvularia Family Parietal cell Nucellar cap Alstroemeriaceae Absent Absent Calochortaceae Absent Present or absent Campynemataceae Present Present Colchicaceae Absent Present Liliaceae Absent Absent Melanthiaceae - Present Present or absent Chionographideae Melanthiaceae - Present Melanthieae Melanthiaceae - Present Narthecieae Philesiaceae Present Present Smilacaceae Present Present Trilliaceae Present Present Uvulariaceae Absent Absent Family References(*) Alstroemeriaceae Stenar, 1925; Cave, 1966 Calochortaceae Cave, 1941 Campynemataceae Dutt, 1970; Dahlgren & Lu, 1985; Goldblatt, 1986 Colchicaceae Dahlgren, 1927; Cave, 1967 Liliaceae Dahlgren, 1927; Stenar, 1927; Haque, 1951; Yufen & Jia-Heng, 1990; Berg, 1962 Melanthiaceae - Oikawa, 1961 Chionographideae Melanthiaceae - Ono, 1929; Stenar, Melanthieae 1928; Eunus, 1950, 1951 Melanthiaceae - Ono, 1926, 1929; Narthecieae Varitchak, 1940 Philesiaceae Cave, 1966 Smilacaceae Dahlgren et al., 1985 Trilliaceae Dahlgren, 1927; Berg, 1962 Uvulariaceae Bjornstadt, 1970; Alden, 1912; Dahlgren, 1927; Ogura, 1964
(*) References to Dahlgren (1927) and Cave (1967) include literature cited therein. Stenar's (1952) reference to Luzuriagaceae is not included, as Luzuriaga latifolia is correctly Eustrephus latifolius, which belongs in Asparagales, not Liliales.
Parietal cells are lacking in some families of Commelinales sensu Chase et al., 1995a (commelinoid families) (Table II), notably those of (a) the clade comprising Xyridaceae and Eriocaulaceae, and (b) the poalean clade (Linder & Kellogg, 1995), with the exception of Flagellariaceae, which is probably the sister taxon to other Poales (Kellogg & Linder, 1995). On present evidence this indicates two commelinoid tenuinucellate lineages (Table II). In Poaceae the ovule is always either crassinucellate or tenuinucellate with a nucellar cap (Dahlgren & Clifford, 1982). Festucoid grasses are largely tenuinucellate (Aulbach-Smith & Herr, 1984), indicating that such variation may be significant at the genus or subfamily levels although further review is necessary to determine this.
Table II Micropylar nucellar structures in commelinoid families
Family Nucellus Anarthriaceae Tenuinucellate Arecaceae Crassinucellate Bromeliaceae Crassinucellate Cannaceae Crassinucellate Cartonemataceae Crassinucellate Centrolepidaceae Tenuinucellate Commelinaceae Crassinucellate (tenuinucellate in Cyanotis) Costaceae Crassinucellate Cyperaceae Crassinucellate Dasypogonaceae Crassinucellate Ecdeiocoleaeeae Tenuinucellate Eriocaulaceae Tenuinucellate Flagellariaceae Crassinucellate Haemodoraceae Crassinucellate Hanguanaceae Unknown Heliconiaceae Crassinucellate Hydatellaceae Unknown Joinvilleaceae Unknown, but nucellar cap present (Fig. 14B) Juncaceae Crassinucellate Marantaceae Crassinucellate Mayacaceae Tenuinucellate Musaceae Crassinucellate Philydraceae Crassinucellate Poaceae Tenuinucellate or crassinucellate Pontederiaceae Crassinucellate Rapateaceae Crassinucellate Restionaceae Tenuinucellate (except dlexgeorgia) Sparganiaceae Crassinucellate Strelitziaceae Crassinucellate Thurniaceae Unknown Typhaceae Crassinucellate