Vessels in Zingiberaceae

Home , Aframomum, Aframomum alboviolaceum, Alpinia caerulea, Burbidgea, Cautleya, Elettariopsis

IAWA Journal, Vol. 21 (1), 2000: 61–76

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 phylogenetic relationships among related taxa. The distribution and specialization 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 philippinensis. Stems and leaves had only tracheids except for Aulotandra kamerunensis, which had vessels with simple perforation plates. The perforation plates and lateral walls of vessel elements were examined for the presence of pit membranes or their remnants with both scanning and transmission electron microscopy. The presence and condition of pit membranes 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 primitive and the most advanced can be found in extant monocotyledons. Indeed, the presence of such a range of tracheary element structure in extant monocotyledons provides evidence for drawing conclusions about probable evolutionary sequences. The family Zingiberaceae (order Zingiberales) is a tropical group of monocotyledons. The Zingiberales includes eight families (Musaceae, Strelitziaceae, Lowiaceae, Heliconiaceae, Zingiberaceae, Costaceae, Cannaceae, and Marantaceae) representing 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 different 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 examined 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 transmission 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 collection 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 macerated 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 transmission 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.

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Table 1. Zingiberaceae. Key: genus/species with authority, VIC collection number, herbarium and herbarium accession number or botanic garden; if the latter is not available the locality or collectorʼs name and number if present is listed. Herbaria abbreviations as in Index Herbariorum.

Aframomum alboviolaceum (Ridley) K. Schum., M 1652, F 1459380 hanburyi K. Schum., M 1653, F 761877 masina K. Schum., M 1654, F 1584673 melegueta (Roscoe) K. Schum., M 1656, F 532416 melegueta (Roscoe) K. Schum., M 1657, F 1714561 sanguineum K. Schum., M 1655, F 1543305 Alpinia caerulea (R. Br.) Benth., CA164, Brisbane, Australia calcarata Roscoe, M 486, Kew japonica (Thunb.) Miq., M 497, Howard, Cuba sanderae Hort. Sander, M 487, Howard, Cuba zerumbet (Pers.) B.L. Burtt & R.M. Smith, M 496, Soledad, Cuba zerumbet (Pers.) B.L. Burtt & R.M. Smith, M 1440, Kew 299-60-29903 Amomum compactum Solander, M 1636, UCSB Greenhouse magnificum Benth., M 489, unknown magnificum Benth., M 1460, Kew Aulotandra kamerunensis Loesener, M 1651, F 762553 Boesenbergia prainiana Schlechter, M 1466, Kew Burbidgea schizocheila auteur, M 1650 Camptandra latifolia Ridley, M 1642, GH 14451 ovata Ridley, M 1643, GH J.W. Purseglove parvula (Baker) Ridley, M 1644, GH M.R. Henderson Cautleya robusta Baker, M 1454, Kew 396-78-03877 spicata (Smith) Baker, M 1467, Kew Curcuma longa L., M 1270, Fairchild 1848 longa L., M 1290, UCSB Greenhouse pallida Lour., M 1277, UCSB Greenhouse petiolata Roxb., M 493, unknown Elettaria cardamomum Maton, M 1436, Kew 000-73-12394 cardamomum Maton, M 488, Kingston Green, Rhode Island Elettariopsis curtisii Baker, M 1465, Kew Gagnepainia godefroyi (Baill.) K. Schum., M 1646, GH Herb. L. Pierre Geostachys elegans Ridley, M 1666, MO 2463096 elegans Ridley, M 1673, MO 2220317 Globba schomburgkii Hook. f., M 1295, UCSB Greenhouse schomburgkii Hook. f., M 1463, Kew winniti C.H. Wright, M 1264, Fairchild 70517 sp. M 1464, Kew Hedychium coronarium J. Koenig, M 495, Soledad, Cuba gardnerianum Roscoe, M 1462, Kew greenei W.W. Smith, M 1283, UCSB Greenhouse horsfieldiiWall., M 1435, Kew 105-76-00792 sp. CA646, Natal Hitchenia glauca Wall., M 1645, GH (from Kew)

