Fibonacci spirals in a brown alga [Sargassum muticum (Yendo) Fensholt] and in a land plant [Arabidopsis thaliana (L.) Heynh.]: a case of morphogenetic convergence

• Autorzy: Peaucelle A. , Couder Y.
• Języki publikacji: EN

Abstrakty

EN

In this article, the morphology of a brown alga is revisited and compared to the phyllotaxis of land plants. The alga, Sargassum muticum (Yendo) Fensholt has a highly organized thallus with a stipe, the stem-like main axis, and hierarchically organized lateral branches of successive orders. Around each of these axes, the lateral organs: blades, side-branches, and receptacles grow in a spiral disposition. As in land plants, this organization is related to an apical mode of growth. Measurements performed along the mature differentiated axes as well as in their meristematic regions confirm the similarity of the large-scale organization of this brown alga with that of the land plants. In particular, the divergence angle between successive elements has similar values and it results from the existence around the meristem of parastichies having the same Fibonacci ordering. This is remarkable in view of the fact that brown algae (Phaeophyceae) and land plants (Embryophyta) are two clades that diverged approximately 1800 million years ago when they were both unicellular organisms. We argue that the observed similarity results from a morphogenetic convergence. This is in strong support of the genericity and robustness of self-organization models in which similar structures, here Fibonacci related spirals, can be obtained in various situations in which the genetic and physiological implementation of development can be of a different nature.

• Wydawca: -
• Czasopismo: Acta Societatis Botanicorum Poloniae
• Rocznik: 2016
• Tom: 85
• Numer: 4
• Opis fizyczny: Article 3526 [15p.], fig.,ref.

Twórcy

autor

Peaucelle A.

• Institut Jean-Pierre Bourgin, UMR1318 INRA-AgroParisTech, INRA Centre de Versailles-Grignon, France
• Matieres et Systemes Complexes, Universite Paris 7 Denis Diderot, CNRS UMR 7057, Batiment Condorcet, 10 rue Alice Domon et Leonie Duquet, 75205 Paris cedex 13, France

autor

Couder Y.

• Matieres et Systemes Complexes, Universite Paris 7 Denis Diderot, CNRS UMR 7057, Batiment Condorcet, 10 rue Alice Domon et Leonie Duquet, 75205 Paris cedex 13, France

