families and Magnoliaceae are 7 of 10 families of the hete- rogeneous primitive order Magnoliales sensu Cronquist. (1988), although Winteraceae is placed in a ...
Morphology of the outer integument in three primitive angiosperm families
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Ryoko Imaichi, Masahiro Kato, and Hiroshi Okada
Abstract: Scanning electron microscope examinations were performed to characterize the developmental morphology of the outer integument in several species of the three families Annonaceae (Cananga odorata var. fruticosa, Goniothalamus macrophyllus, and Stelechocarpus burahol), Eupomatiaceae (Eupomatia laurina), and Winteraceae (four Tasmannia species). In all species examined, the inner integument arises as an annular ring, but the outer integument initiates as a semiannular outgrowth interrupted on the concave side of the funiculus; the outer integument then becomes hood-shaped. The inner integument overtops the outer one at maturity, and the micropyle consists only of an endostome. Data from the present and previous studies support the hypothesis that the outer integument is hood-shaped in magnolialean angiosperms and that the bilaterally symmetrical, bladelike outer integument is homologous with the ovuliferous sporophyll of the glossopterids. The micropyle consisting of an endostome might be in a primitive state, compared with a bistomic one. Key words: developmental morphology, integument, micropyle, phylogenesis, primitive angiosperms, scanning electron microscopy.
Resume : Les auteurs ont conduit des examens en microscopie Clectronique par balayage afin de caractiriser la morphologie du dkveloppement du tkgument externe chez plusieurs espkces de trois familles dlAnnonaceae (Cananga odorata var. fruticosa, Goniothalamus macrophyllus et Stelechocarpus burahol), Eupomatiaceae (Eupomatia laurina) et Winteraceae (quatre espkces de Tasrnannia). Chez toutes les espkces exarninCes, le tegument interne apparait sous forme de bagues annulaires, rnais le tCgument externe dCbute cornrne une excroissance semi-annulaire interrornpue du cBtC concave du funicule; le tCgument externe prend alors la forrne d'une calotte. Le tCgurnent interne se superpose au tCgurnent externe B rnaturitC, et le micropyle est rCduit a un endostorne. Les donnCes de cette Ctude et d'Ctudes antCcCdentes supportent l'hypothkse que le tCgurnent externe est en forrne de calotte chez les angiosperrnes rnagnoliennes et que le tCgument externe en forrne de lame et bilateralernent syrnCtrique est hornologue avec la sporophylle ovulifkre des glossoptCrides. Le rnicropyle consistant en un endostorne pourrait Ctre prirnitif cornparativernent a un rnicropyle bistornique. Mots clLs : rnorphogCnkse, tCgurnent, rnicropyle, phylogenkse, angiospermes primitives, rnicroscopie Clectronique par balayage. [Traduit par la rCdaction]
Introduction Bitegmic, as well as anatropous and crassinucellar, ovules are the most common in and unique to angiosperms, in particular primitive angiosperms (Eames 1961; Stebbins 1974; Bouman 1984; Cronquist 1988; Takhtajan 1991 ; Johri et al. 1992; Stewart and Rothwell 1993). The outer integument, like the inner one, had been generally considered to be cupshaped (Bouman 1984; Johri et al. 1992). However, recent
Received August 10, 1994.
R. Imaichi.' Faculty of Agriculture, Tarnagawa University, 6-1-1 Tarnagawagakuen, Machida, Tokyo 194, Japan.
M. Kato. Botanical Gardens, Faculty of Science, University of Tokyo, 3-7-1 Hakusan, Tokyo 112, Japan. H. Okada. Department of Biology, Faculty of Science, Osaka University, 1-16 Machikaneyarna, Toyonaka, Osaka 560, Japan.
'
Author to whom all correspondence should be addressed.
