| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
What's this? |
Development and Morphogenesis |
2UMR de Genetique Vegetale, Ferme du Moulon, 91190 Gif-sur-Yvette, France; 3Botany Department, University of Stellenbosch, Private Bag X1, Matieland 7602, South Africa; 4Laboratoire Ecologie Systématique et Evolution, CNRS UMR 8079, Université Paris-Sud, 91405 Orsay cedex, France
Received for publication June 3, 2004. Accepted for publication December 9, 2004.
ABSTRACT
Pollen aperture patterns vary widely in angiosperms. An increasing number of studies indicate that aperture pattern ontogeny is correlated with the way in which cytokinesis that follows male meiosis is completed. The formation of the intersporal callose walls that isolate the microspores after meiosis was studied in four species with different aperture patterns (two monocots, Phormium tenax and Asphodelus albus, and two eudicots, Helleborus foetidus and Protea lepidocarpodendron). The way in which post-meiotic cytokinesis is performed differs between all four species, and variation in callose deposition appears to be linked to aperture pattern definition.
Key Words: aperture pattern ontogeny • callose • cytokinesis • eudicot • meiosis, monocot • pollen
Angiosperm pollen grains are composed of two or three cells enclosed within a complex multilayered wall. Apertures are well-defined areas of the pollen surface where the external part of the wall, the exine, is reduced or absent. They accommodate variation in pollen volume, the passage of water during pollen rehydration, and the exit of the pollen tube during pollen germination. Aperture shape, structure, number and distribution constitute the aperture pattern of a pollen grain. Angiosperms are widely diverse in their aperture patterns (Walker and Doyle, 1975
). This diversity is structured in two morphological groups according to the main taxonomic divisions (Walker and Doyle, 1975
; Blackmore and Crane, 1998
). Eudicots, also known as the tricolpate clade, usually produce pollen with three equatorial apertures, but species producing pollen with two or four to six equatorial apertures are commonly observed. Basal angiosperms and monocots usually produce pollen with a single distal polar aperture (monosulcate pollen) or a set of morphologies with a few equatorial (or nearly equatorial) apertures.
In angiosperms, microsporogenesis is surprisingly variable (Sampson, 1975
; Longly and Waterkeyn, 1979a
, b
; Bandhari, 1984
; Brown, 1991
). Microsporogenesis of species differ in three ways: (1) in the timing of the nuclear divisions relatively to the cytoplasmic divisions (cytokinesis can be successive, simultaneous or intermediate), (2) in the orientation of the meiotic axes (tetragonal, rhomboidal, tetrahedral, decussate, and intermediate tetrad types result from such variation), (3) in the way callose is deposited to form the cleavage walls during cytokinesis. In 1935, Wodehouse proposed that cytokinesis following meiosis could be involved in aperture pattern ontogeny. Since then, an increasing number of studies have linked aperture pattern ontogeny to meiosis (Blackmore and Crane, 1998
; Ressayre et al., 2002
; Furness and Rudall, 2004
). Recently, a developmental model based on the cytological events that occur during meiosis was proposed. The model suggests that the combination of the different variable elements during meiosis is sufficient to account for the most widespread patterns, opening the opportunity to study both proximal and distal causes of such a diversification (Ressayre et al., 2002
).
However, several aspects of the model still need to be investigated and its generality remains to be demonstrated. The model is based on the hypothesis that for angiosperms species displaying six or less apertures, the progress in cytokinesis defines the places where apertures will meet within tetrads. More precisely, the model predicts that apertures will meet in the regions where cytokinesis is completed, a hypothesis initially proposed by Wodehouse (1935)
. In the model, this mechanism is supposed to apply both to polar and nonpolar patterns, polar apertures being additionally defined by the position of the spindle pole in the second meiosis (Ressayre et al., 2002
). While there is experimental evidence to show that the definition of polar apertures is determined by the distribution of the second meiotic poles (Dover, 1972
; Sheldon and Dickinson, 1983
, 1986
), there is no evidence supporting the idea that the relationships between apertures in polar species are determined by cytokinesis.
