| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Development and Morphogenesis |
2Laboratoire Ecologie, Evolution et Systématique, Unité Propre de Recherche de l'Enseignement Supérieur Associée au CNRS 8079, Bâtiment 362, Université Paris-XI, 91405 Orsay Cedex, France; 3Institut des Sciences de l'Evolution de Montpellier-CC61, Université Montpellier II, 34095 Montpellier Cedex 5, France
Received for publication May 22, 2001. Accepted for publication September 13, 2001.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
This apportionment is achieved by radial arrays of microtubules organized around the nuclei. The cleavage planes are defined in the overlapping regions of opposing arrays extending from different nuclei. We followed the establishment of these arrays in two different lines of plants belonging to the genus Nicotiana that produce pollen grains with different aperture numbers. Different distributions of the microtubules have been observed, which can be interpreted as resulting from variation in the interactions between nuclei; these distributions appear to be correlated with aperture number.
As a consequence, we propose that simultaneous cytokinesis allows the formation of multiple pollen morphologies. This mechanism is consistent with aperture number distribution within angiosperms and provides clues to help our understanding of the evolution of aperture number.
Key Words: aperture • callose • cytokinesis • meiosis • microtubules • Nicotiana • pollen • Solanaceae
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
). A major step in organ or organism development is the definition of symmetry planes and polarity (Jürgens, Grebe, and Steinmann, 1997
; Quatrano and Shaw, 1997
; Jan and Jan, 1998
; Twell, Park, and Lalanne, 1998
; Wolpert et al., 1998
; Bowerman and Shelton, 1999
). Polarity is often determined by an asymmetric mitotic cell division. Complex cell divisions, such as meiosis, even if completely symmetrical, could provide spatial cues for cell patterning. It has been known for decades that for low aperture number in plant pollen, the ontogeny of aperture sites is linked with the meiotic divisions that produce four microspores from a single microsporocyte (Wodehouse, 1935
).
Pollen apertures are well-defined areas of the pollen surface where the external part of the wall (ectexine) is reduced or absent. They function as openings, permitting pollen-tube germination, exchanges with the surrounding medium, and preventing pollen wall breakage. Wide variation in aperture number and position has been described among angiosperm species, especially among eudicots (Wodehouse, 1935
; Van Campo, 1976
). Most eudicot species produce pollen grains with three apertures, yet species producing pollen grains with 4–6 or up to 100 apertures are also known. Some variation occurs at the intraspecific level and even within a single plant (pollen heteromorphism; Wodehouse, 1935
; Van Campo, 1966, 1976
; Dajoz, Till-Bottraud, and Gouyon, 1991
). This provides a useful tool for understanding how aperture position is determined; to achieve this, the developmental process leading to the different patterns are compared.
In eudicots, several cellular mechanisms inducing the formation of aperture sites have been described. Apertures can be formed (1) by inhibition of primexine synthesis by close apposition of endoplasmic reticulum shields against the callosic wall (Heslop-Harrison, 1963
), (2) by formation of callose knobs at future aperture sites preventing primexine deposition (Waterkeyn and Bienfait, 1970
), or (3) by the formation of "interstitial bodies" that extend into the wall of callose at aperture sites and around which the primexine will be deposited (Rowley, 1975
). These different cellular mechanisms can lead to the formation of the same aperture patterns (i.e., the same aperture number and location). Conversely, different aperture patterns can be achieved by the same cellular mechanisms, as exemplified by heteromorphism. This study is only concerned with the ontogeny of pattern formation and not with aperture site definition; these appear to be two different phenomena.
