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Three Cell Fusions During Double Fertilization Le´ veillard, T., and Sahel, J.-A. (2010). Sci. Transl. Mohand-Said, S., Deudon-Combe, A., Hicks, D., Venkatesh, A., Ma, S., Le, Y.Z., Hall, M.N., Ru¨ egg, Med. 2, 26ps16. Simonutti, M., Forster, V., Fintz, A.C., Le´ veillard, M.A., and Punzo, C. (2015). J. Clin. Invest. 125, T., Dreyfus, H., and Sahel, J.A. (1998). Proc. Natl. 1446–1458. Le´ veillard, T., Mohand-Saı¨d, S., Lorentz, O., Hicks, Acad. Sci. USA 95, 8357–8362. D., Fintz, A.-C., Cle´ rin, E., Simonutti, M., Forster, Xiong, W., MacColl Garfinkel, A.E., Li, Y., Beno- V., Cavusoglu, N., Chalmel, F., et al. (2004). Nat. Punzo, C., Kornacker, K., and Cepko, C.L. (2009). witz, L.I., and Cepko, C.L. (2015). J. Clin. Invest. Genet. 36, 755–759. Nat. Neurosci. 12, 44–52. 125, 1433–1445. Three Cell Fusions during Double Fertilization Stefanie Sprunck1 and Thomas Dresselhaus1,* 1Cell Biology and Plant Biochemistry, Biochemie-Zentrum Regensburg, University of Regensburg, 93053 Regensburg, Germany *Correspondence: [email protected] http://dx.doi.org/10.1016/j.cell.2015.04.032 Fertilization of both egg and central cell is a major distinguishing feature of flowering plants. Now, Maruyama et al. report a third cell fusion event between the persistent synergid and the fertilized central cell shortly after double fertilization in Arabidopsis. This causes rapid dilution of pollen tube attractant(s), preventing polytubey. Almost 120 years ago, Sergei Gavrilovich Arabidopsis, usually only one pollen tube phenomenon was named as synergid- Navashin (1898) and Le´ on Guignard arrives at the embryo sac and communi- endosperm fusion (SE fusion; Figure 1). (1899) described independently for the cates with the synergids until the tube tip Using various fluorescent markers to first time that two fertilization events occur bursts simultaneously with the first syner- label the cytosol, mitochondria, and in lily, a major model plant at that time. gid, termed receptive synergid. A block to endoplasmic reticulum, Maruyama et al. The universality of this observation was polytubey (arrival of excess pollen tubes) show by time-lapse imaging the mixing confirmed in numerous flowering plant is established soon after fertilization and of persistent synergid and endosperm species (angiosperms) and is now widely minimizes the risk of polyspermy (fusion cytoplasm about 5 hr after fertilization, considered as a major feature distinguish- of a female gamete with multiple sperms). when the fertilized central cell or primary ing angiosperms from all other organisms. However, plants are capable of attracting endosperm nucleus starts to divide. During the double-fertilization event, one multiple pollen tubes—for example, when They further show fusion of plasma sperm cell fuses with the egg cell, forming gamete fusion fails—to maximize repro- membranes of both cells, which was the embryo, and a second sperm cell fer- ductive success. In Arabidopsis, the sec- never observed in unfertilized ovules. tilizes the central cell, which develops into ond synergid, persistent synergid, was Even more important and significant the endosperm. This sounds simple, but shown to be responsible for polytubey in are the experiments in which they inves- fertilization in angiosperms is a very com- the case of fertilization failure and con- tigate the quick dilution of the pollen plex process: the two genetically identical tinues to attract pollen tubes until it de- tube attractant AtLURE1 (Takeuchi and and immobile sperm cells are transported generates (Beale et al., 2012; Kasahara Higashiyama, 2012). AtLURE1 signals via the pollen tube over long distances et al., 2012). It was further indicated that quickly decrease in the degenerated (e.g., up to 30 cm in maize) through the successful double fertilization induces a receptive synergid after sperm release maternal tissues of the flower in order to block to polytubey and thus avoids the but remain high in the persistent synergid. deliver them to the ovule. Many hurdles delivery of additional sperm cells to the A rapid decrease of AtLURE1 signals have to be taken before the pollen tube embryo sac. But how is this block to poly- was observed to coincide with the mea- finally arrives at the embryo sac harboring tubey established? Nature has an aston- surements of the dilution of cytoplasmic the two female gametes, egg and central ishingly simple solution for this problem, components. The attractant disappears cell, as well as a number of accessory which is now reported in this issue of almost completely within 36 min after cells, including two synergids (Figure 1). Cell by Maruyama et al. (2015): the persis- initiation of SE fusion, a time point when The synergids are known as gland cells tent synergid fuses with the huge fertilized the primary endosperm nucleus divides. playing a leading role in pollen tube central cell (about 20 times larger volume, The induction of SE fusion and thus rapid attraction and sperm release (for review, which even quickly increases