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Torus-Bearing Pit Membranes in Species of Osmanthus

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Torus-Bearing Pit Membranes in Species of Osmanthus IAWA Journal, Vol. 31 (2), 2010: 217–226 TORUS-BEARING PIT MEMBRANES IN SPECIES OF OSMANTHUS Roland Dute1, 5, David Rabaey2, John Allison1 and Steven Jansen3, 4 SUMMARY Torus thickenings of pit membranes are found not only in gymnosperms, but also in certain genera of dicotyledons. One such genus is Osmanthus. Wood from 17 species of Osmanthus was searched for tori. Fourteen spe- cies from three of the four sections investigated possessed these thick- enings. Ten of the species represent new records. Only the three New Caledonian species of Section Notosmanthus lacked tori. This observation in combination with other factors serves to isolate this section from the remainder of the genus. Key words: Notelaea, Osmanthus, pit membrane, torus. INTRODUCTION Osmanthus is a member of the Oleaceae (Olive Family), a moderate-sized family with circa 24 genera and 615 spp. (Stevens 2001). There are 33 natural species within the genus (Table 1; Xiang et al. 2008), and they show a tropical to temperate distribution (Bailey & Bailey 1976; Denk et al. 2001; Xiang et al. 2008). Generally, individual shrubs are found in moist forests (Hsieh et al. 1998; Chou et al. 2000; Denk et al. 2001), frequently on steep slopes (Green 1958). In some instances populations are sub- ject to monsoon conditions and hence to periods of relatively low rainfall (Yang et al. 2008; Hua 2008). Tori are thickenings of intervascular pit membranes found not only in gymnosperm, but also in angiosperm wood, including that of Osmanthus (Dute et al. 2008; Dute et al. 2010). Tori were first observed in O. fragrans, O. heterophyllus, and O. × fortunei (a hybrid between O. fragrans & O. heterophyllus [Green 1958]) by Ohtani and Ishida (1978) and later in O. aurantiacus (subsumed within O. fragrans by Green 1958), O. insularis and O. rigidus (insufficiently known species, Green 1958) by Ohtani (1983). Subsequently, Dute and Rushing (1987, 1988) discovered tori in O. americanus (native to the southeastern U.S.A.) and elucidated the mechanism of torus synthesis. Rabaey et al. (2006) extended the list with the discovery of tori in O. serratulus and O. suavis. 1) Department of Biological Sciences, Auburn University, Life Sciences Building, Auburn, Alabama 36849-5407, U.S.A. 2) Laboratory of Plant Systematics, K.U. Leuven, Kasteelpark Arenberg 31, Box 2437, B-3001 Leuven, Belgium. 3) Institute of Systematic Botany and Ecology, Ulm University, Albert-Einstein-Allee 11, D-89081, Ulm, Germany. 4) Jodrell Laboratory, Royal Botanic Gardens, Kew, TW9 3DS, Richmond, Surrey, U.K. 5) To whom correspondence should be addressed [E-mail: [email protected]]. Downloaded from Brill.com10/01/2021 04:40:49AM via free access 218 IAWA Journal, Vol. 31 (2), 2010 Table 1. Taxonomy of Osmanthus as modified from Xianget al. (2008). Binomials in bold identify the species whose wood was observed in the present study. The asterisks denote those species previously found to have tori. Section 1. Leiolea (Section 4 Osmanthus continued) O. americanus* O. gracilinervis O. marginatus O. hainanensis O. matsumuranus O. henryi O. minor O. heterophyllus* O. scortechinii O. insularis* O. sumatranus O. iriomotensis O. kaoi Section 2. Notosmanthus O. lanceolatus O. austrocaledonicus O. pubipedicellatus O. cymosus O. reticulatus O. monticola O. serrulatus* Section 3. Linocieroides O. urceolatus O. didymopetalus O. venosus O. yunnanensis Section 4. Osmanthus O. × fortunei O. armatus O. attenuatus Section 5. Siphosmanthus O. cooperi O. decorus O. enervius O. delavayi O. fordii O. suavis* O. fragrans* O. × burkwoodii Comparative wood anatomy (Patel 1978; Baas et al. 1988) showed a close relation- ship among the genera Osmanthus, Phillyrea, Notelaea and Nestegis. Recent analysis of chloroplast DNA (Wallander & Albert 2000) confirmed the relationship among these four genera along with a fifth,Picconia . Investigations of wood from species of Phillyrea, Nestegis, Notelaea and Picconia showed the presence of tori only in Pic- conia (Dute et al. 2008; Rabaey et al. 2008), a small genus of only two species native to Macaronesia. Tori in species of Osmanthus and other angiosperms are not known to put the plant at a disadvantage under moist conditions, yet the torus is of such a diameter as to oc- clude a pit aperture during aspiration. Because the torus is thicker than the margo, it is less porous and provides greater mechanical support, which may prevent rupture of the pit membrane (Dute & Rushing 1987). Clearly, tori could provide an advantage under conditions of drought stress by lowering the risk of air-seeding, i.e. the induction of cavitation of air sucked through the largest pore of a pit membrane into a functional, water-filled tracheary element. Although six distinct species of Osmanthus have been investigated for tori (Table 1), there are about 33 species in nature (Table 1; Xiang et al. 2008). The aim of this study was