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(American Journal of Botany. 2001;88:1935-1944.)
© 2001 Botanical Society of America, Inc.

Anatomy and Morphology

Structure and ultrastructure of leaf and calyx glands in Galphimia brasiliensis (Malpighiaceae)1

María A. Castro2,4, Andrea S. Vega3 and María E. Múlgura3

2Laboratorio de Anatomía Vegetal, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, 1428 Buenos Aires, Argentina; and 3Instituto de Botánica Darwinion, Labardén 200, C.C. 22, 1642 Buenos Aires Argentina

Received for publication December 12, 2000. Accepted for publication April 3, 2001.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The present study describes the anatomical structure of calyx and leaf glands in Galphimia brasiliensis and analyzes the mechanism of secretion. The glands are marginal and suprabasal, cup-shaped, sessile, and scarcely visible with the naked eye. Light microscopy reveals the following features: a thin, smooth cuticle; unistratified secretory cells; subglandular parenchyma; and vascular bundle supply composed of phloem and xylem with abundant druses of calcium oxalate. Transmission electron microscopy reveals the presence of secretory cells with conspicuous nuclei, dense cytoplasm, lipid droplets, numerous vesicles, mitochondria, Golgi, rough endoplasmic reticulum (RER), and elongated plastids with osmiophilic contents. The secretion reaches the apoplastic space and accumulates beneath the cuticle. Finally, the viscous, translucent exudate is eliminated by mechanical rupture of the cuticle. Histochemical analysis confirms that lipids are the main constituent. Small amounts of polysaccharides were also identified.

Key Words: anatomy • calyx glands • Galphimia brasiliensis • leaf glands • Malpighiaceae


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The family Malpighiaceae includes ~66 genera and 1200 species and is distributed in tropical and subtropical regions of both hemispheres (Anderson, 1990 ). Nearly 950 species are endemic to the New World, northern South America being the major center of diversity (Anderson, 1979 ).The Malpighiaceae show an important variation in habitat preferences, types of fruits (Anderson, 1979 ), pollen morphology (Lobreau-Callen, 1984 ), and chromosome numbers (Fouët, 1966 ), although flowers are very similar in morphology ("floral conservatism"; see Anderson, 1979 ) and in different aspects of their floral biology.

The presence of calyx glands disposed in pairs constitutes a derived character of the Malpighiaceae (Anderson, 1990 ) and represents a character with diagnostic value in this family. Generally, the New World species have abaxial glands on the sepals that contain lipids (Vogel, 1974 ; Anderson, 1990 ) whose function is to attract pollinators, while leaf blades have two extrafloral nectaries in their lower third. Several authors (e.g., Hauman-Merck, 1912 ; Raw, 1979 ; Steiner, 1985 ; Sazima and Sazima, 1989 ; Vogel, 1990 ) have mentioned a close association between the Malpighiaceae and bees of Anthophoridae subfamily, which collect lipids or pollen and lipids (Raw, 1979 ) with specialized organs. The structure and position of the oil-collecting organs are correlated with the types of oil glands used by different bees (Neff and Simpson, 1981 ). In the Malpighiaceae, bees of the tribe Centridini are intimately associated with plants that have glands with a layer of active secretory epithelial cells (Neff and Simpson, 1981 ).

Hauman-Merck (1912) mentioned the presence of nectar in calyx glands of Stigmaphyllon Adr. Juss., but according to Lobreau-Callen (1989) , while in Malpighiaceae species in the New World the calyx glands produce lipids and traces of carbohydrates, it is the opposite in Old World species. Vogel (1990) uses this argument to support his idea about the transformation of the secretions in calyx glands from nectar to lipids.

The genus Galphimia Cav. belongs to the tribe Galphimieae of the subfamily Byrsonimoideae within the Malpighiaceae (Anderson, 1977 ). Galphimia includes approximately ten species in tropical and subtropical America, with a disjunct distribution (Niedenzu, 1928 ). Most of the species grow in Central America; only one, Galphimia brasiliensis (L.) Adr. Juss., grows in South America (northeastern Argentina, southern Brazil, Bolivia, Paraguay, and Uruguay). In the genus Galphimia, calyx glands are greatly reduced or absent (Anderson, 1977 ), and G. brasiliensis has been considered to be in the group of species lacking them (Niedenzu, 1928 ; Lobreau-Callen, 1989 ). However, we observed that calyx glands are present in variable sizes, numbers, and positions within each flower.

