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0 Department of Biology, University of Southwestern Louisiana, Lafayette, Louisiana 70504-2451 USA
Received for publication February 1, 1999. Accepted for publication May 4, 1999.
ABSTRACT
Patterns of cytoskeletal organization during distinct polarizations that characterize pollen development in the sedge Carex blanda (Cyperaceae) were studied by correlated methods of immunohistochemistry and confocal and transmission electron microscopy. As is typical of the family Cyperaceae, Carex produces a unique pollen type known as a pseudomonad in which all four microspores of the tetrad are enclosed within the wall of a single pollen grain. Only one member of the tetrad is functional and the other three abort. The pseudomonads are precisely oriented in the locule with the functional microspore in the wide abaxial portion of the wedge-shaped cytoplasm adjacent to the tapetum, and the degenerative microspores are packed tightly in the pointed adaxial portion. A unique sequence of post-meiotic developmental events reflects both intracellular and intercellular polarity. Development includes: (1) random placement of tetrad nuclei in the coenocytic sporocyte after meiosis, (2) interrupted cytokinesis resulting in a tetrad of nuclei that migrates as a unit into the narrow adaxial tip, (3) completion of unequal cytokinesis and centering of the functional nucleus in the wide abaxial portion of the microsporocyte via a radial array of microtubules and microfilaments, (4) unequal mitosis resulting in a small generative cell at the proximal surface of the functional microspore (adjacent to the abortive microspores), and (5) recentering of the vegetative nucleus in the abaxial cytoplasm via a radial cytoskeletal array.
Key Words: Cyperaceae • cytoskeleton • development • polarity • pollen
The pollen grain represents the entire male gametophyte generation of seed plants and as such is one of the simplest multicellular plants known. Nevertheless, its ontogeny involves several distinct developmental programs, including transition from sporophytic to gametophytic generation, differentiation of vegetative and generative cells, and elaboration of the ornate pollen exine. Accordingly, the plant makes a heavy genetic investment in the complex and vital process of pollen development. The molecular and developmental biology of pollen has been the subject of several recent reviews (Bedinger, 1992
; McCormick, 1993
; Tanaka, 1997
).
The pattern of cell division leading to quadripartitioning of the microsporocyte into a tetrad of predictably arranged microspores, the positioning of the germinal apertures, and the highly polarized first pollen mitosis that produces the generative cell and the vegetative cell are striking examples of cytomorphogenesis occurring in rapid succession. We have proposed that a major component of pollen morphogenesis in these cells lacking preprophase bands of microtubules is the establishment of nuclear cytoplasmic domains via nuclear-based radial microtubule systems (RMSs) that define domains of cytoplasm and determine placement of walls (Brown and Lemmon, 1991a, 1992a, 1996
). This model assumes additional levels of developmental control through the establishment of polarity, which may be reflected in spindle orientation and nuclear migrations.
Perhaps nowhere is polarity of pollen development better expressed than in grasses (Poaceae) and sedges (Cyperaceae) where pollen morphology develops in relationship to surrounding tissues of the anther. Both of these large and diverse families of monocotyledons exhibit an unusual peripheral arrangement of pollen in which a single uniseriate cylinder of pollen grains is arranged in the anther locule so that each grain is in contact with the tapetum. However, because of major differences in the processes of pollen development, the peripheral arrangements in the Poaceae and Cyperaceae are thought to be nonhomologous (Kirpes, Clark, and Lersten, 1996
). In grasses, precise orientation of the meiotic spindles preserves the peripheral arrangement of the four microspores (reviewed by Christensen and Horner, 1974
; Kirpes, Clark, and Lersten, 1996
). The spindles of meiosis I are aligned parallel to the long axis of the anther, and cytokinesis at right angles to the locule wall results in a dyad with one cell above the other, both still in contact with the tapetum (Reeves, 1928
; Staiger and Cande, 1990
). The spindles of meiosis II are both oriented at right angles to the long axis of the anther; cytokinesis cuts off microspores side by side in an isobilateral or tetragonal arrangement in which all four microspores contact the tapetum. Each microspore develops a single germinal aperture on the surface contacting the tapetum, and the nucleus migrates to the opposite surface prior to the first pollen mitosis. Although the development of a large vacuole contributes to displacing the nucleus to the periphery (Christensen and Horner, 1974
; Raghavan, 1988
; Charzynska and Lenart, 1989
; Bedinger, 1992
), microtubules are thought be involved in the final positioning (Terasaka and Niitsu, 1990
; Bedinger, 1992
; Eady, Lindsey, and Twell, 1995
).
