The Megagametophyte in Anarthria (Anarthriaceae ...

The Megagametophyte in Anarthria (Anarthriaceae, Poales) and Its Implications for the Phylogeny of the Poales H. P. Linder; P. J. Rudall American Journal of Botany, Vol. 80, No. 12. (Dec., 1993), pp. 1455-1464. Stable URL: http://links.jstor.org/sici?sici=0002-9122%28199312%2980%3A12%3C1455%3ATMIA%28P%3E2.0.CO%3B2-R American Journal of Botany is currently published by Botanical Society of America.

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American Journal of Botany 80(12): 1455-1464.

1993.

H. P. LINDER~ AND P. J. RUDALL Bolus Herbarium, Department of Botany, University of Cape Town, Rondebosch 7700, South Africa; and

The Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, England

The development and structure of the rnegagametophyte of Anarthria (Anarthriaceae), Aphelia, and Centrolepis (Centrolepidaceae) are described. Anarthriaceae has tenuinucellate ovules and thePolygonum type ofmegagametophyte development, both characters typical of the Poales. However, it lacks the anticlinally elongated nucellar epidermis and numerous large starch bodies observed in the megagametophyte of Centrolepidaceae, both characters also present in Restionaceae. This relatively generalized megagametophyte structure is consistent with data from the chloroplast genome, which suggest that Anarthriaceae are not as closely related to Restionaceae as previously assumed. New data from the megagametophyte are analyzed cladistically together with other available information on the poalean families. The results show that there are two possible positions for Anarthriaceae: either as sister to Poaceae, Joinvilleaceae, Restionaceae, Ecdeiocoleaceae, and Restionaceae, or as sister to only the latter three families. The new data also allow a critical reevaluation of the phylogenetic position of Centrolepidaceae, which is either basal to the poalean clade (based on microgametophyte data), or embedded in the Restionaceae (based on anther structure and rnegagametophyte data).

Anarthriaceae, with one genus and six species, has generally been regarded as the sister-group to the southern Temperate monocot family Restionaceae (Johnson and Briggs, 198 1; Dahlgren and Rasmussen, 1983; Campbell and Kellogg, 1987; Linder, 1987; Rudall and Linder, 1988), and these two families have been related to Poaceae and Joinvilleaceae (Campbell and Kellogg, 1987). However, the position of Centrolepidaceae has remained unclear. Hamann (1975) suggested that it may be a neotonous group of Restionaceae, and would thus be embedded in Restionaceae. This opinion was apparently followed by Dahlgren and Rasmussen (1 983) who indicated that Restionaceae were paraphyletic relative to Centrolepidaceae. Linder and Ferguson (1985) suggested on the basis of pollen morphology that Centrolepidaceae is not closely related to the Poales. Campbell and Kellogg (1987) also considered Centrolepidaceae to be relatively distantly related to Restionaceae. The understanding of the relationships of these families is strongly dependent on available data. Although Poaceae is relatively well known in some respects, information on the other families is generally inadequate. Restionaceae has recently received some attention (Linder, 1984; Harborne, Boardley, and Linder, 1985; Linder and Ferguson, 1985; Kircher, 1986; Rudall and Linder, 1988; Linder, 1992), while Centrolepidaceae were studied in some detail by Hamann (1962, 1975), Cutler (1969), and Prakash (1970). Rudall (1990) reported on the megagametophyte of Ecdeiocoleaceae, and the megagametophyte of Joinvilleaceae was described by Campbell and Kellogg (1 987). However, the megagametophyte of Anarthriaceae is hith: erto unknown, making a critical investigation of the phylogenetic relationship between Centrolepidaceae and Res-

' Received for publication 22 March 1993; revision accepted 17 June 1993. The authors thank Kathy Meney for taking them into the field; Kingsley Dixon for providing vehicles and organizing accommodation; and the Foundation for Research Development for supporting HPL. Author for correspondence.