Velloziaceae Tenuinucellate Xyridaceae Tenuinucellate Zingiberaceae Crassinucellate Family References(*) Anarthriaceae Linder & Rudall, 1993 Arecaceae Dahlgren et al., 1985 Bromeliaceae Dahlgren et al., 1985 Cannaceae Dahlgren et al., 1985 Cartonemataceae Grootjen, 1983b Centrolepidaceae Hamann, 1975; Linder & Rudall, 1993 Commelinaceae Hamann, 1964; Dahlgren et al., 1985 Costaceae Dahlgren et al., 1985 Cyperaceae Dahlgren et al., 1985 Dasypogonaceae Rudall, 1994 Ecdeiocoleaeeae Rudall, 1990 Eriocaulaceae Hamann, 1964; Monteiro-Scanavacca & Mazzoni, 1978 Flagellariaceae Subramanyam & Narayana, 1972 Haemodoraceae Steinecke & Hamann, 1989 Hanguanaceae Heliconiaceae Dahlgren et al., 1985 Hydatellaceae Joinvilleaceae Juncaceae Dahlgren et al., 1985 Marantaceae Grootjen, 1983a Mayacaceae Venturelli & Bouman, 1986 Musaceae Dahlgren et al., 1985 Philydraceae Hamann, 1964, 1966 Poaceae Aulbach-Smith & Herr, 1984 Pontederiaceae Hamann, 1964 Rapateaceae Venturelli & Bouman, 1988 Restionaceae Rudall & Linder, 1988; this paper Sparganiaceae Muller-Doblies, 1969 Strelitziaceae Dahlgren et al., 1985 Thurniaceae Typhaceae Muller-Doblies, 1970 Velloziaceae Menezes, 1976 Xyridaceae Hamann, 1964 Zingiberaceae Dahlgren et al., 1985
(*) References to Dahlgren et al., 1985, include literature cited therein.
In some taxa the distal part of the nucellus degenerates entirely before anthesis, but in many monocotyledons it remains intact, sometimes forming a layer of enlarged cytoplasmrich secretory cells, as in Tulbaghia (Fig. 7A) and Ornithogalum, which Tilton (1980a) called a nucellar cap. Tilton (1980a) differentiated between a nucellar cap, which is rounded, and a nucellar beak, which is pointed and sometimes extends into the micropyle. Nucellar beaks are apparently most frequent in dicotyledons. In Tilton's definition a nucellar cap may be either uniseriate or multiseriate, but for most authors it is always multiseriate, following periclinal divisions of the dermal cells. Dahlgren (1940) noted that the nucellus sometimes becomes destroyed more rapidly at the sides of the embryo sac than at the proximal and micropylar ends. He proposed the term "petasus" for the remnant at the micropylar end, although this is more commonly called an "epistase" (Maheshwari, 1950).
[Figure 7 ILLUSTRATION OMITTED]
In a few commelinoid taxa, such as Eichhornia (Pontederiaceae) (Fig. 8A), the persistent nucellar epidermis becomes markedly elongated near the micropyle. This character state is a synapomorphy linking Restionaceae (Fig. 10A) and Centrolepidaceae (Fig. 9) (Linder & Rudall, 1993), although otherwise rare; for example, it is absent from Abolbodaceae (Fig. 11A), Bromeliaceae, Ecdeiocoleaceae (Fig. 12B), Eriocaulaceae (Fig. 13B, C), Flagellariaceae (Fig. 10B), Hydatellaceae (Fig. 12A), Joinvilleaceae (Fig. 14B), Juncaceae (Fig. 14A), Philydraceae (Fig. 14C), Rapateaceae (Fig. 11B), and Xyridaceae. Multiseriate nucellar caps occur in a wide range of taxa, such as Blanclfordia (Fig. 6B), Flagellaria (Fig. 10B), Joinvillea (Fig. 14B), Philesiaceae (Fig. 15), Smilax (Fig. 16B), Trillium (Fig. 17C), and Xanthorrhoea (Fig. 5C).