The developmental model permits us to test this hypothesis. If relationships between apertures are indeed determined by cytokinesis, convergence in cytokinesis can be expected between polar and nonpolar species displaying the same relationships between apertures within tetrads. Reciprocally, species displaying different distribution of apertures within tetrads should differ in terms of cytokinesis. To test these aspects of the model, we studied the pattern of callose deposition in four selected species (Asphodelus albus Miller; Phormium tenax J.R. Forst. and G. Forst.; Protea lepicarpodendron (L.) L.; Helleborus foetidus L.) that, on the one hand, display common developmental features, including simultaneous cytokinesis (Fig. 1A), multiplanar tetrads and a two-step production of the intersporal callose walls, but on the other hand, differ in aperture patterns (Fig. 1B). As a result, the only differences expected would pertain to the direction of callose deposits during the formation of the intersporal walls. Asphodelus albus produces monosulcate pollen (Huynh, 1976
), that is, pollen that displays a single distal furrow (Fig. 1B-a). Phormium tenax produces trichotomosulcate pollen, that is, pollen that displays a single furrow placed at the distal pole of the grain and is divided into three branches (Rudall et al., 1997
). Protea lepicarpodendron produces triporate pollen (Ertdman, 1952
) and H. foetidus L. produces tricolpate pollen (Echlin and Godwin, 1968
). The first two species are monocots and belong to the order Asparagales (families Asphodelaceae and Phormiaceae, respectively). The last two species are basal eudicots that belong to the Proteaceae and the Ranunculaceae respectively. The two eudicot species differ in the arrangement of apertures within their tetrads. The apertures of H. foetidus are joined in pairs within the tetrads, as is the common condition in eudicots (Fig. 1Bd), an arrangement known as the Fisher's arrangement of apertures (Fisher, 1890
). The apertures of P. lepicarpodendron are joined three by three in the tetrads (Fig. 1Bc). This is known as the Garside's arrangement of apertures (Garside, 1946
). The extremities of the trichotomosulcus of monocots are recorded in the literature to follow Garside's arrangement (Fig. 1Bb; Huynh, 1971
). Differences in cytokinesis are expected within both the monocot and eudicot clades as the species differ in aperture distribution within tetrads. In contrast, P. tenax (monocot) and P. lepicarpodendron (dicot) display the same relationships of apertures within the tetrads (Garside's arrangement). As a result, convergence in cytokinesis is expected in both species.
|
Plant material
Fresh flower buds of each species were collected. Material of A. albus was collected on the campus of the University of Paris-Sud, Orsay, France. Material of P. tenax was collected at the Museum National d'Histoire Naturelle, Paris, France. Material of H. foetidus was collected in the wild in mountains in the south of France (Col du Coq and Col de Porte, Chartreuse, France), while material of P. lepicarpodendron was collected in the Jan S. Marais Reserve (Stellenbosch, South Africa).
Staining
Fresh buds were collected and dissected immediately. The sporogenous cells were extracted from one anther and mounted in acetocarmine to determine the meiotic stage of the bud. When buds were found to be undergoing meiosis, the remaining anthers were squashed in aniline blue (modified from Arens, 1949
) to observe callose wall formation using epifluorescence and a Zeiss Axiophot microscope with filter set 01 (excitation 345, emission 425 nm long pass). When buds were at the tetrad stage, some anthers were mounted in aniline blue to observe callose, while the rest was mounted in congo red (Stainier et al., 1967
) to observe aperture pattern within the tetrads. Acetocarmine and congo red preparations were observed with a Zeiss Axiophot microscope (light microscopy). In A. albus, aperture pattern within tetrads was also observed using epifluorescence and a Zeiss Axiophot microscope with filter set 07 (excitation 495, emission 520 nm long pass).
RESULTS
In all species studied, cleavage wall formation appears to be a two-step process. First, the cytoplasm of the future microspores is separated by the formation of callosic cell plates. Second, additional callose deposition takes place on the cell plates. Cell plate formation was identical within the monocots and within the eudicots, but differed between the two groups (clades), while patterns of additional callose deposition differed among all four species.
Cell plate formation
In both monocot species, cytokinesis began with the formation of small discs of callose in the cytoplasm of the dividing cells (Fig. 2a, e). These discs rapidly joined in the center of the dividing cells, and six cleavage walls separating the four future microspores became visible (Fig. 2b–d and f–h). The progression of cell plates continued toward the surrounding wall of the dividing cell. Cell plate formation then appeared to progress centrifugally. In A. albus small ingrowths of callose were also seen during the extension of the cell plates (Fig. 2b, c). These ingrowths appear to predict the places were cell plates will meet with the outer wall surrounding the dividing microsporocyte.
|
Tetrads
In the four species, almost all tetrads are multiplanar. In these multiplanar tetrads, six cleavage walls intersect in the center of the dividing cells (Fig. 2d, h, l, p). In both eudicots and in P. tenax, all cleavage walls appeared to be identical and orientated at 120° angles relatively to each other (Fig. 2h, l, p). Two different shapes of cleavage walls were detected in A. albus. In at least some tetrads of this species, two of the cleavage walls are large and crossed the other walls at angles of close to 180°, while the four others are smaller and crossed the other walls at angles of close to 90° (Fig. 2d). A few uniplanar tetrads were also observed in all the species except in P. lepicarpodendron, where all the tetrads are tetrahedral.
