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Lnduction of Polarity in Fucoid Zygotes

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Lnduction of Polarity in Fucoid Zygotes The Plant Cell, Vol. 9, 1O1 1-1 020, July 1997 O 1997 American Society of Plant Physiologists lnduction of Polarity in Fucoid Zygotes Darryl L. Kropf' Department of Biology, University of Utah, Salt Lake City, Utah 841 12 INTRODUCTION Early events 'in the vegetative development of higher land Developing embryos of many land plants, including Arabidop- plants are difficult to investigate because the young embryo sis, undergo a similar pattern of cell divisions (Figure 1; see is encased in the ovarian tissue of the previous gametophytic also Laux and Jürgens, 1997, in this issue). and sporophytic generations. Recently, genetic approaches This review highlights recent progress in understanding have succeeded in identifying mutations that alter early devel- the polarization of fucoid zygotes, with an emphasis on opment (Jürgens, 1995; see also Laux and Jürgens, 1997, in early events involved in polarity induction in Pelvetia. this issue), but cellular and physiological analyses of higher Readers are directed to a comprehensive review (Kropf, plant embryogenesis remain tedious. 1992) and to other more specialized reviews (Goodner and Brown algae of the family Fucales (comprising the genera Quatrano, 1993; Kropf, 1594; Berger and Brownlee, 1995; Fucus and Pelvetia) are, however, very tractable for investi- Fowler and Quatrano, 1995; Quatrano and Shaw, 1997) for gating early plant embryogenesis, especially the establish- additional analyses and opinions. ment of developmental polarity. These marine organisms grow attached to rocks in the intertidal zone and are typi- cally 0.25 to 0.5 m in height at maturity. Zygotes, eggs, and sperm are shed from fronds of mature plants in the labora- POLARITY INDUCTION tory and can easily be harvested in gram quantities, free of other tissues. Young zygotes attach firmly to the substra- tum, and populations of adhering zygotes transit synchro- The induction of polarity in fucoid zygotes is a continuum of nously through early development. overlapping events that occur during the first 10 hr after fer- In the Fucales, mature eggs are radially symmetric, and tilization (AF). For convenience, I consider polarity induction cell polarization does not occur until after fertilization. The to occur in two stages: axis selection, followed by axis am- primary developmental axis is organized early in the first cell plification. Events occurring during these stages are consid- cycle and defines the growth axis of the young embryo. Un- ered below, and models describing polarity induction are like higher plants, in which positional cues are often conveyed presented later. by neighboring cells, fucoid zygotes develop autonomously and therefore rely on environmental signals for spatial infor- mation to orient their nascent axes. In the laboratory, an en- tire population can be induced to establish axes in parallel Axis Selection by the application of externa1 vectors such as unidirectional light (Jaffe, 1968). A few hours after polarization, localized Axis selection is the process by which the position of the de- growth occurs at one pole of the nascent axis, as shown in velopmental axis is specified. To select an axis, a zygote Figure 1. must perceive a signal, transduce that signal, and mark the The first zygotic division is an invariant, asymmetric divi- developmental polarity. sion, with the cell plate oriented transverse to the growth Fucoid eggs have no demonstrable cellular asymmetries, axis. The smaller rhizoid cell contains the growing apex and and axis selection must therefore occur during or after fertil- is the precursor to the holdfast of the alga; the larger thallus ization. The egg pronucleus resides in the center of the egg cell gives rise to the stipe and fronds of the mature plant cell, and microtubules nucleate uniformly from the surface of (Figure 1). After the initial division of the zygote, the rhizoid the pronucleus and radiate toward the cortex (Swope and cell elongates and repeatedly divides transverse to the Kropf, 1993). Short rods of F-actin are randomly oriented growth axis, whereas the thallus cell undergoes proliferative and uniformly distributed throughout the cortex (Kropf et al., divisions, each of which is transverse to the previous division. 1992), and organelles are uniformly distributed throughout the cytoplasm (Brawley et al., 1976b). Glycoproteins are dis- tributed in patches over the entire surface of the egg E-mail [email protected]; fax 801-581 -4668. (Stafford et al., 1992). 