Brown Algae as a Model for Plant Organogenesis

  • Kenny A. Bogaert
  • Alok Arun
  • Susana M. Coelho
  • Olivier De Clerck
Part of the Methods in Molecular Biology book series (MIMB, volume 959)

Abstract

Brown algae are an extremely interesting, but surprisingly poorly explored, group of organisms. They are one of only five eukaryotic lineages to have independently evolved complex multicellularity, which they express through a wide variety of morphologies ranging from uniseriate branched filaments to complex parenchymatous thalli with multiple cell types. Despite their very distinct evolutionary history, brown algae and land plants share a striking amount of developmental features. This has led to an interest in several aspects of brown algal development, including embryogenesis, polarity, cell cycle, asymmetric cell division and a putative role for plant hormone signalling. This review describes how investigations using brown algal models have helped to increase our understanding of the processes controlling early embryo development, in particular polarization, axis formation and asymmetric cell division. Additionally, the diversity of life cycles in the brown lineage and the emergence of Ectocarpus as a powerful model organism, are affording interesting insights on the molecular mechanisms underlying haploid-diploid life cycles. The use of these and other emerging brown algal models will undoubtedly add to our knowledge on the mechanisms that regulate development in multicellular photosynthetic organisms.

Key words

Brown algae Development Polarization Asymmetric cell division Auxin Hormone Life cycle Cell cycle Fucus Ectocarpus 

References

  1. 1.
    van den Hoek C, Mann DG, Jahns HM (1995) Algae: an introduction to phycology. Cambridge University Press, Cambridge, pp. 623Google Scholar
  2. 2.
    Andersen RA (2004) Biology and systematics of heterokont and haptophyte algae. Am J Bot 91:1508–1522PubMedGoogle Scholar
  3. 3.
    Riisberg I et al (2009) Seven gene phylogeny of heterokonts. Protist 160:191–204PubMedGoogle Scholar
  4. 4.
    Khan H et al (2007) Plastid genome sequence of the cryptophyte alga Rhodomonas salina CCMP1319: lateral transfer of putative DNA replication machinery and a test of chromist plastid phylogeny. Mol Biol Evol 24:1832–1842PubMedGoogle Scholar
  5. 5.
    Sanchez-Puerta M, Delwiche CF (2007) A hypothesis for plastid evolution in chromalveolates. J Phycol 44:1097–1107Google Scholar
  6. 6.
    Wang Y, Joly S, Morse D (2008) Phylogeny of dinoflagellate plastid genes recently transferred to the nucleus supports a common ancestry with red algal plastid genes. J Mol Evol 66:175–184PubMedGoogle Scholar
  7. 7.
    Le Corguillé G et al (2009) Plastid genomes of two brown algae, Ectocarpus siliculosus and Fucus vesiculosus: further insights on the evolution of red-algal derived plastids. BMC Evol Biol 9:253PubMedGoogle Scholar
  8. 8.
    Janouskovec J et al (2010) A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proc Natl Acad Sci USA 107:10949–10954PubMedGoogle Scholar
  9. 9.
    Green BR (2011) After the primary endosymbiosis: an update on the chromalveolate hypothesis and the origins of algae with Chl c. Photosynth Res 107:103–115PubMedGoogle Scholar
  10. 10.
    Baurain D et al (2010) Phylogenomic evidence for separate acquisition of plastids in cryptophytes, haptophytes and stramenopiles. Mol Biol Evol 27:1698–1709PubMedGoogle Scholar
  11. 11.
    Cavalier-smith T (1999) Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J Eukaryot Microbiol 46:347–366PubMedGoogle Scholar
  12. 12.
    Delwiche CF (2007) Algae in the warp and weave of life: bound by plastids. In: Brodie J, Lewis J (eds) Unravelling the algae: the past, present, and future of algal systematics, pp. 7–20. Taylor and Francis: Boca Raton, FLGoogle Scholar
  13. 13.
    Yoon HS et al (2002) The single, ancient origin of chromist plastids. Proc Natl Acad Sci USA 99:15507–15512PubMedGoogle Scholar
  14. 14.
    Yoon HS et al (2004) A molecular timeline for the origin of photosynthethic eukaryotes. Mol Biol Evol 21:809–818PubMedGoogle Scholar
  15. 15.
    Elias M, Archibald JM (2009) Sizing up the genomic footprint of endosymbiosis. BioEssays 31:1273–1279PubMedGoogle Scholar
  16. 16.
    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 208:200–209PubMedGoogle Scholar
  17. 17.
    Ritter A et al (2008) Copper stress induces biosynthesis of octadecanoid and eicosanoid oxygenated derivatives in the brown algal kelp Laminaria digitata. New Phytol 180:809–821PubMedGoogle Scholar
  18. 18.
    Silberfeld T et al (2010) A multi-locus time-calibrated phylogeny of the brown algae (Heterokonta, Ochrophyta, Phaeophyceae): investigating the evolutionary nature of the “brown algal crown radiation”. Mol Phylogenet Evol 56:659–674PubMedGoogle Scholar
  19. 19.
    Kawai H et al (2003) Schizocladia ischiensis: a new filamentous marine chromophyte belonging to a new class, Schizocladiophyceae. Protist 154:211–228PubMedGoogle Scholar
  20. 20.
    Brown JW, Sorhannus U (2010) A molecular genetic timescale for the diversification of autotrophic stramenopiles (Ochrophyta): substantive underestimation of putative fossil ages. PLoS One 5:11Google Scholar
  21. 21.
    Bell G (1997) The evolution of the life cycle of brown seaweeds. Biol J Linn Soc 60:21–38Google Scholar
  22. 22.
    de Reviers B, Rousseau F, Draisma SGA (2007) Classification of the Phaeophyceae from past to present and current challenges, in Unravelling the algae: the past, present, and future of algal systematics. In: Brodie J, Lewis J (eds) The systematics association special volume series, pp. 267–284. Taylor and Francis: Boca Raton, FLGoogle Scholar
  23. 23.