[Figures 8-17 ILLUSTRATION OMITTED]
V. Proximal (Chalazal) Region of Nucellus
The structure of the proximal end of the nucellus, adjacent to the chalaza, is variable and often includes modifications such as a hypostase or enlarged dermal cells. Some families have specialised structures in this region; for example, in the dicot family Podostemonaceae there is a nucellar plasmodium, which is a multinucleate haustorial protoplast (Arekal & Nagendran, 1975). In Pandanus (Pandanaceae), nucellar cells between the hypostase and the embryo sac enlarge and break off into the embryo sac, where they further divide (Fagerlind, 1940; Cheah & Stone, 1975). Proximal nucellar structures include the hypostase, postament, podium, and perisperm. Tilton (1980b) reviewed earlier literature and recommended the consistent use of individual terms for specific modifications, such as pseudochalaza, nucellar plasmodium, hypostase, postament, chalazal proliferating tissue, and Zuleitungsbahn (conducting passage) or Starkestrasse (starch route). Of these, at least the latter four are often present in monocotyledons.
In contrast to many eudicots, especially Asteridae, the proximal part of the nucellus at anthesis is often substantial in monocots (Maze & Bohm, 1973; Cave, 1975; Berg, 1978, 1996). The commonest condition for Lilianae (Rudall, 1994) is one where the proximal nucellus is short and broad, without enlarged dermal cells, but often with a hypostase and a fairly extensive subdermal region at the proximal ends around the sides of the embryo sac, but not towards the chalaza. This type occurs in many monocot taxa (e.g., Figs. 5C, 7B, 8B, 10A, 14B, 17C, 18, 19, 20, 26) including the putative basal monocot Acorus (Mucke, 1908; Buell, 1938), where the hypostase is massive (Fig. 21A, B). In Johnsonia, nucellar cells often become thick-walled (Fig. 8C). In some other taxa, the nucellus is insubstantial around the sides, but more substantial toward the chalaza, as in Dianella (Fig. 16A), Cyanella (Fig. 22), Tecophilaea (Fig. 23A, where it later persists as a postament: Fig. 23B). In Dasypogonaceae (Fig. 24) there is a massive proximal chalazal region (see perisperm, below). Ashurmetov and Yengalucheva (in press), citing earlier Russian-language literature, reported a substantial proximal region of the nucellus in Allium, with apparently high physiological activity in this region in some species. In some taxa, such as Tofieldia (Fig. 25B) and Aletris (Fig. 17A, B), the nucellus as a whole is less substantial at anthesis, and in others, such as Velloziaceae (Fig. 25A, C) and Eriocaulaceae (Fig. 13B, C), it is insubstantial or almost non-existent.
[Figures 18-26 ILLUSTRATION OMITTED]
As Tilton (1980b) observed, the term "hypostase" originally denoted all modifications of the proximal part of the nucellus (e.g., Johansen, 1928). However, later definitions, including that of Schnarf (1929) and Maheshwari (1950), are less broad and more useful. The hypostase is a well-defined group of cells immediately adjacent to the embryo sac (i.e., subtending the antipodals), normally poor in cytoplasmic contents and with thickened, refractive cell walls, which are partially suberinised or lignified. It is present before fertilisation, although sometimes persisting after fertilisation. A hypostase is found in many monocot taxa. Tilton (1980b) described the hypostase of Ornithogalum caudatum (Hyacinthaceae), which is typical of the type found in many other Lilianae, such as Galtonia (Fig. 6A), Borya (Fig. 8B), and Crocus (Fig. 18B) Rudall et al., 1984). In Acorus there is a massive hypostase, which is a present from early stages (Fig, 21A, B).
Many authors (e.g., Maheshwari, 1950; Tilton, 1980b) have speculated that the hypostase is related to the translocation of nutrients into the megagametophyte and embryo. It forms a barrier between the ovular vascular strand and the embryo sac, inhibiting the growth of the embryo sac into the chalaza (van Tieghem, 1901; Dahlgren, 1940). Coe (1954) demonstrated that in Zephyranthes relatively insoluble carbon-containing compounds were concentrated in the cells of the nucellus except the hypostase, indicating that the impermeable hypostase compels water and food to pass around it. According to Bor and Bouman (1974), in Euphorbia the hypostase is absorbed by the developing embryo and endosperm. In Allium odorum the hypostase becomes protoplasmic (Haberlandt, 1923).
