Abstract
Key message
Recent understandings ofArabidopsiszygote.
Abstract
Body axis formation is essential for the proper development of multicellular organisms. The apical-basal axis in Arabidopsis thaliana is determined by the asymmetric division of the zygote, following its cellular polarization. However, the regulatory mechanism of zygote polarization is unclear due to technical issues. The zygote is located deep in the seed (ovule) in flowers, which prevents the living dynamics of zygotes from being observed. In addition, elucidation of molecular pathways by conventional forward genetic screens was not enough because of high gene redundancy in early development. Here, we present a review introducing two new methods, which have been developed to overcome these problems. Method 1: the two-photon live-cell imaging method provides a new system to visualize the dynamics of intracellular structures in Arabidopsis zygotes, such as cytoskeletons and vacuoles. Microtubules form transverse rings and control zygote elongation, while vacuoles dynamically change their shapes along longitudinal actin filaments and support polar nuclear migration. Method 2: the transcriptome method uses isolated Arabidopsis zygotes and egg cells to reveal the gene expression profiles before and after fertilization. This approach revealed that de novo transcription occurs extensively and immediately after fertilization. Moreover, inhibition of the de novo transcription was shown to sufficiently block the zygotic division, thus indicating a strong possibility that yet unidentified zygote regulators can be found using this transcriptome approach. These new strategies in Arabidopsis will help to further our understanding of the fundamental principles regarding the proper formation of plant bodies from unicellular zygotes.
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References
Abiko M, Maeda H, Tamura K et al (2013) Gene expression profiles in rice gametes and zygotes: identification of gamete-enriched genes and up- or downregulated genes in zygotes after fertilization. J Exp Bot 64:1927–1940. https://doi.org/10.1093/jxb/ert054
Autran D, Baroux C, Raissig MT et al (2011) Maternal epigenetic pathways control parental contributions to Arabidopsis early embryogenesis. Cell 145:707–719. https://doi.org/10.1016/j.cell.2011.04.014
Babu Y, Musielak T, Henschen A, Bayer M (2013) Suspensor length determines developmental progression of the embryo in Arabidopsis. Plant Physiol 162:1448–1458. https://doi.org/10.1104/pp.113.217166
Bayer M, Nawy T, Giglione C et al (2009) Paternal control of embryonic patterning in Arabidopsis thaliana. Science 323:1485–1488. https://doi.org/10.1126/science.1167784
Braun M, Baluška F, von Witsch M, Menzel D (1999) Redistribution of actin, profilin and phosphatidylinositol-4,5-bisphosphate in growing and maturing root hairs. Planta 209:435–443. https://doi.org/10.1007/s004250050746
Breuninger H, Rikirsch E, Hermann M et al (2008) Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis Embryo. Dev Cell 14:867–876. https://doi.org/10.1016/j.devcel.2008.03.008
Chakrabortty B, Willemsen V, de Zeeuw T et al (2018) A plausible microtubule-based mechanism for cell division orientation in plant embryogenesis. Curr Biol 28:3031.e2–3043.e2. https://doi.org/10.1016/j.cub.2018.07.025
Chen J, Strieder N, Krohn NG et al (2017) Zygotic genome activation occurs shortly after fertilization in maize. Plant Cell 29:2106–2125. https://doi.org/10.1105/tpc.17.00099
Chen J, Kalinowska K, Müller B et al (2018) DiSUMO-LIKE Interacts with RNA-binding proteins and affects cell-cycle progression during maize embryogenesis. Curr Biol 28:1548.e5–1560.e5. https://doi.org/10.1016/j.cub.2018.03.066