to investigate other Osmanthus species for the presence of a torus. Such data would: 1) help with the taxonomic circumscription of this feature in the Oleaceae and 2) provide information for future introduction of new, drought-tolerant species into the horticulture market of the southeastern U.S.A. (Werner 2007). Downloaded from Brill.com10/01/2021 04:40:49AM via free access Dute, Rabaey, Allison & Jansen — Tori in Osmanthus 219 Table 2. Herbarium specimens of Osmanthus and Osmarea used in this study. BR = Natio- nal Botanic Garden, Brussels; K = herbarium of the Royal Botanic Gardens, Kew. Species Herbarium Date of collection Collector(s) no. O. americanus Benth. & Hook. f. BR unknown unknown O. americanus (L.) Gray K Jan 1938 Naruda 2023 O. armatus Diels BR 25 Feb 2009 Rabaey s.n. (liv. col. 19673925) O. austrocaledonicus (Vieill.) Knobl. K unknown White 2200 O. austrocaledonicus (Vieill.) BR unknown MacKee 29532 Knobl. subsp. austrocale- donicus O. austrocaledonicus (Vieill.) K unknown Guillaumin 28014 Knobl. subsp. austrocale- donicus O. austrocaledonicus (Vieill.) K unknown Deplanche 14 Knobl. subsp. austrocale- donicus var. austrocaledonicus O. austrocaledonicus (Vieill.) BR unknown Bamps 6000 Knobl. subsp. badula (Vieill. ex Pancher & Sebert) P.S. Green O. austrocaledonicus (Vieill.) K 1 Nov 1929 Franc 2405 Knobl. subsp. badula (Vieill. ex Pancher & Sebert) P.S. Green O. austrocaledonicus (Vieill.) K 12 April 1968 Bernardi 12767 Knobl. subsp. collinus (Schltr.) P.S. Green O. austrocaledonicus (Vieill.) K 11 October 1963 Green 1294 Knobl. subsp. collinus (Schltr.) P.S. Green O. cymosus (Guillaumin) K 18 October 1982 McKee 40928 P.S. Green O. enervius Masam. & Mori BR unknown Taiwan Forestry Research Institute 17310 O. fragrans Lour. BR unknown Likkir & Kemp s.n. O. fragrans Lour. K 31 December 1974 Geesink et al. 8002 O. heterophyllus (G. Don) BR unknown Coplan P.S. Green O. insularis Koidz. BR unknown Yokoyama 1132 O. insularis Koidz. K 03 May 1917 Wilson 8367 O. kaoi (Liu & Liao) S.Y. Lu BR unknown Sheng-You Lu 13487 O. marginatus (Champ. ex BR unknown Taam 193 Benth.) Hemsl. continued on the next page Downloaded from Brill.com10/01/2021 04:40:49AM via free access 220 IAWA Journal, Vol. 31 (2), 2010 (Table 2 continued) Species Herbarium Date of collection Collector(s) no. O. marginatus (Champ. ex K 03 July 1933 How 71028 Benth.) Hemsl. O. matsumuranus Hayata BR unknown Omarina 17854 O. matsumuranus Hayata K 6 October 1928 Poilane 15828 O. minor P.S. Green BR unknown Taam O. minor P.S. Green K 27 May 1914 W.J.T. 10949 O. monticola (Schltr.) Knobl. BR unknown Bamps 5754 O. monticola (Schltr.) Knobl. K 13 May 1951 Guill. & Baum 11238 O. scortechinii King & Gamble K 14 May 1975 de Wilde & de Wilde- Duyfjes 16912 O. scortechinii King & Gamble K unknown Holttum 10732 O. venosus Pamp. BR unknown Sino-American Ghuizou Botanical Expedition 1693 O. yunnanensis (Franch.) BR 25 Feb 2009 Rabaey s.n. (liv. col. P.S. Green 19392003) Osmarea × burkwoodii Burkwood & Skipwith K 17 April 1969 Burkwood & Skipwith s.n. MATERIALS AND METHODS Sources of wood specimens examined in this study are listed in Table 2. Specimens were prepared for light microscopy by two methods. In the first method, small segments were removed from the branches of herbarium specimens with a razor blade. The segments were placed in 95% ethanol under vacuum for one hour; the ethanol was replaced once and the segments left to soak overnight. Next, the segments were infiltrated with and embedded in JB-4 resin. Cross sections of 1.5 to 3 μm in thick- ness were cut on a Sorvall MT-2b ultramicrotome using a glass knife. Sections were heat-fixed to glass slides, stained with benzoate-buffered, aqueous toluidine blue O, embedded in Permount mounting medium (Fisher Scientific, Fair Lawn, New Jersey, U.S.A.), and topped with a coverslip. A Nikon Biophot microscope with a Nikon D-70 digital camera attachment was used to observe and photograph specimens. In the second method for light microscopy, thin sections (10–15 μm) were prepared using a sliding microtome (Reichert, Vienna, Austria). A mixture of 0.5% safranin in 50% ethanol and 1% alcian blue in water (35: 65, v/v) was used as a staining solution. After staining, sections were washed with distilled water, dehydrated with ethanol and treated with the clearing agent Parasolve (Prosan, Merelbeke, Belgium). The sections were embedded in Euparal (Agar Scientific Ltd, Essex, U.K.). LM-observations were carried out with a Dialux 20 (Leitz, Wetzlar, Germany) fitted with an oil immersion objective. Digital images were made with a PixeLINK PL-B622CF camera. Herbarium specimens were prepared for scanning electron microscopy (SEM) also by two different procedures. Branch segments of O. austrocaledonicus and O. scortechinii were split lengthwise exposing radial longitudinal sections. Split segments were affixed Downloaded from Brill.com10/01/2021 04:40:49AM via free access Dute, Rabaey, Allison & Jansen — Tori in Osmanthus 221 to aluminum stubs with double-stick, carbon-impregnated tape.
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