Additional callose deposits and aperture pattern
Asphodelus albus
Additional callose deposits are observed near the callose wall surrounding the developing tetrad, at the intersection of the cleavage walls (Fig. 3a). In multiplanar tetrads, they are apparently more abundant on the two largest cell plates and very faint on the four others (Fig. 3b). Callose deposition progressed from the intersections of the cell plates toward the middle of the cleavage walls. As a result, in tetrahedral tetrads, additional callose deposits led to the formation of two patches of callose on the two largest cleavage walls (Fig. 3b). The sulcus formed orthogonally to these cleavage walls (Fig. 4a– f). In tetragonal tetrads, callose deposits were concentrated near the callose wall surrounding the tetrad at the intersection of the cleavage walls, leading to the formation of two patches on both sides of the tetrads (Fig. 3c, d). The sulcus also formed orthogonally relative to the cleavage walls (Fig. 4g, h).
|
|
DISCUSSION
Cytoplasmic division following meiosis appears to be as variable as aperture pattern itself in the four species studied. As expected if it is involved in aperture pattern ontogeny, cytokinesis takes place in a different way in each of the four species. In addition, aperture distribution within tetrads appears to correlate with the places where cytokinesis is completed, both in polar and nonpolar species. All the data provided by the comparison among the four species support the hypothesis that both in polar and nonpolar species, cytokinesis is involved in aperture pattern ontogeny. Our results thus strongly support the theoretical model of pollen aperture development proposed by Ressayre et al. (2002)
.
The present study also contributes new information on two aspects. First, we show that cell plate formation progresses differently in monocots and eudicots, although cytokinesis following male meiosis is a two-step process (cell plate formation followed by additional callose deposition) in both clades (Waterkeyn, 1962
; Longly and Waterkeyn, 1979a
). Each step is apparently independent of the other. Second, we found that within the species where cell plate formation and additional callose deposits do not progress in the same way, aperture sites coincide with the last points of callose deposition and not with the last points of contact between the cytoplasm of the dividing cells as stated by Wodehouse (1935)
.
Cell plate formation: one way for monocots, another for eudicots
In both eudicot species, cell plate formation begins at the edges of the cleavage planes and progresses toward the center of the dividing cell. Although centripetal progression of isolated cell plates has, to our knowledge, never before been recorded, such a progression appears consistent with other reports of cleavage wall formation in core eudicots (Longly and Waterkeyn, 1979a
, b
; Brown, 1991
; Ressayre et al., 2001
). In these species, cell plate formation is synchronized with additional callose deposits and both progress centripetally. Formation of isolated cell plates has been described in H. foetidus, although no indication of cell plate progression (centripetal or centrifugal) was provided (Waterkeyn, 1962
). Centrifugal cell plate formation has been described in two Proteaceae species (Blackmore and Barnes, 1995
). This discrepancy between Proteaceae species is difficult to explain and further studies are required to investigate whether these species indeed differ in cell plate formation. If this was confirmed to be the case, the distribution of both types of cell plate formation should be determined. Centripetal progression is markedly different from the known progression of the cell plate formation during plant mitosis in general (Heese et al., 1998
) and from the progression of cell plates during male meiosis in monocots in particular (Longly and Waterkeyn, 1979a
; Brown, 1991
). During plant mitosis, cytokinesis is initiated in late anaphase with the formation of a phragmoplast, a complex array of microtubules and actin microfilaments. The phragmoplast is composed of short, overlapping microtubules of opposite polarity formed at the center of the cell. From here, they progress centripetally towards the cell walls. Callose vesicles move along the microtubules of the phragmoplast and coalesce to form a cell plate that expands centifugally along with the phragmoplast. Cell plate formation during plant meiosis has never been described in such detail (Otegui and Staehelin, 2000
), but has been recorded to progress centrifugally in a similar fashion to what we observed in the two monocot species in the present study (Longly and Waterkeyn, 1979a
; Brown, 1991
; Brown and Lemmon, 1996
). Other studies have indicated that plant meiosis may or may not resemble mitosis in terms of the formation of a phragmoplast, depending on the specific plant species studied (Brown and Lemmon, 1996
). Because we did not label microtubules, we do not know whether a phragmoplast is produced in the two monocot species studied.
