Blackwell Science, LtdOxford, UKBOJBotanical Journal of the Linnean Society0024-4074The Linnean Society of London, 2004? 2004 145? 437443 Original Article SYSTEMATIC POSITION OF AUSTROTAXUS A. V. F. CH. BOBROV Botanical Journal of the Linnean Society, 2004, 145, 437–443. With 3 figures Seed morphology and anatomy of Austrotaxus spicata (Taxaceae) and its systematic position ALEXEY V. F. CH. BOBROV1*, ALEXANDER P. MELIKIAN2, MIKHAIL S. ROMANOV3 and ALEXEY N. SOROKIN3 1 Department of Recent Deposits and Pleistocene Palaeogeography, Geographical Faculty, and Department of Higher Plants, Biological Faculty, M. V. Lomonosov Moscow State University, 119992, Moscow, Russian Federation 3 Main Botanic Garden of Russian Academy of Sciences, 127276, Botanical St., 4, Moscow, Russian Federation 2 Received August 2002; accepted for publication December 2003 The anatomy and ultrastructure of seed envelopes of a New Caledonian endemic Austrotaxus spicata were examined for the first time. The systematic position and phylogenetic relations of Austrotaxus were analysed in light of these data. The structure of aril and spermoderm were investigated to demonstrate the similarities with Phyllocladus as well as with Taxus and Pseudotaxus. On the basis of all female reproductive organ characters, Austrotaxus appeared to be fairly isolated and its placing in the independent family Austrotaxaceae was confirmed from the standpoint of comparative anatomy of the seed coat. Taking into consideration that the heterobathmy of features can be the most distinctively traced in the structure of reproductive organs, evaluating the extent of evolutionary advancement of Austrotaxus seems to be rather difficult. However, it is evident that the relationship of Austrotaxus either with Taxaceae or with Podocarpaceae s.l. is considerably remote. © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society, 2004, 145, 437–443. ADDITIONAL KEYWORDS: aril – Austrotaxaceae – Phyllocladaceae – phylogeny – Podocarpaceae – Podocarpales – seed coat – Taxales. INTRODUCTION The flora of New Caledonia contains abundant endemics. Many monotypic genera, both gymnosperms and flowering plants, pose problems for botanists. Austrotaxus spicata Compton can be added to these taxa. The problem of Austrotaxus and its phylogenetic relations has been constantly disputed since its first description (Compton, 1922) to the present day. There are three interpretations of its systematic position and phylogeny. Compton (1922), Saxton (1934) and many other scientists (Koidzumi, 1932; Florin, 1944, 1948b, 1951, 1954; Janchen, 1949; Sporne, 1967; Gaussen, 1979; Hart, 1987; Page, 1990) included Austrotaxus in the family Taxaceae s.l. Compton (1922) pointed out the close similarities in seed morphology of representaET AL. *Corresponding author. E-mail: avfch_bobrov@mail.ru tives of Austrotaxus, Taxus L. and Amentotaxus Pilg. Amentotaxus also resembles Austrotaxus in habit, leaf morphology, terminal position of seed on the axillary pedicle and presence of scales at the base of a seed (Bobrov, 1997d). Based on studies of embryology of Austrotaxus and its reproductive organs, Saxton (1934) considered the genus to be an archetype of the genus Taxus. Some features are present in both genera, e.g. late aril development (it never fuses with the spermoderm and covers most of the seed), morphological specialities of pollen grains, gametogenesis and embryogeny. As Saxton assumed, the aril in Taxus, morphologically slightly reduced, its specialized peltate microsporophylls as well as other significant traits of reproductive and vegetative organs were derived from the morphological peculiarities of Austrotaxus. Li (1953), Greguss (1955) and Takhtajan (1956) placed Austrotaxus spicata in the Podocarpaceae s.l., © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society, 2004, 145, 437–443 437 438 A. V. F. CH. BOBROV ET AL. based on close similarities in wood structure of Austrotaxus and Podocarpus L’Hérit. ex Pers. s.l., the existence of microstrobilate aggregations in Austrotaxus and two species of Podocarpus s.l. (P. andina Poepp. ex Endl. and P. taxifolia Humb., Boupl. & Kunt), and their common geographical distribution (Austrotaxus and podocarps occur chiefly in the Southern