The Embryology and Systematic Relationships of serratum (: Juncales) Author(s): Sioban L. Munro and H. Peter Linder Source: American Journal of Botany , Jun., 1997, Vol. 84, No. 6 (Jun., 1997), pp. 850- 860 Published by: Wiley Stable URL: https://www.jstor.org/stable/2445821

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This content downloaded from 86.59.13.237 on Tue, 06 Jul 2021 08:55:19 UTC All use subject to https://about.jstor.org/terms American Journal of Botany 84(6): 850-860. 1997.

THE EMBRYOLOGY AND SYSTEMATIC RELATIONSHIPS OF PRIONIUM SERRATUM (JUNCACEAE: JUNCALES)1

SIOBAN L. MUNRO2 AND H. PETER LINDER

Botany Department, University of Cape Town, Rondebosch 7700, Cape Town, South Africa

Although Prionium is included in Juncaceae, rbcL sequence data indicate that Juncaceae is paraphyletic, with most genera closer to than to Prionium. Cyperaceae and Juncales have embryological synapomorphies: thus embryology is used to test the monophyly of Juncaceae. The embryology of Prionium is described and its systematic position discussed. Material was prepared using standard methods of paraffin embedding. Additional embryological data were extracted from the literature. The anther in Prionium is tetrasporangiate, and the wall has an epidermis, an endothecium and middle layer, and an irregularly bilayered, glandular secretory tapetum. Microsporogenesis is probably simultaneous; pollen is ulcerate with a granular exine, in tetrahedral and cross tetrads, and trinucleate at release. The trilocular ovary contains many cras- sinucellate ovules probably having a Polygonum-type embryo sac. Endosperm is helobial and the embryo is of the Onagrad type, Juncus variation. The seed is testal-tegmic and germination is epigeal. The embryology of Prionium is most like that of Juncaceae, which shares several synapomorphies with Cyperaceae. Some of the characters in Cyperaceae may be inter- preted as specialized forms of those found in Juncaceae. Embryology supports the monophyly of Cyperaceae and Juncales, but not Juncaceae; thus the position of Prionium remains unresolved.

Key words: Cyperaceae; embryology; Eriocaulaceae; Flagellariaceae; Juncaceae; Prionium serratum; Typhaceae.

Prionium, a monotypic genus, is restricted to South in Juncaceae are closer to Cyperaceae than to Prionium, Africa where it occurs on oligotrophic soils along streams thus suggesting that Juncaceae sensu Dahlgren, Clifford, in the South Western Cape, extending along the coast into and Yeo (1985) are paraphyletic. This is corroborated by southern Kwazulu/Natal. Prionium has a woody, decum- the peculiar leaf anatomy of Prionium (Cutler, 1969) and bent rhizome, which is clothed in old sheathing leaf bases the presence of flavone C-glycosides found only in and is topped by a crown of serrate, tristichously inserted Prionium among members of Juncaceae (Williams and leaves. In addition, the plant often grows to several me- Harborne, 1975). tres in height. This growth form is bizarre in comparison Embryological data provide numerous synapomor- to other members of Juncaceae, which are usually small phies for both Cyperaceae and the Juncales (Linder and and herbaceous. Kellogg, 1995) and embryology therefore has the poten- Prionium forms dense monospecific stands, which usu- tial to test the monophyly of Juncaceae sensu lato. As ally grow in the beds of streams and rivers. The mass of Prionium is embryologically unknown, this study de- woody rhizomes act to bind the soil, thereby building up scribes the embryology of Prionium serratum (L.f.) Dre- river beds, ameliorating flooding events, and filtering wa- ge ex E. Mey and discusses its implications for the sys- ter. Prionium produces numerous seeds, which germinate tematic relationships of Prionium. in open spaces along river banks, but is also able to form new plants by budding along the woody rhizome. MATERIALS AND METHODS There is little morphological information available for Inflorescences of P. serratum at different developmental stages were Prionium except with regard to anatomy, which has been collected from three localities in the South Western Cape, South Africa well documented by Cutler (1969) and vascular construc- (Table 1) and fixed in formalin-acetic acid-ethanol (FAA) (17 ethanol: tion and development, which is covered by Zimmerman 2 formalin: 1 acetic acid vlv). Flowers and seeds were prepared ac- and Tomlinson (1968). The leaf and stem flavonoid cording to standard methods of paraffin embedding and sectioning. Se- chemistry have been surveyed by Williams and Harborne rial sections of 10 p.m were stained in a safranin-fast green combination (1975) for Prionium as well as for Juncaceae. (Johansen, 1940). For observations of microspore nuclei, pollen grains Prionium is usually included in Juncaceae (Cutler, at different stages in development were cleared using Herr's (1971) 1969; Dahlgren and Clifford, 1982; Dahlgren, Clifford, clearing agent [2 lactic acid: 2 chloral hydrate: 2 phenol: 2 clove oil: 1 and Yeo, 1985; Simpson, 1995), a small family of eight xylene (by mass)] for 12-18 h. Pollen and seeds were also sputter- to ten genera, which is restricted to the southern hemi- coated with gold-palladium for scanning electron microscopy (SEM). sphere, except for the cosmopolitan genera Juncus and Embryological data on Juncaceae and related families viz. Cyperaceae Luzula. On the other hand, rbcL sequence data (Chase et (Juncales), (Juncales), Flagellariaceae (), Eriocaula- al., 1993; Plunkett et al., 1995) indicate that most genera ceae (Commelinales), and Typhaceae (Typhales) were extracted from the available literature for comparison.