The location of apertures during development suggests the existence of a close relationship between aperture pattern definition and the cytoplasmic partition that completes meiosis (for a review see Blackmore and Crane, 1998
). In most eudicots, cytokinesis during meiosis is delayed until the two nuclear divisions are completed (simultaneous cytokinesis). There are a few exceptions. In several species of Proteaceae and Podostemaceae, successive cytokinesis has been recorded (cytokinesis is successive when each nuclear division is followed by a cytoplasmic one) (Razi, 1949
; Blackmore and Barnes, 1995
). When cytokinesis is simultaneous, the axes of the second nuclear division are usually orthogonal, leading to a tetrahedral configuration of the four haploid nuclei within the cytoplasm of the microsporocytes. The cytoplasmic domains centered on the nuclei are defined by radial arrays of microtubules (MTs) that extend from the nuclear envelope after depolymerization of the meiotic spindles (Brown and Lemmon, 1992
). Six cleavage planes are defined in the regions where radial arrays extending from each of the four nuclei intersect (Fig. 1A–C). As shown in Fig. 1A, the four nuclei are arranged at the summits of a tetrahedron. Separation of the four microspores thus occurs along six planes, each crossing one of the six edges of the tetrahedron. Each microspore is in contact with the three others along three planes, one with its partner in the second meiotic division, and the two others with the partners of the other second meiotic division. Cytokinesis is completed by deposition of callose in the cleavage planes (Longly and Waterkeyn, 1979a, b
). Apertures are readily visible, while microspores still remain within tetrads. In "core" eudicot species producing tri-aperturate pollen grains, apertures are joined by pairs and defined at the last points of contact persisting between adjacent microspores at the end of cytokinesis (Wodehouse, 1935
). The existence of a fundamentally different aperture pattern reported in tri-aperturate Proteaceae (apertures are joined three by three in four groups; Garside, 1946
) further confirms the involvement of cytokinesis in aperture pattern ontogeny (Blackmore and Crane, 1998
). As in "core" eudicots, cytokinesis is simultaneous, tetrads are tetrahedral, and apertures are formed at the last points of cytoplasmic contact. The difference lies in the way callose is deposited within the cleavage planes, which leads to a different distribution of the places where cytokinesis is completed (Blackmore and Barnes, 1995
). This paper focuses on "core" eudicots and examines how cytokinesis is involved in aperture pattern definition by comparing species producing producing tri- and species producing tetra-aperturate pollen. In "core" eudicot plants producing tetra-aperturate microspores, the fourth aperture of each microspore results from the duplication of the pair of apertures placed between microspores descending from the same second meiotic division (Huynh, 1968
).
|
have developed a model that uses information in the microsporocytes to predict the apportionment of the cytoplasm to each microspore and the number of apertures in the pollen. According to this model, interactions between the four nuclei present in the cytoplasm of the dividing microsporocytes can account for the partition into four equal-sized domains (Fig. 1A–C) and for aperture pattern determination (Fig. 1D–E). Bipolar interactions between nuclei result in the formation of tri-aperturate microspores, whereas tripolar interactions between nuclei lead to the formation of tetra-aperturate microspores. This model also predicts other aspects in the formation of tri-aperturate or tetra-aperturate microspores: (1) the cleavage planes should be identical in the two cases and (2) the duplication that leads to tetra-aperturate microspores should be accompanied by a modification of the cytokinetic apparatus, due to interactions with other nuclei.
To investigate whether interactions between nuclei, mediated through MTs, could be responsible for aperture patterns ontogeny, we examined the radial arrays of MTs in two species of the genus Nicotiana by immunofluorescence labelling. Pollen grains produced by N. sylvestris have three apertures, and the ones produced by N. tabacum have four apertures. We also followed callose deposition and cell plate formation to investigate whether cytokinesis and aperture ontogeny are related, as Wodehouse (1935)
proposed long ago. The result of this analysis is that both microtubule (MT) distribution during cytokinesis and callose deposition in the cleavage planes are different in the two kinds of plants. This provides a cytological support for our theoretical model of aperture definition.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Floral bud stage determination
To determine floral bud stage, one of the five anthers in each bud was immediately extracted and squashed in Belling's aceto-carmine (nucleus staining). Depending on the approximate stage of the buds, the remaining anthers were prepared for one of the following observations.
Slide preparation for microscopy
We used several techniques that target different components, wall or internal structures. Staining of apertures within tetrads is possible only at the end of the tetrad stage. The anthers were put on a slide in a drop of Congo red mixed with technical maleic hydrazyde, following Stainier, Huard, and Bronkers (1967)
. Apertures appeared as dark areas within a lightly red-colored wall. Staining of callose during cytokinesis was performed at all stages from the beginning of cytokinesis until the tetrad stage. Cells were mounted in aniline blue 0.1% (mass volume ratio, m/v) prepared in 0.1 mol/L K3PO4 (Kho and Baer, 1968
).
