The evo-devo of multinucleate cells, tissues, and organisms, and an alternative route to multicellularity

Evolution and Development

Volumn 15, Issue 6, 2013, Pages 466-474

  Niklas, Karl J ^a   Cobb, Edward D ^a   Crawford, David R ^b  

^a Department of Obstetrics Gynecology   (United States)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALGA; CLADISTICS; DEVELOPMENTAL BIOLOGY; EVOLUTIONARY BIOLOGY; PLANT COMMUNITY; TERRESTRIAL ECOSYSTEM;

EID: 84888059863     PISSN: 1520541X     EISSN: 1525142X     Source Type: Journal    
DOI: 10.1111/ede.12055     Document Type: Article

References (61)

1. Anderson, J. T., Willis, J. H., and Mitchell-Olds, T. 2011. Evolutionary genetics of plant adaption. Trends Genet. 27: 258-266.
2. Arnellos, A., Moreno, A., and Ruiz-Mirazo, K. 2013. Organizational requirements for multicellular autonomy: insights from a comparative case study. Biol. Philos. (doi: 10.1007/s10539-013-9387-x).
3. Assaad, F. F. 2001. Plant cytokinesis. Exploring links. Plt. Physiol. 126: 509-516.
4. Assaad, F. F., Huet, Y., Mayer, U., and Jürgens, G. 2001. The cytokinesis gene KEULE encodes a Sec1 protein that binds the syntaxin KNOLLE.J. Cell. Biol. 152: 531-543.
5. Baluška, F., Volkmann, D., Menzel, D., and Barlow, P. 2012. Strasburger's legacy to mitosis and cytokinesis and its relevance to the cell theory. Protoplasma 249: 1151-1162.
6. Beer, R., and Arber, A. 1919. On the occurrence of multinucleate cells in vegetative tissues. Proc. Royal Soc. London, Series B 91: 1-17.
7. Biao, D., Parthasarathy, M. V., Niklas, K. J., and Turgeon, R. 1988. A morphometric analysis of the phloem-unloading pathway in developing tobacco leaves. Planta 176: 307-318.
8. Bonduriansky, R., and Day, T. 2009. Nongenetic inheritance and its evolutionary implications. Ann. Rev. Ecol. Evol. Syst. 40: 103-125.
9. Børgesen, F. 1905. Contributions à la connaissance du genre Siphonocladus Schmitz. Overs. K. Dansk. Vidensk. Selsk. Forhandl. 1905: 259-291.
10. Bower, F. O. 1881. On the germination and histology of the seedlings of Welwitchia mirabilis. Quart. J. Micr. Sci. 21: 15-30.
11. Burkholder, P.R., and McVeigh, I. 1941. " Multinucleate" plant cells. Bull. Torrey Bot. Club 68: 395-396.
12. Buss, L. W. 1987. The evolution of individuality. Princeton University Press, Princeton.
13. Carlton, J. G., and Martin-Serrano, J. 2007. Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316: 1908-1912.
14. Carlton, J. G., and Martin-Serrano, J. 2009. The ESCRT machinery: new functions in viral and cellular biology. Biochem. Soc. Trans. 37: 195-199.
15. Cocquyt, E., Verbruggen, H., Leliart, F., and De Clerck, O. 2010. Evolution and cytological diversification of the green seaweeds (Ulvophyceae). Mol. Biol. Evol. 27: 2052-2061.
16. Cole, K. M., and Sheath R. G. (eds.). 1990. Biology of the Red Algae. Cambridge University Press, New York.
17. Dhonukshe, P., Baluška, F., Schlicht, M., Hlavacka, A., Sǎmaj, J., Friml, J., and Gadell, T. W.J. Jr., 2006. Endocytosis of cell surface material mediates cell plate formation during plant cytokinesis. Develop. Cell 10: 137-150.
18. Ding, B., Itaya, A., and Woo, Y.-M. 1999. Plasmodesmata and cell-to-cell communication in plants. Inter. Rev. Cytol. 190: 251-316.