I Manuscript received 17 June 1996; revision accepted 8 November 1996. RESULTS The authors wish to thank Andrew Spinks and Tony Verboom for Anther and microspores-The anther is tetrasporan- reading through an earlier draft version and also, Paula Rudall and Dennis Stevenson for critically reviewing this manuscript. This research giate (Fig. 1), the wall comprising a single-layered epi- was supported by the Foundation for Research and Development (FRD). dermis, endothecium, and middle layer and a bilayered, 2 Author for correspondence. uninucleate tapetum of the glandular secretory type (Fig.

850

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TABLE 1. Voucher list of specimens collected for embryology. (Fig. 23). The endosperm in the micropylar chamber is initially acellular (Fig. 22), becoming cellular later, at Collector Collector's Locality no. which time the chalazal chamber consists of a few crushed cells and several disorganized nuclei (Fig. 23). Linder 5 770 Palmiet River bridge, S. W. Cape Linder 5 771 Palmiet River, S. W. Cape Linder 5773 Silvermine Nature Reserve, Cape Peninsula Embryogeny-The zygote (Fig. 24) formed through Munro 1 Algeria Forest Station, Clanwilliam, S. W. Cape syngamy divides to form a two-tiered proembryo con- sisting of a terminal cell, CA, and a basal cell, CB (Fig. 25). This develops into a three-celled, two-tiered proem- 2). Anther wall formation was not observed, but the num- bryo when CA divides longitudinally (Figs. 26, 27) and ber of layers present suggests the monocotyledonous further into a four-celled, three-tiered proembryo when type. The middle layer is ephemeral, degenerating shortly CB divides transversely producing two daughter cells, M before the microspores develop into pollen grains. Mi- and CI (Fig. 28). The latter division is the only contri- crosporogenesis is probably simultaneous (Figs. 3-5) bution of the basal cell to embryo development and this with pollen released in tetrahedral (Fig. 6) as well as is thus of the Onagrad type. The two cells of CA divide tetragonal (Fig. 7) tetrads, each grain being ulcerate with longitudinally to form a quadrant, tier Q. This is followed a slightly granular exine (Fig. 6) and three-celled at the by a longitudinal division of M, the middle cell. Tier CI shedding stage (Fig. 8). divides transversely to form two superposed cells N and N', which results in a four-tiered (Q, M, N, and N'), four- Ovary, nucellus, megagametophyte, and integu- celled proembryo (Figs. 29-31). At this stage, the cells ments-The trilocular ovary (Fig. 9) contains numerous of the epidermal initials (tier Q) are cut off without the anatropous ovules borne in two rows on each axile pla- formation of octants (Figs. 32, 33). This pattern of de- centa (Fig. 10). The style is much reduced, such that only velopment is the Juncus variation. Following this, tier Q the three stigmata remain at the apex of the ovary (Fig. undergoes several divisions to form two parts L and L' 11). The surface of each stigma is covered in sessile pa- causing the basal region of the embryo to become pear pillae. shaped (Fig. 34). Tier N' divides transversely forming The ovule is crassinucellate, with an archesporial cell two superposed cells 0 and P, which form the suspensor cutting off a parietal cell (Fig. 12), which undergoes fur- (Fig. 34). At this stage tiers M, L', and L undergo several ther divisions to form the nucellar tissue (Fig. 13). This divisions and increase in size (Fig. 34). Following this, results in the megaspore mother cell being deep seated tiers P and 0 are reduced to a single cell (N'), while tiers within the ovule (Fig. 13). N and M proliferate (Figs. 35, 36). Later in the devel- Although the tetrad stage of megasporogensis was not opment, the suspensor (tiers N' and N) is reduced leaving observed it is likely that the development of the embryo tier M in this region (Figs. 35, 36). sac follows the Polygonum type. This is indicated by the The mature embryo consists of a root cap region and presence of a single functional cell (functional mega- the piliferous layer (tissue originating from tier M) (Fig. spore) and three degenerating cells, which are crushed at 37), the plumule (tissue from L'), the central cylinder and the micropylar end of the ovule (Fig. 14), followed by a the cotyledon (tissue originating from some of tier L' and division of the functional cell to form two daughter cells most of tier L) and the outer layer of the cotyledon (tissue (Figs. 15, 16). The mature embryo sac consists of three originating from tier Q) (Fig. 38). persistent antipodals (Fig. 17), two polar nuclei that do not fuse before fertilization (Figs. 18, 19), and the egg Seed-The seed is trigonal, ovate to widely ovate in apparatus (Figs. 17, 20) of which the filiform apparatus shape and very small (:700 ,um long) (Fig. 39). The in the synergids is persistent (Fig. 17). mature embryo is linear and embedded within the en- The ovule is surrounded by two bilayered integuments dosperm (Fig. 38). The endosperm surrounds the coty- (Fig. 21). The inner integument is initiated when the ar- ledon and is enclosed by a distinct outer layer (possibly chesporial cell differentiates (Fig. 12), while the outer an aleurone layer) (Fig. 38). The cotyledon can be dis- integument is initiated only as the megaspore mother cell tinguished by the vascular trace and plumule (Fig. 38). differentiates. When the megaspore mother cell divides, The seed coat develops from both integuments (Fig. 38). both integuments appear complete (Fig. 13). The inner- The outer seed coat is loose around the inner seed coat most layer of the inner integument becomes filled with a and consists of loosely packed cells (Figs. 38, 40). The red-staining substance (probably tannin) in the later inner seed coat, by contrast, is tougher and envelops the stages of embryo sac development (Fig. 21). The micro- endosperm and embryo, consisting of elongate, tightly pyle is endostomic and is only formed at the mature em- packed cells (Figs. 38, 41). The inner seed coat seems to bryo sac stage (Fig. 21). be derived from the inner layer of the inner integument since this appears to contain the same tannin observed in Endosperm formation-Endosperm formation is of the latter developmental stages (Fig. 38). the helobial type, in which the primary endosperm nu- cleus divides to form a small chalazal and a large micro- Seedling-Germination is epigeal with the base of the pylar chamber (Fig. 22). A greater number of nuclear green cotyledon emerging from the seed, and following divisions occur in the micropylar chamber than in the contact with the soil growing upward, raising the seed chalazal chamber, which only undergoes a few divisions coat from the soil surface (Fig. 40A). Toward the base (Fig. 22). The chalazal chamber is crushed by the ex- of the cotyledon, in the region of the root cap and pili- panding micropylar chamber and the nuclei degenerate ferous layer, the primary root (radicle) differentiates,