Labelling of MTs and nuclei was performed at all stages, from the beginning of meiosis until the end of cytokinesis. The protocol for cell preparations was adapted from Traas, Burgain, and Dumas De Vaulx (1989)
. Fixation, enzymatic digestion, and membrane permeabilization were all performed by adding products to buffer A (50 mmol/L Pipes, 5 mmol/L EGTA [ethylene glycol bis {2-aminoethyl ether}-N,N,N'N'-tetraacetic acid], 5 mmol/L MgSO4, pH = 6.9; Traas, Burgain, and Dumas De Vaulx, 1989
). Fixation was achieved by squashing the anthers in freshly prepared fixative (8% of formaldehyde in buffer A). After 30 min at room temperature, cells were rinsed three times in buffer A. To digest the anther tissues and the microsporocyte wall of callose, anthers were squashed in buffer A supplemented with 5% (volume/volume ratio, v/v) DMSO (dimethyl sulfoxide), 0.03% (v/v) Igepal CA-630 Sigma (instead of Nonidet P40 in Traas, Burgain, and Dumas De Vaulx, 1989
) and 0.5% (m/v) of each of three following enzymes: macerozyne Onozuka-R10 (Yakult, Honsha, Tokyo, Japan), cellulase (Onozuka-R10 Sigma), and beta-glucuronidase (HA-4 Sigma). The cells were incubated for 40 min at 30°C. Additional permeabilization of the plasma membrane was performed for 30 min using 0.1% (v/v) of Triton X-100 in buffer A at room temperature. Cells were washed twice again in buffer A and finally stored in water. Cells were then allowed to attach to poly-L-lysine coated slides. Immunofluorescence labeling was performed by adding the different antibodies in buffer B (162 mmol/L NaCl, 8 mmol/L Na2HPO4, 2 mmol/L K2HPO4, 10 mmol/L EGTA, 2 mmol/L MgCl2, 0.3% [m/v] BSA, pH = 7.4) adapted from Rusig, Le Guyader, and Ducreux (1994)
. Cells were treated with monoclonal anti-alpha and anti-beta tubulin (N 356 and N 357 Amersham, Little Chalfont, UK) 0.2% (v/v) of each in buffer B overnight at room temperature. After rinsing the slides three times with buffer B, a 1% (v/v) FITC (fluorescein isothiocyanate) conjugate antimouse IgG antibody (N 1031 Amersham) diluted in buffer B was added for at least 6 h at room temperature. To stain nuclei, 7.5 mmol/L propidium iodide in 10 mmol/L MgCl2 was applied for 15 min. After slides were rinsed three times in buffer B, they were mounted in citifluor.
Microscopy
Congo red preparations were observed with a Zeiss Axiophot microscope with transmitted light. The epifluorescence Zeiss Axiophot microscope was used with filter set 01 (excitation 345, emission 425 nm long pass) for aniline blue staining. Confocal laser scanning microscopy and double immunofluorescence analysis were performed using a TCS4D confocal microscope based on a Leica DM microscope interfaced with a mixed gas Argon/Krypton laser (Leica Laser Technik, Heidelberg, Germany). Simultaneous double fluorescence acquisitions were performed using the 488-nm and 568-nm laser lines to excite both FITC and propidium iodide using an oil immersion Plan APO objective (NA = 1.3).
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
|
|
|
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
). Our study provides a possible mechanism underlying this link: aperture number could be influenced by MT distribution and intersporal wall formation.
In the studied plants, meiosis proceeds as it is usually described in eudicots (Brown and Lemmon, 1988
; Traas, Burgain, and Dumas De Vaulx, 1989
; Peirson, Bowling, and Makaroff, 1997
). The two nuclear divisions proceed without cytoplasmic partition, resulting in a transitory syncytium of four haploid nuclei forming a tetrahedron. During the reformation of the nuclei, "secondary spindles" of MTs appear. They define the cytoplasmic domains around the nuclei (Brown and Lemmon, 1991
). The formation of these arrays apparently begins as a random process, MTs being nucleated first around nuclei without preferential direction.
The shape of the "secondary spindles" differs according to the number of apertures the pollen grains will have. The differences appear long before callose deposition begins. They are maintained when callose deposition proceeds and are associated with differences in the way the microspores are separated. Narrow connections between the cytoplasm of adjacent cells are observed where narrow "secondary spindles" were recorded, and apparently broader ones were observed (although with some difficulty) where broad "secondary spindles" were present. In N. sylvestris, the tri-aperturate plant, six pairs of apertures (one per cleavage plane) were observed, corresponding to six narrow cytoplasmic junctions between cells, in the regions where the arrays of MTs are maintained. In N. tabacum cv Xanthi, two pairs of apertures were formed in two of the six cleavage planes, whereas in the four others, one pair of apertures was formed. This is consistent with our observation of two (out of six) broader "secondary" spindles per tetrad.
