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The asymmetric division of the Arabidopsis zygote: from cell polarity to an embryo axis

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Abstract

During plant embryogenesis, a simple body plan consisting of shoot and root meristem that are connected by the embryo axis is set up by the first few rounds of cell divisions after fertilization. Postembryonically, the elaborate architecture of plants is created from stem cell populations of both meristems. Here, we address how the main axis (apical-basal) of the plant embryo is established from the single-celled zygote and the role that the asymmetric division of the zygote plays in this process. We will mainly draw on examples from the model plant Arabidopsis, for which several key regulators have been identified during the last years.

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References

  • Armenta-Medina A, Demesa-Arévalo E, Vielle-Calzada JP (2011) Epigenetic control of cell specification during female gametogenesis. Sex Plant Reprod 24

  • Basu S, Sun H, Brian L, Quatrano RL, Muday GK (2002) Early embryo development in Fucus distichus is auxin sensitive. Plant Physiol 130:292–302

    Article  PubMed  CAS  Google Scholar 

  • Bayer M, Nawy T, Giglione C, Galli M, Meinnel T, Lukowitz W (2009) Paternal control of embryonic patterning in Arabidopsis thaliana. Science 323:1485–1488

    Article  PubMed  CAS  Google Scholar 

  • Bencivenga S, Colombo L, Masiero S (2011) Cross talk between the sporophyte and the megagametophyte during ovule development. Sex Plant Reprod 24

  • Berger F, Taylor A, Brownlee C (1994) Cell fate determination by the cell wall in early Fucus development. Science 263:1421–1423

    Article  PubMed  CAS  Google Scholar 

  • Bergmann DC, Lukowitz W, Somerville CR (2004) Stomatal development and pattern controlled by a MAPKK kinase. Science 304:1494–1497

    Article  PubMed  CAS  Google Scholar 

  • Berleth T, Jürgens G (1993) The role of the Monopteros gene in organising the basal body region of the Arabidopsis embryo. Development 118:575–587

    Google Scholar 

  • 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 14:867–876

    Article  PubMed  CAS  Google Scholar 

  • Chen D, Ren Y, Deng Y, Zhao J (2010) Auxin polar transport is essential for the development of zygote and embryo in Nicotiana tabacum L. and correlated with ABP1 and PM H+-ATPase activities. J Exp Bot 61:1853–1867

    Article  PubMed  CAS  Google Scholar 

  • Dong J, MacAlister CA, Bergmann DC (2009) BASL controls asymmetric cell division in Arabidopsis. Cell 137:1320–1330

    Article  PubMed  Google Scholar 

  • Dunoyer P, Schott G, Himber C, Meyer D, Takeda A, Carrington JC, Voinnet O (2010) Small RNA duplexes function as mobile silencing signals between plant cells. Science 328:912–916

    Article  PubMed  CAS  Google Scholar 

  • Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426:147–153

    Article  PubMed  CAS  Google Scholar 

  • Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Müller P, Delbarre A, Ueda T, Nakano A, Jürgens G (2003) The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112:219–230

    Article  PubMed  CAS  Google Scholar 

  • Genger RK, Kovac KA, Dennis ES, Peacock WJ, Finnegan EJ (1999) Multiple DNA methyltransferase genes in Arabidopsis thaliana. Plant Mol Biol 41:269–278

    Article  PubMed  CAS  Google Scholar 

  • Gerlach-Cruse D (1969) Embryo- und Endospermentwicklung nach einer Röntgenbestrahlung der Fruchtknoten von Arabidopsis thaliana. Radiat Bot 9:433–442

    Article  Google Scholar 

  • Golden TA, Schauer SE, Lang JD, Pien S, Mushegian AR, Grossniklaus U, Meinke DW, Ray A (2002) SHORT INTEGUMENTS1/SUSPENSOR1/CARPEL FACTORY, a Dicer homolog, is a maternal effect gene required for embryo development in Arabidopsis. Plant Physiol 130:808–822

    Article  PubMed  Google Scholar 

  • Goodner B, Quatrano RS (1993) Fucus embryogenesis: a model to study the establishment of polarity. Plant Cell 5:1471–1481

    Article  PubMed  Google Scholar 

  • Haecker A, Gross-Hardt R, Geiges B, Sarkar A, Breuninger H, Herrmann M, Laux T (2004) Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131:657–668

    Article  PubMed  CAS  Google Scholar 

  • 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 126:1387–1395

    PubMed  CAS  Google Scholar 

  • 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 16:1610–1615

    Article  PubMed  CAS  Google Scholar 

  • Hardtke CS, Berleth T (1998) The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 17:1405–1411

    Article  PubMed  CAS  Google Scholar 

  • Jenkins N, Saam JR, Mango SE (2006) CYK-4/GAP provides a localized cue to initiate anteroposterior polarity upon fertilization. Science 313:1298–1301

