FINE STRUCTURE OF THE ENDOTHECIUM AND DEVELOPING XYLEM IN PHASEOLUS VULGARIS
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1 New Phytol. (1982) 91, FINE STRUCTURE OF THE ENDOTHECIUM AND DEVELOPING XYLEM IN PHASEOLUS VULGARIS BY JEAN M. WHATLEY Botany School, South Farks Road, Oxford, OXl 3RA, U.K. {Accepted 1 January 1982) SUMMARY Differentially thickened wall bars are formed in cells of the anther endothecium as well as in the xylem. In Phaseolus vulgaris both types of wall bar appear to he lignified. As thickening takes place, Golgi hodies become numerous, endoplasmic reticulum proliferates and both types of organelle occupy characteristic sites within the cell. Thickening begins at an early stage of xylem development but in the endothecium it is long delayed. Subsequent loss of cytoplasm is associated with increasing vacuolation of xylem elenients, but may be associated with plasmolysis in the endothecium. INTRODUCTION In young anthers of Fhaseolus vulgaris the sporogenous tissue is surrounded by four distinctive cell layers, the epidermis, endothecium, middle layer and tapetum. All cells within each layer have a similar structural organization characteristic of that layer but different from that in cells of the other layers. This sharp distinction is only lost adjacent to the stomium. The anther epidermis arises from epidermal initials which only divide anticlinically. The other layers (including the pollen mother cells) arise from hypodermal initials and undergo both periclinal and anticlinal divisions (Foster and Gifford, 1974). During development of the anther the cells of the middle layer and tapetum break down leaving only the epidermis and endothecium intact. As the pollen matures, and only then, the walls of the endothecium develop characteristically thickened bars in all cells, except those in Ae immediate neighbourhood of the future stomium or dehiscence furrow. These differentially thickened bars, superficially at least, resemble those which develop in xylem elements. However, the two types of thickening can differ chemically. In a histochemical study of Chenopodium rubrum, de Fossard (1969) found that the endothecial thickenings, unlike the walls of other types of cell in the anther, contained a high proportion of a-cellulose. A negative result was obtained for all 'ignin tests on the Chenopodium endothecium, but the wall thickenings of other species, viz. Borago officinalis may, like those in xylem, be lignified (de Sablon, ^^85, cited in Eames, 1961). In Fhaseolus vulgaris the wall thickenings of both the ^ ^dothecium in mature anthers and the xylem in young leaves give a similar red staining reaction with phloroglucinol HCl suggesting that in this species also the ^i^dothecial bars are lignified. Like the fern annulus, the specialized wall thickenings of the endothecium are elieved to be associated with dehiscence, but the precise means by which this is Accomplished is unclear. Indeed many aspects of endothecium development ^^i unresolved; few papers on the subject have been published and, as far as aware, none have described the fine structure of this interesting cell layer. '^28-646X/82/O7O $03.00/ The New Phytologist
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3 Fine structure of Phaseolus 563 MATERIAL AND METHODS Immature flower buds were collected from plants of Phaseolus vulgaris cv. Canadian Wonder and arranged in size classes of 1-5 to 2*0 mm; 2-0 to 25 mm; 25 to 3-0 mm; 3-0 to 3-5 mm; 35 to 4-0 mm. The stamens were removed, fixed for 2 h in 3% glutaraldehyde in 0-1 M sodium cacodylate buffer, ph 7 2, rinsed in buffer, post-fixed and stained for 1-5 h in osmium tetroxide. Following dehydration in a graded ethanol series the stamens were transferred to acetone before embedding in Epon 812. Thin sections were post-stained in lead citrate. Segments of vascular tissue from developing primary leaves of P. vulgaris seedlings were similarly prepared for examination in the electron microscope. RESULTS Successive stages of anther development can be found in flower buds of increasing size classes. It is already known that thickening of endothecial walls takes place at a comparatively late stage of pollen development (de Fossard, 1969). In Phaseolus, thickening of the wall of the endothecium has only been found in buds larger than 2-5 mm in anthers in which tapetal cell breakdown has begun and the pollen is binucleate (Table 1). The life-span of fully differentiated, but still intact Table 1. Anther development in flowers of different sizes Flower bud length (mm) O O