Hostname: page-component-76fb5796d-25wd4 Total loading time: 0 Render date: 2024-04-26T04:25:32.364Z Has data issue: false hasContentIssue false

Advances in the study of egg activation of higher plants

Published online by Cambridge University Press:  14 December 2018

Li Peng
Affiliation:
School of Life Sciences, Ningxia University, Yinchuan 750021, China Key Laboratory of Ministry of Education for Protection and Utilization of Special Biological Resources in Western China, Yinchuan 750021, China
Zhen Kai Li
Affiliation:
School of Life Sciences, Ningxia University, Yinchuan 750021, China Key Laboratory of Ministry of Education for Protection and Utilization of Special Biological Resources in Western China, Yinchuan 750021, China
Xiao Li Ding
Affiliation:
School of Life Sciences, Ningxia University, Yinchuan 750021, China Key Laboratory of Ministry of Education for Protection and Utilization of Special Biological Resources in Western China, Yinchuan 750021, China
Hui Qiao Tian*
Affiliation:
School of Life Sciences, Xiamen University, Xiamen 361005, China
*
Address for correspondence: Hui Qiao Tian, School of Life Sciences, Xiamen University, Xiamen, Fujian 361102, China. Tel: +11 86 592 2186486. E-mail: hqtian@xmu.edu.cn

Summary

Fertilization in higher plants induces many structural and physiological changes in the fertilized egg, and represents the transition from the haploid female gamete to the diploid zygote, the first cell of a sporophyte. Some changes are induced extremely rapidly following fusion with sperm cells and are the preclusions of egg activation. This review focuses on the early changes that occur in the egg after fusion with sperm cells, but before nuclear fusion. Reported changes include cell shrinkage, cell wall formation, polarity change, oscillation in Ca2+ concentration, and DNA synthesis. In addition, the current understanding of egg activation is summarized and the possible functional relevance of the changes is explored.

Type
Review Article
Copyright
© Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Antoine, AF, Faure, JE, Cordeiro, S, Dumas, C, Rougier, M and Feijó, JA (2000) A Ca2+ influx is triggered and propagates in the zygote as a wavefront during in vitro fertilization of flowering plants. Proc Natl Acad Sci USA 97, 1064310648.Google Scholar
Antoine, AF, Faure, JE, Dumas, C and Feijó, JA (2001) Differential contribution of cytoplasmic Ca2+ and Ca2+ influx to gamete fusion and egg activation in maize. Nat Cell Biol 3, 11201123.Google Scholar
Ashley, T (1972) Zygote shrinkage and subsequent development in some Hibicus hybrids . Planta 108, 303317.Google Scholar
Bartoli, G, Felici, C and Ruffini, CM (2016) Female gametophyte and embryo development in Helleborus bocconei Ten. (Ranunculaceae). Protoplasma 254, 491504.Google Scholar
Bayer, M, Slane, D and Jürgens, G (2017) Early plant embryogenesis-dark ages or dark matter? Curr Opin Plant Biol 35, 3036.Google Scholar
Beale, KM, Leydon, AR and Johnson, AMA (2012) Gamete fusion is required to block multiple pollen tubes from entering an ovule. Curr Biol 22, 10901094.Google Scholar
Berger, F, Hamamura, Y, Ingouff, M and Higashiyama, T (2008) Double fertilization-caught in the act. Trends Plant Sci 13, 437443.Google Scholar
Bhojwani, SS and Bhatnagar, SP (1974) The Embryology of Angiosperms. Vikas Publishing House PVT Ltd, New Delhi Bombay Bangalore Cacutta Kanpur, pp. 161182.Google Scholar
Carmichael, JS and Friedman, WE (1995) Double fertilization in Gnetum gnemon: the relationship between the cell cycle and sexual reproduction. Plant Cell 7, 19751988.Google Scholar
Chaubal, R and Reger, BJ (1990) Relatively high calcium is localized in synergid cells of wheat ovaries. Sex Plant Reprod 3, 98102.Google Scholar
Chaubal, R and Reger, BJ (1992a) Calcium in the synergid cells and other regions of pearl millet ovaries. Sex Plant Reprod 5, 3446.Google Scholar
Chaubal, R and Reger, BJ (1992b) The dynamics of calcium distribution in the synergid cells of wheat after pollination. Sex Plant Reprod 5, 206213.Google Scholar