tionaceae difficult. In this paper we report on the development and structure of the megagametophyte on Anarthria, with some additional observations on the megagametophyte of Centrolepidaceae, and discuss the systematic implications of these observations. MATERIALS AND METHODS Material (Table 1) was collected in the field near Perth, Western Australia, in the spring of 1990 and 1992, and was fixed in formalin-aceto-alcohol for at least 2 days, before being transferred to 70% alcohol. Ovules were carefully dissected out of the pseudanthia of Centrolepis or the ovaries of Anarthria and Aphelia, and placed onto microscope slides in a modified version of Herr's clearing fluid (lactic acid-chloral hydrate-phenol-clove oil-Histoclear, 2:2:2:2: 1 by weight). The slides were examined using differential interference contrast (DIC) optics on a Leitz Dialux 20 photomicroscope. Some flowers were also embedded in Paraplast using standard methods of wax embedding, and serially sectioned using a rotary microtome. Serially sectioned material was stained in safranin and Alcian blue, dehydrated through an alcohol series to 100% alcohol, then Histoclear, mounted in Euparal, and examined using normal bright field objectives on the same microscope. Cladistic analyses were carried out using Wagner parsimony, with Farris's (1988) program Hennig86. Cyperaceae, Juncaceae, Sparganiaceae, and Typhaceae were used as the outgroup for all the analyses, as these families are all related to the pooid families, but the precise relationship between them is not clear. The analyses were performed using ie*, which should find all equal length trees (Platnick, 1989). The cladograms were produced with the program CLADOS, produced by Nixon (1992). RESULTS Anarthria-The ovule is tenuinucellate, as there is no division of the archesporial cell to form a primary parietal

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AMERICAN JOURNAL OF BOTANY

[Vol. 80 DISCUSSION

TABLE 1. Material examined. Anarthriaceae Anarthria gracilis R.Br. A. humilis Nees A. laevis R.Br. A. prolifera R.Br. A. scabra R.Br.

Meney s.n. Linder 6079 Linder 6069 Linder 6042 Meney s.n.

Centrolepidaceae Aphelia brizula F . Muell. Centrolepis pilosa Hieron. Centrolepis glabra Hieron.

Linder 5547 Linder 5562 Rudall 25

cell. Megagametophyte development was observed in Anarthria laevis and conforms to the Polygonum type. A large megasporocyte (Fig. 1) by two divisions gives rise to a linear tetrad of megaspores (Fig. 2), of which the chalazal one is functional (Figs. 3, 4). Further divisions of the functional megaspore result in an 8-nucleate megagametophyte. In mature ovules (Figs. 10-14) the inner integument is tanniferous; the nucellus is uniseriate at the micropylar end with isodiametric cells, and a refractive hypostase is present at the chalazal end. Within the megagametophyte, the hypostase subtends three small antipodal cells. Each antipodal has a single nucleus, but sometimes with more than one prominent nucleus. The egg apparatus consists of two synergids and an egg cell. In Anarthria laevis, the polar nuclei fuse early to form a secondary nucleus that is usually associated with the egg apparatus. However, in Anarthria gracilis, the polar nuclei (Fig. 7) remain separate in the central region or at opposite ends of the megagametophyte after pollen penetration. Starch grains were absent, except following fertilization in Anarthria gracilis, where small numbers of very small spherical bodies resembling minute starch granules were present in the cytoplasm surrounding the polar nuclei in the central cell (Figs. 7, 8). Large prominent starch grains of the type found in Restionaceae (Rudall and Linder, 1988) and Centrolepidaceae (Figs. 15, 16) were never observed in

Anarthria. Centrolepidaceae-The ovule is tenuinucellate. Megagametophyte development conforms to the Polygonum type. A linear tetrad of megaspores is formed (Fig. 5), of which the chalazal one is functional (Fig. 6). Further divisions of the functional megaspore result in an 8-nucleate megagametophyte (Figs. 15, 16). The inner integument of the mature ovule contains tannins. At the micropylar end the nucellus consists of a single layer of elongated cells. The mature megagametophyte (Figs. 15, 16) is elongated and 8-nucleate, with a hypostase, and with three relatively large antipodal cells, two polar nuclei in the central cell, and an egg apparatus consisting of two synergids and an egg cell. The large synergids are elongated and protrude into the micropyle, with prominent thickenings forming a filiform apparatus (Fig. 16). The central cell contains copious large, prominent starch grains. Although binucleate antipodals were observed in one specimen of Centrolepis glabra, in most material of Centrolepidaceae antipodal cells were uninucleate.