19. Fagerberg, W. R., Hodges, E., and Dawes, C. J. 2010. Development and potential roles of cell-wall trabeculae in Caulerpa mexicana (Chlorophyta). J. Phycol. 46: 309-315.
20. Foe, V. E., and Alberts, B. M. 1983. Studies of nuclear and cytoplasmic behavior during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J. Cell Sci. 61: 31-70.
21. Folse, H. J., and Roughgarden, J. 2010. What is an individual organism? A multilevel selection perspective. Quart. Rev. Biol. 85: 447-472.
22. Fritsch, F. R. 1965. The Structure and Reproduction of the Algae. Vol. I and II. Cambridge University Press, Cambridge.
23. Goff, L. J., and Coleman, A. W. 1990. DNA: Microspectrofluorometric studies. In K. M. Cole and R. G. Sheath (eds.). Biology of the Red Algae. Cambridge University Press, New York: pp. 43-72.
24. Graham, L. E. 1996. Green algae to land plants: an evolutionary transition. J. Plant Res. 109: 241-251.
25. Graham, L. E., Graham, J. M., and Wilcox, L. W. 2009. Algae. 2nd Ed. Benjamin Cummings, San Francisco.
26. Gray, M. W., Lukeš, J., Archibald, J. M., Keeling, P. J., and Doolittle, W. F. 2010. Irremediable complexity? Science 330: 920-921.
27. Grosberg, R. K., and Strathmann, R. R. 2007. The evolution of multicellularity: a minor major transition? Ann. Rev. Ecol. Evol. Syst. 38: 621-654.
28. Hadzi, J. 1953. An attempt to reconstruct the system of animal classification. Syst. Zool. 2: 145-154.
29. Hommersand, M. H., and Fredericq, S. 1990. Sexual reproduction and cystocarp development. In K. M. Cole and R. G. Sheath (eds.). Biology of the Red Algae. Cambridge University Press, New York, pp. 43-72.
30. Hanson, E. D. 1977. The Origin and Early Evolution of Animals. Wesleyan University Press, Middletown, Connecticut.
31. Herron, M. D., and Michod, R. E. 2008. Evolution of complexity in the volvocine algae: Transitions in individuality through Darwin's eye. Evolution 62: 436-451.
32. Huxley, J. S. 1912. The Individual in the Animal Kingdom. Cambridge University Press, Cambridge.
33. Imoto, Y., Yoshida, Y., Yagisawa, F., Kuroiwa, H., and Kuroiwa, T. 2011. The cell cycle, including mitotic cycle and organelle division cycles, as revealed by cytological observations. J. Electron Micro. 60: S117-S136.
34. Ispolatov, I., Ackermann, M., and Doebeli, M. 2012. Division of labor and the evolution of multicellularity. Proc. Natl. Acad. Sci. (USA) 274: 1768-1776.
35. Kirk, D. L. 2005. A twelve-step program for evolving multicellularity and a division of labor. Bioessays 27: 299-310.
36. Laurent, M., and Kellershohn, N. 1999. Multistability: a major means of differentiation and evolution in biological systems. Trends Biochem. Sci. 24: 418-422.
37. Le Claire, J. W. 1982. Cytomorphological aspects of wound healing in selected Siphonocladales (Chlorphyceae). J. Phycol. 18: 379-382.
38. Lee, R. E. 2008. Phycology. 4th Ed. Cambridge University Press, New York.
39. Lessie, P. E., and Lovett, J. S. 1968. Ultrastructural changes during sporangium formation and zoospore differentiation in Blastocladiella emersonii. Amer. J. Bot. 55: 220-236.
40. Lewis, L. A., and McCourt, R. M. 2004. Green algae and the origin of land plants. Amer. J. Bot. 91: 1535-1556.