    Graham M, Vásquez J (2007) Global ecology of the giant kelp Macrocystis: from ecotypes to ecosystems. Oceanogr Mar Biol 45:39–88Google Scholar
  24. 24.
    Parker BC (1965) Translocation in the giant kelp Macrocystis I. rates, direction, quantity of C14-labeled products and fluorescein. J Phycol 1:41–46Google Scholar
  25. 25.
    Parker BC, Huber J (1965) Translocation in Macrocystis. II. Fine structure of the sieve tubes. J Phycol 1:172–179Google Scholar
  26. 26.
    Peters AF, Burkhardt E (1998) Systematic position of the kelp endophyte Laminarionema elsbetiae (Ectocarpales sensu lato, Phaeophyceae) inferred from nuclear ribosomal DNA sequences. Phycologia 37:114–120Google Scholar
  27. 27.
    Burkhardt E, Peters AF (1998) Molecular evidence from nrDNA its sequences that Laminariocolax (Phaeophyceae, Ectocarpales sensu lato) is a worldwide clade of closely related kelp endophytes. J Phycol 34:682–691Google Scholar
  28. 28.
    Niklas K (2000) The evolution of plant body plans—a biomechanical perspective. Ann Bot London 85:411–438Google Scholar
  29. 29.
    Coelho SM et al (2002) Spatiotemporal patterning of reactive oxygen production and Ca2+ wave propagation in Fucus rhizoid cells. Plant Cell 14:2369–2381PubMedGoogle Scholar
  30. 30.
    Coelho SMB, Brownlee C, Bothwell JHF (2008) A tip-high, Ca(2+)-interdependent, reactive oxygen species gradient is associated with polarized growth in Fucus serratus zygotes. Planta 227:1037–1046PubMedGoogle Scholar
  31. 31.
    Peters AF et al (2008) Life-cycle-generation-specific developmental processes are modified in the immediate upright mutant of the brown alga Ectocarpus siliculosus. Development 135:1503–1512PubMedGoogle Scholar
  32. 32.
    Bisgrove SR (2007) Cytoskeleton and early development in fucoid algae. J Integr Plant Biol 49:1192–1198Google Scholar
  33. 33.
    Hable WE, Hart PE (2010) Signaling mechanisms in the establishment of plant and fucoid algal polarity. Mol Reprod Dev 77:751–758PubMedGoogle Scholar
  34. 34.
    Coelho SM et al (2007) Complex life cycles of multicellular eukaryotes: new approaches based on the use of model organisms. Gene 406:152–170PubMedGoogle Scholar
  35. 35.
    Coelho SM et al (2011) OUROBOROS is a master regulator of the gametophyte to sporophyte life cycle transition in the brown alga Ectocarpus. Proc Natl Acad Sci USA 108:11518–11523PubMedGoogle Scholar
  36. 36.
    Cock JM et al (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465:617–621PubMedGoogle Scholar
  37. 37.
    Dittami SM et al (2009) Global expression analysis of the brown alga Ectocarpus siliculosus (Phaeophyceae) reveals large-scale reprogramming of the transcriptome in response to abiotic stress. Genome Biol 10:R66PubMedGoogle Scholar
  38. 38.
    Heesch S et al (2010) A sequence-tagged genetic map for the brown alga Ectocarpus siliculosus provides large-scale assembly of the genome sequence. New Phytol 188:42–51PubMedGoogle Scholar
  39. 39.
    Gschloessl B, Guermeur Y, Cock JM (2008) HECTAR: a method to predict subcellular targeting in heterokonts. BMC Bioinformatics 9:393PubMedGoogle Scholar
  40. 40.
    Ritter A et al (2010) Copper stress proteomics highlights local adaptation of two strains of the model brown alga Ectocarpus siliculosus. Proteomics 10:2074–2088PubMedGoogle Scholar
  41. 41.
    Lau S et al (2009) Auxin signaling in algal lineages: fact or myth? Trends Plant Sci 14:182–188PubMedGoogle Scholar
  42. 42.
    Cho GY, Lee SH, Boo SM (2004) A new brown algal order, Ishigeales (Phaeophyceae), established on the basis of plastid protein-coding rbcL, psaA, and psbA region comparisons. J Phycol 40:921–936Google Scholar
  43. 43.
    Kawai H et al (2007) Molecular phylogeny of Discosporangium mesarthrocarpum (Phaeophyceae) with a reinstatement of the Order Discosporangiales. J Phycol 43:186–194Google Scholar
  44. 44.
    Peters AF, Ramirez ME (2001) Molecular phylogeny of small brown algae, with special reference to the systematic position of Caepidium antarcticum (Adenocystaceae, Ectocarpales). Cryptogamie Algol 22:187–200Google Scholar
  45. 45.
    Bothwell JH et al (2010) Role of endoreduplication and apomeiosis during parthenogenetic reproduction in the model brown alga Ectocarpus. New Phytol. 188:111–21 doi:10.1111/j.1469-8137.2010.03357.x
  46. 46.
    John PCL, Qi R (2008) Cell division and endoreduplication: doubtful engines of vegetative growth. Trends Plant Sci 13:121–127PubMedGoogle Scholar
  47. 47.
    Müller DG (1967) Generationswechsel, Kernphasenwechsel und Sexualität der Braunalge Ectocarpus siliculosus im Kulturversuch. Planta 75:39–54Google Scholar
  48. 48.
    Cheung AY, Wu H-M (2008) Structural and signaling networks for the polar cell growth machinery in pollen tubes. Annu Rev Plant Biol 59:547–572PubMedGoogle Scholar
  49. 49.
    Xu T et al (2010) Cell surface- and Rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143:99–110PubMedGoogle Scholar
  50. 50.