Maheshwari (1950), following Dahlgren (1939), cited Zostera as a good example of a well-developed hypostase. However, judging from the illustrations, this tissue is not a typical thick-walled hypostase (although it is adjacent to the antipodals), but an enlarged thin-walled region of the nucellus, possibly with a storage function, as in, e.g., Dasypogonaceae and Rapateaceae (see perisperm below). Kuo et al. (1990) referred to a similar tissue in fruits of Phyllospadix (Zosteraceae) as a nucellar projection, the only part of the nucellus that persists for a while during fruit development, although it is eventually crushed in the mature fruit. In Phyllospadix the nucellar projection sometimes develops transfer cells, with numerous fine wall ingrowths, indicating that it may have a role in controlling the physiological development of the seed.
Makde (1981) described a prominent persistent "hypostase" in Cyperaceae. However, the tissue concerned is not strictly a hypostase because (1) it does not directly subtend the antipodals and (2) in the unfertilised ovule the cells are thin walled, with dense cytoplasm and a distinct nucleus. Only later, after fertilisation and during seed development, do these cells enlarge and become thickened and tanniniferous. Makde (1981) speculated that this tanniniferous tissue in Cyperaceae may well have a role for water and nutrient regulation in the mature seed (i.e., a role similar to that of the hypostase in the ovule).
B. ENLARGED DERMAL CELLS AND CONDUCTING PASSAGE (ZULEITUNGSBAHN)
The proximal region of the nucellus is often several-layered. In dicotyledons, Wilms (1980) demonstrated a several-layered proximal nucellus in Spinacia (spinach) and related the different layers to various functions. The early proliferation of nucellar tissue at the proximal end would tend to cut off the passage of nutrients from the funicular bundle to the original proximal tissue and hence the megagametophyte, and the central elongated cells possibly form a conducting route (Zuleitungsbahn: Westermaier, 1897) for such nutrient transfer (e.g., Fig. 18A). Reserve metabolites are probably stored in the proliferated lateral cells. Tilton (1980b) also described such a conducting passage between the vascular supply and hypostase in Ornithogalum, and cited other examples in monocotyledons.
In Lomandra (Fig. 27), an Australian member of Asparagales, the proximal nucellar region is relatively long and several-layered. Dermal cells are enlarged and there is little subdermal tissue, but a long central conducting passage (Zuleitungsbahn) is present, consisting of axially oriented, sometimes darker-staining cells connecting the chalazal vascular supply with the large antipodals (Rudall, 1994). A similar markedly enlarged proximal dermal layer, usually associated with large embryo sac nuclei, especially antipodals, also occurs in other members of the recircumscribed family Lomandraceae (Rudall & Chase, 1996; Chase et al., 1996). In this case, the nucellus data are highly congruent with the rbcL tree, and an enlarged dermal region represents the most consistent apomomorphy for Lomandraceae.
[Figure 27 ILLUSTRATION OMITTED]
Such enlarged dermal cells are unusual, but not unique in angiosperms. A similar type occurs in some members of the asparagoid family Themidaceae (Berg, 1996; Fay & Chase, 1996) and the lilioid family Uvulariaceae, at least in Scoliopus (Berg, 1962), Disporum (Bjornstadt, 1970), and Tricyrtis (Westermaier, 1897). In Tricyrtis the entire nucellus is narrow and elongated (Fig. 6A). Among dicotyledons, Boesewinkel (1989) reported a remarkably similar nucellus type in the insectivorous dicot genera Drosera and Dionaea, but not in other genera of Droseraceae. He correlated this with a dizonate ovule primordium in these taxa (a derived condition from the more usual trizonate one). Rombach (1911) also reported enlarged dermal cells in Crassulaceae. The adaptive significance of this nucellus type is obscure. Boesewinkel (1989) noted starch grains grouped around the nuclei of the enlarged dermal cells in Drosera. In Lomandraceae neither dermal nor central conducting regions contain storage material, so this is presumably not a perisperm, as in the case of the enlarged dermal nucellus cells of Acorus (see below). In Lomandra the dermal cells adjacent to the embryo sac are transfer cells with relatively large surface projections, indicating a transfer of solutes.
