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Advances in the study of zygote activation in higher plants

Published online by Cambridge University Press:  15 October 2020

Dong Xiao Li ,
Shi Jun Chen  and
Hui Qiao Tian Open the ORCID record for Hui Qiao Tian [Opens in a new window]
Dong Xiao Li*
Affiliation:
Henan Institute of Science and Technology, Xinxiang453003, China
Shi Jun Chen
Affiliation:
Henan Institute of Science and Technology, Xinxiang453003, China
Hui Qiao Tian
Affiliation:
School of Life Sciences, Xiamen University, Xiamen, 361005, China
*
Author for correspondence: Dong Xiao Li. Henan Institute of Science and Technology, Xinxiang453003, China. E-mail: dongxiao93@hotmail.com
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Summary

In higher plants, fertilization induces many structural and physiological changes in the fertilized egg that reflect the transition from the haploid female gamete to the diploid zygote – the first cell of the sporophyte. After fusion of the egg nucleus with the sperm nucleus, many molecular changes occur in the zygote during the process of zygote activation during embryogenesis. The zygote originates from the egg, from which some pre-stored translation initiation factors transfer into the zygote and function during zygote activation. This indicates that the control of zygote activation is pre-set in the egg. After the egg and sperm nuclei fuse, gene expression is activated in the zygote, and paternal and maternal gene expression patterns are displayed. This highlights the diversity of zygotic genome activation in higher plants. In addition to new gene expression in the zygote, some genes show quantitative changes in expression. The asymmetrical division of the zygote produces an apical cell and a basal cell that have different destinies during plant reconstruction; these destinies are determined in the zygote. This review describes significant advances in research on the mechanisms controlling zygote activation in higher plants.

Keywords

FertilizationHigher plantsZygote activationZygote genomic activation
Type
Review Article
Information
Zygote , Volume 29 , Issue 1 , February 2021 , pp. 12 - 19
Copyright
© The Author(s), 2020. Published by Cambridge University Press