The establishment of polarity and its subsequent effect on pollen development are even more striking in the sedges. The unique pattern of pollen development in the Cyperaceae has fascinated botanists for over a century (reviewed by Strandhede, 1973
; Kirpes, Clark, and Lersten, 1996
), but the mechanisms controlling it have remained little understood. Pollen development in the Cyperaceae is unusual in that three of the tetrad of microspores abort and are encased along with the functional microspore in a single pollen wall. The resultant pollen grain is generally known as a pseudomonad, although other names such as cryptotetrad and monodynamosporous tetrad (see Smith-White, 1959
; Davis, 1966
) have been applied. This pattern of development is known in only one other group of plants, the tribe Styphelieae of the family Epacridaceae (Smith-White, 1959
), a phylogenetically unrelated dicotyledonous family of Australoasia. In the Cyperaceae the peripheral wedge-shaped pollen grains are arranged like sectors with the axes of polarity arranged along radii of the locule. Each pseudomonad has an adaxial pole at the center of the locule and an abaxial pole at the tapetum lining the periphery of the locule (Strandhede, 1973
). The viable microspore in the pseudomonad is always adjacent to the tapetum, and the three degenerative microspores are located in the pointed adaxial portion of the wedge-shaped pollen grain. Unlike pollen development in grasses where the meiotic spindles are under strict polar control, the meiotic spindle poles in microsporocytes of sedges appear to be randomly placed, and the axis of pollen development does not become apparent until immediately after meiosis.
We investigated the relationship of the cytoskeleton to polarization during pollen development in the sedge Carex blanda (Cyperaceae). Our hypothesis is that the regular arrangement of pseudomonads is a manifestation of polarity at both the cellular and tissue level and is associated with organization of the cytoskeleton. In this paper, we present an account of the cytoskeleton (microtubules and F-actin) during distinct migrations in the highly polarized microsporocyte/pseudomonad.
MATERIALS AND METHODS
Plant material
A large perennial population of Carex blanda Dewey growing near Lafayette, Louisiana provided the material for study. Developmental stages were determined by removing one anther from a floret for an aceto-orcein squash, and the remaining two anthers were prepared for fluorescence or electron microscopy.
Rhodamine-phalloidin fluorescence of microfilaments
Protocols for labeling F-actin follow those of Brown and Lemmon (1995)
and Cleary and Mathesius (1996)
. Microsporocytes/microspores where collected by chopping selected anthers with a thin razor blade directly into a drop of 4% formaldehyde freshly prepared from paraformaldehyde in pH 7.2 phosphate buffer containing 5% dimethyl sulfoxide on a coverslip for 30 min. Cells were covered with a film of agarose-gelatin, rinsed in buffer, and covered with a 0.33 µm solution of rhodamine conjugated phalloidin (Molecular Probes, Eugene, Oregon, USA) prepared from methanolic stock which was partially evaporated and diluted in PBS. The preparations were incubated for 3–5 h in the dark at room temperature, rinsed in buffer and mounted by inverting on a microscope slide in a drop of Mowiol 4/88 containing 0.1% phenylenediamine as an antifade reagent.
Immunofluorescence of microtubules
A complete description of the method can be found in Brown and Lemmon (1995)
. Briefly, anthers in selected stages of development were diced with a thin razor blade directly into 4% formaldehyde freshly prepared from paraformaldehyde in a microtubule-stabilizing buffer (Brown and Lemmon, 1995
) for 1 h. Fixed microsporocytes/microspores were spread onto a coverslip and covered with an agarose-gelatin film, walls digested with enzymes, and cells extracted in Triton X-100. Following a buffer wash, cells were incubated in a monoclonal antibody against yeast tubulin (YOL 1/34, Accurate Chemical and Scientific Corp., Westbury, New York, USA) for 2 h, rinsed in buffer, and incubated for 2 h with secondary antibody conjugated to fluorescein. Cells were counterstained with propidium iodide to detect nucleic acids and mounted in Mowiol as described above.