Chen, SH, Yang, YH, Liao, JP, Kuang, AX and Tian, HQ (2008) Isolation of egg cells and zygotes of Torenia fournieri L. and determination of their surface charge. Zygote 16 179186.Google Scholar
Ciapa, B and Chiri, S (2000) Egg activation: upstream of the fertilization calcium signal. Biol Cell 92, 215233.Google Scholar
Deng, H, Song, YX, Qin, K and Tian, HQ (2012) DNA content and cell cycle changes of male and female gametes of Lycium barbarum L. Plant Physiol J 48, 869873 (In Chinese).Google Scholar
Denninger, P, Bleckmann, A, Lausser, A, Vogler, F, Ott, T, Ehrhardt, DW, Frommer, WB, Sprunck, S, Dresselhaus, T and Grossmann, G (2014) Male-female communication triggers calcium signatures during fertilization in Arabidopsis. Nat Comm 5, 46454657.Google Scholar
Digonnet, C, Aldon, D, Leduc, N, Dumas, C and Rougier, M (1997) First evidence of a calcium transient in flowering plants at fertilization. Development 124, 28672874.Google Scholar
Doblin, MS, Kurek, I, Jacob-Wilk, D and Delmer, DP (2002) Cellulose biosynthesis in plants: from genes to rosettes. Plant Cell Physiol 43, 14071420.Google Scholar
Ducibella, T and Fissore, R (2008) The roles of Ca2+, downstream protein kinases, and oscillatory signaling in regulating fertilization and the activation of development. Dev Biol 315, 257279.Google Scholar
Dumas, C and Rogowsky, F (2008) Fertilization and early seed formation. C R Biol 331, 715725.Google Scholar
Faure, JE and Dumas, C (2001) Fertilization in flowering plants: new approaches for an old story. Plant Physiol 125, 102104.Google Scholar
Faure, JE, Digonnet, C and Dumas, C (1994) An in vitro system for adhesion and fusion of maize gametes. Science 263, 15981600.Google Scholar
Faure, JE, Rotman, N, Fortuné, P and Dumas, C (2002) Fertilization in Arabidopsis thaliana wild type: Developmental stages and time course. Plant J 30, 481488.Google Scholar
Friedman, WE (1991) Double fertilization in Ephedra trifurca, a nonflowering seed plant: the relationship between fertilization events and the cell cycle. Protoplasma 165, 106120.Google Scholar
Friedman, WE (1999) Expression of the cell cycle in sperm of Arabidopsis: implications for understanding patterns of gametogenesis and fertilization in plants and other eukaryotes. Development 126, 10651075.Google Scholar
Fu, Y, Yuan, M, Huang, BQ, Yang, HY, Zee, SY and Brien, TPO (2000) Changes in catin organization in the living egg apparatus of Torena fournieri during fertilization. Sex Plant Reprod 12, 315322.Google Scholar
Ge, LL, Tian, HQ and Russell, SD (2007) Calcium function and distribution during fertilization in angiosperms. Amer J Bot 94, 10461060.Google Scholar
Ge, H, Chang, F and Ma, H (2010) Signaling and transcriptional control of reproductive development in Arabidopsis. Curr Biol 20, 988997.Google Scholar
Hamamura, Y, Nagahara, S and Higashiyama, T (2012) Double fertilization on the move. Curr Opin Plant Biol 15, 7077.Google Scholar
Hamamura, Y, Nishimaki, M, Takeuchi, H, Geitmann, A, Kurihara, D and Higashiyama, T (2014) Live imaging of calcium spikes during double fertilization in Arabidopsis . Nat Comm 5, 47224731.Google Scholar
Han, YZ, Huang, BQ, Guo, FL, Zee, SY and Gu, HK (2002) Sperm extract and inositol 1,4,5-trisphosphate induce cytosolic calcium rise in the central cell of Torenia fournieri . Sex Plant Reprod 15, 187193.Google Scholar
He, CP and Yang, HY (1992) Ultracytochemical localization of calcium in the embryo sac of sunflower. China J Bot 4, 99106.Google Scholar
Hoshino, Y, Scholten, S, von Wiegen, P, Lörz, H and Kranz, E (2004) Fertilization-induced changes in the microtubular architecture of the maize egg cell and zygote—an immunocytochemical approach adapted to single cells. Sex Plant Reprod 17, 8995.Google Scholar
Huang, BQ and Russell, SD (1994) Fertilization in Nicotiana tabacum: cytoskeletal modifications in the embryo sac during synergid degeneration. Planta 194, 200214.Google Scholar