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References

Abiko, M, Furuta, K, Yamauchi, Y, Fujita, C, Taoka, M, Isobe, T and Okamoto, T (2013a). Identification of proteins enriched in rice egg or sperm cells by single-cell proteomics. PLoS One 8, e69578.CrossRefGoogle ScholarPubMed
Abiko, M, Maeda, H, Tamura, K, Hara-Nishimura, I and Okamoto, T (2013b). Gene expression profiles in rice gametes and zygotes: identification of gamete-enriched genes and up- or down-regulated genes in zygotes after fertilization. J Exp Bot 64, 1927–40.CrossRefGoogle ScholarPubMed
Adenot, PG, Mercier, Y, Renard, JP and Thompson, EM (1997). Differential H4 acetylation of paternal and maternal chromatin precedes DNA replication and differential transcriptional activity in pronuclei of 1-cell mouse embryos. Development 124, 4615–25.Google ScholarPubMed
Anderson, SN, Johnson, CS, Chesnut, J, Jones, DS, Khanday, I, Woodhouse, M, Li, C, Conrad, LJ, Russell, SD and Sundaresan, V (2017). The zygotic transition is initiated in unicellular plant zygotes with asymmetric activation of parental genomes. Dev Cell 43, 349–58.CrossRefGoogle ScholarPubMed
Armenta-Medina, A and Gillmor, CS (2019). Genetic, molecular and parent-of-origin regulation of early embryogenesis in flowering plants. Curr Top Dev Biol 131, 497–543.CrossRefGoogle ScholarPubMed
Autran, D, Baroux, C, Raissig, MT, Lenormand, T, Wittig, M, Grob, S, Steimer, A, Barann, M, Klostermeier, UC, Leblanc, O, Vielle-Calzada, J, Rosenstiel, P, Grimanelli, D and Grossniklaus, U (2011). Maternal epigenetic pathways control parental contributions to Arabidopsis early embryogenesis. Cell 145, 707–19.CrossRefGoogle ScholarPubMed
Baroux, C, Blanvillain, R and Gallois, P (2001). Paternally inherited transgenes are down-regulated but retain low activity during early embryogenesis in Arabidopsis. FEBS Lett 509, 11–16.CrossRefGoogle ScholarPubMed
Bartoli, G, Felici, C and Castiglione, MR (2016). Female gametophyte and embryo development in Helleborus bocconei Ten. (Ranunculaceae). Protoplasma 254, 491–504.CrossRefGoogle Scholar
Bayer, M, Nawy, T, Giglione, C, Galli, M, Meinnel, T and Lukowitz, W (2009). Paternal control of embryonic patterning in Arabidopsis thaliana . Science 323, 1485–8.CrossRefGoogle ScholarPubMed
Bhojwani, SS and Bhatnagar, SP (1974). The Embryology of Angiosperms. Vikas Publishing House PVT Ltd: New Delhi Bombay Bangalore Calcutta Kanpur.Google Scholar
Chen, J, Strieder, N, Krohn, NG, Cyprys, P, Sprunck, S, Engelmann, JC, Dresselhaus, T (2017). Zygotic genome activation occurs shortly after fertilization in maize. Plant Cell 29, 2106–25.CrossRefGoogle ScholarPubMed
de Graaf, BHJ and Dewitte, W 2019. Fertilisation and cell cycle in angiosperms. Ann Plant Rev 2, 21–35.Google Scholar
Del Toro-De León, G, García-Aguilar, M and Gillmor, CS (2014). Non-equivalent contributions of maternal and paternal genomes to early plant embryogenesis. Nature 514, 624–7.CrossRefGoogle ScholarPubMed
Del Toro-De León, G, Lepe-Soltero, D and Gillmor, CS (2016). Zygotic genome activation in isogenic and hybrid plant embryos. Curr Opin Plant Biol 29, 148–53.CrossRefGoogle ScholarPubMed
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, 869–73 (in Chinese).Google Scholar
Deveaux, Y, Toffano-Nioche, C, Claisse, G, Thareau, V, Morin, H, Laufs, P, Moreau, H, Kreis, M, Lecharny, A (2008). Genes of the most conserved WOX clade in plants affect root and flower development in Arabidopsis. BMC Evol Biol 8, 291–310.CrossRefGoogle ScholarPubMed
Dosch, R, Wagner, DS, Mintzer, KA, Runke, G, Wiemelt, AP and Mullins, MC (2004). Maternal control of vertebrate development before the midblastula transition: mutants from the zebrafish I. Dev Cell 6, 771–80.CrossRefGoogle ScholarPubMed
Dresselhaus, T, Cordts, S and Lörz, H (1999). A transcript encoding translation initiation factor eIF-5A is stored in unfertilized egg cells of maize. Plant Mol Biol 39, 1063–71.CrossRefGoogle ScholarPubMed
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, 1065–75.Google ScholarPubMed
García-Aguilar, M and Gillmor, CS (2015). Zygotic genome activation and imprinting: parent-of-origin gene regulation in plant embryogenesis. Curr Opin Plant Biol 27, 29–35.CrossRefGoogle ScholarPubMed
Guo, L, Jiang, L, Zhang, Y, Lu, XL, Xie, Q, Weijers, D and Liu, CM (2016). The anaphase-promoting complex initiates zygote division in Arabidopsis through degradation of cyclin B1. Plant J 86, 161–74.CrossRefGoogle ScholarPubMed
Haecker, A, Gross-Hardt, R, Geiges, B, Sarkar, A, Breuninger, H, Herrmann, M and Laux, T (2004). Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana . Development 131, 657–68.CrossRefGoogle ScholarPubMed
Hu, TX, Yu, M and Zhao, J (2011). Comparative transcriptional analysis reveals differential gene expression between asymmetric and symmetric zygotic divisions in tobacco. PLoS One 6, e27120.CrossRefGoogle ScholarPubMed
Jeong, S, Palmer, TM and Lukowitz, W (2011). The RWP-RK factor GROUNDED promotes embryonic polarity by facilitating YODA MAP kinase signaling. Curr Biol 21, 1268–76.CrossRefGoogle ScholarPubMed
