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Vessels in Zingiberaceae IAWA Journal, Vol. 21 (1), 2000: 61–76 VESSELS IN ZINGIBERACEAE: A LIGHT, SCANNING, AND TRANSMISSION MICROSCOPE STUDY by Jennifer A. Thorsch Department of Ecology Evolution and Marine Biology, University of California, Santa Barbara, CA 93106, U.S.A. SUMMARY The Zingiberales is a tropical group of monocotyledons that includes eight recognized families. The order is considered by most taxono- mists and phylogenists to be a monophyletic lineage of plants, but the phylogenetic relationships among genera are not clearly understood. The tracheary elements in the family Zingiberaceae were examined to characterize the diversity of structure and to better understand the phylo- genetic relationships among related taxa. The distribution and speciali- zation of tracheary elements in roots, stems and leaves of 54 species representing 25 genera were studied. Vessel elements were present in roots of all but one of the species examined, Plagiostachys philippinen- sis. Stems and leaves had only tracheids except for Aulotandra kamerun- ensis, which had vessels with simple perforation plates. The perforation plates and lateral walls of vessel elements were examined for the pres- ence of pit membranes or their remnants with both scanning and trans- mission electron microscopy. The presence and condition of pit mem- branes depended upon the developmental stage, but the perforation plates of mature vessel elements lacked pit membranes entirely. Key words: Zingiberaceae, vessel specialization, pit membranes. INTRODUCTION In the late 1930ʼs, Dr. Vernon I. Cheadle began his studies of tracheary elements in monocotyledons. His research and numerous published papers (Cheadle 1942, 1953; Cheadle & Kosakai 1980; Thorsch & Cheadle 1996) have been based on dozens of monocotyledon families. This paper includes information on tracheary elements in Zingiberaceae, the 30th family we have examined. Results from this and earlier studies have provided information on the origin and specialization of tracheary elements. Monocotyledonous vessels arose from a series of overlapping tracheids by loss of membranes from scalariformly arranged pits in long, oblique ends of tracheids (Cheadle 1953). Those vessel elements that are most like tracheids are considered the most primitive: they are long and narrow, appear angular in transverse view, and have long oblique end walls with many perforations arranged scalariformly. Conversely, vessel elements least like tracheids are most ad- Downloaded from Brill.com09/27/2021 12:36:30AM via free access 62 IAWA Journal, Vol. 21 (1), 2000 vanced: they have shorter lengths, greater diameters, are circular in transverse view, and have a single perforation on transversely placed end walls (simple perforation plates). Gradations between the types of vessel elements considered as most primi- tive and the most advanced can be found in extant monocotyledons. Indeed, the pres- ence of such a range of tracheary element structure in extant monocotyledons pro- vides evidence for drawing conclusions about probable evolutionary sequences. The family Zingiberaceae (order Zingiberales) is a tropical group of monocotyle- dons. The Zingiberales includes eight families (Musaceae, Strelitziaceae, Lowiaceae, Heliconiaceae, Zingiberaceae, Costaceae, Cannaceae, and Marantaceae) represent- ing 88 genera and about 2000 species (Kress 1990). The evolutionary relationships among taxa of Zingiberales have been studied by Tomlinson (1962), Dahlgren and Rasmussen (1983), Kirchoff (1988), and Kress (1990). These investigations were based on anatomical, morphological and/or developmental features. Kress (1990) obtained a fully resolved cladogram of the eight families using 29 binary characters. The four ginger families formed a terminal clade of two lineages with Zingiberaceae + Costa- ceae and Cannaceae + Marantaceae as sister taxa. The four banana families, Musaceae, Strelitziaceae, Lowiaceae and Heliconiaceae, comprised a paraphyletic assemblage of 4 lineages at the base of the cladogram. This phylogenetic hypothesis was tested by Smith et al. (1993) with molecular sequence data. DNA sequences of the chloroplast- encoded rbcL gene from 21 members of Zingiberales and proposed outgroups in mono- cots were employed. This analysis resulted in a single most parsimonious tree, with a topology significantly different from that of the morphological tree. The differences included the paraphyly of the Musaceae, the separation of the Zingiberaceae + Costa- ceae and Cannaceae + Marantaceae, and the basal position for the lineage comprising Costaceae + Marantaceae. Results of studies by Duvall et al. (1993) and Smith et al. (1993) with Haemodoraceae + Pontederiaceae + Commelinaceae clade as the sister group of the Zingiberaneae contrasts with those