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Figs. 1-8. Anthers and pollen grains of P. serratum. 1. TS anther with four sporangia. 2. TS anther sporangium showing wall layers at sporogenesis. Epidermis distinct outermost layer, endothecium distinct but nuclei not prominent, middle layer developed with nuclei visible, tapetum irregularly bilayered with prominent nuclei surrounding sporogenous tissue. 3-4. TS anther sporangium at sporogenesis at two focal levels showing division to form a cross tetrad, nuclei indicated by arrows. 5. TS anther sporangium at sporogenesis showing meiosis, with binucleate cell, indicated

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FigurentAbbreviations:L,t locule;0 ovuillae; PL,mat axhirdleplacna;oVw)vay;arSo stigma;e A,ue tle 2 Sovl hwn archesporial cell;Paitl cl;NEtuctareidermis; aI painera inegumnt Mhc, meyigasporel monethe chel;N nucellus; 01,eris outer integument; Meeoig 1.Lvl, megaspore; D,odgeerain cells;Crse cells.

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Figs. 25-35. LS postfertilization ovules of P. serratum showing embryogenesis. 25. Tlwo-celled proembryo with terminal cell (CA) and basal cell (CB). 26, 27. Three-celled, two-tiered proembryo over two serial sections, basal cell (CB), and terminal cell divided to form two daughter cells (CA). 28. Three-tiered proembryo, basal cell divided to form two daughter cells (M) and (CI), terminal cell (CA). 29-31. Quadrant formation over three serial sections. Tier (CA) has divided to form a qiuadrant (Q), the middle cell divides to form more cells (M), tier (CI) has divided to form

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Figs. 36-42. Postfertilization ovule, seeds, and seedlings of P. serratum. 36. LS post fertilization ovule showing detail of region of suspensor reduction (N'). 37. Differential interferance contrast (DIC) optics image of mature embryo showing root cap region and cotyledon. 38. LS seed showing outer seed coat, inner seed coat, embryo embedded within endosperm, plumule, cotyledon with vascular trace. 39. SEM of seed. 40. SEM e sa. 4.Eo innr sed oat 42. Seedling d (A Two dAys aft i. One

This content downloaded from 86.59.13.237 on Tue, 06 Jul 2021 08:55:19 UTC All use subject to https://about.jstor.org/terms June 1997] MUNRO AND LINDER-EMBRYOLOGY OF PRIONIUM 857 breaking through a slit at the base of the cotyledon (Fig. and Juncaceae), endosperm formation, and hypogeal ger- 40A). The radicle is the initial major functioning root, mination. These characters may be interpreted as spe- but later adventitious roots are formed (Fig. 40D-F). In cialized forms of the states found in Juncaceae. a region immediately above the base of the cotyledon, The development of the pseudomonad shows direct ev- the plumular bud differentiates to form the first foliar idence of the derivation of the pseudomonad (less gen- organ, which emerges through a slit in the cotyledon (Fig. eral) from the tetrad (more general). In Cyperaceae pol- 40B, C). The primary leaf (Fig. 40B) is formed 1 wk len, all four cells in the tetrads develop early in the on- after the cotyledon has emerged and at least three leaves togeny following microsporogenesis, after which three of are formed in the 1st mo of growth (Fig. 40D). The seed- the four grains migrate to the proximal end of the pollen ling (Fig. 40D, E) is thus a miniature replica of the adult grain where they degenerate (Wulff, 1939; Dnyansagar (Fig. 42F), albeit without a woody rhizome. and Tiwari, 1956; Padhye and Moharir, 1958; Padhye, 1960; Khanna, 1963; Davis, 1966; Padhye, 1971; Nagaraj Comparison of embryological data from the litera- and Nijalingappa, 1973; Meyer and Yaroshevskaya, ture-A comparison of the embryological characters of 1976; Dahlgren and Clifford, 1982; Dahlgren, Clifford, Prionium is made within Juncales (i.e., Juncaceae, Cy- and Yeo, 1985; Nijalingappa, 1986; Makde and Bhusku- peraceae, and Thurniaceae) and with three other families te, 1987; John, Ambegaokar, and Srivastava, 1992). The representative of three other orders within the commelin- remaining nucleus is functional and develops into the pol- id monocotyledons (sensu Linder and Kellogg, 1995) in len grain. Table 2. Details of the comparisons are discussed below. Endosperm formation, which in Cyperaceae is of the nuclear type, may be less general than the helobial type DISCUSSION in Juncaceae sensu lato. Although there is no consensus on the direction of evolution in endosperm types (Swamy Comparison with Juncaceae-The embryology of and Parameswaran, 1962; Dahlgren, Clifford, and Yeo, Prionium agrees closely with that known for Juncaceae. 