Hemisphere whereas taxads grow mostly in the Northern). Takhtajan (1956) inclined to support Nakai’s (1938) opinion in placing the genus in its own family Austrotaxaceae. In one of his last papers, Florin (1958) came to the same conclusion. Takhtajan (1986) acknowledged the family Austrotaxaceae Nakai, including it, however, in the order Taxales. Vegetative characters and peculiar leaf anatomy shows clearly that Austrotaxus is intermediate between taxads and podocarps (Ferre, Rouane & Woltz, 1977; Hu, Wang & Wang, 1992). It is impossible therefore to avoid the conclusion that the data on structural specialities of Austrotaxus alone cannot resolve the problem of its systematic position in relation to other coniferous plants. Recently, anatomical features of seeds have been used as characters in plant taxonomy and phylogeny, but in the case of Austrotaxus they have been apparently ignored by investigators. Data on ovules and seed morphology of Austrotaxus, in Schnarf ’s (1937) monograph, appeared to be taken from Saxton’s (1934) article. Studies conducted by Woltz & Bailly (1982) brought some light on the morphology and anatomy of Austrotaxus embryos and seedlings, but the anatomical structure of the seed envelope remains uninvestigated. In order to bridge this gap and to reveal the significance of anatomical traits of seeds in solving systematic and phylogenetic problems, the present study was carried out and the seed morphology, anatomy and ultrastructure of Austrotaxus spicata were investigated. MATERIAL AND METHODS The material was very kindly provided by Prof. E. S. Chavchavadze, the Head of the Botanical Museum, the Komarov Botanical Institute, Russian Academy of Science, Saint-Petersburg. Prior to anatomical investigations, dry seeds were soaked in Strasburger’s mixture and than embedded in paraffin. The seeds were sectioned in transverse and longitudinal directions in relation to their longitudinal axis. Sections with a thickness of 10–20 mm were obtained by using a slide microtome. All sections were stained with phloroglucinol and hydrochloric acid to reveal details of lignification of cell walls in different topographical zones of the seed coat. Sections were preserved in glycerine. All experimental investigations were executed in accor- dance with standard morphological and anatomical procedures (Bondartzev, 1954; Prozina, 1960; O’Brien & McCully, 1981). Anatomical figures were prepared from transverse sections, which are the most informative in the investigation of seed coat anatomy (Schnarf, 1937). RESULTS MORPHOLOGY The brown seed is orthotropous (Fig. 1A), up to 25 mm long and 10–12 mm thick, with undulating surface covered (except in the micropyle area) with the smooth brownish-orange aril, which is not fused with the seed coat (Fig. 1C, D), ellipsoidal, but in cross section, round or oval-quadrangular (Fig. 1C). The micropyle is narrow and bilobed (Fig. 1B). Five to ten decussate scales are situated at the base of the seed. The seed usually has a long pedicle of axillary origin. ANATOMY Aril structure (Fig. 2) varies depending on the region being examined. In the central part, the aril adheres tightly to the seed coat while in the upper part it forms a free collar rising above the micropyle. In the central part, the aril is composed of 23–27 cell layers, differentiated in the following manner. Almost square in outline, epidermal cells are characterized by heavily a sc A C a sc B D Figure 1. Morphology of the seed of Austrotaxus spicata. A, general view. Scale bar = 6 mm. B, view from micropyle. Scale bar = 3.6 mm. C, schematic diagram of longitudinal section of seed. D, schematic cross-section of seed. Abbreviations: a, aril; sc, seed coat. © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society, 2004, 145, 437–443 SYSTEMATIC POSITION OF AUSTROTAXUS 439 oe e oh ext h par par gr in mst scl ih ie Figure 2. Cross-section of the aril of Austrotaxus spicata. Abbreviations: oe, outer epidermis; oh, outer hypodermis; ih, inner hypodermis; ie, inner epidermis; gr in, granular inclusion. thickened outer tangential walls (their thickness accounts for two-thirds of the total cell height) and transparent cytoplasm. The cuticle is rather thin. The hypodermis consists of small cells also