1932

Abstract

Following fertilization in flowering plants (angiosperms), egg and sperm cells unite to form the zygote, which generates an entire new organism through a process called embryogenesis. In this review, we provide a comparative perspective on early zygotic embryogenesis in flowering plants by using the Poaceae maize and rice as monocot grass and crop models as well as as a eudicot model of the Brassicaceae family. Beginning with the activation of the egg cell, we summarize and discuss the process of maternal-to-zygotic transition in plants, also taking recent work on parthenogenesis and haploid induction into consideration. Aspects like imprinting, which is mainly associated with endosperm development and somatic embryogenesis, are not considered. Controversial findings about the timing of zygotic genome activation as well as maternal versus paternal contribution to zygote and early embryo development are highlighted. The establishment of zygotic polarity, asymmetric division, and apical and basal cell lineages represents another chapter in which we also examine and compare the role of major signaling pathways, cell fate genes, and hormones in early embryogenesis. Except for the model , little is known about embryopatterning and the establishment of the basic body plan in angiosperms. Using available in situ hybridization, RNA-sequencing, and marker data, we try to compare how and when stem cell niches are established. Finally, evolutionary aspects of plant embryo development are discussed.

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2021-06-17
2024-04-25
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Literature Cited

  1. 1. 
    Aida M, Tsubakimoto Y, Shimizu S, Ogisu H, Kamiya M et al. 2020. Establishment of the embryonic shoot meristem involves activation of two classes of genes with opposing functions for meristem activities. Int. J. Mol. Sci. 21:5864
    [Google Scholar]
  2. 2. 
    Albertini E, Barcaccia G, Carman JG, Pupilli F. 2019. Did apomixis evolve from sex or was it the other way around?. J. Exp. Bot. 70:2951–64
    [Google Scholar]
  3. 3. 
    Amien S, Kliwer I, Márton ML, Debener T, Geiger D et al. 2010. Defensin-like ZmES4 mediates pollen tube burst in maize via opening of the potassium channel KZM1. PLOS Biol 8:e1000388
    [Google Scholar]
  4. 4. 
    Anderson SN, Johnson CS, Chesnut J, Jones DS, Khanday I et al. 2017. The zygotic transition is initiated in unicellular plant zygotes with asymmetric activation of parental genomes. Dev. Cell 43:349–58.e4
    [Google Scholar]
  5. 5. 
    Antoine AF, Faure JE, Cordeiro S, Dumas C, Rougier M, Feijó JA 2000. A calcium influx is triggered and propagates in the zygote as a wavefront during in vitro fertilization of flowering plants. PNAS 97:10643–48
    [Google Scholar]
  6. 6. 
    Armenta-Medina A, Gillmor CS. 2019. Genetic, molecular and parent-of-origin regulation of early embryogenesis in flowering plants. Curr. Top. Dev. Biol. 131:497–543
    [Google Scholar]
  7. 7. 
    Armenta-Medina A, Lepe-Soltero D, Xiang D, Datla R, Abreu-Goodger C, Gillmor CS. 2017. Arabidopsis thaliana miRNAs promote embryo pattern formation beginning in the zygote. Dev. Biol. 431:145–51
    [Google Scholar]
  8. 8. 
    Autran D, Baroux C, Raissig MT, Lenormand T, Wittig M et al. 2011. Maternal epigenetic pathways control parental contributions to Arabidopsis early embryogenesis. Cell 145:707–19
    [Google Scholar]
  9. 9. 
    Baroux C, Grossniklaus U. 2015. The maternal-to-zygotic transition in flowering plants: evidence, mechanisms, and plasticity. Curr. Top. Dev. Biol. 113:351–71
    [Google Scholar]
  10. 10. 
    Bauer N, Škiljaica A, Malenica N, Razdorov G, Klasić M et al. 2019. The MATH-BTB protein TaMAB2 accumulates in ubiquitin-containing foci and interacts with the translation initiation machinery in Arabidopsis. Front. Plant Sci. 10:1469
    [Google Scholar]
  11. 11. 
    Bayer M, Nawy T, Giglione C, Galli M, Meinnel T, Lukowitz W. 2009. Paternal control of embryonic patterning in Arabidopsis thaliana. Science 323:1485–88
    [Google Scholar]
  12. 12. 
    Bayer M, Slane D, Jürgens G. 2017. Early plant embryogenesis—dark ages or dark matter?. Curr. Opin. Plant Biol. 35:30–36
    [Google Scholar]
  13. 13. 
    Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T et al. 2002. Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–49
    [Google Scholar]
  14. 14. 
    Breuninger H, Rikirsch E, Hermann M, Ueda M, Laux T. 2008. Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Dev. Cell 14:867–76
    [Google Scholar]
  15. 15. 
    Budhiraja R, Hermkes R, Müller S, Schmidt J, Colby T et al. 2009. Substrates related to chromatin and to RNA-dependent processes are modified by Arabidopsis SUMO isoforms that differ in a conserved residue with influence on desumoylation. Plant Physiol 149:1529–40
    [Google Scholar]
  16. 16. 
    Busch M, Mayer U, Jürgens G. 1996. Molecular analysis of the Arabidopsis pattern formation of gene GNOM: gene structure and intragenic complementation. Mol. Gen. Genet. 250:681–91
    [Google Scholar]
  17. 17. 