    Szymanski DB (2009) Plant cells taking shape: new insights into cytoplasmic control. Curr Opin Plant Biol 12:735–744PubMedGoogle Scholar
  51. 51.
    Young RE et al (2008) Analysis of the Golgi apparatus in Arabidopsis seed coat cells during polarized secretion of pectin-rich mucilage. Plant Cell 20:1623–1638PubMedGoogle Scholar
  52. 52.
    Li L, Saga N, Mikami K (2008) Phosphatidylinositol 3-kinase activity and asymmetrical accumulation of F-actin are necessary for establishment of cell polarity in the early development of monospores from the marine red alga Porphyra yezoensis. J Exp Bot 59:3575–3586PubMedGoogle Scholar
  53. 53.
    Dhonukshe P et al (2008) Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. Nature 456:962–966PubMedGoogle Scholar
  54. 54.
    Rosenvinge MLK (1889) Influence des agents extérieurs sur l’organisation polaire dorsiventrale des plantes. Rev Gen Bot 1:135Google Scholar
  55. 55.
    Farmer JB, Williams LJ, Scott DH (1898) Contributions to our knowledge of the Fucaceae: their life history and cytology. Philos Trans R Soc B 190:623–645Google Scholar
  56. 56.
    Corellou F et al (2000) 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 127:1651–1660PubMedGoogle Scholar
  57. 57.
    Yang Z (2008) Cell polarity signaling in Arabidopsis. Annu Rev Cell Dev Bi 24:551–575Google Scholar
  58. 58.
    Kropf DL (1992) Establishment and expression of cellular polarity in fucoid zygotes. Microbiol Rev 56:316–339PubMedGoogle Scholar
  59. 59.
    Paciorek T, Bergmann DC (2010) The secret to life is being different: asymmetric divisions in plant development. Curr Opin Plant Biol 13:1–9Google Scholar
  60. 60.
    Brownlee C, Wood J (1986) A gradient of cytoplasmic free calcium a in growing rhizoid cells of Fucus serratus. Nature 320:624–626Google Scholar
  61. 61.
    Hepler PK (2005) Calcium: a central regulator of plant growth and development. Plant Cell 17:2142–2155PubMedGoogle Scholar
  62. 62.
    Kropf D (1994) Cytoskeletal control of cell polarity in a plant zygote. Dev Biol 165:361–371PubMedGoogle Scholar
  63. 63.
    Fowler JE, Quatrano RS (1997) Plant cell morphogenesis: plasma membrane interactions with the cytoskeleton and cell wall. Annu Rev Cell Dev Biol 13:697–743PubMedGoogle Scholar
  64. 64.
    Berger F, Taylor A, Brownlee C (1994) Cell fate determination by the cell wall in early Fucus development. Science 263:1421–1423PubMedGoogle Scholar
  65. 65.
    Belanger KD, Quatrano RS (2000) Polarity: the role of localized secretion. Curr Opin Plant Biol 3:67–72PubMedGoogle Scholar
  66. 66.
    Brownlee C (1994) Tansley review no. 70 signal transduction during fertilization in algae and vascular plants. New Phytol 127:399–423Google Scholar
  67. 67.
    Dumas C, Gaude T (2006) Fertilization in plants: is calcium a key player? Semin Cell Dev Biol 17:244–253PubMedGoogle Scholar
  68. 68.
    Knoblich JA (2001) Asymmetric cell division during animal development. Nat Rev Mol Cell Bio 2:11–20Google Scholar
  69. 69.
    Knoblich JA (2008) Mechanisms of asymmetric stem cell division. Cell 132:583–597PubMedGoogle Scholar
  70. 70.
    Knapp E (1932) Entwicklungsphysiologische Untersuchungen an Fucaceen-Eiern I. Zur Kenntnis der Polarität der Eier von Cystosira barbata. Planta 14:731–751Google Scholar
  71. 71.
    Hable WE, Kropf DL (2000) Sperm entry induces polarity in fucoid zygotes. Development 127:493–501PubMedGoogle Scholar
  72. 72.
    Hurd AM (1920) Effect of unilateral monochromatic light and group orientation on the polarity of germinating Fucus spores. Bot Gaz 70:25–50Google Scholar
  73. 73.
    Bentrup F, Sandan T, Jaffe L (1967) Induction of polarity in Fucus eggs by potassium ion gradients. Protoplasma 64:254–266Google Scholar
  74. 74.
    Bentrup FW, Jaffe LF (1968) Analyzing the “Group effect”: rheotropic responses of developing Fucus eggs. Protoplasma 65:25–35PubMedGoogle Scholar
  75. 75.
    Novak B, Bentrup FW (1973) Orientation of Fucus egg polarity by electric a. c. and d. c. fields. Biophysik 9:253–260PubMedGoogle Scholar
  76. 76.
    Love J, Brownlee C, Trewavas AJ (1997) Ca2+ and calmodulin dynamics during photopolarization in Fucus serratus zygotes. Plant Physiol 115:249–261PubMedGoogle Scholar
  77. 77.
    Sun H et al (2004) Interactions between auxin transport and the actin cytoskeleton in developmental polarity of Fucus distichus embryos in response to light and gravity. Plant Physiol 135:266–278PubMedGoogle Scholar
  78. 78.
    Bouget F-Y, Gertula S, Quatrano RS (1995) Spatial distribution of poly(A) RNA during polarization of Fucus zygotes is dependent upon microfilaments. Dev Biol 171:258–261PubMedGoogle Scholar
  79. 79.
    Bouget FY et al (1996) Localization of actin mRNA during the establishment of cell polarity and early cell divisions in Fucus embryos. Plant Cell 8:189–201PubMedGoogle Scholar
  80. 80.
    Hadley R, Hable WE, Kropf DL (2006) Polarization of the endomembrane system is an early event in fucoid zygote development. BMC Plant Biol 6:5PubMedGoogle Scholar
  81. 81.