Structure of the megagametophyte-The megagametophyte of Anarthria is very similar to that described for Poaceae (Anton, 1987), Restionaceae (Rudall and Linder, 1988), and Centrolepidaceae (Hamann, 1962; Prakash, 1970; Hamann, 1975), in that it has a Polygonum type development (probably the basal type for monocotyledons) and tenuinucellate ovules. These features were also observed for Centrolepidaceae, thus confirming Hamann's (1 962) observations. Tenuinucellate ovules are characteristic of the Poales, excluding Flagellaria. In several of the larger families, such as Poaceae and Restionaceae, periclinal divisions of the nucellar epidermis may result in the megagametophyte being deeply embedded. This thickened nucellus is termed by Davis (1966) 'pseudocrassinucellate' but in much of the German language this would be referred to a 'crassinucellate', leading to confusion in the literature (Hamann, 1975). The tenuinucellate condition would be described in German as the absence of 'Deckzellen', and is regarded as a quite distinct character (Hamann, 1975). The development of the antipodals is of interest, as the Poaceae often show proliferation of the antipodals (Poaceae variant of the Polygonum type embryo-sac, Anton and Cocucci, 1984), and this has also been reported for Restionaceae. Rudall and Linder (1988) showed that the distribution of proliferation of antipodals is apparently restricted to the African taxa; consequently the most parsimonious interpretation is that of an independent origin of proliferating antipodals in both Restionaceae and Poaceae. However, Hamann (1962) reported that Centrolepis aristata and C. strigosa have binucleate antipodals, a situation that may be considered to be related to antipodal proliferation. Prakash (1 970) could not demonstrate binucleate antipodals for Centrolepisfascicularis, and Hamann (1975) described uninucleate antipodals for Centrolepis glabra and Gaimardia setacea. Our observations here further support the presence of variation for this character in this family. Both Restionaceae (Rudall and Linder, 1988) and Centrolepidaceae (Figs. 15, 16; Hamann, 1962, 1975) have copious large starch bodies in the cytoplast of the central cell of the megagametophyte. Starch may occur in small quantities as a smaller, finer grain in the postfertilization megagametophytes of Anarthria, but is entirely absent from the megagametophytes of Ecdeiocolea (Rudall, 1990) and Flagellaria (Rudall and Linder, 1988). It has also not been reported for Joinvillea (Campbell and Kellogg, 1987), although it may not be so readily observed in thin sections, with bright-field optics. In Poaceae, starch, when present, appears to be restricted to the synergids (Anton, 1987), or in small bodies around the polar nuclei (Cass and Jensen, 1970). The distribution of starch in more distantly related families has not been surveyed. The presence of tanninlike substances in the inner epidermis of the inner integument has been established for Restionaceae (Rudall and Linder, 1988) and Centrolepidaceae (Hamann, 1975). It appears to be absent from Flagellariaceae (Rudall and Linder, 1988) and Ecdeiocoleaceae (Rudall, 1990). Campbell and Kellogg (1 987) did not remark on it for Joinvilleaceae, so it is not clear what the situation is there. Nor has it been noted for

December 19931

LINDERAND RUDALL-MEGAGAMETOPHYTE IN ANARTHRIACEAE

1457

Figs. 1-6. Megaspore development. 1-4. Anarthria laevis. 5 , 6. Centrolepis pilosa. 1. Megaspore mother cell (MM). 2. Tetrad, with megaspores numbered from micropylar to chalazal end (note remains of spindles). 3, 4. 2-nucleate stage; functional megaspore at chalazal end having divided to form two nuclei (N); remains of nonfunctional megaspores visible (R). 5. Tetrad, with megaspores numbered from micropylar to chalazal end. 6 . Functional megaspore (FM); remains of nonfunctional megaspores visible (R). H = hypostace. Bar = 10 wm.

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Figs. 7-9. Anarthria gracilis, composite pictures of optical sections of mature megagametophytes, after pollen tube (Pt) penetration. 7, 8. Micropylar end; polar nuclei (Pn), with few starch grains (St); Sy = synergid. 9. Chalaza1 end, with hypostase (H) subtending three small antipodals (A), each with one or two prominent nucleoli. Pn = polar nuclei. Bar = 10 wm.