    Carman JG. 1997. Asynchronous expression of duplicate genes in angiosperms may cause apomixis, bispory, tetraspory, and polyembryony. Biol. J. Linnean Soc. 61:51–94
    [Google Scholar]
  18. 18. 
    Chen J, Kalinowska K, Müller B, Mergner J, Deutzmann R et al. 2018. DiSUMO-LIKE interacts with RNA-binding proteins and affects cell-cycle progression during maize embryogenesis. Curr. Biol. 28:1548–60.e5
    [Google Scholar]
  19. 19. 
    Chen J, Lausser A, Dresselhaus T. 2014. Hormonal responses during early embryogenesis in maize. Biochem. Soc. Trans. 42:325–31
    [Google Scholar]
  20. 20. 
    Chen J, Strieder N, Krohn NG, Cyprys P, Sprunck S et al. 2017. Zygotic genome activation occurs shortly after fertilization in maize. Plant Cell 29:2106–25Shows that ZGA occurs immediately after fertilization in a highly dynamic pattern.
    [Google Scholar]
  21. 21. 
    Conner JA, Mookkan M, Huo H, Chae K, Ozias-Akins P 2015. A parthenogenesis gene of apomict origin elicits embryo formation from unfertilized eggs in a sexual plant. PNAS 112:11205–10
    [Google Scholar]
  22. 22. 
    Conner JA, Podio M, Ozias-Akins P. 2017. Haploid embryo production in rice and maize induced by PsASGR-BBML transgenes. Plant Reprod 30:41–52
    [Google Scholar]
  23. 23. 
    Costa LM, Marshall E, Tesfaye M, Silverstein KA, Mori M et al. 2014. Central cell-derived peptides regulate early embryo patterning in flowering plants. Science 344:168–72
    [Google Scholar]
  24. 24. 
    Crawford BC, Sewell J, Golembeski G, Roshan C, Long JA, Yanofsky MF. 2015. Genetic control of distal stem cell fate within root and embryonic meristems. Science 347:655–59
    [Google Scholar]
  25. 25. 
    Cyprys P, Lindemeier M, Sprunck S. 2019. Gamete fusion is facilitated by two sperm cell-expressed DUF679 membrane proteins. Nat. Plants 5:253–57
    [Google Scholar]
  26. 26. 
    Czapik R, Izmaiłow R 2001. Zygotic embryogenesis: structural aspects. Current Trends in the Embryology of Angiosperms SS Bhojwani, WY Soh 197–222 Dordrecht, Neth.: Springer
    [Google Scholar]
  27. 27. 
    De Rybel B, Adibi M, Breda AS, Wendrich JR, Smit ME et al. 2014. Integration of growth and patterning during vascular tissue formation in Arabidopsis. Science 345:1255215
    [Google Scholar]
  28. 28. 
    De Rybel B, Mähönen AP, Helariutta Y, Weijers D. 2016. Plant vascular development: from early specification to differentiation. Nat. Rev. Mol. Cell Biol. 17:30–40
    [Google Scholar]
  29. 29. 
    De Rybel B, Möller B, Yoshida S, Grabowicz I, Barbier de Reuille P et al. 2013. A bHLH complex controls embryonic vascular tissue establishment and indeterminate growth in Arabidopsis. Dev. Cell 24:426–37
    [Google Scholar]
  30. 30. 
    de Vries SC, Weijers D. 2017. Plant embryogenesis. Curr. Biol. 27:R870–73
    [Google Scholar]
  31. 31. 
    Del Toro-De León G, García-Aguilar M, Gillmor CS. 2014. Non-equivalent contributions of maternal and paternal genomes to early plant embryogenesis. Nature 514:624–27
    [Google Scholar]
  32. 32. 
    Denninger P, Bleckmann A, Lausser A, Vogler F, Ott T et al. 2014. Male–female communication triggers calcium signatures during fertilization in Arabidopsis. Nat. Commun. 5:4645
    [Google Scholar]
  33. 33. 
    Ding Z, Friml J 2010. Auxin regulates distal stem cell differentiation in Arabidopsis roots. PNAS 107:12046–51
    [Google Scholar]
  34. 34. 
    Ding Z, Wang B, Moreno I, Dupláková N, Simon S et al. 2012. ER-localized auxin transporter PIN8 regulates auxin homeostasis and male gametophyte development in Arabidopsis. Nat. Commun. 3:941
    [Google Scholar]
  35. 35. 
    Doll NM, Royek S, Fujita S, Okuda S, Chamot S et al. 2020. A two-way molecular dialogue between embryo and endosperm is required for seed development. Science 367:431–35
    [Google Scholar]
  36. 36. 
    Dresselhaus T, Johnson MA. 2018. Reproduction: plant parentage à trois. Curr. Biol. 28:R28–30
    [Google Scholar]
  37. 37. 
    Dresselhaus T, Sprunck S, Wessel GM. 2016. Fertilization mechanisms in flowering plants. Curr. Biol. 26:R125–39
    [Google Scholar]
  38. 38. 
    Faure JE, Mogensen HL, Dumas C, Lörz H, Kranz E. 1993. Karyogamy after electrofusion of single egg and sperm cell protoplasts from maize: cytological evidence and time course. Plant Cell 5:747–55
    [Google Scholar]
  39. 39. 
    Faure JE, Rotman N, Fortuné P, Dumas C. 2002. Fertilization in Arabidopsis thaliana wild type: developmental stages and time course. Plant J 30:481–88
    [Google Scholar]
  40. 40. 
