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AOBPreview originally published online on March 12, 2007
Annals of Botany 2007 99(4):755-763; doi:10.1093/aob/mcm011
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© The Author 2007. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Pollen, Tapetum and Orbicule Development in Modiolastrum malvifolium (Malvaceae)

Beatriz G. Galati*, Federico Monacci, Marina M. Gotelli and Sonia Rosenfeldt

Depto. Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Pab. II, Ciudad Universitaria, C1428EHA, Buenos Aires, Argentina

* For correspondence. E-mail galati{at}bg.fcen.uba.ar

Received: 3 November 2006    Returned for revision: 29 November 2006    Accepted: 11 December 2006    Published electronically: 12 March 2007


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 

Background and Aims: Although orbicular functions are still a matter of debate, they are considered by most authors to be exclusively formed by a secretory tapetum. However, the presence of orbicules on a peritapetal membrane associated with a plasmodial tapetum has been described for Abutilon pictum (Malvaceae) in a previous study. Thus, studies on other species of Malvaceae are necessary to corroborate the presence of such bodies in other members of the family. Pollen and microsporangium development of Modiolastrum malvifolium has been studied in this work.

Methods: Anthers at different stages of development were processed for transmission electron microscopy and light microscopy. Membranes and pollen walls resistant to acetolysis were isolated from whole anthers.

Key Results: Microspore tetrads have a tetrahedral arrangement. Pollen grains are shed at the bicellular stage. The tapetum is invasive, non-syncytial and a peritapetal membrane with orbicules is formed.

Conclusions: This is the first report of the presence of orbicules on a peritapetal membrane in a species with a tapetum of an invasive, non-syncytial type. Taking into consideration all the information on the subject, it can be concluded that the presence of orbicules is not a stable criterion to differentiate between a secretory or plasmodial, or intermediate invasive, non-syncytial tapetum.

Key words: Modiolastrum malvifolium, invasive non-syncytial tapetum, orbicules, peritapetal membrane


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
A previous ultrastructural ontogenetic study on pollen development of Abutilon pictum has revealed the presence of a peritapetal membrane with Ubisch bodies or orbicules in the mature anther (Strittmatter et al., 2000). In this species, orbicules as well as the membrane are formed from a plasmodial-type tapetum. The presence of orbicules associated with a peritapetal membrane had not been described before for any other species of Angiospermae.

Although the functions of orbicules are still under discussion, they are considered by most authors to be exclusive of secretory tapeta (Raghavan, 1997; Huysmans et al., 1998; Furness and Rudall, 2001).

Ultrastructural studies on other species are required in order to ascertain whether orbicules are present in other members of the Malvaceae family. Since nothing was known about the embryology of Modiolastrum (Johri et al., 1992), pollen and microsporangium development of M. malvifolium has been studied under light and transmission electron microscope.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Samples of Modiolastrum malvifolium (Griseb.) K. Schum, were collected from garden populations in Zárate, Province of Buenos Aires, and were fixed in FAA (formalin : ethanol : acetic acid : water, 10:50:5:35 voucher : B. G. Galati. 691. Department of Biodiversidad y Biología Experimental, FCEyN, UBA).

For transmission electron microscopy (TEM), anthers at different developmental stages were pre-fixed in 3 % glutaraldehyde in phosphate buffer (pH 7·2) at 2 °C for 2 h and then post-fixed in OSO4 at 2 °C in the same buffer for 3 h. They were dehydrated in an ethanol series and embedded in Spurr's resin (O'Brien and McCully, 1981). Fine sections were prepared using a Sorval ultramicrotome, and stained with uranyl acetate and lead citrate. They were observed and photographed using a JEOL 100C TEM (JOEL USA, Inc. Peabody, MA).

For light microscopy, 1·5-mm thick sections of resin-embedded tissue were prepared and stained with toluidine blue. Anthers were also fixed in FAA, dehydrated in an ethanol series and embedded in paraffin. Sections were cut with a rotatory microtome, stained with safranin-fast green or crystal violet, mounted in synthetic resin and photographed with a Zeiss photomicroscope.