Wall layers established Tapetal cells disorganized Uninucleate pollen Binucleate pollen Endothecial walls thickened Endothecial cytoplasm disorganized n.a. = not applicable. n.a. n.a. endothecium appears to be of short duration. In anthers from most larger flower buds the endothecial cytoplasm appeared highly disorganized, in contrast with that of the epidermis. The broadened cells of the endothecium appeared plasmolysed 3nd the orientation of the bars of thickening was irregular. Cytoplasmic disintegration may well have taken place, but it should not be overlooked that this appearance might have been induced as an artefact during fixation of the ageing cells [see Fig. 2(b)]. In only one anther was the layer of thickened endothecium found to have intact cytoplasm. In endothecial cells of this anther, the endoplasmic '^eticulum (ER) and the Golgi bodies in particular appeared to occupy characteristic sites in relation to the regions of wall thickening and this arrangement of organelles showed some similarity to that found in the developing xylem of primary leaves. ^ig- l.(a) Montage of transmission electron micrographs showing the epidermal, endothecial, "middle and tapetal layers of an anther. The walls of the endothecium have thickened bars. Arrows indicate plasmodesmata. Bud: IS to 3-0 mm. x (b) Scanning electron micrograph of part 01 an anther showing the epidermis, endothecium and pollen grains, x (c) Scanning electron ^icrograph of the endothecium showing the U-shaped bars of wall thickening, x E, 'Epidermis; En, endothecium, M, mitochondrion; ML, middle layer, T, tapetum; Th, thickening.
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5 Fine structure of Phaseolus 565 In Phaseolus endothecial wall thickenings take the form of parallel U-shaped bands [Fig. 1 (a), (b), (c)], with the open part of the U towards the epidermis and with the upper limbs of the U continuous with the adjacent epidermal wall. Occasional plasmodesmata were seen to cross the unthickened areas of wall between the epidermis and the endothecium [Fig. 1 (a)]. Plasmodesmata were much more common between unthickened regions of adjacent endothecial cells [Fig. 2(e)]. Though at earlier stages of anther development many plasmodesmata appeared to link the endothecium and the middle layer, few, if any, could be positively identified after the middle layer cells had become disorganised. As the wall layers of the anther became established, the small proplastids or eoplasts accumulated starch and there was some limited extension of the thylakoid system. Initially there was no obvious difference in the structure of plastids in the different cell layers. By the time the endothecium was fully differentiated, plastids could no longer be distinguished in the disorganized tapetum or middle layer; those in the epidermal and endothecial layers had lost much of their starch. Plastids in the endothecium [Fig. 2(d)] had a few grana and sometimes a non-paracrystalline prolamellar body: those in the epidermis [Fig. 2(c)] had an even more restricted thylakoid system, but, in addition, they often contained irregular tubular arrays characteristic of plastids in mature white fiower petals of Phaseolus (Whatley, 1978). As far as it was possible to tell without extensive serial sectioning, some organelles (ER, Golgi bodies and possibly mitochondria) occupied sites in endothecial cells with thickening or thickened walls which differed markedly from those they occupied prior to thickening. In anthers from the 2*5 to 3-0 mm size class which had binucleate pollen but in which the endothecial walls had not yet begun to thicken the organelles appeared to be randomly distributed [Fig. 2(a)]: both the Golgi bodies and the short cisternae of rough ER were few in number. In the anther with thickened walls and intact cytoplasm, Golgi bodies were numerous; the locally swollen, rough ER was plentiful. Discontinuous cisternae closely paralleled the walls of the endothecium. The cisternae tended to be long where they followed the bars of thickening and shorter adjacent to unthickened parts of the wall. Other discontinuous cisternae sometimes paralleled the nuclear envelope. In thin section the distribution of ER gave the impression of subdividing the cytoplasm into large compartments corresponding to the subdivisions created by the thickened bars [Fig. 3(a), (b), (c)]. Lines of Golgi bodies often occurred parallel the ER, but the orientation of their forming face with respect to ER seemed to be variable. The Golgi bodies lay towards the inside of the pseudo-compartments of cytoplasm rather than outside between the ER and the plasmamembrane on the one hand and the ER and the nuclear envelope on the other. Groups of Golgi bodies Fig. 2.