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Asymmetric Cell Divisions: Zygotes of Fucoid Algae as a Model System

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Cell Division Control in Plants

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 9))

Abstract

Asymmetric cell divisions are commonly used across diverse phyla to generate different kindsof cells during development. Although asymmetric divisions play important roles during developmentin plants, algae, fungi, and animals, emerging data indicate that there is some variability amongstthe mechanisms that are at play in these different organisms. Zygotes of fucoid algae have long servedas models for understanding early developmental processes including cell polarization and asymmetriccell division. In addition, brown algae are phylogenetically distant from other organisms, includingplant models, a feature that makes them interesting from a comparative perspective (Andersen2004; Peters et al. 2004). This monograph focuses on advances made toward understanding howasymmetric divisions are regulated in fucoid algae and, where appropriate, comparisons are made tohigher plant zygotes.

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References

  • Alessa L, Kropf DL (1999) F-actin marks the rhizoid pole in living Pelvetia compressa zygotes. Development 126:201–209

    PubMed  CAS  Google Scholar 

  • Allen VW, Kropf DL (1992) Nuclear rotation and lineage specification in Pelvetia embryos. Development 115:873–883

    Google Scholar 

  • Andersen RA (2004) Biology and systematics of heterokont and haptophyte algae. Am J Bot 91:1508–1522

    PubMed  Google Scholar 

  • Arkowitz RA (2001) Cell polarity: connecting to the cortex. Curr Biol 11:R610–R612

    PubMed  CAS  Google Scholar 

  • Belanger KD, Quatrano RS (2000a) Membrane recycling occurs during asymmetric tip growth and cell plate formation in Fucus distichus zygotes. Protoplasma 212:24–37

    Google Scholar 

  • Belanger KD, Quatrano RS (2000b) Polarity: the role of localized secretion. Curr Opin Plant Biol 3:67–72

    PubMed  CAS  Google Scholar 

  • Berger F, Brownlee C (1993) Ratio confocal imaging of free cytoplasmic calcium gradients in polarising and polarised Fucus zygotes. Zygote 1:9–15

    PubMed  CAS  Google Scholar 

  • Berger F, Brownlee C (1994) Photopolarization of the Fucus sp zygote by blue light involves a plasma membrane redox chain. Plant Physiol 105:519–527

    PubMed  PubMed Central  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Betschinger J, Knoblich JA (2004) Dare to be different: asymmetric cell division in Drosophila, C. elegans, and vertebrates. Curr Biol 14:R674–R685

    PubMed  CAS  Google Scholar 

  • Bisgrove SR, Kropf DL (1998) Alignment of centrosomal and growth axes is a late event during polarization of Pelvetia compressa zygotes. Dev Biol 194:246–256

    PubMed  CAS  Google Scholar 

  • Bisgrove SR, Kropf DL (2001) Asymmetric cell division in fucoid algae: a role for cortical adhesions in alignment of the mitotic apparatus. J Cell Sci 114:4319–4328

    PubMed  CAS  Google Scholar 

  • Bisgrove SR, Kropf DL (2004) Cytokinesis in brown algae: studies of asymmetric division in fucoid zygotes. Protoplasma 223:163–173

    PubMed  CAS  Google Scholar 

  • Bisgrove SR, Nagasato C, Motomura T, Kropf DL (1997) Immunolocalization of centrin in Fucus distichus and Pelvetia compressa (Fucales, Phaeophyceae). J Phycol 33:823–829

    Google Scholar 

  • Bisgrove SR, Henderson DC, Kropf DL (2003) Asymmetric division in fucoid zygotes is positioned by telophase nuclei. Plant Cell 15:854–862

    PubMed  PubMed Central  CAS  Google Scholar 

  • Bouget F-Y, Gerttula S, Quatrano RS (1995) Spatial redistribution of poly(A)+ RNA during polarization of the Fucus zygote is dependent upon microfilaments. Dev Biol 171:258–261

    PubMed  CAS  Google Scholar 

  • Bouget F-Y, Gerttula S, Shaw SL, Quatrano RS (1996) Localization of actin mRNA during the establishment of cell polarity and early cell divisions in Fucus embryos. Plant Cell 8:189–201

    PubMed  PubMed Central  CAS  Google Scholar 

  • Brawley SH, Quatrano RS (1979) Sulfation of fucoidin in Fucus embryos. IV. Autoradiographic investigations of fucoidin sulfation and secretion during differentiation and the effect of cytochalasin treatment. Dev Biol 73:193–205