In Lomandra, at least on the side of the megagametophyte facing the highly vascularised raphe, where there is no outer integument, dermal cells degenerate soon after fertilisation, leaving the Zuleitungsbahn as a resistant strand (postament: see below). The central region resembles a vascular strand in that the cells are narrow and axially elongated; it is closely associated with the integumentary vascular supply but contains no xylem or phloem elements. Westermaier (1897) referred to the region of central, axially elongated cells in Tricyrtis as a conducting passage (Zuleitungsbahn) or starch route (Starkestrasse). Boesewinkel (1989) also considered these central cells in Drosera to be conductive, since they apparently form a conductive strand from the chalaza to the embryo sac. A vascular supply to the nucellus is extremely rare in angiosperms (Bouman, 1984), although there are occasional records of nucellar tracheids. For example, Grove (1941) reported tracheids with spiral thickenings present in the nucellus of Agave lechuguilla, in the region between the chalaza and the megagametophyte. Herr (1995) cited several other examples in dicotyledons.
C. HAUSTORIA AND TRANSFER CELLS
In several Asparagales there are records of so-called chalazal haustoria, where the developing endosperm invades the lateral parts of the proximal nucellus, breaking down the lateral tissue and leaving a central postament (often with a hypostase: see below). Chalazal haustoria are recorded in Anthericum (Schnarf, 1928), Curculigo (Schlimbach, 1924), Cyanella (De Vos, 1950), and Empodium (De Vos, 1949). The term "haustorium" implies increased absorptive activity, and there is clearly an observable pattern of nucellus tissue degeneration, followed by invasion of endosperm, also present in our material of Cyanella (Fig. 13A). De Vos (1950) reported that in Cyanella a few endosperm nuclei migrate into the cavity, then multiply and remain free-nucleate, eventually degenerating. These somewhat loosely defined haustoria are not strictly comparable with the chalazal and micropylar endosperm haustoria found in many Asteridae, such as Lamiaceae (Rudall & Clark, 1992), where distinct well-defined endosperm chambers are formed, often containing a few large coenocytic nuclei which may wander around the periphery of the haustorium.
Transfer cells facilitate passage of solutes across tissue boundaries. Pate and Gunning (1972) noted that transfer cells often occur at an apoplastic boundary, such as the junction between gametophyte and sporophyte, or at boundaries such as embryo/endosperm, embryo/perisperm, and perisperm/endosperm. Nucellar transfer cells are observable using the light microscope in some monocot taxa, and may well be more common than so far recorded. They occur in the persistent nucellar projection of Phyllospadix (Zosteraceae) (Kuo et al., 1990), and in Lomandra (Lomandraceae) in the dermal nucellus tissue adjacent to the megagametophyte (Fig. 27C), which breaks down after fertilisation (Fig. 27D).
D. POSTAMENTS AND PODIA
Postaments and podia are nucellar structures of the developing seed. Postaments often relate directly to the Zuleitungsbahn of the pre-fertilisation ovule nucellus (see above). The terms "postament" and "podium" are sometimes used interchangeably, but represent different structures. Both are persistent remains of the nucellus at the chalazal (proximal) end of the embryo sac. Both could incorporate a hypostase. However, as Dahlgren (1940) correctly observed, there is a critical difference between a postament, which is a resistant nucellar protuberance into the embryo sac (the lateral parts having often been eaten away), and a small resistant group of nucellar cells not projecting into the embryo sac, for which he proposed the term "podium." A podium is therefore an insignificant structure, present in many plants with an insignificant nucellus, such as in Euphorbiaceae and many tenuinucellate Sympetalae (Dahlgren, 1940; Bor & Kapil, 1975).