    Article  PubMed  CAS  Google Scholar 

  • Jürgens G, Mayer U (1994) Arabidopsis. In: Bard J (ed) A colour atlas of developing embryos. Wolfe Publishing, London, pp 7–21

    Google Scholar 

  • Kaplan DR, Cooke TJ (1997) Fundamental concepts in the embryogenesis of dicotyledons: a morphological interpretation of embryo mutants. Plant Cell 9:1903–1919

    Article  PubMed  CAS  Google Scholar 

  • Kropf DL (1997) Induction of polarity in fucoid zygotes. Plant Cell 9:1011–1020

    Article  PubMed  CAS  Google Scholar 

  • Langlands K, Yin X, Anand G, Prochownik EV (1997) Differential interactions of Id proteins with basic-helix-loop-helix transcription factors. J Biol Chem 272:19785–19793

    Article  PubMed  CAS  Google Scholar 

  • Liang HL, Nien CY, Liu HY, Metzstein MM, Kirov N, Rushlow C (2008) The zinc-finger protein Zelda is a key activator of the early zygotic genome in Drosophila. Nature 456:400–403

    Article  PubMed  CAS  Google Scholar 

  • Lucas WJ, Bouché-Pillon S, Jackson DP, Nguyen L, Baker L, Ding B, Hake S (1995) Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270:1980–1983

    Article  PubMed  CAS  Google Scholar 

  • Lukowitz W, Roeder A, Parmenter D, Somerville C (2004) A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell 116:109–119

    Article  PubMed  CAS  Google Scholar 

  • Mansfield SG, Briarty LG (1991) Early embryogenesis in Arabidopsis thaliana. II. The developing embryo. Can J Bot 69:461–476

    Article  Google Scholar 

  • Mayer U, Büttner G, Jürgens G (1993) Apical-basal pattern formation in the Arabidopsis embryo: studies on the role of the gnom gene. Development 117:149–162

    Google Scholar 

  • Mayer KF, 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 95:805–815

    Article  PubMed  CAS  Google Scholar 

  • Meyer S, Scholten S (2007) Equivalent parental contribution to early plant zygotic development. Curr Biol 17:1686–1691

    Article  PubMed  CAS  Google Scholar 

  • Moore T, Haig D (1991) Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet 7:45–49

    PubMed  CAS  Google Scholar 

  • Nakajima K, Uchiumi T, Okamoto T (2010) Positional relationship between the gamete fusion site and the first division plane in the rice zygote. J Exp Bot 61:3101–3105

    Article  PubMed  CAS  Google Scholar 

  • 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 24:2474–2484

    Article  PubMed  CAS  Google Scholar 

  • Ngo QA, Moore JM, Baskar R, Grossniklaus U, Sundaresan V (2007) Arabidopsis GLAUCE promotes fertilization-independent endosperm development and expression of paternally inherited alleles. Development 134:4107–4117

    Article  PubMed  CAS  Google Scholar 

  • Ning J, Peng XB, Qu LH, Xin HP, Yan TT, Sun M (2006) Differential gene expression in egg cells and zygotes suggests that the transcriptome is restructed before the first zygotic division in tobacco. FEBS Lett 580:1747–1752

    Article  PubMed  CAS  Google Scholar 

  • Olsen OA (2004) Nuclear endosperm development in cereals and Arabidopsis thaliana. Plant Cell 16:S214–S227

    Article  PubMed  CAS  Google Scholar 

  • Pagnussat GC, Alandete-Saez M, Bowman JL, Sundaresan V (2009) Auxin-dependent patterning and gamete specification in the Arabidopsis female gametophyte. Science 324:1684–1689

    Article  PubMed  CAS  Google Scholar 

  • Petrasek J, Friml J (2009) Auxin transport routes in plant development. Development 136:2675–2688

    Article  PubMed  CAS  Google Scholar 

  • Pillot M, Baroux C, Vazquez MA, Autran D, Leblanc O, Vielle-Calzada JP, Grossniklaus U, Grimanelli D (2010) Embryo and endosperm inherit distinct chromatin and transcriptional states from the female gametes in Arabidopsis. Plant Cell 22:307–320

    Article  PubMed  CAS  Google Scholar 

  • Qin Y, Zhao J (2006) Localization of arabinogalactan proteins in egg cells, zygotes, and two-celled proembryos and effects of beta-D-glucosyl Yariv reagent on egg cell fertilization and zygote division in Nicotiana tabacum L. J Exp Bot 57:2061–2074

    Article  PubMed  CAS  Google Scholar 

  • Quatrano RS (1990) Polar axis fixation and cytoplasmic localization in Fucus. In: Mahowald AP (ed) Genetics of pattern formation and growth control. Wiley, New York, pp 31–46