(a) The epidermis and endothecium at a stage of anther development prior to the beginning of wall thickening. Bud: 2-0 to 2 5 mm. x (b) The epidermis and endothecium at a late stage of anther development. Endothecial cells are plasmolysed; epidermal cells are not. Bud: 3 0 to 3 5 mm. x2375. (c) Plastid from an epidermal cell in a mature anther. Irregular tubular arrays of membrane (arrows) are present in this section but no thylakoids. Bud: 2 5 to 3 0 mm. x (d) Plastid from an endothecial cell in a mature anther. The thylakoid system is limited in extent hut does include grana. A small starch grain is also present. Bud: 2 5 to 3-0 mm. x (e) Plasmodesmata (arrows) in an unthickened portion of wall between adjacent endothecial cells. ER is prolific and there are several Golgi bodies (asterisk). Bud: 2 5 to 3 0 mm. x (f) Part of a group of Golgi bodies lying close to the junction between a bar of thickening and an unthickened portion of wall. Two pairs of microtubules (arrows) lie adjacent to the thickened bar. Bud: 2-5 to 3-0 mm. x For abbreviations see legend to Figure 1. ANP 91
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7 Fine structure of Phaseolus 567 also appeared to be concentrated close to the right-angled junction between bars of thickening and the adjoining unthickened walls [Fig. 2(f)]. The swollen ends of Golgi cisternae and the associated vesicles commonly had a large inner component which was electron transparent [Fig. 2(f), 3(c)J. Golgi vesicles could be found in close association both with the vacuolar membrane and (where the ER was discontinuous) with the plasma membrane. As with the Golgi bodies, niitochondria often appeared to be lined up within the pseudo-compartments of cytoplasm. In sections approximately parallel to and near the lower wall of the endothecium, a symmetrical arrangement of organelles was several times observed: a thickened bar or wall -^ cisternae of ER -* line of Golgi bodies line of mitochondria -* line of Golgi bodies * cisternae of ER -* a thickened bar or wall [Fig. 3(c)]. However, either extensive serial sectioning or thick sectioning used in conjunction with a high voltage electron microscope would be required to test the validity of this observation. Even if the observation is correct, it would still be unclear whether the arrangement of organelles were functional or merely a response to the limited space available. Although many sections were examined, few microtubules associated with the bars of thickening were positively identified [Fig. 2(f)]. However, structures like lomasomes were seen on the plasma membrane both where it bordered the thickened bars and close to the junction between bars and the adjacent unthickened wall [Fig. 3(d)]. The thickenings themselves appeared fibrillar. In thin sections of xylem elements, at the early stage of development examined, some extensive longitudinal cisternae of rough ER appeared to enclose the central vacuole and nucleus; others ran parallel to the main wall but at some distance in from the plasma membrane [Fig. 4(a)]. To oversimplify, these cisternae may be compared with two much interrupted and irregular cylinders, one set inside the other, and with many interconnections between. Connected externally to the outer ER 'cylinder' in the xylem were transverse flanges of ER [Fig. 4(a), (b)]. These were looped or branched at the ends and appeared to bisect the small cytoplasmic protrusions between adjacent bars of thickening which were more closely spaced than those in the endothecium; the peripheral ER in the endothecium extended around the perimeter of the equivalent but wider, cytoplasmic projections between the bars [Fig. 3(b)]. The overall effect produced in thin sections of xylem was that the entire cytoplasm was again subdivided by rough ER into pseudo-compartments but these were much smaller than those in the endothecium. Each xylem 'compartment' appeared to be packed with Golgi bodies and vesicles [Fig. 4(a)]; often a mitochondrion (sometimes more than one) was also included. The Golgi vesicles of the xylem were more varied in size and content than those in the endothecium; many contained an electron opaque spot [Fig. 4(c)]. Densely packed microtubules closely paralleled the bars of thickening [Fig. 4(d)]. Irregularly Fig. 3.