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(Table 1 continued) Hornstedtia alliacea Valeton, M 1665, MO 2734986 luzanensis Elmer, M 1658, MO 835521 sp. M 1670, MO 2627175 Kaempferia pulchra Ridley, M 1294, UCSB Greenhouse rosea Schweinf., M 1262, Fairchild 71349 Mantisia saltatoria Sims, M 1647, GH J.O. Voigt Plagiostachys parviflora Ridley, M 1660, MO 798759 philippinensis Ridley, M 1659, MO 3242669 Renealmia africana Benth., M 1661, MO 3487885 alpinia (Rottb.) P. Maas, M 1668, MO 2893633 breviscapa Poeppig & Endlicher, M 1662, MO 2919823 cernua (Swartz) J.F. Macbride, M 1663, MO 2713203 cernua (Swartz) J.F. Macbride, M 498, Harvard 474 sp. M 1461, Kew Riedelia sp. M 1671, MO 2612791 sp. M 1672, MO 2743738 Roscoea auriculata K. Schum., M 1453, Kew 037-50-03704 Vanoverberghia diversifolium Elmer, M 1648, GH A.D.E. Elmer sepulchrei Merr., M 1649, GH A.D.E. Elmer Zingiber officinaleRoscoe, M 1289, UCSB Greenhouse

To quantify the level of specialization of tracheary cells in Zingiberaceae, a system developed by Vernon Cheadle was employed. A value of 0 indicates only tracheids present; 1 only scalariform perforation plates; 2 mostly scalariform perforation plates; 3 approximately equal scalariform and simple perforation plates; 4 mostly simple perforation plates and 5 only simple perforation plates.

RESULTS

The photomicrographs presented in the first plate provide an overview of the structure of the vascular tissues in root (Fig. 1) and stem (Fig. 2) of representative species of Zingiberaceae, as seen in transverse sections. A portion of the root stele with alternating strands of xylem (X) and phloem (P) is illustrated by Hedychium coronarium (Fig. 1). The vessels (V) have relatively large diameters. The roots of all species examined, with but one exception (Plagiostachys philippinensis), had vessels with either simple or scalariform perforation plates. In the stems and leaves examined only tracheids were found, except for the stems and leaves of Aulotandra kamerunensis, where vessels with simple perforation plates were observed. Figure 2 shows the arrangement of the xylem (X) and phloem (P) in the stem of Hedychium coronarium. Figures 3 and 4 show leaf vascular bundles in Alpinia zerumbet and Hedychium coronarium. The series of longitudinal sections of vessels from the roots of Alpinia zerumbet (Fig. 5, 8) and Hedychium coronarium (Fig. 6) demonstrates the trends of vessel ele-ment specialization, beginning with less specialized elements that are narrow and

Downloaded from Brill.com09/27/2021 12:36:30AM via free access 66 IAWA Journal, Vol. 21 (1), 2000 have oblique end walls with many perforations arranged scalariformly (Fig. 5), wider elements (Fig. 6) with scalariform perforation plates on transverse end walls, to the wid- est most advanced elements with simple perforations on transverse end walls (Fig. 8). Figures 7, 9 and 10 of separated vessel elements are representative of the range of variation observed in structure and inclination of perforation plates and in the lateral wall pitting in roots, as illustrated by Renealmia sp. (Fig. 7, 9) and Amomum magnificum (Fig. 10). An oblique end wall with many perforations arranged scalariformly (Fig. 7), a slightly oblique (Fig. 10) and transversely oriented (Fig. 9) end walls with simple

Legends of Figures 1–20 (pages 67–71):

Fig. 1 & 2. Transverse sections of Hedychium coronarium. – 1: Portion of the root stele with alternating strands of xylem (X) and phloem (P). – 2: Arrangement of xylem (X) and phloem (P) in the stem. — E = endodermis; TR = tracheid. Scale = 50 μm.

Fig. 3 & 4. Transverse sections of leaves. – 3: Alpinia zerumbet. – 4: Hedychium coronarium. — P = phloem, TR = tracheid, X = xylem. Scale bar = 50 μm.

Fig. 5–10. Vessels in roots. – 5: Alpinia zerumbet. Longitudinal section of a narrow vessel element with an oblique end wall with many perforations arranged scalariformly. – 6: Hedychium coronarium. Longitudinal section of a wider vessel element with a scalariform perforation plate on a transverse end wall. – 7: Renealmia sp. Obliquely oriented scalariform perforation plate of a macerated vessel element. – 8: Alpinia zerumbet. Longitudinal section of a vessel element with a simple perforation plate on the transverse end wall. – 9: Renealmia sp. Simple perforation plate on the transverse end wall. Unusual scalariform, narrow pitting on lateral wall. – 10: Amomum magnificum. A slightly oblique simple perforation plate. Oval elliptical and rounded rectangular pits (arrowheads) characterize the vessel wall pitting in Zingiberaceae. — Scale bar = 25 μm.