    Forzani C, Aichinger E, Sornay E, Willemsen V, Laux T et al. 2014. WOX5 suppresses CYCLIN D activity to establish quiescence at the center of the root stem cell niche. Curr. Biol. 24:1939–44
    [Google Scholar]
  41. 41. 
    Friedman WE, Bachelier JB, Hormaza JI. 2012. Embryology in Trithuria submersa (Hydatellaceae) and relationships between embryo, endosperm, and perisperm in early-diverging flowering plants. Am. J. Bot. 99:1083–95
    [Google Scholar]
  42. 42. 
    Friml J, Vieten A, Sauer M, Weijers D, Schwarz H et al. 2003. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426:147–53
    [Google Scholar]
  43. 43. 
    Gilles LM, Khaled A, Laffaire J-B, Chaignon S, Gendrot G et al. 2017. Loss of pollen-specific phospholipase NOT LIKE DAD triggers gynogenesis in maize. EMBO J 36:707–17
    [Google Scholar]
  44. 44. 
    Gooh K, Ueda M, Aruga K, Park J, Arata H et al. 2015. Live-cell imaging and optical manipulation of Arabidopsis early embryogenesis. Dev. Cell 34:242–51
    [Google Scholar]
  45. 45. 
    Grossniklaus U. 2017. Polyspermy produces tri-parental seeds in maize. Curr. Biol. 27:R1300–2
    [Google Scholar]
  46. 46. 
    Haecker A, Gross-Hardt R, Geiges B, Sarkar A, Breuninger H et al. 2004. Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131:657–68
    [Google Scholar]
  47. 47. 
    Hamamura Y, Nishimaki M, Takeuchi H, Geitmann A, Kurihara D, Higashiyama T. 2014. Live imaging of calcium spikes during double fertilization in Arabidopsis. Nat. Commun. 5:4722
    [Google Scholar]
  48. 48. 
    Hamann T, Benkova E, Bäurle I, Kientz M, Jürgens G. 2002. The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev 16:1610–15
    [Google Scholar]
  49. 49. 
    Hamann T, Mayer U, Jürgens G. 1999. The auxin-insensitive bodenlos mutation affects primary root formation and apical-basal patterning in the Arabidopsis embryo. Development 126:1387–95
    [Google Scholar]
  50. 50. 
    Heimpel GE, de Boer JG. 2008. Sex determination in the Hymenoptera. Annu. Rev. Entomol. 53:209–30
    [Google Scholar]
  51. 51. 
    Horstman A, Bemer M, Boutilier K. 2017. A transcriptional view on somatic embryogenesis. Regeneration 4:201–16
    [Google Scholar]
  52. 52. 
    Iida H, Yoshida A, Takada S. 2019. ATML1 activity is restricted to the outermost cells of the embryo through post-transcriptional repressions. Development 146:dev.169300
    [Google Scholar]
  53. 53. 
    Ingouff M, Sakata T, Li J, Sprunck S, Dresselhaus T, Berger F. 2009. The two male gametes share equal ability to fertilize the egg cell in Arabidopsis thaliana. Curr. Biol. 19:R19–20
    [Google Scholar]
  54. 54. 
    Ishimoto K, Sohonahra S, Kishi-Kaboshi M, Itoh JI, Hibara KI et al. 2019. Specification of basal region identity after asymmetric zygotic division requires mitogen-activated protein kinase 6 in rice. Development 146:dev176305Shows that the MPK3/6 pathway for the establishment and maintenance of the BCL is dispensable for asymmetric zygote division in rice.
    [Google Scholar]
  55. 55. 
    Jacquier NMA, Gilles LM, Pyott DE, Martinant JP, Rogowsky PM, Widiez T. 2020. Puzzling out plant reproduction by haploid induction for innovations in plant breeding. Nat. Plants 6:610–19
    [Google Scholar]
  56. 56. 
    Johri BM, Ambegaokar KB, Srivastava PS. 1992. Comparative Embryology of Angiosperms Berlin/Heidelberg: Springer
  57. 57. 
    Juranič M, Srilunchang KO, Krohn NG, Leljak-Levanic D, Sprunck S, Dresselhaus T. 2012. Germline-specific MATH-BTB substrate adaptor MAB1 regulates spindle length and nuclei identity in maize. Plant Cell 24:4974–91
    [Google Scholar]
  58. 58. 
    Kalinowska K, Chamas S, Unkel K, Demidov D, Lermontova I et al. 2019. State-of-the-art and novel developments of in vivo haploid technologies. Theor. Appl. Genet. 132:593–605
    [Google Scholar]
  59. 59. 
    Kamiya N, Nagasaki H, Morikami A, Sato Y, Matsuoka M. 2003. Isolation and characterization of a rice WUSCHEL-type homeobox gene that is specifically expressed in the central cells of a quiescent center in the root apical meristem. Plant J 35:429–41
    [Google Scholar]
  60. 60. 
    Kao P, Nodine MD. 2019. Transcriptional activation of Arabidopsis zygotes is required for initial cell divisions. Sci. Rep. 9:17159
    [Google Scholar]
  61. 61. 
    Karnahl M, Park M, Krause C, Hiller U, Mayer U et al. 2018. Functional diversification of Arabidopsis SEC1-related SM proteins in cytokinetic and secretory membrane fusion. PNAS 115:6309–14
    [Google Scholar]
  62. 62. 