The objective of this research was to analyze the structural and ultrastructural anatomy and to identify the chemical composition of the leaf and calyx glands in Galphimia brasiliensis in order to verify the homology of both structures.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Plant materials
Both herbarium specimens and fresh material of Galphimia brasiliensis (L.) Adr. Juss. were studied, and voucher specimens were deposited in SI Herbarium (Instituto de Botánica Darwinion). (See Table 1.)


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  		Table 1. Studied materials of Galphimia brasiliensis (L.) Adr. Juss

 
Anatomical studies
Leaves and flowers of G. brasiliensis were fixed in FAA (formalin : ethanol : acetic acid) and then stored in 70% ethanol. The material was dehydrated in an ethanol-alcohol series and embedded in paraffin after infiltration in a vacuum oven. Transverse and longitudinal sections 10 µm thick were cut on a rotary microtome and were double-stained with Safranin-Fast Green (D'Ambrogio de Argüeso, 1986 ). They were examined under a ZEISS (Zeiss, Oberkochen, Germany) Phomi III microscope with and without polarized light.

Histochemical tests for light microscopy were used to detect the possible presence of lipids and polysaccharides in the glandular exudates. Longitudinal sections of fresh material were stained with Sudan Black B to detect lipids (Gahan, 1984 ) and PAS reaction (periodic acid Schiff) for polysaccharides (O'Brien and McCully, 1981 ).

The blades were cleared following the Dizeo de Strittmater technique (1973) ; the type of veination and the position of the glands in the leaf are described in accordance with the terminology proposed by Hickey (1974) .

Light microscopy (LM) studies were made using a Zeiss optic photomicroscope and black and white Kodak Tmax 100 ASA film (Kodak, Rochester, New York, USA). For light microscopy, glands were prepared as for TEM, and sections 1 µm thick were stained with toluidine blue.

For scanning electron microscopy (SEM), glands were removed from herbarium specimens, coated with a gold-palladium alloy, and observed in a Zeiss DSM 940 A scanning electron microscope at the Instituto de Botánica Darwinion, Argentina.

For transmission electron microscopy (TEM), leaf and calyx glands at different stages of development were fixed in 3% glutaraldehyde in 0.1 mol/L phosphate buffer for 3 h at room temperature, washed in buffer, and postfixed in 1.5% osmium tetroxide with the same buffer for 1.5–2 h, dehydrated in an acetone series, and embedded in Spurr resin. The ultrathin sections were cut with glass knives, stained with uranyl acetate followed by lead citrate, and examined in a TEM (JEOL, Tokyo, Japan) JEM 1200 EX II microscope.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
General characters
Galphimia brasiliensis is a small suffrutescens ~50 cm high (Fig. 1) and generally grows in grasslands with sandy and rocky soils. The leaves are opposite and have two linear stipules 1–4 mm long; petioles are 2–4 mm long and are glabrous and glandless (Fig. 2). Blades are 1.5–5.5 cm long and 0.5–1 cm wide, elliptic or narrowly elliptic, glabrous, glaucous, and have an acute apex and brochidodromous venation. In particular, the blades have two extrafloral glands of marginal and suprabasal position (Figs. 2–4).



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  		Fig. 1. Galphimia brasiliensis. (A) Habit. Bar = 1 cm. (B) Flower, detail. Bar = 1 mm. (C) Fruit. Bar = 1 mm

 


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  		Figs. 2–4. Leaf glands. 2. Fragment of the plant showing stipules, petioles, and a pair of opposite leaves with marginal and suprabasal glands. Bar = 1 mm. 3. Leaf gland, detail. Bar = 0.5 mm. 4. Position of leaf glands, detail. Bar = 1 mm. B, blade; EX, exudate; G, gland; P, petiole; S, stipule

 
The inflorescences are terminal, many-flowered pseudoracemes, ~20 cm long. The flowers are zygomorphic and are 1.2 cm in diameter (Figs. 1, 5). The calyx consists of five oval, greenish sepals (2.5–4 mm long), with glands located in marginal and suprabasal position (Fig. 6). The lemon-yellow corolla has imbricate aestivation; it consists of four oval lateral petals (5 mm long) and one oblong posterior petal (also called a "banner petal"; 7.5 mm long). Calyx and corolla become reddish at maturity as a postpollination phenomenon.



