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Pollen Tube Development in Petunia Hybrida Following Compatible and Incompatible Intraspecific Matings

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Pollen Tube Development in Petunia Hybrida Following Compatible and Incompatible Intraspecific Matings J. Cell Sd. 47, 365-383 (1981) 365 Printed in Great Britain © Company of Biologists Limited ig8i POLLEN TUBE DEVELOPMENT IN PETUNIA HYBRIDA FOLLOWING COMPATIBLE AND INCOMPATIBLE INTRASPECIFIC MATINGS MARIA HERRERO* AND H. G. DICKINSON Department of Botany, Plant Science Laboratories, University of Reading, Whiteknights, Reading RG6 2AS, U.K. SUMMARY Pollen tubes formed following compatible and incompatible intraspecific matings in Petunia have been examined with light and electron microscopes. Compatible and incom- patible tubes develop in an identical fashion on the stigma but, on entry into the top 1 mm of the stylar transmitting tissue changes occur both to the cytology of the tubes and their rates of growth. The early cytological changes are common to tubes of both compatibilities but, although both types of tube accelerate on entry into the style, incompatible tubes grow more slowly than compatible. Cytological differences became apparent between compatible and incompatible tubes following a short period of growth in the style, the latter possessing thicker cell walls and a cytoplasm packed with both organelles and reserves. Incompatible tubes subsequently burst or simply cease growth and die. The characteristic image afforded by this cytoplasm resembles that of burst or dead compatible tubes, except in that proportions of the cell com- ponents may differ. These data are discussed in terms of current models proposed to explain pollen tube growth and the operation of the self-incompatibility response in Petunia. INTRODUCTION As in many plants with gametophytic control of pollen compatibility with respect to the style, pollen tubes of Petunia formed following a self-mating fail to reach the ovary. Growing more slowly than tubes from a cross-pollination they eventually cease development in a region some two-thirds of the way down the style. Since much is known of the physiology of and structures involved in pollen tube growth, it is not unreasonable to expect that the differences in development between tubes of different compatibilities might easily be explained by changes in the ultrastructure and physio- logy of the tube cytoplasm. This has not proved to be the case. Striking ultrastructural differences between compatible and incompatible tubes were reported as early as 1966 by van der Pluijm & Linskens who described the walls of incompatible tubes as being far thicker than those derived from compatible crosses. In a comprehensive investigation into the cytology of pollen tube growth in Lyco- persicum (de Nettancourt et al. 1973), the arrest of incompatible pollen tubes was reported to result partly from the cessation of protein synthesis, itself caused by ribosome-coated endoplasmic reticulum forming into concentric whorls (de Nettan- court et al. 1974), and from the binding of an 'incompatibility protein' to wall-precursor containing bodies in the tube cytoplasm. Such results were not fully • Present address: INIA, Apartado 202, Zaragoza, Spain. 366 M. Herrero and H. G. Dickinson confirmed by work on Oenothera (Dickinson & Lawson, 19756) where growth of incompatible tubes appeared to be accompanied in the first instance by changes in the carbohydrate metabolism of the tube, with resultant changes in the cell wall. Data from this investigation did, however, reveal that considerable modification of the cytoplasmic components involved in cellulose biosynthesis is required to permit the very rapid rate of growth characteristic of these tube cells. Because the elongating pollen tubes are embedded in stylar tissue, physiological investigations have not been easy. Work by van der Donk (1974) has, however, shown differences between tubes of differing compatibilities to become evident very soon after pollination. So much so that Linskens (1975) has proposed the 'recognition' stage of the self-incompatibility response to operate in the stigma. Despite the considerable effort expended in these and other investigations, we are still in ignorance both as to the point in tube metabolism at which the self-incompa- tibility mechanism has its primary effect and, indeed, of the means by which pollen tube elongation is arrested. We report here an investigation into these events in Petunia, the results of which are discussed in terms of the accompanying changes that occur in the tissue of the pistil (Herrero & Dickinson, 1979). MATERIALS AND METHODS Details of the plant material used in this study, together with the methods of preparation of tissue for light and electron microscopy are set out in Herrero & Dickinson (1979). The methods for staining resin-embedded material with Coomassie Brilliant Blue (CBB) are described by Fisher (1968). RESULTS Pollen germination and tube growth at the stigma surface Within 30 min of pollination most grains germinate (Fig. 2) and develop a tube at least 30 jim in length. Conspicuous changes overcome the pollen during early stages in germination, firstly a fibrogranular