Poaceae. Tannin in the inner epidermis of the inner integument does occur sporadically in the monocots (e.g., Philydraceae, Hamann, 1966), but its distribution has not been surveyed, and very few embryological reports remark on the staining of the inner epidermis of the inner integument. It is therefore possible that its distribution may have been underestimated. Anticlinal elongation of the nucellar epidermal cells, which has been noted for Centrolepidaceae (Hamann, 1975; and this paper) and Restionaceae (Rudall and Linder, 1988), is absent from Ecdeiocoleaceae (Rudall, 1990), Poaceae (Anton, 1987), and Joinvilleaceae (Campbell and Kellogg, 1987). In the grasses the nucellar epidermis sometimes undergoes periclinal divisions, but is apparently not

elongated. Neither periclinal divisions nor anticlinal elongation were observed here in Anarthriaceae. Phylogenetic implications -Anarthriaceae has generally been placed as the sister-group of Restionaceae, and Johnson and Briggs (198 1) advocated including it in Restionaceae. The character used for this association is the joint possession of peg cells in the chlorenchyma (Cutler, 1969; Campbell and Kellogg, 1987; Linder, 1987). However, the chloroplast genome inversions studied by Doyle et al. (1992) exclude Anarthriaceae from the group consisting of Poaceae, Joinvilleaceae, Restionaceae, and Ecdeiocoleaceae. This is consistent with the information from the megagametophyte, which shc~wsthat Anarthri-

December 19931

LINDERAND RUDALL-MEGAGAMETOPHYTE IN ANARTHRIACEAE

Figs. 10-14. Longitudinal sections of ovary and ovules. 10, 11. Anarthria gracilis. 12. Anarthria scabra. 13, 14. Anarthria prolifera. Note orthotropous ovules pendulous from the inner axile corner of each locule, and the tannins in the inner epidermis of the inner integument. Bars = 100 fim.

December 19931

IN ANARTHRIACEAE LINDERAND RUDALL-MEGAGAMETOPHYTE

TABLE2. Characters used in the cladistic analysis of the poalean clade; first state coded 0, second 1, etc. Character 1: Character 2: Character 3: Character 4: Character 5: Character 6: Character 7:

Character 8: Character 9: Character 10: Character 1 1: Character 12:

Character 13:

Character 14: Character 15:

Character 16:



Character 2 1: Character 22:

Character 23:

t

Leaf insertion distichous/tristichous. Chlorenchyma of culms and leaves' chlorenchyma cells normal/chlorenchyma with peg cells. Flower arrangement in inflorescence various/small, crowded into a head or spadix. Placentation apical lateral (axile or parietal)/basal. Ovule orientation orthotropous/amphitropous or hemianatropous/anatropous. Chromosomes with centromeres normal/centromeres diffuse. Leaf epidermis with all epidermal cells more or less the same/epidermis with long and short cells (cork cells). Silica bodies in the tissues absent/present. Calcium oxalate raphides absent/present. Pollen organization at release in tetraddmonads. Pollen aperture margin structure without an annulus/with an annulus. Pollen aperture operculum absent/present. The coding for this character for Centrolepidaceae would depend on the interpretation of the wall structure, see Linder and Ferguson (1985). Pollen interapertural wall without scrobiculi/with scrobiculi. The coding of this character for Centrolepidaceae depends on the interpretation of the holes through the interapertural wall (Linder and Ferguson, 1985) Micropyle construction bitegmic (exostomic)/endostomic. Multiplication of the antipodals (coded as nonadditive): three antipodals, each with one nucleus, usually ephemeralhhree antipodals with two nuclei each/multiplication of the antipodals. Starch in the megagametophyte present as many large granules, filling the whole central cell/absent or rarely present as some small granules. Ovule crassinucellate/tenuinucellate. Tannins in the inner epidermis of the inner integument usually shortly after fertilization present/ absent. Endosperm formation nuclear/helobial. Stigma morphology (according to Heslop-Harrison and Shivanna (1977) with personal observations for Anarthriaceae, Ecdeiocoleaceae, and Centrolepidaceae) plumose with receptive cells on multiseriate branches/receptive cells on ridges, zones, or heads. Nucellar epidermis at anthesis with cells isodiametrical/elongated. Helobial endosperm types with chalaza1 chamber not forming cells, but if cell walls are formed, then these occur after the micropylar chamber has developed/chalazal chamber with four to 16 cells, developing before the micropylar chamber. Stamens with four microsporangia/two microsporangia (the coding of this character for Restiona-

TABLE2. Continued.