obtained with Bromeliiflorae as out- group (Kress 1990), and suggest reconsideration be made of the cladistic analysis based on morphological features. More recent studies by Kress (1995), utilizing dif- ferent outgroups, additional morphological characters, and molecular data, support the earlier hypothesis on phylogenetic relationships among the eight families of Zingi- berales (Dahlgren & Rasmussen 1983; Kirchoff 1988, Kress 1990). The monophyly of the ginger-families clade is supported as are sister group relationships of Zingibera- ceae + Costaceae and Cannaceae + Marantaceae. The banana-families relationships are moderately resolved in combined data analysis, but further morphological and molecular data are needed. Recent studies by Carlquist and Schneider have focused on the presence of “porous or web-like remnants” in perforation plates of several families including Nymphaeaceae (Schneider et al. 1995; Schneider & Carlquist 1998a, b), Nelumbona- ceae (Schneider & Carlquist 1996), Araceae (Carlquist & Schneider 1998b), Lowiaceae (Carlquist & Schneider 1998a), and several fern families (Schneider & Carlquist 1998a, 1998b; Carlquist & Schneider 1998c). Carlquist and Schneider have suggested that the occurrence of remnants is significant because it may be interpreted as a stage in vessel evolution preceding disappearance of the pit membranes. As part of this study, Downloaded from Brill.com09/27/2021 12:36:30AM via free access Thorsch — Vessels in Zingiberaceae 63 pit membranes in perforation plates and lateral walls of vessel elements were exam- ined with both scanning and transmission electron microscopy to determine whether porous or web-like remnants were present in mature elements of Zingiberaceae. This study on the tracheary elements in Zingiberaceae by light, scanning and trans- mission electron microscopy includes detailed information on the distribution, level of specialization , and the condition of the pit membranes of mature vessel elements. MATERIALS AND METHODS Zingiberaceae are pantropical with the greatest concentration of genera and species in South-East Asia (Dahlgren et al. 1985). They are predominantly forest floor plants growing in humus-rich media in shade or semi-shade habitats. The specimens were selected from preserved material in the Vernon I. Cheadle and Katherine Esau Botanical Collections at UC Santa Barbara, Kew Gardens, and Fairchild Tropical Botanical Gardens. The herbarium material was on loan from Missouri Bo- tanic Garden, Chicago Field Museum and Gray Herbarium (Harvard). In Table 1 the specimens examined are listed alphabetically and include our col- lection numbers (M or CA), as well as the abbreviation for the herbaria from which they were borrowed (if loaned specimens) and the accession numbers. All available plant parts of 54 species from 25 genera were examined. Preserved specimens were rinsed thoroughly with water and dried specimens were rehydrated in several changes of warm water. Tissue was cut into 0.5 cm segments and macer- ated in 40% glacial acetic acid, 50% distilled water and 10% hydrogen peroxide in pressure bottle at 65–75 °C for 5–7 days. The tissue was rinsed in water, stained with Toluidine Blue and gently teased apart with fine needles in glycerin on glass slides. Specimens for SEM studies were prepared in the same manner except the tissue was then teased apart on small glass coverslips attached to SEM stubs. The tissue was al- lowed to air dry in a dust free environment and then sputter coated with gold palla- dium. The material was viewed with an Hitachi S-415A scanning electron microscope. Light microscope sections of many species were prepared from the chemically preserved specimens and also available living material. The living material was fixed in formalin-acetic acid-alcohol. All tissue was processed through a graded acetone series and embedded in Spurrʼs resin (1969). Sections were cut at approx. 1–2 μm with a diamond knife and stained with Toluidine Blue. All the photomicrographs were taken with a Zeiss Ultraphot equipped with a 35 mm camera attachment. Several greenhouse grown specimens of Zingiberaceae were prepared for trans- mission electron microscopy. Root material was carefully excised from pot grown plants and immediately placed in cold 4% glutaraldehyde buffered with 0.1 M so- dium cacodylate at pH 6.8. The material was fixed at 4°C for 3 hours under vacuum, washed for 3 hours in the buffer, and postfixed in 2% osmium tetroxide overnight at 4°C. The tissue was dehydrated in a graded acetone series and embedded in Spurrʼs resin (1969). Sections were cut with diamond knives on a Porter Blum MT2B Ultrami- crotome, stained with uranyl acetate and lead citrate and photographed with a Philips CM10 electron microscope. Downloaded from Brill.com09/27/2021
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