Can. J. Bot. 73: 1242- 1249 (1995). Printed in Canada 1 Imprime au Can
developmental studies have shown that it is hood-shaped in Magnoliaceae (Matsui et al. 1993; Umeda et al. 1994). The outer integument is interrupted on the concave side of the funiculus, and a funicular outgrowth or obturator (Davis 1966) intervenes in the gap of the outer integument in Liriodendron tulipifera and Magnolia grandiflora. Thus, two different entities, the outer integument and obturator, form an outer envelope complex surrounding the inner integument. The ovules are known to have no outer integuments nor prominent outgrowths on the concave side of their funiculi in Degeneriaceae (Swamy 1949), Annonaceae (Lampton 1957 ; Periasamy and Swamy 1961; Mohana Rao 1975, 1979, 1982), Winteraceae (Bhandari 1963; de Boer and Bouman 1974; Prakash et al. 1992), Austrobaileyaceae (Endress 1980a), Eupomatiaceae (Mohama Rao 1983; Johri et al. 1992), and Himantandraceae (Prakash et al. 1984). The six families and Magnoliaceae are 7 of 10 families of the heterogeneous primitive order Magnoliales sensu Cronquist (1988), although Winteraceae is placed in a separate clade termed winteroids by Doyle and Donoghue (1993). Umeda
lrnaichi et al Table 1. Families, species, collection localities, and vouchers of the flowers
examined in this study. Family and species
Locality and voucher
Annonaceae
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Cananga odorata (Lam.) Hook. f. & Thoms. var. fruticosa (Craib) Sincl. Goniothalamus macrophyllus (B1.) Hook. f. & Thoms. Stelechocarpus burahol (Bl.) Hook. f. & Thoms.
Yogyakarta, Central Java (cultivated) Bogor Botanical Garden, Java (cultivated) Bogor Botanical Garden, Java (cultivated, tree No. XXD59); Okada 3390
Eupomatiaceae Eupomatia laurina R.Br.
Mt. Coot-tha Botanical Garden, SE Queensland (cultivated); Kato et al. 38
Winteraceae Tasmannia insipida R.Br. ex DC.
Tasmannia lanceolata (Poir.) A.C.
Smith Tasrnannia piperita Miers Tasmannia stipitata (Vickery) A.C.
Smith
New England National Park, Point Lookout, New South Wales; Okada et al. 190 Mt. Wellington, Tasmania; Okada et al. 746
Vicinity of Habema, W of Wamena, Irian Jaya; Kato et al. 885 New England National Park, Point Lookout, New South Wales; Okada et al. 195
et al. (1994) have hypothesized that the outer integument of those families is hood-shaped as in Magnoliaceae. However, available data are limited to sectioned ovules, and the morphology of the outer integument in those families remains to be investigated. Most workers (Eames 1961; Stebbins 1974; Cronquist 1988; Takhtajan 1991; Stewart and Rothwell 1993) argued that bitegmy appeared in the initial evolution of angiosperms, but a few others (e.g., Taylor 1991) considered that the outer integument was derived from the outer envelope of putatively related gymnosperms. In contrast with the inner integument that is evidently comparable to the single integument of related gymnosperms, the morphological nature and homology of the outer integument characteristic of angiosperms seem to be important and are required to be determined for understanding the origin and evolution of angiosperms. The present study attempted to test the hypothesis (Umeda et al. 1994) that the outer integument is hood-shaped in the families Annonaceae, Eupomatiaceae, and Winteraceae of Magnoliales sensu Cronquist (1988). Although the order has been shown to be polyphyletic (Donoghue and Doyle 1989; Loconte and Stevenson 199 1; Chase et al. 1993; Qiu et al. 1993), the families belonging to it have most of presumably primitive floral characters in common (Eames 1961; ~ r o n quist 1988; Takhtajan 1991). The results obtained here should provide a sound morphological basis for investigating the phylogenesis of the outer integument of angiosperms.
Materials and methods The species examined in this study include three species of Annonaceae, Cananga odorata var. fruticosa (30 samples), Goniothalamus macrophyllus (32), and Stelechocarpus burahol
(3 1); one species of Eupomatiaceae, Eupomatia laurina (40); and four species of Winteraceae, Tasmannia insipida (3), Tasmannia lanceolata (15), Tasmannia piperita (28), and Tasmannia stipitata (20) (Table 1). Materials used were collected in eastern Australia in November and December 1992 and Java, Indonesia in September 1991 and February 1993, and Irian Jaya, Indonesia in December 1993. Among them, flower buds at various developmental stages and flowers at anthesis were obtained for E. laurina (Eupomatiaceae), G. macrophyllus (Annonaceae), and T piperita (Winteraceae), and those of the other species could be collected at fragmentary stages. Voucher specimens of the materials except for C. odorata var. fruticosa, an ornamental shrub, are deposited in the herbarium of the University of Tokyo (TI). Materials were fixed in (formalin - acetic acid - 50 % ethanol (FAA) 5:5:90 vlv), dehydrated in an ethanol series, critical point dried, and coated with gold. Observations were made using a JSM-TI00 SEM (25 kV).