Character 24:


ceae depends on whether Hopkinsia and Lyginia are included in the family. Leaf-blades on adult plants present/highly reduced. The coding of this character for Centrolepidaceae would depend whether the neoteny hypothesis is accepted or not, since if it is, then the leaves on Centrolepidaceae are equivalent to seedling leaves of Restionaceae. 28kb inversion in chloroplast genome (data from Doyle et al., 1992) present/absent. 6kb inversion in chloroplast genome (data from Doyle et al., 1992) present/absent.

aceae have the megagametophytic characters of the poalean clade (i.e., tenuinucellate ovules), but lack the following specialized conditions, which are found in various members of the group: 1) numerous large starch bodies in the central cell, and anticlinally elongated nucellar epidermal cells in both Restionaceae and Centrolepidaceae; 2) tetrasporic megagametophyte development, peri-

sperm, and lack of a hypostace in Ecdeiocoleaceae;

3) multiplication of antipodals in Poaceae and some Res-

tionaceae; 4) absence of tanninlike substances in, at least, Poaceae. The cladistic analysis of all available data (Tables 2, 3) show that on overall data Anarthriaceae are the sister group to Ecdeiocoleaceae plus Restionaceae and Centrolepidaceae. This grouping is based on the joint possession of peg-cells in the chlorenchyma, and on the presence of tanninlike substances in the inner epidermis of the inner integument of the ovule, and is contradicted by the chloroplast genome inversion data of Doyle et al. (1992).

TABLE3. Distribution of characters among the taxa. A question mark indicates that the character is either not known for the taxon, or is variable (both states are possible). Centrolepidaceae have been coded with microgametophytic characters homologous with restioid pollen, and Restionaceae have been coded ignoring the genera Lyginia and Hopkinsia. Cyperaceae Juncaceae Sparganiaceae Typhaceae Restionaceae Flagellariaceae Poaceae Anarthriaceae Joinvilleaceae Centrolepidaceae Ecdeiocoleaceae

10022 1?012 0?102 0?102 01000 00000 00011 01000 00000 00000 01000

10100 10001 00111 00111 00101 ?0101 01101 ?0001 ?I101 0000 1 ?0101

00010 00010 O?OOO O?OOO 11100 ?11?0 11012 11100 1?101 1??O1 1 loo?

?0?01 ?0?11 ?0?11 ?0?11 01000 101?1 11100 110?0 ???O? 0 100 1 11??0

00001 00001 O?OO? 0?001 10110 00001 00000 00001 00000 10 l?? 00010

1 1 ? ? 1 1 0 1 0 ? ?

Figs. 15, 16. Centrolepidaceae, composite pictures of optical sections of mature megagametophytes, each with three antipodal cells (A), two polar nuclei (Pn) surrounded by copious large starch grains (St), two synergids (Sy) with filiform apparatus (F). Egg cell not visible here. 15. Aphelia br~zula.16. Centrolepis pilosa. Bar = 50 pm.

[Vol. 80

I-+

i Juncaceae

Ecdeiocoleaceae

0

rFlagellariaceae I

'

7 2 5 2 6

m

n

a

0

1

0

T ' Poaceae y y : ; :

4 5 13 14 15 Q . ! .I : r

Joinvilleaceae

Fig. 17. Cladogram of the poalean clade showing the two possible positions of Anarthriaceae, with its supporting characters. Tree statistics: length 39 steps, consistency index 69, retention index 73. Character 18, tannins in the integument, was not used, but identical topologies, with slightly different statistics, are obtalned if tannin is coded as present in the Cyperaceae. Synapomorphies are indicated by black bars, parallelisms by empty bars, and reversals by shaded bars.

