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Review of the Sporoderm Ultrastructure of Members of the Asterales S ISSN 0031-0301, Paleontological Journal, 2006, Vol. 40, Suppl. 5, pp. S656–S663. © Pleiades Publishing, Inc., 2006. Review of the Sporoderm Ultrastructure of Members of the Asterales S. V. Polevova Biological Faculty, Moscow State University, Leninskie gory 1, Moscow, 119992 Russia e-mail: [email protected] Received March 23, 2006 Abstract—Palynomorphological characteristics of the order Asterales are discussed. Particular attention is paid to the pollen morphology of basal families of this group and to that of problematic taxa that are considered as sister groups to the group under study. Ultrastructurally similar sporoderms of several families, including (1) Asteraceae, Calyceraceae, and Goodeniaceae; (2) Campanulaceae, Phellinaceae, and Menyanthaceae; (3) Rousseaceae, Abrophyllaceae, and Columelliaceae, are described. Pollen grains of Alseuosmiaceae and Stylidiaceae show unique ultrastructural features of the exine. DOI: 10.1134/S0031030106110128 Key words: Asterales, pollen grains, ultrastructure, phylogenetic systematics. INTRODUCTION MATERIAL AND METHODS At different times, concepts of the group of Aster- Pollen grains of 18 members of 12 families were aceae and its relatives has been considered to include studied. The material was received from the herbarium different families. These variants concerned a distinct of Komarov Botanical Institution of the Russian Acad- circle of taxa. Thus, the system of Takhatajan (1997) emy of Sciences, St. Petersburg. included the subclass Asteridae with 14 families; the (1) Family Goodeniaceae: Brunonia australis system of Thorne (2000) included the suborder Astera- R. Brown and Dampiera eriocephala Vriese. nae with nine families. (2) Family Columelliaceae: Columellia sericea Recently, relationships of Asteraceae have been sig- F.A. Humbolt, A.J.A. Bonpland et C.S. Kunth. nificantly clarified by extensive genosystematic studies. (3) Family Calyceraceae: Calycera eryngioides For example, rbcL sequencing of members of the gen- Remy, Gamocarpa caespitosa R.A. Philippi ex era Carpodetus, Abrophyllum, and Cuttsia, which were C.M. Hicken, and Acicarpha pinnatifida Miers. earlier assigned to the Saxifragaceae sensu lato, has (4) Family Campanulaceae: Platycodon grandiflo- revealed that they compose a separate family, the Rous- rum A. DeCandol. seaceae, and are close to the clade Asterales (Gustafs- Ixerba brexioides son and Bremer, 1997). The genera that currently com- (5) Family Ixerbaceae: A. Cun- pose the families Alseuosmiaceae, Phellinaceae, and ningham. Argophyllaceae, were earlier assigned to different fam- (6) Family Vahliaceae: Vahlia sp. ilies of the Hydrangeales. Karehed et al. (1999) place (7) Family Phellinaceae: Phelline erubescens them between the Campanulaceae- and Stydiaceae- H. Baillon et F.R.R. Schlechter. relations. The order Asterales is considered in this (8) Family Eremosynaceae: Eremosyne pectinata broad sense on the Angiosperm Phylogeny Website S.L. Endlicher. (Stevens, 2001). In addition, this study considers some (9) Family Stylidiaceae: Stylidium graminifolium members of the families that occupy the basal position C.L. Willdenow and Stylidium adpressum Bentham. to Euasterids II, which were discussed in relation to the position of the order Asterales in the dicot system (Sol- (10) Family Argophyllaceae: Argophyllum nitidum tis et al., 2005). J.R. Forster et G. Forster and Corokia buddleioides A. Cunningham. Taxa in the basal part of the systems proposed are of (11) Family Rousseaceae: Abrophyllum ornans particular interest. As a rule, these genera have repeat- (F. Mueller) Bentham and Cuttsia viburnea F. Mueller. edly been moved from order to order in different sys- tems, because they were insufficiently understood. (12) Family Alseuosmiaceae: Alseuosmia linariifo- Therefore, more morphological substantiation is lia A. Cunningham. needed for the verification of their assignment to one All the samples studied were acetolized, described, group (clade) or another. and photographed using an Axioplan-2 light micro- S656 REVIEW OF THE SPORODERM ULTRASTRUCTURE OF MEMBERS OF THE ASTERALES S657 T E E T E T Fl Ect End Fl Ect Fl Ect End End (a) (b) (c) E E T T E T Ect Ect Fl Fl Fl Ect End End End (d) (e) (f) E T T T Ect Ect Ect Fl End End End (g) (h) (i) Fig. 1. Sporoderm ultrastructure, schematic: (a) cavate pollen grains; (b) noncavate pollen grains; (c) echinolophate pollen grains; (d) pollen grains with a double columellate layer; (e) Menyantaceae-type of sporoderm; (f) Campanulaceae-type of sporoderm; (g) noncolumellate medullary sporoderm; (h) columellate-like sporoderm; and (i) simple columellate sporoderm; (a, b, c) sporo- derms of the Asteraceae; (e) sporoderms of the Menyantaceae; (f) sporoderms of the Campanulaceae and