Huang, BQ and Sheridan, WF (1994) Female gametophyte development in maize: Microtubular organization and embryo sac polarity. Plant Cell 6, 845861.Google Scholar
Huang, BQ and Sheridan, FW (1998) Actin coronas in normal and indeterminate gametophyte1 embryo sacs of maize. Sex Plant Reprod 11, 257264.Google Scholar
Huang, BQ, Fu, Y, Zee, SY and Hepler, PK (1999) Three-dimensional organization and dynamic changes of the actin cytoskeleton in embryo sacs of Zea mays and Torenia fournieri . Protoplasma 209, 105119.Google Scholar
Iwano, M, Ngo, QA, Entani, T, Shiba, H, Nagai, T, Miyawaki, A, Isogai, A, Grossniklaus, U and Takayama, S (2012) Cytoplasmic Ca2+ changes dynamically during the interaction of the pollen tube with synergid cells. Development 139, 42024209.Google Scholar
Jensen, WA (1968) Cotton embryogenesis: the zygote. Planta 79, 346366.Google Scholar
Kasahara, RD, Maruyama, D, Hamamura, Y, Sakakibara, T, Twell, D, Higashiyama, T (2012) Fertilization recovery after defective sperm cell release in Arabidopsis . Curr Biol 22, 10841089.Google Scholar
Kranz, E and Lörz, H (1990) Micromanipulation and in vitro fertilization with single pollen grains of maize. Sex Plant Reprod 3, 160169.Google Scholar
Kranz, E and Lörz, H (1993) In vitro fertilization with isolated, single gametes results in zygotic embryogenesis and fertile maize plants. Plant Cell 5, 739746.Google Scholar
Kranz, E, Wiegen, P and Lörz, H (1995) Early cytological events after induction of cell division in egg cells and zygote development following in vitro fertilization with angiosperms gametes. Plant J. 8, 923.Google Scholar
Kumlehn, J, Lorz, H and Kranz, E (1998) Differentiation of isolated wheat zygotes into embryos and normal plants. Planta 205, 327333.Google Scholar
Lau, S, Slane, D, Herud, O, Kong, J and Jürgens, G (2012) Early embryogenesis in flowering plants: setting up the basic body pattern. Annu Rev Plant Biol 63, 483506.Google Scholar
Lord, EM and Russell, SD (2002) The mechanisms of pollination and fertilization in plants. Ann Rev Cell Dev Biol 18, 81105.Google Scholar
Maruyama, D, Hamamura, Y, Takeuchi, H, Susaki, D, Nishimaki, M, Kurihara, D, Kasahara, RD and Higashiyama, T (2013) Independent control by each female gamete prevents the attraction of multiple pollen tubes. Dev Cell 25, 317323.Google Scholar
Miart, F, Desprez, T, Biot, E and Vernhettes, S (2014) Spatio-temporal analysis of cellulose synthesis during cell plate formation in Arabidopsis . Plant J 77, 7184.Google Scholar
Mogensen, HL and Holm, PB (1995) Dynamics of nuclear DNA quantities during zygote development in barley. Plant Cell 7, 487494.Google Scholar
Mogensen, HL, Leduc, N, Natthys-Rochon, E and Dumas, C (1999) Nuclear DNA amounts in the egg and zygote of maize (Zea mays L). Planta 197, 641645.Google Scholar
Nakasaka, H, Yamano, S, Hinokio, K, Nakagawa, K and Yoshizawa, M (2000) Effective activation method with A23187 and puromycin to produce haploid parthenogenones from freshly ovulated mouse oocytes. Zygote 8, 203208.Google Scholar
Ngo, QA, Vogler, H, Lituiev, DS, Nestorova, A and Grossniklaus, U (2014) A calcium dialog mediated by the FERONIA signal transduction pathway controls plant sperm delivery. Dev Cell 29, 491500.Google Scholar
Pónya, Z and Barnabás, B (2001) Microinjected fluorescent phalloidin in vivo reveals F-actin dynamics in isolated egg cells of wheat (Triticum aestivum L.) developed in situ and fertilised in vitro . J Plant Physiol 158, 15271539.Google Scholar
Pónya, Z, Finy, P, Mitykó, J, Dudits, D and Barnabás, B (1999) Optimisation of introducing foreign genes into egg cells and zygotes of wheat (Triticum aestivum L.) via microinjection. Protoplasma 208, 163172.Google Scholar
Raghavan, V (2003) Some reflections on double fertilization, from its discovery to the present. New Phytol 159, 565583.Google Scholar
Roberts, S and Brownlee, C (1995) Calcium influx, fertilisation potential and egg activation in Fucus serratus . Zygote 3, 191197.Google Scholar
