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Egg Activation in Flowering Plants

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Egg Activation in Flowering Plants Sex Plant Reprod (2001) 14:21–26 © Springer-Verlag 2001 REVIEW A.F. Antoine · C. Dumas · J.-E. Faure · J.A. Feijó M. Rougier Egg activation in flowering plants Received: 2 December 2000 / Accepted: 7 June 2001 Abstract Compared to animals and algae, egg activa- cal event is the cortical reaction which involves exocyto- tion in flowering plants is still poorly understood be- sis of cortical granules and elevation of the fertilization cause of the inaccessibility and complexity of the fertili- envelope (Moser 1939). In Lychetinus pictus eggs, a set zation process which is double and internal. However, of events are observed that begins with (see also Stricker the development of in vitro fertilization (IVF) systems in 1999; Whitaker and Steinhardt 1982) (1) immediate cor- maize and a few other plants, despite some limitations, tical [Ca2+] increase (the cortical flash) and membrane offers new possibilities for the study of early post- potential variations (the fertilization potential). Within fusional events and signals leading to egg activation un- the first 5 min, this is followed by (2) a global cytosolic der defined conditions. This review reports recent data [Ca2+] increase (the Ca2+ wave), cortical reaction, activa- on calcium events induced by gamete fusion during tion of kinases and phosphates, proton efflux and in- maize IVF and presents perspectives on the role of calci- crease in O2 consumption (the respiration burst). Within um in egg activation and in early development. 15–20 min we observe (3) initiation of traduction then of replication. Within 60–80 min there is (4) mitosis and Keywords Zea mays · In vitro fertilization · Egg within 85–95 min (5) the first cell division. activation · Calcium Egg activation has been the subject of numerous in- vestigations in both animals and algae (Roberts and Brownlee 1995; Stricker 1999), and involvement of a cy- 2+ 2+ Introduction: tosolic [Ca ] (cyt[Ca ]) increase has been proposed as a egg activation or how to initiate a new organism? key event leading to egg activation at an early stage (Jaffe 1980). This hypothesis has now been validated in a num- Female gametes can be viewed as quiescent cells which ber of species. So far, every species studied shows at least 2+ require fertilization for reactivation. Fertilization triggers a cyt[Ca ] elevation after gamete fusion (for review see “egg activation”, a preprogrammed set of events that Ciapa and Chiri 2000; Stricker 1999). However, each leads to the development of a new individual. These system is characterized by a unique spatio-temporal pat- 2+ events fall into three broad categories: morphological, tern of the cyt[Ca ] elevation. For instance, in Lychetinus physiological and biochemical. Each event is precisely pictus eggs, gamete fusion induces an immediate Ca2+ in- timed and plays a unique role in the activation of devel- flux through voltage-activated calcium channels (the cor- 2+ opment. For instance, in sea urchins, where egg activa- tical flash) during which the cyt[Ca ] elevation is restrict- tion is well documented, the most obvious morphologi- ed to the cortical region of the egg (Shen and Buck 1993). 2+ Then, within 500–3000 s a global cyt[Ca ] increase A.F. Antoine (✉) · C. Dumas · J.E. Faure · M. Rougier spreads as a wave across the cytosol (Gillot and Whitaker Laboratoire de Reproduction et Développement des plantes. 1993; Steinhardt et al. 1977). In contrast, in the echiurian UMR 5667 CNRS, INRA, UCB Lyon 1, ENS Lyon, Urechis caupo gamete fusion induces a single Ca2+ tran- 46 Allée d’Italie, 69364 Lyon Cedex 07, France e-mail: [email protected] sient that does not spread in a wavelike fashion (Stephano Tel.: +33-4-72-72-86-14, Fax: +33-4-72-72-86-00 and Gould 1997). A Ca2+ influx is necessary for this [Ca2+] elevation, although simultaneous Ca2+ release J.A. Feijó cyt Instituto Gulbenkian de Ciência, 2780-156 Oeiras, Portugal from internal stores may also be required. 2+ The proposition that a cyt[Ca ] elevation is necessary Present address: and sufficient for egg activation was also made early (for J.A. Feijó, Centro de Biotecnologia Vegetal, Faculdade de Ciências, Univ. de Lisboa, Campo Grande, review see Epel 1990; Steinhardt et al. 1974; Whitaker Ed.C2, 1749-016 Lisboa, Portugal and Swann 1993). To demonstrate this, it is necessary to 22 2+ prove that (1) an artificial cyt[Ca ] elevation triggers egg present only during a defined time period between polli- activation in unfertilized eggs and that (2) preventing the nation and the first zygotic division, and it may play a 2+ cyt[Ca ] elevation during fertilization inhibits egg acti- role in gamete adhesion and fusion. Polarization pre- vation. Such demonstrations have so far been attempted cedes the first zygotic division; in maize the mass of the only in few species, namely, sea urchin, ascidians and cytoplasm which initially