41. Libby, E., and Rainey, P. B. 2013. A conceptual framework for the evolutionary origins of multicellularity. Phys. Biol. 10: article 035001 (doi: 10.1088/1478-3975/10/035001).
42. Lukowitz, W., Nickle, T. C., Meinke, D. W., Last, R. L., Conklin, P. L., and Sommerville, C. R. 2001. Arabdiopsis cyt1 mutants are deficient in a mannose- 1-phosphate guanylyltransferase and point to a requirement of N-linked glycosylation for cellulose biosynthesis. Proc. Natl. Acad. Sci. (USA) 98: 2262-2267.
43. Lynch, M. 2012. Evolutionary layering and the limits to cellular perfection. Proc. Natl. Acad, Sc. (USA) 109: 18851-18856.
44. Maistro, S., Broady, P. A., Andreoli, C., and Negrisolo, E. 2007. Molecular phylogeny and evolution of the order Tribonematales (Heterokonta, Xanthophyceae) based on analysis of plastidial genes rbcL and psaA. Molec. Phylo. Evol. 43: 407-417.
45. McDonald, K. L., and Pickett-Heaps, J. D. 1976. Ultrastructure and differentiation in Cladophora glomerata. I. Cell division. Amer. J. Bot. 63: 592-601.
46. McGhee, G. R. Jr., 1999. Theoretical Morphology: The Concept and Its Applications. Columbia University Press, New York.
47. McMichael, C. M., and Bednarek, S. Y. 2013. Cytoskeletal and membrane dynamics during higher plant cytokinesis. New Phytol. 197: 1039-1057.
48. Menzel, D. 1988. How do giant plant cells cope with injury? The wound response in siphonous green algae. Protoplasma 144: 73-91.
49. Michod, R. E. 1997. Evolution of the individual. Amer. Nat. 150: S5-S21.
50. Mine, I., Menzel, D., and Okuda, K. 2008. Morphogenesis in giant-celled algae. Inter. Rev. Cell Molec. Biol. 266: 37-83.
51. Nacry, P., Mayer, U., and Juergens, G. 2000. Genetic dissection of cytokinesis. Plant Mol. Bol. 43: 719-733.
52. Niklas, K. J. 2000. The evolution of plant body plans - a biomechanical perspective. Ann. Bot. 85: 411-438.
53. Niklas, K. J., and Kaplan, D. R. 1991. Biomechanics and the adaptive significance of multicellularity in plants. In E. C. Dudley (ed.). The Unity of Evolutionary Biology. Proceedings of the Fourth International Congress of Systematics and Evolutionary Biology. pp. 489-502.
54. Niklas, K. J., and Kutschera, U. 2009. The evolutionary development of plant body plans. Funct. Plant Biol. 36: 682-695.
55. Niklas, K. J., and Newman, S. 2013. The origins of multicellular organisms. Evol. & Develop. 15: 41-52.
56. Pickett-Heaps, J. D., Gunning, B. E., Brown, R. C., Lemmon, B. E., and Cleary, A. L. 1999. The cytoplast concept in dividing plant cells: cytoplasmic domains and the evolution of spatially organized cell. Amer. J. Bot. 86: 153-172.
57. McNaughton, E., and Goff, L. J. 1990. The role of microtubules in establishing nuclear spatial patterns in multinucleate green algae. Protoplasma 157: 19-37.
58. Smith, G. M. 1950. The Fresh-Water Algae of the United States. McGraw-Hill, New York.
59. Schnarf, K. 1931. Vergleichende Embryologie der Angiospermen. Gebrüder Borntraeger, Berlin.
60. Strasburger, E. 1913. Pflanliche Zellen- und Gewebelehre. In R. von Wettstein (ed.). Zellen und Gewebelehre, Morphologie und Entwicklunggeschichte. B.G. Teuber, Leipzig, pp. 1-174.
61. Zalokar, M., and Erk, I. 1976. Division and migration of nuclei during early embryogenesis of Drosophila melanogaster. J. Microsc. Cell. 25: 97-106.