    PubMed  CAS  Google Scholar 

  • Brown RC, Lemmon BE (2001) The cytoskeleton and spatial control of cytokinesis in the plant life cycle. Protoplasma 215:35–49

    PubMed  CAS  Google Scholar 

  • Brownlee C (2004) From polarity to pattern: early development in fucoid algae. In: Lindsey K (ed) Annual plant reviews, vol. 12. Blackwell, Oxford, pp 139–155

    Google Scholar 

  • Busch M, Mayer U, Jurgens G (1996) Molecular analysis of the Arabidopsis pattern formation gene GNOM: gene structure and intragenic complementation. Mol Gen Genet 250:681–691

    PubMed  CAS  Google Scholar 

  • Cheng Q, Pappas V, Hallmann A, Miller SM (2005) Hsp70A and GlsA interact as partner chaperones to regulate asymmetric division in Volvox. Dev Biol 286:537–548

    PubMed  CAS  Google Scholar 

  • Corellou F, Potin P, Brownlee C, Kloareg B, Bouget F-Y (2000a) Inhibition of the establishment of zygotic polarity by protein tyrosine kinase inhibitors leads to an alteration of embryo pattern in Fucus. Dev Biol 219:165–182

    PubMed  CAS  Google Scholar 

  • Corellou FC, Bisgrove SR, Kropf DL, Meijer L, Kloareg B, Bouget F-Y (2000b) A S/M DNA replication checkpoint prevents nuclear and cytoplasmic events of cell division including centrosomal axis alignment and inhibits activation of cyclin dependent kinase-like proteins in fucoid zygotes. Development 127:1651–1660

    PubMed  CAS  Google Scholar 

  • Corellou F, Coelho SMB, Bouget F-Y, Brownlee C (2005) Spatial re-organisation of cortical microtubules in vivo during polarisation and asymmetric division of Fucus zygotes. J Cell Sci 118:2723–2734

    PubMed  CAS  Google Scholar 

  • Cove D, Benzanilla M, Harries P, Quatrano R (2006) Mosses as model systems for the study of metabolism and development. Annu Rev Plant Biol 57:497–520

    PubMed  CAS  Google Scholar 

  • Cowan CR, Hyman AA (2004) Asymmetric cell division in C. elegans: cortical polarity and spindle positioning. Annu Rev Cell Dev Biol 20:427–453

    PubMed  CAS  Google Scholar 

  • Daga RR, Yonetani A, Chang F (2006) Asymmetric microtubule pushing forces in nuclear centering. Curr Biol 16:1544–1550

    PubMed  CAS  Google Scholar 

  • Drews GN, Yadegari R (2002) Development and function of the angiosperm female gametophyte. Annu Rev Genet 36:99–124

    PubMed  CAS  Google Scholar 

  • Fowler JE, Quatrano RS (1997) Plant cell morphogenesis: plasma membrane interactions with the cytoskeleton and cell wall. Annu Rev Cell Dev Biol 13:697–743

    PubMed  CAS  Google Scholar 

  • Gallagher K, Smith LG (1997) Asymmetric cell division and cell fate in plants. Curr Opin Cell Biol 9:842–848

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Green KJ, Kirk DL (1981) Cleavage patterns, cell lineages, and development of a cytoplasmic bridge system in Volvox embryos. J Cell Biol 91:743–755

    PubMed  CAS  Google Scholar 

  • Gualtieri P, Robinson KR (2002) A rhodopsin-like protein in the plasma membrane of Silvetia compressa eggs. Photochem Photobiol 75:76–78

    PubMed  CAS  Google Scholar 

  • Hable WE, Kropf DL (1998) Roles of secretion and the cytoskeleton in cell adhesion and polarity establishment in Pelvetia compressa zygotes. Dev Biol 198:45–56

    PubMed  CAS  Google Scholar 

  • Hable WE, Kropf DL (2000) Sperm entry induces polarity in fucoid zygotes. Development 127:493–501

    PubMed  CAS  Google Scholar 

  • Hable WE, Kropf DL (2005) The Arp2/3 complex nucleates actin arrays during zygote polarity establishment and growth. Cell Motil Cytoskel 61:9–20

    CAS  Google Scholar 

  • Hable WE, Miller NR, Kropf DL (2003) Polarity establishment requires dynamic actin in fucoid zygotes. Protoplasma 221:193–204