after fertil- dilution of AtLURE1 into the early devel- see Dresselhaus and Franklin-Tong, ization), and thereby pollen tube attrac- oping endosperm is sensed by fertilization 2013). In species like the model plant tants are rapidly diluted. This peculiar success of the central cell, but not by 708 Cell 161, May 7, 2015 ª2015 Elsevier Inc. Figure 1. Three Cell Fusion Events Occur during Double Fertilization in Arabidopsis thaliana (Left) The pollen tube is attracted and guided to grow into the ovule by small cysteine-rich proteins (LUREs), which are secreted by two synergids. These are part of the embryo sac, comprising additionally the two female gametes, egg and central cell, and three antipodal cells. (Middle) After pollen tube burst, two immotile sperm cells are released into the receptive synergid that degenerates. Thereafter, one sperm cell fuses with the egg cell (1) and the second sperm with the central cell (2). (Right) Maruyama et al. now show that a third cell fusion takes place after successful fertilization between the persistent synergid and the endosperm, the large fertilized central cell (3). The cytoplasm of both cells are mixed, and thus the pollen tube attractants quickly diluted. Additionally, disintegration of the persistent synergid nucleus is induced, thereby establishing a block to the attraction of excess pollen tubes. the egg cell. However, the fertilized Capsella bursa-pastoris (Schulz and Jen- thereby quickly reducing the amount egg cell contributes independently to a sen, 1968), indicating that this mechanism of secreted signaling molecules and the block of polytubey as it induces rapid exists in all Brassicaceae species. But is terminating function(s) of the absorbed disintegration of the persistent synergid this finding also relevant for other plant cell. It will now be interesting to find nucleus via an unknown ethylene families, such as the economically impor- this connection in other cell fusions. response pathway and thereby addition- tant Gramineae (grasses)? In grasses, In conclusion, this study has demon- ally attenuates AtLURE1 production. multiple pollen tubes arrive almost simul- strated once again how simple and unex- In conclusion, Maruyama et al. use taneously in the vicinity of the embryo pected nature sometimes solves biolog- cutting-edge microscopic imaging of sac (Lausser et al., 2010); therefore, a ical problems. the double-fertilization process to show polytubey block has to be established the establishment of a block to polytubey within seconds or minutes to repel excess REFERENCES by two independent mechanisms (SE pollen tubes. This quick reaction cannot fusion and induced synergid nucleus be achieved by SE fusion or by synergid Beale, K.M., Leydon, A.R., and Johnson, M.A. disintegration), thereby eliminating the disintegration. Moreover, in plant species (2012). Curr. Biol. 22, 1090–1094. persistent synergid and its function(s) with more than two synergids, such Dresselhaus, T., and Franklin-Tong, N. (2013). Mol. 6 in the model plant Arabidopsis. as the extant most basal angiosperm Plant , 1018–1036. The timing of this block (5 hr after Amborella trichopoda (Friedman and Friedman, W.E., and Ryerson, K.C. (2009). Am. J. 96 fertilization and 10 hr after pollination) Ryerson, 2009), it remains to be inves- Bot. , 129–143. appears late but is sufficient in tigated whether persistent synergids Guignard, M.L. (1899). Rev. Gen. Bot. 11, 129–135. Arabidopsis, as the arrival of secondary are all eliminated by the same mecha- Kasahara, R.D., Maruyama, D., Hamamura, Y., pollen tubes was reported to occur nism. Nevertheless, SE fusion may also Sakakibara, T., Twell, D., and Higashiyama, T. (2012). Curr. Biol. 22, 1084–1089. 16 hr after pollination (Kasahara et al., exist in plant species lacking a block to 2012). However, this observation indi- polytubey to remove excess synergid Lausser, A., Kliwer, I., Srilunchang, K.O., and Dres- selhaus, T. (2010). J. Exp. Bot. 61, 673–682. cates that additional mechanisms exist, cells—for example, to provide more Maruyama, D., Vo¨ lz, R., Takeuchi, H., Mori, T., such as the direct or induced release of space in the embryo sac for the devel- Igawa, T., Kurihara, D., Kawashima, T., Ueda, M., repellents by the first leading pollen oping embryo. The elimination of cells Itoh, M., Umeda, M., et al. (2015). Cell 161, this tube, that require degradation or removal is not novel, as it is a prerequisite in issue, 907–918. until secondary pollen tubes are at- many tissues and organs during animal Navashin, S.G. (1898). Bul. Acad. Imp. Sci. tracted. Moreover, it will now be impor- and plant development as well as St Petersburg 9, 377–382. tant to determine the extent to which during reproduction. However, the excite- Schulz, S.R., and Jensen, W.A. (1968). Am. J. Bot. generalizations can be made. Absorption ment about the present study is the 55, 541–552. of the synergids by the developing endo- observation that a highly active signaling Takeuchi, H., and Higashiyama, T.
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