    Kashir J, Deguchi R, Jones C, Coward K, Stricker SA. 2013. Comparative biology of sperm factors and fertilization-induced calcium signals across the animal kingdom. Mol. Reprod. Dev. 80:787–815
    [Google Scholar]
  63. 63. 
    Kato T, Morita MT, Fukaki H, Yamauchi Y, Uehara M et al. 2002. SGR2, a phospholipase-like protein, and ZIG/SGR4, a SNARE, are involved in the shoot gravitropism of Arabidopsis. Plant Cell 14:33–46
    [Google Scholar]
  64. 64. 
    Kawashima T, Maruyama D, Shagirov M, Li J, Hamamura Y et al. 2014. Dynamic F-actin movement is essential for fertilization in Arabidopsis thaliana. eLife 3:e04501
    [Google Scholar]
  65. 65. 
    Kelliher T, Starr D, Richbourg L, Chintamanani S, Delzer B et al. 2017. MATRILINEAL, a sperm-specific phospholipase, triggers maize haploid induction. Nature 542:105–9
    [Google Scholar]
  66. 66. 
    Khanday I, Skinner D, Yang B, Mercier R, Sundaresan V. 2019. A male-expressed rice embryogenic trigger redirected for asexual propagation through seeds. Nature 565:91–95Demonstrates that the egg cell expression of BBM1, initially specific to the male allele, leads to parthenogenesis.
    [Google Scholar]
  67. 67. 
    Kimata Y, Higaki T, Kawashima T, Kurihara D, Sato Y et al. 2016. Cytoskeleton dynamics control the first asymmetric cell division in Arabidopsis zygote. PNAS 113:14157–62
    [Google Scholar]
  68. 68. 
    Kimata Y, Kato T, Higaki T, Kurihara D, Yamada T et al. 2019. Polar vacuolar distribution is essential for accurate asymmetric division of Arabidopsis zygotes. PNAS 116:2338–43Uses live-cell imaging to visualize the dynamics and regulating role of vacuoles for zygote polarity establishment.
    [Google Scholar]
  69. 69. 
    Kimata Y, Ueda M. 2020. Intracellular dynamics and transcriptional regulations in plant zygotes: a case study of Arabidopsis. Plant Reprod 33:89–96
    [Google Scholar]
  70. 70. 
    Koi S, Hisanaga T, Sato K, Shimamura M, Yamato KT et al. 2016. An evolutionarily conserved plant RKD factor controls germ cell differentiation. Curr. Biol. 26:1775–81
    [Google Scholar]
  71. 71. 
    Koizumi K, Wu S, MacRae-Crerar A, Gallagher KL. 2011. An essential protein that interacts with endosomes and promotes movement of the SHORT-ROOT transcription factor. Curr. Biol. 21:1559–64
    [Google Scholar]
  72. 72. 
    Kong J, Lau S, Jürgens G. 2015. Twin plants from supernumerary egg cells in Arabidopsis. Curr. Biol. 25:225–30
    [Google Scholar]
  73. 73. 
    Koszegi D, Johnston AJ, Rutten T, Czihal A, Altschmied L et al. 2011. Members of the RKD transcription factor family induce an egg cell-like gene expression program. Plant J 67:280–91
    [Google Scholar]
  74. 74. 
    Kranz E, Lörz H. 1994. In vitro fertilisation of maize by single egg and sperm cell protoplast fusion mediated by high calcium and high pH. Zygote 2:125–28
    [Google Scholar]
  75. 75. 
    Kranz E, von Wiegen P, Lörz H. 1995. Early cytological events after induction of cell division in egg cells and zygote development following in vitro fertilization with angiosperm gametes. Plant J 8:9–23
    [Google Scholar]
  76. 76. 
    Łabno A, Tomecki R, Dziembowski A. 2016. Cytoplasmic RNA decay pathways—enzymes and mechanisms. Biochim. Biophys. Acta Mol. Cell Res. 1863:3125–47
    [Google Scholar]
  77. 77. 
    Lampert KP. 2008. Facultative parthenogenesis in vertebrates: reproductive error or chance?. Sex Dev 2:290–301
    [Google Scholar]
  78. 78. 
    Lau S, Slane D, Herud O, Kong J, Jürgens G. 2012. Early embryogenesis in flowering plants: setting up the basic body pattern. Annu. Rev. Plant Biol. 63:483–506
    [Google Scholar]
  79. 79. 
    Lee MT, Bonneau AR, Giraldez AJ. 2014. Zygotic genome activation during the maternal-to-zygotic transition. Annu. Rev. Cell Dev. Biol. 30:581–613
    [Google Scholar]
  80. 80. 
    León-Martínez G, Vielle-Calzada JP. 2019. Apomixis in flowering plants: developmental and evolutionary considerations. Curr. Top. Dev. Biol. 131:565–604
    [Google Scholar]
  81. 81. 
    Li C, Xu H, Fu FF, Russell SD, Sundaresan V, Gent JI. 2020. Genome-wide redistribution of 24-nt siRNAs in rice gametes. Genome Res 30:173–84
    [Google Scholar]
  82. 82. 
    Liu C, Li X, Meng D, Zhong Y, Chen C et al. 2017. A 4-bp insertion at ZmPLA1 encoding a putative phospholipase A generates haploid induction in maize. Mol. Plant 10:520–22
    [Google Scholar]
  83. 83. 