The callosic walls were stained with 0·01 % aniline blue, which imparts a yellow fluorescence to callose (O'Brien and McCully, 1981).

Membranes and pollen walls resistant to acetolysis were isolated from whole anthers. The acetolysis was carried out by a modification of Erdtman's method (1960; Genise et al., 1990). Structures resistant to acetolysis were washed with water and mounted in glycerine-jelly. A Zeiss fluorescence microscope was used to study autofluorescence.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Anther ontogeny of M. malvifolium presents six stages of development, thus allowing further comprehension of the ultrastructural details of the formation of pollen grains, the tapetum and the Ubisch bodies.

Stage 1: microspore mother cell (MMC)
The young anther wall consists of an epidermis, endothecium, one middle layer and a tapetum with uninucleate cells (Fig. 1A). Tapetal cells show a conspicuous nucleus and a cytoplasm with small vacuoles, a few endoplasmic reticula of rough type (ERr), plastids, mitochondria and lipid globules (Fig. 2A, B). Cells that will form the endothecium and the middle layer tissues present larger vacuoles and a cytoplasm poorer in organelles (Fig. 2A). Epidermal cells show an electron-dense cytoplasm and the tangential external wall is thickened (Fig. 1A).


Figure 1
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  		FIG. 1. Modiolastrum malvifolium, anther transversal sections under a light microscope. (A) Microspore mother cell stage (mmc). (B) Free, young microspores (m) stage: tapetal cells (tc) with lobules are towards the interior of the locule. (C) Mature microspore (m) stage. The exine wall is formed, tapetal cells (tc) with lobules are more conspicuous. Scale bars = 20 µm.

 


Figure 2
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  		FIG. 2. Microspore mother cell stage observed with a TEM. (A) Microspore mother cell (mmc), tapetal cells (tc), middle layer (ml), endothecium (en). (B) Detail of the microspore mother cell: cytoplasmic connections (arrow), mitochondria (m), nucleus (n) and dictyosomes (d). Scale bars = 2 µm.

 
The microspore mother cell possesses a nucleus of great volume with a conspicuous nucleoli and a dense cytoplasm (Fig. 2A). The latter is filled with numerous small vacuoles and mitochondria, some of these in division. Abundant ERr and some dictyosomes are also observed. There are numerous cytoplasmic connections between these cells and a callosic wall is beginning to form between the plasmalemma and the primary wall (Fig. 2A, B).

Stage 2: microspore tetrads
Tapetal cells walls are degraded and the tapetal nuclei divide. The middle layers are compressed (Fig. 3A).


Figure 3
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  		FIG. 3. (A) Microspore tetrade stage, under a light microscope. (B, C) Observations under an epifluorescence microscope. (B) Microspore tetrad, with fluorescence induced by the callose stained with aniline blue. (C) Autofluorescense of the sporopollenin of the exine wall and orbicules (arrow). Scale bars = 20 µm.

 
The ultrastructure of the cytoplasm of tapetal cells is similar to that presented in the previous stage.

Microspore mother cells undergo simultaneous meiosis, forming tetrads with a tetrahedral arrangement (Fig. 3A). These are surrounded by a thick callosic wall that is fluorescent when stained with aniline blue and irradiated with 365-nm light (Fig. 3B). The cytoplasm of microspores shows numerous free ribosomes, some mitochondria, and abundant plastids and dictyosomes (Fig. 4A, B). At this stage, the primexine fibrilar matrix is starting to develop. On it, the future basal layer, probacula and protectum can be seen as more electron-dense zones (Fig. 4C).


Figure 4
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  		FIG. 4. Microspore tetrad stage observed under a TEM. (A) General aspect of a microspore surrounded by callose wall (arrows). (B) Detail of the microspore cytoplasm with abundant ribosomes and dictyosomes (d). (C) Detail of the beginning of microspore wall formation, with primexine, probacules and protectum. Numerous plastids (p) are observed in the microspore cytoplasm. Scale bar A: 1 µm, B–C: 500 nm.