(a) Part of an endothecial cell showing an extended line of Golgi bodies (arrows). Bud: 2 5 to 3 0 mm. x (b) The junction between bars of wall thickening and the unthickend wall between the endothecium and the epidermis. Cisternae of ER mark the edge of the pseudo compartments of cytoplasm between adjacent thickened bars. Bud: 2 5 to 3 0 mm. x (c) Part of a section parallel and close to the base of an endothecial cell. A long cisterna of ER (double arrow head) runs parallel with the bar of thickening; discontinuous short cisternae (single arrow head) He close to the unthickened wall. Golgi bodies (asterisk) and mitochondria (M) are present. Golgi vesicles (single arrow) lie adjacent to the plasma membrane and contain an electron transparent component. Bud: 2 5 to 3-0 mm. x (d) Lomasome-like structures (arrows) associated with a thickened wall bar. Bud: 2 5 to 3-0 mm. x For abbreviations see legend to Figure
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9 Fine structure of Phaseolus 569 dispersed vesicles of varying size appeared to lie outside the microtubular sheaths [Fig. 4(b)]. The diameter of even the smallest vesicles exceeded the distance between adjacent microtubules. However small structures, usually circular in section, more similar in size to the electron opaque spots than to the many Golgi vesicles which contained them, could sometimes be seen between the plasmamembrane and the bars of wall thickening [Fig. 4(a), (e)]. DISCUSSION During differentiation of both the xylem and the endothecium, the walls develop characteristically thickened bars. In the xylem these bars begin to form soon after the cells are first established; in the endothecium bar development is long delayed. The xylem thickenings become lignified; endothecial bars in some species, including Phaseolus vulgaris, may also be lignified. It is generally assumed that vesicles produced by Golgi bodies play some role in transporting material used during wall formation. In both the xylem and the endothecium, as the walls become thickened, Golgi bodies and their associated vesicles become numerous; In addition, rough ER becomes prolific. The Golgi bodies seems to be concentrated in pseudo-compartments of cytoplasm delimited by ER. However, the size and shape of these pseudo-compartments, like the patterns of wall thickening themselves, differ in the two types of cell: the arrangement of the Golgi bodies within the compartments also differs. In Phaseolus Golgi vesicles in the xylem at the stage of development examined were varied in both size and content but included many which resembled the Class 2 electron transparent vesicles with electron opaque dots described by Goosens-de-Roo (1973). Golgi vesicles in the differentiating endothecium were more uniform. Most contained an electron transparent component; none was seen to contain an electron opaque spot. Although the method of tissue preparation was the same for both the xylem and the endothecium, microtubules were numerous and characteristically sited adjacent to the bars of xylem thickening but could seldom be identified in the endothecium. Whether this virtual absence of associated microtubules from the cytoplasm adjacent to the endothecial thickenings represents a true situation or (perhaps more probably) an artefact of fixation of this particular tissue remains undetermined. Three different, and in part contradictory, suggestions have been made about how sites of fusion between vesicles transporting wall material and the plasmamembrane are controlled and how differential wall thickening is accomplished (summarized in Gunning and Steer, 1975): (1) in developing xylem, sheets of ER prevent access of vesicles to the walls between the bars of thickening and their associated bands of microtubules; conversely, (2) the close juxtaposition of ^icrotubules prevents access of vesicles to the bars and hence fusion with the. 4.(a) An immature xylem element with long parallel cisternae of ER and numerous Golgi bodies and vesicles, x (b) Many microtubules (arrow) are associated with the bars of xylem thickening. Parallel cisternae of ER with branched or looped ends bisect the compartments of cytoplasm between adjacent bars, x (c) Golgi vesicles containing electron opaque spots. ^ (d) Part of a bar of xylem thickening showing its associated sheath of densely packed microtubules. x (e) Numerous small, usually circular, structures (single arrow) lie between Ae plasma membrane and the bar of xylem thickening. Golgi vesicles with electron opaque spots (double arrow) are present in the cytoplasm between cisternae of ER and close to the plasmamembrane. X Eor abbreviations see legend to Figure 1.