Del Toro-De León G, García-Aguilar M, Gillmor SC (2014) Non-equivalent contributions of maternal and paternal genomes to early plant embryogenesis. Nature 514:624–627. https://doi.org/10.1038/nature13620
Dolzblasz A, Nardmann J, Clerici E et al (2016) Stem cell regulation by Arabidopsis WOX genes. Mol Plant 9:1028–1039. https://doi.org/10.1016/j.molp.2016.04.007
Faure J, Rotman N, Fortuné P, Dumas C (2002) Fertilization in Arabidopsis thaliana wild type: developmental stages and time course. Plant J 30:481–488. https://doi.org/10.1046/j.1365-313X.2002.01305.x
Goodner B, Quatrano RS (1993) Fucus embryogenesis: a model to study the establishment of polarity. Plant Cell 5:1471–1481. https://doi.org/10.1105/tpc.5.10.1471
Gooh K, Ueda M, Aruga K et al (2015) Live-cell imaging and optical manipulation of Arabidopsis early embryogenesis. Dev Cell 34:242–251. https://doi.org/10.1016/j.devcel.2015.06.008
Gu Y, Vernoud V, Fu Y, Yang Z (2003) ROP GTPase regulation of pollen tube growth through the dynamics of tip-localized F-actin. J Exp Bot 54:93–101. https://doi.org/10.1093/jxb/erg035
Huang J, Liu H, Chen M et al (2014) ROP3 GTPase contributes to polar auxin transport and auxin responses and is important for embryogenesis and seedling growth in Arabidopsis. Plant Cell 26:3501–3518. https://doi.org/10.1105/tpc.114.127902
Ishimoto K, Sohonahra S, Kishi-Kaboshi M et al (2019) Specification of basal region identity after asymmetric zygotic division requires mitogen-activated protein kinase 6 in rice. Development 146:dev176305. https://doi.org/10.1242/dev.176305
Itoh J, Nonomura K, Ikeda K et al (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiol 46:23–47. https://doi.org/10.1093/pcp/pci501
Jürgens G (1995) Axis formation in plant embryogenesis: cues and clues. Cell 81:467–470. https://doi.org/10.1016/0092-8674(95)90065-9
Kao P, Nodine MD (2019) Transcriptional activation of Arabidopsis zygotes is required for initial cell divisions. Sci Rep 9:17159. https://doi.org/10.1038/s41598-019-53704-2
Kato T, Morita M, Fukaki H 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. https://doi.org/10.1105/tpc.010215
Ketelaar T, Faivre-Moskalenko C, Esseling JJ et al (2002) Positioning of nuclei in Arabidopsis root hairs an actin-regulated process of tip growth. Plant Cell 14:2941–2955. https://doi.org/10.1105/tpc.005892
Kimata Y, Higaki T, Kawashima T et al (2016) Cytoskeleton dynamics control the first asymmetric cell division in Arabidopsis zygote. Proc Natl Acad Sci 113:14157–14162. https://doi.org/10.1073/pnas.1613979113
Kimata Y, Kato T, Higaki T et al (2019) Polar vacuolar distribution is essential for accurate asymmetric division of Arabidopsis zygotes. Proc Natl Acad Sci 116:2338–2343. https://doi.org/10.1073/pnas.1814160116
Krüger F, Schumacher K (2018) Pumping up the volume—vacuole biogenesis in Arabidopsis thaliana. Semin Cell Dev Biol 80:106–112. https://doi.org/10.1016/j.semcdb.2017.07.008
Kurihara D, Kimata Y, Higashiyama T, Ueda M (2017) In vitro ovule cultivation for live-cell imaging of zygote polarization and embryo patterning in Arabidopsis thaliana. J Vis Exp. https://doi.org/10.3791/55975
Kuroiwa H, Nishimura Y, Higashiyama T, Kuroiwa T (2002) Pelargonium embryogenesis: cytological investigations of organelles in early embryogenesis from the egg to the two-celled embryo. Sex Plant Reprod 15:1–12. https://doi.org/10.1007/s00497-002-0139-3
Liao C-Y, Weijers D (2018) A toolkit for studying cellular reorganization during early Arabidopsis thaliana embryogenesis. Plant J 93:963–976. https://doi.org/10.1111/tpj.13841