    PubMed  CAS  Google Scholar 

  • Hadley R, Hable WE, Kropf DL (2006) Polarization of the endomembrane system is an early event in fucoid zygote development. BMC Plant Biol 6:5

    PubMed  PubMed Central  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

    PubMed  CAS  Google Scholar 

  • Heidstra R, Welch D, Scheres B (2004) Mosaic analyses using marked activation and deletion clones dissect Arabidopsis SCARECROW action in asymmetric cell division. Genes Dev 18:1964–1969

    PubMed  PubMed Central  CAS  Google Scholar 

  • Henry CA, Jordan JR, Kropf DL (1996) Localized membrane–wall adhesions in Pelvetia zygotes. Protoplasma 190:39–52

    CAS  Google Scholar 

  • Hoshino H, Yoneda A, Kumagai F, Hasezawa S (2003) Roles of actin-depleted zone and preprophase band in determining the division site of higher-plant cells, a tobacco BY-2 cell line expressing GFP-tubulin. Protoplasma 222:157–165

    PubMed  CAS  Google Scholar 

  • Howard J (2006) Elastic and damping forces generated by confined arrays of dynamic microtubules. Phys Biol 3:54–66

    PubMed  CAS  Google Scholar 

  • Hurd AM (1920) Effect of unilateral monochromatic light and group orientation of germinating Fucus spores. Bot Gaz 70:25–50

    Google Scholar 

  • Jaffe LF (1958) Tropistic responses of zygotes of the Fucaceae to polarized light. Exp Cell Res 15:282–299

    PubMed  CAS  Google Scholar 

  • Jaffe LF (1969) On the centripetal course of development, the Fucus egg, and self-electrophoresis. Dev Biol Suppl 3:83–111

    Google Scholar 

  • Jurgens G (2005) Cytokinesis in higher plants. Annu Rev Plant Biol 56:281–299

    PubMed  Google Scholar 

  • Karyophyllis D, Katsaros C, Dimitriadis I, Galatis B (2000) F-actin organization during the cell cycle of Sphacelaria rigidula (Phaeophyceae). Eur J Phycol 35:25–33

    Google Scholar 

  • Katsaros C, Galatis B (1992) Immunofluorescence and electron microscopic studies of microtubule organization during the cell cycle of Dictyota dichotoma (Phaeophyta, Dictyotales). Protoplasma 169:75–84

    Google Scholar 

  • Katsaros C, Galatis B, Mitrakos K (1983) Fine structural studies on the interphase and dividing apical cells of Sphacelaria tribuloides (Phaeophyta). J Phycol 19:16–30

    Google Scholar 

  • Katsaros C, Karyophyllis D, Galatis B (2006) Cytoskeleton and morphogenesis in brown algae. Ann Bot 97:679–693

    PubMed  PubMed Central  Google Scholar 

  • Kirk DL (2004) Volvox. Curr Biol 14:R599–R600

    PubMed  CAS  Google Scholar 

  • Kirk MM, Ransick A, McRae SE, Kirk DL (1993) The relationship between cell size and cell fate in Volvox carteri. J Cell Biol 123:191–208

    PubMed  CAS  Google Scholar 

  • Kropf DL, Maddock A, Gard DL (1990) Microtubule distribution and function in early Pelvetia development. J Cell Sci 97:545–552

    Google Scholar 

  • Kropf DL, Money NP, Gibbon BC (1995) Role of cytosolic pH in axis establishment and tip growth. Can J Bot 73:S126–S130

    Google Scholar 

  • Kropf DL, Bisgrove SR, Hable WE (1999) Establishing a growth axis in fucoid algae. Trends Plant Sci 4:490–494

    PubMed  CAS  Google Scholar 

  • Laux T, Wurschum T, Breuninger H (2004) Genetic regulation of embryonic pattern formation. Plant Cell 16:S190–S202

    PubMed  PubMed Central  CAS  Google Scholar 

  • Lovy-Wheeler A, Wilsen KL, Baskin TI, Hepler PK (2005) Enhanced fixation reveals the apical cortical fringe of actin filaments as a consistent feature of the pollen tube. Planta 221:95–104

    PubMed  CAS  Google Scholar 

  • Lucas JR, Nadeau JA, Sack FD (2006) Microtubule arrays and Arabidopsis stomatal development. J Exp Bot 57:71–79

