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Comparative Floral Structure and Systematics in Apodanthaceae

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Comparative Floral Structure and Systematics in Apodanthaceae Plant Syst. Evol. 245: 119–142 (2004) DOI 10.1007/s00606-003-0090-2 Comparative floral structure and systematics in Apodanthaceae (Rafflesiales) A. Blarer1, D. L. Nickrent2, and P. K. Endress1 1Institute of Systematic Botany, University of Zurich, Zurich, Switzerland 2Southern Illinois University, Carbondale, Illinois, USA Received September 15, 2003; accepted September 30, 2003 Published online: Feburary 12, 2004 Ó Springer-Verlag 2004 Abstract. Comparative studies on floral morphol- Introduction ogy, anatomy, and histology were performed to identify shared features of the genera of Apo- Apodanthaceae (Rafflesiales) are endopara- danthaceae (Rafflesiales): Apodanthes, Pilostyles, sitic, achlorophyllous herbs. Their vegetative and Berlinianche. Berlinianche was studied for the endophyte, often compared to a fungal myce- first time in detail and its affinity to Apodanth- lium, resides in the host, as in other Raffle- aceae was confirmed. It has a previously unde- siales. The aerial portions of the plant consist scribed hair cushion on the inner perianth organs of flowering shoots, each with a single flower, and inaperturate pollen. Shared features of mem- which burst out of the host’s cortex during bers of Apodanthaceae are: unisexual flowers; development. Flowers are less then a centi- three (or four) alternating di-/tetra- or tri-/hexa- metre across. Apodanthaceae contain three merous whorls of scales of which the inner one or genera: Apodanthes with one or several species two correspond to a perianth; a synandrium with in the Neotropics, Pilostyles with about 20 pollen sacs typically arranged in two rings; opening by a dehiscence line between the two species in the Neotropics, Mediterranean rings of pollen sacs; large vesicular hairs above southwestern Asia, and subtropical south- the synandrium; a gynoecium with four united western Australia, and Berlinianche with two carpels; inferior and unilocular ovaries with four species in subtropical eastern Africa (Kuijt parietal placentae, ovules tenuinucellate, anatro- 1969, Meijer 1993). The reproductive organs pous with two well developed integuments, ori- of these parasites are preceded by three or ented in various directions; a nectary disk. four series of scales. Apodanthes is known to Apodanthaceae share some special structural parasitize Flacourtiaceae (now in Salicaceae; features with Malvales. Chase et al. 2002, APG II 2003), such as Casearia (Gomez 1983, Eliasson 1994) and Key words: Apodanthaceae, Apodanthes, Berlin- Xylosma (Gentry 1993), and representatives of ianche, eudicots, Malvales, parasitic plants, Burseraceae and Meliaceae (Gomez 1983). Pilostyles, Rafflesiales. 120 A. Blarer et al.: Apodanthaceae Pilostyles parasitizes a wide range of Faba- Materials and methods ceae (de Vattimo 1971), and Berlinianche The following species were studied: is restricted to Amherstieae of Fabaceae Apodanthes caseariae Poit.: D. L. Nickrent (Verdcourt 1998). 3007; along trail opposite bus stop and housing Most traditional classifications placed development, ca. 1.0 km S of Rio General, Costa Rafflesiales in or near Aristolochiales (Melchior Rica, buds and open flowers, male and female, 1964, Hutchinson 1969, Takhtajan et al. 1985, parasitic on Casearia sp. (Salicaceae). Takhtajan 1997). In the absence of molecular Pilostyles thurberi A. Gray: D. L. Nickrent data, Rafflesiales were placed as an unresolved 2993; near Benjamin, Texas, USA, buds and open group together with several magnoliid families flowers, male and female, parasitic on Dalea at the base of the angiosperms (APG 1998). frutescens A. Gray (Fabaceae). Later, Hydnoraceae were found to be related to Berlinianche aethiopica (Welw.) Vattimo-Gil: Piperales (Nickrent et al. 2002) and distant A. Blarer 192 (male), 193 (female); near Harare, Zimbabwe, buds and open flowers, parasitic on from the other Rafflesiales. In the APG II Julbernardia globiflora (Benth.) Troupin (Faba- (2003) classification, Rafflesiales (without Hyd- ceae). noraceae) are assigned to a group of taxa of Male and female flowers at anthesis (postan- uncertain position among angiosperms. In a thetic female flowers of Pilostyles) and buds shortly molecular study based on a three gene analysis before anthesis, when available, were fixed in FAA (but only nuclear SSU rDNA sequences for and stored in 70% ethanol or shock-frozen in Rafflesiales), Rafflesiales were found to be liquid nitrogen and stored at )80 °C. They were monophyletic and were placed in eudicots near investigated with light microscopy (LM) and scan- Malvales (Nickrent 2002). Phylogenetic rela- ning electron microscopy (SEM). Specimens were tionships of Apodanthaceae relative to other embedded in Kulzer’s Technovit 2-hydroethyl families of Rafflesiales has been addressed in methacrylate or paraplast (Igersheim 1993, Igers- two molecular studies (Blarer et al. 2000 and heim and Cichocki 1996) and sectioned with a Microm HM 335 rotary microtome and conven- unpublished results). Previous studies of floral tional microtome