Plant Proteus: Brown algal morphological plasticity and underlying developmental mechanisms

Trends in Plant Science

Volumn 17, Issue 8, 2012, Pages 468-477

  Charrier, Bénédicte ^a   Le Bail, Aude ^a,c   De Reviers, Bruno ^b  

^a STATION BIOLOGIQUE DE ROSCOFF   (France)

^b MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; BROWN ALGA; CELL DIVISION; CLASSIFICATION; ENVIRONMENT; EVOLUTION; GENETICS; MECHANOTRANSDUCTION; MORPHOGENESIS; PHYLOGENY; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE;

ADAPTATION, BIOLOGICAL; BIOLOGICAL EVOLUTION; CELL DIVISION; ENVIRONMENT; MECHANOTRANSDUCTION, CELLULAR; MORPHOGENESIS; PHAEOPHYTA; PHYLOGENY; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY;

ALGAE; EMBRYOPHYTA; PHAEOPHYCEAE; RHODOPHYTA;

EID: 84864382208     PISSN: 13601385     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tplants.2012.03.003     Document Type: Review

References (107)

1. Silberfeld T., et al. 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. 2010, 56:659-674.
2. King N., et al. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 2008, 451:783-788.
3. Coelho S.M., et al. OUROBOROS is a master regulator of the gametophyte to sporophyte life cycle transition in the brown alga Ectocarpus. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:11518-11523.
4. Le Bail A., et al. Auxin metabolism and function in the multicellular brown alga Ectocarpus siliculosus. Plant Physiol. 2010, 153:128-144.
5. Le Bail A., et al. ETOILE regulates developmental patterning in the filamentous brown alga Ectocarpus siliculosus. Plant Cell 2011, 23:1666-1678.
6. Peters A.F., et al. Life-cycle-generation-specific developmental processes are modified in the immediate upright mutant of the brown alga Ectocarpus siliculosus. Development 2008, 135:1503-1512.
7. Billoud B., et al. A stochastic 1D nearest-neighbour automaton models early development of the brown alga Ectocarpus siliculosus. Funct. Plant. Biol. 2008, 35:1014-1024.
8. Cock J.M., et al. The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 2010, 465:617-621.
9. Michel G., et al. The cell wall polysaccharide metabolism of the brown alga Ectocarpus siliculosus. Insights into the evolution of extracellular matrix polysaccharides in Eukaryotes. New Phytol. 2010, 188:82-97.
10. Arenas F., et al. Density-dependent regulation in an invasive seaweed: responses at plant and modular levels. J. Ecol. 2002, 90:820-829.
11. Garbary D.J., et al. Structure and development of air bladders in Fucus and Ascophyllum (Fucales, Phaeophyceae). Phycologia 2006, 45:557-566.
12. Reviers, B., ed. (2003) Biologie et Phylogénie des Algues (vol. 2), Belin.
13. Asensi A., et al. Clonal propagation of Laminaria digitata (Phaeophyceae) sporophytes through a diploid cell-filament suspension. J. Phycol. 2001, 37:411-417.
14. Lobban C.S., Harrison P.J. Seaweed Ecology and Physiology 1994, Cambridge University Press.
15. Ducreux G. Experimental modification of the morphogenetic behavior of the isolated sub-apical cell of the apex of Sphacelaria cirrosa (Phaeophyceae). J. Phycol. 1984, 20:447-454.
16. Gall E.A., et al. Parthenogenesis and apospory in the Laminariales: a flow cytometry analysis. Eur. J. Phycol. 1996, 31:369-380.
17. Katsaros C., Galatis B. Thallus development in Dictyopteris membranacea (Phaeophyta, Dictyotales). Br. Phycol. J. 1988, 23:71-88.
18. Fritsch F.E. The Structure and Reproduction of the Algae 1945, Cambridge University Press.
19. Raven J.A. Long-distance transport in non-vascular plants. Plant Cell Environ. 2003, 26:73-85.
20. Katsaros C. Apical cells of brown algae with particular reference to Sphacelariales, Dictyotales and Fucales. Phycol. Res. 1995, 43:43-59.
21. Silberfeld T., et al. Systematics and evolutionary history of pyrenoid-bearing taxa in brown algae (Phaeophyceae). Eur. J. Phycol. 2011, 46:362-378.
22. Rousseau F., De Reviers B. Phylogenetic relationships within the Fucales (Phaeophyceae) based on combined partial SSU+LSU rDNA sequence data. Eur. J. Phycol. 1999, 34:53-64.
23. Le Bail A., et al. Early development pattern of the brown alga Ectocarpus siliculosus (Ectocarpales, Phaeophyceae) sporophyte. J. Phycol. 2008, 44:1269-1281.