A postament is a remnant proximal column of nucellar tissue (Figs. 13A, 23C, 27D). It often leads from the chalazal vascular supply to the embryo sac, often to persistent antipodals, although in Tecophilaea (Fig. 23B) it emerges from a proliferated nucellar tissue. Postament cells are sometimes elongated, and apparently conductive, as Dahlgren (1940) also observed. In dicotyledons, postaments are common in Fagaceae, such as Quercus (Brown & Mogensen, 1972) and Nothofagus (Poole, 1952), where they represent a resistant remnant of nucellar tissue, linking the antipodals and vascular strand after the rest of the nucellus has degenerated. According to Dahlgren (1940), the term "postament" was introduced by Westermaier (1890), and thoroughly treated by Huss (1906), on Ranunculaceae, where there is a prominent postament bearing persistent antipodals. Alternative names for the same type of structure include columella (Westermaier, 1890), coussinet or pedicule (Guignard, 1901), promontoire (Soueges, 1910), pedestal (Palm, 1915; Gaumann, 1919; Capeletti, 1927), and Antipodensockel (antipodal pedestal: Haeckel, 1930). Dahlgren (1940) considered that a postament is normally a resistant column of cells, not a further growth of cells. He did not entirely exclude such cell proliferation from his definition of a postament, but the two tissue types are not homologous. Tissues that result from the later proliferation of the proximal region of the nucellus, such as in Capsella (Schulz & Jensen, 1971), where this region proliferates around the time of fertilisation, are not postaments but probably a type of perisperm (see below). Berg (1996) recorded a postament in Dipterostemon (Themidaceae).
In many cases postaments are associated with enlarged persistent antipodals, as in Lomandraceae (Rudall, 1994). Robertson (1976) referred to the persistent proximal part of the nucellus in the palm Jubaeopsis as a postament; however, this is not a column of tissue but simply a remnant basal region, and therefore correctly a podium.
The postament and central conducting passage (Zuleitungsbahn) are homologous structures at different stages of development, commonly associated with enlarged dermal cells and also with large persistent antipodals. The different terminology emphasises different properties/functions at different stages of development. At the earlier (pre-fertilisation) stage, the axially elongated cells of the Zuleitungsbahn are (presumably) conductive; at the later (post-fertilisation) stage, the cells of the postament are resistant to destruction, although in Lomandra (Fig. 27D) the dermal cells often degenerate on one side only (the side closest to the highly vascularised raphe), so the remaining postament tissue is not a symmetrical column.
In many monocotyledons parts of the nucellus enlarge or proliferate either before or after fertilisation, and have a role as a regulating or storage tissue for the megagametophyte and/or developing embryo. Robbins and Borthwick (1925) demonstrated that in Asparagus, nucellus cells start to enlarge until the sixteenth day after pollination, when they become gradually absorbed and replaced by endosperm, until all that remains is a very narrow pectic layer.
Seed storage tissues derived from the nucellus are termed perisperm, but perisperm may develop even before anthesis. In monocotyledons, there are records of perisperm in a wide range of taxa, but in many cases these tissues are of different structure and origin within the multi-layered nucellus and represent several unique parallel developments. In a few taxa, endosperm is absent from the mature seed, and the only storage tissue is derived from the nucellus (i.e., perisperm). For example, in Hydatellaceae, a small family of two genera (Hydatella and Trithuria), formerly included in Centrolepidaceae (Hamann, 1975, 1976), there is a starchy perisperm (Fig. 12A) and the endosperm is not developed beyond the early stages. In other taxa, perisperm storage products may be used up first, and only endosperm storage tissues persist in the mature seed.
Arnott (1962) recorded a perisperm entirely surrounding the embryo in seeds of Yucca (Agavaceae), rather similar to that described for Eriospermum (Lu, 1985). In Yucca seeds, Homer and Arnott (1966) found membrane-bound protein and oil bodies within the perisperm cells, together with reserve carbohydrates in the thick perisperm cell walls. From rbcL analysis (e.g., Chase et al., 1995a), Yucca and Eriospermum are fairly closely related, although not in the same family. In many Asparagales the proximal region of the nucellus is large, which may pre-adapt them for perisperm formation. Perisperm may indeed be more common in this group than hitherto recorded. For example, until Lu (1985) examined seed development in Eriospermum, its perisperm was recorded as a carnose (fleshy) endosperm.