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  		Figs. 5–6. Calyx glands. 5. Flower, general aspect. Bar = 5 mm. 6. Gland with exudate, detail (arrow). Bar = 1 mm

 
The androecium has ten stamens with subulate filaments (2 mm long) and oblong anthers (1 mm long).

The gynoecium is composed of a tricarpelar and triovulate ovary, with subulate styles (4 mm long). The fruit is a septicidal and loculicidal capsule (Fig. 1) (Múlgura, in press ).

The zygomorphy of the flowers in G. brasiliensis is based on the difference in the form and size of the petals, the imbricate aestivation of the corolla, and the variation in the number and position of the calyx glands. Although the effective pollinator of this species was not detected, the symmetry of these flowers admits only one approach by the visiting insect.

Morphology and anatomy of glands
Leaf and calyx glands exhibit similar structural and ultrastructural organization. Glands are 0.2–0.3 mm high and 0.35–0.4 mm broad, sessile, cup-shaped, with a central slight concavity (Figs. 3, 6–8) are scarcely visible with the naked eye except for the slightly pedicellate leaf and calyx glands observed in the specimen Burkart 7889 (SI).

Light microscopy of longitudinal sections of glands shows these features, from the outside in: cuticle, secretory tissue, a central core of subglandular parenchyma cells, and vascular supply bundles (Figs. 9–11, 14–17). The cuticle is smooth and thin (Figs. 7, 8, 14, 16). The unistratified secretory tissue is composed of tightly packed elongated cells, which form a palisade layer involved in the synthesis and secretion of the exudate. The secretory cells are high and narrow (45.5–71.5 µm long and 7.8–13 µm wide), thin-walled (Fig. 9), and characterized by a densely staining cytoplasm and a relatively large nucleus (Figs. 14, 17). The subglandular parenchyma consists of six to seven layers of isodiametric cells with reduced intercellular spaces. Vascular supply of xylem and phloem reaches the periphery of the subglandular tissue (Figs. 16, 17). High concentrations of calcium oxalate druses (Figs. 12, 13) and a few cubic crystals were observed in this area. The latter are not birefringent in polarized light.



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  		Figs. 9–13. Leaf glands in longitudinal section, LM micrographs. 9–11. Different stages of secretion process. 9. Initial stage: secretory cells and cuticle. Bar = 100 µm. 10. Cuticle unlinked from the secretory cells. Bar = 100 µm. 11. Rupture of the cuticle. Arrows mark point of mechanical rupture (arrow). 12–13. Calcium oxalate crystals in cleared blade. Bar = 100 µm. 12. Without polarized light. Bar = 100 µm. 13. With polarized light. Bar = 100 µm. D, druses; C, cuticle; SC, secretory cells; SP, subglandular parenchyma; VB, vascular bundle

 


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  		Figs. 7–8. Leaf glands, SEM micrographs. 7. Upper view. Bar = 50 µm. 8. Lateral view. Bar = 50 µm

 


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  		Figs. 14–15. Active leaf glands, sections 1 µm thick, LM micrographs. 14. Initial stage: smooth cuticle, secretory cells, subglandular parenchyma. Bar = 50 µm. 15. Exudate beneath the cuticle. Bar = 50 µm. C, cuticle; EX, exudate; SC, secretory cells; SP, subglandular parenchyma

 


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  		Figs. 16–17. Active calyx glands in longitudinal sections, LM micrographs. 16. Initial stage. Bar = 100 µm. 17. Secretory stage. Bar = 50 µm. C, cuticle; SC, secretory cells; SP, subglandular parenchyma; VS, vascular bundles

