TRACHEARY OCCLUSION IN FRONDS OF PTERIDIUM AQUILINUM (L.) KUHN SHOWING APOSPORY
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1 New Phytol. (1982) 90, TRACHEARY OCCLUSION IN FRONDS OF PTERIDIUM AQUILINUM (L.) KUHN SHOWING APOSPORY BY E. SHEFFIELD*, P. R. BELLf AND S. LAIRDf * Cryptogamic Botany Laboratories, University of Manchester, Manchester M13 9PL, U.K. t Department of Botany and Microbiology, University College London, Gower Street, London WCIE 6BT, U.K. {Accepted 19 July 1981) SUMMARY The occlusion of tracheids in aposporous fronds of Pteridium aquilinum attached to parent plants was found to account for the failure of dye to penetrate to the leaf extremities. The agent responsible for this blockage was seen as an electron-opaque layer covering the walls and areas of overlap between tracheids. The aposporous behaviour of attached leaves is attributed to the discontinuation in supply of some influence from the parent plant which results from the tracheary occlusion observed. INTRODUCTION Although the investigation of apospory has been largely concerned with organs severed from plants, a recent study revealed that outgrowths occasionally occur on attached leaves (Sheffield and Bell, 1981a). The development of gametophytic outgrowths from juvenile laminae apparently possessing full vascular connection with the parent plant was accompanied by the failure of a dye to penetrate to the leaf extremities. It was therefore proposed that such aposporous behaviour in attached leaves resulted from cessation of vascular activity within the laminae leading to the deprivation of peripheral tissue of some influence which normally maintained the sporophytic condition. The intention of the present study was to elucidate the nature of the vascular block and to identify the agent preventing xylem flow. MATERIALS AND METHODS Plants of Pteridium aquilinum (L.) Kuhn were raised in aseptic conditions as described by Sheffield and Bell (1981b). Plants which had been cultured for 7 to 10 weeks and in which fronds in contact with the medium had produced aposporous outgrowths were placed in a 1 % solution of eosin (Gurr) so that the roots and parent gametophyte were submerged. After 1 to 2 h aposporous fronds were detached and examined with a Wild M8 stereomicroscope. Portions of lamina containing the site at which dye ceased to penetrate were excised and prepared for electron microscopy as previously described (Sheffield and Bell, 1981a). Similar tissue from non-aposporous laminae, where the dye penetrated freely, was taken as a control. The sections were examined in a Hitachi HS9 or AEI 6B electron microscope X/82/ $02.00/ The New Phytologist
2 322 E. S H E E F I E L D, P. R. B E L L A N D S. LAIRD Material was similarly fixed and dehydrated for light microscopy, but embedding was in L.R. White resin (London Resin Company). Sections were cut at 1-5 /*m, stained witb 0-5 % aq. toluidine blue (Gurr) and examined microscopically using a Leitz Dialux 20 photomicroscope. Four plants cultured for 8 weeks were harvested and portions of the juvenile laminae cut off using a microscalpel. The cut edges of two of the laminae were covered with vaseline, the remaining two left untreated. The plants were then placed in eosin so that only the roots and parent gametophyte were submerged. After 2 h the laminae were examined with the stereomicroscope. RESULTS The tracheids of the juvenile laminae were about 80 /im long and had spiral or annular thickening. The areas of overlap between tracheids were short, averaging about 17/*m, and variously oblique [Fig. l(a) inset]. The primary wall between thickenings was often insubstantial [Fig. l(a)]. In fronds which had found contact with the medium, and which had produced aposporous outgrowths, the tracheids at the limit of penetration of the dye were found to bear an electron-opaque layer on their walls and inner faces. This substance formed a continuous layer beneath which the primary wall and thickenings remained visible [Fig. l(b)]. No pits or pores were detected traversing this deposit. Examination at higher magnification showed that the surface of the electron-opaque layer was uneven and continuous with fibrillar material in the lumen [Fig. l(c)]. No similar deposits were found in tracheids at any site in the control laminae. The cells adjoining the tracheids in some aposporous laminae contained membrane-bound bodies, in the order of 5 /^m and 2 fim wide, containing granules and aggregates of electron-opaque material [Fig. l(d)]. The cytoplasm adjacent to these bodies was ill-defined. Removal of portions of laminae did not prevent eosin rising rapidly to the extremities of all the veins of juvenile laminae. Blockage of the severed ends of the veins with vaseline also failed to stop the fiow to the extremities. DISCUSSION Although vessels have been reported to occur in Pteridium (e.g. Esau, 1965), the juvenile laminae described here contained only tracheids. Despite their relatively short oblique terminal overlaps, the tracheids did not have end plates which could be distinguished from the lateral walls. There were no complete perforations at the ends of the tracheids, fulfilling the second condition distinguishing tracheids from vessels (White, 1963). The middle lamella and primary wall between the gyres Eig. l(a). Junction between two tracheids in a non-aposporous frond. Remnants of primary wall are present between the wall thickenings (arrow), x Inset 1-5/tm section through similar tissue to show area of tracheid overlap, x (h) Junction between tracheids in area of dye stoppage in an aposporous frond. A thick layer of electron-opaque material can be seen covering the walls, fragments of material similar in appearance are present in the lumina (arrows), x (c) End of tracheid in area of dye stoppage in an apoporous frond showing diffuse electron-opaque material in the lumen and deposited on the walls, x (d) Tracheid and adjoining cell in region of dye stoppage in an aposporous frond. Electron-opaque material covers the tracheid walls, and a single-membrane-bound hody containing electron-opaque inclusions can be seen in the adjoining cell (arrow), x