    Shaw SL, Quatrano RS (1996) Polar localization of a dihydropyridine receptor on living Fucus zygotes. J Cell Sci 109:335–342PubMedGoogle Scholar
  82. 82.
    Berger F, Brownlee C (1993) Ratio confocal imaging of free cytoplasmic calcium gradients in polarising and polarised Fucus zygotes. Zygote 1:9–15PubMedGoogle Scholar
  83. 83.
    Wagner VT, Brian L, Quatrano RS (1992) Role of a vitronectin-like molecule in embryo adhesion of the brown alga Fucus. Proc Natl Acad Sci USA 89:3644–3648PubMedGoogle Scholar
  84. 84.
    De Smet I, Beeckman T (2011) Asymmetric cell division in land plants and algae: the driving force for differentiation. Nat Rev Mol Cell Biol 12:177–188PubMedGoogle Scholar
  85. 85.
    Abrash EB, Bergmann DC (2009) Asymmetric cell divisions: a view from plant development. Dev Cell 16:783–796PubMedGoogle Scholar
  86. 86.
    Yamashita YM et al (2007) Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science 315:518–521PubMedGoogle Scholar
  87. 87.
    De Smet I et al (2009) Receptor-like kinases shape the plant. Nat Cell Biol 11:1166–1173PubMedGoogle Scholar
  88. 88.
    Gualtieri P, Robinson KR (2002) A rhodopsin-like protein in the plasma membrane of Silvetia compressa eggs. Photochem Photobiol 75:76–78PubMedGoogle Scholar
  89. 89.
    Robinson KR, Miller BJ (1997) The coupling of cyclic GMP and photopolarization of Pelvetia zygotes. Dev Biol 187:125–130PubMedGoogle Scholar
  90. 90.
    Berger F, Brownlee C (1994) Photopolarization of the Fucus sp. zygote by blue light involves a plasma membrane redox chain. Plant Physiol 105:519–527PubMedGoogle Scholar
  91. 91.
    Kropf D, Bisgrove S, Hable W (1999) Establishing a growth axis in fucoid algae. Trends Plant Sci 4:490–494PubMedGoogle Scholar
  92. 92.
    Robinson K et al (1999) Symmetry breaking in the zygotes of the fucoid algae: controversies and recent progress. Curr Top Dev Biol 44:101–125PubMedGoogle Scholar
  93. 93.
    Jaffe LF, Robinson KR, Nuccitelli R (1974) Local cation entry and self-electrophoresis as an intracellular localization mechanism. Ann NY Acad Sci 238:372–389PubMedGoogle Scholar
  94. 94.
    Nuccitelli R, Jaffe LF (1974) Spontaneous current pulses through developing fucoid eggs. Proc Natl Acad Sci USA 71:4855–4859PubMedGoogle Scholar
  95. 95.
    Nuccitelli R, Jaffe LF (1976) The ionic components of the current pulses generated by developing fucoid eggs. Dev Biol 49:518–531PubMedGoogle Scholar
  96. 96.
    Jaffe LF (1999) Organization of early development by calcium patterns. BioEssays 21:657–667PubMedGoogle Scholar
  97. 97.
    Robinson K, Jaffe L (1975) Polarizing fucoid eggs drive a calcium current through themselves. Science 187:70–72PubMedGoogle Scholar
  98. 98.
    Robinson KR, Cone R (1980) Polarization of fucoid eggs by a calcium ionophore gradient. Science 207:77–78PubMedGoogle Scholar
  99. 99.
    Brownlee C, Pulsford AL (1988) Visualization of the cytoplasmic Ca2+ gradient in Fucus serratus rhizoids: correlation with cell ultrastructure and polarity. J Cell Sci 91:249–256Google Scholar
  100. 100.
    Speksnijder JE et al (1989) Calcium buffer injections block fucoid egg development by facilitating calcium diffusion. Proc Natl Acad Sci USA 86:6607–6611PubMedGoogle Scholar
  101. 101.
    Pu R, Robinson KR (1998) Cytoplasmic calcium gradients and calmodulin in the early development of the fucoid alga Pelvetia compressa. J Cell Sci 111:3197–3207PubMedGoogle Scholar
  102. 102.
    Taylor AR et al (1996) Spatial organization of calcium signaling involved in cell volume control in the Fucus rhizoid. Plant Cell 8:2015–2031PubMedGoogle Scholar
  103. 103.
    Taylor A, Brownlee C (1993) Calcium and potassium currents in the Fucus egg. Planta 189:109–119Google Scholar
  104. 104.
    Nuccitelli R, Jaffe LF (1976) The ionic components of the current pulses generated by developing fucoid eggs. Dev Biol 49:518–531PubMedGoogle Scholar
  105. 105.
    Robinson K (1996) Calcium and the photopolarization of Pelvetia zygotes. Planta 198:378–384Google Scholar
  106. 106.
    Pu R, Wozniak M, Robinson KR (2000) Cortical actin filaments form rapidly during photopolarization and are required for the development of calcium gradients in Pelvetia compressa zygotes. Dev Biol 222:440–449PubMedGoogle Scholar
  107. 107.
    Taylor A, Roberts S, Brownlee C (1992) Calcium and related channels in fertilization and early development of Fucus. Philos Trans R Soc B 338:97–104Google Scholar
  108. 108.
    Brownlee C, Bouget FY, Corellou F (2001) Choosing sides: establishment of polarity in zygotes of fucoid algae. Semin Cell Dev Biol 12:345–351PubMedGoogle Scholar
  109. 109.
    Hable W, Kropf D (1998) Roles of secretion and the cytoskeleton in cell adhesion and polarity establishment in zygotes. Dev Biol 198:45–56PubMedGoogle Scholar
  110. 110.
    Alessa L, Kropf DL (1999) F-actin marks the rhizoid pole in living Pelvetia compressa zygotes. Development 126:201–209PubMedGoogle Scholar
  111. 111.