 
Stage 3: free, young microspores
At this stage, in the inner tangential faces of the tapetal cells an incipient lobe starts to grow towards the locule (Fig. 1B). The tapetal cytoplasm shows a great amount of ERr, whose cisterns appear in a parallel disposition. Abundant dictyosomes are also observed (Fig. 5A, B).


Figure 5
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  		FIG. 5. Observations made under a TEM. (A, B) Free, young microspore stage. (A) Detail of a three-nuclei (n) tapetal cell with elaioplasts (e), abundant ERr and pro-Ubisch (arrow) developing in towards the middle layer, young endothecium. (B) Detail of the radial and tangential inner wall of two tapetal cells (tc) and part of a microspore (m). (C) Microspore with exine wall formed, the peritapetal membrane folded with orbicules (or), and part of a tapetal cell (tc). Scale bars = 1 µm.

 
A membrane is formed over the outer tangential wall of the tapetal cells and in touch with the middle layer. On its inner surface, future orbicules are observed as electron-dense corpuscles (Fig. 5A).

Once the callosic wall disintegrates, microspores are freed. An electron-dense fibrilar substance fills the locule and deposits over the pobacules and protectum (Figs 5B, 6C). There are no differences between the cytoplasm of the microspores at this stage and at the previous stage (Fig. 6C).


Figure 6
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  		FIG. 6. Observations made under a TEM. (A) Peritapetal membrane (arrow) with orbicules (or), and part of an endothecium cell (en). (B) Detail of an orbicule. (C–E) Sequence of pollen grain wall development. (C) Free, young microspore stage: plastid (p), dictyosomes (d); sporopollenin precursors laying over probacules and protectum. (D) Free microspore stage: exine wall not yet compressed; tc, tapetal cell. (E) Mature pollen grain stage: exine wall compressed and filled with tapetal derivates between columellae (arrow); a, amiloplasts. Scale bars: A, E = 1 µm; B, C = 200 nm; D = 500 nm.

 
Stage 4: microspores with a developed exine wall
The lobe of the tapetal cell grows towards the anther locule (Fig. 1C); however, the ultrastructural characteristics of the tapetum remain the same.

The exine wall of the microspores is formed by a basal layer, numerous columellae close to each other, and a thick tectum (Fig. 6D). At this stage, the apertures of the future pollen grains and the intine oncus are formed.

Stage 5: young pollen grain
Tapetal cells do not lose their individuality as they invade the anther locule and surround pollen grains (Fig. 7A).


Figure 7
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  		FIG. 7. Anther transversal section observed under a light microscope. (A) Young pollen grain (pg) stage: tapetal cells (tc) invading the locule. (B) Mature pollen grain stage. Remains of the tapetum, anther wall: epidermis, mature endothecium and peritapetal membrane with orbicules (arrow). Scale bars = 20 µm.

 
The peritapetal membrane is folded and very electron-dense corpuscules are observed on it (Fig. 5C).

The generative cell formed by a mitotic division of the microspore occupies a parietal position. Pollen grains show a very thick wall with an echinate tectum (Fig. 7A).

Stage 6: mature pollen grain
At this stage, tapetal and middle layer cells are mostly degraded (Fig. 7B). The peritapetal membrane is no longer folded, due to an increase in volume of the anther, and it is in direct contact with the endothecium (Figs 7B, 6A). In the latter, cells develop lignified thickenings of the secondary wall, formed as bands through their radial and tangential walls (Figs 7B, 6A).

Solid orbicules, without a central core and of piriform aspect are found on the peritapetal membrane (Fig. 6B). These are fluorescent and react to stains (Crystal violet and toluidine blue) in the same way that the pollen grain exine does (Figs 3C, 7B) and are resistant to acetolysis, as the peritapetal membrane.

The pollen grain wall becomes thinner and collumella separate due to its increase in volume. The exine is more compacted. It has collumella on a thick basal layer and conspicuous supratectum spines. The exine has a very thin endexine layer, and a fibrilar intine with numerous invaginations coated by the plasmalemma can be observed. Some tapetal derivates are left between the collumella (Fig. 6E).