Dahlgren and Clifford (1982, and references therein) regarded Zingiberales as "the main monocotyledonous group with perisperm." Perisperm is sometimes entirely compressed in the mature seed, only the cell walls remaining (e.g., in Musa: Graven et al., 1996). Grootjen (1983a) described a unique "perisperm channel" in Marantacaeae. This is a vascularised region formed by proliferation of the chalaza, which becomes enclosed by the nucellus after fertilisation, as a result of campylotropous curvature. It is therefore not strictly a perisperm, although it lies within the nucellus, and may be homologous with the pachychalaza of Cannaceae (Grootjen & Bouman, 1988) (see below).
In Ecdeiocolea (Ecdeiocoleaceae), there is an unusual proliferation of a group of proximal nucellar cells from the earliest megasporocyte stages (Rudall, 1990). This develops into a distinct region of thin-walled cells immediately adjacent to the megagametophyte; it is possibly a storage tissue, and therefore perisperm. The proximal part of the nucellus is differentiated into two distinct regions, both with a possible nutritive role (Fig. 12B).
In Dasypogon and Calectasia (Dasypogonaceae), the proximal region of the nucellus is a relatively massive starch-containing storage tissue (Fig. 24). Since this is entirely nucellar in origin, this tissue is probably a perisperm, not a chalazosperm (Rudall, 1994). A similarly massive proximal nucellar region, presumably with a storage role, is also present in Zosteraceae (Dahlgren, 1939; Kuo et al., 1990) and Rapateaceae (Fig. 11B) (Venturelli & Bouman, 1988), although not in Abolboda (Abolbodaceae or Xyridaceae) (Fig. 11A).
Although all the the former examples of perisperm are derived from subdermal tissues, in Acorus the perisperm is dermal. In Acorus calamus, Mucke (1908) and Buell (1938) described a unique uniseriate perisperm formed from the entire nucellar epidermis. These cells do not divide, but tend to elongate from an early stage, eventually becoming large and conspicuous and filled with clear, transparent proteinaceous cell contents (Fig. 21C). On the basis of its prominence and composition, they both concluded that this is a storage tissue, and since it derives from the nucellus it is a perisperm. However, it is not homologous with the perisperms of other monocotyledons (or dicotyledons such as some Piperales and Nymphaeales: Dahlgren & Clifford, 1982), which are not derived from the nucellar epidermis.
F. CHALAZOSPERM AND PACHYCHALAZA
The differences among perisperm, chalazosperm, and pachychalaza are not always well-defined in the literature. Perisperm and chalazosperm are not homologous structures. Perisperm is derived from the nucellus and lies on the megagametophyte side of the raphal bundle. Chalazosperm is derived from the chalaza and lies outside the raphal bundle.
A chalazosperm is recorded only in Cyanastrum, which has traditionally been accorded separate family status (Cyanastraceae) due largely to the presence of this structure in the mature seed of some species. However, from analysis of both morphological and molecular data, Cyanastrum belongs in Tecophilaeaceae, especially since Cyanastrum hostifolium (= Kabuyea unpubl.) lacks a chalazosperm and has endosperm. Although Engler (1901) described this tissue as a perisperm, Fries (1919), describing C. cordifolium and C. johnstonii, pointed out that it is not derived from the nucellus, which degenerates after fertilisation, but from the chalaza, outside the raphal bundle. Because of the lack of endosperm in the mature seed, he considered this starch-rich, loosely packed tissue (Fig. 23C) to have a nutritive role for the developing embryo, and therefore coined the term "chalazosperm." However, he conceded that its function is by no means certain, as it has strong similarities with seed-dispersal structures such as arils or elaiosomes, which are often found in Asparagales. Nietsch (1941), in a detailed description of the seed of C. cordifolium, followed the same interpretation. Other members of Tecophilaeaceae are poorly known for this aspect. As far as is known, the embryology of Odontostomum resembles that of Cyanastrum, including the elongation of the fertilised embryo sac and the presence of a chalazal tissue with loose strands of cells (Cave, 1952). In Cyanella (De Vos, 1950), the endosperm becomes cellular (unlike Cyanastrum) and there is an endosperm haustorium (Fig. 13A) (see above). In Tecophilaea seeds there is no chalazosperm, but the chalazal tissue becomes loosely packed (Fig. 23B) and the proximal region of the nucellus proliferates.