24. Graham L.E. Origin Of Land Plants 1993, John Wiley & Sons.
25. Demes K.W., et al. Phenotypic plasticity reconciles incongruous molecular and morphological taxonomies: the giant kelp, Macrocystis (Laminariales, Phaeophyceae), is a monospecific genus. J. Phycol. 2009, 45:1266-1269.
26. Lane C.E., et al. A molecular assessment of northeast Pacific Alaria species (Laminariales, Phaeophyceae) with reference to the utility of DNA barcoding. Mol. Phylogenet. Evol. 2007, 44:634-648.
27. Falace A., Bressan G. Seasonal variations of Cystoseira barbata (Stackhouse) C. Agardh frond architecture. Hydrobiologia 2006, 555:193-206.
28. Chock J.S., Mathieson A.C. Ecological studies of salt-marsh ecad scorpioides (Hornemann) Hauck of Ascophyllum nodosum L) Le Jolis. J. Exp. Mar. Biol. Ecol. 1976, 23:171-190.
29. Pereira T.R., et al. Temperature effects on the microscopic haploid stage development of Laminaria ochroleuca and Sacchoriza polyschides, kelps with contrasting life histories. Cah. Biol. Mar. 2011, 52:395-403.
30. Engelen A.H., et al. Effects of wave exposure and depth on biomass, density and fertility of the fucoid seaweed Sargassum polyceratium (Phaeophyta, Sargassaceae). Eur. J. Phycol. 2005, 40:149-158.
31. Stewart H.L. Morphological variation and phenotypic plasticity of buoyancy in the macroalga Turbinaria ornata across a barrier reef. Mar. Biol. 2006, 149:721-730.
32. Friedland M.T., Denny M.W. Surviving hydrodynamic forces in a wave swept environment: consequences of morphology in the feather boa kelp, Egregia menziesii (Turner). J. Exp. Mar. Biol. Ecol. 1995, 190:109-133.
33. Blanchette C.A. Size and survival of intertidal plants in response to wave action: a case study with Fucus gardneri. Ecology 1997, 78:1563-1578.
34. Dudgeon S.R., Johnson A.S. Thick vs thin: thallus morphology and tissue mechanics influence differential drag and dislodgment of 2 codominant seaweeds. J. Exp. Mar. Biol. Ecol. 1992, 165:23-43.
35. Koehl M.A.R. How do benthic organisms withstand moving water. Am. Zool. 1984, 24:57-70.
36. Koehl M.A.R., Alberte R.S. Flow, flapping, and photosynthesis of Nereocystis luetkeana - a functional comparison of undulate and flat blade morphologies. Mar. Biol. 1988, 99:435-444.
37. Fowler-Walker M.J., et al. Differences in kelp morphology between wave sheltered and exposed localities: morphologically plastic or fixed traits?. Mar. Biol. 2006, 148:755-767.
38. Wernberg T., Thomsen M.S. The effect of wave exposure on the morphology of Ecklonia radiata. Aquat. Bot. 2005, 83:61-70.
39. Koehl M.A.R., et al. How kelp produce blade shapes suited to different flow regimes: a new wrinkle. Integr. Comp. Biol. 2008, 48:834-851.
40. Long J.D., Trussel G.C. Geographic variation in seaweed induced responses to herbivory. Mar. Ecol. Prog. Ser. 2007, 333:75-80.
41. Vanalstyne K.L. Adventitious branching as a herbivore induced defense in the intertidal brown alga Fucus distichus. Mar. Ecol. Prog. Ser. 1989, 56:169-176.
42. Diaz-Pulido G., et al. Herbivory effects on the morphology of the brown alga Padina boergesenii (Phaeophyta). Phycologia 2007, 46:131-136.
43. Lewis S.M., et al. The regulation of morphological plasticity in tropical reef algae by herbivory. Ecology 1987, 68:636-641.
44. Haring R.N., Carpenter R.C. Habitat-induced morphological variation influences photosynthesis and drag on the marine macroalga Pachydictyon coriaceum. Mar. Biol. 2007, 151:243-255.
45. Hurd C.L., et al. Effect of seawater velocity on inorganic nitrogen uptake by morphologically distinct forms of Macrocystis integrifolia from wave-sheltered and exposed sites. Mar. Biol. 1996, 126:205-214.
46. Stewart H.L., Carpenter R.C. The effects of morphology and water flow on photosynthesis of marine macroalgae. Ecology 2003, 84:2999-3012.
47. Goecke F., et al. Chemical interactions between marine macroalgae and bacteria. Mar. Ecol. Prog. Ser. 2010, 409:267-299.
48. Graham M.H., et al. Global ecology of the giant kelp Macrocystis: from ecotypes to ecosystems. Oceanogr. Mar. Biol. 2007, 45:39-88.