Other results also suggest that aperture formation is linked to cleavage. In abnormal tetrads having more than four microspores, the presence of a supernumerary pseudo-microspore generally induces the formation of additional apertures on the adjacent microspores (Ressayre et al., unpublished data). Variation in aperture number can be observed in mutants producing polyads (He et al., 1996
; Peirson et al., 1996
). Mutants that fail to achieve cytokinesis display highly disturbed aperture patterns (Hülskamp et al., 1997
; Spielman et al., 1997
). Because labelling of MTs and staining of callose were lethal to the cells, it was not possible to follow the ontogeny from the end of the nuclear divisions to aperture formation: the causal link between MT distribution and aperture pattern is thus difficult to establish. However, in the two species studied here, the differences in aperture number are correlated with differences in MT distribution and in cleavage planes formation. Because the differences in MT distribution precede the beginning of callose deposition, it is thus plausible that MT distribution determines the way callose is deposited and the number of pairs of apertures that will be formed within a cleavage plane.
Although the arrays of MTs during cytokinesis have been described in N. tabacum (Tiezzi et al., 1992
) and in other species of eudicots (Brown and Lemmon, 1988
; Traas, Burgain, and Dumas De Vaulx, 1989
; Peirson, Bowling, and Makaroff, 1997
), variation in their shape was never reported. However, detecting variation of MT shape requires special attention, and none of the different studies performed so far have either detailed the establishment of the "secondary spindles" or compared two kinds of plants differing by their aperture number. In monocots, by using colchicine to disturb MT formation, it has been shown that aperture positioning and number are linked to the distribution of the MT organizing centers that are formed after the nuclear division (Dover, 1972
; Sheldon and Dickinson, 1986
). In the case of the genus Nicotiana, the mechanism suspected is fundamentally different. The MTs appear to be involved through their participation in cytoplasmic division and not through the distribution of the MT organizing centers. In animals, MTs are involved in the movement and organization of endoplasmic reticulum (ER) and other organelles (Cole and Lippincott-Schwartz, 1995
). In plants, MTs are suspected to be also involved in the movements of organelles. During somatic mitosis MTs are described to be involved in the transport of vesicles of callose during the formation of cell plates (Staehedlin and Hepler, 1996
). Thus a given distribution of microtubules could result in either presence of ER or formation of callose knobs at the future aperture. The MTs would then organize the spatial distribution of future aperture sites in collaboration with nuclei, the ontogeny of the aperture itself due to various processes (described in the introduction).
The differences in MT distribution observed between plants producing tri-aperturate and plants producing tetra-aperturate pollen are consistent with the predictions of our model. According to this model, aperture number could be determined by the kinds of interactions between nuclei that occur during the cytoplasmic partitioning. The future cleavage planes appear to be defined by the interactions of radial arrays of MTs based on the nuclei (Brown and Lemmon, 1991
). These interactions drive the formation of the cleavage planes in the intersection regions of the radial arrays of MTs (Brown and Lemmon, 1992
). Our data suggest that the types of interactions between nuclei can vary. The mechanisms that induce variation in the interactions of the nuclei remain unknown. However, variation in nuclei shape during the dynamic process leading to the establishment of the "secondary spindles" could be responsible for the variation in the interactions between nuclei. The MTs are nucleated during the reformation of the nuclei. If the nucleation begins just at the end of anaphase II, the haploid sets of chromosomes would not have recovered the spherical shape that is observed during telophase II. Sister nuclei would then have an elongated shape parallel to each other. On the contrary, non-sister nuclei would be situated in perpendicular planes. If the distribution of MTs is affected by the amount of nuclei surface, variation of the distribution of the MTs between sister and non-sister nuclei can be expected. This hypothesis remains to be confirmed by observations, but if it holds, heterochrony could be responsible for the variation of aperture patterns observed between our two species; these patterns may also exist within N. tabacum, in which several lines displaying different proportions of pollen with three or four apertures have been recorded (Till-Bottraud et al., 1995
).
