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Downloaded from Brill.Com09/25/2021 01:59:22PM Via Free Access 54 IAWA Journal, Vol IAWA Journal, Vol. 31 (1), 2010: 53–66 TORUS-BEARING PIT MEMBRANES IN CERCOCARPUS Roland Dute1,*, Jaynesh Patel1 and Steven Jansen2,3 SUMMARY Intervascular pit membranes of Cercocarpus possess torus thickenings. The thickenings, or pads, consist of lignified, secondary wall material. Torus pad deposition occurs late in cell ontogeny and is not associated with a microtubule plexus. Half-bordered pit pairs between tracheary elements and parenchyma cells often have a torus pad on the membrane surface facing the conducting cell. In contrast, a thick protective layer fills the pit cavity on the side of the parenchyma cell. Ontogeny of the torus thickenings in Cercocarpus represents a third mode of torus de- velopment in eudicots when compared to that occurring in Osmanthus / Daphne and Ulmus /Celtis. Key words: Bordered pit, Cercocarpus, pit membrane, torus, tracheid, vessel element, xylem. INTRODUCTION At one time, intervascular pit membranes in eudicotyledon woods were thought to be exclusively homogeneous. Then, in 1978, Ohtani and Ishida observed torus-bearing pit membranes in three species of Osmanthus (Oleaceae) and in three species of Daphne (Thymelaeaceae). Further work in several laboratories since that time has increased the number of species with torus-bearing pit membranes to 78 distributed within ten genera and five families (Table 1 and literature cited therein). Our laboratory has been concerned with the ontogeny of such pit membranes. These developmental studies were summarized by Coleman et al. (2004). Basically, two mechanisms of torus manufacture were recognized. One method, as illustrated by Osmanthus americanus and Daphne odora, involved a late deposition of torus pads in association with microtubule clusters. The second method, as found in Celtis occidentalis and Ulmus alata, involved early thickening of the pit membrane without benefit of a microtubule plexus. A recent study described intervascular pit membrane structure in the Rosales with an emphasis on species in the Rosaceae (Jansen et al. 2007). Included in this study were all four species of the genus Cercocarpus (according to Kartesz 1999): C. intricatus S.Wats., C. ledifolius Nutt., C. montanus Raf., and C. traskiae Eastw. Cercocarpus betu- loides Torrey & Gray, as used in this study, is considered a synonym of C. montanus (Kartesz 1999). 1) Department of Biological Sciences, Auburn University, Life Sciences Building, Auburn, Alabama 36849-5407, U. S. A. 2) Jodrell Laboratory, Royal Botanic Gardens, Kew, TW9 3DS, Richmond, Surrey, U. K. 3) Institute of Systematic Botany and Ecology, Ulm University, Albert-Einstein-Allee 11, D-89081 Ulm, Germany. *) To whom correspondence should be addressed [E-mail: [email protected]]. Downloaded from Brill.com09/25/2021 01:59:22PM via free access 54 IAWA Journal, Vol. 31 (1), 2010 Table 1. Eudicot species containing torus-bearing pit membranes in their woods. Family Species Citation Oleaceae Chionanthus retusa Rabaey et al. 2008 Osmanthus americanus Dute & Rushing 1987 O. aurantiacus Ohtani 1983 O. fortunei Ohtani & Ishida 1978; Ohtani 1983 O. fragrans ” ” O. heterophyllus ” ” O. insularis Ohtani 1983 O. rigidus Ohtani 1983 O. serratulus Rabaey et al. 2006 O. suavis ” Picconia azorica Dute et al. 2008; Rabaey et al. 2008 P. excelsa ” ” Thymelaeaceae Daphne acutiloba Dute et al. 1992 D. alpina ” D. altaica ” D. arbuscula ” D. arisanensis Dute et al. 1996 D. aurantiaca ” D. bholua ” D. blagayana Dute et al. 1992 D. × burkwoodii ” D. caucasica ” D. cneorum Dute et al. 1990 D. collina Dute et al. 1992 D. ericoides Dute et al. 1996 D. genkwa Dute et al. 1992 D. glomerata ” D. gnidioides Dute et al. 1996 D. gnidium Dute et al. 1992 D. jasminea Dute et al. 1996 D. kiusiana Ohtani & Ishida 1978; Ohtani 1983 D. laureola Dute et al. 1992 D. miyabeana Ohtani & Ishida 1978; Ohtani 1983 D. odora ” ” D. oleoides Dute et al. 1992 D. papyracea ” D. petraea Dute et al. 1996 D. retusa Dute et al. 1992 D. stapfii Dute et al. 1996 D. striata Dute et al. 1992 D. tangutica ” Wikstroemia albiflora Dute et al. 1996 W. kudoi ” W. pauciflora ” W. yakushimensis ” ………………………………………………………………………………………………… Downloaded from Brill.com09/25/2021 01:59:22PM via free access Dute, Patel & Jansen — Torus-bearing pit membranes 55 (Table 1 continued) Family Species Citation Rosaceae Cercocarpus intricatus Jansen et al. 2007 C. ledifolius ” C. montanus ” C. traskiae ” Ulmaceae Planera aquatica Dute et al. 2004 Ulmus alata Wheeler 1983 U. americana Jansen et al. 2004 U. campestris Czaninski 1979 U. carpinifolia Jansen et al. 2004 U. coritana ” U. cornubiensis ” U. davidiana ” U. diversifolia ” U. effusa ” U. fulva ” U. glabra ” U. japonica ” U. laciniata ” U. macrocarpa ” U. montana ” U. parvifolia ” U. pedunculata ” U. plotii ” U. scabra ” U. thomasii Wheeler 1983 Zelkova acuminata Jansen et al. 2004 Z. crenata ” Z. cretica Jansen et al. 2007 Z. serrata ” Cannabaceae Celtis australis Jansen et al. 2007 