Lukowitz W, Roeder A, Parmenter D, Somerville C (2004) A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell 116:109–119. https://doi.org/10.1016/S0092-8674(03)01067-5
Mansfield S, Briarty L (1991) Early embryogenesis in Arabidopsis thaliana. II. The developing embryo. Can J Bot 69:461–476. https://doi.org/10.1139/b91-063
Mansfield S, Briarty L, Erni S (1991) Early embryogenesis in Arabidopsis thaliana. I. The mature embryo sac. Can J Bot 69:447–460. https://doi.org/10.1139/b91-062
Mizuta Y, Kurihara D, Higashiyama T (2015) Two-photon imaging with longer wavelength excitation in intact Arabidopsis tissues. Protoplasma 252:1231–1240. https://doi.org/10.1007/s00709-014-0754-5
Möller BK, ten Hove CA, Xiang D et al (2017) Auxin response cell-autonomously controls ground tissue initiation in the early Arabidopsis embryo. Proc Natl Acad Sci 114:E2533–E2539. https://doi.org/10.1073/pnas.1616493114
Murata T, Kadota A, Hogetsu T, Wada M (1987) Circular arrangement of cortical microtubules around the subapical part of a tip-growing fern protonema. Protoplasma 141:135–138. https://doi.org/10.1007/BF01272895
Neu A, Eilbert E, Asseck LY et al (2019) Constitutive signaling activity of a receptor-associated protein links fertilization with embryonic patterning in Arabidopsis thaliana. Proc Natl Acad Sci 116:5795–5804. https://doi.org/10.1073/pnas.1815866116
Niklas KJ, Cobb ED, Kutschera U (2016) Haeckel’s biogenetic law and the land plant phylotypic stage. BioScience 66:510–519. https://doi.org/10.1093/biosci/biw029
Nodine MD, Bartel DP (2012) Maternal and paternal genomes contribute equally to the transcriptome of early plant embryos. Nature 482:94–97. https://doi.org/10.1038/nature10756
Palovaara J, Saiga S, Wendrich JR et al (2017) Transcriptome dynamics revealed by a gene expression atlas of the early Arabidopsis embryo. Nat Plants 3:894–904. https://doi.org/10.1038/s41477-017-0035-3
Robert HS, Park C, Gutièrrez C et al (2018) Maternal auxin supply contributes to early embryo patterning in Arabidopsis. Nat Plants 4:548–553. https://doi.org/10.1038/s41477-018-0204-z
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 23:211–217. https://doi.org/10.1007/s00497-009-0129-9
Scheuring D, Löfke C, Krüger F et al (2016) Actin-dependent vacuolar occupancy of the cell determines auxin-induced growth repression. Proc Natl Acad Sci 113:452–457. https://doi.org/10.1073/pnas.1517445113
Schon MA, Nodine MD (2017) Widespread contamination of arabidopsis embryo and endosperm transcriptome data sets. Plant Cell 29:608–617. https://doi.org/10.1105/tpc.16.00845
Schulz R, Jensen WA (1968) Capsella embryogenesis: the egg, zygote, and young embryo. Am J Bot 55:807–819. https://doi.org/10.1002/j.1537-2197.1968.tb07438.x
Sivaramakrishna D (1978) Size relationships of apical cell and basal cell in two-celled embryos in angiosperms. Can J Bot 56:1434–1438. https://doi.org/10.1139/b78-166
Smit ME, Weijers D (2015) The role of auxin signaling in early embryo pattern formation. Curr Opin Plant Biol 28:99–105. https://doi.org/10.1016/j.pbi.2015.10.001
Tian J, Han L, Feng Z et al (2015) Orchestration of microtubules and the actin cytoskeleton in trichome cell shape determination by a plant-unique kinesin. eLife 4:e09351. https://doi.org/10.7554/eLife.09351
Toyota M, Ikeda N, Sawai-Toyota S et al (2013) Amyloplast displacement is necessary for gravisensing in Arabidopsis shoots as revealed by a centrifuge microscope. Plant J 76:648–660. https://doi.org/10.1111/tpj.12324
Ueda M, Zhang Z, Laux T (2011) Transcriptional activation of Arabidopsis axis patterning genes WOX8/9 links zygote polarity to embryo development. Dev Cell 20:264–270. https://doi.org/10.1016/j.devcel.2011.01.009