Results Eupomatiaceae (E. laurina) Four semiglobular ovule primordia are produced in two rows in each of the carpels (Fig. l), which are connate to each other along the entire length. In young ovules beginning to incurve, the inner integument is completely circular around the nucellus; in contrast, the outer integument of young ovules is a semicircular ridge interrupted on the concave side of the funiculus (Figs. 2 and 3). At a later developmental stage, the distal nucellus-integument complex is bent to the funiculus at about right angles and the complex is thicker than the funiculus (Figs. 4 and 5). The inner integument envelopes the nucellus and the outer integument envelopes
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Figs. 1-9. Scanning electron micrographs of E. laurina ovules at successive developmental stages. Fig. 1. Subglobular ovule primordia. Fig. 2. Initiating annular inner integument in incurving ovule primordium. The outer integument has just initiated. Fig. 3. Early development of semiannular outer integument. Fig. 4. Frontal view of ovule with enlarged distal nucellus-integuments portion. Note that the outer integument is interrupted on the funiculus with longitudinal cell files. Fig. 5. Obliquely frontal view of ovule at similar stage to that of Fig. 4. Figs. 6 and 7. Further incurved ovules with both integuments overgrowing nucellus. Fig. 8. Long-ellipsoidal mature ovule with exposed distal end of inner integument (marked by arrow). Fig. 9. Frontal view of micropyle consisting of endostome. e , endostome; f, funiculus; i, inner integument; o, outer integument. Scale bars = 50 pm.
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Figs. 10-98. Scanning electron micrographs of 7: piperita (Figs. 10-16) and 7: lanceolata (Figs. 17 and 18) ovules at successive developmental stages. Fig. 10. Initiation of inner integument. Fig. 11. Developing annular inner integument in incurving ovule. The inner integument develops more slowly on the convex side of funiculus than on its concave side. Scale bars = 20 pm for Figs. 10 and 11. Fig. 12. Developing semiannular outer integument. Fig. 13. Hood-shaped outer integument in more incurved ovule. The distal lateral margins (marked by arrow) are decurrent to funiculus. Fig. 14. Older anatropous ovule with endostome and exostome at the same level. Figs. 15 and 16. Mature ovule. Figure 16 is a magnification of Fig. 15, showing narrow endostome and reversely U-shaped exostome. Note that surface cells on funiculus are much smaller than those of outer integument. Fig. 17. Young, incurved ovule with annular, somewhat lobed inner integument and hood-shaped outer integument. Fig. 18. Mature ovule. e , endostome; f, funiculus; i, inner integument; o , outer integument. Scale bars = 50 pm for Figs. 12- 18.
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Figs. 19 and 20. Scanning electron micrographs of mature ovule of T. insipida. Figure 20 is enlargement of Fig. 19. Arrows indicate the distal lateral margins of hood-shaped outer integument. e , endostome; i, inner integument; o, outer integument. Scale bars = 50 pm.
the inner one to a greater extent than at younger stages. The outer integument is a semicircular interrupted envelope (Figs. 4 and 5). The dermal cells of the outer integument are aligned in parallel to the axis of the nucellus; dermal cells on the concave side of the funiculus near the inner integument are parallel to the axis of the funiculus. Both inner and outer integuments overgrow the nucellus as ovules become anatropous approaching maturity (Figs. 6 and 7). The inner integument covers the nucellus completely to form an endostome. The ovules are long-ellipsoidal and the micropyle consists of the endostome at maturity (Figs. 8 and 9). The distal portion of the inner integument is exposed beyond the outer integument.