Fig. 11–16. SEM photographs of separated vessel elements from roots. – 11: Renealmia sp. Pit membranes (arrows) are intact along front section of lateral wall of vessel with simple perforation plate, but split in most pits along sides of element (arrowheads). – 12: Cautleya robusta. Vessel with scalariform perforation plate. Pit membranes are intact and only a few areas appear to be split. – 13: Curcuma longa. Obliquely oriented scalariform perforation plate. Pit membranes split along lateral wall area (arrows). – 14: Globba winitti. Portion of an irregular scalariform perforation plate (SCP) and the front section of the lateral wall. The pits have remnants of membranes (arrows). – 15 & 16: Globba winitti. Lateral wall of vessel element with pits and pit membrane remnants (arrows). The broad light bands are secondary wall thickenings. The pit membrane remnants appear to be porous or ʻweb-likeʼ. — Scale bar for 11–13 = 10 μm, for 14–16 = 1 μm.

Fig. 17–20. TEM photographs. – 17: Globba winitti. Scalariform perforation plate between two mature vessel elements (V). The pit membrane has completely hydrolyzed and no remnants are present. – 18: Globba winitti. A portion of the lateral wall area of the same vessel in Fig. 17. The pit membranes (arrows) in the lateral wall are reduced to networks of fibrils (arrows), but do not have a porous appearance. – 19: Amomum compactum. View of the end and lateral wall areas of adjacent tracheids. Pit membranes are composed of uniformly disposed fibrillar material (arrows). – 20: Amomum compactum. Lateral wall area between adjacent tracheids with pit membranes (arrows) present. — Scale bar = 1 μm.

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For legends, see page 66.

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For legends, see page 66.

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For legends, see page 66.

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For legends, see page 66.

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For legends, see page 66.

Downloaded from Brill.com09/27/2021 12:36:30AM via free access 72 IAWA Journal, Vol. 21 (1), 2000 perforation plates are illustrated. Oval elliptical and rounded rectangular pits (Fig. 7, 10, arrowheads) are characteristic of the vessel wall pitting in Zingiberaceae. The abun- dant, basically scalariform, narrow pitting in lateral walls of vessels in Renealmia sp. (Fig. 9) roots is somewhat unusual among the roots we examined. Scalariform perforation plates were identified in all species examined except forPlagiostachys philippinensis, where only tracheids were identified. The number of perforations can vary from 2 to well over 50 (Fig. 7 has approximately 13 perforations). Figures 11–16 are micrographs taken with a scanning electron microscope of separated vessel elements from the roots of Renealmia sp., (Fig. 11), Cautleya robusta (Fig. 12), Curcuma longa (Fig. 13) and Globba winitti (Fig. 14–16). Studies with the SEM can provide valuable information on vessel elements, including detail on pitting and the presence of probable perforation plates. A major goal of our studies with the SEM was to examine the perforation plate areas and look for evidence of porous or web-like remnants of the pit membranes at the perforation plate sites. The lateral walls in Figures 11–14 show the pitting with relatively intact pit membranes. In Fig- ure 11 the pit membranes are intact along the front section of the lateral wall (arrows), but appear split in most pits along the sides of the element, possibly due to prepara- tion procedures for the SEM (arrowheads). The pit membranes in Figure 12 are more intact and only a few areas appear to have been split. In Figure 13 the pit membranes are split along the lateral wall area. Figure 14 shows a portion of a scalariform perforation plate and part of the lateral wall of a vessel element. The perforation plate area (SCP) is free of remnants. A few areas (arrows) reveal the presence of possible ʻporousʼ pit membranes along the lateral walls. Figures 15 and 16 are SEM views of pits and pit membranes. The broad light bands are secondary wall thickenings. The porous or web-like material in the pits in Figures 15 and 16 appears to be remnants of pit membranes. In order to examine more closely what appeared as porous pit membranes with the SEM, tissue was prepared for transmission electron microscopy (TEM). Lateral walls in mature vessel elements and tracheids and perforation plates in mature vessel elements were examined. The level of maturity of the cell was determined by the condition of the protoplast. In tracheary elements the protoplast begins to break down after deposition of the secondary wall. The cell contents undergo lysis, resulting in a cell typically devoid of protoplasmic content at maturity. Scanning electron microscopy (SEM) does not allow the maturity of the cells to be determined with a great degree of accuracy. TEM not only reveals the developmental stage of cells, but also provides a more gentle processing procedure, eliminating the need for harsh chemicals and high temperatures utilized during macerations and sputter coating for the SEM. All three of these procedures may cause artifacts and tearing or spreading of the delicate hydrolyzed pit membranes. Serial sections through mature vessel elements were examined to determine the presence or absence of pit membranes at the perforation plates and also to determine the condition of the pit membranes of bordered pits in the lateral wall areas bordering the perforation plates. The perforation plate shown in Figure 17 (Globba winitti) is representative of the structural condition observed at scalariform perforation plates