Confocal laser scanning microscopy (CLSM)
Fluorescence was examined with a BioRad MRC 600 confocal laser scanning microscope (BioRad USA, Cambridge, Massachusetts, USA). Microsporocytes/microspores were optically sectioned at 1-µm intervals. For presentation of three-dimensional spatial relationships, stereomicrograph pairs were created by assembling the successive images with a negative pixel shift in one file and positive pixel shift in a second file using BioRad Z-series projection software.
Transmission electron microscopy (TEM)
Anthers were fixed in 4% glutaraldehyde in 0.1 mol/L phosphate buffer (pH 6.9), post-fixed in 0.8% osmium ferricyanide (Hepler, 1981), dehydrated in a graded acetone series, and infiltrated with Spurr's resin (all at room temperature). Ultrathin sections were collected on grids and stained with methanolic uranyl acetate followed by lead citrate and studied with an Hitachi H-600 TEM.
Terminology
Two standard sets of terms are used in describing axes of polarity—one set in reference to the locule and the other in reference to the tetrad. In the locule, the adaxial pole is closest to the center of the locule and the abaxial pole is away from it, or adjacent to the surrounding tapetum (Strandhede, 1973
). In the tetrad, proximal is the center of the former microsporocyte and distal is at the periphery (Erdtman, 1952
).
RESULTS
Microsporogenesis
The wedge-shaped pseudomonads of C. blanda develop in a precise arrangement in locules of the anther with the viable microspore in the wide abaxial portion adjacent to the tapetal wall and the three degenerative microspores in the narrow adaxial tips (Fig. 1). This unusual arrangement is not achieved until after completion of meiosis.
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The microtubules in the complex of phragmoplasts appear to be organized into tufts with multiple foci near the nuclear envelopes and diverging ends in register on either side of a conspicuous unstained (dark) zone (Figs. 8, 9). The tufts of microtubules are clearly visible in stereo reconstruction of the complete phragmoplast complex that knits the quartet of nuclei together (Fig. 10). Ultrastructurally, the subsets of microtubules that make up the phragmoplast complex can be seen as bipolar bundles that terminate in electron-dense areas at the cell plate and converge at the nuclear envelopes (Fig. 11). Microtubules of the phragmoplast complex, which persist after deposition of cell plates, arch between peripheral surfaces of adjacent nuclei (Fig. 11), but do not expand into the cortical cytoplasm. Cell plates are deposited in the phragmoplast complex (Fig. 11), but remain thin and confined to the interzonal regions among nuclei.
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The spindle of microspore mitosis is asymmetrically located in the microspore with the generative pole terminating close to the proximal wall that separates the functional microspore from the abortive microspores (Fig. 18). Spindles may be produced in the degenerative microspores but mitosis is irregular and asynchronous (compare the two pseudomonads in Fig. 19). The chromosomes may fail to move on the spindles or they may separate and interzonal phragmoplasts may be initiated, but complete cytokinesis was never observed in the abortive microspores. The metaphase spindle of the functional microspore typically comprises a sharply focused vegetative (distal) pole and a broader generative (proximal) polar region adjacent to the poles of the abortive spindles (Fig. 18). The proximal spindle poles of the degenerative microspores converge at the generative pole of the functional microspore (Fig. 18) as if recruited by some common factor that influences spindle pole aggregation.
In the functional microspore, phragmoplast assembly is initiated in the interzone between the sister groups of chromosomes in late anaphase (Fig. 18). The phragmoplast microtubules become organized into fusiform bundles on either side of an unstained midzone and shorten as the phragmoplast expands beyond the interzone (Fig. 19). The margins of the expanding phragmoplast/cell plate curve to form a dome that surrounds the generative nucleus (Fig. 20). The phragmoplast becomes nearly spherical before joining with the proximal wall separating the functional microspore from the degenerative microspores (Fig. 21). This results in a highly asymmetric cell division that cuts off a small generative cell at the proximal pole, leaving the vegetative nucleus in the remainder of the cytoplasm (Figs. 20, 21). An RMS is produced from the vegetative nucleus as it becomes centered in the vegetative cytoplasm of the functional microspore (Fig. 22). Staining of organellar DNA shows an aggregation of organelles at the proximal surfaces of both generative cell and vegetative cell (Fig. 22).