The proposed mechanism of aperture number definition provides an explanation for the high frequency and widespread occurrence among eudicots of pollen heteromorphism (Wodehouse, 1935
; Ertdman, 1952
; Van Campo, 1976
; Pozhidaiev, 1993
; Mignot et al., 1994
). In the anthers of heteromorphic plants producing tri- and tetra-aperturate pollen grains, mixtures of microspores having different aperture numbers are found within the same tetrad (Huynh, 1968
; Mignot, Dajoz, and Till-Bottraud, 1995
). Heteromorphism could be due to variation in nuclei interaction between nuclei belonging to the same microsporocyte or between microsporocytes. Heteromorphism thus appears as a side effect of simultaneous meiosis, which allows a variation in the nature of interaction between nuclei (this is impossible with successive meiosis). In view of this, whenever aperture site definition is caused by a mechanism such as that described for Nicotiana, there is no constraint preventing the plants from producing several pollen morphs differing in their aperture number. Conversely, changes in aperture number (typically from three to four apertures) should be easy to achieve. The distribution of the variation in aperture patterns in eudicots is consistent with these hypotheses. A survey based on Ertdman (1952)
indicates that at least one heteromorphic species is present in more than half of the families of eudicots across all the eudicots orders (except Garryales and Aquifoliales, but the data concerning these two orders are too scarce) and that the same range of morphologies are observed throughout eudicots.
|
FOOTNOTES |
|---|
4 Author for reprint requests (tel.: (33) 1 69 15 65 29; Fax: (33) 1 69 15 73 53; Adrienne.Ressayre{at}esv.u-psud.fr
)
5 Present address: Laboratoire Génome, Populations, Interactions, CC63, Université Montpellier II, 34095 Montpellier Cedex 5, France
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
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
Bowerman B. C. A. Shelton 1999 Cell polarity in the early Caenorhabditis elegans embryo. Current Opinion in Genetics and Development 9: 390-395[CrossRef][ISI][Medline]
Brown R. C. B. E. Lemmon 1988 Microtubules associated with simultaneous cytokinesis of coenocytic microsporocytes. American Journal of Botany 75: 1848-1856[CrossRef][ISI]
Brown R. C. B. E. Lemmon 1991 The cytokinetic apparatus in meiosis: control of division plane in the absence of a pre-prophase band of microtubules. In C. Lloyd [ed.], The cytoskeletal basis of plant growth and form, 259–273. Academic Press, London, UK
Brown R. C. B. E. Lemmon 1992 Control of division plane in normal and griseofulvin treated microsporocytes of Magnolia. Journal of Cell Science 103: 1031-1038
Cole B. N. J. Lippincott-Schwartz 1995 Organization of organelles and membrane traffic by microtubules. Current Opinion in Cell Biology 7: 55-64[CrossRef][ISI][Medline]
Dajoz I. I. Till-Bottraud P. H. Gouyon 1991 Evolution of pollen morphology. Science 253: 66-68
Dover G. A. 1972 The organisation and polarity of pollen mother cells of Triticum aestivum. Journal of Cell Science 11: 699-711
Ertdman G. 1952 Pollen morphology and plant taxonomy: angiosperms. Almqvist and Wiksell, Stockholm, Sweden
Garside S. 1946 The developmental morphology of the pollen of Proteaceae. South African Journal of Botany 12: 27-34
He C. U. Tirlapur M. Cresti M. Peja D. E. Crone J. P. Mascarenhas 1996 An Arabidopsis mutant showing aberration in male meiosis. Sexual Plant Reproduction 9: 54-57
Heslop-Harrison J. 1963 An ultrastructural study of pollen wall ontogeny in Silene pendula. Grana Palynologica 4: 7-24
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][ISI][Medline]
Huynh K. L. 1968 Etude de l'arrangement du pollen dans la tétrade chez les angiospermes sur la base de données cytologiques. Bulletin de la Société Botanique Suisse 78: 151-191
Jan Y. N. L. Y. Jan 1998 Asymmetric cell divisions. Nature 392: 775-778[CrossRef][Medline]
Jürgens G. M. Grebe T. Steinmann 1997 Establishment of cell polarity during early plant development. Current Opinion in Cell Biology 9: 849-852[CrossRef][ISI][Medline]