49. Stewart H.L. The role of spatial and ontogenetic morphological variation in the expansion of the geographic range of the tropical brown alga, Turbinaria ornata. Integr. Comp. Biol. 2008, 48:713-719.
50. 2, on generation of receptor potential. J. Membrane Biol. 2008, 221:27-37.
51. Li Z.G., Gong M. Mechanical stimulation induced cross adaptation in plants: an overview. J. Plant Biol. 2011, 54:358-364.
52. Hackney J.M., et al. Influence of hydrodynamic environment on composition and macromolecular organization of structural polysaccharides in Egregia menziesii cell walls. Planta 1994, 192:461-472.
53. Kraemer G.P., Chapman D.J. Biomechanics and alginic acid composition during hydrodynamic adaptation by Egregia menziesii (Phaeophyta) juveniles. J. Phycol. 1991, 27:47-53.
54. Kraemer G.P., Chapman D.J. Effects of tensile force and nutrient availability on carbon uptake and cell wall synthesis in blades of juvenile Egregia menziesii (Turn.) Aresch. (Phaeophyta). J. Exp. Mar. Biol. Ecol. 1991, 149:267-278.
55. Humphrey T.V., et al. Sentinels at the wall: cell wall receptors and sensors. New Phytol. 2007, 176:7-21.
56. Monshausen G.B., Gilroy S. Feeling green: mechanosensing in plants. Trends Cell Biol. 2009, 19:228-235.
57. Kohorn B.D. WAKs; cell wall associated kinases - commentary. Curr. Opin. Cell Biol. 2001, 13:529-533.
58. Kohorn B.D., et al. Pectin activation of MAP kinase and gene expression is WAK2 dependent. Plant J. 2009, 60:974-982.
59. Kloareg B., Quatrano R.S. Structure of the cell walls of marine algae and ecophysiological functions of the matrix polysaccharides. Oceanogr. Mar. Biol. 1988, 26:259-315.
60. Hoffman B.D., et al. Dynamic molecular processes mediate cellular mechanotransduction. Nature 2011, 475:316-323.
61. Schwartz M.A. Integrins and extracellular matrix in mechanotransduction. Csh. Perspect. Biol. 2010, 2.
62. Hable W.E., Kropf D.L. The Arp2/3 complex nucleates actin arrays during zygote polarity establishment and growth. Cell Motil. Cytoskeleton 2005, 61:9-20.
63. Chehab E.W., et al. Thigmomorphogenesis: a complex plant response to mechano-stimulation. J. Exp. Bot. 2009, 60:43-56.
64. 32. Plant Physiol. 1979, 63:1003-1009.
65. Charrier B., et al. Development and physiology of the brown alga Ectocarpus siliculosus: two centuries of research. New Phytol. 2008, 177:319-332.
66. Katsaros C., et al. Diaphragm development in cytokinetic vegetative cells of brown algae. Bot. Mar. 2009, 52:150-161.
67. Kawai H., et al. Schizocladia ischiensis: a new filamentous marine chromophyte belonging to a new class, Schizociadiophyceae. Protist 2003, 154:211-228.
68. Lucas W.J., et al. Plasmodesmata - bridging the gap between neighboring plant cells. Trends Cell. Biol. 2009, 19:495-503.
69. Bouget F.Y., et al. Position dependent control of cell fate in the Fucus embryo: role of intercellular communication. Development 1998, 125:1999-2008.
70. Pellegrini L., et al. Use of lanthanum as a marker of apoplastic transport in Cystoseira nodicalis (Fucales, Cystoseiraceae). Can. J. Bot. 1991, 69:18-25.
71. Ritter A., et al. Copper stress induces biosynthesis of octadecanoid and eicosanoid oxygenated derivatives in the brown algal kelp Laminaria digitata. New Phytol. 2008, 180:809-821.
72. Tarakhovskaya E.R., et al. Phytohormones in algae. Russ. J. Plant Physiol. 2007, 54:163-170.
73. Hannapel D.J. A model system of development regulated by the long-distance transport of mRNA. J. Integr. Plant Biol. 2010, 52:40-52.
74. Chitwood D.H., et al. Pattern formation via small RNA mobility. Gene Dev. 2009, 23:549-554.
75. Nehr Z., et al. Space-time decoupling in the branching process in the mutant étoile of the filamentous brown alga Ectocarpus siliculosus. Plant Signal. Behav. 2011, 6.
76. Dworetzky B., et al. Effect of growth substances on apical dominance in Sphacelaria furcigera (Phaeophyta). J. Phycol. 1980, 16:239-242.
77. Moss B. Apical dominance in Fucus vesiculosus. New Phytol. 1965, 64:387-392.
78. Williams L.G. Growth regulating substances in Laminaria agardhii. Sci. Total Environ. 1949, 110:169-170.
79. Benjamins R., et al. PINOID-mediated signaling involves calcium-binding proteins. Plant Physiol. 2003, 132:1623-1630.