 
Transmission electron microscopy observations reveal that the dense appearance of the cytoplasm results from an abundance of ribosomes, rough endoplasmic reticulum (RER), mitochondria, Golgi, numerous small and translucent vesicles, plastids, and a large vacuole containing ergastic substances (Figs. 21, 25, 30, 31). The RER is composed of narrow cisternae dispersed in cytoplasm or closely stacked near the plasma membrane (Figs. 18, 22, 26). Mitochondria are elliptic or globular, occur in great numbers and possess many well-developed cristae. They are dispersed or aggregated in the cytoplasm (Figs. 21, 28–30). Golgi are particularly present in active secretory cells and are abundant in the presecretory stage. Numerous vesicles containing convoluted membranes can be seen and probably represent deposits of membrane material synthesized by the active secretory cells. Vesicles fused with the tonoplast are observed during the synthesis of the secretory products (Figs. 22, 26). Plastids are frequent, enlarged, and unusually shaped, with starch and dense zones (Figs. 21, 24, 29, 30, 32). Large vacuoles containing dense ergastic substances mixed with other more translucent products were observed (Fig. 23). Some lipid droplets are present in the cytoplasm (Figs. 24, 26). The inner side of the outer periclinal secretory cell wall presents slight ingrowths associated with plasma membrane invagination (Fig. 18).



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  		Figs. 18–26. Secretory cells in active leaf glands, TEM micrographs. 18. Outer tangential cell wall and slight ingrowth. Bar = 500 nm. 19–20. Exudate crossing the wall: note, in Fig. 20 the exudate is reaching the subcuticular space. Bars = 1 µm. 21, 24. Plastids and mitochondria. Bars = 1 µm and 200 nm, respectively. 22. RER. Bar = 500 nm. 23. Large vacuole containing ergastic substances. Bar = 2 µm. 25. Conspicuous nucleus. Bar = 1 µm. 26. RER, lipids, and vesicles with convoluted membranes. Bar = 200 nm. C, cuticle; EX, exudate; L, lipids; M, mitochondria; P, plastids; RER, rough endoplasmic reticulum; V, vacuole; VE, vesicle; WI, wall ingrowths. respectively. 22. RER. Bar = 500 nm. 23. Large vacuole containing ergastic substances. Bar = 2 µm. 25. Conspicuous nucleus. Bar = 1 µm. 26. RER, lipids, and vesicles with convoluted membranes. Bar = 200 nm. C, cuticle; EX, exudate; L, lipids; M, mitochondria; P, plastids; RER, rough endoplasmic reticulum; V, vacuole; VE, vesicle; WI, wall ingrowths

 
In the active stage and with the onset of secretion, the exudate released into the apoplastic space flows toward the wall and begins to accumulate beneath the cuticle (Figs. 18–20, 27–29). The cuticle is smooth; neither pores nor pore-like structures were observed. Its mechanical rupture results from pressure of the accumulated exudate or the action of insect visitors (Figs. 15, 19, 20, 27).

The exudate of both glands is translucent and slightly viscous, composed mainly of lipids with small amounts of sugars (Figs. 3, 6). Histochemical tests with Sudan Black B confirm the presence of abundant lipids through an intensive dark blue stain. The PAS reaction corroborates the presence of traces of polysaccharides.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
The present study was undertaken to elucidate the structural and ultrastructural features related to the anatomy and secretion mechanism of calyx and leaf glands in Galphimia brasiliensis.

Flowers of G. brasiliensis have been considered actinomorphic by Lobreau-Callen (1989) ; however, the imbricate aestivation of the corolla and the variation in number and disposition of calyx glands are characters that determine the flower's zygomorphy. The number, size, and position of the calyx glands are variable among flowers of the same inflorescence and among inflorescences of the same plant. Although this species has been included in the group with eglandular flowers (Niedenzu, 1928 ; Lobreau-Callen, 1989 ), there may be two to zero calyx glands on each sepal. Vogel (1990) has interpreted the presence of single glands as the result of fusion of a pair of glands; however, our observation of some flowers with pairs of glands in which one of the glands was notably reduced suggests that single glands result from loss, not fusion.