TEM shows that in prophase of microspore mitosis the large spherical nucleus in the functional microspore is centrally located and the cytoplasm is nonvacuolate (Fig. 23). Organelles surround the nucleus and are concentrated in the region between the nucleus and the small degenerative nuclei (Fig. 23). Chromatin becomes condensed in the three abortive microspores in the narrow tip as well as in the large functional microspore (Fig. 23). The metaphase plate of the first pollen mitosis is displaced proximally, and both poles appear to terminate in regions of endoplasmic reticulum (Fig. 24). Organelles are dispersed in the cytoplasm surrounding the spindle (Fig. 24). The phragmoplast, which was initiated in the interzone (Fig. 19), curves around the generative nucleus. Phragmoplast microtubules at the margins of the hemispherical cell plate end blindly in the cytoplasm of both generative and vegetative cell (Fig. 25). The adaxial pole of a locule showing portions of two pseudomonads at a late stage of cytokinesis following microspore mitosis is shown in Fig. 22. A hemispherical cell plate surrounds the generative cell, which inherits both plastids and mitochondria (Fig. 26) as shown by fluorescence in Fig. 22.
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The peripheral arrangement of pseudomonads in Carex results from a unique sequence of developmental events (summarized diagrammatically in Fig. 27), which reflect both intracellular and intercellular polarity. The mechanism by which pollen develops in peripheral arrangement differs in grasses and sedges. In grasses, the precise orientation of meiotic spindles results in all tetrad members remaining in contact with the tapetum. In Carex, the meiotic spindles are variously placed, and the peripheral arrangement of pollen stems from an unusual manifestation of post-meiotic polarity. This difference is reflected in the mechanism of distal germinal aperture (pore) placement in the two taxa. In grasses, the pore develops at a site previously occupied by one of the meiotic spindle poles (Dover, 1972
), while in Carex development of the distal pore is not directly related to the former location of a spindle pole.
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), Carex and other members of the Cyperaceae undergo simultaneous cytokinesis upon the completion of meiosis (Shah, 1962
; Strandhede, 1973
; present study). In addition to the primary phragmoplasts between sister nuclei, secondary phragmoplasts form at interfaces of opposing arrays of microtubules emanating from nonsister nuclei as is typical of simultaneous cytokinesis (Brown and Lemmon, 1991a
). Subsequent events in Carex, however, are atypical. Normally, in simultaneous cytokinesis (Brown and Lemmon, 1991b
) the primary and secondary phragmoplast/cell plates expand to merge in the center and join with the microsporocyte wall to cleave four microspores of equal size. In Carex, the phragmoplasts join in the center of the microsporocyte but do not expand into the cortex beyond the nuclei and the radial microtubules extending from nuclei to the parental walls disappear. Narrowing of the phragmoplast complex brings the nuclei into a compact tetrahedral arrangement even though the telophase II arrangement might have been otherwise. At this time there are cell plates separating the tetrad members, but the cortical cytoplasm remains undivided. The tight quartet of nuclei, which is no longer anchored by nuclear-based radial microtubules, migrates into the narrow end of the microsporocyte. Once in the narrow end, the phragmoplasts expand and cell plates join with the parental wall. Three of the nuclei are walled off in small amounts of cytoplasm leaving the fourth nucleus in the large remaining mass of cytoplasm. Thus, the division of the cytoplasm is decidedly unequal and results in a single large functional microspore and three small nuclei, which subsequently abort. This interruption of what would normally be a mechanism of equal partitioning of the cytoplasm into a tetrad of individual spores is a key feature of pseudomonad development.