Inside the vegetative cell cytoplasm there can be found extensive cisterns of the ERr, numerous mitochondria and abundant amyloplasts (Fig. 8A, B). The generative cell is completely enclosed by the cytoplasm of the vegetative cell. The former possesses a conspicuous nucleus and a reduced cytoplasm with scarce mitochondria and bodies with concentric intravacuolar membranes. It presents a thin, irregular wall that is transparent to electrons (Fig. 8B).


Figure 8
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  		FIG. 8. Mature pollen grain observed under a TEM. (A) General aspect of the pollen grain: generative cell (arrow) surrounded by the vegetative cell; vn, vegetative nucleus. (B) Detail of the generative cell, with a conspicuous nucleus (gn), reduced cytoplasm with some plastids (p), thin, electron-transparent irregular wall. The vegetative cell cytoplasm presents abundant thickened cisterns of the ERr, mitochondria (m) and amiloplast (a). Scale bars: A = 2 µm; B = 500 nm.

 
The generative cell is surrounded by numerous vesicles with a fibrilar content of low electron density in contact with more and smaller vesicles (Fig. 8B). Both kinds of vesicles are also regularly dispersed throughout the rest of the cytoplasm of the vegetative cell.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
At the microspore mother cell (MMC) stage numerous cytoplasmic connections are observed while the callose wall starts to form and the primary wall is still present. The existence of such connections has been reported for many angiosperms (Heslop-Harrison, 1964, 1966a, b). Lycopersicum presents some plasmodesmata, the diameter of which may allow the passage of small plastids (Pacini and Cresti, 1978; Polowick and Sawhney, 1992). It seems that only small particules could pass through these connections in M. malvifolium. According to Heslop-Harrison (1964, 1966a, b), these connections allow a synchronic development of the archesporium.

The mitochondria and dictyosomes found on the cytoplasm of the MMC suggest great metabolic activity. Due to the activity of the dictyosomes, numerous vesicles in the cytoplasmic periphery are present. This indicates the possible role of dictyosomes in the production of callose (Heslop-Harrison, 1966a).

The generative cell of the mature pollen grain is enclosed by the vegetative one, and is surrounded by lots of low-electron-density vesicles, which are associated with a great number of small vesicles. The former are reminiscent of ‘p-particles’ described for pollen grains of some species of gramineae; these particles are bodies that possess polysaccharide precursors of wall reserves derived from dictyosome activity (Heslop-Harrison and Heslop-Harrison, 1992; Heslop-Harrison and Heslop-Harrison, 1993; Heslop-Harrison et al., 1997).

Due to the presence of a myosinic cover of the p-particles and of actin fibrils in the cytoplasm of the vegetative cell of some species, its function seems to be related to cellular motility based on the interaction between actin and myosin (Heslop-Harrison et al., 1997). The vesicles observed in M. malvifolium may have a similar function, related in this case to the movement of the generative cell during pollen-tube germination. An immunocytochemic study of the presence of myosin and actin in these vesicles would be necessary to corroborate its function.

At the free microspore stage, a material with a similar electron density to sporopollenin fills the whole locule and deposits over the pollen grain wall. Similar observations have been recorded in Jacaranda mimosifolia (Galati and Strittmatter, 1999), Passiflora ssp. (Amela García et al., 2002) and Oxalis articulata (Rosenfeldt and Galati, 2005). Such material might be considered to be one of the sporopollenin precursors originated by the tapetum (Heslop-Harrison, 1971).

In M. malvifolium, tapetal cells loose their walls and become multinucleate at the tetrad stage, and their intrusion towards the interior of the locule begins at the microspore stage. This sequence has been observed in most of the dicotyledons that have tapeta of the plasmodial type (Pacini et al., 1985). However, in M. malvifolium tapetal cells were observed to invade and occupy the entire locule, but they did not fuse and never developed to form a true plasmodium, as each protoplast kept its individuality. This type of tapetum has been described as invasive non-syncytial, or intermediate, and according to Pacini et al. (1985) it corresponds to ‘type six’ of their classification. It has been cited for few families of the Angiosperms: Gentianaceae, Dipsacaceae, Asteraceae, Heliconiaceae (Pacini et al., 1985), Nymphaceae (Furness and Rudall, 2001), Cannaceae (Tiwari and Gunning, 1986; Furness and Rudall, 1998), Triuridaceae (Furness et al., 2002), Velloziaceae (Furness and Rudall, 2006) and Brassicaceae (Murgia et al., 1991).