Some monocotyledons have seeds with a massive chalazal storage region (pachychalaza), as in most gymnosperms (Takaso & Bouman, 1986). The difference between chalazosperm and pachychalaza is not well defined. Grootjen and Bouman (1988) described pachychalazal seeds in Cannaceae, in which mitotic activity during ovule development causes the chalaza and basal part of the nucellus to become massive. Since there is no clear distinction between chalaza and nucellus, they called this region a pachychalaza rather than chalazosperm, and noted that in this respect Cannaceae differ markedly from other Zingiberales.
The monocot nucellus is highly variable in the mature ovule, from relatively massive (e.g., in Dasypogonaceae: Fig. 24) to almost non-existent (e.g., in Velloziaceae: Fig. 25A). Specialised nucellar structures are present in some taxa, often of systematic significance, although establishment of homologies is sometimes problematic. The nucellus clearly has a role in nutrition of the megagametophyte, either before or after fertilisation, and either as a regulating or storage tissue, indicated by the presence of nucellar transfer cells in some taxa: in Phyllospadix (Zosteraceae) in the persistent nucellar projection (Kuo et al., 1990), and in Lomandra (Lomandraceae) in the dermal nucellus tissue adjacent to the embryo sac (Fig. 27C), which breaks down after fertilisation (Fig. 27D). The nucellus may be pre-adapted to develop into various different types of storage or nutritive structures (perisperm). Perisperm has evolved several times in monocotyledons. Indeed, even in taxa lacking a well-developed perisperm, it is probable that the megagametophyte derives nutrients from the breakdown of the nucellus, before the endosperm is well-developed.
Character states relating to the nucellus may be presented as follows:
1. Position of megasporocyte: Megasporocyte separated from the epidermis by one or several parietal layers (crassinucellate) = 0; megasporocyte hypodermal (adjacent to dermal layer of nucellus) (tenuinucellate) = 1.
2. Nucellar cap: Dermal layer of nucellus lacking periclinal divisions = 0; with periclinal divisions (nucellar cap) = 1.
3. Nucellar epidermis: Dermal layer of nucellus not elongated = 0; cells anticlinally elongated at anthesis = 1.
4. Hypostase: Absent = 0; present at anthesis = 1. (Hypostase defined as a well-defined group of cells with thickened, refractive cell walls, immediately adjacent to the embryo sac and subtending the antipodals.)
5. Zuleitungsbahn/postament: Absent = 0; present at anthesis (Zuleitungsbahn) or post-fertilisation (postament) = 1. (Haustoria may relate to this character: see above.)
6. Perisperm: Absent = 0; subdermal = 1; dermal = 2. (Dermal perisperm is currently an autapomorphy for Acorus. Subdermal types may require some further assessment of homologies.)
7. Chalazosperm: Absent = 0; present = 1. (Currently an autapomorphy for Cyanastrum, although may be homologous with chalazal elaiosomes or pachychalaza in other taxa.)
Many thanks to Thomas Stutzel (University of Bochum), for allowing me to examine and photograph some of the excellent collection of microscope slides compiled by the late U. Hamann and his students (taxa marked with an asterisk in figure captions). Mark Engelman (Colegio de Postgraduados, Montecillo, Mexico) and Mary Gregory (RBG, Kew) kindly provided some translations from German and Russian literature, together with helpful discussion, and Dennis Stevenson (The New York Botanical Garden) commented on the manuscript.
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|Author:||Rudall, Paula J.|
|Publication:||The Botanical Review|
|Date:||Apr 1, 1997|
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