Additional callose deposits: a key role in aperture pattern determination?
The species studied differed markedly in terms of additional callose deposits on cell plates. The pattern of callose deposition is hard to follow: callose observed by epifluorescence is a translucent material, and callose deposits within tetrads are observed across the callose wall surrounding the tetrad. In addition, tetrahedral tetrads are complex tridimensional objects that hide part of the cleavage walls that isolate the microspores behind the other walls. Observation of the different areas of a single tetrad is rarely possible. In extreme cases, additional callose deposits are so abundant that they prevent any detailed observation of the underlying patterns. As a result, one can only form a general idea of the progression of callose depositition. Two main ways of callose deposition were observed (Fig. 5; note that the figure only indicates the progression of the callose deposits and does not present a realistic image of additional callose deposits). In A. albus and H. foetidus, additional callose deposition begins at the intersection of the cleavage walls and progresses centripetally inwards along the cell plates (only on two of the cleavage walls in A. albus). Alternatively, in P. tenax and P. lepicarpodendron, callose deposition begins on the cell plate and progresses centrifugally towards the intersection of the cleavage walls (this time our observation is consistent with the observations made in the two other Proteaceae species studied by Blackmore and Barnes [1995]
). We thus observed a convergence in patterns of callose deposition between monocots and eudicots, while cell plate formation remains different between these clades. Interestingly, cell plate formation and additional callose deposition appear to be completely independent. This was already known to be true for monocots and basal angiosperms, but has never been confirmed for eudicots (Longly and Waterkeyn, 1979a
, b
; Bandhari, 1984
; Blackmore and Crane, 1998
). This study thus confirms that cleavage wall formation is the result of two independent variable elements, namely cell plate formation and additional callose deposition.
|
The present study has implications for our understanding of the genetic control of aperture pattern. It appears to be a highly complex character despite its apparent simplicity. Both the model (Ressayre et al., 2002
) and the observations reported here converge to indicate that aperture pattern is determined by the places where cytokinesis following meiosis is completed. The places themselves are determined by a number of events (cytokinesis type, orientation of the second meiotic axes that affects tetrad shape and pattern of callose deposition following cell plate formation) that individually appear to be controlled by at least one gene. The cell progression cycle during male meiosis is probably controlled by several genes (Magnard et al., 2001
). Several non-allelic mutants presenting cytokinesis defects leading to microsporogenesis failure have been described in potatoes (Mok and Peloquin, 1975
) and in Arabidopsis mutants (Peirson et al., 1996
; Hülskamp et al., 1997
; Spielman et al., 1997
). A mutant disrupting the normal orientation of the second meiotic axes has also been described in potatoes (Mok and Peloquin, 1975
). In the same way, callose deposition and degradation is controlled by several different genes (Fei and Sawhney, 1999
). Our study indicates that the genetic system controlling cell plate formation and additional callose deposits is almost certainly different. In addition, the genetic control of additional callose deposits is plausibly quantitative because the amount of additional callose deposits as well as their progression vary strongly between species. For example in monocots, depending on the species, the additional callose deposits have been described to be either absent or inconsistent, present but not oriented, or present and progressing either centripetally or centrifugally (Sampson, 1969
; Longly and Waterkeyn, 1979b
; Ressayre, 2001
). Additional variation can be described; there are, for example, several different ontogenetic pathways for producing apertures in angiosperms (Rowley, 1975
). As a result, aperture pattern appears to be a highly complex character controlled by at least half a dozen genes, but probably by many more.
FOOTNOTES
1 A. R. received a financial support from the Société de Secours des Amis des Sciences and the Singer-Polignac Foundation. 