3 Tracheary occlusion in Pteridium/row<i5 323
4 324 E. S H E F F I E L D, P. R. B E L L AND S. LAIRD of secondary wall thickening were nevertheless insubstantial in some specimens examined, presumably due to the hydrolysis of the primary wall found in a wide range of ferns (Warmbrodt and Evert, 1978, 1979a, b). It seems likely, therefore, that xylem flow passes through both the lateral and terminal regions of tracheids in young fronds oi Pteridium. The presence of a layer of material covering the walls and interfaces of the tracheids could therefore account for the cessation of xylem flow previously reported in such fronds (Sheffield and Bell, 1981a). Electron-opaque deposits overlying the secondary wall of tracheary elements have been seen in a large number of plants. The 'warty layer' of gymnosperms and angiosperms (e.g. Liese, 1965) and deposits seen in some pteridophytes (e.g. Tarchi and Francalanci, 1973) are thought to represent remnants of the original protoplast lining the walls (Warmbrodt and Evert, 1978). These deposits, however, take the form of discrete aggregates, and never a complete covering such as that reported here. The absence of an electron-opaque layer in non-aposporous tracheids of juvenile fronds of Pteridium suggests this layer is not produced by degeneration of the protoplast. In that event, it must consist of substances travelling inwards from surrounding cells, or upwards from preceding cells. No profiles, however, were seen which suggested that the membrane-bound bodies containing electron-opaque material in cells adjacent to the tracheids discharged their contents into them. Indeed the presence of the electron-opaque layer coincided with the appearance of the membrane-bound bodies, whereas if the layer was derived from them a sequential relationship would have been expected. Membranebound inclusions rather similar in appearance have been observed in normal vascular tissue of several pteridophytes (e.g. Perry and Evert, 1975; Warmbrodt and Evert, 1979) and so their presence in aposporous tissue is thought to be coincidental rather than of causal significance. The occluding material is therefore thought to result from substances travelling upwards within the xylem. Profiles such as those seen in Fig. l(b) and (c) are consistent with the suggestion that contents of the lumen of the tracheids are becoming deposited on to the walls. It is possible that solutes travelling upwards in the xylem precipitate at this point and form the layer observed. Physiological changes resulting from the contact of a frond with the medium might account for this change in solubility. The process would therefore be analogous to that of gummosis, 'the deposition of complex and variable substances, commonly referred to as gum, in xylem in response to physiological disturbance' (Esau, 1948). It might be expected that the aqueous conditions experienced by tissue in contact with medium would eliminate the water potential of the cells and halt transpiration. The experiments with truncated laminae show, however, that xylem flow results at least partially from root pressure. Ingress of water and solutes into the laminae would therefore continue so long as the tracheids were not completely occluded. The period required for the accumulation of sufficient material to occlude the tracheids is though to account for the delays observed in the production of outgrowths by attached fronds contacting the medium. Although detached fronds produce outgrowths after only a few days of culture, attached fronds in contact with medium take considerably longer (Sheflield and Bell, 1981a), and it seems from the present investigation that this lag corresponds to the time needed for the blocking of the tracheids. We therefore have further evidence that aposporous behaviour results from a cessation of the supply of certain substances reaching the lamina by way of the xylem from the parent plant (Sheffield and Bell, 1981a). Since the occluding material described here showed no firm specificity of
5 Tracheary occlusion in Pteridium fronds 325 staining reaction, showing some affinity for osmium, uranyl acetate and lead citrate when used in isolation, the chemical composition of this layer is at present unknown. Experiments are therefore continuing in order to determine the exact nature of this material. REFERENCES ESAU, K. (1948). Anatomic effects of the viruses of Pierce's disease and phony peach. Hilgardia, 18, ESAU, K. (1965). Plant Anatomy. John Wiley & Sons, New York. LiESE, W. (1965). The warty layer. In: Cellular Ultrastructure of Woody Plants (Ed. by W. A. Cote), pp Syracuse University Press, Syracuse. PERRY, J. W. & EVERT, R. E. (1975). Structure and development of the sieve elements in Psilotum nudum. American Journal of Botany, 62, SHEFFIELD, E. & BELL, P. R. (1981a). Cessation of vascular activity correlated with aposporous development in Pteridium aquilinum (L.) Kuhn. New Phytologist, 88, SHEFFIELD, E. & BELL, P. R. (1981b). Experimental studies of apospory in ferns. Annals of Botany, 47, TARCHI, A. M E. & FRANCALANCI, C. (1973). Osservazioni suh' ultrastruttura delle cellule cribose di Psilotum nudum (L.) Beau V. Caryologia, 26, WARMBRODT, R. D. & EVERT, R. E. (1978). Comparative leaf structure of six species of heterosporous ferns. Botanical Gazette, 139, WARMBRODT, R. D. & EVERT, R. E. (1979a). Comparative leaf structure of several species of homosporous leptosporangiate ferns. American Journal of Botany 66, WARMBRODT, R. D. & EVERT, R. E. (1979b). Comparative leaf structure of six species of eusporangiate and protoleptosporangiate ferns. Botanical Gazette, 140, WHITE, R. A. (1963). Tracheary elements of the ferns. II. Morphology of tracheary elements; conclusions. American Journal of Botany, 50,
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