    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

    PubMed  CAS  Google Scholar 

  • Marcus AI, Dixit R, Cyr RJ (2005) Narrowing of the preprophase microtubule band is not required for cell division plane determination in cultured plant cells. Protoplasma 226:169–174

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • McCarthy EK, Goldstein B (2006) Asymmetric spindle positioning. Curr Opin Cell Biol 18:79–85

    PubMed  CAS  Google Scholar 

  • McClinton RS, Sung R (1997) Organization of cortical microtubules at the plasma membrane in Arabidopsis. Planta 201:252–260

    PubMed  CAS  Google Scholar 

  • Motomura T (1994) Electron and immunofluorescence microscopy on the fertilization of Fucus distichus (Fucales, Phaeophyceae). Protoplasma 178:97–110

    Google Scholar 

  • Motomura T, Nagasato C (2004) The first spindle formation in brown algal zygotes. Hydrobiologia 512:171–176

    Google Scholar 

  • Murata T, Sugai M (2000) Photoregulation of asymmetric cell division followed by rhizoid development in the fern Ceratopteris prothalli. Plant Cell Physiol 41:1313–1320

    PubMed  CAS  Google Scholar 

  • Nadeau JA, Sack FD (2002) Stomatal development in Arabidopsis. In: Somerville CR, Meyerowitz EM (eds) The Arabidopsis book. American Society of Plant Biologists, Rockville, MD, pp 1–28

    Google Scholar 

  • Nadeau JA, Sack FD (2003) Stomatal development: cross talk puts mouths in place. Trends Plant Sci 8:294–299

    PubMed  CAS  Google Scholar 

  • Nagasato C (2005) Behavior and function of paternally inherited centrioles in brown algal zygotes. J Plant Res 118:361–369

    PubMed  Google Scholar 

  • Nagasato C, Motomura T (2002a) Influence of the centrosome in cytokinesis of brown algae: polyspermic zygotes of Scytosiphon lomentaria (Scytosiphonales, Phaeophyceae). J Cell Sci 115:2541–2548

    PubMed  CAS  Google Scholar 

  • Nagasato C, Motomura T (2002b) Ultrastructural study on mitosis and cytokinesis in Scytosiphon lomentaria zygotes (Scytosiphonales, Phaeophyceae) by freeze-substitution. Protoplasma 219:140–149

    PubMed  CAS  Google Scholar 

  • Nagasato C, Motomura T, Ichimura T (1999) Influence of centriole behavior on the first spindle formation in zygotes of the brown alga Fucus distichus (Fucales, Phaeophyceae). Dev Biol 208:200–209

    PubMed  CAS  Google Scholar 

  • Okamoto T, Scholten S, Lorz H, Kranz E (2005) Identification of genes that are up- or down-regulated in the apical or basal cell of maize two-celled embryos and monitoring their expression during zygote development by a cell manipulation- and PCR-based approach. Plant Cell Physiol 46:332–338

    PubMed  CAS  Google Scholar 

  • Otegui M, Staehelin LA (2000) Syncytial-type cell plates: a novel kind of cell plate involved in endosperm cellularization of Arabidopsis. Plant Cell 12:933–947

    PubMed  PubMed Central  CAS  Google Scholar 

  • Park SK, Rahman D, Oh SA, Twell D (2004) Gemini pollen 2, a male and female gametophytic cytokinesis defective mutation. Sex Plant Rep 17:63–70

    CAS  Google Scholar 

  • Peters AF, Marie D, Scornet D, Kloareg B, Cock JM (2004) Proposal of Ectocarpus siliculosus (Ectocarpales, Phaeophyceae) as a model organism for brown algal genetics and genomics. J Phycol 40:1079–1088

    Google Scholar 

  • Peters NT, Kropf DL (2006) Kinesin-5 motors are required for organization of spindle microtubules in Silvetia compressa zygotes. BMC Plant Biol 6:19

    PubMed  PubMed Central  Google Scholar 

  • Pickett-Heaps J, Gunning BE, Brown R, Lemmon B, Cleary A (1999) The cytoplast concept in dividing plant cells: cytoplasmic domains and the evolution of spatially organized cell. Am J Bot 86:153–172

    PubMed  CAS  Google Scholar 

  • Pu R, Robinson KR (2003) The involvement of Ca2+ gradients, Ca2+ fluxes, and CaM kinase II in polarization and germination of Silvetia compressa zygotes. Planta 217:407–416