December 19931

m

L~NDER AND RUDALL-MEGAGAMETOPHYTE IN ANARTHRIACEAE 4

10 19

-

C yperaceae

Ecdeiocoleaceae

1

Fig. 18. Cladogram with microgametophytic characters coded according to Linder and Ferguson (1985). This analysis produced two trees with length of 41 steps, consistency index of 65, and retention index of 70. The trees differed in their placement of Anarthriaceae, not of Centrolepidaceae, and only one tree is presented, with the characters supporting the critical nodes indicated. Character 17, tannins in the integument, was not used. Synapomorphies are indicated by black bars, parallelisms by empty bars, and reversals by shaded bars.

However, the distribution of the tanninlike substances is poorly known, and does occur in at least some more distantly related monocot families. It may well be that the absence, rather than presence, of tanninlike substances is significant. If this is the case, then two equal length trees are retrieved (Fig. 17). These trees differ in the placement of Anarthriaceae: either basal to the Poaceae plus Restionaceae clade, or basal to the Restionaceae clade. Clarification of the position of Anarthriaceae, and of the structure of its megagametophyte, allows a reinterpretation of the position of Centrolepidaceae. If Centrolepidaceae are coded for the pollen characters according to Linder and Ferguson (1985), and Restionaceae are presumed to be monophyletic, then Centrolepidaceae emerge as basal to the poalean clade (Fig. 18). The clade is then defined by the orthotropous ovules, and the group excluding Centrolepidaceae by microgametophytic characters. Megagametophytic characters are highly homoplasious by this interpretation, with parallelisms between Restionaceae and Centrolepidaceae. If the pollen characters are coded as unknown for Centrolepidaceae (as in Table 2), this family emerges as the sister-group to Restionaceae (Fig. 17),based on two megagametophytic characters and one anther character. However, this grouping would challenge the monophyly of Restionaceae. Centrolepidaceae have anthers that have been reduced to two microsporangia, from the normal condition of four microsporangia. Anarthriaceae have four microsporangia, as do the genera Hopkinsia and Lyginia

of Restionaceae, while all other Restionaceae have anthers very similar to those ofcentrolepidaceae. If Centrolepidaceae, Lyginia, Hopkinsia, and the African and Australian groups of the Restionaceae are used as terminals in an analysis, then it is evident that the centrolepids group with the bulk of Restionaceae, forming a sister-group relationship with Hopkinsia and Lyginia. Although Hopkinsia and Lyginia are embryologically unknown, it would make no difference to the result whether they have the ovular and megagametophytic characters of the Restionaceae or Anarthria. The absence of the peculiar anatomical characters of Restionaceae in Centrolepidaceae could be accounted for by the hypothesis that these plants are neotonous Restionaceae as Hamann (1975) suggested. Linder (in press) has shown that many of the curious culm features of the restionaceous anatomy are absent in seedlings, and traces of the sclerenchymatous stele of the Restionaceae have been reported for Centrolepidaceae (Cutler, 1969). This hypothesis would also account for the presence of leaf blades in Centrolepidaceae. These have been shown to be generally well developed in all investigated Restionaceae seedlings, thus extending Hamann's (1975) anecdotal observation that one species of Restionaceae has seedlings similar to Centrolepid reproductively mature plants. Megagametophytic data on Anarthriaceae are consistent with the hypothesis of Doyle et al. (1992) that the family is not included in the Poaceae plus Restionaceae clade. However, the data indicate that Anarthriaceae are