Winteraceae (T. piperita, T. lanceolata, T. stipitata, and T. insipida) Tasmannia piperita initiates 14- 19 semiglobular ovule primordia. The inner integument is initiated in incurving ovules, as an annular ring around near the apex of the nucellus; the inner integument on the convex side of the funiculus appears to develop more slowly (Figs. 10 and 11). As the ovules are more incurved, the outer integument develops (Fig. 12). In semimature and mature ellipsoidal ovules, the distal lateral margins of the outer integument are decurrent to the funiculus, indicating the hood-shaped outer integument (Fig. 13); the micropyle may consist of the endostome surrounded by the exostome (Figs. 14 - 16). The exostome shows a reverse U-shape in top view (Fig. 16). The dermal cells of the outer integument are much larger than those on the concave side of the funiculus. Seven to 10 ovules are produced in each carpel of 7: lanceolata. In the youngest ovules examined, which are curved at little over 90" to the axis of the funiculus, the inner integument is circular with short distal lobes, and the outer integument is semicircular or hood-shaped (Fig. 17). The distal, lateral margins of the outer integument are decurrent to the lateral portions of the funiculus. As the ovules grow further,
the inner integument always overtops the outer one. The mature ovules are globose-ellipsoidal, and the micropyle is formed by the inner integument (Fig. 18). Ovules of 7: stipitata examined showed very similar development and morphology to those of 7: lanceolata. The distal, lateral margins of the outer integument are decurrent to the lateral portions of the funiculus. The funiculus is longer and more bent to make the ovules strongly anatropous than in 7: laceolata. Ovules of 7: insipida shortly after anthesis, which were collected from flowers with one or two of four to six petals remaining, are anatropous and ellipsoidal (Figs. 19 and 20) as in 7: piperiata. The outer integument shows a reverse omega shape in top view, indicating that the outer integument is hood-shaped (Fig. 20).
Annonaceae (G. macrophyllus, C. odorata var. fruticosa, and S. burahol) Four (G. macrophyllus), six to eight (C. odorata var. fruticosa), and six (S. burahol) ovules are produced in two rows on the placenta. Ovules are formed as semiglobular outgrowths. As ovules begin incurving, the inner integument forms around the nucellus in all species (Fig. 21). Both integuments on the convex side of the funiculus develop later than the other portions (Figs. 22, 23, 26, and 28). The inner integument is circular; the outer integument is semicircular and interrupted on the concave side of the funiculus (Fig. 24). At a semimature stage the ovules are anatropous, and the outer integument encloses the inner integument (Fig. 24). Mature oiules are globose-ellipsoidal and the distal portion of the inner integument are exposed beyond the outer integument such that the micropyle is formed by an endostome (Figs. 25, 27, and 29).
Discussion Previous anatomical studies indicate that the outer integument is lacking on the concave side of the funiculus in most magnolialean families (Swamy 1949; Lampton 1957; Periasamy and Swamy 1961; Bhandari 1963; de Boer and Bouman 1974; Mohana Rao 1975, 1979, 1982, 1983; Endress 1980a, 1980b; Bouman 1984; Prakash et al. 1984, 1992; Johri et al. 1992). The present scanning electron microscope study reveals that the outer integument is hood-shaped in several species of the Annonaceae, Eupomatiaceae, and Winteraceae. Similar outer integument morphology occurs in the Magnoliaceae (Matsui et al. 1993; Umeda et al. 1994). As regards the evolutionary trend of angiosperm ovules, many authors (e.g., Eames 1961; Bouman 1984; Cronquist 1988; Johri et al. 1992) believe that ovules lacking outer integuments on the concave side of their funiculi are extremely derived from those with annular outer integuments. However, recent developmental studies (Matsui et al. 1993; Umeda et al. 1994) demonstrated that in Magnoliaceae the hood-shaped outer integument, together with the funicular outgrowth, forms an outer envelope complex, although it was erroneously considered to be annular (e.g., Bouman 1984). In addition, the present study shows that the outer integument in the three primitive families has no indication that the hood-shaped integument is a modification of the cupular one.
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Figs. 21-29. Scanning electron micrographs of ovules at successive developmental stages. Figs. 21 -25. Goniothalarnus macrophyllus. Figs. 26 and 27. Cananga odorata var. fruticosa. Figs. 28 and 29. Stelechocarpus burahol. Fig. 21. Incurving ovule with initiating inner integument. Fig. 22. Annular inner integument, which develops slowly on the convex side of funiculus. Fig. 23. More incurved ovule with developing semiannular outer integument. Fig. 24. Older ovule with integuments enclosing nucellus. Fig. 25. Mature ovule with exposed endostome. Figs. 26 and 28. Incurved ovules with annular inner integuments and initiating semiannular outer integuments. Figs. 27 and 29. Mature ovules with exposed endostomes. e, endostome; i , inner integument; o, outer integument. Scale bars = 50 pm.