    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 122:2623–2630PubMedGoogle Scholar
  112. 112.
    Bothwell JHF et al (2006) Biolistic delivery of Ca2+ dyes into plant and algal cells. Plant J 46:327–335PubMedGoogle Scholar
  113. 113.
    Bisgrove S (2007) Asymmetric cell divisions: zygotes of fucoid algae as a model system. Plant Cell Monogr 9:323–341Google Scholar
  114. 114.
    Hable WE, Kropf DL (2005) The Arp2/3 complex nucleates actin arrays during zygote polarity establishment and growth. Cell Motil Cytoskel 61:9–20Google Scholar
  115. 115.
    Varvarigos V, Galatis B, Katsaros C (2007) Radial endoplasmic reticulum arrays co-localize with radial F-actin in polarizing cells of brown algae. Eur J Phycol 42:253–262Google Scholar
  116. 116.
    Katsaros C, Karyophyllis D, Galatis B (2006) Cytoskeleton and morphogenesis in brown algae. Ann Bot London 97:679–693Google Scholar
  117. 117.
    Panteris E, Apostolakos P, Galatis B (2006) Cytoskeletal asymmetry in Zea mays subsidiary cell mother cells: a monopolar prophase microtubule half-spindle anchors the nucleus to its polar position. Cell Motil Cytoskel 63:696–709Google Scholar
  118. 118.
    Baluska F et al (2000) Root hair formation: F-actin-dependent tip growth is initiated by local assembly of profilin-supported F-actin meshworks accumulated within expansin-enriched bulges. Dev Biol 227:618–632PubMedGoogle Scholar
  119. 119.
    Fu Y et al (2005) Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell 120:687–700PubMedGoogle Scholar
  120. 120.
    Mathur J et al (2003) Mutations in actin-related proteins 2 and 3 affect cell shape development in Arabidopsis. Plant Cell 15:1632–1645PubMedGoogle Scholar
  121. 121.
    Fu Y, Wu G, Yang Z (2001) Rop GTPase-dependent dynamics of tip-localized F-actin controls tip growth in pollen tubes. J Cell Biol 152:1019–1032PubMedGoogle Scholar
  122. 122.
    Gu Y et al (2005) A Rho family GTPase controls actin dynamics and tip growth via two counteracting downstream pathways in pollen tubes. J Cell Biol 169:127–138PubMedGoogle Scholar
  123. 123.
    Brembu T et al (2006) A RHOse by any other name: a comparative analysis of animal and plant Rho GTPases. Cell Res 16:435–445PubMedGoogle Scholar
  124. 124.
    Perez P, Rincón SA (2010) Rho GTPases: regulation of cell polarity and growth in yeasts. Biochemical J 426:243–253Google Scholar
  125. 125.
    Fowler JE et al (2004) Localization to the rhizoid tip implicates a Fucus distichus Rho family GTPase in a conserved cell polarity pathway. Planta 219:856–866PubMedGoogle Scholar
  126. 126.
    Hable WE, Reddy S, Julien L (2008) The Rac1 inhibitor, NSC23766, depolarizes adhesive secretion, endomembrane cycling, and tip growth in the fucoid alga, Silvetia compressa. Planta 227:991–1000PubMedGoogle Scholar
  127. 127.
    Hamant O, Traas J (2010) The mechanics behind plant development. New Phytol 185:369–385PubMedGoogle Scholar
  128. 128.
    Kropf DL, Bisgrove SR, Hable WE (1998) Cytoskeletal control of polar growth in plant cells. Curr Opin Cell Biol 10:117–122PubMedGoogle Scholar
  129. 129.
    Katsaros C, Reiss HD, Schnepf E (1996) Freeze-fracture studies in brown algae: putative cellulose-synthesizing complexes on the plasma membrane. Eur J Phycol 31:41–48Google Scholar
  130. 130.
    Schubetaler A, Hirn S, Katsaros C (2003) Cellulose synthesizing terminal complexes and morphogenesis in tip-growing cells of Syringoderma phinneyi (Phaeophyceae). Phycol Res 51:35–44Google Scholar
  131. 131.
    Michel G et al (2010) The cell wall polysaccharide metabolism of the brown alga Ectocarpus siliculosus. Insights into the evolution of extracellular matrix polysaccharides in Eukaryotes. New Phytol 188:82–97PubMedGoogle Scholar
  132. 132.
    Katsaros C (2003) F-actin cytoskeleton and cell wall morphogenesis in brown algae. Cell Biol Int 27:209–210PubMedGoogle Scholar
  133. 133.
    Karyophyllis D, Katsaros C, Dimitriadis I (2000) F-actin organization during the cell cycle of Sphacelaria rigidula (Phaeophyceae). Eur J Phycol 35:25–33Google Scholar
  134. 134.
    Bisgrove SR, Kropf DL (2001) Cell wall deposition during morphogenesis in fucoid algae. Planta 212:648–658PubMedGoogle Scholar
  135. 135.
    Motomura T (1994) Electron and immunofluorescence microscopy on the fertilization of Fucus distichus (Fucales, Phaeophyceae). Protoplasma 178:97–110Google Scholar
  136. 136.
    Corellou F et al (2005) Spatial re-organisation of cortical microtubules in vivo during polarisation and asymmetric division of Fucus zygotes. J Cell Sci 118:2723–2734PubMedGoogle Scholar
  137. 137.
    Peters NT, Kropf DL (2010) Asymmetric microtubule arrays organize the endoplasmic reticulum during polarity establishment in the brown alga Silvetia compressa. Cytoskeleton 67:102–111PubMedGoogle Scholar
  138. 138.
    Sieberer BJ et al (2005) Microtubules guide root hair tip growth. New Phytol 167:711–719PubMedGoogle Scholar
  139. 139.
