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Structure and Macromolecular Composition of the Seed Coat of Musaceae UvA-DARE (Digital Academic Repository) Structure and macromolecular composition of the seed coat of Musaceae Graven, P.; de Koster, C.G.; Boon, J.J.; Bouman, F. DOI 10.1006/anbo.1996.0013 Publication date 1996 Published in Annals of Botany Link to publication Citation for published version (APA): Graven, P., de Koster, C. G., Boon, J. J., & Bouman, F. (1996). Structure and macromolecular composition of the seed coat of Musaceae. Annals of Botany, 77, 105-122. https://doi.org/10.1006/anbo.1996.0013 General rights It is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), other than for strictly personal, individual use, unless the work is under an open content license (like Creative Commons). Disclaimer/Complaints regulations If you believe that digital publication of certain material infringes any of your rights or (privacy) interests, please let the Library know, stating your reasons. In case of a legitimate complaint, the Library will make the material inaccessible and/or remove it from the website. Please Ask the Library: https://uba.uva.nl/en/contact, or a letter to: Library of the University of Amsterdam, Secretariat, Singel 425, 1012 WP Amsterdam, The Netherlands. You will be contacted as soon as possible. UvA-DARE is a service provided by the library of the University of Amsterdam (https://dare.uva.nl) Download date:04 Oct 2021 Annals of Botany 77: 105–122, 1996 Structure and Macromolecular Composition of the Seed Coat of the Musaceae PETER GRAVEN*†, CHRIS G. DE KOSTER†, JAAP J. BOON† and FERRY BOUMAN* * Hugo de Vries-Laboratory, Uniersity of Amsterdam, Kruislaan 318, 1098 SM Amsterdam and † FOM Institute of Atomic and Molecular Physics, Unit for Mass Spectrometry of Macromolecular Systems, Kruislaan 407, 1098 SJ Amsterdam, The Netherlands Received: 20 June 1995 Accepted: 30 August 1995 Mature seed coats of representatives of all three genera of Musaceae were analysed for macromolecular composition with various mass spectrometric techniques and compared with scanning electron microscopy and light microscopy in combination with histochemical techniques. Mass spectrometric techniques are more sensitive and more specific in identifying macromolecular compounds than histochemical methods. The macromolecular ‘fingerprint’ of the seed coats of Musaceae showed unique components of aromatic phenols. The seed coat structure of all three genera is homogeneous within the Musaceae. It is characteristic at the family level and most complex within the Zingiberales. Very remarkable are the separation of the outer cell walls from the exotestal layer, exposing a secondary surface with silica crystals, and the relatively thick mesotesta which protects the seed, e.g. against the biting forces and passage through the digestive tracts of dispersing agents. Germination takes place with an operculum and is facilitated by a predetermined rupture layer in the micropylar collar. The musaceaous seed presents a good example of the solution of conflicting demands of protection and germination. # 1996 Annals of Botany Company Key words: Musaceae, Musa, Ensete, Musella, seed coat, pyrolysis (gas chromatography) mass spectrometry, histochemistry, anatomy, macromolecules, silica, lignin, cellulose, vegetable polyphenols, operculum, germination. to which the bananas belong, there are three genera: Musa INTRODUCTION L., with about 35 species, Ensete Bruce., with three species Hardly anything is known about the chemistry of seed and a more obscure genus Musella (Fr.) C. Y. Wu with one coats. The biochemical and histochemical literature on species. The acceptance of the Musella as a distinct genus is seeds is almost fully focused on the composition of storage only provisional (Manchester and Kress, 1993). A number material in embryo and endosperm. The functional in- of genera formerly mostly included in the Musaceae are terpretation of the seed coat is an almost unexplored field of nowadays placed in the separated families Strelitziaceae, research, because of the lack of reliable data on the presence Heliconiaceae and Lowiaceae (Nakai, 1941; Tomlinson, and distribution of macromolecular components. Currently 1962; Cronquist, 1981; Dahlgren and Rasmussen, 1983). it is possible to describe the anatomy in more detail with Each taxon possesses a comparable range of anatomical microscopical and histochemical techniques and to study variation which overlaps to a minimum with other groups the macromolecular composition of the testal layers of the within the Zingiberales (Tomlinson, 1962). The family is mature seed with mass spectrometrical techniques. tropical-subtropical Asian (Musa, Musella) and African In source pyrolysis mass spectrometry (PyMS) is a relative (Ensete), but Musa-cultivars are nowadays cultivated simple method to obtain information from plant tissue at troughout the tropical regions of the world. the molecular level (Boon, 1989). The PyMS analysis Most edible cultivated clones are seedless whereas other provides a chemical ‘fingerprint’ of the seed coat. Chemical plants, wild or cultivated, produce one to many seeds. identification of individual pyrolysis products is performed Breeding programs are hindered by the low seed set, as well by using pyrolysis gas chromatography (PyGC) combined as by slow and non-uniform germination (Shepherd, 1954; with mass spectrometry (PyGCMS). Stotzky, Cox and Goose, 1962). The ovary of Musa is three The order Zingiberales is a well-defined and coherent locular, contains numerous ovules, and develops into a taxon. Within this order there are questions about the longish berry. The fruit of Musa contains a higher number relation of seed coat structure and chemistry to germination. of seeds than that of Ensete. The seeds rarely attain 1 cm in The Musaceae represents the most basal lineage in the order diameter, whereas the seeds of Ensete are mostly larger, up (Manchester and Kress, 1993). This basal position of the to 1±8 cm, although there may be some overlap in size. The Musaceae, its special type of germination and its well- shape of the seeds varies greatly, is often irregularly and differentiated seed coat forms an interesting subject to study sharply angular, either rarely globose or smooth. The the relation of structure, macromolecular composition and variability in shape of the pale or dark brown to black seeds functions of the testal layers, and moreover to produce a is due to compression between neighbouring seeds new data set relevant for macrosystematic research. (Simmonds, 1960). The embryological literature has been In most recent classifications the family of the Musaceae, summarized by Davis (1966), that on seed anatomy by 0305-7364}96}020105­18 $12.00}0 # 1996 Annals of Botany Company 106 Graen et al.—Composition of Musaceaous Seed Coats Netolitzky (1926) and Takhtajan (1985). In earlier studies with a hexane}dichloromethane mixture (1:1 v}v), after 3 h McGahan (1961a) described the anatomy of the seed of it was centrifuged, the pellet was suspended in deionized Musa balbisiana and Bouharmont (1963) the development water, dried and extracted with an ethanol}acetone mixture of the ovule to mature seed in Musa acuminata. (1:1 v}v) for another 3 h, and finally washed several times The ovule is anatropous, bitegmic, and crassinucellar, in deionized water. The homogenized and extracted seed with a multi-layered outer integument and a thin inner coat material was suspended in a few drops of water. integument. The micropylar part of the seed coat develops into an operculum or seed lid. This operculum is surrounded Transmethylation by a characteristic micropylar collar. During germination the seed lid is displaced by the elongating radical-hypocotyl For methylation of phenolic hydroxyl and carboxyl axis (McGahan, 1961b). The mature seed contains mainly groups, a small droplet of 2±5% (w}v) tetramethyl- endosperm, which is copious, starchy and mealy, with large, ammonium (TMAH) was added to the wet sample on the eccentric, compound starch grains, and some perisperm wire of the direct insertion probe prior to PyMS and (Cronquist, 1981). The endosperm is initially nuclear, PyGCMS experiments. becoming cellular later, and extends during its development at the expense of the perisperm. The embryo remains Silylation relatively small, is situated under the operculum and is partly enclosed by the micropylar collar. In the ovular stage An off-line pyrolysate was prepared by placing a few a trichomatous aril develops out of the funicle surrounding drops of an aqueous suspension of extracted seed coat on a the seed coat (Netolitzky, 1926; Friedrich and Strauch, wire with a Curie point of 510 mC. The wire was dried under 1975). According to Friedrich and Strauch (1975) the aril rotation in vacuum. After drying the wire was placed in a becomes reduced and only some small vestiges can be found glass liner and the glass liner was flushed for a minute with near the funicle on the mature seed. argon, directly followed by pyrolysis at atmospheric Seeds of Ensete can be distinguished from those of Musa pressure. The procedure was repeated several times with a by a rimmed hilar depression that is nearly as wide as the new wire in the same glass liner and the final condensate seed itself. Seeds of Musella resemble those of Musa, being that formed on the inner wall of the glass liner was collected. distinguished from Ensete by the lack of a wide hilar Silylation of the off-line pyrolysate was performed by depression and rim (Manchester and Kress, 1993). Most adding 70 µl of BSTFA}TMSCL [N.O.bis(TMS) species of Musa have a rough verrucate seed coat, whereas trifluoroamide}trimethylchlorosilane] in 235 µl pyridine to the seed coat of Musella and Ensete is smooth. the sample in the dark. After 24 h the pyridine was In this study data from scanning electron microscopy evaporated by flushing with nitrogen and the reaction (SEM), light microscopy (LM), histochemistry and mass product was resuspended in dichloromethane and analysed spectrometry are compared, to acquire insight into the with GCMS.
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