1985; Kapil and Bhatnagar, 1991; Takhtajan, 1991; Fried- Prionium shares numerous embryological features with man, 1994), it is likely that helobial endosperm formation Juncaceae, viz. a glandular secretory tapetum, a single is general in commelinid monocotyledons (Dahlgren, middle layer, simultaneous microsporogenesis, pollen in Clifford, and Yeo, 1985). tetrads, and three-celled pollen at release, a crassinucel- Hypogeal germination in Cyperaceae may be special- late ovule, Polygonum-type embryo sac, helobial endo- ized compared with epigeal germination in Juncaceae sperm formation, Onagrad embryogeny of the Juncus sensu lato. However, hypogeal and epigeal germination variation, a testal-tegmic seed, and epigeal germination are widespread in the commelinid monocotyledons and (Table 2). Although a few differences [e.g., tapetum ir- evolutionary polarity is difficult to determine. In general regularly bilayered in Prionium vs. one layered in Jun- though, it would appear that hypogeal germination is de- caceae (except in Oxychloe where it is two); absence of rived from epigeal germination (Tillich, 1995). Therefore, rhomboidal tetrads at pollen release in Prionium vs. pres- Cyperaceae is specialized embryologically with respect ence in Juncaceae (Table 2)] do exist between Prionium to Juncaceae and the embryological data give evidence and Juncaceae, the embryology of Prionium nevertheless of the monophyly of Cyperaceae. Conversely, the embry- seems to be juncaceous. The occurrence of tetragonal tet- ological data present no evidence for the monophyly of rads in Juncaceae is extraordinary and is inconsistent Juncaceae plus Prionium, but excluding Cyperaceae. with the mechanism of simultaneous microsporogenesis The embryological characters that are known for Thur- which suggests that there may be some variation in this niaceae are anther and microspore characters (Table 2). character or some reshuffling in microspore positions af- Based on these (e.g., a glandular secretory tapetum and ter microsporogenesis (P. Rudall, personal communica- simultaneous microsporogenesis), Thumiaceae is closely tion). This may also be interesting with respect to micro- allied to both Juncaceae sensu lato and Cyperaceae. The sporogenesis in Cyperaceae where the relative positions pollen of Thurniaceae does, however, ally Thurniaceae of microspores change before three of them degenerate more closely to Juncaceae than to Cyperaceae because (P. Rudall, personal communication). the pollen is in tetrads and the pollen morphology is sim- ilar (Erdtman, 1944). However, the female embryology Comparison with Cyperaceae and Thurniaceae-Jun- is unknown, as is endosperm formation, embryogeny, and caceae sensu lato have several embryological features in germination. Therefore the systematic position of Thur- common with Cyperaceae (Linder and Kellogg, 1995), niaceae based on embryological evidence is unresolved. viz. a glandular secretory tapetum, simultaneous micro- sporogenesis, a crassinucellate ovule, a Polygonum-type Comparison with Flagellariaceae, Eriocaulaceae, embryo sac, Onagrad embryogeny of the Juncus varia- and Typhaceae-The embryology of Prionium differs tion, and a testal-tegmic seed (Table 2). Of these simul- markedly from that of Flagellariaceae (Poales), Eriocau- taneous microsporogenesis and Onagrad embryogeny of laceae (Commelinales), and Typhaceae (Typhales) (Table the Juncus variation are probably synapomorphies for 2). This is most evident when comparing the male em- Juncaceae plus Cyperaceae: however, because the embry- bryological characters and embryogeny. Microsporogen- ology of Thurniaceae is unknown, generalizations about esis in these three families is successive, pollen is re- embryological synapomorphies of Juncales cannot be leased as monads and each grain is usually two-celled made. (although they may also be three-celled in Eriocaula- Cyperaceae differs from Juncaceae in pollen arrange- ceae), while the embryogeny of these three families is of ment (pseudomonad in Cyperaceae vs. tetrad in Prionium the Asterad type (Table 2). These differences in embry-