Bibliografia

• 1. Yoon HS, Hackett JD, Ciniglia C, Pinto G, Bhattacharya D. A molecular timeline for the origin of photosynthetic eukaryotes. Mol Biol Evol. 2004;21:809–818. https://doi.org/10.1093/molbev/msh075
• 2. Keeling PJ, Burger G, Durnford DG, Lang BF, Lee RW, Pearlman RE, et al. The tree of eukaryotes. Trends Ecol Evol. 2005;20:671–676. https://doi.org/10.1016/j.tree.2005.09.005
• 3. Hedges SB, Marin J, Suleski M, Paymer M, Kumar S., Tree of life reveals clock-like speciation and diversification. Mol Biol Evol. 2015;32:835–845. https://doi.org/10.1093/molbev/msv037
• 4. Church AH. On the interpretation of phenomena of phyllotaxis. London: Humphrey Milford and Oxford University Press; 1920. (Botanical Memoirs).
• 5. Shaw AJ, Szövényi P, Shaw B. Bryophyte diversity and evolution: windows into the early evolution of land plants. Am J Bot. 2011;98:352–369. https://doi.org/10.3732/ajb.1000316
• 6. Schimper KF. Beschreibung des Symphytum Zeyheri und seiner zwei deutschen Verwandten der S. bulborum Schimp und S. tuberosum Jacq. Heidelberg: Winter; 1835.
• 7. Braun A. Vergleichende Untersuchung über die Ordnung der Schuppen an den Tannenzapfen. Nova Acta Academiae Caesareae Leopoldino-Carolinae. 1831;15:195–402. https://doi.org/10.5962/bhl.title.69200
• 8. Bravais L, Bravais A. Essai sur la disposition des feuilles curvisériées. Annales des Sciences Naturelles. Botanique. 1837;7:42–110.
• 9. Hofmeister W. Allgemeine Morphologie der Gewachse, Handbuch der Physiologischen Botanik. Leipzig: Engelmann; 1868.
• 10. Richards FJ. Phyllotaxis: its quantitative expression and relation to growth in the apex. Philos Trans R Soc Lond B. 1951;235:510–564. https://doi.org/10.1098/rstb.1951.0007
• 11. Snow M, Snow R, Minimum area and leaf determination. Proc Proc R Soc Lond B Biol Sci. 1952;139:545–566. https://doi.org/10.1098/rspb.1952.0034
• 12. van Iterson G. Mathematische und microscopisch-anatomische Studien über Blattstellungen, nebst Betraschungen ûber den Schalenbau der Miliolinen. Jena: G. Fisher; 1907.
• 13. Douady S, Couder Y. Phyllotaxis as a physical self-organized growth process. Phys Rev Lett. 1992;68:2098–2101. https://doi.org/10.1103/PhysRevLett.68.2098
• 14. Douady S, Couder Y. Phyllotaxis as a dynamical self organizing process Part I: the spiral modes resulting from time-periodic iterations. J Theor Biol. 1996;178:255–273. https://doi.org/10.1006/jtbi.1996.0024
• 15. Douady S, Couder Y. Phyllotaxis as a dynamical self organizing process Part II: the spontaneous formation of a periodicity and the coexistence of spiral and whorled patterns. J Theor Biol. 1996;178:275–294. https://doi.org/10.1006/jtbi.1996.0025
• 16. Douady S, Couder Y. Phyllotaxis as a dynamical self organizing process Part III: the simulation of the transient regimes of ontogeny. J Theor Biol. 1996;178:295–312. https://doi.org/10.1006/jtbi.1996.0026
• 17. Couder Y. Initial transitions, order and disorder in phyllotactic patterns: the ontogeny of Helianthus annuus, a case study. Acta Soc Bot Pol. 1998;67:129–150. https://doi.org/10.5586/asbp.1998.016
• 18. Fritsch FE. The structure and reproduction of the algae. Cambridge: Cambridge University Press; 1945.
• 19. Charrier B, Le Bail A, de Reviers B. Plant proteus: brown algal morphological plasticity and underlying developmental mechanisms. Trends Plant Sci. 2012;17(8):468–477. https://doi.org/10.1016/j.tplants.2012.03.003
• 20. Bogaert KA, Arun A, Coelho SM, de Clerck O. Brown algae as a model for plant organogenesis. Methods Mol Biol. 2013;959:97–125. https://doi.org/10.1007/978-1-62703-221-6_6
• 21. Jensen JB. Morphological studies in Cystoseiraceae and Sargassaceae (Phaeophyceae), with special reference to apical organization. Berkeley, CA: University of California Press; 1974. (University of California Publications in Botany; vol 68).
• 22. Popper ZA, Michel G, Herve C, Domozych DS, Willats WGT, Tuohy MG, et al. Evolution and diversity of plant cell walls: from algae to flowering plants. Annu Rev Plant Biol. 2011;62:567–590. https://doi.org/10.1146/annurev-arplant-042110-103809
• 23. Agardh CA. Species algarum rite cognitae, cum synonymis differentiis specificis et descriptionibus succintis. Vol. 1, Part 1. Lundae: E. Mavritii; 1820.
• 24. Yoshida T. Japanese species of Sargassum subgenus Bactrophycus (Phaeophyta, Fucales). Journal of the Faculty of Science, Hokkaido University. Series 5, Botany. 1983:13(2):99–246.
• 25. Yoshida T, Majima T, Marui M, Apical organization of some genera of Fucales (Phaeophyta) from Japan. Journal of the Faculty of Science, Hokkaido University. Series 5, Botany. 1983;13(1):49–56.