According to Pacini (1990), Pacini and Franchi (1993) and Huysmans et al. (1998), one of the main characteristics of secretory tapeta is the production of orbicules. Pacini et al. (1985) considered such structures not to appear in species characterized by a plasmodial tapetum. However, there are three reports on the presence of corpuscles with electron density and structure similar to orbicules (although not confirmed as such) in plasmodial tapeta: Gentiana acaulis (Lombardo and Carraro, 1976), Butomus umbellatus (Fernando and Cass, 1994) and Tradescantia virginiana (Tiwari and Gunning, 1986; Raghavan, 1997). These reports do not indicate anything about their resistance to acetolysis or about being related to a peritapetal membrane.

Heslop-Harrison (1969) noted that there is a peritapetal membrane resistant to acetolysis in certain Compositae possessing a plasmodial tapetum. He reported that it is formed during exine deposition, but made no reference to the presence of orbicules.

In previous research on Abutilon pictum (Malvaceae; Srittmatter et al., 2000), corpuscles attached to a peritapetal membrane that surrounds the plasmodial tapetum have been observed. These corpuscles have the same reaction to colourants, the same electron density, autofluorescense and resistance to acetolysis as orbicules. This was the first account of the presence of orbicules on a peritapetal membrane (Strittmatter et al., 2000). Although M. malvifolium presents an invasive, non-syncytial tapetum, it shows similar characteristics to those cited for A. pictum.

Thus, according to the observations made in this study and in the previous report on A. pictum, it can be concluded that the presence of orbicules is not a stable criterion to differentiate between a secretory and plasmodial, or invasive, non-syncytial tapetum.


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 

    Amela García MT, Galati BG, Anton AM. (2002) Microsporogenesis, microgametogenesis and pollen morphology of Passiflora spp. (Passifloraceae). Botanical Journal of the Linnean Society 139:383–394.

    Fernando DD and Cass DD. (1994) Plasmodial tapetum and pollen wall development in Butomus umbellatus (Butomaceae). American Journal of Botany 8:1592–1600.

    Furness CA and Rudall PJ. (1998) The tapetum and systematics in monocotyledons. Botanical Review 64:201–239.

    Furness CA and Rudall PJ. (2001) The tapetum in basal Angiosperms: early diversity. International Journal of Plant Science 162:375–392.

    Furness CA and Rudall PJ. (2006) Comparative structure and development of pollen and tapetum in Pandanales. International Journal of Plant Science 167:331–348.

    Furness CA, Rudall PJ, Eastman A. (2002) Contribution of pollen and tapetal characters to the systematics of Triuridaceae. Plant Systematics and Evolution 235:209–218.

    Galati BG and Strittmatter LI. (1999) Correlation between pollen development and Ubisch bodies ontogeny in Jacaranda mimosifolia (Bignoniaceae). Beiträge zur Biologie der Planzen 71:249–260.

    Genise J, Palacios RA, Hoc PS, Carrizo R, Moffat L, Mom MP, et al. (1990) Observaciones sobre la biología floral de Prosopis (Leguminosae, Mimosoideae). II. Fases florales y visitantes en el distrito chaqueño serrano. Darwiniana 30:71–85.

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    Heslop-Harrison J and Heslop-Harrison Y. (1993) Vapour phase activation, intracellular motility and germination in the triporate pollen of Epilobium angustifolium. Botanica Acta 106:331–337.

    Heslop-Harrison J, Heslop-Harrison Y, Heslop-Harrison JS. (1997) Motility in ungerminated grass pollen: association of myosin with polysaccharide-containing wallprecursor bodies (p-particles). Sexual Plant Reproduction 10:65–66.

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