Ueda M, Aichinger E, Gong W et al (2017) Transcriptional integration of paternal and maternal factors in the Arabidopsis zygote. Genes Dev 31:617–627. https://doi.org/10.1101/gad.292409.116
van Dop M, Fiedler M, Mutte S et al (2020) DIX domain polymerization drives assembly of plant cell polarity complexes. Cell 180:427.e12–439.e12. https://doi.org/10.1016/j.cell.2020.01.011
Vidali L, Rounds CM, Hepler PK, Bezanilla M (2009) Lifeact-mEGFP reveals a dynamic apical F-actin network in tip growing plant cells. PLoS ONE 4:e5744. https://doi.org/10.1371/journal.pone.0005744
Wang H, Ngwenyama N, Liu Y et al (2007) Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19:63–73. https://doi.org/10.1105/tpc.106.048298
Webb MC, Gunning BE (1991) The microtubular cytoskeleton during development of the zygote, proembryo and free-nuclear endosperm in Arabidopsis thaliana (L.) Heynh. Planta 184:187–195. https://doi.org/10.1007/BF00197947
Xiao W, Custard KD, Brown RC et al (2006) DNA methylation is critical for Arabidopsis embryogenesis and seed viability. Plant Cell 18:805–814. https://doi.org/10.1105/tpc.105.038836
Yang Z (2008) Cell polarity signaling in Arabidopsis. Annu Rev Cell Dev Biol 24:551–575. https://doi.org/10.1146/annurev.cellbio.23.090506.123233
Yoshida S, van der Schuren A, van Dop M et al (2019) A SOSEKI-based coordinate system interprets global polarity cues in Arabidopsis. Nat Plants 5:160–166. https://doi.org/10.1038/s41477-019-0363-6
Zhang M, Wu H, Su J et al (2017) Maternal control of embryogenesis by MPK6 and its upstream MKK4/MKK5 in Arabidopsis. Plant J 92:1005–1019. https://doi.org/10.1111/tpj.13737
Zhao J, Xin H, Qu L et al (2013) Dynamic changes of transcript profiles after fertilization are associated with de novo transcription and maternal elimination in tobacco zygote, and mark the onset of the maternal-to-zygotic transition. Plant J 65:131–145. https://doi.org/10.1111/j.1365-313X.2010.04403.x
Zhao P, Zhou X, Shen K et al (2019) Two-step maternal-to-zygotic transition with two-phase parental genome contributions. Dev Cell 49:882.e5–893.e5. https://doi.org/10.1016/j.devcel.2019.04.016
Zheng J, Han SW, Rodriguez-Welsh MF, Rojas-Pierce M (2014) Homotypic vacuole fusion requires VTI11 and is regulated by phosphoinositides. Mol Plant 7:1026–1040. https://doi.org/10.1093/mp/ssu019
Zhou X, Shi C, Zhao P, Sun M (2018) Isolation of living apical and basal cell lineages of early proembryos for transcriptome analysis. Plant Reprod 32:105–111. https://doi.org/10.1007/s00497-018-00353-6
Zhou X, Liu Z, Shen K et al (2020) Cell lineage-specific transcriptome analysis for interpreting cell fate specification of proembryos. Nat Commun 11:1366. https://doi.org/10.1038/s41467-020-15189-w
Acknowledgements
We received funding supports from Japanese Society for the Promotion of Science: Grant-in-Aid for JSPS Research Fellow (19J30006 for Y.K.), Grant-in-Aid for Scientific Research on Innovative Areas (19H05676 and 19H05670 for M.U.), Grant-in-Aid for Scientific Research (B, 19H03243 for M.U.), and Grant-in-Aid for Challenging Exploratory Research (19K22421 for M.U.). We would like to thank Editage (www.editage.com) for English language editing.
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Kimata, Y., Ueda, M. Intracellular dynamics and transcriptional regulations in plant zygotes: a case study of Arabidopsis. Plant Reprod 33, 89–96 (2020). https://doi.org/10.1007/s00497-020-00389-7
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DOI: https://doi.org/10.1007/s00497-020-00389-7