Downloaded from Brill.com09/27/2021 12:36:30AM via free access Thorsch — Vessels in Zingiberaceae 73 between two mature vessel elements (V) with TEM. Neither porous nor web-like remnants were observed at perforation plates in any mature vessel elements of Zingi- beraceae. A portion of the lateral wall area is shown in Figure 18. The pit membranes in the bordered pits are reduced to networks of fibrils (arrows), but do not have a porous appearance. Mature tracheids were also studied with the TEM to determine the condition of the pit membranes. Figure 19 (Amomum compactum) is a view of end and lateral wall areas of adjacent tracheids. Pit membranes composed of fibrillar material are present in these areas. In Figure 20, the lateral wall area between the adjacent tracheids has pit membranes composed of fibrillar material. None of the pit membranes of tracheids observed with the TEM had a porous appearance.

DISCUSSION

Evidence for the specialization and evolutionary origin of vessel elements in monocotyledons was initially presented by Cheadle (1942) and subsequently confirmed by studies of hundreds of species in numerous monocotyledon families (Cheadle 1953; Thorsch & Cheadle 1996). This study of Zingiberaceae supports the findings that vessels arose in roots. Only Aulotandra kamerunensis had vessel elements in stems and leaves, and these had simple perforation plates. Vessel elements were present in the roots in all but one species examined, Plagio- stachys philippinensis. The level of specialization of vessels as measured by their perforation plates is summarized in Table 2. Values in the table are defined in the Materials and Methods section and are also included as a footnote to Table 2. Obvi- ously, the vessel elements in Zingiberaceae are not highly specialized. The vessels in roots had a value of 1.17. The values for the specialization in stems and leaves would have been 0, however Aulotandra kamerunensis had vessels with simple perforation plates in the stems and leaves, which raised the overall average to values of 0.07 and 0.04, respectively. Carlquist and Schneider (1998a) examined the vessel elements in one species, Orchi- dantha maxillarioides (Ridl.) K. Schum., in the family Lowiaceae within the Zingi- berales. These vessel elements had long scalariform perforation plates, with pit membrane remnants, in both roots and rhizomes. Comparing the degree of vessel element specialization in four families, Carlquist and Schneider (1998a) concluded that vessel elements in Lowiaceae, as represented by those in O. maxillarioides, are only slightly more specialized than those in Acoraceae, Juncaginaceae, and Scheuchzeriaceae. They suggested that Lowiaceae has a primitive position within the Zingiberales. In a separate study (unpublished), we examined about 70 species representing 24 genera in the Marantaceae family. The level of specialization of vessel elements was compared with our Zingiberaceae data. Vessels, some with simple perforations, were found in all root material. In the shoot system, a few vessels with scalariform perforations were found in the rhizomes of three species in three genera, in stems of two species in two genera and in leaves of four species in four genera. The values for vessel element specialization of Marantaceae are 1.46 for roots, 0.24 for stems and 0.05