    Google Scholar 

  • Ray S, Golden T, Ray A (1996) Maternal effects of the short integument mutation on embryo development in Arabidopsis. Dev Biol 180:365–369

    Article  PubMed  CAS  Google Scholar 

  • Robert S, Kleine-Vehn J, Barbez E, Sauer M, Paciorek T, Baster P, Vanneste S, Zhang J, Simon S, Covanova M, Hayashi K, Dhonukshe P, Yang Z, Bednarek SY, Jones AM, Luschnig C, Aniento F, Zazimalova E, Friml J (2010) ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell 143:111–121

    Article  PubMed  CAS  Google Scholar 

  • Schier AF (2007) The maternal-zygotic transition: death and birth of RNAs. Science 316:406–407

    Article  PubMed  CAS  Google Scholar 

  • Schlereth A, Moller BK, Liu W, Kientz M, Flipse J, Rademacher EH, Schmid M, Jürgens G, Weijers D (2010) MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464:913–916

    Article  PubMed  CAS  Google Scholar 

  • Shevell DE, Leu W-M, Gilimor CS, Xia G, Feldmann KA, Chua N-H (1994) EMB30 is essential for normal cell division, cell expansion, and cell adhesion in Arabidopsis and encodes a protein that has similarity to Sec 7. Cell 77:1051–1062

    Article  PubMed  CAS  Google Scholar 

  • Sprunck S, Groß-Hardt R (2011) Nuclear behavior, cell polarity and cell specification in the female gametophyte. Sex Plant Reprod 24

  • Steinmann T, Geldner N, Grebe M, Mangold S, Jackson CL, Paris S, Galweiler L, Palme K, Jürgens G (1999) Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286:316–318

    Article  PubMed  CAS  Google Scholar 

  • Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie DY, Dolezal K, Schlereth A, Jürgens G, Alonso JM (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133:177–191

    Article  PubMed  CAS  Google Scholar 

  • Twell D (2011) Male gametogenesis and germline specification in flowering plants. Sex Plant Reprod 24

  • van der Graaff E, Laux T, Rensing SA (2009) The WUS homeobox-containing (WOX) protein family. Genome Biol 10:248

    Article  PubMed  Google Scholar 

  • Wang H, Ngwenyama N, Liu Y, Walker JC, Zhang S (2007) Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19:63–73

    Article  PubMed  Google Scholar 

  • Weijers D, Friml J (2009) Snapshot: auxin signaling and transport. Cell 136:1172

    Article  PubMed  CAS  Google Scholar 

  • Weijers D, Van Hamburg JP, Van Rijn E, Hooykaas PJ, Offringa R (2003) Diphtheria toxin-mediated cell ablation reveals interregional communication during Arabidopsis seed development. Plant Physiol 133:1882–1892

    Article  PubMed  CAS  Google Scholar 

  • 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 10:265–270

    Article  PubMed  CAS  Google Scholar 

  • Wu X, Chory J, Weigel D (2007) Combinations of WOX activities regulate tissue proliferation during Arabidopsis embryonic development. Dev Biol 309:306–316

    Article  PubMed  CAS  Google Scholar 

  • Xiao W, Custard KD, Brown RC, Lemmon BE, Harada JJ, Goldberg RB, Fischer RL (2006) DNA methylation is critical for Arabidopsis embryogenesis and seed viability. Plant Cell 18:805–814

    Article  PubMed  CAS  Google Scholar 

  • Xu T, Wen M, Nagawa S, Fu Y, Chen JG, Wu MJ, Perrot-Rechenmann C, Friml J, Jones AM, Yang Z (2010) Cell surface- and rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143:99–110

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Julien Bellis, Chulmin Park, and Leron Katsir for helpful comments on the manuscript. We would like to apologize to those colleagues whose valuable work was not discussed due to space constraints. We gratefully acknowledge financial support from the Deutsche Forschungsgemeinschaft (Arabidopsis Functional Genomic Network) and the EU (SIREN) to T.L., and from the GRK1305 fellowship to Z.Z.

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  1. Faculty of Biology, Albert-Ludwigs University Freiburg, Schänzlestrasse 1, 79104, Freiburg, Germany

    Zhongjuan Zhang & Thomas Laux

  2. Freiburg Institute of Advanced Studies, University of Freiburg, Albertstr. 19, 79104, Freiburg, Germany

    Thomas Laux

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  1. Zhongjuan Zhang
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  2. Thomas Laux
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Correspondence to Thomas Laux.

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Communicated by Thomas Dresselhaus.

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Zhang, Z., Laux, T. The asymmetric division of the Arabidopsis zygote: from cell polarity to an embryo axis. Sex Plant Reprod 24, 161–169 (2011). https://doi.org/10.1007/s00497-010-0160-x

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