matrix (Figs. 1, 3) that encased the mature grain Fig. 1. Colpal region of uninucleate microspore (p), still retained in the anther. Fibrils (/) are visible in the sculptured exine, facing the loculus (/). x 8620. Fig. 2. Scanning electron micrograph of mature pollen grain (g) on the stigma (s). Note the absence of any deposition on the exine surface. The globules (/) are presumably derived from the stigmatic fluid. A germinal pore (p) is also visible, x 5640. Fig. 3. Low-power transmission micrograph of material shown in Fig. 6. The exine (e) is free from fibrils. The vegetative nucleus (n) and a germinal pore (/>) are also shown, x 2050. Fig. 4. Light-microscopic preparation of pollen grain germinating on the stigma, reacted to reveal acid phosphatase. Higher levels of the enzyme, which appears to be in packets, are contained in the tube (f) than the grain (g). x 730. Pig. 5. Tip of pollen tube growing on the stigmatic surface. Note the spherical vesicles (arrows). The cell wall (w) is fibrous and disorganized, and the ground cyto- plasm very electron-opaque, x 16300. Pollen tube development in Petunia 367 368 M. Herrero and H. G. Dickinson in the anther becomes no longer detectable and, secondly, marked changes occur in the pollen cytoplasm. Here, instead of the electron-opaque protoplast characteristic of the grain prior to dispersal, a more electron-lucent cytoplasm is seen, containing increased amounts of rough endoplasmic reticulum, dictyosomes, and associated vesicles. The plasma membrane, previously smooth and featureless, now appears active, and is formed into numerous small projections associated with vesicles. Other components of this germinating protoplast are droplets of unsaturated lipid, diffuse fibrous masses, mitochondria, the vegetative nucleus and the generative cell. Although all the microbodies present in the cytoplasm appear identical under the electron microscope, light-microscopic histochemical tests indicate 2 classes of microbody to be present, one containing acid phosphatase (Fig. 4) and the other a peroxidase. The peroxidase-containing bodies survive for only some 60 min after germination, whereas those containing acid phosphatase may be found throughout development of the pollen tube. Clearly the cytoplasm of the young pollen tube on the stigma surface is contin- uous with that of the pollen grain, but since differences occur in the composition of the cytoplasm between the various regions of the tube, these areas are probably more helpfully described individually. At the tube tip, the cytoplasm is comparatively electron-opaque and the protoplast surface very irregular, such that the plasma membrane is undetectable (Fig. 5). At this surface are numerous vesicles, similar to those seen near dictyosomes deeper in the cytoplasm. The wall of the pollen tube tip consists solely of loosely woven fibrils showing no particular organization (Fig. 5). Back from the tip, the plasma membrane of the tube becomes better defined and the fibrils of the wall organized in particular directions (Fig. 6). Even at this point, the presence of callose is neither indicated by electron microscopy nor by cytochemical tests. While only small mitochondria may occasionally be discerned in the cytoplasm of the tube tip, here these organelles are far more frequent. Conspicuous also are large aggregates of fibrous material, similar to that of the tube wall, and masses of folded membrane reminiscent of the myelin figures of animal cells. Numerous vesicles still populate this cytoplasm, many of which appear associated either with the plasma membrane or with the fibrous masses (Fig. 6). Examination of the pollen tube wall close to the grain reveals it to consist of an outer, well organized fibrillar layer and an inner, electron-lucent layer adjacent to the plasma membrane (Fig. 7). Conspicuous in this cytoplasm are large numbers of Fig. 6. Transverse section of pollen tube, as depicted in Fig. 5, but further back from the tip. Large fibrous masses are present (/), as are vesicles (arrows) and mitochondria (w). «>, wall, x 21400. Fig. 7. As Fig. 5, further back along the tube towards the grain, showing the presence of a thin electron-lucent layer (p) between the plasma membrane (arrows) and the fibrous wall (w). x 15200. Fig. 8. Transverse section of pollen tube, as depicted in Figs. 6, 7. Here the cytoplasm is more electron-lucent, containing elements of rough endoplasmic reticulum (e), mitochondria (m), and a paramural body (p). The lipidic stigmatic fluid (s) is also visible, x 14170. Pollen tube development in Petunia 369 . 8 370 M. Herrero and H. G. Dickinson membranous cisternae, normally identified with paramural bodies (Fig. 8). This cytoplasm is also rich in rough endoplasmic reticulum, mitochondria, plastids and microbodies (Figs. 7, 8). Light-microscopic tests indicate callose to be present in this wall (Fig. 10) and bodies containing acid phosphatase to populate the protoplast. By the time the tube has grown to a length of some 200 /tm the vegetative nucleus and the generative cell are also to be found in this region (Fig. 9). A large vacuole has developed in the pollen grain by this stage, sometimes extending into the tube itself.
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