Glands on leaves and sepals exhibit similar structural and ultrastructural organization. Light microscopy study of longitudinal sections reveals these features from the outside in: cuticle, secretory tissue, a central core of subglandular parenchyma cells, and vascular supply bundles. This anatomical pattern of organization is the same as that observed by Cocucci, Holgado, and Anton, (1996) in Dinemandra ericoides Adr. Juss., but in this species the secretory cells are clavate shaped and unlinked for more than 90% of their length. In G. brasiliensis, the secretory cells are elongated, tightly packed, and linked throughout their length.

The TEM observations showed that several ultrastructural changes occur with the onset of secretion. Active secretory cells exhibit a conspicuous nucleus, dense cytoplasm, lipid droplets, numerous vesicles, mitochondria, Golgi, RER, and elongated plastids with osmiophilic contents. The secretion reaches the apoplastic space and accumulates beneath the cuticle. Finally, in both types of glands, the scarce translucent exudate is eliminated by mechanical rupture of the cuticle.

Due to the reduced size of glands and the scarce exudate, only histochemical tests were made. Presence of lipids was detected with Sudan Black B. These results do not support the conclusions provided by several authors (Lobreau-Callen, 1989 ; Anderson, 1990 ; Vogel, 1990 ) who agree that in Malpighiaceae leaf glands are nectaries that produce sugars but not oils.

Calyx glands in Old World species are reported to be nectaries while these in New World species are lipophilic glands (Faegri and van der Pijl, 1979 ). Baker (1978) analyzed the lipophilic secretion of Malpighiaceae and found small amounts of sugars and amino acids. Vinson et al. (1997) analyzed the floral chemistry of Byrsonima crassifolia (L.) H.B.K. and found two types of floral oils: the most common type contained a trace of carbohydrate; the other type had large amounts of an unknown lipid that was more polar than the standards.

In both calyx and leaf glands of G. brasiliensis, the presence of abundant lipids and small amounts of sugars probably indicates that the lipophilic glands derive from nectaries. Vogel (1990) suggested that the occurrence in some nectars of small amounts of lipids and sugar traces in some floral oils supports the view that these change were feasible.

Finally, the present study confirms that leaf and calyx glands are homologous structures. According to W. and Ch. Anderson (University of Michigan, personal communication) it seems quite possible that the glands on the sepals are simply a continuation of the expression of the genes from the leaves, and that the real function of the glands, assuming there is one, has to do with their role on the leaves. In Galphimia the calyx glands represent an independent evolution from leaf glands, providing a model that may explain the origin of the large calyx glands found in many other Malpighiaceae from the glands on the abaxial surface of the leaves in ancestral plants.



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  		Figs. 27–32. Secretory cells in active calyx glands, TEM micrographs. 27. Exudate crossing the wall (arrow). Bar = 500 nm. 28. Cytoplasm with mitochondria, wall and exudate in the apoplastic space. Bar = 500 nm. 29. Mitochondria and plastids. Note drops of exudate in the apoplastic space (arrow). Bar = 200 nm. 30. Mitochondria, plastids, and Golgi. Bar = 500 nm. 31. Conspicuous nuclei and dense cytoplasm. Bar = 1 µm. 32. Radial cell wall between two consecutive secretory cells and unusually shaped plastids. Bar = 500 nm. C, cytoplasm; EX, exudate; G, Golgi; M, mitochondria; N, nuclei; P, plastid; V, vacuole

 

   FOOTNOTES
 
1 The authors thank Dr. William R. Anderson for his critical review of the manuscript and valuable suggestions and Graphic Designer Tomás E. Aversa. This work was supported by Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, PIP 0800/98). Back

4 Author for reprint requests (mac{at}bg.fcen.uba.ar ). Back


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Anderson W. R. 1977 Byrsonimoideae, a new subfamily of the Malpighiaceae. Leandra 7: 5-18

Anderson W. R. 1979 Floral conservatism in Neotropical Malpighiaceae. Biotropica 11: 219-233