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included in the poalean clade, with Poaceae, Joinvilleaceae, Restionaceae, Centrolepidaceae, and Ecdeiocoleaceae. Of the other available information, microgametophytic structure and sporophytic characters, except for the peg-cells in the chlorenchyma, are also consistent with this hypothesis. The contradiction between the chloroplast genome inversion data and the anatomical data can only be resolved by further data sets, not yet available. Centrolepidaceae may be embedded in Restionaceae. Its exact position cannot as yet be determined, but the genera Hopkinsia and Lyginia appear to be basal to Centrolepidaceae plus the rest of Restionaceae. This suggests that some family realignments may be necessary; however, more data are needed to test this hypothesis. LITERATURE CITED ANTON,A. M. 1987. Grass gametophytes: their origin, structure, and relation with the sporophyte. In T. R. Soderstrom, K. W. Hilu, C. S. Campbell, and M. E. Barkworth [eds.], Grass systematics and evolution, chapt. 2, 11-20. Smithsonian Institution Press, Washington, DC. -, AND A. E. COCUCCI. 1984. The grass megagametophyte and its possible phylogenetic implications. Plant Systematics and Evolution 146: 117-121. CAMPBELL, C. S., AND E. A. KELLOGG.1987. Sister group relationships of the Poaceae. In T. R. Soderstrom, K. W. Hilu, C. S. Campbell, and M. E. Barkworth [eds.], Grass systematics and evolution, chapt. 20, 2 17-224. Smithsonian Institution Press, Washington, DC. CASS,D. D., AND W. A. JENSEN. 1970. Fertilization in barley. American Journal of Botany 57: 62-70. CUTLER,D. F. 1969. Juncales. In C. R. Metcalfe [ed.], Anatomy of the monocotyledons, 1-343. Clarendon Press, Oxford. R. M. T., AND F. N. RASMUSSEN.1983. Monocotyledon DAHLGREN, evolution: characters and phylogenetic estimation. EvolutionaryBi010gy 16: 255-395. DAVIS,G. L. 1966. Systematic embryology of the angiosperms. John Wiley and Sons, New York, NY. D. GARVIN, AND M. J. ANDERSON. DOYLE,J. J., J. I. DAVIS,R. J. SORENG, 1992. Chloroplast DNA inversions and the origin of the grass family (Gramineae). Proceedings of the National Academy of Sciences, USA 89: 7722-7726.

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FARRIS,J. S. 1988. Hennig86 reference. Published by the author. HAMANN, U. 1962. Beitrag zur Embryologie der Centrolepidaceae mit Bemerkungen ueber den Bau der Blueten und Bluetenstaende und die systematische Stellung der Familie. Berichte der deutschen Botanischen Gesellschaft 75: 153-1 7 1. . 1966. Embryologische, morphologisch-anatomische und systematische Untersuchungen an Philydraceen. Willdenowia Beiheft 4: 1-178. -. 1975. Neue Untersuchungen zur Embryologie und Systematik der Centrolepidaceae. Botanische Jahrbuecher der Systematik 96: 154-191. HARBORNE, J. B., M. BOARDLEY, AND H. P. LINDER. 1985. Variations in flavonoid patterns within the genus Chondropetalum (Restionaceae). Phytochernistry 24: 273-278. HESLOP-HARRISON, Y., AND K. R. SHIVANNA.1977. The receptive surface of the angiosperm stigma. Annals ofBotany 4 1: 1233-1 258. JOHNSON, L. A. S., AND B. G. BRIGGS. 1981. Three old southern families-Myrtaceae, Proteaceae and Restionaceae. In A. Keast [ed.], Ecological biogeography of Australia, 429-469. Junk, Utrecht. KIRCHER,P. 1986. Untersuchungen zur Blueten- und Infloreszenzmorphologie, Embryologie und Systematik der Restionaceen im Vergleich mit Gramineen und venvandte Familien. Dissertationes Botanicae 94: 1-21 9. LINDER,H. P. 1984. A phylogenetic classification of the genera of the Africa Restionaceae. Bothalia 15: 11-76. -. 1987. The evolutionary history of the Poales/Restionales-a hypothesis. Kew Bulletin 42: 297-3 18. . 1992. The structure and evolution of the female flower of the African Restionaceae. Botanical Journal of the Linnean Society 109: 401-425. . In press. Restionaceae seedlings: morphology, anatomy, and systematic implications. International Journal o f Plant Science. -, AND I. K. FERGUSON.1985. On the pollen morphology and phylogeny of the Restionales and Poales. Grana 24: 65-76. NIXON,K. C. 1992. CLADOS version 1.2. Published by the author. PLATNICK,N. I. 1989. An empirical comparison of microcomputer parsimony programs, 11. Cladistics 5: 145-1 6 1. PRAKASH,N. 1970. The floral development and embryology of Centrolepis fascicularis. Phytomorphology 19: 285-29 1. RUDALL,P. J. 1990. Development of the ovule and megagametophyte in Ecdeiocolea monostachya. Australian Systematic Botany 3: 265274. , AND H. P. LINDER. 1988. Megagametophyte and nucellus in Restionaceae and Flagellariaceae. American Journal of Botany 75: 1777-1786.