occupies a central position mammals (see Evans and Kopf 1998; Stricker 1999). shifts to the apical pole of the zygote (Mòl et al. 1994). In plants, egg activation was first analyzed in easily Historically, the development of in vitro fertilization accessible systems such as fucoid algae (Brownlee (IVF) systems has proved to be useful for analysis of egg 2+ 1994). In Fucus, egg activation is triggered by a cyt[Ca ] activation in animals and algae. In flowering plants, de- increase which is localized to the cortical region and velopment of such systems has been delayed due to the takes place simultaneously throughout the egg (Roberts necessity of isolating male and female gametes (for re- 2+ 2+ et al. 1994). This cyt[Ca ] increase results from a Ca view see Chaboud and Perez 1992; Theunis et al. 1991) influx through voltage-gated calcium channels that is before performing in vitro fusion (for review see Kranz triggered by fertilization (Taylor and Brownlee 1993). 1999; Kranz and Dresselhaus 1996). The earliest plant Minutes after fusion, exocytosis of the cortical granules IVF system was developed by Kranz and co-workers is observed and a new cell wall is synthesized (Brawley (Kranz et al. 1991) who used electric pulses to induce fu- et al. 1976a). Subsequently, the zygote starts to polarise sion between an egg cell and a male gamete in Zea mays. (Brawley et al. 1976b) and the first cell division is un- Using this IVF system, whole plants could be regenerat- equal (for review see Robinson et al. 1999). Thus, mech- ed from in vitro fusion products using feeder cells anisms of egg activation in algae and in animals, which (Kranz and Lörz 1993). The same technique was also both use naturally free-living gametes for fertilization, used to produce endosperm in vitro by fusing a male ga- appear analogous. In flowering plants, the situation is mete and the central cell (Kranz et al. 1998). In maize, different and more complex because fertilization is dou- alternative IVF systems were also developed which used ble and internal. During double fertilization, two male Ca2+ as a mediator of fusion instead of an electrical pulse gametes undergo gametic fusion; one fuses with the egg (Faure et al. 1994; Kranz and Lörz 1994). IVF systems cell, giving rise to the embryo, and the other fuses with were also developed in other species (Coix, Sorghum, the central cell, giving rise to the endosperm (Russell Hordeum, Triticum and Nicotiana) using either electro-, 1992). In contrast to animals and algae, male gametes calcium- or PEG-mediated fusion (Kovacs et al. 1994; seem to be non-motile and female gametes are deeply Kranz et al. 1995: Sun et al. 2000). All of these IVF sys- embedded in the female tissues. Given these differences, tems give direct access to the egg activation events in- it is important to investigate whether egg activation in duced by gametic fusion, and to early embryogenesis flowering plants follows the same principle as in other (for review see Dumas and Faure 1995; Rougier et al. organisms. 1996; Kranz 1999; Faure and Dumas 2001). Despite the usefulness of these IVF systems for the study of egg activation in flowering plants, data obtained What do we know about egg activation should always be carefully viewed in light of the fact in flowering plants? that in vitro fertilization conditions differ from those in vivo. In vivo, fertilization processes take place inside Events triggering egg activation following in vivo fertili- maternal tissues which can interact with the egg cell. In zation in flowering plants are poorly understood. A num- contrast, IVF systems permit analysis of fusion and acti- ber of ultrastructural studies in various species have re- vation events without the influence of maternal tissues ported reorganization of the egg cell following its fertili- and under defined conditions. Another difference is that zation (for reviews, see Russell 1993; Van Went and the male gametes used for IVF are isolated directly from Willemse 1984). Changes in zygote volume and in the mature pollen instead of being liberated following their number of ribosomes or organelles such as endoplasmic transport through the pistil inside a pollen tube, a step reticulum or dictyosomes have been reported in addition that may be important for their final maturation. In addi- to the synthesis of a cell wall around the zygote. In tion, egg cells used for IVF (with the exception of barley, maize, data is derived mainly from electron microscopy wheat and rape seed, see Kranz 1999) are treated with studies (Diboll 1968; Van Lammeren 1986). The most cell wall degrading enzymes, a treatment which may af- documented aspect of maize egg activation is the in- fect their physiology. Finally, the in vitro fusion media, volvement of the cytoskeleton. Pollination induces accu- used at present, contain no nutrients to support the meta- mulation of actin patches in the cytosol which later accu- bolic reactivation undergone during egg activation.
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