Sato, A, Toyooka, K and Okamoto, T (2010) Asymmetric cell division of rice zygotes located in embryo sac and produced by in vitro fertilization. Sex Plant Reprod 23, 211217.Google Scholar
Sauter, M, von Wiegen, P, Lörz, H and Kranz, E (1998) Cell cycle regulatory genes from maize are differentially controlled during fertilization and first embryonic cell division. Sex Plant Reprod 11, 4148.Google Scholar
Scott, R, Armstrong, SJ, Doughty, J and Spielman, M (2008) Double fertilization in Arabidopsis thaliana involves a polyspermy block on the egg but not the central cell. Mol Plant 1, 611619.Google Scholar
Sherwood, RT (1995) Nuclear, DNA amount during sporogenesis and gametogenesis in sexual and aposporous buffelgrass. Sex Plant Reprod 8, 8590.Google Scholar
Shivanna, KR (2016) Fertilization in flowering plants. Resonance 21, 10071018.Google Scholar
Somerville, C (2006) Cellulose synthesis in higher plants. Annu Rev Cell Dev Biol 22, 5378.Google Scholar
Spielman, M and Scott, RJ (2008) Polyspermy barriers in plants: from preventing to promoting fertilization. Sex Plant Reprod 21, 5365.Google Scholar
Sprunck, S (2010) Let’s get physical: gamete interaction in flowering plants. Biochem Soc Trans 38, 635640.Google Scholar
Sprunck, S and Gross-Hardt, R (2011) Nuclear behavior, cell polarity, and cell specification in the female gametophyte. Sex Plant Reprod 24, 123136.Google Scholar
Stricker, SA (1999) Comparative biology of calcium signaling during fertilization and egg activation in in animals. Dev Biol 211, 157176.Google Scholar
Tian, HQ and Russell, SD (1997a) Calcium distribution in fertilized and unfertilized ovules and embryo sacs of Nicotiana tabacum L. Planta 202, 93105.Google Scholar
Tian, HQ and Russell, SD (1997b) Micromanipulation of male and female gametes of Nicotiana tabacum: I. isolation of gametes. Plant Cell Rep 16, 555560.Google Scholar
Tian, HQ, Zhu, H and Russell, SD (2000) Calcium changes in ovules and embryo sacs of Plumbago zeylanica L. Sex Plant Reprod 13, 1120.Google Scholar
Tian, HQ, Yuan, T and Russell, SD (2005) Relationship between double fertilization and the cell cycle in male and female gametes of tobacco. Sex Plant Reprod 17, 243252.Google Scholar
Tirlapur, UK, Van Went, JL and Cresti, M (1993) Visualization of membrane calcium and calmodulin in embryo sacs in situ and isolated from Petunia hybrid L. and Nicotiana tabacum L. Ann Bot 17, 161167.Google Scholar
Tirlapur, UK, Kranz, E and Cresti, M (1995) Characterisation of isolated egg cells, in vitro fusion products and zygotes of Zea mays L. using the technique of image analysis and confocal laser scanning microscopy. Zygote 3, 5764.Google Scholar
Ueda, M and Laux, T (2012) The origin of the plant body axis. Curr Opin Plant Biol 15, 578584.Google Scholar
Van Went, JL (1970) The ultrastructure of the egg and central cell of Petunia. Acta Bot. Neerl. 19, 313322.Google Scholar
Webb, MC and Gunning, BES (1991) The microtubular cytoskeleton during development of the zygote, proembryo and free-nuclear endosperm in Arabidopsis thaliana (L.) Heynh. Planta 184, 187195.Google Scholar
Webb, MC and Gunning, BES (1994) Embryo sac development in Arabidopsis thaliana II. The cytoskeleton during megagametogenesis. Sex Plant Reprod 7, 153163.Google Scholar
Weterings, K and Russell, SD (2004) Experimental analysis of the fertilization process. Plant Cell 16, s107s118.Google Scholar
Yang, SJ, Wei, DM and Tian, HQ (2015) Isolation of sperm cells, egg cells, synergids and central cells from Solanum verbascifolium L. J. Plant Biochem Biotech 24, 400407.Google Scholar
Ye, XL, Yeung, EC and Zee, SY (2002) Sperm movement during double fertilization of a flowering plant, Phaius tankervilliae. Planta 215, 6066.Google Scholar
Zhang, YN, Wei, DM, He, EM, Miao, S, Tian, HQ, Russell, SD (2010) Isolation of male and female gametes of rice. Crop Sci 50, 24572463.Google Scholar
Zhao, P and Sun, MX (2015) The maternal-to-zygotic transition in higher plants: available approaches, critical limitations, and technical requirements. Curr Top Dev Biol 113, 373398.Google Scholar