    Liu Y, Li X, Zhao J, Tang X, Tian S et al. 2015. Direct evidence that suspensor cells have embryogenic potential that is suppressed by the embryo proper during normal embryogenesis. PNAS 112:12432–37Demonstrates that, following laser ablation of the AC, the top cell of the BCL divides like an AC.
    [Google Scholar]
  84. 84. 
    Lu KJ, De Rybel B, van Mourik H, Weijers D. 2018. Regulation of intercellular TARGET OF MONOPTEROS 7 protein transport in the Arabidopsis root. Development 145:dev152892
    [Google Scholar]
  85. 85. 
    Lu K-J, van 't Wout Hofland N, Mor E, Mutte S, Abrahams P et al. 2020. Evolution of vascular plants through redeployment of ancient developmental regulators. PNAS 117:733–40
    [Google Scholar]
  86. 86. 
    Márton ML, Cordts S, Broadhvest J, Dresselhaus T. 2005. Micropylar pollen tube guidance by egg apparatus 1 of maize. Science 307:573–76
    [Google Scholar]
  87. 87. 
    Mayer KFX, Schoof H, Haecker A, Lenhard M, Jürgens G, Laux T. 1998. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–15
    [Google Scholar]
  88. 88. 
    Meyer S, Scholten S. 2007. Equivalent parental contribution to early plant zygotic development. Curr. Biol. 17:1686–91
    [Google Scholar]
  89. 89. 
    Moffitt JR, Hao J, Wang G, Chen KH, Babcock HP, Zhuang X. 2016. High-throughput single-cell gene-expression profiling with multiplexed error-robust fluorescence in situ hybridization. PNAS 113:11046–51
    [Google Scholar]
  90. 90. 
    Mol R, Matthys-Rochon E, Dumas C. 1994. The kinetics of cytological events during double fertilization in Zea mays L. Plant J 5:197–206
    [Google Scholar]
  91. 91. 
    Möller BK, ten Hove CA, Xiang D, Williams N, López LG et al. 2017. Auxin response cell-autonomously controls ground tissue initiation in the early Arabidopsis embryo. PNAS 114:E2533–39
    [Google Scholar]
  92. 92. 
    Nakel T, Tekleyohans DG, Mao Y, Fuchert G, Vo D, Groß-Hardt R. 2017. Triparental plants provide direct evidence for polyspermy induced polyploidy. Nat. Commun. 8:1033
    [Google Scholar]
  93. 93. 
    Nalabothula N, McVicker G, Maiorano J, Martin R, Pritchard JK, Fondufe-Mittendorf YN. 2014. The chromatin architectural proteins HMGD1 and H1 bind reciprocally and have opposite effects on chromatin structure and gene regulation. BMC Genom 15:92
    [Google Scholar]
  94. 94. 
    Nardmann J, Zimmermann R, Durantini D, Kranz E, Werr W. 2007. WOX gene phylogeny in Poaceae: a comparative approach addressing leaf and embryo development. Mol. Biol. Evol. 24:2474–84
    [Google Scholar]
  95. 95. 
    Natesh S, Rau MA 1984. The embryo. Embryology of Angiosperms BM Johri 377–444 Berlin/Heidelberg: Springer
    [Google Scholar]
  96. 96. 
    Neu A, Eilbert E, Asseck LY, Slane D, Henschen A et al. 2019. Constitutive signaling activity of a receptor-associated protein links fertilization with embryonic patterning in Arabidopsis thaliana. PNAS 116:5795–804An analysis of protein features determining the constitutive activity of the paternal YODA regulator SSP in promoting basal fate.
    [Google Scholar]
  97. 97. 
    Nodine MD, Bartel DP. 2012. Maternal and paternal genomes contribute equally to the transcriptome of early plant embryos. Nature 482:94–97
    [Google Scholar]
  98. 98. 
    Ogawa E, Yamada Y, Sezaki N, Kosaka S, Kondo H et al. 2015. ATML1 and PDF2 play a redundant and essential role in Arabidopsis embryo development. Plant Cell Physiol 56:1183–92
    [Google Scholar]
  99. 99. 
    Ohashi-Ito K, Saegusa M, Iwamoto K, Oda Y, Katayama H et al. 2014. A bHLH complex activates vascular cell division via cytokinin action in root apical meristem. Curr. Biol. 24:2053–58
    [Google Scholar]
  100. 100. 
    Ohnishi Y, Kokubu I, Kinoshita T, Okamoto T. 2019. Sperm entry into the egg cell induces the progression of karyogamy in rice zygotes. Plant Cell Physiol 60:1656–65
    [Google Scholar]
  101. 101. 
    Ohnishi Y, 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
    [Google Scholar]
  102. 102. 
    Ohnishi Y, Okamoto T. 2017. Nuclear migration during karyogamy in rice zygotes is mediated by continuous convergence of actin meshwork toward the egg nucleus. J. Plant Res. 130:339–48
    [Google Scholar]
  103. 103. 
    Olmedo-Monfil V, Durán-Figueroa N, Arteaga-Vázquez M, Demesa-Arévalo E, Autran D et al. 2010. Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464:628–32
    [Google Scholar]
  104. 104. 