Kho Y. O. J. Baer 1968 Observing pollen tubes by means of fluorescence. Euphytica 17: 298-302[ISI]
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
Mignot A. I. Dajoz I. Till-Bottraud 1995 Heteromorphism of pollen aperture number and heterogeneity in post-meiotic tetrads in two Viola species and Nicotiana tabacum. Compte-Rendus de l'Académie des Sciences 318: 453-457
Mignot A. C. Hoss I. Dajoz C. Leuret J. P. Henry J. M. Dreuillaux E. Heberlebors I. Till-Bottraud 1994 Pollen aperture polymorphism in angiosperms: importance, possible causes and consequences. Acta Botanica Gallica 141: 109-122[ISI]
Peirson B. N. S. E. Bowling C. A. Makaroff 1997 A defect in synapsis causes male sterility in a T-DNA-tagged Arabidopsis thaliana mutant. Plant Journal 11: 659-669[CrossRef][ISI][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
Pozhidaiev A. E. 1993 Polymorphism of pollen in the genus Acer (Aceraceae). Grana 32: 79-85
Quatrano R. S. S. L. Shaw 1997 Role of the cell wall in the determination of cell polarity and the plane of cell division in Fucus embryos. Trends in Plant Science 2: 15-21[CrossRef][ISI]
Razi B. A. 1949 Embryological studies of two members of the Podostemaceae. Botanical Gazette 111: 211-218[CrossRef]
Ressayre A. B. Godelle A. Mignot P. H. Gouyon 1998 A morphogenetic model accounting for pollen aperture pattern distribution in flowering plants. Journal of Theoretical Biology 193: 321-334[CrossRef][ISI][Medline]
Rowley J. R. 1975 Germinal aperture formation in pollen. Taxon 24: 17-25[CrossRef]
Rusig A. M. H. Le Guyader G. Ducreux 1994 Dedifferentiation and microtubule reorganization in the apical cell protoplast of Sphacelaria (Phacophyceae). Protoplasma 179: 83-94[CrossRef][ISI]
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][ISI]
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]
Staehelin L. A. P. K. Hepler 1996 Cytokinesis in higher plants. Cell 84: 821-824[CrossRef][ISI][Medline]
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
Tiezzi A. J. Bednara C. Del Casino A. Bartalesi G. Cai A. Moscatelli 1992 The microtubular cytoskeleton during pollen development and pollen tube growth in Nicotiana tabacum. In E. Ottaviano, D. L. Mulcahy, M. Sari Gorla, and G. Bergamini Mulcahy [eds.], Angiosperm pollen and ovules, 224–232. Springer-Verlag, New York, New York, USA
Till-Bottraud I. A. Mignot R. De Paepe I. Dajoz 1995 Pollen heteromorphism in Nicotiana tabacum (Solanaceae). American Journal of Botany 82: 1040-1048[CrossRef][ISI]
Traas J. A. S. Burgain R. Dumas De Vaulx 1989 The organisation of the cytoskeleton during meiosis in eggplant (Solanum melongena (L.)): microtubules and F-actin are both necessary for coordinated meiotic division. Journal of Cell Science 92: 541-550
Twell D. S. K. Park E. Lalanne 1998 Asymmetric division and cell-fate determination in developing pollen. Trends in Plant Science 3: 305-310
Van Campo M. 1966 Variations polliniques intraflorales. Adansonia 6: 55-64
Van Campo M. 1976 Patterns of pollen morphological variation within taxa. In I. K. Ferguson and M. Muller [eds.], The evolutionary significance of the exine, 125–137. Academic Press, London, UK
Waterkeyn L. A. Bienfait 1970 On a possible function of the callosic special wall in Ipomea purpurea (L.) Roth. Grana 10: 13-20
Wodehouse R. P. 1935 Pollen grains: their structure, identification and significance in science and medicine. McGraw-Hill, New York, New York, USA
Wolpert L. R. Beddington J. Brockes T. Jessel P. Lawrence E. Meyerowitz 1998 Principles of development. Current Biology and Oxford University Press, London, UK
This article has been cited by other articles:
|
|
 |
|
  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]
|
|
|
|
|
|
L. PENET, S. NADOT, A. RESSAYRE, A. FORCHIONI, L. DREYER, and P. H. GOUYON Multiple Developmental Pathways Leading to a Single Morph: Monosulcate Pollen (Examples From the Asparagales) Ann. Bot., January 2, 2005; 95(2): 331 - 343. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. Parre and A. Geitmann More Than a Leak Sealant. The Mechanical Properties of Callose in Pollen Tubes Plant Physiology, January 1, 2005; 137(1): 274 - 286. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