    Peters NT et al (2007) Phospholipase D signaling regulates microtubule organization in the fucoid alga Silvetia compressa. Plant Cell Physiol 48:1764–1774PubMedGoogle Scholar
  140. 140.
    Shimamura M et al (2004) Gamma-tubulin in basal land plants: characterization, localization, and implication in the evolution of acentriolar microtubule organizing centers. Plant Cell 16:45–59PubMedGoogle Scholar
  141. 141.
    McCarthy EK, Goldstein B (2006) Asymmetric spindle positioning. Curr Opin Cell Biol 18:79–85PubMedGoogle Scholar
  142. 142.
    Yamashita YM, Fuller MT (2008) Asymmetric centrosome behavior and the mechanisms of stem cell division. J Cell Biol 180:261–266PubMedGoogle Scholar
  143. 143.
    Van Damme D (2009) Division plane determination during plant somatic cytokinesis. Curr Opin Plant Biol 12:745–751PubMedGoogle Scholar
  144. 144.
    Nagasato C, Motomura T (2002) Influence of the centrosome in cytokinesis of brown algae: polyspermic zygotes of Scytosiphon lomentaria (Scytosiphonales, Phaeophyceae). J Cell Sci 115:2541–2548PubMedGoogle Scholar
  145. 145.
    Bisgrove S, Henderson D, Kropf D (2003) Asymmetric division in fucoid zygotes is positioned by telophase nuclei. Plant Cell 15:854–862PubMedGoogle Scholar
  146. 146.
    Katsaros C (1992) Immunofluorescence study of microtubule organization in some polarized cell types of selected brown algae. Bot Acta 105:400–406Google Scholar
  147. 147.
    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 226:241–245PubMedGoogle Scholar
  148. 148.
    Panteris E et al (2004) A cortical cytoplasmic ring predicts the division plane in vacuolated cells of Coleus: the role of actomyosin and microtubules in the establishment and function of the division site. New Phytol 163:271–286Google Scholar
  149. 149.
    Müller S, Wright AJ, Smith LG (2009) Division plane control in plants: new players in the band. Trends Cell Biol 19:180–188PubMedGoogle Scholar
  150. 150.
    Oh SA et al (2010) The tobacco MAP215/Dis1-family protein TMBP200 is required for the functional organization of microtubule arrays during male germline establishment. J Exp Bot 61:969–981PubMedGoogle Scholar
  151. 151.
    Doonan JH, Cove DJ, Lloyd CW (1985) Immunofluorescence microscopy of microtubules in intact cell lineages of the moss, Physcomitrella patens. I. Normal and CIPC-treated tip cells. J Cell Sci 75:131–147PubMedGoogle Scholar
  152. 152.
    Lloyd C, Chan J (2006) Not so divided: the common basis of plant and animal cell division. Nat Rev Mol Cell Biol 7:147–152PubMedGoogle Scholar
  153. 153.
    Dhonukshe P, Vischer N, Gadella TWJ (2006) Contribution of microtubule growth polarity and flux to spindle assembly and functioning in plant cells. J Cell Sci 119:3193–3205PubMedGoogle Scholar
  154. 154.
    Chan J et al (2005) Localization of the microtubule end binding protein EB1 reveals alternative pathways of spindle development in Arabidopsis suspension cells. Development 17:1737–1748Google Scholar
  155. 155.
    Katsaros C et al (2009) Diaphragm development in cytokinetic vegetative cells of brown algae. Bot Mar 52:150–161Google Scholar
  156. 156.
    Nagasato C et al (2010) Membrane fusion process and assembly of cell wall during cytokinesis in the brown alga, Silvetia babingtonii (Fucales, Phaeophyceae). Planta 232:287–298PubMedGoogle Scholar
  157. 157.
    Bisgrove SR, Kropf DL (2004) Cytokinesis in brown algae: studies of asymmetric division in fucoid zygotes. Protoplasma 223:163–173PubMedGoogle Scholar
  158. 158.
    Motomura T, Nagasato C, Kimura K (2010) Cytoplasmic inheritance of organelles in brown algae. J Plant Res 123:185–192PubMedGoogle Scholar
  159. 159.
    Fowler J, Quatrano R (1995) Cell polarity, asymmetric division, and cell fate determination in brown algal zygotes. Semin Dev Biol 6:347–358Google Scholar
  160. 160.
    Kropf D, Kloareg B, Quatrano R (1988) Cell wall is required for fixation of the embryonic axis in Fucus zygotes. Science 239:187–190PubMedGoogle Scholar
  161. 161.
    Kropf DL, Coffman HR, Kloareg B, Glenn P, Allen VW (1993) Cell wall and rhizoid polarity in Pelvetia embryos. Dev Biol 160:303–314PubMedGoogle Scholar
  162. 162.
    Rusig AM, Guyader H, Ducreux G (1993) Microtubule organization in the apical cell of Sphacelaria (Phaeophyceae) and its related protoplast. Hydrobiologia 260–261:167–172Google Scholar
  163. 163.
    Scheres B, Benfey PN (1999) Asymmetric cell division in plants. Annu Rev Plant Phys 50:505–537Google Scholar
  164. 164.
    Dong J, MacAlister CA, Bergmann DC (2009) BASL controls asymmetric cell division in Arabidopsis. Cell 137:1320–1330PubMedGoogle Scholar
  165. 165.
    Cartwright HN, Humphries JA, Smith LG (2009) PAN1: a receptor-like protein that promotes polarization of an asymmetric cell division in maize. Science 323:649–651PubMedGoogle Scholar
  166. 166.
    Muday GK (2001) Maintenance of asymmetric cellular localization of an auxin transport protein through actin cytoskeleton. J Plant Growth Regul 19:385–396Google Scholar
  167. 167.
    He Y-C et al (2007) Tobacco zygotic embryogenesis in vitro: the original cell wall of the zygote is essential for maintenance of cell polarity, the apical-basal axis and typical suspensor formation. Plant J 49:515–527PubMedGoogle Scholar
  168. 168.