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Table 2. Occurrence and specialization of vessels in Zingiberaceae.1 Species Root Stem Leaf Species Root Stem Leaf Aframomum Elettaria alboviolaceum M 1652 1 0 0 cardamomum M 1436 2 – – hanburyi M 1653 – 0 0 cardamomum M 488 1 – 0 masina M 1654 – – 0 Average 1.5 – 0 melegueta M 1656 2 0 0 Elettariopsis melegueta M 1657 2 0 0 curtisii M 1465 – – 0 sanguineum M 1655 – – 0 Average – – 0 Average 1.7 0 0 Gagnepainia Alpinia godefroyi M 1646 – 0 0 caerulea CA 164 – 0 0 Average – 0 0 calcarata M 486 – 0 0 japonica M 497 1 – 0 Geostachys sanderae M 487 – – 0 elegans M 1666 – 0 0 zarumbet M 496 1 0 0 elegans M 1673 – – 0 zarumbet M 1440 1 – – Average – 0 0 Average 1 0 0 Globba schomburgkii M 1295 1 – 0 Amomum schomburgkii M 1463 1 – – compactum M 1636 1 0 0 winniti M 1264 1 – 0 magnificum M 489 – 0 0 sp. M 1464 1 – – magnificum M 1460 3 – 0 Average 1 – 0 Average 2 0 0 Hedychium Aulotandra coronarium M 495 1 0 0 kamerunensis M 1651 – 2 2 gardnerianum M 1462 1 0 0 Average – 2 2 greenei M 1283 1 – – horsfieldiiM 1435 – – 0 Boesenbergia sp. CA 646 2 0 0 prainiana M 1466 – – 0 Average 1.25 0 0 Average – – 0 Hitchenia Burbidgea glauca M 1645 – – 0 schizocheila M 1650 – 0 0 Average – – 0 Average – 0 0 Hornstedtia Camptandra alliacea M 1665 – 0 – latifolia M 1642 1 0 0 luzanensis M 1658 2 0 0 ovata M 1643 1 0 0 sp. M 1670 – – 0 parvula M 1644 1 0 0 Average 2 0 0 Average 1 0 0 Kaempferia Cautleya pulchra M 1294 1 – – robusta M 1454 – – 0 rosea M 1262 1 – 0 spicata M 1467 1 – 0 Average 1 – 0 Average 1 – 0 Mantisia Curcuma saltatoria M 1647 – 0 0 longa M 1270 1 – 0 Average – 0 0 longa M 1290 1 – 0 Plagiostachys pallida M 1277 1 – 0 parviflora M 1660 1 0 0 petiolate M 493 – – 0 philippinensis M 1659 0 0 0 Average 1 – 0 Average 0.5 0 0

1) A value of 0 indicates only tracheids present; 1 only scalariform perforation plates; 2 mostly scalariform perforation plates; 3 approximately equal scalariform and simple perforation plates; 4 mostly simple perforation plates, and 5 only simple perforation plates.

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(Table 2 continued)

Species Root Stem Leaf Species Root Stem Leaf Renealmia Roscoea africana M 1661 – 0 0 auriculata M 1453 1 – – alpinia M 1668 – 0 0 Average 1 – – breviscapa M 1662 1 0 0 cernua M 1663 – 0 0 Vanoverberghia cernua M 498 – – 0 diversifolium M 1648 – 0 0 sp. M 1461 1 – 0 sepulchrei M 1649 – – 0 Average 1 0 0 Average – 0 0 Riedelia sp. M 1671 2 0 0 Zingiber sp. M 1672 1 – 0 officinaleM 1289 1 – 0 Average 1.5 0 0 Average 1 – 0 Average for Zingiberaceae 1.17 0.07 0.04 for leaves. Our data on vessel specialization supports Kressʼ (1995) phylogeny based on combined molecular and morphological data, which places the Marantaceae with the Cannaceae in a sister clade to the Zingiberaceae–Costaceae clade. As mentioned previously, Carlquist and Schneider (Schneider & Carlquist 1996, 1998a, 1998b; Carlquist & Schneider 1998c) have reported on the presence of pit membrane remnants in vessel elements in several families of monocotyledons. Ear- lier, Carlquist (1992) provided a summary of the literature on the presence of membrane remnants in perforation plates of vessel elements in dicotyledons, in addition to original observations on more that 30 families. Carlquist presented several possible interpretations for the presence of the membrane remnants. Based on the 1992 study and their SEM investigations of monocotyledons, Carlquist and Schneider (1998a) have suggested that the remnants may represent an early stage in vessel evolution. During the present investigation several vessels had what appeared with the SEM to be pit membrane remnants. Because the SEM does not allow one to determine with certainty the developmental state of the cells, fixed tissues were prepared for exami- nation with the TEM. Another concern was that the harsh chemicals used in macerat- ing tissues and removing paraffin from sectioned material and the sputter coating step for SEM may cause artifacts and tearing or spreading of the delicate pit membranes. None of the perforation plates of mature vessel elements viewed with the TEM had pit membrane remnants. By contrast, the bordered pits in lateral wall areas of both mature vessels and tracheids had pit membranes composed of uniformly disposed fibrillar material. Preliminary studies of mature vessels in Marantaceae with theTEM failed to show the presence of pit membrane remnants at the perforation plates. The current investigation clearly demonstrates the importance of using the TEM to confirm results obtained with the SEM on the presence or absence of pit membranes in mature vessel elements, and the structure of those that are present.

ACKNOWLEDGEMENTS

I wish to thank Deborah D. Fisher for her assistance with the scanning electron microscopy and with the macerations.

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