2 Author for correspondence (e-mail: ressayre{at}moulon.inra.fr
) phone: 01.69.33.23.359, fax: 01.69.33.23.40
LITERATURE CITED
Arens K. 1949 Prova de calose por meio da microscopia a luz fluorescente e aplicações do metodo. Lilloa 18: 71-75
Bandhari N. N. 1984 The microsporangium. In B. M. Johri [ed.], The embryology of angiosperms, 71–80. Springer Verlag, Berlin, Germany
Blackmore S. S. H. Barnes 1995 Garside's rule and the microspore tetrads of Grevillea rosmarinifolia A. Cunningham and Dryandra polycephala Bentham (Proteaceae). Review of Palaeobotany and Palynology 85: 111-121
Blackmore S. P. R. Crane 1998 The evolution of apertures in the spores and pollen grains of embryophytes. In S. J. Owens and P. J. Rudall [eds.], Reproductive biology, 159–182. Royal Botanic Garden, Kew, UK
Brown R. C. 1991 The cytokinetic apparatus in meiosis: control of division plane in the absence of a preprophase band of microtubules. In C. W. Lloyd [ed.], The cytoskeletal basis of plant growth and form, 269–273. Academic Press, London, UK
Brown R. C. B. E. Lemmon 1996 Nuclear cytoplasmic domains, microtubules and organelles in microsporocytes of the slipper orchid Cypripedium californicum A. Gray dividing by simultaneous cytokinesis. Sexual Plant Reproduction 9: 145-152
Diaz Lifante Z. 1996 Pollen morphology of Asphodelus L. (Asphodelacaea): taxonomic and phylogenetic inferences at the infrageneric level. Grana 35: 24-32[Web of Science]
Dover G. A. 1972 The organisation and polarity of pollen mother cells of Triticum aestivum. Journal of Cell Science 11: 699-711
Echlin P. H. Godwin 1968 The ultrastructure and ontogeny of pollen in Helleborus foetidus L. II. Pollen grain development through the callose special stage. Journal of Cell Science 3: 175-186
Ertdman G. 1952 Pollen morphology and plant taxonomy: angiosperms. Almqvist and Wiksell, Stockholm, Sweden
Fei H. V. K. Sawhney 1999 MS32-regulated timing of callose degradation during microsporogenesis in Arabidopsis is associated with the accumulation of stacked rough ER in tapetal cells. Sexual Plant Reproduction 12: 188-193[CrossRef][Web of Science]
Fisher H. 1890 Beitrage zur vergleichenden Morphology der Pollenkörner (Thesis), Breslau University, Breslau, Germany (now Wroclaw University, Wroclaw, Poland)
Furness C. A. P. J. Rudall 2004 Pollen aperture evolution—a crucial factor for eudicot success?. Trends in Plant Science 9: 154-158[CrossRef][Web of Science][Medline]
Garside S. 1946 The developmental morphology of the pollen of Proteaceae. South African Journal of Botany 12: 27-34
Heese M. U. Mayer G. Jurgens 1998 Cytokinesis in flowering plants: cellular process and developmental integration. Current Opinion in Plant Biology 1: 486-491[CrossRef][Web of Science][Medline]
Hülskamp M. N. S. Parekh P. Grini K. Schneitz I. Zimmermann R. E. Pruitt 1997 The STUD gene is required for male specific cytokinesis after telophase II of meiosis in Arabidopsis thaliana. Developmental Biology 187: 114-124[CrossRef][Web of Science][Medline]
Huynh K. L. 1971 Etude de l'arrangement du pollen dans la tétrade chez les Angiospermes sur la base de données cytologiques. III. Le pollen trilète du genre Dianella Lam. (Liliaceae). Beitrage zur Biologi der Planzen 47: 277-286
Huynh K. L. 1976 Arrangement of some monosulcate, disulcate, trisulcate, dicolpate and tricolpate pollen types in the tetrads, and some aspects of evolution in the angiosperms. In I. K. Ferguson and M. Muller [eds.], The evolutionary significance of the exine, 101–124. Academic Press, London, UK
Longly B. L. Waterkeyn 1979a Etude de la cytocinèse. II. Structure et isolement des plaques cellulaires microsporocytaires. La Cellule 72: 227-242
Longly B. L. Waterkeyn 1979b Etude de la cytocinèse. III. Les cloisonnements simultanés et successifs des microsporocytes. La Cellule 73: 65-80
Magnard J. L. M. Yang Y. C. Chen M. Leary S. McCormick 2001 The Arabidopsis gene Tardy asynchronous meiosis is required for the normal pace and synchrony of cell division during male meiosis. Plant Physiology 127: 1157-1166