Kimata, Y, Kato, T, Higaki, T, Kurihara, D, Yamada, T, Segami, S, Morita, MT, Maeshima, M, Hasezawa, S, Higashiyama, T, Tasaka, M and Ueda, M (2019). Polar vacuolar distribution is essential for accurate asymmetric division of Arabidopsis zygotes. Proc Natl Acad Sci USA 116, 2338–43.CrossRefGoogle ScholarPubMed
Maheshwari, P (1950). An Introduction to the Embryology of Angiosperms. McGraw-Hill Book Co. Inc., New York.CrossRefGoogle Scholar
Memili, E and First, NL (2000). Zygotic and embryonic gene expression in cow: a review of timing and mechanisms of early gene expression as compared with other species. Zygote 8, 87–96.CrossRefGoogle ScholarPubMed
Mogensen, HL and Holm, PB (1995). Dynamics of nuclear DNA quantities during zygote development in barley. Plant Cell 7, 487–94.CrossRefGoogle ScholarPubMed
Mogensen, HL, Leduc, N, Matthys-Rochon, E and Dumas, C (1999). Nuclear DNA amounts in the egg and zygote of maize (Zea mays L). Planta 197, 641–5.Google Scholar
Niedojadło, K, Pięciński, S, Smoliński, DJ and Bednarska-Kozakiewicz, E (2012). Ribosomal RNA of Hyacinthus orientalis L. female gametophyte cells before and after fertilization. Planta 236, 171–84.CrossRefGoogle ScholarPubMed
Nodine, MD and Bartel, DP (2012). Maternal and paternal genomes contribute equally to the transcriptome of early plant embryos. Nature 482, 94–7.CrossRefGoogle ScholarPubMed
Ohnishi, Y and Okamoto, T (2015). Karyogamy in rice zygotes: actin filament-dependent migration of sperm nucleus, chromatin dynamics, and de novo gene expression. Plant Signal Behav 10, e989021.CrossRefGoogle ScholarPubMed
Okamoto, T (2017). Analysis of proteins enriched in rice gamete. Methods Mol Biol, 1669, 251–63.CrossRefGoogle ScholarPubMed
Okamoto, T, Higuchi, K, Shinkawa, T, Isobe, T, Lörz, H, Koshiba, T and Kranz, E (2004). Identification of major proteins in maize egg cells. Plant Cell Physiol 10, 1406–12.CrossRefGoogle Scholar
Okamoto, T, Scholten, S, Lörz, H and Kranz, E (2005). Identification of genes that are up- or down-regulated in the apical or basal cell of maize two-celled embryo and monitoring their expression during zygote development by a cell manipulation- and PCR-based approach. Plant Cell Physiol 46, 332–8.CrossRefGoogle ScholarPubMed
Peng, L, Li, ZK, Ding, XL and Tian, HQ (2018). Advances in the study of egg activation of higher plants. Zygote 26, 435–42.CrossRefGoogle Scholar
Rahman, MH, Toda, E, Kobayashi, M, Kudo, T, Koshimizu, S, Takahara, M, Iwami, M, Watanabe, Y, Sekimoto, H, Yano, K and Okamoto, T (2019). Expression of genes from paternal alleles in rice zygotes and involvement of OsASGR-BBML1 in initiation of zygotic development. Plant Cell Physiol 60, 725–37.CrossRefGoogle ScholarPubMed
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, 41–8.CrossRefGoogle Scholar
Schier, AF (2007). The maternal–zygotic transition: death and birth of RNAs. Science 316, 406–7.CrossRefGoogle ScholarPubMed
Schultz, RM (1993). Regulation of zygotic gene activation in the mouse. Bioessays 15, 531–8.CrossRefGoogle ScholarPubMed
Sukawa, Y and Okamoto, T (2018). Cell cycle in egg cell and its progression during zygotic development in rice. Plant Reprod 31, 107–16.CrossRefGoogle ScholarPubMed
Tadros, W and Lipshitz, HD (2009). The maternal-to-zygotic transition: a play in two acts. Development 136, 3033–42.CrossRefGoogle ScholarPubMed
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, 243–52.CrossRefGoogle Scholar
Toda, E, Ohnishi, Y and Okamoto, T (2018). An imbalanced parental genome ratio affects the development of rice zygotes. J Exp Bot 69, 2609–19.CrossRefGoogle ScholarPubMed
Uchiumi, T, Shinkawa, T, Isobe, T and Okamoto, T (2007). Identification of the major protein components of rice egg cells. J Plant Res 120, 575–9.CrossRefGoogle ScholarPubMed
Ueda, M, Zhang, Z and Laux, T (2011). Transcriptional activation of Arabidopsis axis patterning genes WOX8/9 links zygote polarity to embryo development. Dev Cell 20, 264–70CrossRefGoogle ScholarPubMed
Ueda, M, Aichinger, E, Gong, W, Groot, E, Verstraeten, I, Vu, LD, Smet, ID, Higashiyama, T, Umeda, M and Laux, T (2017). Transcriptional integration of paternal and maternal factors in the Arabidopsis zygote. Gene Dev 31, 617–22.CrossRefGoogle ScholarPubMed
Vielle-Calzada, JP, Baskar, R and Grossniklaus, U (2000). Delayed activation of the paternal genome during seed development. Nature 404, 91–4.CrossRefGoogle ScholarPubMed
Yu, D, Jiang, L, Gong, H and Liu, CM (2012). EMBRYONIC FACTOR 19 encodes a pentatricopeptide repeat protein that is essential for the initiation of zygotic embryogenesis in Arabidopsis . J Integr Plant Biol 54, 55–64.CrossRefGoogle Scholar
Yu, TY, Shi, DQ, Jia, PF, Tang, J, Li, HJ, Liu, J and Yang, WC (2016). The Arabidopsis receptor kinase ZAR1 is required for zygote asymmetric division and its daughter cell fate. PLoS Genet 12, e1005933 CrossRefGoogle ScholarPubMed
Zhao, Y, Hu, Y, Dai, M, Huang, L and Zhou, D (2009). The WUSCHEL-related homeobox gene WOX11 is required to activate shoot-borne crown root development in rice. Plant Cell 21, 736–48.CrossRefGoogle ScholarPubMed