with clear cytoplasm but with the cell walls only slightly thickened. Three zones can be readily distinguished in the main aril-forming tissue. The three or four outermost celllayers are represented by large parenchymatous cells with small intercellular ducts. Their walls are weakly thickened; cell content is colourless. Minute thinwalled cells filled with green granulated contents form 15–17 middle layers. Larger cells with weakly coloured cytoplasm and thickened dark orange walls constitute the innermost two or three layers. The inner epidermis is made up of very small cells with slightly and uniformly thickened walls; both walls and cytoplasm are colourless. A thin cuticle is present. No vascular elements were found. At the sheath-like part surrounding the micropyle, the aril consists of four or five cell layers. Outer and inner epidermises are fairly close in structure, being composed of large cells with heavily thickened outer tangential walls covered with relatively thin cuticle. The transitional zone between ground tissues is represented by two or three layers of markedly compressed thin-walled tannin-containing cells. The total number of cell layers forming the seed coat (Fig. 3) is 21–25. Exotesta consists of an outer epidermis followed by a hypodermal zone. Epidermal cells are large and radially elongated with pronounced Figure 3. Cross-section of the seed coat of Austrotaxus spicata. Abbreviations: e, epidermis; h, hypodermis; scl, sclerenchyma; par, parenchyma; ext, exotesta; mst, mesotesta. thickening of radial and especially outer tangential walls. Cell lumina are triangular in outline. A thin cuticle is present. There are two or three hypodermal layers of colourless parenchymatous cells with evenly thickened walls. The mesotesta may be divided into two zones – the outer parenchymatous and the inner sclerenchymatous. The former is represented by four to five layers of thin-walled tanniniferous cells. Small tightly placed cells are polygonal in outline, have uniformly thickened walls and form 14–16 layers of the sclerified zone. In the four ‘angles’ of the seed the thickness of sclerenchyma approaches 22–24 cell layers. The total number of cell layers here is about 29– 33. Endotesta is obliterated. DISCUSSION RELATIONSHIPS WITH PODOCARPACEAE S.L. The results of the present investigation indicate that in seed envelope structure, Austrotaxus has some affinity with the Taxaceae s.l. as well as with Podocarpaceae s.l., perhaps a little closer to the latter. Analysing previously published data on aril and seed coat structure of taxads and based on our own examination of Taxus, Torreya Arn., Amentotaxus, Cephalotaxus Siebold & Zucc. ex Endl. seed coat structure as well as more than 100 Podocarpaceae species from all 18 genera (sensu Page, 1990), we deduce that Austrotaxus is close to those members of the Podocarpaceae s.l. that have orthotropous ovules and seeds with reduced aril (Phyllocladus Rich. & Mirb.) or lack an aril (Microstrobos J. Garden & L. A. S. Johnson = Pherosphaera W. Archer). © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society, 2004, 145, 437–443 440 A. V. F. CH. BOBROV ET AL. The genus Microstrobos is undoubtedly isolated due to extreme specialization; its connection with Phyllocladus and Austrotaxus is hypothetical and hardly probable. In contrast, a number of Phyllocladus species and Austrotaxus share certain features of aril anatomy, namely: large-celled external epidermis with heavily thickened tangential walls, the presence of an outer and inner hypodermis with tannin-containing cellwalls and/or cavities, and the complete absence of a vascular system (Bobrov, Melikan & Yembaturova, 1999). To a certain extent, Austrotaxus and the most primitive representatives of the genus Phyllocladus resemble each other. The exotesta of both is well differentiated, with the epidermis made up of large cells and ‘stony’ hypoderm; the mesotesta has two distinct zones – parenchotesta and sclerotesta. However, there are some differences in the seed envelope structure of these two genera. The aril epidermis in Phyllocladus has no stomata; in Austrotaxus the aril parenchyma is differentiated distinctively, whereas in most of the seven Phyllocladus species studied it is