knife (grade D); both transverse morphological and anatomical features of and longitudinal sections were with a few excep- Apodanthaceae were only fragmentary, not tions cut at 5 lm. Sections were stained with comparative and without use of serial ruthenium red and toluidine blue (Weber and microtome sections or the SEM. Taxa thus Igersheim 1994) and mounted in Histomount on studied include: Pilostyles (Guillemin 1834, glass slides. Some materials (especially male flowers Solms-Laubach 1874b, as Apodanthes in of Apodanthes) were difficult to section with either Robinson 1891, Endriss 1902, Harms 1935, paraffin or paraplast embedding due to heavily Kummerow 1962, Rutherford 1970), Berlinian- tanniferous tissues. Standard specimen preparation che (as Pilostyles: Solms-Laubach 1874b, procedures were used for osmium tetroxide impreg- Harms 1935) and Apodanthes (Harms 1935; de nated samples for SEM studies. Vouchers and Vattimo 1955, 1956, 1971, 1978; Gentry 1973). slides are deposited at the Institute of Systematic Botany of the University of Zu¨rich (Z), Switzer- In the majority of these studies, neither serial land. microtome sections nor the SEM were utilized. Only in the study of ovules and seeds in Apodanthes and Pilostyles and ovules in Results Berlinianche by Bouman and Meijer (1994) was SEM used. Androecium and gynoecium are surrounded The objective of this study is to compare by a number of sterile organs. As it is the floral structure of the three genera of uncertain whether they are all perianth organs Apodanthaceae and to discuss relationships of (tepals, or sepals and petals) or whether the the genera and the position of Apodanthaceae outer ones are bracts (and thus not floral in Rafflesiales. organs), we refer to them as ‘‘scales’’ in the A. Blarer et al.: Apodanthaceae 121 Results, before we give an interpretation in the scales of the three whorls are inserted at Discussion. different levels. The inner whorl is inserted at Scales of Berlinianche aethiopica. Anthetic the level of the nectary, the outer one close to flowers are globose or ellipsoid, firm, red, and the base of the floral shoot. A sinusoid, six- odourless (Fig. 1A). The scales are arranged in angled, thick nectary disk surrounding the several series. They can be interpreted as three reproductive organs is shaped by the bases of whorls (see Discussion). Scale number changes the inner scales (Figs. 2, 4). from three in the outer whorl to six in the other In the outer two whorls, vascular bundles whorls. Of the six scales of the middle whorl, are not visible. In the scales of the inner whorl, three alternate with the scales of the outer transverse sections show multiple small vascu- whorl, and three are in front of those of the lar bundles in the lower third of their length. outer whorl. The six scales of the inner whorl However, small vascular bundles are found at alternate with those of the middle whorl the insertion sites of all whorls. The vascular (Fig. 10A). We did not find variation in scale bundles are thin and few-celled in TS (Figs. 2, number except in the inner whorl, which is 4). sometimes heptamerous (Fig. 5). Aestivation Stomata could not be found in the scales in all whorls is imbricate: in the outer whorl it but are present on the nectary disk. The scales is sometimes contort; in the middle whorl three are rich in tanniferous tissue. Neither cells with scales cover the other three, the former are starch or oxalate crystals, nor oil and mucilage those that alternate with those of the outer cells were found. whorl; in the inner whorl, aestivation is Reproductive structures in male flowers of sometimes contort. However, aestivation in Berlinianche aethiopica. The androecium con- the outer and inner whorl is somewhat irreg- sists of a tubular synandrium, which surrounds ular and there is no predominant pattern the sterile gynoecium. Anthers and filaments (Fig. 10A). The scales are free. They are are not differentiated. The synandrium con- broadly ovate to elliptic, rounded at the apex, tains two rings of c. 15 extrorse pollen sacs have thin margins (one to two cell layers each. The upper ring has a slightly smaller thick), and are persistent. The scales of the diameter. The number of pollen sacs may differ inner whorl differ from the other ones in their slightly in the two rings and they are neither thicker insertion area. In addition, they are strictly superposed nor alternating with each covered with elongate, one- to four-celled, other. Opening is by a continuous dehiscence uniseriate hairs adaxially at the base. The line between the two rings of pollen sacs. In the Fig. 1. Flowers of Apodanthaceae. A Berlinianche aethiopica, male (A. Blarer 192; photo by same). B Pilostyles thurberi, male (D. L. Nickrent 2293; photo by K. Robertson). C Apodanthes caseariae, male (D. L. Nickrent 3007; photo by same). Scale bars c. 1 mm 122 A. Blarer et al.: Apodanthaceae Fig. 2. Berlinianche aethiopica, anthetic male flowers with open pollen sacs. A Schematic LS. B–Q TS series. B Level of stylar head. C Level of vesicular hairs above androecium. D Level of pollen sacs. E Level of free staminal tube. F Level of hair cushion on inner perianth organs.
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