    Palovaara J, de Zeeuw T, Weijers D. 2016. Tissue and organ initiation in the plant embryo: a first time for everything. Annu. Rev. Cell Dev. Biol. 32:47–75
    [Google Scholar]
  105. 105. 
    Peng L, Li ZK, Ding XL, Tian HQ. 2018. Advances in the study of egg activation of higher plants. Zygote 26:435–42
    [Google Scholar]
  106. 106. 
    Pi L, Aichinger E, van der Graaff E, Llavata-Peris CI, Weijers D et al. 2015. Organizer-derived WOX5 signal maintains root columella stem cells through chromatin-mediated repression of CDF4 expression. Dev. Cell 33:576–88
    [Google Scholar]
  107. 107. 
    Prigge MJ, Platre M, Kadakia N, Zhang Y, Greenham K et al. 2020. Genetic analysis of the Arabidopsis TIR1/AFB auxin receptors reveals both overlapping and specialized functions. eLife 9:e54740
    [Google Scholar]
  108. 108. 
    Qu LH, Zhou X, Li X, Li SS, Zhao J et al. 2017. The autonomous cell fate specification of basal cell lineage: The initial round of cell fate specification occurs at the two-celled proembryo stage. Plant J 91:1051–63
    [Google Scholar]
  109. 109. 
    Rademacher EH, Lokerse AS, Schlereth A, Llavata-Peris CI, Bayer M et al. 2012. Different auxin response machineries control distinct cell fates in the early plant embryo. Dev. Cell 22:211–22
    [Google Scholar]
  110. 110. 
    Radoeva T, Albrecht C, Piepers M, de Vries S, Weijers D. 2020. Suspensor-derived somatic embryo-genesis in Arabidopsis. Development 147:dev188912
    [Google Scholar]
  111. 111. 
    Radoeva T, Lokerse AS, Llavata-Peris CI, Wendrich JR, Xiang D et al. 2019. A robust auxin response network controls embryo and suspensor development through a basic helix loop helix transcriptional module. Plant Cell 31:52–67
    [Google Scholar]
  112. 112. 
    Radoeva T, Vaddepalli P, Zhang Z, Weijers D. 2019. Evolution, initiation, and diversity in early plant embryogenesis. Dev. Cell 50:533–43
    [Google Scholar]
  113. 113. 
    Rahman MH, Toda E, Kobayashi M, Kudo T, Koshimizu S et al. 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
    [Google Scholar]
  114. 114. 
    Robert HS, Grones P, Stepanova AN, Robles LM, Lokerse AS et al. 2013. Local auxin sources orient the apical-basal axis in Arabidopsis embryos. Curr. Biol. 23:2506–12
    [Google Scholar]
  115. 115. 
    Robert HS, Grunewald W, Sauer M, Cannoot B, Soriano M et al. 2015. Plant embryogenesis requires AUX/LAX-mediated auxin influx. Development 142:702–11
    [Google Scholar]
  116. 116. 
    Robert HS, Park C, Gutièrrez CL, Wójcikowska B, Pěnčík A et al. 2018. Maternal auxin supply contributes to early embryo patterning in Arabidopsis. Nat. Plants 4:548–53Demonstrates that fertilization-induced auxin biosynthesis in the integuments is necessary for early embryo development.
    [Google Scholar]
  117. 117. 
    Rosa A, Brivanlou AH. 2017. Role of microRNAs in zygotic genome activation: modulation of mRNA during embryogenesis. Methods Mol. Biol. 1605:31–43
    [Google Scholar]
  118. 118. 
    Rövekamp M, Bowman JL, Grossniklaus U. 2016. Marchantia MpRKD regulates the gametophyte-sporophyte transition by keeping egg cells quiescent in the absence of fertilization. Curr. Biol. 26:1782–89
    [Google Scholar]
  119. 119. 
    Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T et al. 2007. Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446:811–14
    [Google Scholar]
  120. 120. 
    Sato A, Toyooka K, Okamoto T. 2010. Asymmetric cell division of rice zygotes located in embryo sac and produced by in vitro fertilization. Sex. Plant Reprod 23:211–17
    [Google Scholar]
  121. 121. 
    Schlereth A, Möller B, Liu W, Kientz M, Flipse J et al. 2010. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464:913–16
    [Google Scholar]
  122. 122. 
    Scholten S, Lörz H, Kranz E. 2002. Paternal mRNA and protein synthesis coincides with male chromatin decondensation in maize zygotes. Plant J 32:221–31
    [Google Scholar]
  123. 123. 
    Schon MA, Nodine MD. 2017. Widespread contamination of Arabidopsis embryo and endosperm transcriptome data sets. Plant Cell 29:608–17
    [Google Scholar]
  124. 124. 
    Schulz KN, Harrison MM. 2019. Mechanisms regulating zygotic genome activation. Nat. Rev. Genet. 20:221–34
    [Google Scholar]
  125. 125. 
    Scott RJ, Armstrong SJ, Doughty J, Spielman M. 2008. Double fertilization in Arabidopsis thaliana involves a polyspermy block on the egg but not the central cell. Mol. Plant 1:611–19
    [Google Scholar]
  126. 126. 
    Sekhon RS, Lin H, Childs KL, Hansey CN, Buell CR et al. 2011. Genome-wide atlas of transcription during maize development. Plant J 66:553–63
    [Google Scholar]
  127. 127. 