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ological characters show clearly that the embryology of families of Monocotyledons. Smithsonian Contributions to Botany Prionium is most like members of Juncales and therefore 71: 1-73. HERR, J. M. 1971. A new clearing-squash technique for the study of based on embryology Prionium is closely allied to Jun- ovule development in angiosperms. American Journal of Botany caceae, Cyperaceae, and Thurniaceae. 58: 785-790. JOHANSEN, D. A. 1940. Plant microtechnique. McGraw Hill, New York, Systematic position of Prionium based on embryolo- NY gy-The embryological data support the monophyly of . 1950. Plant embryology: embryogeny of the Spermatophyta. Prionium, Juncaceae and Cyperaceae (i.e., Juncales). Chronica Botanica Company, Waltham, MA. However, the position of Thumia remains unknown be- JOHRI, B. M. K., B. AMBEGAOKAR, AND P. S. SRIVASTAVA. 1992. Com- parative embryology of angiosperms. Springer-Verlag, Berlin. cause the female embryology and embryogeny are not JUGUET, M. 1969. Embryologie veg6tale. Embryogenie des Juncacees. known. Embryology does not provide evidence for either D6veloppement de l'embryon chez le Luzula pilosa (L.) Willd. the monophyly of Juncaceae sensu strictum or Juncaceae Comptes rendus hebdomadaires des seances de l'academie des sci- sensu lato. Thus, the embryological data used neither fal- ences, Paris, serie D, 268: 3036-3039. sify nor corroborate the rbcL position of Prionium. . 1972. Observations embryogeniques chez les Cyperacees et les Juncacees. Congres des societes savantes Tours, de Paris 1968. Comptes rendus section des sciences 3: 547-572. LITERATURE CITED . 1973. Expression precoce de la monocotyledonie et mise en place du cotyledon et du point v6g6tatif de la tige chez quelques ANTON, A. M., AND A. E. Cocucci. 1984. The grass megagametophyte Monocotyledones, aves quelques remarques sur les types de sy- and its possible phylogenetic implications. 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