homogeneous; the parenchotesta is situated to the periphery of the sclerotesta in the Austrotaxus’s mesotesta, whereas in Phyllocladus the location of the tissues tends to be the opposite (Ph. alpinus Hook. f., Ph. hypophyllus Hook. f., Ph. major Pilg., Ph. protractus (Warb.) Pilg.), or the mesotesta is uniformly sclerified (Ph. toatoa Molloy, Ph. trichomanoides D. Don in Lamb.) and there is only one species (Ph. asplenifolius (Labill.) Hook. f) characterized by the same type of zonation as in Austrotaxus (Bobrov et al., 1999). Moreover, Austrotaxus differs greatly from Phyllocladus in some other structural specialities, e.g. axial parenchyma in the secondary xylem (Greguss, 1955; Chavchavadze, 1979), the absence of phylloclades (Eichler, Engler & Prantl, 1889; Compton, 1922; Keng, 1978), and pollen morphology (Phyllocladus grains have pronounced (though markedly reduced) air sacci, whereas Austrotaxus pollen grains have no sacs (Saxton, 1934; Pocknall, 1981)], and overall architecture of male and female reproductive organs [Saxton, 1934; Gaussen, 1974, 1979; Tomlinson, Takaso & Rattenbury, 1989). However, the differences between Austrotaxus and other genera from Podocarpaceae s.l. are even stronger. Most podocarps have an epimatium or seeds covered by testa and tegmen (Bobrov, 1996; Melikian & Bobrov, 1997a, 2000), features missing in Austrotaxus. Thus the genus can be compared only with arillate Podocarpaceae members. However, the aril in Austrotaxus is radial symmetrical, whereas podocarps (Saxe-Gothaea Lindl., Microcachrys Hook. ex Hook. f., Falcatifolium de Laub., Metadacrydium Baum.-Bod. ex A. V. F. Ch. Bobrov & Melikian, Lagarostrobos Quinn, Lepidothamnus Phil., Corneria A. V. F. Ch. Bobrov & Melikian, Gaussenia A. V. F. Ch. Bobrov & Melikian) possess an asymmetrical aril (Melikian & Bobrov, 1997b, c). Ovules and seeds in Austrotaxus are straight whereas true orthotropous seeds have never been reported in Podocarpaceae s.l. RELATIONSHIPS WITH TAXACEAE S.L. Austrotaxus stands even further apart from Taxaceae s.l. (incl. Taxus, Pseudotaxus W. C. Cheng (= Nothotaxus Florin), Torreya and Amentotaxus) and Cephalotaxaceae. According to our original data (Melikian & Bobrov, 1997c, 2000; Bobrov & Karpun, 1998; Bobrov & Sorokin, 2002), fleshy, vascularized, extremely histologically differentiated, and supplied with resin and/ or secretory ducts the outer seed envelope of Torreya, Amentotaxus and Cephalotaxus (usually defined as ‘aril’, but we incline to consider it an epimatium) fused with the seed coat has almost nothing in common with that of Austrotaxus, which is composed of fewer cell layers, free not only of distinctive topographical zonality, but also of any traces of vascular, resin or secretory system. In addition the aril and seed coat in Austrotaxus do not fuse. Thus, we consider that it is more correct to treat the outer coat of seeds of Amentotaxus, Torreya and Cephalotaxus as an outer integument (Bobrov, 1996, 1997a, b, c, d; Melikian & Bobrov, 1997a, b, c, 2000; Bobrov & Karpun, 1998; Bobrov & Sorokin, 2002). In our opinion, the genera Amentotaxus, Torreya and Cephalotaxus have bitegmic ovules and seeds covered with testa and tegmen and they do not have either an epimatium or aril. The exceptionally peculiar process of ovule development in Torreya and Amentotaxus on the one hand and in Cephalotaxus on the other (Oliver, 1903; Kemp, 1959; Singh, 1961; Keng, 1969) considerably isolates these genera from each other and from the rest of the conifers (with the exception of Nageia Gaertn., Retrophyllum C. N. Page (= Decussocarpus de Laub. s.s.) and Acmopyle Pilg. – Bobrov, 1996, 1997a, b, c, d; Bobrov & Karpun, 1998; Melikian & Bobrov, 1997a, b, c, 2000; Bobrov & Sorokin, 2002). Anatomically the seed envelopes of Austrotaxus seem to be somewhat close to those of Taxus and Pseudotaxus, but the difference between these genera is particularly evident in leaf morphology and anatomy (de Laubenfels, 1953; Hu et al., 1992), structure of stomata (Florin, 1931; Hu et al., 1992), xylem features (Greguss, 1955) and morphology of male reproductive organs (Saxton, 1934; Wilde, 1977; Gaussen, 1979). Even though the aril in Taxus and Pseudotaxus is not vascularized and never fuses with the spermoderm, neither