Recent morphological and molecular systematic studies (e.g., Donoghue and Doyle 1989; Loconte and Stevenson 1991; Chase et al. 1993; Qiu et al. 1993) proposed phylogenetic trees in which the Magnoliales sensu Cronquist (1988) is a polyphyletic assemblage of families. Doyle and Donoghue (1993) placed Winteraceae in a separate clade termed winteroids. Based on these trees, it seems likely that the hood-shaped outer integument, like anatropy and crassinucellus, in members of the Magnoliales is a shared ancestral (symplesiomorphic) rather than advanced character state. Further, it can be predicted that the outer integument is
basically hood-shaped throughout angiosperms with anatropous ovules. Other phylogenetic analyses based on morphological and integrated morphological and rRNA data indicate that paleoherbs are basal in angiosperms (e.g., Taylor and Hickey 1992; Doyle et al. 1994). Paleoherbs such as Chloranthaceae and Piperaceae have orthotropous ovules, while Nymphaeaceae has anatropous ovules (Bouman 1984; Johri et al. 1992; van Miegroet and Dujardin 1992). Precise phylogenetic relationships will be useful to determine whether orthotropous ovules of the paleoherbs are primitive or derivative.
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Stebbins (1974), Retallack and Dilcher (198 I), and Stewart and Rothwell(1993) proposed the hypothesis that the outer integument is homologous to the ovuliferous sporophyll of the glossopterid seed fern. In this gymnosperm, the three-dimensionally architectured female reproductive organ consisted of unitegmic, orthotropous ovules on the inner surface of an infolding sporophyll and a hypothetically carpelhomologous vegetative leaf subtending or bearing the sporophyll on the adaxial side. Kato (1990, 1991) speculated that anatropy was derived from leaf hyponasty by heterochrony. The occurrence of the hood-shaped, or bilaterally symmetrical bladelike, outer integument in the three primitive families described here, as well as in Magnoliaceae (Matsui et al. 1993; Umeda et al. 1994), is consistent with those hypotheses about the phylogenesis of angiosperm ovules. There is an alternative hypothesis of the phylogenetic polarity from orthotropous ovules with cupular outer integuments to anatropous ovules (Bocquet and Bersier 1960; Taylor 1991). The latter ovules are most common in putatively primitive angiosperms, while the former are much fewer (Davis 1966; Bouman 1984). Taylor (1991), following Crane (1985), considered Bennettitales and other fossils to be the sister group to angiosperms. Nishida (1994) showed that the outer envelope of bennettitalean ovules, which was believed by Taylor (1991) to be homologous with the outer integument of angiosperms, is a thin membrane and argued that they are not homologous. The micropyle is formed only by an endostome in most primitive magnolialean angiosperms (Swamy 1949; Periasamy and Swamy 1961; Bhandari 1963; de Boer and Bouman 1974; Mohana Rao 1979, 1983; Endress 1980a; Prakash et al. 1984, 1992; Johri et al. 1992; present study). The ovules with the overtopping inner integument of E. laurina, examined here, are more similar to Mohana Rao's (1983) description and illustration of sectioned ovules than to Kamelina's (198 1). Presumed phylogenetic enlargement of the outer integument, along with the appearance of a funicular outgrowth as in Magnoliaceae (Matsui et al. 1993; Umeda et al. 1994) or the fusion of the margins of the outer integument into a cupular one, might have given rise to more complete protection of ovules. Associated with this, bistomic micropyles might have been produced. A similar polarity of the micropyle was hypothesized by Taylor (1991), based on the putative homology between the outer envelope of Bennettitales and the outer integument of angiosperms. This comparison is not supported by Nishida (1994).
Acknowledgements We are grateful to Dr. L.W. Jessup and Dr. P.D. Bostock, Queensland Department of Primary Industries, Professor G.J. White, Dr. J.B. Williams, and Dr. N. Prakash, New England University for their kind assistance on field trips, and the directors of Bogor Botanical Garden and Mt. Coot-tha Botanical Garden for the flower materials. We also thank the Indonesian Institute of Sciences (LIPI) and the Research and Development Centre for Biology, LIPI, for sponsorship for a field study in Irian Jaya. This study was in part supported by grant-in-aid No. 04041034 for the Monbusho International Scientific Research Program, and No. 07640935 for Scientific Research from the Ministry of Education, Science and Culture.
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