    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 57:2061–2074PubMedGoogle Scholar
  169. 169.
    De Schutter K et al (2007) Arabidopsis WEE1 kinase controls cell cycle arrest in response to activation of the DNA integrity checkpoint. Plant Cell 19:211–225PubMedGoogle Scholar
  170. 170.
    Corellou F et al (2001) Cell cycle in the Fucus zygote parallels a somatic cell cycle but displays a unique translational regulation of cyclin-dependent kinases. Plant Cell 13:585–598PubMedGoogle Scholar
  171. 171.
    Bothwell JHF et al (2008) Ca2+ signals coordinate zygotic polarization and cell cycle progression in the brown alga Fucus serratus. Development 135:2173–2181PubMedGoogle Scholar
  172. 172.
    Kishimoto T (1988) Metaphase by a maturation-promoting factor. Dev Growth Differ 30:105–115Google Scholar
  173. 173.
    Arion D, Meijer L (1989) M-phase-specific protein kinase from mitotic sea urchin eggs: cyclic activation depends on protein synthesis and phosphorylation but does not require DNA or RNA synthesis. Exp Cell Res 183:361–375PubMedGoogle Scholar
  174. 174.
    Budirahardja Y, Gönczy P (2009) Coupling the cell cycle to development. Development 136:2861–2872PubMedGoogle Scholar
  175. 175.
    van den Berg C et al (1995) Cell fate in the Arabidopsis root meristem determined by directional signalling. Nature 378:62–65PubMedGoogle Scholar
  176. 176.
    Jaeger J, Irons D, Monk N (2008) Regulative feedback in pattern formation: towards a general relativistic theory of positional information. Development 135:3175–3183PubMedGoogle Scholar
  177. 177.
    Bhalerao RP, Bennett MJ (2003) The case for morphogens in plants. Nat Cell Biol 5:939–943PubMedGoogle Scholar
  178. 178.
    Katsaros CI (1995) Apical cells of brown algae with particular reference to Sphacelariales, Dictyotales and Fucales. Phycol Res 43:43–59Google Scholar
  179. 179.
    Gaillard J, L’Hardy-Halos MT (1984) Morphogenesis of Dictyota dichotoma (Huds.) Lamouroux (Phaeophyceae, Dictyotales). Ann Sci Nat Bot Biol 6:111–133Google Scholar
  180. 180.
    Bouget FY, Berger F, Brownlee C (1998) Position dependent control of cell fate in the Fucus embryo: role of intercellular communication. Development 125:1999–2008PubMedGoogle Scholar
  181. 181.
    Augier H (1976) Les hormones des algues. Etat actuel des connaissances. I-Recherche et tentatives d’identification des auxines. Bot Mar 19:127–144Google Scholar
  182. 182.
    Augier H (1976) Les hormones des algues. Etat actuel des connaissances. II—Recherche et tentatives d’identification des gibbérellines, des cytokinines et de diverses autres substances de nature hormonale. Bot Mar 19:245–254Google Scholar
  183. 183.
    Augier H (1976) Les hormones des algues. Etat actuel des connaissances. III-Rôle des hormones dans les modalités de croissance et de développement des thalles. Bot Mar 19:351–378Google Scholar
  184. 184.
    Augier H (1977) Les hormones des algues. Etat actuel des connaissances. IV—Rôle des hormones dans les divers métabolismes cellulaires et dans les mécanismes de reproduction sexuée et asexuée; rôle écologique. Bot Mar 20:1–12Google Scholar
  185. 185.
    Augier H (1977) Les hormones des algues. Etat actuel des connaissances. V-Index alphabétique par espèces des travaux de caractérisation des hormones endogènes. Bot Mar 20:187–204Google Scholar
  186. 186.
    Augier H (1977) Les hormones des algues. Etat actuel des connaissances. VI-Index alphabétique par espéces des travaux sur le rôle des hormones dans la vie des algues. Bot Mar 20:363–380Google Scholar
  187. 187.
    Augier H (1978) Les hormones des algues. Etat actuel des connaissances. Vll-Applications, conclusion, bibliographie. Bot Mar 21:175–197Google Scholar
  188. 188.
    Evans LV, Trewavas AJ (1991) Is algal development controlled by plant growth substances? J Phycol 21:322–326Google Scholar
  189. 189.
    Basu S et al (2002) Early embryo development in Fucus distichus is auxin sensitive. Plant Physiol 130:292PubMedGoogle Scholar
  190. 190.
    Stirk W, Novák O, Hradecká V (2009) Auxins and abscisic acid in Ulva fasciata (Chlorophyta) and Dictyota humifusa (Phaeophyta): towards understanding their biosynthesis and homoeostasis. Eur J Phycol 44:231–240Google Scholar
  191. 191.
    Bertilsson L, Palmer L (1972) Indole-3-acetic acid in-human cerebrospinal fluid identification and quantification by mass fragmentography. Science 177:74–76PubMedGoogle Scholar
  192. 192.
    Fries L (1977) Growth regulating effects of phenylacetic acid and p-hydroxy phenylacetic acid on Fucus spiralis L. (Pheophyta, Fucales) in axenic culture. Phycologia 16:451–455Google Scholar
  193. 193.
    Fries L (1988) Ascophyllum nodosum (Phaeophyta) in axenic culture and its response to the endophytic fungus Mycosphaerella ascophylli and epiphytic bacteria. J Phycol 24:333–337Google Scholar
  194. 194.
    Simon S, Petrášek J (2011) Why plants need more than one type of auxin. Plant Sci 180:454–460PubMedGoogle Scholar
  195. 195.
    Novotny AM, Forman M (1974) The relationship between changes in cell wall composition and the establishment of polarity in Fucus embryos. Dev Biol 40:162–173PubMedGoogle Scholar
  196. 196.