80. Cosse A., et al. Dynamic defense of marine macroalgae against pathogens: from early activated to gene-regulated responses. Adv. Bot. Res. 2007, 46:221-266.
81. Blomster T., et al. Apoplastic reactive oxygen species transiently decrease auxin signaling and cause stress-induced morphogenic response in Arabidopsis. Plant Physiol. 2011, 157:1866-1883.
82. Hable W.E., Hart P.E. Signaling mechanisms in the establishment of plant and fucoid algal polarity. Mol. Reprod. Dev. 2010, 77:751-758.
83. Rusig A.M., et al. Ontogenesis in the Fucophyceae: case studies and comparison of fucoid zygotes and Sphacelaria apical cells. Cryptogamie Algol. 2001, 22:227-248.
84. Ouichou A., Ducreux G. Cell cortex and cell wall connections in the apical cell of Sphacelaria. C. R. Acad. Sci. Iii-Vie 2000, 323:727-733.
85. Katsaros C., et al. Cytoskeleton and morphogenesis in brown algae. Ann. Bot. 2006, 97:679-693.
86. Peters N.T., Kropf D.L. Asymmetric microtubule arrays organize the endoplasmic reticulum during polarity establishment in the brown alga Silvetia compressa. Cytoskeleton 2010, 67:102-111.
87. Fowler J.E., et al. Localization to the rhizoid tip implicates a Fucus distichus Rho family GTPase in a conserved cell polarity pathway. Planta 2004, 219:856-866.
88. Peters N.T., Kropf D.L. Kinesin-5 motors are required for organization of spindle microtubules in Silvetia compressa zygotes. BMC Plant Biol. 2006, 6.
89. Hadley R., et al. Polarization of the endomembrane system is an early event in fucoid zygote development. BMC Plant Biol. 2006, 6:5.
90. Quatrano R.S., Shaw S.L. Role of the cell wall in the determination of cell polarity and the plane of cell division in Fucus embryos. Trends Plant Sci. 1997, 2:15-21.
91. Bisgrove S.R., Kropf D.L. Cell wall deposition during morphogenesis in fucoid algae. Planta 2001, 212:648-658.
92. 2+ signals coordinate zygotic polarization and cell cycle progression in the brown alga Fucus serratus. Development 2008, 135:2173-2181.
93. Corellou F., et al. Cell cycle-dependent control of polarised development by a cyclin-dependent kinase-like protein in the Fucus zygote. Development 2001, 128:4383-4392.
94. Corellou F., et al. Cell cycle in the Fucus zygote parallels a somatic cell cycle but displays a unique translational regulation of cyclin-dependent kinases. Plant Cell 2001, 13:585-598.
95. Huysman M.J.J., et al. Genome-wide analysis of the diatom cell cycle unveils a novel type of cyclins involved in environmental signaling. Genome Biol. 2010, 11:R17.
96. Besnard F., et al. Organogenesis from stem cells in planta: multiple feedback loops integrating molecular and mechanical signals. Cell. Mol. Life Sci. 2011, 68:2885-2906.
97. Hay A., Tsiantis M. KNOX genes: versatile regulators of plant development and diversity. Development 2010, 137:3153-3165.
98. Hackett J.D., et al. Phylogenomic analysis supports the monophyly of cryptophytes and haptophytes and the association of Rhizaria with Chromalveolates. Mol. Biol. Evol. 2007, 24:1702-1713.
99. Hampl V., et al. Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic 'supergroups'. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:3859-3864.
100. Patron N.J., et al. Multiple gene phylogenies support the monophyly of cryptomonad and haptophyte host lineages. Curr. Biol. 2007, 17:887-891.
101. Riisberg I., et al. Seven gene phylogeny of heterokonts. Protist 2009, 160:191-204.
102. Cavalier-Smith T. Kingdoms Protozoa and Chromista and the eozoan root of the eukaryotic tree. Biol. Lett. 2010, 6:342-345.
103. Parfrey L.W., et al. Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:13624-13629.
104. Sauvageau C. Remarque sur les Sphacélariacées. J. Bot. 1903, 17:45-56. 69-95, 333-353, 378-422.
105. Moe R.L., Silva P.C. Morphology and taxonomy of Himantothallus (including Phaeoglossum and Phyllogigas), an Antarctic member of the Desmarestiales (Phaeophyceae). J. Phycol. 1981, 17:15-29.
106. Bradshaw A.D. Evolutionary significance of phenotypic plasticity in plants. Adv. Genet. 1965, 13:115-155.
107. Sultan S.E. Phenotypic plasticity for plant development, function and life history. Trends Plant Sci. 2000, 5:537-542.