10 57O J- M. WHATLEY plasma membrane can only take place between adjacent thickenings; (3) microtubules may 'lift' the plasma membrane away from the wall; new wall material flowing into this space then forms the thickenings. In the xylem and endothecium of Phaseolus vulgaris each of which has its own pattern of wall thickening, both the ER and the Golgi bodies appear to be characteristically disposed but in different patterns during maturation of the two types of cell. In the xylem, concentrations of small electron opaque structures similar in size to the electron opaque spots in nearby Golgi vesicles have been found in the 'space' parallel to and lying between the plasma membrane and the wall bars. These electron opaque structures might perhaps be the contents released from Golgi vesicles following their fusion with the plasma membrane, but this would be difficult to confirm. In the endothecium lines of Golgi bodies appear to parallel the bands of thickening but the two are often separated by cisternae of ER; other small groups of Golgi bodies are often concentrated in the angle where the thickened bars join the unthickened wall and it is here, where the ER is discontinuous, that Golgi vesicles lie adjacent to the plasma membrane. Occasional lomasome-like structures have been seen both where the plasma membrane borders the thickenings and where the bars meet the unthickened wall. In otber types of cell, e.g. collenchyma, lomasomes have been shown by autoradiography to contain the wall matrix polysaccharides, pectins and hemicelluloses (Cox and Juniper, 1973). In both the xylem and the endothecium, the completion of thickening seems to be associated with the beginning of cytoplasmic disintegration. Xylem maturation is associated with increased vacuolation and a progresive reduction in volume of the degenerating cytoplasm. In the endothecium the apparently rapid disintegration seems to be associated with plasmolysis and a general collapse of the cytoplasm. However, this conclusion must be treated with caution as the osmotic properties and the fine structure of degenerating tissue are often considerably altered during preparation for examination in the electron microscope. ACKNOWLEDGEMENTS I should like to thank Mrs Lysbeth Richards for her help in preparing the anthers for electron microscopy. REFERENCES Cox, G. C. & JUNIPER, B. E. (1973). Autoradiographic evidence for paramurai body function. Nature, 234, 116^117. EAMES, A. J. (1961). Morphology of the Angiosperms. McGraw Hill, New York. FossARD, R. A. DE (1969). Development and histochemistry of the endothecium in the anthers of in 1''^^" grown Chenopodium rubrum L. Botanical Gazette, 130, FOSTER, A. S. & GIFFORD, E. M. JR (1974). Comparative Morphology of Vascular Plants. W. H. Freeman & Company, San Francisco. GOOSEN-DE-ROO, L. (1973). The relationship between cell organelles and cell wall thickenings in priman tracheary elements of cucumber. I. Morphological aspects. Acta Botanica Neerlandica, 22, 279 3u GUNNING, B. E. S. & STEER, M. W. (1975). Ultrastructure and the Biology of Plant Cells. Edward AW London. SABLON, L. DU (1885). Recherches sur la structure et de la dehiscence de antheres. Annales des Naturelles {Botanique) Serie, 1, (cited in Eames, 1961). WHATLEY, J. M. (1978). A suggested cycle of plastid developmental interrelationships. New Phytologist
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