    Corellou F et al (2000) Inhibition of the establishment of zygotic polarity by protein tyrosine kinase inhibitors leads to an alteration of embryo pattern in Fucus. Dev Biol 219:165–182PubMedGoogle Scholar
  197. 197.
    Bouget F-Y, Corellou F, Kropf DL (2001) Fucoid algae as model organisms for investigating early embryogenesis. Cah Biol Mar 42:101–107Google Scholar
  198. 198.
    Le Bail A et al (2010) Auxin metabolism and function in the multicellular brown alga Ectocarpus siliculosus. Plant Physiol 153:128–144PubMedGoogle Scholar
  199. 199.
    Cooke TJ et al (2002) Evolutionary patterns in auxin action. Plant Mol Biol 49:319–338PubMedGoogle Scholar
  200. 200.
    Niklas KJ, Kutschera U (2009) The evolutionary development of plant body plans. Funct Plant Biol 36:682–695Google Scholar
  201. 201.
    De Smet I et al (2010) Unraveling the evolution of auxin signaling. Plant Physiol 155:209–221PubMedGoogle Scholar
  202. 202.
    Matsuzaki M et al (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653–657PubMedGoogle Scholar
  203. 203.
    Nozaki et al (2007) A 100%-complete sequence reveals unusually simple genomic features in the hot-spring red alga Cyanidioschyzon merolae. BMC Biol 5:28PubMedGoogle Scholar
  204. 204.
    Rensing SA et al (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–69PubMedGoogle Scholar
  205. 205.
    Paciorek T et al (2005) Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435:1251–1256PubMedGoogle Scholar
  206. 206.
    McLachlan J, Chen LC, Edelstein T (1971) The culture of four species of Fucus under laboratory conditions. Can J Bot 49:1463–1469Google Scholar
  207. 207.
    Waaland JR, Stiller JW, Cheney DP (2004) Macroalgal candidates for genomics. J Phycol 40:26–33Google Scholar
  208. 208.
    Schreiber E (1935) Über Kultur und Geschlechtsbestimmung von Dictyota dichotoma. Planta 24:266–275Google Scholar
  209. 209.
    Müller D (1962) Über jahres- und lunarperiodische Ersheinungen bei einigen Braunalgen. Bot Mar 4:140–155Google Scholar
  210. 210.
    Bittner L et al (2008) Molecular phylogeny of the Dictyotales and their position within the Phaeophyceae, based on nuclear, plastid and mitochondrial DNA sequence data. Mol Phylogenet Evol 49:211–226PubMedGoogle Scholar
  211. 211.
    Dorrell RG, Smith AG (2011) Do red and green make brown? Perspectives on plastid acquisitions within chromalveolates. Eukaryot Cell 10:856–868PubMedGoogle Scholar
  212. 212.
    Hampl V et al (2009) Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic “supergroups”. Proc Natl Acad Sci USA 106:3859–3864PubMedGoogle Scholar
  213. 213.
    Burki F et al (2007) Phylogenomics reshuffles the eukaryotic supergroups. PLoS One 2:e790PubMedGoogle Scholar
  214. 214.
    Burki F, Shalchian-Tabrizi K, Pawlowski J (2008) Phylogenomics reveals a new “megagroup” including most photosynthetic eukaryotes. Biol Lett 4:366–369PubMedGoogle Scholar
  215. 215.
    Burki F et al (2009) Large-scale phylogenomic analyses reveal that two enigmatic protist lineages, telonemia and centroheliozoa, are related to photosynthetic chromalveolates. Genome Biol Evol 1:231–238PubMedGoogle Scholar
  216. 216.
    Koonin EV (2010) The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol 11:209PubMedGoogle Scholar
  217. 217.
    Patron NJ, Inagaki Y, Keeling PJ (2007) Multiple gene phylogenies support the monophyly of cryptomonad and haptophyte host lineages. Curr Biol 17:887–891PubMedGoogle Scholar
  218. 218.
    Evans LV, Callow JA, Callow M (1982) The biology and biochemistry of reproduction and early development in Fucus. In: Round FE, Chapman DJ (eds) Progress in phycological research, 1st edn, pp. 68–110. Elsevier, AmsterdamGoogle Scholar
  219. 219.
    De Clerck O (2003) The genus Dictyota in the Indian Ocean. Opera Botanica Belgica 13: 1–205Google Scholar
  220. 220.
    Bartsch I et al (2008) The genus Laminaria sensu lato: recent insights and developments. Eur J Phycol 43:1–86Google Scholar
  221. 221.
    Parente M, Neto A (2003) Morphology and life history of Scytosiphon lomentaria (Scytosiphonaceae, Phaeophyceae) from the Azores. J Phycol 39:353–359Google Scholar
  222. 222.
    Tatarenkov A et al (2005) Intriguing asexual life in marginal populations of the brown seaweed Fucus vesiculosus. Mol Ecol 14:647–651PubMedGoogle Scholar
  223. 223.
    Hwang I-K, Kim H-S, Lee WJ (2005) Polymorphism in the brown alga Dictyota dichotoma (Dictyotales, Phaeophyceae) from Korea. Mar Biol 147:999–1015Google Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Kenny A. Bogaert
    • 1
  • Alok Arun
    • 2
    • 3
  • Susana M. Coelho
    • 2
    • 4
  • Olivier De Clerck
    • 1
  1. 1.Phycology Research Group, Department of Biology, Center for Molecular Phylogenetics and EvolutionGhent UniversityGhentBelgium
  2. 2.Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7139, Laboratoire International Associé Dispersal and Adaptation in Marine Species, Station Biologique de RoscoffRoscoff CedexFrance
  3. 3.Laboratoire International Associé Dispersal and Adaptation in Marine Species, CNRS, UMR 7139RoscoffFrance
  4. 4.Laboratoire International Associé Dispersal and Adaptation in Marine Species, UMR 7139, Station Biologique de RoscoffRoscoffFrance

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