external nor internal hypoderm is differentiated. The seed coat of Taxus and Pseudotaxus differs significantly from that of Austrotaxus in some ultrastructural traits of the exotesta (e.g. in the degree and character of wall thickening in epidermal cells). The mesotesta consists of homogeneous sclerenchymatous tissue (Schnarf, 1937; Florin, © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society, 2004, 145, 437–443 SYSTEMATIC POSITION OF AUSTROTAXUS 441 Table 1. Arillate taxa of Podocarpales and Taxales with orthotropous ovules and seeds. Abbreviations: oe, outer epidermis; oh, outer hypodermis; ih, inner hypodermis; ie, inner epidermis; e, epidermis; h, hypodermis; scl, sclerenchyma; par, parenchyma;//– ‘or’ Features Phyllocladus Austrotaxus Pseudotaxus Taxus Habit Wood parenchyma1 Photosynthetic structures2 trees/shrubs absent phylloclades (amphistomic// hypostomic) monocyclic solitary helical, 30–70, bilateral tall tree scanty to abundant hypostomic leaves to 15 cm long polystems trees//shrubs scanty amphistomic needles to 35 mm long amphicyclic in spikes helical, 1–2 (to 5) perisporangiate shrub scanty hypostomic needles to 25 mm long monocyclic solitary helical, ?, perisporangiate 2 (abaxial) 2–3 (few 4–5) 4–5 (4) 5–9 ellipsoidal with 2 reduced sacci seeds on axils of helical bracts on short shoot covers seed on 1/3–2/3 height spheroidal without sacci solitary terminal seed on long axil shoot polyhedrical without sacci solitary terminal seed on short axil shoot covers seed on 5 /6 height polyhedrical without sacci solitary terminal seed on short axil shoot rounded oe & oh, par; ie e&h scl par 2 rounded oe & oh, par, ie e scl par 2 Stomata2 Microstrobilus position3 Disposition, number and morphology of microsporophylls3 No. of microsporangia per microsporophyll3 Pollen grain morphology4 Structure of female reproductive organs5 Morphology of aril5 Shape of micropyle5 Histology of aril5 Structure of exotesta5 Structure of mesotesta5 Structure of endotesta5 No. of derivatives of vascular bands in seed coats5 bilobed oe & oh, par, ie e&h scl//scl + par//par + scl par//fibres 2 covers seed excepting micropyle bilobed oe & oh, par, ih & ie e&h par + scl obliterated 2 amphicyclic solitary helical, 6–14, peltate covers seed on 2/3–5/4 height 1 Chavchavadze (1979), Greguss (1955); 2Ferre et al. (1977), Florin (1931, 1948a,b), Gaussen (1974, 1979), Hu et al. (1992), Keng (1974), (1978), de Laubenfels (1953); 3Gaussen (1974, 1979), Sporne (1967), Takhtajan (1956), Wilde (1977); 4Pocknall (1981), Saxton (1934), Sporne (1967), Takhtajan (1956); Prof N. R. Meyer-Melikian, pers. comm.; 5original data. 1948a; Bobrov & Karpun, 1998; Bobrov & Sorokin, 2002). Vegetative and reproductive traits of Austrotaxus, Taxus, Pseudotaxus and Phyllocladus are compared in Table 1. SYSTEMATIC POSITION We conclude that based on vegetative and, more importantly, reproductive organs Austrotaxus combines the features of various genera belonging to Taxales and Podocarpales. Taking into account all the data obtained on seed envelope morphology and anatomy, we suggest it is advisable to admit the family status of Austrotaxaceae Nakai 1938 and to keep Austrotaxus in an intermediate position between taxads and podocarps. ACKNOWLEDGEMENTS We thank Prof. E. S. Chavchavadze, the Head of the Botanical Museum, Komarov Botanical Institute, Russian Academy of Science, Saint-Petersburg (LE) for the supply of specimens for our investigations. This investigation was carried out in the framework of the research project STRUCTURA SEMINUM & FRUCTUM PLANTARUM SPERMATOPHYTORUM INFERIORUM PROJECT – SSFPSI-project supported by Russian Foundation for Basic Research (RFBR, grants 99-04-48322 and 02-04-49751) at M. V. Lomonosov Moscow State University. We are much indebted to Prof. D. Edwards for the correction of the English text and the anonymous reviewer for positive criticism. © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society, 2004, 145, 437–443 442 A. V. F. CH. BOBROV ET AL. REFERENCES Bobrov AVFCh. 1996. Bitegmal’njie semena predstaviteley porjadkov Podocarpales, Cephalotaxales i Taxales. [Bitegmic seeds of representatives of orders Podocarpales, Cephalotaxales and Taxales]. 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