Phellinaceae; (g) sporo- derm of the Stylidiaceae; (h) sporoderm of the Alseuosmiaceae; and (i) sporoderms of the Columelliaceae, Rousseaceae, Abrophyl- laceae, and Ixerbaceae. Designations: (End) endexine; (Ect) ectexine; (Fl) foot layer; (T) tectum; and (E) echina (spine or spinule). scope in glycerol-jelly slides. Nonacetolized pollen ectexine contains a vast cavity between the columellae grains were studied under Hitachi and Camscan scan- and foot layer, so that the ectexine retains its integrity ning electron microscopes. For transmission electron only along the apertural margins. In some members, the microscopy, all samples of pollen grains were stained foot layer is partially (Calendula; Kosenko and with 2% OsO4, processed in alcohol, stained with uranyl Polevova, 2001) or completely (subfamily Barnadesio- acetate in 70% alcohol, dehydrated, put in acetone, and ideae) reduced, and hollow chambers of various sizes embedded in epoxy mixture (Weakley, 1972). Ultrafine and shape occur in the columellae. Noncavate pollen sections were made using an ultramicrotome, addition- grains (Fig. 1b) have a double columellate layer and ally stained after Reynolds (Geyer, 1973), and studied occur in different tribes, particularly often in the sub- under a Jeol-100 transmission electron microscope. family Cichorioideae. The morphological diversity of the noncavate ectexine is expressed in various shape and arrangement of inner columellae. Thus, echinolo- RESULTS: THE MAJOR MORPHOLOGICAL phate pollen grains have slender (high and thin) inner CHARACTERISTICS OF POLLEN GRAINS columellae that are only present under spines and OF THE FAMILIES STUDIED ridges (lophae) (Fig. 1c). Spinulose noncavate pollen Asteraceae grains have massive (thick) inner columellae, which are densely positioned and, in the upper part, are trans- Pollen grains of the Asteraceae have long been stud- formed into a reticulate infratectum and into outer col- ied, and a considerable bulk of information about their umellae covered with a tectum. Pollen grains of all morphology has been obtained (Skvarla et al., 1977; Asteraceae have a well-developed endexine, which Meyer-Melikian et al., 2004). Pollen grains of the often becomes thicker and layered in the apertural Asteraceae are three-colporate, medium-sized or large, regions (Polevova, 2004). ellipsoidal or spheroid, more rarely, hexagonal (some members of the tribes Cichorieae, Liabeae, and Ver- nonieae). The colpi are usually long, occasionally Goodeniaceae shortened (Ambrosia and Xanthium) or indistinct (some Cichorieae). The sculpture is echinate (spinulose or spi- In terms of pollen morphology, the majority of gen- nose) or echinolophate. The majority of representatives era of the Goodeniaceae are most similar to the Aster- of the family have cavate pollen grains (Fig. 1a). The aceae (Fig. 1d). Pollen grains of the Goodeniaceae are PALEONTOLOGICAL JOURNAL Vol. 40 Suppl. 5 2006 S658 POLEVOVA Plate 9 µ 10 µm 2 3 m 3 µ 1 10 m 15 µm 3 µm 5 6 3 µm 4 3 µm 7 3 µm 8 µ 9 3 m 6 µm 10 µ 11 3 m 12 10 µm 3 µm 3 µm 13 14 10 µm 3 µm 15 10 µm 16 17 PALEONTOLOGICAL JOURNAL Vol. 40 Suppl. 5 2006 REVIEW OF THE SPORODERM ULTRASTRUCTURE OF MEMBERS OF THE ASTERALES S659 three-colporate, ellipsoidal–nearly spherical, medium- surface is spinose or spinulose (Campanuloideae; Pl. 9, sized, or small (in Dampiera), and arranged in square fig. 11), striate or reticulate (Lobelioideae), or smooth tetrads in members of Leschenaultia. The colpi are (Cyphioideae and Sphenocleiodeae; Pl. 9, fig. 17). The long, the ores are narrowly ellipsoidal, equatorially general structural pattern of the ectexine resembles that elongated or with an indistinct outline (Dampiera). The of the Menyanthaceae (Pl. 10, fig. 14); two rows of col- surface sculpture (Pl. 9, figs. 5, 10) is verrucate with umellae of identical height and width are seen in sec- numerous perforations, striate (Dampiera and Anthod- tions. The inner columellae are more loosely arranged, ium), or pitted (Leschenaultia). The ectexine has a dou- they may be rooted in the endexine rather than in the ble columellate layer (Pl. 10, figs. 5, 10), while the foot layer (foot layer is absent) (Parishella, Codonop- endexine is thinner than the foot layer to a varying sis, Platycodon, and Ostrowskia). The outer row is con- degree. Members of the genus Dampiera have a simple stituted by columellae that are separated by densely columellate ectexine and an extremely thin endexine. spaced narrow channels. The endexine is usually well developed (Dunbar, 1984; Shrestka and Tarasevich, 1992; Tarasevich and Shrestka, 1992). Calyceraceae The Calyceraceae are very similar in pollen mor- phology to the Asteraceae and Goodeniaceae (Fig. 1d). Phellinaceae Pollen grains of the Calyceraceae are three-colporate, The family Phellinaceae is virtually
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