    PubMed  CAS  Google Scholar 

  • Quatrano RS (1982) Cell-wall formation in Fucus zygotes: a model system to study the assembly and localization of wall polymers. In: Brown RM (ed) Cellulose and other natural polymer systems: biogenesis, structure, and degradation. Plenum, New York, pp 45–59

    Google Scholar 

  • Robinson KR, Miller BJ (1997) The coupling of cyclic GMP and photopolarization of Pelvetia zygotes. Dev Biol 187:125–130

    PubMed  CAS  Google Scholar 

  • Robinson KR, Lorenzi R, Ceccarelli N, Gualtieri P (1998) Retinal identification in Pelvetia fastigiata. Biochem Biophys Res Commun 243:776–778

    PubMed  CAS  Google Scholar 

  • Scheres B, Benfey P, Dolan L (2002) Root development. In: Somerville CR, Meyerowitz EM (eds) The Arabidopsis book, DOI:10.1199/tab.0101. American Society of Plant Biologists, Rockville, MD, pp 1–18

    Google Scholar 

  • Schmitt R (2003) Differentiation of germinal and somatic cells in Volvox carteri. Curr Opin Microbiol 6:608–613

    PubMed  CAS  Google Scholar 

  • Schumaker KS, Dietrich MA (1998) Hormone-induced signaling during moss development. Annu Rev Plant Phys Plant Mol Biol 49:501–523

    CAS  Google Scholar 

  • Shaw SL, Quatrano RS (1996) The role of targeted secretion in the establishment of cell polarity and the orientation of the division plane in Fucus zygotes. Development 122:2623–2630

    PubMed  CAS  Google Scholar 

  • Shevell DE, Leu W-M, Gillmor 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 Sec7. Cell 77:1051–1062

    PubMed  CAS  Google Scholar 

  • Souter M, Lindsey K (2000) Polarity and signalling in plant embryogenesis. J Exp Bot 51:971–983

    PubMed  CAS  Google Scholar 

  • Swope RE, Kropf DL (1993) Pronuclear positioning and migration during fertilization in Pelvetia. Dev Biol 157:269–276

    PubMed  CAS  Google Scholar 

  • Torres-Ruiz RA (2004) Polarity in Arabidopsis embryogenesis. In: Lindsey K (ed) Annual plant reviews, vol 12. Blackwell, Oxford, pp 157–191

    Google Scholar 

  • Torres-Ruiz R, Jurgens G (1994) Mutations in the FASS gene uncouple pattern formation and morphogenesis in Arabidopsis development. Development 120:2967–2978

    PubMed  CAS  Google Scholar 

  • Twell D, Park SK, Lalanne E (1998) Asymmetric division and cell-fate determination in developing pollen. Trends Plant Sci 3:305–310

    Google Scholar 

  • Varvarigos V, Galatis B, Katsaros C (2005) A unique pattern of F-actin organization supports cytokinesis in vacuolated cells of Macrocystis pyrifera (Phaeophyceae) gametophytes. Protoplasma 226:241–245

    PubMed  CAS  Google Scholar 

  • Wadsworth P (2005) Cytokinesis: Rho marks the spot. Curr Biol 15:R871–R874

    PubMed  CAS  Google Scholar 

  • Wasteneys GO (2002) Microtubule organization in the green kingdom: chaos or self-order? J Cell Sci 115:1345–1354

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Weterings K, Apuya NR, Bi Y, Fischer R, Harada JJ, Goldberg RB (2001) Regional localization of suspensor mRNAs during early embryo development. Plant Cell 13:2409–2425

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wu J-Q, Kuhn JR, Kovar DR, Pollard TD (2003) Spatial and temporal pathway for assembly and constriction of the contractile ring in fission yeast cytokinesis. Dev Cell 5:723–734

    PubMed  CAS  Google Scholar 

  • Zernicka-Goetz M (2004) First cell fate decisions and spatial patterning in the early mouse embryo. Semin Cell Dev Biol 15:563–572

    PubMed  CAS  Google Scholar 

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Correspondence to Sherryl R. Bisgrove .

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Bisgrove, S.R., Kropf , D.L. (2007). Asymmetric Cell Divisions: Zygotes of Fucoid Algae as a Model System. In: Verma, D.P.S., Hong, Z. (eds) Cell Division Control in Plants. Plant Cell Monographs, vol 9. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7089_2007_134

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