• 26. Norton TA. The growth and development of Sargassum muticum. J Exp Mar Bio Ecol. 1977;26:41–53. https://doi.org/10.1016/0022-0981(77)90079-X
• 27. Kane DF, Chamberlain AHL. Laboratory growth studies on Sargassum muticum (Yendo) Fensholt. I. Seasonal growth of whole plants and lateral sections. Botanica Marina. 1978;22:1–9. https://doi.org/10.1515/botm.1979.22.1.1
• 28. Chamberlain HL, Gorham J, Kane DF, Lewey SA. Laboratory growth studies on Sargassum muticum (Yendo) Fensholt. II. Apical dominance. Botanica Marina. 1978;22:11–19.
• 29. Critchley AT. Sargassum muticum: a morphological description of European material. J Mar Biol Assoc U K. 2009;63:813–824. https://doi.org/10.1017/S002531540007123X
• 30. Peaucelle A, Morin H, Traas J, Laufs P. Plants expressing a miR164-resistant CUC2 gene reveal the importance of postmeristematic maintenance of phyllotaxy in Arabidopsis. Development. 2007;134(6):1045–1050. https://doi.org/10.1242/dev.02774
• 31. Yang W, Schuster C, Beahan CT, Charoensawan V, Peaucelle A, Basic A, et al. Regulation of meristem morphogenesis by cell wall synthases in Arabidopsis. Curr Biol. 2016;26:1404–1415. https://doi.org/10.1016/j.cub.2016.04.026
• 32. Mirabet V, Besnard F, Vernoux T, Boudaoud A. Noise and robustness in phyllotaxis. PLoS Comput Biol. 2012;8(2):e1002389. https://doi.org/10.1371/journal.pcbi.1002389
• 33. Refahi YG, Farcot E, Jean-Marie A, Pulkkinen M, Vernoux T, Godin C. A stochastic multicellular model identifies biological watermarks from disorders in self-organized patterns of phyllotaxis. eLife. 2016;5:e14093. https://doi.org/10.7554/eLife.14093
• 34. Klemm MF, Hallam ND. Branching patterns and growth in Cystophora (Fucales, Phaeophyta). Phycologia. 1987;26:252–261. https://doi.org/10.2216/i0031-8884-26-2-252.1
• 35. Katsaros CI. Apical cells of brown algae with particular reference to Sphacelariales, Dictyotales and Fucales. Phycological Res. 1995;43:43–59. https://doi.org/10.1111/j.1440-1835.1995.tb00004.x
• 36. D’Arcy Thompson W. On growth and form. Vols 1 and 2. Cambridge: Cambridge University Press; 1917. https://doi.org/10.5962/bhl.title.11332
• 37. Couder Y. Viscous fingering as an archetype for growth patterns. In: Batchelor GK, Moffat HK, Worster MG, editors. Perspectives in fluid dynamics. Cambridge: Cambridge University Press; 2000. p. 53–104.
• 38. Couder Y. Patterns with open branches or closed networks: growth in scalar or tensorial fields. In: Fleury V, Gouyet JF, Leonetti M, editors. Branching in nature. Berlin: EDP Sciences and Springer; 2001. p. 1–22. https://doi.org/10.1007/978-3-662-06162-6_1
• 39. Kylin H. Studien über die Entwicklungsgeschichte der Florideen. Stockholm: Almqvist & Wiksells; 1923. [Kungliga Svenska Vetenskapsakademiens Handlingar; vol 63(11)].
• 40. Katsaros C, Karyophyllis D, Galatis B. Cytoskeleton and morphogenesis in brown algae. Ann Bot. 2006;97:679–693. https://doi.org/10.1093/aob/mcl023
• 41. Hamant O, Heisler MG, Jönsson H. Krupinski P, Uyttewaal M, Bokov P, et al. Developmental patterning by mechanical signals in Arabidopsis. Science. 2008;322:1650–1655. https://doi.org/10.1126/science.1165594
• 42. Heisler MG, Hamant O, Krupinski P, Uyttewaal M, Ohno C, Jönsson H, et al. Alignment between PIN1 polarity and microtubule orientation in the shoot apical meristem reveals a tight coupling between morphogenesis and auxin transport. PLoS Biol. 2010;8:e1000516. https://doi.org/10.1371/journal.pbio.1000516
• 43. Peaucelle A, Louvet R, Johansen JN, Salsac F, Morin H, Fournet F, et al. Transcription factor BELLRINGER modulates phyllotaxis by regulating the expression of a pectin methylesterase in Arabidopsis. Development. 2011;138:4733–4741. https://doi.org/10.1242/dev.072496
• 44. Peaucelle A, Braybrook SA, Le Guillou L, Bron E, Kuhlemeier C, Höfte H. Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis. Curr Biol. 2011;21:1720–1726. https://doi.org/10.1016/j.cub.2011.08.057
• 45. Augier, H. Les hormones des algues. Etat actuel des connaissances. VII. Applications conclusions et bibliographie. Botanica Marina. 1978;21:175–197. https://doi.org/10.1515/botm.1978.21.3.175
• 46. Bradley PM. Plant hormones do have a role in controlling growth and development of algae. J Phycol. 1991;27:317–321. https://doi.org/10.1111/j.0022-3646.1991.00317.x
• 47. Tarakhovskaya ER, Maslov YI, Shishova MF. Phytohormones in algae. Russ J Plant Physiol. 2007;54:163–170. https://doi.org/10.1134/S1021443707020021
• 48. Sun H, Basu S, Brady SR, Luciano RL, Muday GK. Interactions between auxin transport and the actin cytoskeleton in developmental polarity of Fucus distichus embryos in response to light and gravity. Plant Physiol. 2004;135:266–278. https://doi.org/10.1104/pp.103.034900

Identyfikatory

DOI

10.5586/asbp.3526