Mok D. W. S. S. J. Peloquin 1975 Three mechanisms of 2n pollen formation in diploid potatoes. Canadian Journal of Genetic and Cytology 17: 217-225
Otegui M. L. A. Staehelin 2000 Cytokinesis in flowering plants: more than one way to divide a cell. Current Opinion in Plant Biology 3: 493-502[CrossRef][Web of Science][Medline]
Peirson B. N. H. A. Owen K. A. Feldmann C. A. Makaroff 1996 Characterization of three-male sterile mutants of Arabidopsis thaliana exhibiting alterations in meiosis. Sexual Plant Reproduction 9: 1-16
Ressayre A. 2001 Equatorial aperture pattern in monocots: same definition rules as in eudicots? The example of two species of pontederiaceae. International Journal of Plant Sciences 162: 1219-1224[CrossRef]
Ressayre A. B. Godelle C. Raquin P.-H. Gouyon 2002 Aperture pattern ontogeny in angiosperms. Journal of Experimental Zoology (Molecular and Developmental Evolution) 294: (Supplement) 122-135
Ressayre A. C. Raquin A. Mignot B. Godelle P.-H. Gouyon 2001 Correlated variation in microtubule distribution, callose deposition during male post-meiotic cytokinesis, and pollen aperture number across Nicotiana species (Solanaceae). American Journal of Botany 89: 393-400[CrossRef][Web of Science]
Rowley J. R. 1975 Germinal aperture formation in pollen. Taxon 24: 17-25[CrossRef]
Rudall P. J. C. A. Furness M. W. Chase M. F. Fay 1997 Microsporogenesis and pollen sulcus type in Asparagales (Lilianae). Canadian Journal of Botany 75: 408-430
Sampson F. B. 1969 Cytokinesis in pollen mother cells of angiosperms, with emphasis on Laurelia novae-zelandia (Monimiaceae). Cytologia 34: 627-634[Web of Science]
Sampson F. B. 1975 Aperture orientation in Laurelia pollen (Atherospermataceae Syn. subfamily Atherospermoideae of Monimiaceae). Grana 15: 153-157
Sheldon J. M. H. G. Dickinson 1983 Determination of patterning in the pollen wall of Lilium henryi. Journal of Cell Science 63: 191-208[Abstract]
Sheldon J. M. H. G. Dickinson 1986 Pollen wall formation in Lilium: the effect of chaotropic agents, and the organisation of the microtubular cytoskeleton during pattern development. Planta 168: 11-23[CrossRef][Web of Science]
Spielman M. D. Preuss F.-L. Li W. E. Browne R. J. Scott 1997 TETRASPORE is required for male meiotic cytokinesis in Arabidopsis thaliana. Development 124: 2645-2657[Abstract]
Stainier F. D. Huard F. Bronkers 1967 Technique de coloration spécifique de l'exine des microspores jeunes encore groupées en tétrade. Pollen et Spores 9: 367-370
Walker J. W. J. A. Doyle 1975 The bases of angiosperm phylogeny, palynology. Annals of the Missouri Botanical Garden 62: 664-723[CrossRef][Web of Science]
Waterkeyn L. 1962 Les parois microsporocytaires de nature callosique chez Helleborus et Tradescantia. La Cellule 62: 225-255
Wodehouse R. P. 1935 Pollen grains, their structure, identification and significance in science and medicine. McGraw-Hill, New York, New York, USA
CiteULike Complore Connotea Del.icio.us Digg Facebook Reddit Technorati Twitter What's this?
This article has been cited by other articles:
|
|
 |
|
  B. Albert, A. Matamoro-Vidal, C. Raquin, and S. Nadot Formation and function of a new pollen aperture pattern in angiosperms: The proximal sulcus of Tillandsia leiboldiana (Bromeliaceae) Am. J. Botany, February 1, 2010; 97(2): 365 - 368. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. L. P. Nunes, C. Bona, M. C. d. C. Moco, and A. I. Coan Release of developmental constraints on tetrad shape is confirmed in inaperturate pollen of Potamogeton Ann. Bot., October 1, 2009; 104(5): 1011 - 1015. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Nadot, C. A. Furness, J. Sannier, L. Penet, S. Triki-Teurtroy, B. Albert, and A. Ressayre Phylogenetic comparative analysis of microsporogenesis in angiosperms with a focus on monocots Am. J. Botany, November 1, 2008; 95(11): 1426 - 1436. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. BANKS, S. FEIST-BURKHART, and B. KLITGAARD The Unique Pollen Morphology of Duparquetia (Leguminosae: Caesalpinioideae): Developmental Evidence of Aperture Orientation Using Confocal Microscopy Ann. Bot., July 1, 2006; 98(1): 107 - 115. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