1012 The Plant Cell A derived organelles persist through much of the first cell cy- B cle and have the potential to serve as positional markers. However, preliminary evidence indicates that the nucleus and perinuclear material, as marked by centrosomal posi- tion, do not align with the developmental axis until after growth begins (S.R. Bisgrove, unpublished results); there- fore, they are unlikely to be involved in ais selection. In- stead, polarity is likely to be perceived and marked in the plasma membrane and cell cortex (see below). Although the mechanisms by which sperm may mark the plasma mem- brane or cortex are unknown, Ca2+ levels increase just be- C D neath the plasma membrane at the sperm entry site (Roberts et al., 1994), and it is possible that, in turn, this local elevation in Ca2+activity triggers regional structural changes (see Trewavas and Malhó, 1997, in this issue). Environmental Cues The putative sperm-induced axis is weak and can be over- ridden by vectorial information in the environment (Jaffe, 1958; Robinson, 1996b). Approximately 3 hr AF, Pelvetia and Fucus zygotes secrete an adhesive symmetrically over the surface of the zygote and attach firmly to the substratum (Vreeland et al., 1993; Vreeland and Epstein, 1996). Once at- Figure 1. Embryogenesis in Pelvetia and Arabidopsis. tached, zygotes begin to sense and respond to an impres- sive number of very different environmental cues. Indeed, (A) to (C) Pelvetia embryogenesis. (A) Unfertilized egg. (B) Two- the developmental axis, and, hence, the position of rhizoid celled embryo displaying localized rhizoid growth and invariant divi- sion. (C) Eight-celled embryo with transverse divisions in descen- outgrowth, can be controlled by the application of unidirec- dants of the rhizoid cell. tional light, gradients of ions or ionophores, gravity (G. Muday, (D) Arabidopsis embryo. The young embryo is morphologically simi- personal communication),flow of seawater, temperature gra- lar to the Pelvetia embryo. dients, and many other factors (Jaffe, 1968). Plane polarized Arrows indicate the first division plane of the zygote. light induces the formation of two rhizoids (Jaffe, 1958), indi- cating that vectorial information does not simply result in ròta- tion of the putative sperm-induced axis. Zygotes are sensitive to each gradient for a restricted period, and the windows of The Role of Sperm Entry: An Open Question sensitivity overlap for many gradients (Bentrup, 1984). The mechanisms by which environmental gradients are The role of sperm entry in inducing polarity in fucoid eggs is perceived and transduced are almost totally unknown in unclear (Roberts et al., 1993). Sperm entry is sufficient for plants (see Trewavas and Malhó, 1997, in this issue). In- polar development; externa1 vectorial information (e.g., light) deed, the diversity of stimuli that can elicit developmental is not required for localized rhizoid outgrowth, oriented cell axis selection in zygotes of the Fucales indicates that multi- division, or subsequent development. These observations ple, converging signal transduction pathways are involved. are consistent with sperm entry inducing an initial axis, and in However, to date, only the photopolarization pathway has a related brown alga, Cystosira, rhizoid growth occurs at the been investigated in detail. Unidirectional ultraviolet or blue sperm entry site in the absence of vectorial cues (Knapp, light induces rhizoid growth from the shaded hemisphere of 1931). However, the spatial relationship between sperm entry the zygote (Hurd, 1920; Robinson, 1996a), and the activa- and rhizoid outgrowth has not been investigated in Pelvetia or tion of cortical photoreceptors (Jaffe, 1958) preferentially Fucus, the organisms in which nearly all of the subsequent stimulates plasma membrane redox chains at the presump- polarity studies have been conducted. tive rhizoid (i.e., shaded) pole (Berger and Brownlee, 1994). If sperm entry induces polarity, then the sperm entry site Photopolarization is inhibited by acidification or alkaliniza- must somehow be marked in the egg cytoplasm. The sperm tion of the cytosol (Kropf et al., 1995) and by disruption of eyespot, mitochondria (Brawley et al., 1976a), and cen- F-actin (Quatrano, 1973), but the roles of redox potential, trosomes (Motomura, 1994) migrate with the sperm pronu- cytosolic ions, and the cytoskeleton in signal transduction cleus and are deposited on the zygotic nucleus at the site of remain a mystery. Likewise, the mechanism by which the pronuclear fusion, as shown in Figure 2A. These sperm- rhizoid pole is marked is unknown. Polarity in Fucoid Zygotes 1013 sperm pronucleus \ F-actin | DHP receptor zygotid an g c eg nuclei A current flow •:vi-.cytosoli gradienn cio t centrosome celB 3 l wall * F2; vitronectin-like protein MtOC '.<- jelly ~ actin mRNA microtubule o secretory vesicle Figure 2. Summary of Structural and Physiological Changes during the First Zygotic Cell Cycle. Centrosome. AF r h e (A inherite)On e sar d paternally organellesd an , , microtubules F-actid an , uniformle nar y distribute zygotie th n di c cytoplasm. Zygotes. AF r h ) Fou 7 (B secreto rt e local jelly electricad ,an l current flows throug celle hth . Inward curren jell positioned e ytan ar shadee th n do d side of the zygote. Centrosomes separate and begin to migrate along the nuclear envelope. F-acti corte(Ce AF dihydropyridinth )d r Seveh n i xan 0 1 no t e receptor plasme th n si a membrane accumulat presumptive th t ea e rhizoid- Se . cretion becomes targeted to this site, depositing the sulfated fucan F2 in the wall and causing local cortical clearing.
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