Migration of the tetrad nuclei along the abaxial/adaxial axis is the first manifestation of the intercellular polarity that dominates all subsequent events. The generative and vegetative nuclei resulting from microspore mitosis in the functional microspore will be located along this same developmental axis. The factors of induction and the mechanisms for sensing and establishing this polarity are unknown. The arrangement of microspores with respect to the locule suggests that a physiological gradient is imposed upon the microsporocytes by the surrounding tapetum (Strandhede, 1973
) and that, once established, it is maintained as an intracellular polarity throughout abortion of three microspores and polarized division of the functional microspore to produce the generative and vegetative cells (Fig. 27).
It seems likely that the position of a nucleus influences its fate, be it to abort or become the single functional nucleus. In most simple terms, one of the nuclei seems positioned to command the bulk of the cytoplasm that presumably contains, or responds to, undefined factors specifying continued development. Further evidence for this observation has been provided by cytological evidence. In pseudomonads of the related genus Eleocharis, nuclei with unbalanced chromosome numbers are as likely to survive in the larger abaxial portion of cytoplasm as are nuclei with balanced chromosome numbers (Strandhede, 1973
). A similar argument for cytoplasmic control of nuclear fate is made in analysis of pseudomonad development in the tribe Styphelieae of the family Epacridaceae (Smith-White, 1959
). Pseudomonad development in this group differs in several ways from that described in the Cyperaceae. In the Styphelieae, pollen arrangement is central (packed in the locule rather than occurring as a single layer at the periphery) and polarity appears intracellular as developing pseudomonads are random with reference to neighbors or the surrounding anther. Following meiosis, the tetrad nuclei are widely spaced in the cytoplasm and migrate to a 3 + 1 arrangement before partitioning of the cytoplasm. In some members of this group there is evidence of cytoplasmic asymmetry prior to migration, which might favor one nucleus over the others. Microspore mitosis shows an inversion of the usual polarity in that the generative cell is cut off at the distal surface rather than the proximal surface as is typical of most angiosperms including Carex. In grasses, an axis is established in each of the microspores, whereas only a single axis is functional in the pseudomonads of the Styphelieae and Carex. In the Styphelieae, the axis is intracellular only, whereas in Carex the intracellular axis (proximal/distal) is also oriented as a radius of the locule (adaxial/abaxial).
As the functional microspore begins to differentiate, an extensive cytoskeletal system of microtubules and microfilaments radiates evenly from the nucleus into the cytoplasm. This suggests that the nuclear surface serves as a major site for cytoskeletal organization during delimitation of the functional microspore. The radial systems appear to function in centering the nucleus in the enlarging microspore, defining the cytoplasm that the nucleus will control and reorganizing the cytoplasm. RMSs are involved in establishing nuclear cytoplasmic domains within coenocytes, e.g., cyst formation in Acetabularia (Menzel, 1986
), microsporocytes undergoing simultaneous cytokinesis (Brown and Lemmon, 1991a, 1992a, 1996
), megagametogenesis (Huang and Sheridan, 1994
), and early stages of endosperm development (Brown, Lemmon, and Olsen, 1994
; Olsen, Brown, and Lemmon, 1995
). In some cases, cytoplasmic domains are established by astral microtubules or plastid-based RMSs in advance of karyokinesis and the daughter nuclei are distributed into the precociously determined domains (Brown and Lemmon, 1997
; Pickett-Heaps et al., 1999
). The nuclear cytoplasmic domains play a role in spatial control of cytokinesis with phragmoplasts and cell plates positioned at the periphery of the RMS.
In most cases, phragmoplasts are triggered at the interface of opposite microtubule arrays emanating from adjacent nuclei, but in rare cases (e.g., cellularization of the embryo sac) a phragmoplast may form at the periphery of an unopposed RMS. Similarly the hemispherical cell plate in microspore mitosis after expanding beyond the interzone is unopposed in the vegetative cell and curves around the perimeter of the generative RMS (Brown and Lemmon, 1992b
; present study). Similarly, we interpret the formation of anomalous cell walls that sometimes cut off small corners of cytoplasm in the functional microspores of the Carex pseudomonad as forming at the perimeter of the domain of cytoplasm defined by the symmetrical RMS.