C. laevigata Wheeler 1983 C. occidentalis ” C. reticulata ” Intervascular pit membranes of this genus appeared thickened under the light mi- croscope. These thickenings resolved themselves as tori when viewed with the electron microscope. This observation represented a new record for tori in angiosperms, and the first (and so far only) recorded instance of tori in the Rosaceae (Jansenet al. 2007). The aims of the present study were to investigate torus ontogeny in Cercocarpus, and to compare the developmental sequence with that of previously investigated species. Downloaded from Brill.com09/25/2021 01:59:22PM via free access 56 IAWA Journal, Vol. 31 (1), 2010 Table 2. Sources of Cercocarpus wood specimens examined in this study. Taxon Herbarium Date of Collection Collector(s) No. C. betuloides Torrey & A.Gray AUA 29 June 1966 Crampton 7776 C. betuloides Torrey & A.Gray AUA 17 June 2007 Boyd s.n. C. betuloides Torrey & A.Gray K unknown Clokey & Templeton 4596 C. intricatus Wats. DAV 14 May 1977 Levin 1248 C. ledifolius Nutt. K 12 June 2005 S. Jansen, accession number 1980-6418 C. montanus Raf. K unknown Baker et al. 392 C. montanus Raf. var. argentus (Rydb.) F.L. Martin AUA 17 Aug 1980 Drost 72 var. paucidentatus (S.Wats.) F. L. Martin K unknown Rehder 397 var. paucidentatus (S.Wats.) F.L. Martin K unknown Rehder 56 C. traskiae Eastw. AHUC 6 April 1982 Crampton s.n. MATERIALS AND METHODS Sources of wood specimens examined in this study are listed in Table 2. Wood segments from herbarium specimens were prepared for light (LM), transmis- sion electron (TEM), and scanning electron (SEM) microscopy according to the methods of Dute et al. (2008). For light microscopy, wood specimens from Cercocarpus mon- tanus and C. betuloides were cut transversely with a razor blade and the resulting seg- ments soaked in two changes of absolute ethanol (30 minutes apiece). The material was then placed in absolute acetone overnight followed by gradual infiltration of the speci- mens with Spurr’s resin (Spurr 1969). Cross sections of 1.5 µm were cut on a Sorvall MT-2b ultramicrotome using a glass knife. Sections were affixed to glass slides and stained using benzoate-buffered, aqueous toluidine blue O (TBO). Images were captured using a Nikon D-70 digital camera attached to a Nikon Biophot microscope. For TEM, Spurr’s-embedded material was sectioned at about 80 nm using a dia- mond knife mounted in the MT-2b ultramicrotome. The resulting ultrathin sections were placed on copper grids, stained either with 1% KMnO4 in 1% sodium citrate (Donaldson 2002) or with uranyl acetate/lead citrate, and observed with a Zeiss EM 10 transmission electron microscope using an accelerating voltage of 60 kV. Unstained sections were viewed as controls for the KMnO4 treatment. For SEM, herbarium specimens from all four species were split to expose either radial or tangential longitudinal surfaces and attached to aluminum stubs using carbon- impregnated double stick tape. Exposed wood surfaces were coated with gold-palladium. The resulting preparations were viewed with a Zeiss DSM 940 operated at 15 kV or a Zeiss EVO 50 at 20 kV. Living branches from four individuals of C. betuloides were collected on 17 June 2007 and on 7 July 2008 in California. The collecting sites were a series of road cuts in a chaparral environment at 752 m altitude on the Los Angeles County/San Ber- nardino County border. The coordinates are 34° 10' 38.68" N; 117° 40' 32.59" W. The specimens were returned on ice in plastic bags to Auburn and preserved the next day. Downloaded from Brill.com09/25/2021 01:59:22PM via free access Dute, Patel & Jansen — Torus-bearing pit membranes 57 Routine procedures were used for TEM preparation of wood segments (Dute & Rushing 1988) that included glutaraldehyde primary fixation, osmium postfixation, dehydration and embedment in Spurr’s resin. Ultrathin sections were cut, placed on copper grids, and stained with uranyl acetate and lead citrate. Monitor sections of 1.5 µm were cut, mounted on glass slides, and stained with TBO for viewing with LM. Spurr’s embedded herbarium material of C. montanus was sectioned transversely at 3 µm, mounted on glass slides, and stained with 0.01% acriflavin hydrochloride according to the procedure of Donaldson (2002). Qualitative lignin distribution was determined using fluorescence microscopy (Donaldson 2002; Coleman et al. 2004). Abbreviations used in the figures in this study: A = pit aperture; AN = annulus; M = margo of pit membrane; MI = microtubules; P = axial parenchyma cell; T = tracheid; TO = torus thicken- ing; V = vessel member. — Note: Figures 4, 5 & 7 are images of C. montanus; the remaining images are of C. betuloides. Figures 1–3. Torus location and anatomy. – 1: Cross section of Cercocarpus wood show- ing a vessel member, tracheids, and an axial parenchyma cell. Tori are indicated by un- labeled arrows. – 2: Aspirated pit membrane between two tracheids in an herbarium speci- men. Note the comparative diameter of the torus and that of the pit apertures.
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