Anderson W. R. 1990 The origin of the Malpighiaceae—the evidence from morphology. Memoirs of the New York Botanical Garden 64: 210-224

Baker H. G. 1978 Chemical aspects of the pollination biology of woody plants in the tropics. In P. B. Tomlinson and M. H. Zimmermann [eds.], Tropical trees as living systems, 57–82. University Press, Cambridge, UK

Cocucci A. A. A. M. Holgado A. M. Anton 1996 Estudio morfológico y anatómico de los eleóforos pedicelados de Dinemandra ericoides, Malpigiácea endémica del desierto de Atacama, Chile. Darwiniana 34: 183-192

D' Ambrogio de Argüeso A. 1986 Manual de técnicas en histología vegetal. Hemisferio Sur Sociedad Anónima, Buenos Aires, Argentina

Dizeo de Strittmater C. 1973 Nueva técnica de diafanización. Boletín de la Sociedad Argentina de Botánica 15: 126-129

Faegri K. L. van der Pijl 1979 The principles of pollination ecology, 3rd ed. Pergamon Press, Oxford, UK

Fouët M. 1966 Contribution à l'étude cyto-taxonomique des Malpighiacées. Adansonia 6: 457-505

Gahan P. B. 1984 Plant histochemistry and cytochemistry: an introduction. Academic Press, New York, New York, USA

Hauman-Merck L. 1912 Sobre la polinización de una Malpighiácea del género Stigmaphyllon. Physis (Buenos Aires) 1: 81-87

Hickey L. J. 1974 Clasificación de la arquitectura de las hojas de las dicotiledóneas. Boletín de la Sociedad Argentina de Botánica 16: 1-26

Lobreau-Callen D. 1984 Pollen et paleobotanique des Malpighiaceae. Revue de Paléobiologie, volumen spécial: 131–138

Lobreau-Callen D. 1989 Les Malpighiaceae et leurs pollinisateurs. Coadaptation ou coévolution. Bulletin du museum national d'histoire naturelle. Section B, Adansonia:, Botanique phytochimie 11: 79-94

Múlgura M. E. In press. Malpighiaceae. In N. Bacigalupo [ed.], Flora ilustrada de Entre Ríos. Colección Científica del Instituto Nacional de Tecnología Agropecuaria 6 (4). Instituto Nacional de Tecnología Agropecuaria (INTA), Buenos Aires, Argentina

Neff J. L. B. B. Simpson 1981 Oil-collecting structures in the Anthophoridae (Hymenoptera): morphology, function, and use in systematics. Journal of the Kansas Entomological Society 54: 95-123[ISI]

Niedenzu F. 1928 Malpighiaceae. In A. Engler [ed.], Das Pflanzenreich, 141 (1-3): 1–870. Wilhelm Engelmann, Leipzig, Germany

O'Brien T. P. M. E. McCully 1981 The study of plant structure: principles and selected methods. Termarcarphi PTY, Melbourne, Australia

Raw A. 1979 Centris dirrhoda (Anthophoridae), the bee visiting West Indian cherry flowers (Malpighia punicifolia). Revista de Biología Tropical 27: 203-205

Sazima M. I. Sazima 1989 Oil-gathering bees visit flowers of eglandular morphs of the oil-producing Malpighiaceae. Botanica Acta 102: 106-111[ISI]

Steiner K. E. 1985 Functional dioecism in the Malpighiaceae: the breeding system of Spachea membranacea Cuatr. American Journal of Botany 72: 1537-1543[CrossRef][ISI]

Vinson S. B. H. J. Williams G. W. Frankie G. Shrum 1997 Floral lipid chemistry of Byrsonima crassifolia (Malpighiaceae) and a use of floral lipids by Centris bees (Hymenoptera: Apidae). Biotropica 29: 76-83[CrossRef][ISI]

Vogel S. 1974 Ölblumen und ölsammelnde Bienen. Tropische und Subtropische Pflanzenwelt 7: 1-267

Vogel S. 1990 History of the Malpighiaceae in the light of pollination ecology. Memoirs of the New York Botanical Garden 55: 130-142




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