The next event in pollen development is alignment of the spindle axis for microspore mitosis with the predetermined polarity. In all angiosperms, the first pollen mitosis is highly asymmetric and involves reorganization of the cytoplasm including migration of the nucleus from a centric position to the periphery of the microspore (Tanaka, 1997
). In most cases, the generative nucleus is cut off at the proximal surface. However, in some cases the nucleus may migrate to the distal pole as in orchids with massed pollen (polyads) (Brown and Lemmon, 1992b
). The mechanism of asymmetric placement of the nucleus in preparation for the highly unequal pollen mitosis is not completely understood. In Phalaenopsis, nuclear migration is associated with a generative pole microtubule system (Brown and Lemmon, 1991c
), but no such system is present in the slipper orchid Cypripedium (Brown and Lemmon, 1994
) or other monocotyledons [e.g., Tradescantia (Terasaka and Niitsu, 1990
) and Carex (present study)]. Instead, a distinct perinuclear microtubule system may be associated with asymmetric positioning of the nucleus and exclusion of large organelles from the generative cell domain (Tanaka, 1997
). It has been shown that even in vacuolate pollen (e.g., grasses) where a large vacuole is instrumental in moving the nucleus, microtubules are required for final positioning and anchoring of the nucleus at the periphery (Terasaka and Niitsu, 1990
). The necessity of asymmetric division in the genetic regulation of development is supported by discovery that the gene lat 52, which is necessary for pollen tube growth, is expressed only in the vegetative cell (Eady, Lindsey, and Twell, 1995
). Tobacco microspores treated with low concentrations of colchicine to induce an equal division show that lat 52 is expressed in both daughter cells, indicating a lack of cell differentiation.
In Carex, a reorganization of the cytoskeleton occurs during formation of the spindle of the first pollen mitosis. The spindle will be aligned along the proximal/distal axis of the tetrad which is coincidental with the intercellular adaxial/abaxial axis. Early in prophase, microtubules rearrange and accumulate around the nucleus. Cone-shaped tufts of microtubules appear in association with the nuclear envelope. These subsets of microtubules appear similar to microtubule-converging centers (MTCCs) described during transitions in Haemanthus endosperm (Smirnova and Bajer, 1994
). The MTCCs in the distal portion of the microspore remain in the same orientation as the RMS with converging tips (presumably the minus ends) at the nuclear envelope, while those in the proximal portion appear to reverse their orientation with diverging tips (presumably the plus ends) at the nuclear envelope. At the proximal pole, which represents the displaced center of the original microsporocyte, the numerous tufts of microtubules are oriented in the correct position to contribute to the spindle. Although the polarity of pollen mitosis in Phalaenopsis is reversed (the generative pole is distal rather than proximal), the generative half of the spindle is nevertheless formed in advance of the vegetative (Brown and Lemmon, 1992c
). This suggests that the generative pole is precocious or dominant, regardless of whether its position in the microspore is distal or proximal. As the spindle is assembled in the functional microspore of Carex, small spindles are formed in the abortive microspores. One pole of each spindle is adjacent to the proximal pole of the functional microspore. This indicates that spindle orientation in abortive microspores is still responding to basic distal-proximal polarity, even though the proximal pole is displaced from its original position in the center of the microsporocyte and the abortive microspores rarely complete mitosis.
The hierarchy of polar expression in developing pollen of Carex provides a model for analyzing the establishment and involvement of cytoplasmic asymmetry in polar development in multicellular higher plants. The behavior of the quartet of nuclei in response to polarity suggests similarities to development of the female gametophyte (reviewed by Russell, 1993
). The egg and polar nucleus differentiate from the synergids by a process that is well documented but mechanistically no better understood. This suggests that polar development of male and female gametophytes is under similar controls as has long been suspected from similarities in migration and cellularization of gametophytes (Swamy, 1946
) as well as examples such as feminization of pollen grains (Stow, 1933
). This correlation suggests that experimentation using pollen development in the Cyperaceae as a model system will do much to elucidate basic developmental mechanisms in flowering plants, particularly those involved in sporogenesis and gametogenesis.
FOOTNOTES
1 The authors thank NSF for support under grant MCB-9726968015 and Linda LeBlanc and Hong Nguyen for technical support and help with preparation of illustrations. 
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