    Sivaramakrishna D. 2011. Size relationships of apical cell and basal cell in two-celled embryos in angiosperms. Can. J. Bot. 56:1434–38
    [Google Scholar]
  128. 128. 
    Smit ME, Llavata-Peris CI, Roosjen M, van Beijnum H, Novikova D et al. 2020. Specification and regulation of vascular tissue identity in the Arabidopsis embryo. Development 147:dev186130
    [Google Scholar]
  129. 129. 
    Sprunck S. 2020. Twice the fun, double the trouble: gamete interactions in flowering plants. Curr. Opin. Plant Biol. 53:106–16
    [Google Scholar]
  130. 130. 
    Sprunck S, Rademacher S, Vogler F, Gheyselinck J, Grossniklaus U, Dresselhaus T. 2012. Egg cell-secreted EC1 triggers sperm cell activation during double fertilization. Science 338:1093–97
    [Google Scholar]
  131. 131. 
    Sprunck S, Urban M, Strieder N, Lindemeier M, Bleckmann A et al. 2019. Elucidating small RNA pathways in Arabidopsis thaliana egg cells. bioRxiv 525956. https://doi.org/10.1101/525956
    [Crossref]
  132. 132. 
    Srilunchang KO, Krohn NG, Dresselhaus T. 2010. DiSUMO-like DSUL is required for nuclei positioning, cell specification and viability during female gametophyte maturation in maize. Development 137:333–45
    [Google Scholar]
  133. 133. 
    Steinmann T, Geldner N, Grebe M, Mangold S, Jackson CL et al. 1999. Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286:316–18
    [Google Scholar]
  134. 134. 
    Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie DY et al. 2008. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133:177–91
    [Google Scholar]
  135. 135. 
    Sukawa Y, Okamoto T. 2018. Cell cycle in egg cell and its progression during zygotic development in rice. Plant Reprod 31:107–16
    [Google Scholar]
  136. 136. 
    Takada S, Jürgens G. 2007. Transcriptional regulation of epidermal cell fate in the Arabidopsis embryo. Development 134:1141–50
    [Google Scholar]
  137. 137. 
    Takada S, Takada N, Yoshida A. 2013. ATML1 promotes epidermal cell differentiation in Arabidopsis shoots. Development 140:1919–23
    [Google Scholar]
  138. 138. 
    Takahashi T, Mori T, Ueda K, Yamada L, Nagahara S et al. 2018. The male gamete membrane protein DMP9/DAU2 is required for double fertilization in flowering plants. Development 145:dev170076
    [Google Scholar]
  139. 139. 
    ten Hove CA, Lu KJ, Weijers D. 2015. Building a plant: cell fate specification in the early Arabidopsis embryo. Development 142:420–30
    [Google Scholar]
  140. 140. 
    Tian H, Wabnik K, Niu T, Li H, Yu Q et al. 2014. WOX5-IAA17 feedback circuit-mediated cellular auxin response is crucial for the patterning of root stem cell niches in Arabidopsis. Mol. Plant 7:277–89
    [Google Scholar]
  141. 141. 
    Ueda M, Aichinger E, Gong W, Groot E, Verstraeten I et al. 2017. Transcriptional integration of paternal and maternal factors in the Arabidopsis zygote. Genes Dev 31:617–27Shows that paternal SSP/YDA signaling phosphorylates WRKY2, leading to upregulation of WOX8 in the zygote.
    [Google Scholar]
  142. 142. 
    Ueda M, Berger F. 2019. New cues for body axis formation in plant embryos. Curr. Opin. Plant Biol. 47:16–21
    [Google Scholar]
  143. 143. 
    Ueda M, Zhang Z, Laux T. 2011. Transcriptional activation of Arabidopsis axis patterning genes WOX8/9 links zygote polarity to embryo development. Dev. Cell 20:264–70
    [Google Scholar]
  144. 144. 
    van Dop M, Fiedler M, Mutte S, de Keijzer J, Olijslager L et al. 2020. DIX domain polymerization drives assembly of plant cell polarity complexes. Cell 180:427–39.e12
    [Google Scholar]
  145. 145. 
    van Dop M, Liao CY, Weijers D. 2015. Control of oriented cell division in the Arabidopsis embryo. Curr. Opin. Plant Biol. 23:25–30
    [Google Scholar]
  146. 146. 
    Vastenhouw NL, Cao WX, Lipshitz HD. 2019. The maternal-to-zygotic transition revisited. Development 146:dev161471
    [Google Scholar]
  147. 147. 
    Vijverberg K, Ozias-Akins P, Schranz ME. 2019. Identifying and engineering genes for parthenogenesis in plants. Front. Plant Sci. 10:128
    [Google Scholar]
  148. 148. 
    Vroemen CW, Langeveld S, Mayer U, Ripper G, Jurgens G et al. 1996. Pattern formation in the Arabidopsis embryo revealed by position-specific lipid transfer protein gene expression. Plant Cell 8:783–91
    [Google Scholar]
  149. 149. 
    Wang C, Liu Q, Shen Y, Hua Y, Wang J et al. 2019. Clonal seeds from hybrid rice by simultaneous genome engineering of meiosis and fertilization genes. Nat. Biotechnol. 37:283–86
    [Google Scholar]
  150. 150. 
    Wang K, Chen H, Miao Y, Bayer M. 2020. Square one: zygote polarity and early embryogenesis in flowering plants. Curr. Opin. Plant Biol. 53:128–33
    [Google Scholar]
  151. 151. 
    Wang L, Yuan J, Ma Y, Jiao W, Ye W et al. 2018. Rice interploidy crosses disrupt epigenetic regulation, gene expression, and seed development. Mol. Plant 11:300–14
    [Google Scholar]
  152. 152. 
    Wang X, Allen WE, Wright MA, Sylwestrak EL, Samusik N et al. 2018. Three-dimensional intact-tissue sequencing of single-cell transcriptional states. Science 361:eaat5691
    [Google Scholar]
  153. 153. 
    Weijers D, Schlereth A, Ehrismann JS, Schwank G, Kientz M, Jürgens G. 2006. Auxin triggers transient local signaling for cell specification in Arabidopsis embryogenesis. Dev. Cell 10:265–70
    [Google Scholar]
  154. 154. 
    Wendrich JR, Möller BK, Uddin B, Radoeva T, Lokerse AS et al. 2015. A set of domain-specific markers in the Arabidopsis embryo. Plant Reprod 28:153–60
    [Google Scholar]
  155. 155. 
    Wu CC, Li FW, Kramer EM. 2019. Large-scale phylogenomic analysis suggests three ancient superclades of the WUSCHEL-RELATED HOMEOBOX transcription factor family in plants. PLOS ONE 14:e0223521
    [Google Scholar]
  156. 156. 
    Wuest SE, Vijverberg K, Schmidt A, Weiss M, Gheyselinck J et al. 2010. Arabidopsis female gametophyte gene expression map reveals similarities between plant and animal gametes. Curr. Biol. 20:506–12
    [Google Scholar]
  157. 157. 
    Yang KJ, Guo L, Hou XL, Gong HQ, Liu CM. 2017. ZYGOTE-ARREST 3 that encodes the tRNA ligase is essential for zygote division in Arabidopsis. J. Integr. Plant Biol. 59:680–92
    [Google Scholar]
  158. 158. 
    Yoshida S, Barbier de Reuille P, Lane B, Bassel GW, Prusinkiewicz P et al. 2014. Genetic control of plant development by overriding a geometric division rule. Dev. Cell 29:75–87
    [Google Scholar]
  159. 159. 
    Yu TY, Shi DQ, Jia PF, Tang J, Li HJ et al. 2016. The Arabidopsis receptor kinase ZAR1 is required for zygote asymmetric division and its daughter cell fate. PLOS Genet 12:e1005933
    [Google Scholar]
  160. 160. 
    Zeng L, Zhang Q, Sun R, Kong H, Zhang N, Ma H. 2014. Resolution of deep angiosperm phylogeny using conserved nuclear genes and estimates of early divergence times. Nat. Commun. 5:4956
    [Google Scholar]
  161. 161. 
    Zhang Z, Tucker E, Hermann M, Laux T. 2017. A molecular framework for the embryonic initiation of shoot meristem stem cells. Dev. Cell 40:264–77.e4
    [Google Scholar]
  162. 162. 
    Zhao P, Begcy K, Dresselhaus T, Sun M-X. 2017. Does early embryogenesis in eudicots and monocots involve the same mechanism and molecular players?. Plant Physiol 173:130–42
    [Google Scholar]
  163. 163. 
    Zhao P, Zhou X, Shen K, Liu Z, Cheng T et al. 2019. Two-step maternal-to-zygotic transition with two-phase parental genome contributions. Dev. Cell 49:882–93.e5Demonstrates that rapid maternal transcript degradation is followed by large-scale de novo zygotic transcription.
    [Google Scholar]
  164. 164. 
    Zhao P, Zhou X, Zheng Y, Ren Y, Sun M-X. 2020. Equal parental contribution to the transcriptome is not equal control of embryogenesis. Nat. Plants 6:1354–64Shows that parental genomes contribute equally to ACL and BCL, but a strong maternal effect occurs on the BCL.
    [Google Scholar]
  165. 165. 
    Zhong Y, Chen B, Li M, Wang D, Jiao Y et al. 2020. A DMP-triggered in vivo maternal haploid induction system in the dicotyledonous Arabidopsis. Nat. Plants 6:466–72
    [Google Scholar]
  166. 166. 
    Zhong Y, Liu C, Qi X, Jiao Y, Wang D et al. 2019. Mutation of ZmDMP enhances haploid induction in maize. Nat. Plants 5:575–80
    [Google Scholar]
  167. 167. 
    Zhou LZ, Juranić M, Dresselhaus T. 2017. Germline development and fertilization mechanisms in maize. Mol. Plant 10:389–401
    [Google Scholar]
  168. 168. 
    Zhou S, Jiang W, Zhao Y, Zhou DX. 2019. Single-cell three-dimensional genome structures of rice gametes and unicellular zygotes. Nat. Plants 5:795–800
    [Google Scholar]
  169. 169. 
    Zhou X, Guo Y, Zhao P, Sun MX. 2018. Comparative analysis of WUSCHEL-related homeobox genes revealed their parent-of-origin and cell type-specific expression pattern during early embryogenesis in tobacco. Front. Plant Sci. 9:311
    [Google Scholar]
  170. 170. 
    Zhou X, Liu Z, Shen K, Zhao P, Sun MX. 2020. Cell lineage-specific transcriptome analysis for interpreting cell fate specification of proembryos. Nat. Commun. 11:1366
    [Google Scholar]
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